Chapter 8 Fluid Dynamics in Seagrass Ecology—from Molecules to Ecosystems Evamaria W. Koch* Horn Point Laboratory, University of Maryland Center for Environmental Science, P.O. Box 775, Cambridge, MD 21613, USA Josef D. Ackerman Faculty of Environmental Sciences & Departments of Botany and Zoology, University of Guelph, Guelph, ON, Canada N1G 2W1; email: ackerman@uoguelph.ca Jennifer Verduin School of Biological Sciences & Biotechnology, Murdoch University, Murdoch WA 6150, Australia; email: j.verduin@murdoch.edu.au Michael van Keulen School of Biological Sciences & Biotechnology, Murdoch University, Murdoch WA 6150, Australia; email: keulen@mail.murdoch.edu.au I. Introduction Fluid dynamics is the study of the movement of fluids. Among other things, it addresses velocity, acceleration, and the forces exerted by or upon fluids in motion (Daugherty et al., 1985; White, 1999; Kundu and Cohen, 2002). Fluid dynamics affects every aspect of the existence of seagrasses from the smallest to the largest scale: from the nutrients they obtain to the sediment they colonize; from the pollination of their flowers to the import/export of organic matter to adjacent systems; from the light that reaches their leaves to the organisms that live in the seagrass habitats. Therefore, fluid dynamics is of major importance in seagrass biology, ecology, and ecophysiology. Unfortunately, fluid dynamics is often overlooked in seagrass systems (Koch, 2001). This ∗ Author for correspondence, email: koch@hpl.umces.edu chapter provides a general background in fluid dynamics and then addresses increasingly larger scales of fluid dynamic processes relevant to seagrass ecology and physiology: molecules (µm), leaves and shoots (mm to cm), seagrass canopies (m), seagrass landscapes (100–1,000 m), and seagrasses as part of the biosphere (>1,000 m). Although gases are also fluids, this chapter is restricted to water (i.e. compressed fluids), how it flows through seagrasses, the forces it exerts on the plants, and the implications that this has for seagrass systems. Seagrasses are not only affected by water in motion, they also affect the currents, waves and turbulence of the water masses surrounding them. This capacity to alter their own environment is referred to as “ecosystem engineering” (Jones et al., 1994, 1997; Thomas et al., 2000). Readers are also encouraged to consult a recent review by Okubo et al. (2002) for a discussion on flow in terrestrial and aquatic A. W. D. Larkum et al. (eds.), Seagrasses: Biology, Ecology and Conservation, pp. 193–225. c 2006 Springer.
194 E. W. Koch, J. D. Ackerman, J. Verduin and M. van Keulen vegetation including freshwater plants, seagrasses, and kelp. II. Fluid Dynamics: Fundamentals The general aspects of water flow in aquatic systems can be understood through a number of fluid dynamic concepts that have been developed largely for steady state conditions, i.e. when there are no temporal fluctuations in the water flow (Fischer et al., Abbreviations A – cross sectional area C – celerity or phase velocity of waves Cd – drag coefficient Cs – concentration on the seagrass surface Cw – concentration in the water column D – molecular diffusivity D – depth DBL – diffusive boundary layer δ – diffusive boundary layer thickness δ D – diffusive boundary layer (=DBL) δ I –inertial sublayer or logarithmic (log) layer δ v –viscous sublayer Fd – friction or viscous drag Fp – form or pressure drag g – acceleration due to gravity H – water depth H – wave height h – canopy height J – flux κ – von Karman constant l – length scale λ – wavelength m – mass µ – molecular or dynamic viscosity p – hydrostatic or dynamic pressure Q – volume flow rate ρ – density REI – relative wave exposure index Re – Reynolds number Recrit – critical Reynolds number St – Stanton number T – wave period τ – shear stress τ o – boundary shear stress τ W – wall shear stress u – current velocity u ∗ – friction velocity Uk – critical velocity Uo – free stream velocity ν–kinematic viscosity x – horizontal distance x – principal flow direction y – cross-stream direction z – vertical direction or depth z o – roughness height 1979; White, 1999; Kundu and Cohen, 2002). In the absence of motion, seawater is described by: (i) density (ρ, i.e. mass/volume), which is used preferentially over mass (m) in fluids; (ii) kinematic viscosity (ν) which is a measure of how easily the fluid will flow (i.e. ν = µ/ρ, where µ is the molecular or dynamic viscosity); and (iii) hydrostatic pressure ( p), which is a function of the depth from the water surface (i.e. p = ρgz, where g is the acceleration due to gravity and z is the depth—note that the depth can be the distance from the water surface to the seafloor or the height from the seafloor to the water surface; see below). The introduction of energy into a fluid causes fluid motion, and the motion in natural systems is generated by pressure gradients (d p/dz) as result of gradients in water surface elevation or depth (dz/dx; where x is the horizontal distance) and/or density (dρ/dz). The major source of this energy input is the sun, which causes winds that lead to changes in surface elevation (i.e. dz/dx; waves, currents, and seiches in embayments), and thermal gradients (i.e. dρ/dz) that lead to expansion, instabilities, and mixing. Other sources include inputs of freshwater and other chemical constituents (i.e. dρ/dz), tides and currents due to gravitation and acceleration of the earth-moon and earth-sun systems (i.e. dz/dx), and the Coriolis force due to the earth’s rotation (i.e. dz/dx) (Kundu and Cohen, 2002). The flow in seawater is described with respect to a fixed Cartesian reference frame (Eulerian perspective) with x defining the principal flow direction, y defining the cross-stream direction, and z defining the vertical direction. Whereas it is common in geophysics to define z as the depth (i.e. with respect to the water surface), it is equally appropriate and perhaps more informative to use height (i.e. defined with respect to the seafloor) as the vertical direction (e.g. Ackerman and Okubo, 1993). The volume flow rate (Q), as defined by the velocity (u) of the fluid that passes through a given cross sectional area A (which is usually defined with respect to the x and y; i.e. dxdy), is conserved because seawater is an incompressible fluid. This continuity principle is one of the essential elements of fluid dynamics, which, among other things, is used to determine mass balances of water-borne materials (e.g. Hemond and Fechner, 1994). The flow of water leads to a second type of pressure, the dynamic pressure ( p = 1/ 2 ρu2 ), which, when added together with the hydrostatic pressure, is constant along a flow streamline (i.e. Bernoulli’s principle). Chapter 8 Fluid Dynamics in Seagrass Ecology Bernoulli’s principle, which states that the sum of the hydrostatic pressure and dynamic pressure along a streamline are constant (Vogel, 1994), helps to explain flow-induced pressure changes (i.e. lift) that occur within, around, and under seagrass canopies (e.g. Nepf and Koch, 1999). Drag is another important force that acts downstream of obstacles. It has two additive components: (i) the friction or viscous drag that exists due to the interaction of the obstacle’s surface with the water, which can be defined algebraically (i.e. Fd = 1/2Cd ρAu2 , where Cd is the drag coefficient, a shape and flow dependent constant); and (ii) the dynamic, form or pressure drag (Fp ) that exists under high flows when flows separate from boundaries, which cannot be expressed algebraically and must, therefore, be determined empirically. As u increases, the dynamic drag contributes a disproportionate fraction of the total drag. It is important to note that drag is a force that operates opposite to the flow direction in that it “sucks” a moving object upstream or a stationary object downstream. Water flow can exhibit a number of different properties that depend on the temporal and spatial scales under investigation. Water flow could either be smooth and regular as if the fluid flows in layers (i.e. laminar flow) or rough and irregular as if the flow is “chaotic” (i.e. turbulent flow). This depends on the velocity and the length scale (i.e. temporal and spatial scale, respectively) under investigation as defined by the Reynolds number (Re = luρ/µ or more simply Re = lu/ν; where l is the length scale appropriate for the hypothesis being tested). Re, which is the non-dimensional ratio of inertial to viscous forces in a fluid, defines four regimes that grade into one another: (i) creeping flow (Re ≪ 1), which occurs at very low flows and spatial scales such as those experienced by individual bacteria cells; (ii) laminar flow (1 < Re < 103 ) as defined above; (iii) transitional flow (Re ∼ O(103 ); i.e. of the order of 103 ), which involves the production of eddies and disturbances in the flow and is characterized by a critical Re (Recrit ) defined for a particular geometry and flow; and (iv) fully turbulent flow (Re ≫ 103 ). Associated with these flow patterns are important differences related to the fluid dynamic forces (e.g. friction vs. pressure drag) and mass transfer processes (diffusion vs. advection) that operate under the different regimes (see below; White, 1999; Kundu and Cohen, 2002). Moreover, because Re is scale dependent, it is possible to experience multiple flow regimes simul- 195 taneously in the flow field depending on the spatial scale under investigation. Consequently, flow is almost always turbulent at large spatial scales such as seagrass beds, but it can also be laminar on the scale of seagrass leaves and flowers (e.g. Ackerman and Okubo, 1993; Koch, 1994). This not-so-subtle distinction can influence the application and interpretation of physiological and ecological processes in seagrass canopies (see Section III). As indicated above, the flow conditions become more complicated when water approaches a boundary (e.g. seagrass canopy, leaves, or seafloor, depending on the scale) or any obstacle for that matter. The water cannot normally penetrate boundaries, except for the most porous ones (see reviews in Boudreau and Jørgensen, 2001; Okubo et al., 2002), and more importantly, the water molecules directly next to a boundary stick to the boundary rather than slip by it. This no-slip condition leads to the development of a velocity gradient perpendicular to the boundary (Fig. 1), as the velocity at the boundary will be zero relative to the free stream velocity (U0 ). As the water flows downstream, the velocity gradient will grow in size and a slower moving layer of fluid will develop next to the boundary, which is referred to as the boundary layer under turbulent conditions, otherwise technically it is a deformation layer (Prandtl and Tietjens, 1934). This boundary layer, which is defined by velocities <0.99 U0 , has a thickness of δ that is relatively small and can be expressed as a function of Re and x. Initially it appears laminar in nature, but the boundary layer will become turbulent when the local Re (Rex = ux/ν) approaches a critical value of 3 to 5 × 105 , in the case of a flat plate oriented parallel to the flow. In nature, this transition is accelerated by the presence of roughness or obstacles on the boundary (Schlichting, 1979; Nikora et al., 2002; Fig. 1) including undulations on macroalgal blades (Hurd and Stevens, 1997). In addition to the streamwise structure in a fully developed boundary layer, there is important vertical structure as well. The first layer directly adjacent to the boundary is the viscous sublayer (δ v ≈ 10ν/u ∗ where u ∗ is the friction velocity, which is a velocity scale that provides an indication of the mass transfer within the boundary layer) in which the forces (or stresses if surface forces are considered) are largely viscous, and consequently the mass transfer in this layer is slow and dominated by diffusion, especially within the thin diffusional sublayer (also called the diffusive boundary layer; DBL) at the bottom of this 196 E. W. Koch, J. D. Ackerman, J. Verduin and M. van Keulen Fig. 1. Velocity (U ) gradient/profile adjacent to smooth (left) and rough (right) boundaries. Weak currents (solid line) generate a relatively thick boundary layer (1) when compared with boundary layers (2) generated by faster currents (dashed curve). Names of boundary layer zones are provided for the fast flowing water velocity profile. When the boundary (such as a seagrass leaf) is rough (e.g. due to the presence of epiphytic organisms), a roughness height (arrow) extends the boundary layer farther into the water column. Consequently, the flux of nutrients and carbon from the water column to the boundary is reduced. layer (δ D ≈ ν/u ∗ (ν/D)−a , where D is the molecular diffusivity and a is a constant equal to 1/2 or 1/3; (Lorke et al., 2003). It is important to note that δ D ≪ δ v , which relates to the fact that the molecular diffusion of momentum (i.e. ν ∼ 10–6 m2 s–1 ) is much larger than the molecular diffusion of a scalar quantity like CO2 (i.e. D ∼ 10–9 m2 s–1 ). The next layer is the inertial sublayer or logarithmic (log) layer (δ I ≈ 0.15δ), which is a region of exponentially increasing velocity; hence, it is dominated by inertial forces (or stresses) and mass transfer occurs through turbulent advection. The outer layer of the boundary layer is the largest layer, and it represents a transition to the free stream flow (it is referred to as the Ekman layer in situations where the Coriolis force causes rotation of the flow; Fig. 1). Boundary layers exist embedded in one another as they are defined by spatial scale (e.g. Ackerman, 1986; Boudreau and Jørgensen, 2001); consequently, it is possible to define boundary layers around plant epiphytes, flowers, leaves, canopies, and the benthos. In this sense, there is a benthic boundary layer (BBL) above the seagrass canopy, and separate boundary layers around individual shoots, leaves, flowers, and the smaller constituents described above. In addition, it is important to note that there may also be boundary layers generated by other types of water motion (e.g. wave current boundary layers), but this topic is beyond the scope of this review. For biolog- ically relevant information on this topic see Denny (1988). Another important consequence of the no-slip condition at a boundary is the tractile or shearing force that the boundary imparts on the fluid, which is a tangential force causing rotation of the fluid next to the boundary. A boundary or wall shear stress (τ 0 or τ W ) is defined as the quotient of the shearing force and the area of the boundary, and τ W = µdu/dz within the viscous (or laminar) sublayer and τ W = ρu2∗ in general. In practice, it is difficult to measure the shear force or the aerial extent of the boundary or to apply the algebraic relationships, and thus a number of methods have been developed to measure τ directly using force balances in flow chambers or indirectly using velocity gradients based on the law of the wall (u = u ∗ /κ ln(z/z 0 ), where κ = 0.4 is the von Karman constant, and z 0 is the roughness height; see Fig. 1; for a review of techniques and references for the measurement of bed shear stress see Ackerman and Hoover (2001). The velocity gradient method involves applying the law of the wall to the velocities measured in the log layer of the boundary layer. In this case, u ∗ is equal to κ multiplied by the slope of the linear regression of velocity on the natural logarithm transformed distances from the boundary, and z 0 is equal to e raised to the value of the x intercept of the same regression. This method has been applied successfully above and Chapter 8 Fluid Dynamics in Seagrass Ecology within seagrass canopies (e.g. Fonseca and Fisher, 1986; Gambi et al., 1990; Ackerman and Okubo, 1993). It is important to note that other engineering models have been applied to rough canopies such as corals and seagrasses with the direct measurement of canopy friction and the use of the Stanton number, St (uptake rate by the surface/advection over the surface), to determine the efficiency of canopy uptake (e.g. Thomas et al., 2000; Thomas and Cornelisen, 2003). Reconfiguration of seagrass canopies under higher flow conditions (e.g. Fonseca et al., 1982; Ackerman, 1986), and/or unsteadiness due to monamis (waving of the canopy; see Section V.C) caused by an instability of the mean velocity profile (Ackerman and Okubo, 1993; Ghisalberti and Nepf, 