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First published online January 17, 2007
Journal of Experimental Biology 210, 522-532 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02679
The interaction of CO2 concentration and spatial location on O2 flux and mass transport in the freshwater macrophytes Vallisneria spiralis and V. americana
1 Department of Integrative Biology, University of Guelph, Guelph, Ontario,
N1G 2W1, Canada
2 Faculty of Environmental Sciences, University of Guelph, Guelph, Ontario,
N1G 2W1, Canada
* Author for correspondence (e-mail: ackerman{at}uoguelph.ca)
Accepted 5 December 2006
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CBL) values measured
directly from O2 profiles were 48±2% and 21±1% of the
predicted theoretical CBL values at the upstream and
downstream locations, respectively. It is evident that physiological processes
involving mass transport are coupled and vary in space. Mass transport
investigations of biological systems based solely on hydrodynamic measurements
need to be interpreted with caution.
Key words: hydrodynamics, morphology, photosynthesis, kinetic limitation, mass transfer limitation, DIC, carbon uptake, concentration boundary layer, momentum boundary layer
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;
Nishihara et al., 2005;
Badgley et al., 2006). In the
case of aquatic macrophytes, variations in processes such as nutrient uptake
and photosynthesis are influenced by abiotic and biotic conditions (e.g.
nutrient history, nutrient concentration, water flow, temperature and light)
(Hurd et al., 1996;
Nishihara et al., 2005;
Badgley et al., 2006). The
kinetics of these mass transfer and uptake processes can be linear or
nonlinear and can differ among nutrients and species. For example, in the red
alga Laurencia brongniartii, the uptake kinetics were linear for
nitrate and nonlinear for ammonium
(Nishihara et al., 2005),
whereas nonlinear kinetics were observed for both nutrients in the brown alga
Scytothamnus australis (Phillips
and Hurd, 2004). Indeed, physiology ultimately determines the rate
of such processes; however, the transport of nutrients to the surface of
aquatic macrophytes governs whether the process is kinetically or mass
transfer limited (Sanford and Crawford,
2000; Nishihara and Ackerman,
2006).
Dissolved inorganic carbon (DIC) is available to aquatic macrophytes in the
form of CO and HCO3–
(Madsen and Sand-Jensen,
1991). Whereas HCO3– is the primary
form of DIC available in marine environments due to relatively high pH, the
dominant form of DIC in freshwater varies with ambient pH. However, in cases
where alkalinities are low, freshwater macrophytes have greater access to
dissolved CO2. Increases in CO2 concentrations are,
therefore, thought to benefit freshwater and marine macrophytes capable of
HCO3– uptake that have a higher affinity (i.e.
sensitivity) for CO2 (Madsen
and Sand-Jensen, 1991; Invers
et al., 2001). In general, DIC uptake (i.e. photosynthesis) can be
described by a rectangular hyperbola, where for low DIC, photosynthesis rates
are directly proportional to the DIC concentration, and for large DIC,
photosynthesis rates are saturated
(Maberly and Madsen, 1998;
Invers et al., 2001;
Nishihara and Ackerman, 2006).
The delivery of DIC to supply photosynthesis occurs through diffusive and
advective transport, and differences in rates occur as a result of the
different concentrations and diffusivities of CO2 and
HCO3–. Indeed, in calm water, diffusive transport
can serve as the primary mechanism by which DIC is transported to a
macrophyte, whereas in flowing water advective transport becomes the dominant
mechanism of mass transport. Increased DIC mass transfer rates resulting from
advection can also supply proportionately more DIC in the form of
CO2 (Nishihara and Ackerman,
2006). Therefore, the ecophysiology of aquatic macrophytes is
influenced by the mass transport of nutrients, and in conditions where water
velocities and ambient concentrations are low, productivity can be limited by
mass transport (Stevens and Hurd,
1997; Cornelisen and Thomas,
2006; Nishihara and Ackerman,
2006).
