JXB Advance Access originally published online on January 10, 2005
Journal of Experimental Botany 2005 56(412):777-786; doi:10.1093/jxb/eri063
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
RESEARCH PAPER |
Adaptations to increasing hydraulic stress: morphology, hydrodynamics and fitness of two higher aquatic plant species
UMR CNRS 5023, Ecology of Fluvial Hydrosystems, Université Claude Bernard–Lyon I, F-69622 Villeurbanne Cedex, France
* To whom correspondence should be addressed. Fax: +33 4 72 43 11 41. E-mail: sara{at}avosnes.univ-lyon1.fr
Received 8 July 2004; Accepted 24 October 2004
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Sessile organisms often exhibit morphological changes in response to permanent exposure to mechanical stimulation (wind or water movements). The adaptive value of these morphological changes (hydrodynamic performance and consequences on fitness) has not been studied extensively, particularly for higher plants submitted to flow stress. The aim was to determine the adaptive value of morphological patterns observed within two higher aquatic plant species, Berula erecta and Mentha aquatica, growing along a natural flow stress gradient. The hydrodynamic ability of each ramet was investigated through quantitative variables (drag coefficient and E-value). Fitness-related traits based on vegetative growth and clonal multiplication were assessed for each individual. For both species, the drag coefficient and the E-value were explained only to a limited extent by the morphological traits used. B. erecta exhibited a reduction in size and low overall plant drag at higher flow velocities, despite high drag values relative to leaf area, due to a low flexibility. The plants maintained their fitness, at least in part, through biomass reallocation: one tall ramet at low velocity, but shorter individuals with many interconnected stolons when flow velocity increased. For M. aquatica, morphological differences along the velocity gradient did not lead to greater hydrodynamic performance. Plant size increased with increasing velocities, suggesting the indirect effects of current favouring growth in high velocities. The fitness-related traits did not demonstrate lower plant fitness for high velocities. Different developmental constraints linked to plant morphology and trade-offs between major plant functions probably lead to different plant responses to flow stress.
Key words: Drag, ecomorphology, fitness, hydraulic ecology, hydrodynamic performance, mechanical constraint, morphological adaptation, submerged aquatic vegetation
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
A general paradigm in ecomorphology (Arnold, 1983
; Wainwright, 1994; Koehl, 1996) consists of focusing on the link between the morphology of organisms and performance in a given environment. Analysis of the performance of a given structure through mechanistic relationships contributes to elucidating the adaptive value of a phenotype in a given environment (Ricklefs and Miles, 1994). ‘Morphology’ refers to the way an organism is built, at any level of organization (Koehl, 1996). ‘Performance’ refers to the relative efficiency of an organism confronted with a given environmental pressure (Wainwright, 1994; Koehl, 1996). In the case of exposure to flow stress, the hydrodynamic performance of a plant is its ability to withstand hydrodynamic forces induced by water movement (e.g. through morphological adjustments). Sultan (1987) considered fitness as ‘the adaptedness of an organism to its environment, which results in its relative success in survival and reproductive output’. Like other sessile organisms, aquatic plants exposed to moving fluids encounter mechanical forces: a drag force (parallel to flow) and a lift force (perpendicular to flow) (Koehl, 1982). To avoid uprooting, minimization of these forces is a major functional consideration for such organisms. Therefore, any morphological adjustment that leads to decreased plant drag, without negative consequences to fitness (long-term survival and reproduction), could be interpreted as an adaptation to flow stress. Adaptation is considered here as a ‘benefit on the organism with regard to its present relationship with its environment’ (Sultan, 1987).
Wind, water movements, and mechanical stimulation are environmental constraints that shape the morphologies of sessile organisms, and which have been widely studied in the case of herbaceous terrestrial plants (Jaffe, 1973), trees (Telewski and Jaffe, 1986), macroalgae (Koehl and Alberte, 1988; Armstrong, 1989; Blanchette, 1997), aquatic mosses (Biehle et al., 1998), and macrophytes (Idestam-Almquist and Kautsky, 1995; Boeger and Poulson, 2003). In moving water, morphological differences observed for exposed individuals of a given species have been associated with (i) resistance to breakage and uprooting through sturdier structures, (ii) avoidance of stress through reduced size or prostrated growth-forms, or (iii) reduction of hydrodynamic resistance through increased flexibility or reconfiguration abilities (Koehl and Alberte, 1988; Blanchette, 1997; Pratt and Johnson, 2002). Some causal relationships between morphology and hydrodynamic performance have been established for macroalgae, through theoretical studies and hydrodynamic comparisons of differently exposed thalli (Armstrong, 1989; Gaylord et al., 1994; Blanchette, 1997). Surprisingly, this question has hardly been addressed for higher aquatic plants, despite their extensive morphological variability in response to water movement (Idestam-Almquist and Kautsky, 1995; Madsen et al., 2001).