2002) and waves (Koch, 1996; Koch and Gust, 1999) represents a challenge to researchers. Even so, τ is the preferred form (over u) of expressing hydrodynamic conditions near boundaries (leaves, flowers, sediment etc; see Nowell and Jumars, 1984). Hydrodynamic conditions in the environment are rarely stationary, especially in wave-dominated seagrass habitats where a more appropriate characterization of the fluid environment is that it varies in a periodic fashion with each passing wave. Waves represent the movement of energy through a fluid and exhibit a periodic motion, especially when viewed at an interface (e.g. the water surface). In this case, the passing wave (crest followed by trough) causes a submersed object on the surface to move in a circular or orbital fashion, the diameter of which is equal to the wave height (H ). The orbital motions also extend downward through the fluid in a series of orbitals that diminish in diameter with depth until a depth (z) of 1/2λ (where λ is the wavelength) is reached. The classification of waves can be based on the disturbing force that creates them, the restoring force that destroys them, and their wavelength (Garrison, 2000). The disturbing force is the source of energy that causes the wave, which can be (i) wind stress acting on water surface causing capillary and gravity waves, (ii) the arrival of surge or sea wave causing swell, (iii) wind setup in an embayment creating seiches, (iv) a change in atmospheric pressure causing short-lived storm surge, and (v) large disturbances (landslides, volcanic eruptions, earthquake) that cause seismic waves (or tsunami; the so-called tidal waves that are actually due to gravitational inertial forces). The restoring forces that reduce the disturbance to the water surface include 197 (a) surface tension due to the molecular cohesion of water molecules, which works for small waves (i.e. λ <1.73 cm; capillary waves) and, (b) gravity that operates on larger waves (i.e. λ ≫ 1.73 cm). Whereas the wavelength can be used to distinguish differences among the smallest of waves, it really provides a measure of wave size and relationship to energy; the smaller the wavelength, the higher the energy. Some typical relationships include (1) wind waves (λ <60– 150 m), (2) seiches (λ is large and a function of the basin size), (3) seismic waves (λ <200 km), and (4) tides (λ = 1/2 circumference of earth; note that tides are caused by gravity and inertia). Seagrasses experience each of these types of waves, but the most common are wind waves, swell, and tides (tides can be viewed as long waves). Wind waves develop from capillary waves to gravity waves as a function of the wind strength and direction and the fetch (length of the unrestricted zone over which the wind stress operates). Wind waves are affected by local wind conditions, and are generally of a short period, T (T is time it takes for a wave to pass a fixed point). Wave action has a direct impact on the ecosystem, with obvious effects on sediment transport, boundary layer processes and physical stresses (Denny, 1988; Koch and Gust, 1999). There has also been some suggestions that fetch (relative wave exposure index) is an important factor affecting seagrass on a landscape level (e.g. Fonseca and Bell, 1998; Hovel et al., 2002; Krause-Jensen et al., 2003). Just as the size of the wave is determined by the wavelength, the shape of the orbit is determined by the water depth. In deep water (i.e. z > 1/2λ) the orbits are circular, whereas in shallow water (i.e. z <1/20λ) the orbits become elliptical or flatter due to the influence of the bottom. Intermediate waves (i.e. 1/20λ < z < 1/2λ) are more complicated as they combine characteristics of deep and shallow water waves. Deep water √ waves travel at a celerity or phase velocity C = gλ/2π or λ/T (∼1.56 T ), but shallow water waves are slower due to the influence of the √ √ bottom and travel at C = gz (or 3.1 z), which is why waves build up in shallow areas (Denny, 1988). Waves travel in a wave train, which is a progression of groups of waves of similar λ from the same origin. Energy is lost by the leading wave, which eventually dissipates, but a new trailing edge wave is created from this energy. In deep water, the waves progress with C ∝ λ but the wave train has a group velocity of C ∝ 1/2λ, whereas in shallow water the celerity of the individual waves slow until the wave and group 198 E. W. Koch, J. D. Ackerman, J. Verduin and M. van Keulen celerities are equal. It is important to note that waves and wave trains are not isolated from one another; circumstances can lead to destructive interference with calm periods between wave trains and constructive interference with the generation of large waves including rogue wavees due to the convergence of many waves. As indicated above, a number of changes occur as waves enter the nearshore and ultimately reach the shore. The waves become shallow water waves as the wave train encounters the friction (shear stress) of the bottom or seagrass canopy, the wave orbits become more elliptical in shape near the bottom, and the wave crests become more pronounced. This can lead to wave-induced transport in a process referred to as Stokes drift, which may be of considerable importance in many coastal environments (Monismith and Fong, 2004). The steepness of the wave becomes unstable if it is greater than 1:7 (H :λ) and the water at the crest begins to travel faster than the water near the bottom and it will break into a plunging wave, spilling wave, or surging wave depending on the steepness and topography of the bottom. Since waves approach the shore at different angles, they are unlikely to break simultaneously and may refract from the original direction leading to the complexity of waves experienced in coastal seagrass beds (Koch and Gust, 1999). Realistically, the fluid dynamic conditions within these nearshore regions are affected by a number of factors including tides and wind waves, all of which lead to significant changes in the surface elevation and water flow within seagrass beds. The general predictions are that seagrasses, like other benthic vegetation, increase the bottom shear stress and hence have a wave dampening affect (see Section V.B., below). This process has been relatively well characterized for coastal kelp forests (see review in Okubo et al., 2002), but has yet to be examined in a thorough manner for seagrasses. Clearly, additional efforts are needed in this area. Whereas, the ultimate goal of studying fluid dynamic concepts is to better understand ecological processes in seagrasses, it is important to note that vegetative flows remain the most complex and difficult flows to describe and understand (Raupach et al., 1991; Finnigan, 2000). Therefore, applications in vegetated flows have typically involved steady state condition (i.e. non turbulent), although some progress in unsteady flows has been made with respect to seaweeds (Gaylord and Denny, 1997). Fortunately, this realization provides a challenge to those interested in the biological, chemical, geological, and physical processes that occur in seagrass systems. III. Micro-Scale Processes at the Molecular Level (µm) As water flows through seagrass beds, a boundary layer develops on the sediment surface as well as on each seagrass component exposed to the moving water (leaf, short-shoot, flower) (Ackerman, 1986; Fonseca and Kenworthy, 1987; Koch, 1994; Cornelisen and Thomas, 2002). The faster the water moves, the thinner the diffusive boundary layer (DBL, or δ D ) becomes (Massel, 1999; Fig. 1) and, consequently, the faster the transfer of molecules from the water column to the sediment and/or seagrass. It follows that when currents are weak, the flux of molecules to the seagrass surface may be limited by diffusion through the δ D (i.e. physical limitation). Under those conditions, many biological sites or enzymes in the seagrass tissue are available to assimilate molecules when/if they reach the plant’s surface (Koch, 1994; Cornelisen and Thomas, 2002). After a critical velocity (Uk ) is reached (Fig. 2), the transfer Fig. 2. An example of uptake kinetics by seagrass leaves exposed to increasing current velocities (U ). Uk is the critical current velocity at which uptake rate saturates (equivalent to Ik in photosynthesis x irradiance curves). At currents below Uk (1), uptake is mass transfer-limited and at currents above Uk (3), uptake is kinetically limited. A combination of both limitations may occur at flows around Uk (2). If nutrient concentration in the water column increases, the curve is likely to shift upwards. Additionally, other types of responses to water flow are also possible (see text). Chapter 8 Fluid Dynamics in Seagrass Ecology of molecules through the δ D is no longer the limiting factor. Instead, the capacity of biological uptake sites or enzymes to assimilate molecules that reached the plant surface becomes limiting (Koch, 1994). In this case, the conditions are said to be kinetically (and not physically) limiting. When velocities are at intermediate levels, around Uk , a combination of physical (δ D ) and kinetic (enzymes) limitations may influence the uptake of nutrients (Sanford and Crawford, 2000). At velocities below 3–5 cm s–1 (Uk ), photosynthesis (i.e. carbon uptake) in Thalassia testudinum and Cymodocea nodosa is δ D limited, whereas at velocities above Uk , photosynthesis seems to be limited by the kinetics of Rubisco (Koch, 1994). Interestingly, a similar Uk value was found for the kelp Macrocystis integrifolia (Stevens and Hurd, 1997). In contrast, some seagrass studies were unable to detect a kinetic limitation in the assimilation of nutrients in flowing water (i.e. no Uk ), instead, assimilation was δ D limited up to the maximum velocity tested: 20 cm s–1 for Thalassia testudinum and its epiphytes (Cornelisen and Thomas, 2002) and 34 cm s–1 for Zostera marina (Fonseca and Kenworthy, 1987). This difference may be due in part to experimental conditions. Specifically, studies in which assimilation was only a function of velocity were performed with entire plants rooted in sediment and covered by epiphytes, while the experiments in which assimilation was a function of velocity and enzyme kinetics were done with epiphyte-free leaves, in the laboratory. For further discussion of the role of diffusive boundary layers on photosynthesis, see Larkum et al., Chapter 14. Mass transfer to seagrass leaves does not only depend on the velocity and δ D thickness but also on: (1) the thickness of the periphyton layer (complex of debris, mucus, bacteria, algae, small animals, and sediment particles) on the seagrass leaves (Jones et al., 2000), (2) the reactions occurring within the periphyton layer (Sand-Jensen et al., 1985; Jones et al., 2000; Cornelisen and Thomas, 2002) and (3) the concentration of the molecules in the water column adjacent to the seagrasses-periphyton complex (Sanford and Crawford, 2000). The water interstitial to the periphyton is expected to be static (with the exception of occasional sweep events; Nikora et al., 2002); therefore, δ D increases linearly with periphyton thickness (Jones et al., 2000). Consequently, the spatial scale for diffusion of molecules from the water column to the leaf surface is longer and δ D -limited conditions are more likely to occur. 199 The critical δ D thickness at Uk has been estimated to be 98 µm and 280 µm for periphyton-free leaves of Cymodocea nodosa and Thalassia testudinum, respectively (Koch, 1994), whereas the δ D on artificial leaves with periphyton was quantified to be 950 µm in thickness (Jones et al., 2000). The δ D limitation of molecules such as nitrogen, phosphorous and carbon may be further exacerbated by the reactions occurring within the periphyton layer. Epiphytic algae tend to assimilate biologically important molecules before they reach the seagrass surface (Jones et al., 2000; Sanford and Crawford, 2000; Cornelisen and Thomas, 2002), thereby competing for vital nutrients (Sand-Jensen et al., 1985). If the uptake kinetics of epiphytes is more efficient than that of seagrasses, the microalgae could potentially outcompete the seagrasses in the uptake of nutrients (including carbon) from the water column (Sand-Jensen et al., 1985; Beer and Koch, 1996; Cornelisen and Thomas, 2002). According to Fick’s first law: J=D Cw − Cs δD where J is the flux of molecules, Cw the concentration in the water column, and Cs the concentration on the seagrass surface. δ D limiting conditions become less important as the concentration of nutrients (Cw ) in the water column increases (i.e. eutrophication). Under such eutrophic conditions, uptake is controlled by the kinetics of periphyton and seagrasses (Sanford and Crawford, 2000). As a result, one can hypothesize that as coastal waters become more eutrophic, mass transfer-limitations may become less important to seagrasses, but this is a complex process as the growth of the epiphytes as a function of the nutrient concentration also needs to be taken into account. Additionally, when uptake rates are δ D limited, kinetic processes become less important and the uptake rates become a function of the planar area of seagrasses and epiphytes exposed to water flow. As indicated above, the Stanton number (St), a dimensionless number, can also be used to quantify the efficiency of a seagrass canopy to remove nutrients from the water, as it is the flux of a chemical to a surface divided by its advection past the surface (e.g. Thomas et al., 2000). St can be obtained via direct measurements of nutrient uptake and velocity measurements, or can be calculated. 200 E. W. Koch, J. D. Ackerman, J. Verduin and M. van Keulen The calculated values have not always matched the measured values possibly due to the dependence of St on the friction coefficient (Thomas et al., 2000), a parameter that decreases as the seagrass canopy bends when exposed to increasing velocities (Fonseca and Fisher, 1986). Additionally, the St only parameterizes the transport into the canopy, i.e. it parameterizes the flux across the interface defined by the top of the canopy, not the diffusive sub-layers on individual leaves. The discussion of fluxes of inorganic nutrients through the DBL so far assumed steady state flows. In nature, the thickness of the δ D tends to fluctuate over time and space (Koch, 1994). Wave-induced oscillatory flows and/or large-scale turbulent eddies tend to disrupt the δ D for short periods of time (fractions of a second) during which the δ D is stripped away and the supply of molecules near the blade surface is replenished (Nikora et al., 2002). If these pulses of enriched water near the seagrass leaf occur on a regular basis such as under wave-dominated conditions, the flux of nutrients to the plant surface is expected to be enhanced (Stevens and Hurd, 1997). As indicated in Section II, little is currently known about the physiological implications of δ D fluctuations on seagrass leaves. IV. Processes at the Shoot Level (mm–cm) When considering the hydrodynamic forces exerted on an individual seagrass shoot, the entire canopy (group of shoots) needs to be taken into consideration. The canopy tends to attenuate currents and waves thereby reducing the forces exerted on individual shoots. Even at the edge of the canopy, seagrass shoots may be sheltered to a certain extent by the presence of adjacent shoots (Granata et al., 2001). It follows that the biomechanical properties of seagrass shoots (a response to the forces exerted on them) are also altered by the canopy characteristics and the capacity of the canopy to attenuate currents and waves. Therefore, a feedback mechanism is expected between seagrass shoots, canopies, and the fluid forces that act on them. A. The Role of Fluid Dynamics in Epiphytic Growth on Seagrass Shoots Epiphytes growing on seagrass leaves are commonly related to the nutrient concentrations in the water column (Frankovich and Fourqurean, 1997). Epiphyte levels are even used as indicators of eutrophication (Stankelis et al., 2003). Unfortunately, little is known about ecological factors (other than light and nutrients) that regulate epiphytic growth on seagrass leaves (Pinckney and Micheli, 1998; see also Borowitzka et al., Chapter 19). Due to the lack of data on the effect of currents on seagrass epiphytes, one can only speculate that epiphyte biomass should increase proportionally with water flow as a result of decreased