Mass transfer rates are a function of the freestream velocity (U),
the molecular diffusivities (D) of DIC, the concentration gradient
(
C=CS–CB) between the
bulk water (CB) and the surface concentrations
(CS), and the geometry of the macrophyte. An increase in
U or C will increase mass transfer rates and thus
provide more DIC, leading to higher rates of photosynthesis
(Nishihara and Ackerman,
2006). Mass transfer rates may vary with location, as in the case
of a flat plate oriented parallel to the flow, where mass transfer rates
decrease monotonically with increasing downstream direction
(Schlichting and Gersten,
2000). Whether the mass transfer rates of nutrients vary spatially
over the surface of a macrophyte, and thus influence physiological processes,
remains to be determined.
The freshwater angiosperms, Vallisneria spiralis L. and
Vallisneria americana Michx., are found throughout Europe and North
America, respectively, and occupy similar niches in their respective
environments (Sculthorpe,
1967). Both species can assimilate
HCO3– (Prins
et al., 1980; Madsen and
Sand-Jensen, 1991) and can be found in waters high in alkalinity
(i.e. 100–1400 mmol m–3
HCO3–) (Pip,
1984). More importantly, a key morphological trait that
differentiates the two is the spiral twist found in V. spiralis
(Fig. 1A), unlike the
relatively flat leaves of V. americana
(Fig. 1B). Little is known
about the function of the twist; however, morphological features, which
present a more complex geometry than that of a flat surface, have been found
to enhance mass transport and physiological processes in other aquatic
organisms (Hurd et al., 1996;
Falter et al., 2005). V.
spiralis and V. americana provide an excellent opportunity to
determine whether and how physiological processes are influenced by physical
and environmental factors in two closely related species. The objective of
this study is, therefore, to determine: (1) how the O2 flux of
V. spiralis and V. americana is influenced by CO2
concentrations and velocity; (2) how O2 flux and mass transfer
rates vary with respect to spatial location; and (3) how a flat and twisted
leaf morphology affects O2 flux and mass transport.
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). The photosynthetically active radiation (PAR) level was
maintained at 7.3 µmol photon m–2 s–1 (16
h:8 h L:D), as measured in the center of the aquaria with a 4
sensor
(QSL2101, Biospherical Instruments, San Diego, CA, USA), to discourage the
growth of microalgae and other potential fouling organisms.
Experimental setup
The experimental setup is described in detail elsewhere
(Nishihara and Ackerman, 2006;
Nishihara and Ackerman, 2007).
Briefly, a 10 cmx10 cmx100 cm long (water depth: 5–8 cm)
flow chamber, with flow straighteners in the first 12 cm, was operated at
freestream velocities of 0.5, 0.8, 1.1, 1.8, 2.1, 3.3, 4.1 and 6.6 cm
s–1. Velocity profiles in the empty flume were determined
using digital particle image velocimetry (PIV) at the location of the leading
edge of the leaf (56 cm downstream of the flow straighteners), and were
uniform in shape, especially at the height where the O2 profiles
were obtained above leaf surfaces (3 cm above the flume bottom)
(Nishihara and Ackerman,
2006). The flow chamber water was maintained at 24°C, and
aerated to maintain O2 and CO2 saturation, using a
mixture of tapwater [pH=9.2±0.2 (mean ± s.e.m.)] and deionized
water having a final HCO3– concentration of 460
mmol m–3. PAR (153 µmol photon m–2
s–1) was provided by a slide projector with a quartz lamp
(General Electric, Fairfield, CT, USA) adjusted with neutral density filters.
The bulk O2 concentration and O2 profiles in the CBL
were determined using OXN and OX25 oxygen microsensors (Unisense, Aarhus,
Denmark), respectively. The O2, pH and water temperature were
recorded continuously by a computer.
V. spiralis and V. americana leaves were selected from
the culture that were: (1) free of obvious epiphytes; (2) at least 8 cm long;
(3) twisted only once in a 8 cm span in the case of V. spiralis; and
(4) without undulations along the length and width of the leaf in the case of
V. americana. The leaves were trimmed to size (8 cm in length), the
cut ends were sealed with wax, and allowed to acclimate overnight in the flow
chamber water. Leaf sections were glued (cyanoacrylate-based adhesive) to a
wire stand, and placed in the working section of the flow chamber,
perpendicular to the light source, and parallel to the flow. After each
experiment, images of sections of the leaf approximately 1 cm2 from
the upstream and downstream locations (i.e. 1 cm and 7 cm from the leading
edge of the leaf, respectively) were taken and the samples were frozen
(–20°C) for later chlorophyll a+b analysis.
