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First published online May 18, 2006
Journal of Experimental Biology 209, 2170-2181 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02254
Hydrodynamic consequences of flexural stiffness and buoyancy for seaweeds: a study using physical models
Department of Integrative Biology, University of California, Berkeley, CA 94720, USA
Accepted 5 April 2006
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Summary |
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Key words: flexural stiffness, buoyancy, seaweed, Turbinaria ornate, hydrodynamic force, relative velocity.
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;
Patterson et al., 1991;
Atkinson and Bilger, 1992). For
photosynthetic organisms, an upright posture may reduce shading by neighbors
(e.g. Hay, 1986;
Holbrook et al., 1991;
Wing and Patterson, 1993), and
can increase the amount and intensity of light intercepted, as light is
absorbed and scattered with depth (Mann
and Lazier, 1996). The greater the water velocity an organism
experiences, the thinner the boundary layer between the surface of the
organism and the ambient flow, and rates of mass transport across this
boundary layer are faster (e.g. Koch,
1994; Gonen et al.,
1995). At the same time, however, momentum transfer from ambient
water to an organism's surface is also greater across thin boundary layers and
can increase hydrodynamic forces experienced by the organism. Thus, there are
trade-offs between the advantages (increased uptake rates and light
interception) and the disadvantages (increased hydrodynamic forces) of
maintaining an upright posture in moving water.
Mechanisms to maintain an upright posture
Aquatic organisms can maintain upright postures by two mechanisms: (1)
having high flexural stiffness, or (2) by being buoyant. The flexural
stiffness (EI) of a structure is a measure of the resistance of that
structure to bending, and depends on both the cross-sectional dimensions of
the structure, measured as the second moment of area (I), and on the
stiffness (resistance to deformation) of its material, measured as the elastic
modulus (E) (Wainwright et al.,
1976). Buoyancy maintains an organism in an upright position by
imparting a net upward force that functions to maintain it in and restore it
to its erect position. Buoyancy in marine algae is usually produced by
pneumatocysts (air bladders) in blades, although other mechanisms exist such
as porous, honeycomb-like tissue that traps and retains gas within it
(Stevens et al., 2002). The
buoyancy of an organism, then, is a function of the volume of its
pneumatocysts and the density of its tissue relative to the density of the
water in which it is immersed. Although both buoyancy and flexural stiffness
maintain benthic organisms in upright positions, these mechanisms (an upward
restoring force vs resistance to deflection) may have different
hydrodynamic consequences for upright benthic marine organisms.
Unidirectional and wavy flow conditions
In steady unidirectional flow, drag is experienced by organisms as they are
pulled in the downstream direction by water moving around them. To escape high
water velocities and forces, organisms that can bend may be pushed down toward
the substratum into slowly moving water lower in the boundary layer. Organisms
may also be reconfigured into streamlined shapes by water motion, reducing the
projected area exposed to the flow and the width of their downstream wake and
the drag experienced (e.g. Koehl,
1984; Koehl and Alberte,
1988; Vogel,
1994). Thick boundary layers can form on the surfaces of organisms
in slow steady unidirectional flow and can present a barrier to gas and
nutrient transfer from the ambient water to the organism (e.g.
Patterson and Sebens, 1989;
Koch, 1993;
Hurd and Stevens, 1997).
In waves, organisms are exposed to a periodic reversal of flow velocity.
Stiff upright organisms that do not move with the flow can be subject to drag,
and acceleration reaction forces. Drag is proportional to the square of the
velocity of water relative to the frond and acceleration reaction is
proportional to its acceleration, and the magnitude of these forces changes as
flow accelerates and decelerates past an organism
(Denny, 1988). Flow reversal
in waves can disrupt boundary layers that form over the surface of the
organism, and the exchange of gases and nutrients to and from an organism may
be enhanced in turbulent or thin, newly forming boundary layers (e.g.
Koch, 1994;
Stevens et al., 2003;
Reidenbach et al., 2006).
Thus, wavy habitats have the potential to be hydrodynamically challenging for
organisms trying to remain attached to the substratum, but can be rewarding in
terms of increased potential for mass transfer for organisms that are able to
persist (Norton et al., 1981;
Carpenter et al., 1991;
Falter et al., 2005).
Objectives of this study
This study was conducted to address the following question. What are the
effects of different magnitudes of EI and buoyancy on hydrodynamic
forces and relative velocity on a benthic alga in unidirectional and wavy
flow?
I addressed this question using Turbinaria ornata (Turner)J.
Agardh, a brown macroalga that uses either buoyancy or flexural stiffness to
maintain an upright position in very different flow habitats. Turbinaria
ornata is abundant across reef systems throughout French Polynesia
(Payri and N'Yeurt, 1997).