mass transfer limitation (e.g. Cornelisen and Thomas, 2002). But the interaction between the grazing community and water flow also needs to be taken into consideration as strong currents (and/or high waves) may eliminate grazers allowing more epiphytes to grow under strong flow conditions (an indirect effect of water flow on epiphytes; Schanz et al., 2002). Only a few studies have evaluated the effect of waves on epiphytic loading on seagrass leaves. Although no difference was found in total epiphyte biomass in a wave-exposed and a sheltered seagrass habitat (Pinckney and Micheli, 1998), it seems that the composition of the epiphytic layer is responsive to water flow. Diatoms, coralline, and some filamentous algae dominate under wave-exposed conditions, while blue-green and other filamentous algae dominate under calm conditions (Kendrick and Burt, 1997; Pinckney and Micheli, 1998). This difference has been attributed to the size of the epiphytes on seagrass leaves (i.e. the influence of drag). Natural fluctuations in water flow also affect the epiphytic community. If an epiphytic community develops during relatively calm conditions, species with high drag (i.e. large area exposed to the flow) may become dominant, but if the flow increases over a short period of time (e.g. storms), these epiphytes are then removed (Cambridge, 1979; Biggs, 1996). B. Hydrodynamic Forces Exerted on Shoots and Shoot Biomechanics Our knowledge of the forces exerted by flowing water on seagrass shoots or the biomechanical properties of seagrass shoots is very limited. We know that most seagrasses tolerate a wide range of water motion, from stagnant water to relatively high velocities (100 cm s–1 , Phillips, 1980; Dierssen et al., 2003). In the short-term (minutes), this is likely due to their capacity to bend as the velocity increases thereby minimizing drag (by minimizing the leaf area Chapter 8 Fluid Dynamics in Seagrass Ecology exposed to the flow; Sand-Jensen, 2003). Reproductive shoots of Zostera marina were found to be approximately one order of magnitude stiffer than macroalgae but two to three orders of magnitude less stiff than trees (Patterson et al., 2001), allowing seagrass shoots to bend and, as a result, minimize drag (Fonseca et al., 1982; Sand-Jensen, 2003). In a terrestrial grass (Arundinaria tecta), the sheath contributed 33% of the overall bending stiffness (Niklas, 1998). Perhaps the sheath surrounding the base of seagrass shoots also increases the bending stiffness of seagrass shoots making them stiffer than macroalgae. In the long term (weeks), seagrasses likely acclimate to water flow through growth changes in anatomy and morphology such that drag, breakage, and dislodgement are minimized. Eutrophication has been shown not to alter the tensile strength that Zostera marina leaves can withstand (Kopp, 1999). Another aspect to be considered in the estimation of the drag exerted on seagrass shoots is the epiphytes that colonize their leaves. Epiphytes on a red alga (Odonthalia floccosa) increased the drag exerted on the macrophyte (Ruesink, 1998). It is likely that this would also happen with epiphytes on seagrass shoots. The risk of being dislodged due to excessive drag is highest during storm events when waves and currents are at their maximum (Fd α u 2 ). Massive loss of Zostera marina is expected when currents reach values above 4 m s–1 (Kopp, 1999). One mechanism to cope with this risk seems to be the existence of a few strong (reproductive) seagrass shoots that can resist extreme events and protect the other shoots in a population (Patterson et al., 2001). Within a population, vegetative male shoots of Phyllospadix torreyi tended to be dislodged at lower flows than the female plants (Williams, 1995). The forces exerted on seagrasses exposed to waves are more complex than those in unidirectional flows. As water in waves accelerates in different directions during the course of each wave, organisms exposed to such unsteady flows are subjected to acceleration reaction forces as well as drag (Koehl, 1984). These forces are higher than in unidirectional flows at the same instantaneous velocity (Koehl et al., 1991) and the maximum drag occurs at a different time than the maximum acceleration reaction forces. In these wave-swept environments, a long flexible shape (Fig. 3) can minimize the forces exerted on the anchoring system (roots in the case of seagrasses). This is confirmed by the finding that 201 leaves of Posidonia australis become longer as wave exposure increases (Larkum, 1976). The long leaves tend to move in one direction during the passage of a wave. If the leaves begin to move in the other direction before they are fully extended (Fig. 3), they will sway back and forth with the waves without imposing too much drag on the roots (Koehl, 1984). C. Water Flow Around Seagrass Shoots—Ecological Implications Seagrass shoots are obstructions to flowing water. When considering the vertical scale, seagrass shoots are exposed to a gradient of velocities in the canopy and benthic boundary layers. Due to the no-slip condition, the slowest flows are found near the sediment surface and the strongest flows near the top of the canopy. As a result of this vertical difference in velocities and the horizontal differences in upstream versus downstream velocities around a shoot, a vertical pressure gradient develops on the downstream side of the seagrass shoot: high pressure near the bottom where the currents are relatively slow and low pressure farther up in the water column where currents are stronger. This leads to the development of significant ascending flows (i.e. as high as 15% of ambient) immediately downstream of seagrass shoots (Fig. 4; Nepf and Koch, 1999). Pressure gradients around shoots (Huettel and Gust, 1992) can also lead to the intrusion of water into permeable sediments upstream of the shoot (high pressure zone; Koch and Huettel, 2000) and porewater upwelling downstream of the shoot (low pressure zone) (Nepf and Koch, 1999). For example, around a single Thalassia testudinum shoot exposed to a current speed of 10 cm s–1 , water was found to penetrate 2.5 cm into the permeable sediments (Fig. 4); a depth an order of magnitude larger than that affected by diffusion (Jørgensen and Boudreau, 2001). This flow-induced intrusion of water into seagrass-colonized permeable sediments may bring organic particles (Huettel et al., 1996) closer to the root zone and remove toxic compounds from the sediments such as sulfide (Koch, 1999a). Most of the impact of water intrusion into the sediment occurs over the first 6 h which coincides with semi-diurnal tides (Koch and Huettel, 2000). Therefore, the exchange between the sediments and the water column seems to be maximized in seagrass habitats in which the current direction changes every 6 h. 202 E. W. Koch, J. D. Ackerman, J. Verduin and M. van Keulen Fig. 3. Waving of seagrass leaves in wave-dominated habitats: (A) Phyllospadix torreyi at approximately 2.5 m depth at Punta Morro, Pacific coast of Mexico and (B) Halodule wrightii at approximately 1 m depth, north of Placencia, Belize. The lines were traced over individual leaves in order to emphasize the bending pattern. Note that the leaves are continuously moving back and forth every few seconds with the passage of waves. Photos: E.W. Koch. The combination of the pressure-induced upwelling of porewater and the vertical ascending flows immediately downstream of the seagrass shoots colonizing permeable sediments appear to generate a slow “stream” connecting the sediment porewater and the water column at mid-height in the seagrass canopy (Nepf and Koch, 1999; Fig. 4). Under these circumstances, exchanges between the sediment Chapter 8 Fluid Dynamics in Seagrass Ecology 203 Fig. 4. Vertical ascending flows and porewater flows generated by pressure gradients around a seagrass shoot. As seagrass shoots live in the benthic boundary layer (see velocity (U ) profile on the left), the top of the shoot experiences faster velocities and lower pressure than the bottom of the shoot. As a result, a vertical ascending flow is generated downstream of the shoot. This water then disperses horizontally at the point where the leaves bend over with the flow. Due to the pressure gradients generated on the sediment surface when the flowing water impacts the seagrass shoot, water also penetrates into permeable sediments leading to a zone in which the porewater is washed out by the overlying water. Z , distance above the sediment interface. Modified from Nepf and Koch (1999) and Koch and Huettel (2000). It is possible that the upwelling porewater may be transported high into the water column via the above processes. porewater and the water column are not driven by diffusion but by advection (Huettel and Webster, 2001). This process could benefit the seagrasses by bringing recently remineralized nutrients and carbon to seagrass leaves (Nepf and Koch, 1999). D. The Role of Fluid Dynamics in Seagrass Reproduction Pollination in water (hydrophily) is uncommon in angiosperms, and restricted mostly to the monocotyledons, including the seagrasses (Les et al., 1997; Ackerman, 2000, Chapter 4, this volume). It is relevant to contrast seagrass with their freshwater relatives. Pollination in freshwater plants involves pollen or detached-floating anthers contacting the stigmas of floating or partly submerged carpellate flowers/inflorescences or submerged pollen “showering” (sedimenting) to stigmas from elevated an- thers (Arber, 1920; Sculthorpe, 1967; Cook, 1982). Pollination in seagrasses, however, involves pollination underwater (i.e. hydrophily or submarine pollination), in which pollination occurs through the action of currents (Ackerman, 1995). In some cases (i.e. shallow seagrass populations that may be exposed to the air and the single species Enhalus acaroides), pollination may occur on the water surface (ephydrophily) when the pollen or stamens touch exposed stigmas (Cox, 1988). The concept that surface pollination (or pollination in two dimensions) was responsible for the evolution of seagrass pollination modes (Cox, 1988) is unsound because it assumes that pollen transport is random and, thus, recurrent, which is not the case, as wind generated movements are directional, not random (Ackerman, 1995). Seagrasses possess a number of morphological features that appear to be associated with submerged or submarine pollination, notably their filamentous pollen shapes (Ackerman, 1995), which evolved 204 E. W. Koch, J. D. Ackerman, J. Verduin and M. van Keulen convergently–multiple times in the Najadales and functionally in the Hydrocharitales (Pettitt, 1984; Ackerman, 1995, 2000). Pettitt (1984) reviewed the research pertaining to seagrass pollination biology, but that review was limited taxonomically with respect to pollen transport and capture mechanisms. The situation has improved, but remains largely limited to the mechanistic studies of submarine pollination in the north temperate species, Zostera marina (Ackerman, 1986, 1993, 1995, 1997a,b, and 2002). Fortunately, recent progress has been made with respect to other species including Amphibolis antarctica (Verduin et al., 1996), Posidonia australis and Posidonia sinuosa (Smith and Walker, 2002). The mechanics of pollination in Z. marina were studied in a laboratory flow chamber using stroboscopic photography and in the field using physical models of pollen and adhesive surfaces deployed in the canopy (Ackerman, 1997a,b, 2002). Pollination was found to occur under laminar and relatively viscous conditions at the scale of flowers (i.e. low Re; see Niklas, 1992; Vogel, 1994), and was affected by the emergence of female flowers from within the inflorescence. The emergence of flowers (and other reproductive organs in subsequent phenological processes) led to an increase in the fluid shear stress (τ ) in the local flow (Ackerman, 1997a), which caused the filamentous pollen (2.7 mm × 7.5 µm diameter) to rotate and cross streamlines toward female flowers (Ackerman, 1997b). The axial force responsible for the pollen motion varied directly with the length and aspect ratio of the pollen (Forgacs and Mason, 1958). Consequently, filamentous pollen need only be close to female flowers to pollinate by: (i) direct interception on stigmas; (ii) rotation within one half a pollen length of stigmas; and (iii) by being redirected through streamlines toward flowers (Ackerman, 1997b). Ancestral spherical pollen, on the other hand, could only pollinate via direct interception due to the limited axial force exerted on the spherical-shaped body. Canopy flow conditions at the scale of leaves and flowers were laminar, which indicates that observations would be similar to those in the laboratory flow chamber (Ackerman and Okubo, 1993; Ackerman, 2002). Higher recovery of filamentous pollen models compared to spherical ones also supports the biomechanical model (Ackerman, 2002). Moreover, field observations of pollination in Amphibolis were consistent with the predictions from Z. marina (Verduin et al., 1996), as were results from Posidonia (Smith and Walker, 2002). It is important to note that seagrasses can maintain relatively high outcrossing rates through hydrophily (Ruckleshaus, 1995; Waycott and Sampson, 1997; Reusch, 2000; Waycott et al., Chapter 2). This is especially true for populations found under conditions that promote pollen dispersal, such as exposed bays (e.g. Waycott and Sampson, 1997). It is reasonable to conclude that the strong convergence of filiform pollen morphologies in seagrasses indicates a similar convergence in pollination mechanisms linked to fluid dynamics. Further research from a diversity of seagrass taxa will be needed to determine the validity of this statement. Seed dispersal phenomena in seagrasses are somewhat analogous to pollination mechanisms in that they are poorly recognized but have become better understood in recent years (Van der Pijl, 1972; Orth et al., Chapter 5). This is in part due to the clonal nature of seagrasses in which rhizomatous growth, in addition to anchoring and binding of sediments, was viewed as the principal mechanism of population growth. However, the occurrence of annual populations (e.g. Keddy and Patriquin, 1978), colonization of new areas (e.g. Turner, 1983), and recovery from small and large-scale disturbances (e.g. Rasmussen, 1977; Inglis, 2000) via seeds has led to the realization that seed dispersal is important in this group. There is considerable diversity in seed biology and ecology related to the polyphyletic nature of seagrasses (e.g. Les et al., 1997) and their evolutionary innovations. For example, 7 of the 12/13 genera of seagrasses have dormant seeds, with geocarpy (releasing seeds under the sediments) occurring in Halodule, Cymodocea, and Halophila (Inglis, 2000). Geocarpy appears to facilitate recovery from disturbances in Halodule, where dispersal involves near-bed saltational movements analogous to sediment transport, and high densities of seeds accumulate in dugong feeding depressions (Inglis, 2000). Other species, which have reproductive organs elevated above the seafloor, such as Z. marina, have small, negatively buoyant seeds that sink in still water, and that likely move on the order of 1–10 m horizontally in the water column, depending on the canopy flow (see Okubo et al., 2002). Sometimes seeds (5–13% of seeds in Long Island Sound) are released with a bubble of gas (presumably from the lacunar spaces in the infructescence), which can extend dispersal distances on the order of 10–100 m (Churchill et al., 1985). Longer distance dispersal Chapter 8 Fluid Dynamics in Seagrass Ecology 205 Fig. 5. Vertical velocity (U) profiles (thick solid lines) in seagrass canopies exposed to 5 cm s−1 (A), 10 cm s−1 (B) and 20 cm s−1 (C). Z , distance above the sediment interface. Note that, as velocity increases, the angle of bending of the canopy increases and the canopy height (dashed horizontal line) decreases. Based on a flume experiment using a short (16 cm) and dense (1,000 shoots m−2 ) Zostera marina canopy (Gambi et al. 1990). (e.g. 100 m–10 km) occurs through the floatation of buoyant diaspores (i.e. fruits and seeds) and detached infructescences and/or whole reproductive shoots, which “sweepstake” because of the positive buoyancy provided by the lacunar gas system (e.g. Harwell and Orth, 2002; Lacap et al., 2002; see review in Orth et al., Chapter 5). In