Chlorophylla+b content was determined as described
(Nishihara and Ackerman,
2006). These two closely related species were chosen in part
because their physiologies were assumed to be similar.
Measured variables
The effect of the experimental factors (i.e. species-leaf configuration,
upstream vs downstream measurement location on the leaf surface,
CO2 concentration and velocity) on O2 flux, mass
transport and the thickness of the concentration boundary layer
(CBL) were investigated by profiling the O2
concentration above the leaves (z=0–0.5 cm) of each leaf at
x=1 and 7 cm downstream from the leading edge of the leaf (i.e. the
upstream and downstream locations). The CO2 concentration was
adjusted to 1.71 mmol m–3 and 17.1 mmol m–3
by adding 50 mmol m–3 Tris buffer and appropriate amounts of
HCl (i.e. to obtain a pH of 7.5 and 8.5, respectively) to the water in the
flow chamber (Stumm and Morgan,
1996). During the course of the experiments pH and
HCO3– concentrations remained stable, regardless
of aeration, and no negative effects of the buffer on photosynthesis were
observed. At least 5 min elapsed prior to determining the O2
profiles for each species-leaf configuration, measurement location, and
CO2 concentration at all U and a randomized block design
was used to minimize the effects of acclimation time. A total of nine V.
spiralis and six V. americana leaves were analyzed at 1.71 mmol
m–3 CO2 and six V. spiralis and six
V. americana leaves were analyzed at 17.1 mmol m–3
CO2. Eight V. americana leaves were also reconfigured from
a flat to twisted configuration by gently twisting the leaf to mimic V.
spiralis, and maintaining the abaxial surface to the O2
microsensor. In this case, experiments were conducted at 17.1 mmol
m–3 CO2 at the downstream location in the flat and
twisted configurations.
Theory
The O2 flux (J), mass transfer coefficient
(kc), and the concentration boundary layer thickness
(CBL) were determined by fitting a hyperbolic tangent model
to the measured O2 profiles
(Nishihara and Ackerman,
2007):
 | (1) |
=(CS–C)/(CS–CB)
is the dimensionless concentration, a is a parameter that describes the slope
of the model at z=0, and b is a parameter that defines the invariant
portion of the O2 profile. By taking the first derivative of the
model and evaluating the concentration gradient at the leaf surface
(z=0), J can be determined from Fick's first law:
 | (2) |
).
To determine how the experimental factors influence O2 flux, the
relationship between O2 flux (Jchla+b) and
velocity were analyzed through linear and a nonlinear regression, using:
 | (3) |
).
The mass transfer of O2 was analyzed by determining the local
Sherwood number (Shx) for each mass transfer coefficient
(kc) determined from the O2 profiles.
kc was calculated by dividing J by the
O2 concentration gradient (C) between the leaf
surface and bulk water. Shx, which is the ratio of the
advective to diffusive flux that provides a measure of the relative importance
of advection, was determined by:
 | (4) |
A local Reynolds number (Rex), which is the ratio of
inertial to viscous forces in the boundary layer above the leaf, was
determined to elucidate the effects of U and x on
Shx, by:
 | (5) |
is the molecular diffusivity of momentum
(0.922x10–6 m2 s–1 at
24°C), recognizing that:
 | (6) |
) and B and C are a function of the flow regime. When rates of
physiological processes are slow compared to mass transfer rates (i.e. kinetic
limitation) and the concentration boundary layer is laminar, A=0.464, B=0.5
and C=0.33, whereas when the concentration boundary layer is turbulent,
A=0.030, B=0.8 and C=0.6 (Kays et al.,
2005). Sc is the Schmidt number, which is the ratio of
the momentum diffusivity to the molecular diffusivity. A linear regression of
the double log plot of Shx/ScC vs
Rex provides estimates of parameters A and B. Parameter C was
set to 0.33 for the analysis, since there was no a priori way of
determining the regime of the boundary layer. Note that this in no way affects
the estimates of B, which is the parameter of interest in this study, since
ScC is constant at the experimental conditions
investigated (Sc=384 for O2 at 24°C).