Plants exposed to flow generally present growth modifications and morphological changes (e.g. size reduction, changes in biomass allocation) (Idestam-Almquist and Kautsky, 1995; Coops and Van der Velde, 1996). Opposite morphological adjustments can be observed for different species submitted to the same hydraulic constraint (e.g. opposite size variations; Puijalon and Bornette, 2004). The hydrodynamic efficiency of these morphological changes has rarely been assessed in higher plant species (Madsen et al., 2001). For this purpose, it is necessary to assess differences in hydrodynamic performance (and fitness-related differences) of forms that have grown in contrasting hydraulic conditions (Wainwright, 1994; Koehl, 1996). The mechanical advantage of a given morphology (e.g. gain in terms of drag or lift) determines the adaptive value of morphological changes (Sultan, 2000; Debat and David, 2001). As this gain can be negatively selected through a lower fitness, ecomorphological studies should also consider some ecological or biological traits that give information on relative plant fitness.
In this study, two higher aquatic plant species were considered, Berula erecta (Hudson) Coville and Mentha aquatica L., co-occurring along a gradient of increasing flow velocity. Both species have contrasting morphologies. M. aquatica forms long, horizontal runners above ground and relatively rigid erect stems. Its leaves are entire and opposite. B. erecta is a stoloniferous species, consisting of a rosette of petiolated dissected leaves. These contrasting morphologies (erect stems versus rosette) probably require different functional adjustments in the adaptation to flow. This study investigates the functional implications of morphological differences between individuals of these two species colonizing different current velocities. The objectives were (Fig. 1) (i) to determine if morphological changes identified along the increasing stress (i.e. hydraulic) gradient correspond to increasing hydrodynamic abilities of the plants, and (ii) to demonstrate the adaptive value of these morphological changes through the conservation of plant fitness.
|
In this study, morphology was documented at the whole plant level, through morphological measurements on plants collected in situ. Plant performance was assessed through quantitative variables (drag coefficient and E-value, both calculated from drag measurements) allowing a comparison of shape to be made without size-effect. As virtually no sexual reproduction occurs in riffles, fitness was assessed from traits based on vegetative growth and clonal multiplication (Liao et al., 2003
; Santamaria et al., 2003). |
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Study sites and plant collection
B. erecta (Apiaceae) and M. aquatica (Lamiaceae) colonize calcareous nutrient-poor flowing habitats (Carbiener et al., 1990
). Plants were collected in a riverine wetland located in the Rhône River floodplain. Five flow-patches of about 1 m2 were selected along a gradient of increasing velocity. Four out of the five flow patches were common to both species and only patch 1 (flow velocity=0) differed for the two species. Water-depth was 0.2 m on average in all patches, except for patch 1 of B. erecta, which was deeper (0.7 m on average). Flow-patches were separated from each other by only a few metres. All patches were characterized by similar substrate grain size and water physico-chemistry.
As the wetland drains seepage water from the river, its discharge is highly correlated with the river discharge. Therefore, the flow velocity encountered by plants was extrapolated for the four months preceding plant sampling. For this purpose, flow velocity measured on patches at several dates was regressed against daily Rhône River discharge (Table 1). Four flow velocity measurements were made at random on each patch, avoiding hydraulic shelters (big cobbles, tall plants), on 17 dates. Flow velocity was measured with a propeller (C2 current meter, OTT Messtechnik GmbH & Co. KG, Kempten, Germany) at a water depth of 40% above the substrate, which gives a good estimation of the average flow velocity in the water column (Dingman, 1984). No flood scouring occurred during the 4 months preceding plant sampling.
|
All the experiments were carried out during the growing season, from 1 to 11 July 2002 for M. aquatica and from 1 to 14 April 2003 for B. erecta.
Eight submerged individual plants (ramets) were collected from distinct clones in each flow patch, for each species. A ramet of M. aquatica was defined as a shoot end comprising four rooted nodes. An individual ramet of B. erecta was defined as a single rooted rosette. Any horizontal stolon growing from the ramet was removed. After collection, the plants were stored in aerated tap water at 16 °C, for a maximum of 2 d until measurements were made.
Drag and morphological trait measurements were made on the same individuals.