the latter case, seeds may be released from the plant while it is floating, or when the plant reaches the shore. Lastly, seeds may be transported in the guts of birds, sea turtles, and fish (e.g. Baldwin and Lovvorn, 1994), leading to potentially large dispersal distances on the order of 100 m–1,000 km, especially in migrating birds. It is interesting to note the morphological/ ecological specializations that evolved in Phyllospadix, which is found in wave-exposed environments where it is a dominant successional species (Wyllie-Echeverria and Ackerman, 2003). In this case, dispersal is facilitated by wave action by an undescribed mechanism, but recruitment is limited to areas that have branching macrophytes with cylindrical thalli onto which the bifid, barbed fruits attach (Turner, 1983). This is a form of obligate facultative succession in that there is no recruitment in the absence of the correct type of turf-forming algae. V. Processes at the Canopy Level (m) Fluid dynamic processes at the canopy level are the most studied and best understood. Based on more than two decades of research, it is well-accepted that seagrass beds attenuate currents and waves and, as a result, tend to accumulate organic and inorganic particles as well as spores and larvae in the canopy. These concepts are now being refined and new questions linking water flow and seagrasses are being addressed. This section provides a general background on classical concepts and then focuses on new trends in fluid dynamics at the canopy level. A. Attenuation of Currents by Seagrass Canopies: A Classical Concept The presence of seagrass canopies in the benthic boundary layer (BBL) alters the roughness of the bottom (Fonseca and Fisher, 1986; Nepf and Vivoni, 2000; Granata et al., 2001). As a result, the vertical flow profile shown in Fig. 1 is altered (Fig. 5), especially when the plants occupy a large portion of the water column, i.e. when H/h <10 (H is the water depth and h the canopy height; Nepf and Vivoni, 2000). Reduced flows are common within the canopy 206 E. W. Koch, J. D. Ackerman, J. Verduin and M. van Keulen Fig. 6. Vertical velocity (U) profile (solid line) showing relative flow intensification near the bottom, which is a result of the vertical seagrass biomass (B) distribution (shaded area). Z , distance above the sediment interface. Adapted from Ackerman and Okubo (1993; Zostera marina). Also observed for Thalassia testudinum (koch, 1996), Amphibolis griffithii (van Keulen, 1997), and Amphibolis antarctica (Verduin and Backhaus, 2000). due to the deflection of the current over the canopy and a loss of momentum within the canopy (Fonseca et al., 1982; Fonseca and Fisher, 1986; Gambi et al., 1990; Koch, 1996; Wallace and Cox, 1997; Koch and Gust, 1999; Verduin and Backhaus, 2000; Peterson et al., 2004). As a result, depending on the seagrass species and shoot density, water speed in the canopy can be 2 to >10 times slower than outside the bed (Ackerman, 1986; Gambi et al., 1990). This process can also trap water within dense seagrass canopies during low tide, leading to a water height difference between vegetated and adjacent unvegetated areas (Powell and Schaffner, 1991). Velocities within seagrass canopies are commonly <10 cm s–1 but can be as high as 100 cm s–1 (see review by Koch, 2001). Even relatively short seagrasses (Zostera novazelandica, 15 cm) or beds with relatively low densities (Zostera marina, 100–200 shoots m–2 ) still seem to reduce velocity (Worcester, 1995; Heiss et al., 2000). When measuring velocities at a relatively fine scale (cm), flow intensification near the bottom (i.e. relatively faster flows in the region of the sheaths or vertical stems, Fig. 6) may be observed depending on the vertical biomass distribution (Ackerman and Okubo, 1993; Koch, 1996; Koch and Gust, 1999; Nepf and Vivoni, 2000; Verduin and Backhaus, 2000; van Keulen and Borowitzka, 2002). This is due to the fact that the sheaths (e.g. Thalassia testudinum and Zostera marina) or stems (e.g. Amphibolis griffithii and A. antarctica) are less effective in reducing the flow and extracting momentum (Fig. 6) than the vegetated regions above the sheaths and stems that are filled with leaves. Similarly, velocities increase near the top of the canopy as the leaf area is reduced and eventually disappears. A number of canopy flow models have been applied to terrestrial plant canopies using empiricallyfit parameters to modify the law of the wall (review in Okubo et al., 2002). This approach has been recently Chapter 8 Fluid Dynamics in Seagrass Ecology 207 Fig. 7. Wave attenuation (open circles) as a function of water depth/tidal fluctuation (black boxes). Wave attenuation was based on the significant wave height in a Ruppia maritima bed in comparison to an adjacent unvegetated area at Bishop’s Head Point, Chesapeake Bay, USA. Note that these data were collected in June when the plants were reproductive. Wave attenuation was highest at low tide when the canopy occupied the entire water column. Negative wave attenuation represents periods in which wave height was larger in the vegetated site than the unvegetated site. Source of data: E.W. Koch. applied to Z. marina with some success, although there were a number of inconsistencies with field observations as would be expected (Abdelrham, 2003; Peterson et al., 2004). This type of approach provides some indication of the general pattern of flow within an eelgrass canopy, but its utility will likely be limited by species-specific differences in canopy vegetative profiles and the lack of detailed studies of canopy flow in these systems. Future development will need to apply the mixing layer analogy. Realistically, the ability to model canopy flow phenomena is a goal that speaks to the need for detailed canopy flow profiles in the laboratory and the field. B. Wave Attenuation by Seagrass Canopies: A Concept in Development tween 20 and 76% over 1 m length when the plants were occupying the entire water depth (Fonseca and Cahalan, 1992), whereas field studies measured values between 1.6 and 80% (Koch, 1996; Prager and Halley, 1999). Our general understanding is that wave attenuation is highest when seagrasses occupy a large portion (>50%) of the water column (Ward et al., 1984; Fonseca and Cahalan, 1992; Fig. 7), but reduction in wave energy (15 s waves) has also been observed in a 5 m deep Amphibolis antarctica bed (Verduin and Backhaus, 2000) and reduction of orbital velocities (3–4 s waves) at a 15 m deep Posidonia oceanica bed (Granata et al., 2001) where the plants occupied only a small portion of the water column. C. Monamis “Seagrasses are able to modify current flow and sediment composition, yet little information exists describing their effect on waves.” This statement with which Fonseca and Cahalan (1992) started their paper more than 10 years ago is still true today. Many papers begin by describing the importance of seagrasses, including their capacity to attenuate waves, but the studies which led to this generalization are few. A flume study measured wave attenuations be- Canopy flow is complex because it is a function of the drag or resistance exerted by the vegetation on the fluid, which is likely to vary spatially due to stem spacing and vertically due to the vegetation profile (Okubo et al., 2002). One important consequence of this realization is the propagation of wavelike oscillations or monamis (mo = aquatic plant; nami = wave; Ackerman and Okubo, 1993) caused 208 E. W. Koch, J. D. Ackerman, J. Verduin and M. van Keulen by Kelvin-Helmholtz instabilities that generate large coherent vortices at the interface between the canopy and the overlaying water column, where the velocity profiles exhibit an inflection point. These vortices can penetrate into the canopy (Ghisalberti and Nepf, 2002) and interact with the flexible and buoyant plants in a hydroelastic response due to the buoyancy created by gas-filled lacunae and propagate downstream over the canopy causing the shoots to wave in a coherent manner (Ghisalberti and Nepf, 2002). This synchronous motion of seagrasses results in enhanced vertical transport between the water column and the canopy (Ghisalberti and Nepf, 2002). The ecological consequence of monamis is the potential to increase larval recruitment (Grizzle et al., 1996) and nutrient uptake. contrast, when seagrasses are exposed to monamis in unidirectional flows, or wave-dominated conditions, the back and forth motion of the leaves (Fig. 8C, D, and E) enhances vertical exchange (Koch and Gust, 1999; Ghisalberti and Nepf, 2002). This suggests that nutrient uptake should be highest at the upper portion of the canopy (Nepf and Vivoni, 2000), but this is also where the oldest and least biologically active portions of the seagrass leaves are located. Perhaps the vertical mixing zone at the top of the canopy is more important in the recruitment process bringing larvae and spores into the canopy (Grizzle et al., 1996) than in the flux of nutrient and carbon molecules. D. Water Flow and Nutrient Uptake in Seagrass Canopies The ecological role of seagrass canopies in the ecology of benthic and pelagic organisms is becoming increasingly clear, especially in the case of crustaceans and fish (e.g. Kenyon et al., 1999; Thayer et al., 1999; Etherington and Eggleston, 2000; Nagelkerken et al., 2001). Many of these organisms are ecologically and economically important species that settle in or on the leaves and shoots of seagrasses as epiphytes for a portion of their life history (Eckman, 1987; Borowitzka and Lethbridge, 1989; Newell et al., 1991; Grizzle et al., 1996). Larval settlement appears to be a function of larval supply (i.e. flux), the fluid dynamic interaction with boundaries on which settlement occurs, and larval behavior (e.g. Abelson and Denny, 1997; Okubo et al., 2002). As indicated above, flows through vegetated areas are quite complex, and consequently, a mechanistic understanding of faunal recruitment in seagrass canopies is lacking at present, although recent efforts have been directed to these ends (e.g. Palmer et al., 2004). Fortunately, there are a number of processes and taxonomic systems including sediment dynamics in which the role of canopy flow has been examined. A recent estimate from the field indicates that the potential for particle contact with a leaf surface approaches certainty under particular flow conditions in a Zostera marina canopy (Ackerman, 2002; see Section IV.D). The situation is more complex in terms of larval settlement. The general pattern that emerges is that settlement is higher in vegetated areas in the case of bivalve larvae (e.g. scallops) settling on Z. marina leaves (Eckman, 1987) and filamentous benthic algae (Harvey et al., 1995). For example, blue mussel recruitment on Z. marina leaves can Nutrient uptake at the canopy level is a function of water velocity. Increasing velocities lead to higher uptake of ammonium in Thalassia testudinum and Halodule wrightii (Thomas et al., 2000) and their epiphytes (Cornelisen and Thomas, 2002). At the same time, as velocity increases, the leaves bend, decreasing the obstruction/friction of the canopy. As a result, the efficiency of the canopy to remove ammonium from the water column decreases at high velocities (Thomas et al., 2000), unless leaf flapping due to monamis or the orbital motion of waves cause mixing within the canopy (Wallace and Cox, 1997; Koch and Gust, 1999; Ghisalberti and Nepf, 2002). The depth that the upper, highly turbulent flow at the top of the canopy (with relatively high nutrient levels) penetrates into the canopy is a function of the percent of the water column that is occupied by the canopy and the density of the shoots (Nepf and Vivoni, 2000). Dense canopies occupying most of the water column have narrow zones of high turbulence “skimming flow” at the top of their canopies. Therefore, the flux of nutrients to areas deep within the canopy may be limited. Mixing and vertical exchange between the water column and the seagrass canopy are a function of the prevailing hydrodynamic conditions and also of how seagrasses respond to them by bending, flexing, waving, etc. When leaves bend under strong currents, the canopy height decreases collapsing the leaves onto each other, “closing” the canopy (Fig. 8A and B) and limiting vertical exchange (Koch and Gust, 1999). In E. Faunal Recruitment in Seagrass Canopies Chapter 8 Fluid Dynamics in Seagrass Ecology 209 Fig. 8. Bending cycles seagrass canopies undergo when exposed to unidirectional (A and B) and oscillatory (C, D and E) flows. During a flood tide, leaves bend in the direction of the flow (A) and hours later, during the ebb tide, leaves bend in the opposite direction (B). These are considered “closed” canopies where conditions within the canopy are relatively stagnant. In contrast, in wave-dominated habitats, seagrass leaves bend in one direction (C), become somewhat upright (D) and bend in the opposite direction (E) in a matter of seconds (wave period). This process leads to rapid “opening” (vertical leaves) and “closing” (bent leaves) of the canopy and enhances the exchange between the canopy and the water column above it (Koch and Gust, 1999). The intermediate phase (D) is non-existent in habitats characterized by swell—leaves just sway back and forth, never becoming upright or fully extended (see Fig. 3A). be considerable (i.e. >90 postlarvae per cm of leaf; Newell et al., 1991; reviewed in Ackerman et al., 1994), and it has been suggested that the monamis facilitate high settlement rates through increasing the likelihood of larval encounter with undulating leaves and the mixing that occurs under monami conditions (Grizzle et al., 1996). Clearly, plant–animal interactions mediated by the interaction of seagrass canopies and fluid dynamics is an important subject where future inquiry is warranted. F. Direct and Indirect Effects of Tides on Seagrass Canopies Seagrasses exist in areas that are affected by tidal flow, which can lead to desiccation of leaves, and limit the depth distribution and light availability of habitats. Tides can also intensify or relieve the effect of waves on seagrass canopies. As indicated in Section II, most of a wave’s energy (orbital velocity) is located near the water surface. Therefore, assuming an equal wave climate, seagrass canopies are exposed to more wave energy during low tides than at high tides (e.g. Ochieng and Erftemeijer, 1999; Koch, 2001; Krause-Jensen et al., 2003; Middelboe et al., 2003). The degree of tidal exposure and the capacity of different seagrass species to tolerate desiccation and high light levels (including ultraviolet-B radiation) affect their minimum depth of distribution (Stapel et al., 1997; Koch, 2001). Additionally, tides also affect the light availability in seagrass habitats. During periods of high or low tide at noon, 210 E. W. Koch, J. D. Ackerman, J. Verduin and M. van Keulen seagrasses are exposed to extreme light levels in the middle of the day and intermediate light levels in the morning and afternoon (ebb or flood), i.e. these plants will be exposed to long hours of saturating light. In contrast, when high tides occur in the morning and afternoon (semi-diurnal tides), the light levels in the middle of the day may be saturating (ebb or flood), but the number of hours of saturating light will be reduced due to the high water during the remainder of the day (Koch and Beer, 1996). These scenarios are also complicated by turbidity (Koch and Beer, 1996). G. Self-Shading in Seagrass Canopies Exposed to Tides, Currents and Waves Although seagrass leaves contain gas-filled lacunae and tend to become erect in the water column, the leaves will comply with the flow generated by tidal currents and waves. During low tide, when seagrass leaves in the intertidal area rest on top of each other, self-shading is at its maximum. This process is reversed as the tide returns to its full level. Under unidirectional flows, the degree of bending in the direction of the flow is a function of the magnitude of the current (Fonseca et al., 1982). It follows that self-shading is expected to be highest when currents are strongest and the leaves are collapsed onto each other. Leaf flapping also occurs under wavedominated conditions (Koch and Gust, 1999), relieving some of the self-shading as flecks of light penetrate the leaf mass or canopy at the frequency of flapping. Short-term (seconds) flecks of light referred