Fronds of T. ornata in calm backreef habitats have flexible stipes
and airbladders that make them buoyant. Fronds in forereef habitats exist
under waves and are stiff, do not possess airbladders, and are not buoyant
(Stewart, 2004). The
production of airbladders is a plastic trait that can be induced by
transplanting forereef fronds to calm backreef sites
(Stewart, 2006a). Buoyancy of
backreef fronds increases with reproductive maturity, corresponding also with
decreases in stipe strength and extensibility
(Stewart, 2006b), contributing
to the potential for rafting of mature buoyant fronds that is an important
dispersal mechanism for this alga (Payri
and Stiger, 2001). In addition to differences in EI and
buoyancy, forereef and backreef fronds also differ morphologically in other
ways, forereef fronds exhibiting `dwarfism' in relation to backreef fronds
(Payri, 1984). Backreef fronds
are longer, have a longer bladed portion, thinner stipes and shorter blades
than forereef fronds (Stewart,
2006a).
A previous study examined the hydrodynamic effect of the two naturally
occurring levels of EI and buoyancy of Turbinaria ornata in
the field, and found that these differences in EI alone did not
result in different hydrodynamic consequences, but that the combination of the
EI and buoyancy of backreef fronds resulted in lower force and
relative velocity than experienced by forereef fronds in waves
(Stewart, 2004). This study
expands upon that work by using physical models of T. ornata to
explore degrees of EI and buoyancy beyond that available in real
algae. Using these models in controlled flow environments in the laboratory, I
investigate the general mechanisms responsible for differences in hydrodynamic
force experienced by buoyant and stiff fronds in both unidirectional and wavy
flow.
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Materials for each type of model
Six types of backreef and forereef models were constructed with a range of
buoyancies and EI values (Fig.
2). Three replicates of each type of model were constructed from
both the backreef and the forereef molds. Models of forereef and backreef
models differed in several morphological characteristics
(Table 1). The effect of length
was removed from the experiment by constructing forereef and backreef to be
the same total length (14 cm).
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The six types of models (very flexible, flexible, flexible non-buoyant, extra-buoyant, stiff and rigid) were constructed using the silicone molds from the following materials:
Note: all models were buoyant except those made non-buoyant by addition of weight.
Measuring buoyancy of models
To quantify the buoyant force experienced by each model, buoyant force
(FB) was determined using the equation:
 | (1) |
where g is the acceleration due to gravity (9.81 m
s-2), V is the volume of the alga, 
a is
the density of the alga and w is the density of the freshwater
that was used for all experiments in this study (998 kg m-3 at
20°C) (Vogel, 1994). The
volume of models was determined by measuring displacement of the volume of
water in a graduated cylinder. Dividing the mass of each model by its volume
yielded estimates of its density. The mass of each frond was determined from
the mean of two measurements (to the nearest 0.01 g) using a precision balance
(Explorer model, Ohaus Corporation, Bradford, MA, USA).
Determining flexural stiffness of models
Flexural stiffness (EI) was determined for three stipes of each
type of backreef and forereef model (Table
2). The basal portion of stipes of models (just above the
holdfast) was used to determine the extension ratio (
), as based on
observations in the field this was the location on the frond where the
majority of bending and breaking occurred.
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Elastic moduli (E) were measured by conducting tensile
stress-extension tests on model stipes, as described elsewhere
(Koehl and Wainwright, 1977),
using a materials testing machine (Model 1122, Instron Corp., Norwood, MA,
USA). The extension ratio () for each model was calculated using the
equation:
 | (2) |
where Lo is the original length of the test portion of
the stipe, and L is the length of that portion of the stipe at the
time it broke. The force with which the stipe resisted the extension was
measured to the nearest 0.001 N. Stress (N m-2) experienced by
stipes of models was calculated by dividing the force with which the stipe
resisted extension by the cross-sectional area of it at the point that it
broke. The diameter of each stipe at its break was measured using digital
calipers to the nearest 0.01 mm and the area was calculated using the equation
for the area of a circle, as stipes were roughly circular in cross-section.
The elastic modulus (E) for each model was determined from the slope
of the straight portion of the curve made by plotting stress vs
extension ratio for each stipe (Wainwright
et al., 1976).
The second moment of area (I) is a measure of the distribution of
material around the axis of bending and is proportional to its radius raised
to the fourth power. The I of each stipe was calculated using the
equation for I for a circular cross-section:
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where d is the diameter of the stipe measured as described above. The EI of the rigid model was taken to be the EI of the thin
where d is the diameter of the stipe measured as described above.
The EI of the rigid model was taken to be the EI of the thin
stainless steel rods to which the stiff models were attached. The E
of the stainless steel rod was determined from published values
(Wainwright et al., 1976) and
the I of the rod was determined as above.
Water flow
Unidirectional flow
Force experienced by models in unidirectional flow was measured in a
recirculating flow tank with a working section of 0.35 mx0.50
mx2.00 m described elsewhere
(Martinez, 2001). Flow
velocity was measured using an Acoustic Doppler Velocimeter (ADV) (Sontek,
Inc., San Diego, CA, USA). The mean flow speed at each of six heights above
the floor of the flume over 30 s at five motor settings (16, 32, 50, 67, 73 cm
s-1) were measured. Water depth in the flume was 35 cm. The
velocity of the flow as a function of the height above the bottom of the flume
is shown in Fig. 3.