For a laminar concentration boundary layer, CBL was
determined from the model fit to the measured O2 profiles
(Eqn 1) and is defined as the
distance from the leaf surface where the O2 concentration is 99% of
the bulk concentration (Nishihara and
Ackerman, 2007). The relationship between CBL
and U and x can be analyzed in a form similar to that of
Eqn 6, by substituting
Shx with CBLx–1
Sc–0.33, recognizing that the CBL can
be expressed as:
 | (7) |
DSL) can be defined, where diffusive transport
becomes important (i.e. analogous to a laminar concentration boundary layer)
(Dade, 1993),
 | (8) |
=
u*2, where is the
density of water and is the boundary shear stress determined from the
1/7 power-law (White,
1999).
kc, Shx and the
DSL can also be determined from hydrodynamic measurements of
the momentum boundary layer (Nishihara and
Ackerman, 2006). Vertical profiles of the momentum boundary layer
at the upstream and downstream locations were obtained for V.
spiralis and V. americana in the flat and twisted configurations
using PIV. Shear velocities, which were determined by multiplying the von
Karman constant (
=0.41) by the slope of the velocity vs
ln(z) in the logarithmic portion of the boundary layer
(Ackerman and Hoover, 2001),
were used to estimate kc and the DSL
(Dade, 1993) where:
 | (9) |
DSL is determined from
Eqn 8. The
Shx in a turbulent concentration boundary layer is
determined by substituting kc into
Eqn 4.
Statistical analysis
Statistica 6.1 (Statsoft, Inc., Tulsa, OK, USA) and R (R Development Core
Team, 2006) were used to analyze the data. Linear and nonlinear regressions
were used as appropriate, and an F-test was used to determine whether
these were significant, ANCOVA was used to determine whether differences in
slopes of the linear regressions were significant, and Tukey's test was used
to examine multiple comparisons. For regression analyses of
Shx and CBL, determined from
O2 profiles, log(Rex) was the covariate and
species-leaf configuration (i.e. V. spiralis, V. americana and V.
americana in the twisted configuration), position and CO2
concentration were the factors. In the case of PIV determined
Shx and DSL,
log(Rex) was the covariate and species-leaf configuration
and measurement location were the factors. Significance was defined at
P=0.05 and values are reported as mean ± s.e.m., except for
the nonlinear regressions where s.e.m. is asymptotic.
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)
and is comparable to other studies involving aquatic macrophytes
(Madsen and Sand-Jensen,
1991).
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In contrast, the relationship between the O2 flux at 1.71 mmol m–3 CO2 and U varied with location along the leaf, but not with species (Fig. 2B). O2 profiles were difficult to determine at the higher velocities for V. spiralis and V. americana at this CO2 concentration because the concentration gradient was too thin to profile. Specifically, eight downstream O2 profiles were obtained at 4.1 and 6.6 cm s–1 for V. spiralis, compared to V. americana where five profiles were obtained at 3.3 and 4.1 cm s–1 and none at 6.6 cm s–1 at the upstream location; only four profiles at 4.1 cm s–1 and two profiles at 6.6 cm s–1 were obtained at the downstream location. Nevertheless, the O2 flux at the upstream location was greater than the downstream location when U<Vsat=1.8±0.9 cm s–1 (Fig. 2B). The O2 flux was nonlinear at the upstream location, and Eqn 3 was fit to the data. An F-test revealed that the most appropriate model for this location was a reduced form (common V and Jmax in Eqn 3; r2=0.26, F(2,13)=2.94, P=0.026), since neither a full model nor a common V model was significant (F(11,13)=0.26, P=0.79 and F(11,12)=0.48, P=0.50, respectively) (Table 1). In contrast, at the downstream location, O2 flux appeared to increase linearly with U, and a linear model was applied to the data. In this case, an ANCOVA revealed that the slopes for the two species were not significantly different (F(1,11)=0.23, P=0.64) and species had no effect on O2 flux (F(1,12)=0.023, P=0.88), therefore a common linear model was applied to these data (r2=0.67, F(1,13)=29.61, P<0.0001) (Table 1).