to as “lightflecks” (Fig. 9), are also generated in areas exposed to waves. The light that reaches the water surface is focused at the crest of the waves and dispersed at the trough of the waves (Wing and Patterson, 1993; Fig. 9). This results in “dancing lights” in shallow areas such as seagrass beds due to the propagation of lightflecks. The frequency of lightflecks resembles that of the passing waves (Wing and Patterson, 1993). Although the effect of lightflecks on seagrass productivity was never tested, productivity is likely to be enhanced as has been demonstrated in phytoplankton and macroalgae (Dromgoole, 1988; Greene and Gerard, 1990; Wing and Patterson, 1993; Wing et al., 1993). H. Seagrass Canopies as Depositional Environments: Not a Universal Concept Historical evidence of seagrass beds as depositional environments is borne out of the loss of seagrasses (due to wasting disease or grazing) resulting in the erosion of sediments (Rasmussen, 1977; Hine et al., 1987). Many authors suggested that seagrass canopies are areas where sediments deposit and accumulate (Grady, 1981; Almasi et al., 1987; Patterson and Black, 1999; Gacia and Duarte, 2001), largely due to the reduction of velocity and turbulence intensity (e.g. Fonseca et al., 1983; Ackerman and Okubo, 1993; Worcester, 1995; Verduin and Backhaus, 2000; Granata et al., 2001), i.e. a reduction in stress on the sediment surface due to reduced flow speed within the canopy that leads to a reduction in resuspension and thus, an increase in accumulation (Lopez and Garcia, 1998). This accumulation can be seasonal, especially during summer when seagrasses are at their maximum density, but in winter, when the plants disappear or decrease in density, resuspension may be greater than deposition (van Keulen and Borowitzka, 2003). Often, the presence of seagrass rhizomes and roots in the sediment through the winter is sufficient to stabilize the sediments. The size of the seagrass species also affects sediment accumulation. Although bigger species may be better for sediment deposition (Fonseca and Fisher, 1986), small seagrasses such as Halophila decipiens and Zostera novazelandica can still alter the sediments they colonize (Fonseca, 1985, 1989; Heiss et al., 2000). More recent efforts have focused on the role of seagrass canopies in trapping and retaining sediments, which appears to be related to sediment contact with leaves (Gacia et al., 1999; Agawin and Duarte, 2002). Epiphytic layers on seagrass leaves may contribute to the entrapment of particles in seagrass beds by increasing the roughness of the canopy and increasing the boundary layer on the leaf surface; i.e. expanding the area in which water flow is reduced thereby facilitating the entrapment of particles (Vermaat et al., 2000). Whereas, seagrasses are generally viewed as agents that trap particles and stabilize the sediments, resuspension, especially of fine sediments with high organic content, can occur under high wave exposure and current flow (Fonseca et al., 1983; Fonseca and Bell, 1998). In highly waveexposed sites where seagrasses do not attenuate Chapter 8 Fluid Dynamics in Seagrass Ecology 211 Fig. 9. Lightflecks form in areas where the surface of the water is not flat, instead, it has waves (A). The light that reaches the water surface (vertical arrows above wave) is focused by wave crests and is dissipated by wave troughs. In the area where the light is focused, lightflecks form. Under the right combination of water depth and wavelength (i.e. water depth in the focusing range), lightflecks can be observed on the seafloor as seen in a shallow Thalassia testudinum bed in the Florida Keys, USA (B). Photo: E.W. Koch. 212 E. W. Koch, J. D. Ackerman, J. Verduin and M. van Keulen Fig. 10. Patch of Zostera marina at Crown Breach, Alameda, California, USA, containing coarser sediment than the surrounding area. This may be a result of turbulence generated by the seagrass leaves (Koch, 1993). As a result, finer particles are resuspended while coarser particles remain. Note that this patch was located at a water depth of 0.9 m and is a single genet (i.e. a true clonal unit) as it originated from one single seed that germinated in February 2003. Photo taken in August 2003 by Mark Fonseca. water flow as effectively as in unidirectional (tidal) flows (Koch and Gust, 1999), sediment characteristics within and outside seagrass beds differed little to none (Hoskin, 1983; Edgar and Shaw, 1991; Koch, 1999b; van Keulen and Borowitzka, 2003). Actually, in some cases, sediment in a vegetated area can be coarser than in the adjacent unvegetated area (Koch, 1993; Fig. 10). VI. Hydrodynamically-Mediated Processes at the Landscape Level (100–1000 m) A number of studies have analyzed how seagrass canopies alter local hydrodynamic conditions and, with that, affect their own productivity, associated biota, sediments, and the water column surrounding them. In contrast, hydrodynamic studies in sea- grass habitats at the landscape level are less common. While most studies at the canopy level assume that the shoot density is homogenous (Vidono et al., 1997), at the landscape level, it is becoming clear that seagrasses are spatially heterogeneous (Robbins and Bell, 1994). In this section, we address flow-related causes of seagrass heterogeneity and hydrodynamic consequences of seagrass patchiness. A. Seagrass Landscapes and the Substrates they Colonize Although seagrass landscapes represent a simpler system than terrestrial landscapes in terms of species diversity and structure (Robbins and Bell, 1994), a mosaic of different seagrass species, shoot characteristics, associated biota, and sediment elevations and types exist. Responses of individual plants to water Chapter 8 Fluid Dynamics in Seagrass Ecology 213 Fig. 11. Diagram of seagrass distribution in habitats characterized by high wave energy. In shallows areas where waves are felt on the bottom (1), sediment movement is constant (arrows) not allowing seagrasses to become established. In this area (1), some seagrasses are capable of colonizing non-shifting substrates such as rocks. In contrast, in deeper areas sheltered from the waves (2, i.e. below the maximum wave penetration depth represented by the dashed line), sediment movement is reduced allowing seagrasses to become established. The maximum depth of distribution of the seagrasses is limited by light availability (3). motion accumulate and may be the basis of seagrass landscape patterns perceived at coarser scales of resolution (Fonseca, 1996). Hydrodynamic forces may also affect seagrass habitat requirements such as light availability, sediment characteristics, and substrate stability (Ben Alaya, 1972; Cooper, 1982; van Katwijk and Hermus, 2000; Fig. 10), thereby altering the pattern of distribution even further (feedback). In shallow areas with relatively high wave energy, the substrate is usually characterized by coarse shifting sand (Dan et al., 1998) and/or rocks. The shifting sediments remain unvegetated due to continuous erosion and burial of recruits (Shepherd and Robertson, 1989; Hemminga and Duarte, 2000; Frederiksen et al., 2004). Some seagrasses are able to colonize rocks (a stable substrate) in these shallow, high wave-energy areas by modifying their root system. The genus Phyllospadix, which colonizes the rocky intertidal in the north Pacific (WyllieEcheverria and Ackerman, 2003), is an example of this. However, in Corsica (Mediterranean), Posidonia oceanica is found on rocks in shallow areas where sand grains are moving back and forth every few seconds due to the passage of waves (Fig. 11) (Koch, personal observation), yet it colonizes soft substrates at depths below the maximum wave penetration depth. Other seagrasses capable of colonizing hard as well as soft substrates are Thalassodendron ciliatum (Bandeira and Nilsson, 2001) in Mozambique (Bandeira, 2002) and Amphibolis antarctica in Australia (Ducker et al., 1977). What makes one species more adaptable to different substrates than others is presently unknown. Landscape level studies for seagrasses on rocky substrates are limited; therefore, the remaining discussion will address seagrass meadows colonizing soft substrates. B. Hydrodynamically Generated Patchiness in Seagrass Meadows The mosaic of patterns observed in seagrass landscapes is often a result of natural perturbations such as erosion and burial by sand waves (Harlin and Thorne-Miller, 1982; Fonseca et al., 1983; Marbà et al., 1994; Marbà and Duarte, 1995; Fonseca and Bell, 1998; Bell et al., 1999; Fig. 12) and/or disturbances caused by fauna (Orth, 1975; Ogden, 1980; Preen, 1995), storms (Preen et al., 1995; Fonseca and Bell, 1998) and/or disease (den Hartog, 1987). Anthropogenic causes (eutrophication, boat and mooring scars, fishing gear scars) can also contribute to seagrass patchiness (Cambridge, 1975; Walker et al., 1989; Creed and Filho, 1999; Orth et al., 2002). Here we will focus on flow-related generation of patchiness. 214 E. W. Koch, J. D. Ackerman, J. Verduin and M. van Keulen Fig. 12. Complex seagrass landscape due to the presence of sand waves (arrow) in a Zostera marina bed at Horn Harbor, Chesapeake Bay, USA. Photo: R.J. Orth. The disturbances that lead to patchiness in seagrass landscapes range in scale from the complete but local destruction of seagrass ecosystems (Dan et al., 1998) to the creation of smaller (10’s of meters) unvegetated depressions in continuous meadows, termed “blowouts” (Patriquin, 1975; see review in Short and Wyllie-Echeverria, 1996; Fonseca and Bell, 1998). The magnitude and frequency of disturbances is what determines the degree of patchiness of a seagrass meadow (Fonseca et al., 1983; Fonseca and Bell, 1998; Hemminga and Duarte, 2000). It can therefore be assumed that more extreme events would result in erosion and complete or partial loss of seagrasses (with little recovery), whereas periods of reduced disturbance may result in coalescence of the patches and the formation of more continuous meadows (Fonseca et al., 1983; Kirkman and Kirkman, 2000). This concurs with numerous reports of widespread loss of meadows as a result of hurricanes and cyclones (Birch and Birch, 1984; Williams, 1988; Rodriguez et al., 1994; Preen et al., 1995; Moncreiff et al., 1999; Whitfield et al., 2002), and the extensive colonization of seagrasses (pioneering or climax species) during periods of reduced disturbance (Kirkman, 1985; Kendrick et al., 2000). Note that some studies report no damage to seagrasses after the passage of hurricanes (Thomas et al., 1961; Tilmant et al., 1994; Dawes et al., 1995). In areas with continuous high wave energy, seagrass ecosystems can be: (i) non-existent (Dan et al., Chapter 8 Fluid Dynamics in Seagrass Ecology 1998); (ii) depth restricted (when sufficient light is available, seagrasses colonize areas below the maximum wave penetration depth; Krause-Jensen et al., 2003; Middelboe et al., 2003); (iii) dominated by more robust species (e.g. Amphibolis griffithii and Posidonia coriacea); and (iv) patchier as the disturbance of high waves may hinder the lateral expansion of some seagrass beds (Kendrick et al., 2000; Frederiksen et al., 2004). In contrast, in sheltered waters, seagrass meadows tend to be more continuous and are colonized by relatively more fragile species (e.g. some Posidonia spp) (Kirkman and Kuo, 1990). Under calm conditions, creation of openings in meadows appears not to lead to further wide-scale loss, although regrowth into the damaged areas can be slow (Walker et al., 1989; Meehan and West, 2000; Orth et al., 2002). The degree of wave exposure can be quantified by applying the relative wave exposure index (REI) first developed by Keddy. This index takes into account the wind direction and intensity and fetch and has been successfully linked to landscape features in seagrass habitats (Fonseca and Bell, 1998; Fonseca et al., 2000, 2002; Hovel et al., 2002; Krause-Jensen et al., 2003; Frederiksen et al., 2004). When wave-dissipating structures (e.g. sand bars, sills, coral or oyster reefs) occur in the seagrass system, the bathymetry may also have to be taken into account in order to properly estimate the wave exposure using the REI. A mixture of unvegetated and densely vegetated areas in close proximity may characterize intermediate disturbance regimes. For example, Posidonia sinuosa meadows in habitats of moderate water flow are characterized by dense rows of plants interchanged with strips of bare sand (Bridgwood, 2002). A similar gradient of patterns has been reported for meadows of Zostera marina subject to gradients in velocity and wave energy (Fig. 12), with the proposal that the structural integrity of the habitat would deteriorate with increasing habitat fragmentation (den Hartog, 1971; Fonseca et al., 1983; Fonseca and Bell, 1998). Another common cause for complex seagrass mosaic patterns is the hydrodynamically-mediated movement of sand waves and sand dunes through seagrass meadows (Marbà et al., 1994; Walker et al., 1996; Bridgwood, 2002; Paling et al., 2003; van Keulen and Borowitzka, 2003; Frederiksen et al., 2004). Changes in sediment height, a result of water flow, can be significant and rapid (10’s of cm over periods of hours) (Paling et al., 2003), and larger sand 215 dunes can travel through meadows on a time scale of months (Walker et al., 1996; Bridgwood, 2002; van Keulen and Borowitzka, 2003). The degree to which these large amounts of sediment negatively affect the seagrasses creating unvegetated patches depends on their tolerance for sedimentation, the amount of sediment deposited, and the period the plants remain buried. Sedimentation rates of 2 to 13 cm year–1 can be coped with by large (e.g. Enhalus acoroides) as well as by fast growing (e.g. Halophila) seagrasses as well as by plants with vertical stem elongation (e.g. Cymodocea nodosa, C. serrulata and Syringodium isoetifolium) (Vermaat et al., 1996). Subaqueous dune migration appears to maintain Cymodocea meadows in a continuous state of colonization which is ultimately responsible for the characteristic patchy landscape (Marbà and Duarte, 1995). Even when sediments completely cover the leaves of small, slow-growing plants, some seagrasses are able to survive as long as the sediment is removed by currents or waves in a matter of weeks (Halodule wrightii survived after being buried for 2 months; Phillips, 1980). Other seagrasses such as Posidonia oceanica are able to increase vertical growth from 5 to 7 mm year–1 to 52 mm year–1 when (partially) covered by sand waves (Boudouresque and de Grissac, 1983). In contrast, Zostera marina seems to have little or no tolerance to sedimentation regardless of the sediment type (Mills and Fonseca, 2003). C. Effect of Patchiness on Flow and Flow-Related Processes When considering processes in seagrass meadows, spatial homogeneity is usually assumed, but in nature, patchy seagrass landscapes are more common than homogenous ones. This patchiness may have a major effect on physical, geological, chemical, and biological processes. For example, gaps in the canopy allow an accelerated influx of water into the canopy (Granata et al., 2001), replenishing nutrients, introducing spores and propagules, eroding sediment and increasing mixing in general. The distance currents can penetrate the edge of a seagrass bed before becoming equilibrated with respect to momentum has been estimated to be between 1 m (Fonseca and Fisher, 1986) and 50 boundary layers (assumed to be equal to the height of the canopy; Nowell and Jumars, 1984; Granata et al., 2001). 