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For logistical reasons, the waves used in this experiment were much smaller
in period (2 s period) and amplitude (10 cm) than the waves that T.
ornata experiences in the field (8-10 s period with amplitudes 
0.5-1
m and larger during storms). While the horizontal displacement of water in
waves in the tank is shorter than under waves on the reef, its is 30 cm in
each direction, just longer than twice the length of the models (2x14
cm) indicating that water in the wave tank did move further in each direction
than the potential maximum displacement of the models but to a lesser degree
than water moves on the forereef. The results of this experiment are not
intended to be directly applicable to a forereef of a barrier reef, but to
provide a common wave field to identify general mechanisms by which
morphology, stiffness and buoyancy affect hydrodynamic performance. Therefore
the implications of results from the wave tank are discussed in a general
context of oscillatory flow.
Force measurements
Force experienced by the models was recorded using a force transducer made
according to a published design (Koehl,
1977) and details of its construction are reported elsewhere
(Stewart, 2004). The force
plate was situated under a false bottom in the flume so that only a 1 cm high
sting extended up into the flow. Models were attached at the base of their
stipes with a single cable tie as low as possible to the sting of the force
transducer so as to not affect the bending of the model. The response time of
the force transducer was 0.01 s. Voltages from the force transducer were
recorded at 10 Hz using BiobenchTM software (National Instruments,
Austin, TX, USA) on a laptop computer via a bridge amplifier and a
DAQ 1200 card (National Instruments).
Force transducers were calibrated by hanging weights from a string attached to the transducer, which sat horizontally on a table. The string was laid over a pulley attached to the edge of the table so that the mass of the weight caused a horizontal displacement of the transducer. Weights ranging from 0.01 N to 2.0 N were hung from the transducer in both the positive and negative directions. Each weight was hung three times and the mean of the voltages registered for each weight was used to calculate a linear regression (r2=0.88) for the voltages measured as a function of force.
Measurements of motion of models
A video of the motion of the models in the oscillatory flow was recorded on
a digital video recorder at 60 frames s-1 during the force
experiments at 60 frames s-1. Video was synchronized with the force
recordings using an event marker, which consisted of a small LED light that
was illuminated in front of the video camera for several seconds at the
beginning of each run, simultaneously putting a visual marker on the video and
a voltage spike on the recordings of the water flow and force. This enabled
synchronization of video frames with voltage signals from the force
transducer.
The movement of the distal tip of each frond was digitized at 0.1-s intervals from the video using MotusTM Peak 3.0 software (Inition Ltd., London, UK) for 20 s of each trial. Because the motion of the very flexible models differed a great deal along the length of the model, a second point mid-way along the length of the model (7 cm from the tip) was also digitized. This positional data was then converted to instantaneous velocity by taking the difference in position between intervals and dividing by 0.1 s. Calculations were done using Matlab 6.5 software (The Mathworks Inc., Natick, MA, USA).
Relative velocity calculations
The relative water velocity past the surface of each model was estimated
using the simultaneous video recording of the model and the flow velocity
recordings during each trial. For each 20 s trial, algal velocity was
subtracted from the corresponding water velocity for the same instant, giving
an estimate of the water velocity relative to the frond during each 0.1 s
interval. Because the flow velocity was measured at a constant height of 14
cm, and models moved in the flow and were not always upright, relative
velocities may overestimate velocity, particularly for flexible models when
they were bent over into slower moving flow in the boundary layer in
unidirectional flow. However, because the conclusions drawn from these
experiments are expressed as relative patterns they will not be affected by
this slight overestimation. Because both the water and the alga exhibited
oscillatory movement in the waves, velocities were recorded as positive
(toward the left as viewed through the digital camera) and negative (toward
the right) values. Data of water velocity, force, the position of the model
and relative velocity at the surface of the model for each model were then
synchronized for comparison.
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Effect of EI
Drag force increased with EI for backreef and forereef fronds
(Fig. 6A). The amount the
models deflected downstream in the flow increased with decreasing EI
(Fig. 7). At the highest flow
speed, the width of the bladed portion of the most flexible models was
60% of their width at the lowest flow speed, indicating that they were
compacted by the water moving around them. Other models were not compacted
significantly, even at the highest flow speed
(Fig. 8).
Effect of buoyancy
Buoyant models experienced higher forces
(Fig. 6A) and deflected less in
unidirectional flow (Fig. 7)
than their non-buoyant counterparts of the same EI.
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Effect of EI
Models of higher EI experienced higher force in waves than models
of lower EI (Kruskall-Wallis H=29.09, d.f.=5,
P<0.05) (Fig. 6B).