Mass transfer
The Shx for the O2 profiles increased with
Rex for all species-leaf configurations, CO2
concentrations, and measurement locations
(Fig. 3). Measurement location
had a significant effect on the slope of the regressions
(F(2,58)=9.94, P=0.0002) and the individual
regressions for each species-leaf configuration and measurement location were
significant (r2>0.68, P<0.05; see
Table 2A). There were no
significant differences among slopes (i.e. logB) at the upstream location
(P>0.05), which was similar to previous results for V.
americana (0.45±0.04)
(Nishihara and Ackerman, 2006)
and for theoretical laminar mass transport over a flat plate (0.5)
(Schuepp, 1993). Whereas the
intercepts were not significant, they were much greater than the theoretical
value for parameter A for a constant surface flux boundary condition in a
laminar boundary layer [i.e.
log(0.464Sc–0.33)=–1.18
(Schlichting and Gersten,
2000)]. In contrast, the slopes at the downstream location were
heterogeneous (P<0.05; Table
2A), although a multiple comparisons test, indicated that the
slopes for V. spiralis (0.87±0.09) and V. americana
(0.82±0.07) in the twisted configuration at 17.1 mmol
m–3 CO2 were similar (P>0.05), as were
V. americana at 17.1 mmol m–3 CO2
(0.70±0.10) and V. spiralis at 1.71 mmol m–3
CO2 (0.69±0.05). The slopes determined at the downstream
location were of similar order to the theoretical value for mass transport in
a turbulent concentration boundary layer over a flat plate (0.8)
(Kays et al., 2005). The
log-transformed intercepts (P>0.05) were not significantly
different from zero; however, they were greater than predicted by a
theoretical turbulent concentration boundary layer [i.e.
log(0.030Sc–0.33)=–2.37
(Schlichting and Gersten,
2000)].
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The shear velocities determined from the PIV ranged from 0.040±0.002 to 0.7±0.1 cm s–1, and the u* values at the upstream locations were always greater than those measured at the downstream location at each velocity (Table 3). Moreover, u* increased with freestream velocity for all species-leaf configurations and measurement locations. The Shx determined from hydrodynamic measurements (i.e. PIV results) also increased with increasing Rex (Fig. 4). The slope of the Shx–Rex regression did not vary with measurement location (F(1,39)=0.21, P=0.65), which is in contrast to the Shx determined from the O2 concentration boundary layer. However, there was a species-leaf configuration effect (F(2,40)=4.53, P=0.017), where the slope for the regressions at the downstream location of V. americana in the twisted configuration was significantly different from all the other slopes (P<0.05), except for the slope determined at the downstream location of V. spiralis (Table 2B). The intercepts determined at the upstream locations were significantly different from zero (P<0.05), in contrast to the downstream locations (Table 2). Regardless, these values were also larger than that predicted by the turbulent concentration boundary layer.
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Concentration boundary layer
The CBL determined from the O2 profiles and
the DSL determined from the PIV measurements decreased with
increasing velocity and Rex for both species-leaf
configuration and measurement location
(Fig. 5). Whereas
CBL determined from the O2 profiles appeared
similar in shape and thickness at both locations
(Fig. 5A,C), the
CBL was thinner at the upstream location when normalized to
distance from the leading edge of the leaf (i.e. plotted vs
Rex) (Fig.