216 E. W. Koch, J. D. Ackerman, J. Verduin and M. van Keulen These values can be affected by the density of the bed and the vertical distribution of biomass. In dense beds, unidirectional water flow is smoothly directed over the top of the seagrass canopy as “skimming flow” (Nowell and Jumars, 1984; Fonseca and Kenworthy, 1987), effectively trapping a layer of water within the canopy (Koch and Gust, 1999), i.e. increasing the residence time. Under such conditions, nutrient concentrations within the vegetation may be quite low (Moore et al., 1996). In contrast, a reduction in shoot density leads to increased flow intrusion and velocity within the canopy (van Keulen, 1997). Therefore, reducing seagrass density could permit an increase in turbulence and mixing within the meadow, with an associated increase in nutrient exchange and uptake, and the potential for increased sediment resuspension. This subject needs further attention. VII. Hydrodynamic Processes at the Meso-Scale Level (>1,000 m) A. Seagrasses in the Biosphere Seagrass meadows are one of several plant communities found in coastal areas around the world. Marshes and mangroves line the intertidal area of shorelines of seagrass-colonized temperate and tropical systems, respectively. The hydrodynamic functions of each of these communities can be quite similar: attenuation of currents and waves leading to deposition of particles and the stabilization of the substrate (Knutson et al., 1982; Knutson, 1988; Massel et al., 1999; Möller et al., 1999). When considering these communities as a part of a larger coastal ecosystem, interactions between seagrasses and marshes/mangroves as well as with adjacent animal communities such as oyster and coral reefs start to emerge (see Section VII.B). Water masses may have traveled over extensive distances, interacting with pelagic and benthic organisms before they reach seagrass beds. For example, during the flood tide, water masses may travel over sediments colonized by a variety of microalgae and benthic organisms such as a coral polyps and reefs before reaching the seagrass bed. In contrast, during ebb flow, the water that reaches seagrass beds may have resided in an estuary, a mangrove, or a marsh system for a period of time. Each of these plant and animal communities tends to alter the water mass in its chemical and/or physical properties directly or indirectly (Bulthuis et al., 1984). When these waters are then transported into seagrasses meadows, they also affect these plant communities. Therefore, a link between seagrasses and adjacent plant and animal communities is expected. B. Linking Seagrasses and Adjacent Communities via Water Flow 1. Linking Seagrasses and Adjacent Systems via Tidal Fluxes Tidal flows link terrestrial, estuarine, and marine systems. The residence time of a water mass in a seagrass habitat (determined by the tidal fluxes) may have a profound effect on seagrass distribution. Short residence times (days) allow pollutants and excess nutrients to be flushed out of a system before harming seagrasses (Kitheka et al., 1996). In contrast, long residence times promote the accumulation of nutrients and the growth of phytoplankton and nuisance algae while suppressing the growth of seagrasses via low light availability (Rysgaard et al., 1996; Herbert, 1999). Coral reefs, seagrass beds, and mangrove forests often co-occur in tropical coastal systems suggesting an interaction of sorts, determined by tidal flows. For example, coastal wetlands such as marshes and mangroves assimilate nutrients leaching from land and thereby reduce the nutrient level reaching adjacent seagrass systems (Valiela and Cole, 2002) during ebb flows. These authors suggested that landderived N loads from 20 to 1,000 kg N ha−1 year–1 seem to be a critical range for seagrass survival in shallow waters. When N loads are higher, wetlands are no longer able to remove sufficient N through denitrification, and N burial, and tidal currents will carry the excess nutrients into the seagrass beds. Excess nutrients can then lead to the loss of the seagrasses. Therefore, adjoining plant systems (wetlands and seagrasses) are not isolated units but are likely to be linked (Valiela and Cole, 2002). Seagrass beds are among the most productive systems on the planet (Dring, 1994) and experience relatively low grazing losses with most leaf production being shed (Cebrian and Duarte, 2001; Mateo et al., Chapter 7). This amounts to a considerable Chapter 8 Fluid Dynamics in Seagrass Ecology quantity of detrital material which can remain within the seagrass meadow or can be exported. The fate of seagrass detritus depends, to a large extent, on the magnitude of currents, waves, and tides (Ochieng and Erftemeijer, 1999) and the nature of the leaves: some leaves float on becoming detached while others sink (Zieman et al., 1979). Floating leaves are more likely to be exported by tidal currents, but leaves that sink and form detritus locally may also be exported onto adjacent beaches or the deep sea during storm events and/or spring tides (Hemminga and Nieuwenhuize, 1990; Kirkman and Kendrick, 1997; Ochieng and Erftemeijer, 1999). It appears that in many instances detritus remains within the originating ecosystem, being recycled more or less in situ (Hemminga and Nieuwenhuize, 1991; Paling, 1991). In other cases, large amounts of seagrass detritus are transported into adjacent estuaries contributing to the estuarine carbon cycle (Bach et al., 1986; Cebrian and Duarte, 2001; Mateo et al., Chapter 7). Seagrass fragments have even been found at great depths in ocean basins (>1,000 m) where, it is postulated, they comprise an important food source for a number of invertebrate detritivores (Menzies et al., 1967; Menzies and Rowe, 1969; Wolff, 1976, 1979; Suchanek et al., 1985), as well as pelagic fishes and crustaceans (Williams et al., 1987). Litter washed up onto beaches also supports a wide range of invertebrates (Kirkman and Kendrick, 1997; Ochieng and Erftemeijer, 1999), and the location where the litter is deposited (high tide line or storm line) determines where invertebrates will find the highest availability of food. Litter that remains in shallow waters provides protection from erosion (Ochieng and Erftemeijer, 1999) and a habitat for juvenile fish (Lenanton et al., 1982; Robertson and Lennaton, 1984), but the reliability of this habitat depends on the local hydrodynamic conditions. Tidal flows do not only link adjacent communities but can also isolate them. For example, in an estuary in Kenya, organic particles efflux and reflux between mangroves and seagrasses during each tidal cycle (Hemminga et al., 1994). During the ebb, POM effluxes from the mangroves reaching the seagrasses; during the flood, particles resuspended in the seagrass meadow (in part, particles generated in the mangroves and deposited in the seagrasses) reach the mangroves (Hemminga et al., 1994). These particles never make it to the adjacent coral reef 217 due to trapping of the high turbidity plume by the tide and onshore winds (Fig. 13; Kitheka, 1996; Kitheka et al., 1996; Miyajima et al., 1998). Turbid waters could be detrimental to the reef-forming coral polyps (Johannes, 1975). As a result of the wave attenuation by the coral reef and the tidal isolation of the corals, mangroves, seagrasses and the coral reef can co-exist just a few kilometers apart along the Kenyan coast. This process is likely to also apply to other reef–seagrass–mangrove associations throughout the world. 2. Linking Seagrasses and Adjacent Ecosystems via Wave Attenuation Several plant and animal communities (mangroves, marshes, corals, and oyster reefs) adjacent to seagrass meadows tend to attenuate waves, protecting shorelines from erosion (Knutson et al., 1982; Knutson, 1988; Massel et al., 1999; Möller et al., 1999). The decrease in waves by mangroves and marshes leads to sediment deposition (Othman, 1994) and, consequently, reduced water turbidity. A mangrove forest as narrow as 50–150 m can completely attenuate wave heights of up to 1 m (Othman, 1994), while a marsh can attenuate more than 80% of the incoming wave energy (Möller et al., 1999). Theoretically, seagrasses could benefit from this wave reduction especially during ebb flows as the water mass that resides in the mangroves or marshes will have lower turbidity. In turn, sub-tidal seagrass meadows adjacent to mangroves and marshes can minimize the impact of waves on marshes and mangroves via wave attenuation (van Katwijk, 2000). Seagrasses also require relatively sheltered conditions in order to become established and thrive (Fonseca and Bell, 1998; Robbins and Bell, 2000; Koch, 2001), conditions that may have been previously found in the shelter of the once extensive oyster reefs in Chesapeake Bay (USA) and of sand bars in Tampa Bay (USA) (Lewis, 2002). Whereas some wave attenuation is expected to be beneficial for seagrass establishment, excessive wave attenuation may also be detrimental to seagrasses. When wave energy is extremely low, sediments tend to be relatively fine and to have elevated organic content (Wanless, 1981; Almasi et al., 1987; Fonseca, 1996; Fonseca and Bell, 1998), conditions which are not always favorable to seagrasses (Koch, 2001). 218 E. W. Koch, J. D. Ackerman, J. Verduin and M. van Keulen Fig. 13. Hydrodynamic link (or lack thereof) between a coral reef, seagrass bed and mangrove forest in Gazi Bay (Kenya) via the flux of oceanic water, seagrass-affected water and mangrove-affected water during a neap high tide (a), a spring low tide (b), and a neap low tide (c). E and Q f refer to evaporation and freshwater input, respectively. Note that when the tide is rising (flood) during a neap high tide (a), the oceanic water (OW) moves over the coral reef into the seagrass habitat pushing the seagrass-affected water (SGW—open circles) toward the mangrove habitat and the mangrove-affected water (MW—dots) is restricted to the mangrove forest. In contrast, during a spring low tide (b), the oceanic water is restricted to the area offshore from the coral reef, the seagrass-affected water extends to the coral reef and the mangrove affected water covers the seagrass and mangrove habitats (but does not reach the coral reef). If only a neap low tide (c) occurs, the oceanic water penetrates farther into the lagoon than during the spring low tide and the seagrass-affected water remains in the seagrass habitat, not reaching the coral reef. Under these conditions, the mangrove-affected water extends somewhat into the seagrass habitat but not to the same extent as during the spring low tide. Source: Kitheka (1997). [Reproduced with permission from Academic Press/Elsevier]. VIII. Summary and Outlook Fluid dynamics is an essential component of seagrass ecology as it affects every aspect of the plants and their habitats, from the smallest to the largest scales. Over the last decades, we have begun to understand how seagrass beds attenuate waves and currents. Now we begin a new phase of fine tuning previous findings and revising classical concepts. This is leading to exciting new developments such as (i) how currents interact with seagrass canopies as if the plants were part of a mixing layer instead of only a perturbation in the benthic boundary layer; (ii) the relative role of deposition and resuspension in seagrass beds, which may be quite dynamic; and (iii) how the aforementioned processes are affected by unsteady conditions. It is also becoming clear that not all seagrasses have the same biomechanical properties, and major differences exist in the extent to which different seagrasses influence, Chapter 8 Fluid Dynamics in Seagrass Ecology and are influenced by, water flow. Vegetated flows are amongst the most complicated and least understood types of water flow which makes this subject a great gateway for exciting new developments and advancements in science. Acknowledgments Dr. Heidi Nepf, Dr. Mark Fonseca, and an anonymous reviewer provided valuable comments on an earlier draft of the manuscript. Evamaria Koch would like to thank the Cooperative Institute for Coastal and Estuarine Environmental Technology (CICEET) for financial support to collect the data presented in Fig. 7. Joe Ackerman would like to acknowledge the support of funds from NSERC and the Canada Research Chair program. Tracey Saxby is thanked for making the figures for this chapter. References Abdelrham MA (2003) Effects of eelgrass Zostera marina canopies on flow and transport. Mar Ecol Prog Ser 248: 67–83 Abelson A and Denny M (1997) Settlement of marine organisms in flow. Annu Rev Ecol Systematics 28: 317–39 Ackerman JD (1986) Mechanistic implications for pollination in the marine angiosperm, Zostera marina L. Aquat Bot 24: 343–353 Ackerman JD (1993) Pollen germination and pollen tube growth in the marine angiosperm, Zostera marina L. Aquat Bot 46: 189–202 Ackerman JD (1995) Convergence of filiform pollen morphologies in seagrasses: Functional mechanisms. Evol Ecol 9: 139– 153 Ackerman JD (1997a) Submarine pollination in the marine angiosperm, Zostera marina: Part I. The influence of floral morphology on fluid flow. Am J Bot 84: 1099–1109 Ackerman JD (1997b) Submarine pollination in the marine angiosperm, Zostera marina: Part II. Pollen transport in flow fields and capture by stigmas. Am J Bot 84: 1110–1119 Ackerman JD (2000) Abiotic pollen and pollination: Ecological, functional, and evolutionary perspectives. Plant Systematics Evol 222: 167–185 Ackerman JD (2002) Diffusivity in a marine macrophyte bed: Implications for submarine pollination and dispersal. Am J Bot 89: 1119–1127 Ackerman JD and Hoover T (2001) Measurement of local bed shear stress in streams using a Preston-static tube. Limnol Oceanogr 46: 2080–2087 Ackerman JD and Okubo A (1993) Reduced mixing in a marine macrophyte canopy. Funct Ecol 7: 305–309 Ackerman JD, Sim B, Nichols SJ and Claudi R (1994) A review of the early life history of the zebra mussel (Dreissena polymorpha): Comparisons with marine bivalves. Can J Zool 72: 1169–1179 219 Agawin NSR and Duarte CM (2002) Evidence of direct particle trapping by a tropical seagrass meadow. Estuaries 25: 1205– 1209 Almasi MN, Hoskin CM, Reed JK and Milo J (1987) Effects of natural and artificial Thalassia on rates of sedimentation. J Sedimentary Petrology 57: 901–906 Arber A (1920) Water Plants, A Study of Aquatic Angiosperms. Cambridge University Press, Cambridge Bach SD, Thayer GW and Lacroix MW (1986) Export of detritus from eelgrass (Zostera marina) beds near Beaufort, North Carolina, USA. Mar Ecol Prog Ser 28: 265–278 Baldwin JR and Lovvorn JR (1994) Expansion of seagrass habitat by the exotic Zostera japonica, and its use by dabbling ducks and brant in Boundary Bay, British Columbia. Mar Ecol Prog Ser 103: 119–127 Bandeira SO (2002) Leaf production rates of Thalassodendron ciliatum from rocky and sandy habitats. Aquat Bot 72: 13–24 Bandeira SO and Nilsson PG (2001) Genetic population structure of the seagrass Thalassodendron ciliatum in sandy and rocky habitats in southern Mozambique. Mar Biol 139: 1007–1012 Beer S and Koch EW (1996) Photosynthesis of seagrasses vs. marine macroalgae in globally changing CO2 environments. Mar Ecol Prog Ser 141: 199–204 Bell SS, Robbins BD and Jensen SL (1999) Gap dynamics in a seagrass landscape. Ecosystems 2: 493–504 Ben Alaya H (1972) Repartition et conditions d’installation de Posidonia oceanica et Cymodocea nodosa dans le golfe de Tunis. Bull Inst Natl Sci Tech Oceanogr Peche Salammbo 2: 331–416 Biggs BJF (1996) Hydraulic habitat of plants in streams. Regulated Rivers Res Manag 12: 131–144 Birch WR and Birch M (1984) Succession and pattern of tropical intertidal seagrasses in Cockle Bay, Queensland, Australia: A decade of observations. Aquat Bot 19: 343–367 Borowitzka MA and Lethbridge RC (1989) Seagrass epiphytes. In: Larkum AWD, McComb AJ and Shepherd SA (eds) Biology of Seagrasses, pp 458–499. Elsevier, Amsterdam, The Netherlands Boudouresque CF and de Grissac J (1983) Seagrass populations (Posidonia oceanica) in the Mediterranean: Interactions between plants and sediments. J de Recherché Oceanographique. Paris 8: 99–122 Boudreau BP and Jørgensen BB (2001) The Benthic Boundary Layer. Oxford University Press, New York Bridgwood SD (2002) The structure and function of windrows in meadows of the seagrass Posidonia sinuosa. Honours Thesis, Murdoch University Bulthuis D, Brand GW and Mobley MC (1984) Suspended sediments and nutrients in water ebbing from grass-covered and denuded tidal mudflats in an Australian embayment. Aquat Bot 20: 257–266 Cambridge ML (1975) Seagrasses of south-western Australia with special reference to the ecology of Posidonia australis in a polluted environment. Aquat Bot 1: 149–161 Cambridge ML (1979) Technical report on seagrasses. Department of Conservation and Environment, Perth, Western Australia, Cockborn Sound Environmental Study Report 7: 100 pp Cebrian J and Duarte CM (2001) Detrital stocks and dynamics of the seagrass Posidonia oceanica in the Spanish Mediterranean. Aquat Bot 70: 295–309 220 E. W. Koch, J. D. Ackerman, J. Verduin and M. van Keulen Churchill AC, Nieves G and Brenowitz AH (1985) Floatation and dispersal of eelgrass seeds by gas bubbles. Estuaries 8: 352–354 Cook CDK (1982) Pollination mechanisms in the Hydrocharitaceae. In: Symoens JJ, Hooper S and