How much a model moved with the flow affected the force it experienced. Models
that moved during the fastest flows and stopped moving after the peak velocity
of the wave cycle had passed experienced lower relative velocities and lower
forces than those that stopped moving with the flow at faster flow velocities.
Stiffer models moved shorter distances in each wave than did more flexible
models (Fig. 9). The timing of
the movement of the model, with respect to water velocity, also differed with
flexural stiffness (Fig. 10).
Stiffer models only moved with the fastest flows, and when flow slowed down,
stiff models began to right themselves. Flexible models moved with fast flows
and kept moving as flow speed decreased. The most flexible models moved with
even the slowest flows and kept traveling in the direction of flow for the
entire time the water moved in one direction
(Fig. 11).
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All models except the very flexible models moved in waves as one unit, the tip moving in line with the rest of the model. However, the most flexible models had portions moving in different directions as they experienced whiplashing. Whiplashing occurs as the basal portion of a long, flexible structure becomes fully extended in the direction of flow, decelerates to a halt but the distal portion keeps moving and accelerates as occurs when cracking a whip. This occurs because of conservation of angular momentum, which is proportional to angular velocity multiplied by the mass of an object. Along the length of an object there is progressively less mass towards its tip, and as mass decreases, angular velocity increases. Consequently, the tip of an object can move faster than the surrounding fluid even after the basal portion has stopped moving, or has even begun to move in the opposite direction. In the very flexible models, the tip (point 1) of the model lagged behind the middle of the model (point 2) (Fig. 11). The tips of the models were whipped forward and back and at times were moving faster than the ambient water. These very flexible models experienced maximum forces at their bases when the middle of the model (point 2) was pulled in the direction of flow. Tips of very flexible models were extended in the direction of flow after the maximum force was experienced (Fig. 11).
The relative velocity at the surface of the distal tip of the model at the time of peak force increased with increasing EI of models (Fig. 12). Relative velocity of the very flexible models was negative because the tips (point 1) of the models were moving faster than the surrounding water at the time of peak force.
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Non-buoyant and extra-buoyant models experienced higher relative velocities at the time of peak force than buoyant models of the same EI (Fig. 12).
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;
Bouma et al., 2005). In
unidirectional flow, stiffness reduced the amount that models deflected,
exposing them to faster water higher in the boundary layer, and reduced the
amount that models were reconfigured into streamlined shapes by moving water.
As drag force is proportional to the plan area of an organism
(Denny et al., 1985), the
upright, un-streamlined shapes of stiff models resulted in higher drag than
deflected, compacted flexible models. In waves, stiffness reduced the amount
that models moved with the water, increasing the relative velocities at their
surfaces and the drag that they experienced.
To persist in high-flow habitats, stiff organisms must have other
attributes to prevent being dislodged. Stiff organisms in areas of rapid
unidirectional flow or high-energy waves might be expected to be small, and in
general, many organisms in high-flow habitats are shorter than their
counterparts in calm habitats (e.g. Norton
et al., 1981; Blanchette,
1997; Stewart and Carpenter,
2003). Turbinaria ornata in high-energy forereef habitats
is stronger (Stewart, 2004),
and has a morphology that is shorter with thicker stipes and blade
attachments, and fewer blades than fronds from calm backreef habitats
(Stewart, 2006a). Aggregation
may also provide a strategy for survival in high flow, as high drag
experienced by individuals can translate into modification of the physical
environment via reduction of hydrodynamic energy in aggregations
(Jackson and Winant, 1983;
Worcester, 1995;
Jackson, 1997;
Johnson, 2001). For example,
stiff seagrass dissipates up to three times as much wave energy as flexible
seagrass at densities of 450-1850 individuals m-2
(Bouma et al., 2005).
Flexibility in unidirectional flow
In unidirectional flow, organisms with low EI encounter velocities
approaching ambient velocity because they are strung out in the direction of
flow and are not moving with it (Koehl,
1984). However, flexibility allows organisms to be reconfigured
into streamlined shapes in moving water, potentially reducing the drag force
that they experience (e.g. Koehl and
Alberte, 1988; Carrington,
1990; Gaylord et al.,
1994). Flexible organisms may also lie along or be pushed down to
the substratum, where they may experience reduced flow velocities low in the
boundary layer and avoid high relative velocities and forces
(Koehl, 1984). This may also
decrease the moment arm of the imposed force, effectively reducing the stress
experienced by deflected organisms
(Gaylord and Denny, 1997).
However, organisms low in the boundary layer may face transport limitation in
slow water velocities (Boynton et al.,
1981; Wheeler,
1988; Stewart and Carpenter,
2003). Flexible seaweeds may ameliorate mass transfer limitation
by the fluttering of their blades, which disrupts boundary layers on their
surfaces but may also increase the force that they experience
(Koehl and Alberte, 1988).