5B,D). ANCOVA revealed that measurement location affected the rate
of change of the thickness of the CBL with respect to
Rex [i.e.
log(CBLx–1Sc–0.33)
varied with Rex] and significant differences were detected
between measurement locations (F(2,64)=8.53,
P<0.0001). The slopes of the regressions at the upstream location
were homogeneous (P>0.05), whereas they were heterogeneous at the
downstream location (P<0.05;
Table 4). The slopes of V.
spiralis at both CO2 concentrations were similar
(P>0.05), as were both leaf configurations of V.
americana (P>0.05) at both CO2 concentrations
(Table 4). There was some
overlap between the species-leaf configurations, where the slopes V.
spiralis at 1.71 mmol m–3 CO2 were similar to
those of V. americana and the slopes of V. americana at 1.71
mmol m–3 CO2 were similar to those of V.
spiralis. The CBL among species-leaf configuration,
measurement location and CO2 concentration were similar
(P>0.05); however, the average CBL values at
both measurement locations were thinner at the upstream (48±2%) and
downstream locations (21±1%) compared to the theoretical
CBL (based on Eqn
7).
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The diffusive sublayer thickness (DSL) determined from
Eqn 8, using the measured shear
velocities, was similar in thickness to theoretical estimates of the
DSL determined from the 1/7 power law
(White, 1999) at the leading
edge (106±6% of the theoretical DSL;
Fig. 5E) whereas at the
trailing edge the DSL was 51±2% of the theoretical
DSL (Fig.
5E,F).
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;
Lobban and Harrison, 1994;
Schippers et al., 2004;
Nielsen et al., 2006). In this
study, O2 flux was similar in both species at low CO2
concentrations. However, increasing the CO2 concentration only
enhanced the photosynthesis rates of V. spiralis, with no effect on
V. americana. It is evident that V. spiralis is better able
to respond to the higher CO2 concentrations and increase its
O2 flux.
The difference in O2 flux between V. spiralis and
V. americana is likely due to physiological
(Fig. 2A) rather than
morphological differences, given that the twisted configuration of V.
americana did not enhance O2 flux through increases in the
mass transfer coefficient (see below). Moreover, given that DIC was held
constant and that the HCO3– concentrations at both
CO2 concentrations were similar (i.e. 460 mmol m–3
HCO3–), the increase in O2 flux with
increases in CO2 concentration implies that the flux of
CO2 is greater for V. spiralis than V. americana.
Regardless of the ability to use both CO2 and
HCO3– (Prins
et al., 1980; Madsen and
Sand-Jensen, 1991), the enhancement of O2 flux in
V. spiralis suggests differences in CO2 affinity between
the two species, namely that V. spiralis has a higher affinity for
CO2. Such variations in CO2 affinity are not uncommon,
and in general freshwater macrophytes that depend on CO2 as the
sole source of carbon have the highest affinity for CO2
(Madsen and Sand-Jensen,
1991). Freshwater macrophytes such as V. spiralis and
V. americana, which are able to use
HCO3–, are intermediate in their affinity for
CO2, whereas marine macrophytes that exist in relatively high pH
waters have the lowest CO2 affinity
(Madsen and Sand-Jensen,
1991).
As already mentioned, the effect of low CO2 concentrations was
similar between the species; however, the relationship between O2
flux and velocity varied spatially. Specifically, O2 flux was
saturated at Vsat >1.8±0.9 cm
s–1 at the upstream location, but O2 flux
continued to increase with velocity at the downstream location
(Fig. 2B). This linear
relationship suggests that photosynthesis is mass transfer limited at the
downstream location. However, O2 flux did not vary spatially at the
high CO2 concentration, where the O2 flux saturated at
both measurement locations for both species
(Fig. 2A). Evidently, the
behavior of nutrient uptake varies spatially on leaf surfaces at low nutrient
concentrations. Spatial heterogeneity in mass transport has not been
incorporated in current models that couple physiology and mass transport
processes (e.g. Sanford and Crawford,
2000). Although, interactions of nutrient concentrations and mass
transport have been observed in the nutrient uptake rates of seagrasses
(Cornelisen and Thomas, 2006),
marine algae (Hurd et al.,
1996) and corals (Badgley et
al., 2006), and in photosynthesis rates of marine macrophytes
(Wheeler, 1980), periphyton
(Larkum et al., 2003) and
V. americana (Nishihara and
Ackerman, 2006), little is known about how freestream velocities
affect the spatial variability in nutrient uptake.