Compère P (eds) Studies on Aquatic Vascular Plants, pp 1–15. Royal Botanical Society of Belgium, Brussels Cooper G (1982) Reimplantation de Posidonia oceanica— protection des implants. Bull Ecol 13: 65–73 Cornelisen CD and Thomas FIM (2002) Ammonium uptake by seagrass epiphytes: Isolation of the effects of water velocity using an isotope label. Limnol Oceanogr 47: 1223–1229 Cox PA (1988) Hydrophilous pollination. Annu Rev Ecol Systematics 19: 261–280 Creed JC and Filho GMA (1999) Disturbance and recovery of the macroflora of a seagrass (Halodule wrightii Ascherson) meadow in the Abrolhos Marine National Park, Brazil: An experimental evaluation of anchor damage. J Exp Mar Biol Ecol 235: 285–306 Dan A, Moriguchi A, Mitsuhashi K and Terawaki T (1998) Relationship between Zostera marina beds and bottom sediments, wave action offshore in Naruto, southern Japan (Original Title: Naruto chisaki ni okeru amamo-ba to teishitsu oyobi haro tono kankei). Fisheries Eng (Japan)/Suisan Kogaku (Japan) 34: 299–304 Daugherty RL, Franzini JB and Finnemore EJ (1985) Fluid Mechanics with Engineering Applications, 8th ed. McGraw-Hill, New York Dawes CJ, Bell SS, Davis RA, McCoy ED, Mushinsky HR and Simon JL (1995) Initial effects of Hurricane Andrew on the shoreline habitats of southwestern Florida. J Coastal Res 21: 103–110 den Hartog C (1971) The dynamic aspect in the ecology of sea-grass communities. Thalassia Jugoslavica 7: 101– 112 den Hartog C (1987) “Wasting disease” and other dynamic phenomena in Zostera beds. Aquat Bot 27: 3–14 Denny MW (1988) Biology and the Mechanics of the WaveSwept Environment.Princeton University Press, Princeton, NJ Dierssen H, Zimmerman R, Leathers R, Downesand T and Davis C (2003) Ocean color remote sensing of seagrass and bathymetry in the Bahamas Banks by high-resolution airborne imagery. Limnol Oceanogr 48: 444–455 Dring MJ (1994) The Biology of Marine Plants. Cambridge University Press, Cambridge Dromgoole FI (1988) Light fluctuations and the photosynthesis of marine algae. II. Photosynthetic response to frequency, phase ratio and amplitude. Funct Ecol 2: 211–219 Ducker SC, Foord NJ and Knox RB (1977) Biology of Australian seagrasses: The genus Amphibolis C. Agardh (Cymodoceaceae). Aust J Bot 25: 67–95 Eckman JE (1987) The role of hydrodynamics in recruitment, growth and survival of Argopecten irradians (L.) and Anomia simplex (D’Orbigny) within eelgrass meadows. J Exp Mar Biol Ecol 106: 165–191 Edgar GJ and Shaw C (1991) Inter-relationships between sediment, seagrasses, benthic invertebrates and fishes in shallow marine habitats off South-Western Australia. The Marine Flora and Fauna of Rottnest Island, Western Australia, pp 429–442. Western Australian Museum, Perth, Western Australia Etherington LL and Eggleston DB (2000) Large-scale blue crab recruitment: Linking postlarval transport, post-settlement planktonic dispersal, and multiple nursery habitats. Mar Ecol Prog Ser 204: 179–198 Finnigan J (2000) Turbulence in plant canopies. Annu Rev Fluid Mech 32: 519–571 Fischer HB, List EJ, Koh RCY, Imberger J and Brooks NH (1979) Mixing in Inland and Coastal Waters. Academic Press, San Diego Fonseca MS (1985) The use of flume to measure stability of deepwater seagrass (Halophila decipiens) meadows. Estuaries 8: 75A Fonseca MS (1989) Sediment stabilization by Halophila decipiens in comparison to other seagrasses. Estuarine Coastal Shelf Sci 29: 501–507 Fonseca Mark S (1996) Scale Dependence in the Study of Seagrass Systems. pp 95–104. In: John Kuo, Ronald C. Phillips, Diana L. Walker and Hugh Kirkman (eds.), Seagrass Biology, Proceedings of an International Workshop, Western Australia, January 25–29, 1996. Fonseca MS and Bell SS (1998) Influence of physical setting on seagrass landscapes near Beaufort, North Carolina, USA. Mar Ecol Prog Ser 171: 109–121 Fonseca MS and Cahalan JA (1992) A preliminary evaluation of wave attenuation for four species of seagrass. Estuarine Coastal Shelf Sci 35: 565–576 Fonseca MS and Fisher JS (1986) A comparison of canopy friction and sediment movement between four species of seagrass with reference to their ecology and restoration. Mar Ecol Prog Ser 29: 15–22 Fonseca MS, Fisher JS, Zieman JC and Thayer GW (1982) Influence of the seagrass, Zostera marina, on current flow. Estuarine Coastal Shelf Sci 15: 351–364 Fonseca MS and Kenworthy WJ (1987) Effects of current on photosynthesis and distribution of seagrasses. Aquat Bot 27: 59–78 Fonseca MS, Kenworthy WJ and Whitfield PE (2000) Temporal dynamics of seagrass landscapes: A preliminary comparison of chronic and extreme disturbance events. In: Pergent G, Pergent-Martini C, Buia MC and Gambi MC (eds) Proceedings 4th International Seagrass Biology Workshop, Sept. 25–Oct. 2, 2000, pp 373–376. Corsica, France Fonseca MS, Whitfield PE, Kelly NM and Bell SS (2002) Modeling seagrass landscape pattern and associated ecological attributes. Ecol Appl 12: 218–237 Fonseca MS, Zieman JC, Thayer GW and Fisher JS (1983) The role of current velocity in structuring seagrass meadows. Estuarine Coastal Shelf Sci 17: 367–380 Forgacs OL and Mason SG (1958) The flexibility of wood-pulp fibers. TAPPI 41: 695–704 Frankovich TA and Fourqurean JW (1997) Seagrass epiphyte loads along a nutrient availability gradient, Florida Bay, USA. Mar Ecol Prog Ser 159: 37–50 Frederiksen M, Krause-Jensen D, Holmer M and Laursen JS (2004) Spatial and temporal variation in eelgrass (Zostera marina) landscapes: Influence of physical setting. Aquat Bot 78: 147–165 Gacia E and Duarte CM (2001) Sediment retention by a Mediterranean Posidonia oceanica meadow: The balance between deposition and resuspension. Estuarine Coastal Shelf Sci 52: 505–514 Chapter 8 Fluid Dynamics in Seagrass Ecology Gacia E, Granata TC and Duarte CM (1999) An approach to the measurement of particle flux and sediment retention within seagrass (Posidonia oceanica) meadows. Aquat Bot 65: 255– 268 Gambi MC, Nowell ARM and Jumars PA (1990) Flume observations on flow dynamics in Zostera marina (eelgrass) beds.Mar Ecol Prog Ser 61: 159–169 Garrison T (2000) Essentials of Oceanography, 2nd ed. Wadsworth, Belmont Gaylord B and Denny MW (1997) Flow and flexibility. I—Effects of size, shape and stiffness in determining wave forces on the stipitate kelps Eisenia arborea and Pterygophora californica. J Exp Biol 200: 3141–3164 Ghisalberti M and Nepf HM (2002) Mixing layers and coherent structures in vegetated aquatic flows. J Geophysical Res 107: C2, 10.1029 Grady JR (1981) Properties of seagrass and sand flat sediments from the intertidal zone of St. Andrew Bay, Florida. Estuaries 4: 335–344 Granata TC, Serra T, Colomer J, Casamitjana X, Duarte CM and Gacia E (2001) Flow and particle distributions in a nearshore meadow before and after a storm. Mar Ecol Prog Ser 218: 95–106 Greene RM and Gerard VA (1990) Effects of high-frequency light fluctuations on growth and photoacclimation of the red alga Chondrus crispus. Mar Biol 105: 377–344 Grizzle RE, Short FT, Newell CR, Hoven H and Kindblom L (1996) Hydrodynamically induced synchronous waving of seagrasses: Monami and its possible effects on larval mussel settlement. J Exp Mar Biol Ecol 206: 165–177 Harlin MM and Thorne-Miller B (1982) Seagrass-sediment dynamics of a flood tidal delta in Rhode Island (USA). Aquat Bot 14: 127–138 Harvey M, Bourget E and Ingram RG (1995) Experimental evidence of passive accumulation of marine bivalve larvae on filamentous epibenthic structures. Limnol Oceanogr 40: 94– 104 Harwell MC and Orth RJ (2002) Long-distance dispersal potential in a marine macrophyte. Ecology 83: 3319–3330 Heiss WM, Smith AM and Probert PK (2000) Influence of the small intertidal seagrass Zostera novazelandica on linear water flow and sediment texture. N Z J Mar Freshwater Res 34: 689– 694 Hemminga MA and Duarte CM (2000) Seagrass Ecology. Cambridge University Press, Cambridge Hemminga MA and Nieuwenhuize J (1990) Seagrass wrackinduced dune formation on a tropical coast (Banc-Darguin, Mauritania). Estuarine Coastal and Shelf Sci 31: 499–502 Hemminga MA and Nieuwenhuize J (1991) Transport, deposition and in situ decay of seagrasses in a tropical mudflat area (Banc d’Arguin, Mauritania). Neth J Sea Res 27: 183–190 Hemminga MA, Slim FJ, Kazungu J, Ganssen GM, Nieuwenhuize J and Kruyt NM (1994) Carbon outwelling from a mangrove forest with adjacent seagrass beds and coral reefs (Gazi Bay, Kenya). Mar Ecol Prog Ser 106: 291–301 Hemond HF and Fechner EJ (1994) Chemical Fate and Transport in the Environment. Academic Press, San Diego Herbert RA (1999) Nitrogen cycling in coastal ecosystems. FEMS Microbiol Rev 23: 563–590 Hine AC, Evans MW, Davis RA and Belknap D (1987) Depositional response to seagrass mortality along a low-energy, 221 barrier island coast: West-Central Florida. J Sedimentary Petrology 57: 431–439 Hoskin CM (1983) Sediment in seagrasses near Link Port, Indian River, Florida. Florida Scientist 46: 153–161 Hovel KA, Fonseca MS, Meyer DL, Kenworthy WJ and Whitfield PE (2002) Effects of seagrass landscape structure, structural complexity and hydrodynamic regime on macroepibenthic faunal densities in North Carolina seagrass beds. Mar Ecol Prog Ser 243: 11–24 Huettel M and Gust G (1992) Impact of bioroughness on interfacial solute exchange in permeable sediments. Mar Ecol Prog Ser 89: 253–267 Huettel M and Webster IT (2001) Porewater flow in permeable sediments. In: Boudreau BP and Jørgensen BB (eds) The Benthic Boundary Layer, pp 144–179. Oxford University Press, New York Huettel M, Ziebis W and Forster S (1996) Flow-induced uptake of particulate matter in permeable sediments. Limnol Oceanogr 41: 309–322 Hurd CH and Stevens CL (1997) Flow visualization around single- and multiple-bladed seaweeds with various morphologies. J Phycol 33: 360–367 Inglis GJ (2000) Disturbance-related heterogeneity in the seed banks of a marine angiosperm. J Ecol 88: 88–99 Johannes RE (1975) Pollution and degradation of coral reef communities. In: Wood EJF and Johannes RE (eds) Tropical Marine Pollution, pp 13–51. Elsevier, Amsterdam Jones CG, Lawton JH and Shachak M (1994) Organisms as ecosystem engineers. Oikos 69: 373–386 Jones CG, Lawton JH and Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78: 1946–1957 Jones JI, Eaton JW and Hardwick K (2000) The influence of periphyton on boundary layer conditions: A pH microelectrode investigation. Aquat Bot 67: 191–206 Jørgensen BB and Boudreau BP (2001) Diagenesis and sediment-water exchange. In: Boudreau BP and Jørgensen BB (eds) The Benthic Boundary Layer, pp 211–244. Oxford University Press, New York Keddy J and Patriquin DG (1978) An annual form of eelgrass in Nova Scotia. Aquat Bot 5: 163–170 Kendrick GA and Burt JS (1997) Seasonal changes in epiphytic macro-algae assemblages between offshore exposed and inshore protected Posidonia sinuosa seagrass meadows, Western Australia. Botanica Marina 40: 77–85 Kendrick GA, Hegge BJ, Wyllie A, Davidson A and Lord DA (2000) Changes in seagrass cover on Success and Parmelia Banks, Western Australia between 1965 and 1995. Estuarine Coastal Shelf Sci 50: 341–353 Kenyon RA, Haywood MDE, Heales DS, Loneragan NR, Pendrey RC and Vance DJ (1999) Abundance of fish and crustacean postlarvae on portable artificial seagrass units: Daily sampling provides quantitative estimates of the settlement of new recruits. J Exp Mar Biol Ecol 232: 197– 216 Kirkman H (1985) Community structure in seagrasses in southern Western Australia. Aquat Bot 21: 363–375 Kirkman H and Kendrick GA (1997) Ecological significance and commercial harvesting of drifting and beach-cast macro-algae and seagrasses in Australia: A review. J Appl Phycol 9: 311– 326 222 E. W. Koch, J. D. Ackerman, J. Verduin and M. van Keulen Kirkman H and Kirkman J (2000) Long-term seagrass meadow monitoring near Perth, Western Australia. Aquat Bot 67: 319– 332 Kirkman H and Kuo J (1990) Pattern and process in southern Western Australian seagrasses. Aquat Bot 37: 367– 382 Kitheka JU (1996) Water circulation and coastal trapping of brackish water in a tropical mangrove-dominated bay in Kenya. Limnol Oceanogr 41: 169–176 Kitheka JU (1997) Coastal tidally driven circulation and the role of water exchange in the linkage between tropical coastal ecosystems. Estuarine Coastal Shelf Sci 45: 177–187 Kitheka JU, Ohowa BO, Mwashote BM, Shimbira WS, Mwaluma JM and Kazungu JM (1996) Water circulation dynamics, water column nutrients and plankton productivity in a well-flushed tropical bay in Kenya. J Sea Res 35: 257–268 Koch EW (1993) Hydrodynamics of flow through seagrass canopies. PhD Dissertation, University of South Florida, St. Petersburg, USA, 123 pp Koch EW (1994) Hydrodynamics, diffusion-boundary layers and photosynthesis of the seagrasses Thalassia testudinum and Cymodocea nodosa. Mar Biol 118: 767–776 Koch EW (1996) Hydrodynamics of a shallow Thalassia testudinum bed in Florida, USA. In: Kuo J, Phillips RC, Walker DI and Kirkman H (eds) Seagrass Biology—Proceedings of an International Workshop, pp 105–110. Western Australia Museum, Perth, Australia Koch EW (1999A) Preliminary evidence on the interdependent effect of currents and porewater geochemistry on Thalassia testudinum seedlings. Aquat Bot 63: 95–102 Koch EW (1999B) Sediment resuspension in a shallow Thalassia testudinum bed. Aquat Bot 65: 269–280 Koch EW (2001) Beyond light: Physical, geological and geochemical parameters as possible submersed aquatic vegetation habitat requirements. Estuaries 24: 1–17 Koch EW and Beer S (1996) Tides, light and the distribution of Zostera marina in Long Island Sound, USA. Aquat Bot 53: 97–107 Koch EW and Gust G (1999) Water flow in tide- and wavedominated beds of the seagrass Thalassia testudinum. Mar Ecol Prog Ser 184: 63–72 Koch EW and Huettel M (2000) The impact of single seagrass shoots on solute fluxes between the water column and permeable sediments. Biol Marina Mediterr 7: 235–239 Koehl MAR (1984) How do benthic organisms withstand moving water? Am Zool 24: 57–70 Koehl MAR, Hunter T and Jed J (1991) How do body flexibility and length affect hydrodynamic forces in sessile organisms in wave versus in currents? Am Zool 31: 60A Kopp BS (1999) Effects of nitrate fertilization and shading on physiological and biomechanical properties of eelgrass (Zostera marina). PhD Dissertation. University of Rhode Island, USA, 187 pp Knutson PL (1988) Role of coastal marshes in energy dissipation and shore protection. In: Hook DD, McKee WH, Smith HK, Gregory J, Burrell VG, DeVoe MR, Sojka RE, Gilbert S, Banks R, Srolzy LH, Brooks C, Matthews TD and Shear TH (eds) The Ecology and Management of Wetlands, pp 161–175. Timber Press, Portland, OR Knutson PL, Seelig WN and Inskeep MR (1982) Wave damping in Spartina alterniflora marshes. Wetlands 2: 87–104 Krause-Jensen D, Pedersen MF and Jensen C (2003) Regulation of eelgrass (Zostera marina) cover along depth gradients in Danish coastal waters. Estuaries 26: 866–877 Kundu PK and Cohen IM (2002) Fluid Mechanics, 2nd ed. Academic Press, San Diego Lacap CDA, Vermaat JE, Rollon RN and Nacorda HM (2002) Propagule dispersal of the SE Asian seagrasses Enhalus acoroides and Thalassia hemprichii. Mar Ecol Prog Ser 235: 75–80 Larkum AWD (1976) Ecology of Botany Bay: Growth of Posidonia australis in Botany Bay and other bays of the Sydney basin. Aust J Mar Freshwater Res 27: 117–127 Lenanton RCJ, Robertson AI and Hansen JA (1982) Nearshore accumulations of detached macrophytes as nursery areas for fish. Mar Ecol Prog Ser 9: 51–57 Les DH, Cleland MA and Waycott M (1997) Phylogenetic studies in the Alismatidae, II: Evolution of marine angiosperms (seagrasses) and hydrophily. Systematic Bot 22: 443–463 Lewis RR (2002) The potential importance of the longshore bar system to the persistence and restoration of Tampa Bay seagrass meadows. Proceedings of the Conference on Seagrass Management: It’s not Just Nutrients. August 22–24, 2000. St. Petersburg, FL, USA Lopez F and Garcia M (1998) Open-channel flow through simulated vegetation: Suspended sediment transport modeling. Water Resources Res 34: 2341–2352 Lorke A, Müller B, Maerki M and Wüest A (2003) Breathing sediments: The control of diffusive transport across the sedimentwater interface by periodic boundary-layer turbulence. Limnol Oceanogr 48: 2077–2085 Marbà N, Cebrian J, Enriquez S and Duarte CM (1994) Migration of large-scale subaqueous bedforms measured with seagrasses (Cymodocea nodosa) as tracers. Limnol Oceanogr 39: 126– 133 Marbà N and Duarte CM (1995) Coupling of seagrass (Cymodocea