Flexibility in waves
Flexible organisms can move back and forth in the bi-directional flow under
waves. During the time an organism moves with the flow, it experiences low
relative velocities at its surface as it moves along at ambient velocity, and
rates of mass transfer may be reduced as nutrients and gases are depleted from
surrounding water. However, if an organism moving with the flow becomes
extended in the direction of flow before the flow reverses, the relative
velocity will increase as water continues to pass by. Due to the short period
of waves in the tank, the flexible and very flexible models moved with the
flow for most of their excursion in each direction, as would longer seaweeds
in large waves.
This `going with the flow' strategy reduced the force experienced by these
models in waves. As a flexible organism moves with the flow, little force is
imposed during this portion of the cycle
(Koehl, 1986). However, by
moving with the flow an organism gains momentum, and this can impose an
inertial force if the organism reaches the end of its tether before the flow
reverses and is jerked abruptly to a halt
(Denny et al., 1998). Such
inertial forces can be high if the organism is moving rapidly when it is
jerked to a halt and when a large proportion of the mass of the organism is
situated at its end (Friedland and Denny,
1995). Inertial forces were not experienced by any of the models
in this experiment due to the relatively slow velocity of the waves in the
wave tank, and the even distribution of mass along the length of models.
However, dependent on the type and velocity of flow, the wave period and
amplitude, the length, flexibility and distribution of mass along the stipe,
inertial jerk forces can be substantial, and the effect of `going with the
flow' may alternatively decrease or increase the forces experienced by
flexible organisms in waves.
In this experiment whiplashing reduced the force experienced at the bases
of the most flexible models. Ends of whiplashing models moved in the opposite
direction to the flow because the water had reversed by the time the tips of
the models were completely pulled to their full length in one direction. This
resulted in the tips of these models moving faster than the surrounding water
and negative relative velocities at the tips of these models resulting in low
force experienced in waves. However, at higher oscillatory velocities,
whiplashing may lead to tattering or tearing as the ends of the frond are
snapped, similar to the way a whip cracks
(Gaylord and Denny, 1997).
Effect of buoyancy
Cost of buoyancy
Buoyancy is a mechanism that produces upright postures in marine organisms
without investing much energy into structural support. However, production and
maintenance of buoyancy may have associated costs. For example, reduced
photosynthetic rates have also been noted in algal blades possessing
pneumatocysts relative to those without
(Kilar et al., 1989).
Therefore, if both stiffness and buoyancy impose costs to an organism while
both function to maintain its upright position in the water column, it is not
surprising that stiff, buoyant organisms are uncommon in nature. Buoyant
organisms tend to be flexible. The consequences of buoyancy to hydrodynamic
forces depend on the degree of buoyancy and the type of flow an organism
experiences.
Moderate buoyancy
A moderate level of buoyancy (defined here as just enough to impart
positive buoyancy) does not prevent a flexible organism from moving with the
motion of the water around it, but functions to return an organism to an
upright posture as the flow slows. Moderate buoyancy is an effective strategy
in areas of low or moderate unidirectional flow, where maintaining an upright
posture allows organisms to take advantage of faster flow higher in the
boundary layer, enhancing mass transfer. Examples of such areas include areas
exposed to tidal currents where water flows for hours in one direction before
reversing, and in backreefs where water passes over the reef crest and moves
in one direction to the mouth of an adjacent bay, creating unidirectional flow
through the backreef.
Buoyancy, combined with flexibility, can create a buffer against high forces for organisms that are exposed to periodic pulses of high water velocity (e.g. occasional waves in areas dominated by tidal currents), or in waves. During periods of high flow they can be pushed down into the slower flow close to the substratum, where they may escape high hydrodynamic forces, but are righted by their buoyancy after the flow slows. By this mechanism, flexible, moderately buoyant organisms can resist dislodgement during occasional or periodic high-flow events without investing additional resources in structural support.
By providing a mechanism to return an alga to an upright posture after it
has compacted in response to water motion, buoyancy may also increase light
interception. Compaction of fronds or thalli into streamlined shapes can lead
to self-shading of blades layered on top of one another. Passive righting and
spreading of compacted blades can help to maximize light interception for
plants that may be exposed to frequent pulses of high velocities
(Harder et al., 2004).
The combination of moderate buoyancy and flexibility may also be an effective mechanism in areas where the height of the water changes due to tidal exchange, as this combination enables organisms to remain at or near the surface of the water throughout the tidal cycle without the danger of becoming exposed to the air at low tide, as might happen with a stiff organism taller than the water depth at low tide.
High buoyancy
Extra-buoyant models used in this experiment had buoyant forces 5x
higher than real fronds and the results show that they behaved like stiff
models in the amount they were deflected, and in the timing of their movement
relative to peak forces in both unidirectional flow and in waves. Because very
high buoyancy can result in high forces in moving water, this is not a
strategy well suited to high-flow habitats. As with T. ornata, other
buoyant seaweeds in high-flow areas have also been reported to have reduced
buoyancy via air bladders that are absent or smaller than those of
their counterparts in calm habitats
(Burrows and Lodge, 1954;
Chapman, 1961;
Jordon and Vadas, 1972;
Russell, 1978). In some
species, airbladders may also have more streamlined shapes in high-flow
environments (Bergquist,
1959).