The saturating behavior of O2 flux at the upstream location and
the linearly increasing behavior of O2 flux at the downstream
location suggest that upstream uptake and associated decrease of nutrients in
the concentration boundary layer impact physiological processes occurring
downstream (e.g. Chambré and
Acrivos, 1956; Ackerman et al.,
2001). The mechanism(s) responsible for the downstream decrease in
O2 flux observed in this study has yet to be determined; however,
it is likely that the surface concentrations of nutrients decrease with
downstream distance from the leading edge as a result of nutrient depletion in
the concentration boundary layer.
Mass transfer
The consistency of parameter B in the relationship between
Shx and Rex at the upstream location
(0.47–0.52) demonstrates that the concentration boundary layer was
laminar at that location (Fig.
3, Table 2)
(Schlichting and Gersten,
2000). Conversely, parameter B differed significantly among the
downstream locations (0.69 to 0.95; Fig.
3, Table 2), but
none of these values were significantly different (P>0.05) from
the theoretical value of mass transport in a turbulent concentration boundary
layer (B=0.8) (Schlichting and Gersten,
2000). Based on these observations and those of an earlier study
(Nishihara and Ackerman,
2006), it is apparent that the concentration boundary layer of
V. spiralis and V. americana shifts from a laminar to
turbulent regime between Rex of 700 to 1500. These values
are considerably lower than the transitional velocity for momentum over a
smooth flat plate (Rex=3x105)
(Schlichting and Gersten,
2000), but are similar to mass transport phenomena in terrestrial
plant leaves in a turbulent freestream (e.g. Rex=1860)
(Schuepp, 1993).
Given that surface corrugations on a flat surface were demonstrated to
increase mass transfer rates in engineering applications
(Tzanetakis et al., 2004), the
twisted morphology of V. spiralis was predicted to enhance mass
transport. However, the similar shape obtained by twisting V.
americana did not enhance mass transfer rates
(Fig. 3A,B). This is consistent
with the observation that undulations in the blades of the marine macrophyte
Macrocystis integrifolia did not to enhance inorganic nitrogen uptake
(Hurd et al., 1996). However,
the assimilation of DIC has been recently reported to be related to plant
architecture in aquatic angiosperms
(Nielsen et al., 2006) and
similar morphological effects on nutrient uptake have been reported in corals
(Lesser et al., 1994;
Helmuth et al., 1997). It is
possible that the effect of the twist in V. americana was not
detected, due to limitations in the microsensor technique (see below).
Clearly, the influence of morphological features in mass transport remains an
equivocal issue (cf. Thomas and Atkinson,
1997).
Concentration boundary layer
Concentration boundary layers can be estimated through direct measurements
of the scalar (e.g. O2) profile, or indirectly by measuring the
hydrodynamic boundary layer and multiplying by a scaling factor (e.g.
Sc–0.33) (Dade,
1993). It is common to describe the thickness of the concentration
boundary layer that forms around the surface of macrophytes and refer to it as
`boundary layer resistance' to mass transport
(Wheeler, 1980;
Stevens and Hurd, 1997;
Larkum et al., 2003). In this
case, the CBL is given by
CBL=J/(CS–CB),
by assuming that the surface concentration is zero (i.e. the surface is a
perfect sink) (Wheeler, 1980;
Stevens and Hurd, 1997;
Larkum et al., 2003). However,
the CBL determined by this method, may overestimate
CBL (Stevens and Hurd,
1997; Larkum et al.,
2003) as previously demonstrated
(Nishihara and Ackerman,
2006), where the CBL values determined from
O2 profiles were >63% smaller than the CBL
values determined by using the boundary layer resistance model. These
observations suggest that the two assumptions (i.e. spatially homogeneous flux
and a perfect sink condition) invoked to determine the CBL
values may be inappropriate. For example, saturating nutrient uptake rates at
high velocities indicate kinetic limitation (i.e. mass transfer rates >
nutrient uptake rates), which would occur if the nutrient is in excess and the
surface concentration is >0 (Nishihara
and Ackerman, 2006). It is apparent that indirect estimates of the
concentration boundary layer from hydrodynamic theory overestimate mass
transfer rates in aquatic macrophytes.