nodosa) patch dynamics to subaqueous dune migration. J Ecol 83: 381–389 Massel SR (1999) Fluid Mechanics for Marine Ecologists. Springer, Berlin Massel SR, Furukawa K and Brinkman RM (1999) Surface wave propagation in mangrove forests. Fluid Dyn Res 24: 219–249 Meehan AJ and West RJ (2000) Recovery times for a damaged Posidonia australis bed in south eastern Australia. Aquat Bot 67: 161–167 Menzies RJ and Rowe GT (1969) The distribution and significance of detrital turtle grass, Thalassia testudinum, on the deep-sea floor off North Carolina. Int Rev Gesamten Hydrobiologie 54: 217–222 Menzies RJ, Zaneveld JS and Pratt RM (1967) Transported turtle grass as a source of organic enrichment of abyssal sediments off North Carolina. Deep-Sea Res 14: 111–112 Middelboe AL, Sand-Jensen K and Frause-Jensen D (2003) Spatial and interannual variations with depth in eelgrass populations. J Exp Biol Ecol 291: 1–15 Mills KE and Fonseca MS (2003) Mortality and productivity of eelgrass Zostera marina under conditions of experimental burial with two sediment types. Mar Ecol Prog Ser 255: 127– 134 Miyajima T, Koike I, Yamano H and Iizumi H (1998) Accumulation and transport of seagrass-derived organic matter in reef Chapter 8 Fluid Dynamics in Seagrass Ecology flat sediment of Green Island, Great Barrier Reef. Mar Ecol Prog Ser 175: 251–259 Möller I, Spencer T, French JR, Leggett DJ and Dixon M (1999) Wave transformation over salt marshes: A field and numerical modeling study from North Norfolk, England. Estuarine Coastal Shelf Sci 49: 411–426 Moncreiff CA, Randall TA, Caldwell JD, McCall RK, Blackburn BR, Vander Kooy KE and Criss GA (1999) Short-term effects of Hurricane Georges on seagrass populations in the north Chandeleur Islands: Patterns as a function of sampling scale. Gulf Res Rep 11: 74–75 Monismith SG and Fong DA (2004) A note on the potential transport of scalars and organisms by surface waves. Limnol Oceanogr 49: 1214–1217 Moore K, Neckles H and Orth R (1996) Zostera marina growth and survival along a gradient of nutrients and turbidity in the lower Chesapeake Bay. Mar Ecol Prog Ser 142: 247–259 Nagelkerken I, Kleijnen S, Klop T, van den Brand RACJ, Cocheret de la Morinière E and van der Velde G (2001) Dependence of Caribbean reef fishes on mangroves and seagrass beds as nursery habitats: A comparison of fish faunas between bays with and without mangroves/seagrass beds. Mar Ecol Prog Ser 214: 225–235 Nepf HM and Koch EW (1999) Vertical secondary flows in stem arrays. Limnol Oceanogr 44: 1072–1080 Nepf HM and Vivoni ER (2000) Flow structure in depth limited vegetated flow. J Geophysical Res 105: 28,547–28,557 Newell CR, Hidu H, McAlice BJ, Podnieski G, Short F and Kindbloom L (1991) Recruitment and commercial seed procurement of the blue mussel, Mytilus edulis in Maine. J World Aquaculture Soc 22: 134–152 Niklas KJ (1992) Plant Biomechanics. University of Chicago Press, Chicago Niklas KJ (1998) The mechanical roles of clasping leaf sheaths: Evidence from Arundinaria tecta shoots subject to bending and twisting forces. Ann Bot 81: 23–34 Nikora VI, Goring DG and Biggs BJF (2002) Some observations of the effect of micro-organisms growing on the bed of an open channel on the turbulence properties. J Fluid Mech 450: 317– 341 Nowell ARM and Jumars PA (1984) Flow environments of aquatic benthos. Annu Rev Ecol Systematics 15: 303– 328 Ochieng CA and Erftemeijer PLA (1999) Accumulation of seagrass beach cast along the Kenyan coast: A quantitative assessment. Aquat Bot 65: 221–238 Ogden JC (1980) Faunal relationships in Caribbean seagrass beds. In: Phillips RC and McRoy CP (eds) Handbook of Seagrass Biology: An Ecosystem Perspective, pp 173–198. Garland STPM, New York Okubo A, Ackerman JD and Swaney DP (2002) Passive diffusion in ecosystems. In: Okubo A and Levin S (eds) Diffusion and Ecological Problems: New Perspectives, pp 31–106. Springer Verlag, New York Orth RJ (1975) Destruction of eelgrass, Zostera marina, by the cownose ray, Rhinoptera bonasus, in the Chesapeake Bay. Chesapeake Sci 16: 205–208 Orth RJ, Fishman JR, Wilcox DJ and Moore KA (2002) Identification and management of fishing gear impacts in a recovering seagrass system in the coastal bays of the Delmarva Peninsula, USA. J Coastal Res 37: 111–129 223 Othman MA (1994) Value of mangroves in coastal protection. Hydrobiologia 285: 277–282 Paling EI (1991) The relationship between nitrogen cycling and productivity in macroalgal stands and seagrass meadows. PhD Thesis, University of Western Australia, Perth, 316 pp Paling EI, van Keulen M and Wheeler KD (2003) The influence of spacing on mechanically transplanted seagrass survival in a high energy regime. Restoration Ecol 11: 56–61 Palmer MR, Nepf HM, Pettersson TJR and Ackerman JD (2004) Observations of particle capture on a cylindrical collector: Implications for particle accumulation and removal in aquatic systems. Limnol Oceanogr 49: 76–85 Patriquin DG (1975) “Migration” of blowouts in seagrass beds at Barbados and Caricou, West Indies, and its ecological and geological implications. Aquat Bot 1: 163–189 Patterson DM and Black KS (1999) Water flow, sediment dynamics and benthic biology. Adv Ecol Res 29: 155–193 Patterson MR, Harwell MC, Orth LM and Orth RJ (2001) Biomechanical properties of reproductive shoots of eelgrass. Aquat Bot 69: 27–40 Peterson CH, Luettich RA Jr, Micheli F and Skilleter GA (2004) Attenuation of water flow inside seagrass canopies of differing structure. Mar Ecol Prog Ser 268: 81–92 Pettitt JM (1984) Aspects of flowering and pollination in marine angiosperms. Oceanography Mar Biol Annu Rev 22: 315–342 Phillips RC (1980) Responses of transplanted and indigenous Thalassia testudinum and Halodule wrightii to sediment loading and cold stress. Contrib Mar Sci 23: 79–87 Pinckney JL and Micheli F (1998) Microalgae on seagrass mimics: Does epiphyte community structure differ from live seagrasses? J Exp Mar Biol Ecol 221: 59–70 Powell GVN and Schaffner FC (1991) Water trapping by seagrasses occupying bank habitats in Florida Bay. Estuarine Coastal Shelf Sci 32: 43–60 Prager EJ and Halley RB (1999) The influence of seagrass on shell layers and Florida Bay mudbanks. J Coastal Res 15: 1151–1162 Prandtl L and Tietjens OG (1934) Applied Hydro- and Aeromechanics. Dover Publications, New York Preen A (1995) Impacts of dugong foraging on seagrass habitats: Observational and experimental evidence for cultivation grazing. Mar Ecol Prog Ser 124: 201–213 Preen AR, Lee Long WJ and Coles RG (1995) Flood and cyclone related loss, and partial recovery, of more than 1000 km2 of seagrass in Hervey Bay, Queensland, Australia. Aquat Bot 52: 3–17 Rasmussen E (1977) The wasting disease of eelgrass (Zostera marina) and its effects on environmental factors and fauna. In: McRoy CP and Helfferich C (eds) Seagrass Ecosystems, pp 1–52. Marcel Dekker, New York Raupach MR, Antonia AR and Rajagopalan S (1991) Roughwall turbulent boundary layers. Appl Mech Rev 44: 1–25 Reusch TBH (2000) Pollination in the marine realm: Microsatellites reveal high outcrossing rates and multiple paternity in eelgrass Zostera marina. Heredity 85: 459–464 Robbins BD and Bell SS (1994) Seagrass landscapes: A terrestrial approach to the marine subtidal environment. Trends Ecol Evol 9: 301–304 Robbins BD and Bell SS (2000) Dynamics of a subtidal seagrass landscape: Seasonal and annual change in relation to water depth. Ecol 81: 1193–1205 224 E. W. Koch, J. D. Ackerman, J. Verduin and M. van Keulen Robertson AI and Lennaton RCJ (1984) Fish community structure and food chain dynamics in the surf-zone of sandy beaches: The role of detached macrophyte detritus. J Exp Mar Biol Ecol 84: 265–283 Rodriguez RW, Webb RMT and Bush DM (1994) Another look at the impact of hurricane Hugo on the shelf and coastal resources of Puerto Rico, USA. J Coastal Res 10: 278–296 Ruckleshaus MH (1995) Estimation of outcrossing rates and of inbreeding depression in a population of the marine angiosperm, Zostera marina. Mar Biol 123: 583–593 Ruesink JL (1998) Diatom epiphytes on Odonthalia floccosa: The importance of extent and timing. J Phycol 34: 29–38 Rysgaard S, Risgaard-Petersen N and Sloth NP (1996) Nitrification, denitrification, and nitrate ammonification in sediments of two coastal lagoons in southern France. Hydrobiologia 329: 133–141 Sand-Jensen K (2003) Drag and reconfiguration of freshwater macrophytes. Freshwater Biol 48: 271–283 Sand-Jensen K, Revsbach NP and Jorgensen BB (1985) Microprofiles of oxygen in epiphyte communities on submerged macrophytes. Mar Biol 89: 55–62 Sanford LP and Crawford SM (2000) Mass transfer versus kinetic control of uptake across solid-water boundaries. Limnol Oceanogr 45: 1180–1186 Schanz A, Polte P and Asmus H (2002) Cascading effects of hydrodynamics on an epiphyte-grazer system in intertidal seagrass beds of the Wadden Sea. Mar Biol 141: 287– 297 Schlichting H (1979) Boundary-Layer Theory, 7th ed. McGraw Hill, New York Sculthorpe CD (1967) The Biology of Aquatic Vascular Plants. Edward Arnold, London Shepherd SA and Robertson EL (1989) Regional studies— seagrasses of South Australia, Western Victoria and Bass Strait. In: Larkum AWD, McComb AJ and Shepherd SA (eds) Biology of Seagrasses: A Treatise on the Biology of Seagrasses with Special References to the Australian Region, pp 211–229. Elsevier, New York Short FT and Wyllie-Echeverria S (1996) Natural and humaninduced disturbances of seagrasses. Environ Conservation 23: 17–27 Smith NM and Walker DI (2002) Canopy structure and pollination biology of the seagrasses Posidonia australis and P. sinuosa (Posidoneaceae).Aquat Bot 74: 57–70 Stankelis RM, Naylor MD and Boynton WR (2003) Submerged aquatic vegetation in the mesohaline region of the Patuxent estuary: Past, present and future status. Estuaries 26: 186–195 Stapel J, Manuntun R and Hemminga MA (1997) Biomass loss and nutrient redistribution in a Thalassia hemprichii bed following low tide exposure during daylight. Mar Ecol Prog Ser 148: 251–262 Stevens CL and Hurd CH (1997) Boundary-layers around bladed aquatic macrophytes. Hydrobiologia 346: 119–128 Suchanek TH, Williams SL, Ogden JC, Hubbard DK and Gill IP (1985) Utilization of shallow-water seagrass detritus by Caribbean deep-sea macrofauna: Delta-13 C evidence. DeepSea Res 32: 201–214 Thayer GW, Powell AB and Hoss DE (1999) Composition of larval, juvenile, and small adult fishes relative to changes in environmental conditions in Florida Bay. Estuaries 22: 518– 533 Thomas FIM and Cornelisen CD (2003) Ammonium uptake by seagrass communities: Effects of oscillatory versus unidirectional flow. Mar Ecol Prog Ser 247: 51–57 Thomas FIM, Cornelisen CD and Zande JM (2000) Effects of water velocity and canopy morphology on ammonium uptake by seagrass communities. Ecology 81: 2704–2713 Thomas LP, Moore DR and Work RC (1961) Effects of hurricane Donna on the turtle grass beds of Biscayne Bay, Florida. Bull Mar Sci Gulf Caribbean 11: 191–197 Tilmant JT, Curry RW, Jones R, Szmant A, Zieman JC, Flora M, Roblee MB, Smith D, Snow RW and Wanless H (1994) Hurricane Andrew’s effects on marine resources. BioScience 44: 230–237 Turner T (1983) Facilitation as a successional mechanism in a rocky intertidal community. Am Nat 121: 729–738 Valiela I and Cole ML (2002) Comparative evidence that salt marshes and mangroves may protect seagrass meadows from land-derived nitrogen loads. Ecosystems 5: 92–102 van der Pijl L (1972) Principles of Dispersal in Higher Plants, 2nd ed. Springer Verlag, Berlin van Katwijk MM (2000) Possibilities for restoration of Zostera marina beds in the Dutch Wadden Sea. PhD Thesis, University of Nijmegen, The Netherlands 160 pp van Katwijk MM and Hermus DCR (2000) Effects of water dynamics on Zostera marina: Transplantation experiments in the intertidal Dutch Wadden Sea. Mar Ecol Prog Ser 208: 107–118 van Keulen M (1997) Water flow in seagrass ecosystems. PhD Dissertation, Murdoch University, Western Australia van Keulen M and Borowitzka MA (2002) Comparison of water velocity profiles through dissimilar seagrasses measured with a simple and inexpensive current meter. Bull Mar Sci 71: 1257–1267 van Keulen M and Borowitzka MA (2003) Dynamics of sediments along an exposure gradient in a monospecific seagrass meadow in Shoalwater Bay, Western Australia. Estuarine Coastal Shelf Sci 57: 587–592 Verduin JJ and Backhaus JO (2000) Dynamics of plant-flow interactions for the seagrass Amphibolis antarctica: Field observations and model simulations. Estuarine Coastal Shelf Sci 50: 185–204 Verduin JJ, Walker DI and Kuo J (1996) In situ submarine pollination in the seagrass Amphibolis antartica: Research notes. Mar Ecol Prog Ser 133: 307–309 Vermaat JE, Agawin NSR, Fortes MD, Uri JS, Duarte CM, Marbà N, Enriquez S and van Vierssen W (1996) The capacity of seagrasses to survive increased turbidity and siltation: The significance of growth form and light use. Ambio 25: 499– 504 Vermaat JE, Santamaria L and Roos PJ (2000) Water flow across and sediment trapping in submerged macrophyte beds of contrasting growth form. Arch Hydrobiol 148: 549–562 Vidono B, Duarte CM, Middelboe AL, Stefansen K, Lützen T and Nielsen SL (1997) Dynamics of a landscape mosaic: Size and age distributions, growth and demography of seagrass Cymodocea nodosa patches. Mar Ecol Prog Ser 158: 131–138 Vogel S (1994) Life in Moving Fluids, 2nd ed. Princeton University Press, Princeton, NJ, USA Walker DI, Carruthers TJB, Morrison PF and McComb AJ (1996) Experimental manipulation of canopy density in a temperate seagrass [Amphibolis griffithii (Black) den Hartog] Chapter 8 Fluid Dynamics in Seagrass Ecology meadow: Effects on sediments. In: Kuo J, Phillips RC, Walker DI and Kirkman H (eds) Seagrass Biology. Proceedings of an International Workshop, Faculty of Sciences, pp 117–122. University of Western Australia, Perth Walker DI, Lukatelich RJ, Batyan G and McComb AJ (1989) Effect of boat moorings on seagrass beds near Perth, Western Australia. Aquat Bot 36: 69–77 Wallace S and Cox R (1997) Seagrass and wave hydrodynamics. Pacific Coasts and Ports ’97: Proceedings of the 13th Australasian Coastal and Ocean Engineering Conference and the 6th Australasian Port and Harbour Conference, Christchurch, New Zealand, 69–73 Wanless HR (1981) Fining upwards sedimentary sequences generated in seagrass beds. J Sedimentary Petrology 51: 445– 454 Ward LG, Kemp WM and Boynton WE (1984) The influence of waves and seagrass communities on suspended particulates in an estuarine embayment. Mar Geology 59: 85–103 Waycott M and Sampson JF (1997) The mating system of an hydrophilous angiosperm Posidonia australis (Posidoniaceae). Am J Bot 84: 621–665 White FM (1999) Fluid Mechanics, 4th ed. McGraw Hill, Boston, 826 pp Whitfield PE, Kenworthy WJ, Hammerstrom KK and Fonseca MS (2002) The role of a hurricane in the expansion of disturbances initiated by motor vessels on seagrass banks. J Coastal Res 37: 86–99 Williams SL (1988) Disturbance and recovery of a deepwater Caribbean seagrass bed. Mar Ecol Prog Ser 42: 63– 71 225 Williams SL (1995) Surfgrass (Phyllospadix torreyi) reproduction: Reproductive phenology, resource allocation and male rarity. Ecology 76: 1953–1970 Williams PM, Druffel ERM and Smith KL Jr (1987) Dietary carbon sources for deep-sea organisms as inferred from their organic radiocarbon activities. Deep-Sea Res 34: 253– 266 Wing SR, Leichter JJ and Patterson MR (1993) A dynamic model for wave-induced light fluctuations in a kelp forest. Limnol Oceanogr 38: 396–407 Wing SR and Patterson MR (1993) Effects of wave-induced lightflecks in the intertidal zone on photosynthesis in the macroalgae Postelsia palmaeformis and Hedophyllum sessile. Mar Biol 116: 519–525 Wolff T (1976) Utilization of seagrass in the deep sea. Aquat Bot 2: 161–174 Wolff T (1979) Macrofaunal utilization of plant remains in the deep sea. Sarsia 64: 117–136 Worcester SE (1995) Effects of eelgrass beds on advection and turbulent mixing in low current and low shoot density environments. Mar Ecol Prog Ser 126: 223–232 Wyllie-Echeverria S and Ackerman JD (2003) Biogeography and ecology of Northeast Pacific seagrasses. In: Green EP, Short FT and Spalding MD (eds) World Atlas of Seagrasses: Present Status and Future Conservation, pp 199–206. University of California Press, Berkeley Zieman JC, Thayer GW, Robblee MB and Zieman RT (1979) Production and export of sea grasses from a tropical bay. In: Livingstone RJ (ed) Ecological Processes in Coastal and Marine Systems, pp 21–34. Plenum Press, New York