In addition to affecting hydrodynamic forces, buoyancy also imparts tensile
forces on organisms that add to the total force contributing to potential
detachment from the substratum. In T. ornata the buoyant force is
small relative to the hydrodynamic force experienced by the frond in moderate
flow (Stewart, 2004). However,
as buoyancy increases so too does tensile force, and in extra-buoyant
organisms the tensile force could become substantial. The upward component to
total force contributed by buoyancy may act to reduce whiplashing of flexible
organisms (Stevens et al.,
2002), as high buoyant forces function to stretch a flexible
organism toward the surface, extending it and making it move more as a single
unit, reducing whiplashing.
Not buoyant
Flexible organisms that are not buoyant face the possibility of not being
able to support their own weight or right themselves after being pushed over
by water motion. This can be advantageous for reducing hydrodynamic forces in
rapid unidirectional flow where organisms can escape high velocities low in
the boundary layer. However, they face the potential problems of shading and
mass transfer limitation.
The present experiment highlights the fact that the effect of non-buoyancy
on hydrodynamic force depends on the relative degree of non-buoyancy, the
flexural stiffness of the organism, and the type of water flow that the
organism experiences. In waves, non-buoyant flexible organisms that cannot
support their own weight and flop to the substratum may accrue some advantage
by being able to sweep the substratum around them, dislodging young plants and
other potential competitors for space
(Black, 1974;
Velimirov and Griffiths,
1979). Depending on the stiffness of non-buoyant organisms and the
flow velocity they experience, they may slump down onto the substratum or they
may just slump a bit to one side, as was the case for the non-buoyant models
in this experiment, because the flow velocities in the wave tank were not
sufficient to push the non-buoyant models over. If the velocity of the water
in the wavy flow had been higher or the non-buoyant models used in this
experiment had been more flexible, then the non-buoyant models might have been
pushed over further toward the bottom. However, the non-buoyant models in this
experiment were stiff enough to stay upright in the waves used in this
experiment. They therefore experienced high relative velocities and forces,
similar to stiff models in waves.
Conclusions
Upright postures are important for light interception and mass transfer of
benthic organisms. However, an upright posture can also expose organisms to
hydrodynamic forces that may be detrimental. Both EI and buoyancy are
mechanisms to maintain upright postures in water, and each has different
hydrodynamic consequences in unidirectional flow and waves. Stiff algae
experience high forces in moving water, but if they are also strong they can
persist in areas where mass transfer of nutrients and gases is enhanced by
fast flow. Buoyancy can have similar consequences to stiffness for relative
water velocities and hydrodynamic force, because both mechanisms reduce the
amount the organism is deflected in the direction of moving water. However, as
flow speeds increase and hydrodynamic forces overcome the ability of a buoyant
or stiff organism to maintain its upright posture, a stiff organism may break,
whereas buoyancy enables an organism to `rebound' back to an upright posture
after it has been pushed over by moving water.
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Acknowledgments |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Alben, S., Shelley, M. and Zhang, J. (2002). Drag reduction through self-similar bending of a flexible body. Nature 420,479 -481.[CrossRef][Medline]
Atkinson, M. J. and Bilger, R. W. (1992). Effects of water velocity on phosphate uptake in coral reef flat communities. Limnol. Oceanogr. 37,273 -279.
Bergquist, P. L. (1959). A statistical approach to the ecology of Hormosira banksii. Botanica Marina 1, 29-53.
Black, R. (1974). Some biological interactions affecting intertidal populations of the kelp Egregia laevigata.Mar. Biol. 28,189 -198.
Blanchette, C. A. (1997). Size and survival of intertidal plants in response to wave action: a case study with Fucus gardneri. Ecology 78,1563 -1578.[CrossRef]
Bouma, T. J., De Vries, M. B., Low, E., Peralta, G., Tanczos, I. C., Van de Koppel, J. and Herman, P. M. (2005). Trade-offs related to ecosystem engineering: a case study on stiffness of emerging macrophytes. Ecology 86,2187 -2199.
Boynton, W. R., Kemp, W. M., Osborne, K. R. and Jenkins, M. C. (1981). Influence of water circulation rate on in situ measurements of benthic community respiration. Mar. Biol. 65,185 -190.[CrossRef]
Burrows, E. M. and Lodge, S. M. (1954). The analysis of variation within the genus Fucus. In Species Studies in the British Flora (ed. J. E. Lousely), pp.83 -85.London: Botanical Society of the British Isles, British Museum.
Carpenter, R. C., Hackney, J. M. and Adey, W. H. (1991). Measurements of primary productivity and nitrogenase activity of coral reef algae in a chamber incorporating oscillatory flow. Limnol. Oceanogr. 36,40 -49.