The importance of direct measurements of the concentration boundary layer
led to the application of O2 microsensors in boundary layer
research, such as those used in this and other studies
(Glud et al., 1994;
Larkum et al., 2003;
Nishihara and Ackerman, 2006;
Nishihara and Ackerman, 2007).
Evidence suggests that microsensors directly affect the concentration boundary
layer and revealed that the concentration boundary layer, determined by the
DSL, was reduced to 55–75% of the theoretical
DSL (Glud et al.,
1994). It is difficult to assess whether the decrease in the
concentration boundary thickness was caused by the microsensor, given that the
hydrodynamic boundary layer was not characterized in that study
(Glud et al., 1994). However,
it has been suggested that the microsensor has little impact on the
concentration boundary layer at low Reynolds number (Red)
of the microsensor [
6 (Hondzo et al.,
2005)], which ranged from 0.14 to 1.8 in this study. Therefore,
near the surface of the leaf, where velocities are lower than the freestream
velocity (i.e. viscous flow, Red <1), the flow remains
attached to the microsensor. Nevertheless, CBL measured with
the microsensors were 
48% of the theoretical CBL at the
upstream location, which is less that what is predicted by microsensor-induced
compression (Glud et al.,
1994). Therefore, the thinner CBL may also
result from the influence of biological and chemical processes on
O2 flux and concentration boundary layer thickness
(Nishihara and Ackerman,
2006). Given the difficulties in measuring the O2
profiles at high velocities (i.e. >3.3 cm s–1 in this
study) and the possible compression effect of the microsensor, the technique
used in this study may be too coarse to resolve differences between the flat
and twisted leaf morphologies at moderate to high velocities.
Ecological implications
The interaction between physiology and mass transport among species is
complex, and elucidating the mechanisms underlying these processes should
provide insight on how environmental factors influence the biology of aquatic
organisms. In addition, the diversity in these interactions makes it difficult
to predict how environmental alterations including climate change will affect
aquatic ecosystems. Presently, global CO2 levels are increasing,
leading to the acidification of freshwater and marine ecosystems
(Harley et al., 2006).
Macrophytes that are physiologically limited by present CO2 levels
may see a dramatic increase in productivity
(Schippers et al., 2004).
However, in marine systems, where the majority of macrophytes have low
CO2 affinity (Madsen and
Sand-Jensen, 1991), the effects are likely to be small except in
the limited number of marine angiosperms (i.e. seagrasses)
(Invers et al., 2001).
Furthermore, coupled with increased advective transport, the increase in
CO2 mass transfer rates could provide a mechanism for macrophytes
with high CO2 affinity to displace species (e.g. V.
americana) that are less sensitive to increases in CO2. In
areas where water velocities promote high mass transfer rates, small increases
in CO2 could have a significant impact on the distribution of
aquatic macrophytes. However, in marine systems, where the majority of
macrophytes have low CO2 affinity
(Madsen and Sand-Jensen,
1991), the effects are likely to be small. Clearly, further
research is required to elucidate the effects of mass transport on
ecophysiological processes.
Conclusion
Physiological and mass transport mechanisms are coupled and in biological
systems such as aquatic macrophytes these processes vary spatially. The
O2 flux was higher in V. spiralis than in V.
americana when CO2 concentrations were high, but were similar
at the lower CO2 concentration. Importantly, the O2 flux
varied spatially on the leaf surface at low CO2 concentrations,
where O2 flux (i.e. photosynthesis) was kinetically limited at the
upstream location and mass transfer limited at the downstream location.
Further studies are needed to elucidate the effects of morphology on mass
transport and the mechanisms underlying the spatial heterogeneity of
O2 flux and mass transfer rates. Mass transport relationships must
be considered to properly evaluate how changes in environmental conditions
affect the productivity of aquatic ecosystems.
List of abbreviations and symbols
CBL
DSL
C
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Acknowledgments |
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for the upstream and downstream locations of Vallisneria spiralis and
Vallisneria americana (flat and twisted configuration) determined directly
from O2 profiles