Carrington, E. (1990). Mastocarpus papillatus Kutzing. J. Exp. Mar. Biol. Ecol. 139,185 -200.[CrossRef]
Chapman, V. J. (1961). A contribution to the ecology of Egregia laevigataSetchell. Botanica Marina 3,33 -45.
Denny, M. W. (1988). Biology and the Mechanics of the Wave-swept Environment. Princeton, NJ: Princeton University Press.
Denny, M. W., Daniel, T. L. and Koehl, M. A. R. (1985). Mechanical limits to size in wave-swept organisms. Ecol. Monogr. 55,69 -102.[CrossRef]
Denny, M., Gaylord, B., Helmuth, B. and Daniel, T. (1998). The menace of momentum: dynamic forces on flexible organisms. Limnol. Oceanogr. 43,955 -968.
Falter, J. L., Atkinson, M. J. and Coimbra, C. F. M. (2005). Effects of surface roughness and oscillatory flow on the dissolution of plaster forms: evidence for nutrient mass transfer to coral reef communities. Limnol. Oceanogr. 50,246 -254.
Friedland, M. T. and Denny, M. W. (1995). Surviving hydrodynamic forces in a wave-swept environment - consequences of morphology in the feather boa kelp, Egregia menziesii (Turner). J. Exp. Mar. Biol. Ecol. 190,109 -133.[CrossRef]
Gaylord, B. and Denny, M. W. (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.[Abstract]
Gaylord, B., Blanchette, C. A. and Denny, M. W. (1994). Mechanical consequences of size in wave-swept algae. Ecol. Monogr. 64,287 -313.[CrossRef]
Gonen, Y., Kimmel, E. and Friedlander, M. (1995). Gracilaria conferta (Rhodophyta). J. Phycol. 31,768 -773.[CrossRef]
Harder, D. L., Speck, O., Hurd, C. L. and Speck, T. (2004). Reconfiguration as a prerequesite for survival in highly unstable flow-dominated habitats. J. Plant Growth Regul. 23,98 -107.[CrossRef]
Hay, M. E. (1986). Functional geometry of seaweeds: ecological consequences of thallus layering and shape in contrasting light environments. In On the Economy of Plant Form and Function; Sixth Maria Moors Cabot Symposium on Evolutionary Constraints on Primary Productivity (ed. T. J. Givnish), pp.635 -666.Cambridge: Cambridge University Press.
Holbrook, N. M., Denny, M. W. and Koehl, M. A. R. (1991). Intertidal "trees": Consequences of aggregation on the mechanical and photosynthetic properties of sea palms Postelsia palmaeformis Ruprecht. J. Exp. Mar. Biol. Ecol. 146,39 -68.[CrossRef]
Hurd, C. L. and Stevens, C. L. (1997). Flow visualization around single- and multiple-bladed seaweeds with various morphologies. J. Phycol. 33,360 -367.[CrossRef]
Jackson, G. A. (1997). Currents in the high drag environment of a coastal kelp stand off California. Cont. Shelf Res. 17,1913 -1928.[CrossRef]
Jackson, G. A. and Winant, C. D. (1983). Effect of a kelp forest on coastal currents. Cont. Shelf Res. 2, 75-80.
Johnson, A. S. (2001). Drag, drafting, and
mechanical interactions in canopies of the red alga Chondrus crispus.Biol. Bull. 201,126
-135.
Jordon, A. J. and Vadas, R. L. (1972). Influence of environmental parameters on intraspecific variation in Fucus vesiculosus. Mar. Biol. 14,248 -252.
Kilar, J. A., Littler, M. M. and Littler, D. S. (1989). Functional-morphological relationships in Sargassum polyceratium (Phaeophyta): phenotypic and ontogenetic variability in apparent photosynthesis and dark respiration. J. Phycol. 25,713 -720.[CrossRef]
Koch, E. W. (1993). The effect of water flow on photosynthetic processes of the alga Ulva lactuca L. Hydrobiologia 260-261,457 -462.[CrossRef]
Koch, E. W. (1994). Hydrodynamics, diffusion-boundary layers and photosynthesis of the seagrasses Thalassia testudinum and Cymodocea nodosa. Mar. Biol. 118,767 -776.[CrossRef]
Koehl, M. A. R. (1977). Effects of sea anemones
on the flow forces they encounter. J. Exp. Biol.
69, 87-105.
Koehl, M. A. R. (1984). How do benthic organisms withstand moving water? Am. Zool. 24, 57-70.
Koehl, M. A. R. (1986). Seaweeds in moving water: form and mechanical function. In Ecology of Plant Form and Function (ed. T. J. Givnish), pp.603 -634.Cambridge: Cambridge University Press.
Koehl, M. A. R. and Alberte, R. S. (1988). Flow, flapping, and photosynthesis of Nereocystis luetkeana: a functional comparison of undulate and flat blade morphologies. Mar. Biol. 99,435 -444.[CrossRef]
Koehl, M. A. R. and Wainwright, S. A. (1977). Mechanical adaptations in a giant kelp. Limnol. Oceanogr. 22,1067 -1071.
Mann, K. H. and Lazier, J. R. N. (1996). Dynamics of Marine Ecosystems: Biological-Physical Interactions in the Oceans. Cambridge, MA: Blackwell Scientific Publications.
Martinez, M. M. (2001). Running in the surf:
hydrodynamics of the shore crab Grapsus tenuicrustatus. J. Exp.
Biol. 204,3097
-3112.
Norton, T. A., Mathieson, A. C. and Neushul, M. (1981). Morphology and environment. In The Biology of Seaweeds (Botanical Monographs). Vol. 17 (ed. C. S. Lobban and M. J. Wynne), pp.421 -451.Berkeley: University of California Press.
Patterson, M. R. and Sebens, K. P. (1989).
Forced-convection modulates gas-exchange in Cnidarians. Proc. Natl.
Acad. Sci. USA 86,8833
-8836.
Patterson, M. R., Sebens, K. P. and Olson, R. R. (1991). In situ measurements of flow effects on primary production and dark respiration in reef corals. Limnol. Oceanogr. 36,936 -948.
Payri, C. E. (1984). Variations biologiques et morphologiques en fonction du milieu chez Turbinaria ornata (Turner) J. Agardh (Pheophycees) du recif de Tiahura - Ile de Moorea - Polynesie Francaise. Botanica Marina 17,327 -333.
Payri, C. E. and N'Yeurt, D. R. (1997). A revised checklist of Polynesian benthic marine algae. Aust. Syst. Bot. 10,867 -910.[CrossRef]
Payri, C. E. and Stiger, V. (2001). Macroalgal community changes on French Polynesian reefs, 1980-2000. Phycologia 40,111 .
Reidenbach, M. A., Keoseff, J. R., Monismith, S. G., Steinbuck, J. V. and Genin, A. (2006). The effects of waves and turbulence on mass transfer within branched reef corals. Limnol. Oceanogr. 51,1134 -1141.
Russell, G. (1978). Environment and form in the discrimination of taxa in brown algae. In Modern Approaches to the Taxonomy of Red and Brown Algae. Vol. 10 (ed. D. E. G. Irvine and J. E. Price), pp.339 -369.London: Academic Press.
Stevens, C. L., Hurd, C. L. and Smith, M. J. (2002). Field measurement of the dynamics of the bull kelp Durvillaea antarctica (Chamisso) Heriot. J. Exp. Mar. Biol. Ecol. 269,147 -171.[CrossRef]
Stevens, C. L., Hurd, C. L. and Isachsen, P. E. (2003). Modelling of diffusion boundary layers in subtidal macroalgal canopies: the response to waves and currents. Aquat. Sci. 65,81 -91.
Stewart, H. L. (2004). Hydrodynamic consequences of maintaining an upright posture by different magnitudes of stiffness and buoyancy in the tropical alga Turbinaria ornata. J. Mar. Syst. 49,157 -167.[CrossRef]
Stewart, H. L. (2006a). Morphological variation and phenotypic plasticity of buoyancy in the macroalga Turbinaria ornata across a barrier reef. Mar. Biol.Doi 10. 1007/s00227-005-0186-z .
Stewart, H. L. (2006b). Ontogenetic changes in buoyancy, breaking strength, extensibility and reproductive investment in a rafting macroalga Turbinaria ornata (Phaeophyta). J. Phycol. 42,43 -50.[CrossRef]
Stewart, H. L. and Carpenter, R. C. (2003). The effects of morphology and water flow on photosynthesis among and within functional form groups of marine macroalgae. Ecology 84,2999 -3012.[CrossRef]
Velimirov, B. and Griffiths, C. L. (1979). Wave-induced kelp movement and its importance for community structure. Mar. Biol. 22,169 -172.
Vogel, S. (1994). Life in Moving Fluids: The Physical Biology of Flow. Princeton, NJ: Princeton University Press.
Wainwright, S. A., Biggs, W. D., Currey, J. D. and Gosline, J. M. (1976). Mechanical Design in Organisms. New York: John Wiley.
Wheeler, W. N. (1988). Algal productivity and hydrodynamics: a synthesis. In Progress in Phycological Research. Vol. 6 (ed. F. E. Round and D. J. Chapman), pp. 23-58.Biopress.
Wing, S. R. and Patterson, M. R. (1993). Effects of wave-induced lightflecks in the intertidal zone on photosynthesis in the macroalgae Postelsia palmaeformis and Hedophyllum sessile (Phaeophyceae). Mar. Biol. 116,519 -525.[CrossRef]
Worcester, S. E. (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.
Zar, J. H. (1999). Biostastical Analysis. Upper Saddle River, NJ: Prentice-Hall.
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