Measurements of drag forces
Plant drag was measured under controlled conditions in an open water flume (Sagnes et al., 2000). Two different hydrodynamic balances were used to measure plant drag, allowing drag measurements along two ranges of drag values. The first, used for M. aquatica, was adapted for measuring high drag values (Statzner et al., 1999; Barrat-Segretain et al., 2002) (Fig. 2a). Plants were fixed by a flexible ribbon to a hollow base (15 cm long, 9.5 cm wide, 4.5 cm high), in the natural growth position. The second balance (modified from the device used by Sagnes et al., 2000), used for B. erecta, was adapted for measuring lower drag values. Plants were tied to a profiled stainless steel rod fixed to the balance (Fig. 2b). The rod formed an L-shaped right-angle with a 5 cm long horizontal segment parallel to the flow, close to the flume bottom, on the downstream side of the vertical segment. Plants were fixed to the downstream end of the horizontal part of the rod.
|
Roots and other below-ground parts of the plants were removed before measurements to avoid additional drag.
During drag measurements, flow velocity was measured in the water flume at a water depth of 40% of total depth (from the bottom), with the propeller used in the field, placed approximately 1 m upstream of the drag measuring device to avoid flow disturbance.
Flow velocity and drag were recorded simultaneously over 30 s. Drag was calculated as the mean of 300 values (10 values s–1).
For each plant, drag was measured for at least 10 different flow velocities (maximum=13) over the range 0.1–1.15 m s–1. Under each of these velocity conditions, the projections of the height (y) of the plant above the horizontal plane of the anchoring point and of the maximal length of the plant (x) downstream from the anchoring point were measured. The bending angle of the plant was calculated from these measurements: 
=tan–1 (yxx–1) (Sand-Jensen, 2003).
During drag measurements, water depth in the flume was maintained at approximately 18.0 cm (18.0±0.5 cm and 18.2±0.5 cm, mean ±SD, for B. erecta and M. aquatica, respectively, NS, P <0.001, t-test).
Plant drag was calculated as the difference between the (plant+device) drag and the drag of the device at the same velocity (see rationale in Sagnes et al., 2000). The drag of the device alone (base or rod) was measured in a comparable velocity range and fitted with polynomial curves to determine the drag values corresponding to each velocity condition used with plants.
The hydrodynamic performance of the plants was assessed through (i) quantitative variables describing relative drag and plant reconfiguration, and (ii) estimation of the absolute overall forces exerted on each plant for the five velocity conditions corresponding to the five patches.
Quantitative measures of hydrodynamic abilities of plants: drag coefficient and E-value:
Drag coefficient (Cd) represents drag relative to flow velocity and leaf area exposed to flow. It is usually considered as a dimensionless standard variable allowing comparison of drag experienced by objects of different shapes (Vogel, 1984). Drag coefficients were calculated using the standard equation: Cd=2D/(
SU2), where D is drag (N), is the density of water (kg m–3), S is the total leaf area (m2), and U the flow velocity (m s–1). Cd was then plotted against flow velocity. Under similar flow conditions, Cd is lower for more hydrodynamically adapted shapes and typically decreases following an exponential model with increasing flow velocity (Vogel, 1984, 1994). The threshold value of Cd reached by plants at the highest velocities was used as a measure of the ability of a plant to withstand high current velocity. Because flow velocity regulation in the flume is inaccurate for high velocities, a model of the form Cd=f(U)=aUb (a and b are constants) (Bell, 1999) was used for calculating Cd for the upper velocity limit of the water flume (i.e. 1.15 m s–1). Cd (1.15 m s–1) was called the minimum drag coefficient (Cdmin) and was used for comparing the hydrodynamic abilities of individuals sampled in the different flow patches.
For B. erecta, Cd always decreased as flow velocity increased, and the curve shape was consistent with theoretical curves (i.e. a decrease of Cd values with flow velocity). Consequently, all points were included in the model. By contrast, for M. aquatica, with increasing experimental velocities, some curves exhibited an initial increase of Cd up to a maximum value (reached for flow velocity around 0.3 m s–1), followed by the expected decreasing trend. This shape for the Cd=f (velocity) curves has already been observed by Hawes and Smith (1995), and could be due to spatial reconfiguration of plant foliage at low velocities (Vogel, 1994). To avoid complex modelling of the initial rise of the curves that probably does not play any role in the Cdmin value, the decreasing part of the curves only was used for Cdmin estimation. To get homogeneous modelling for all individuals of M. aquatica, all curves were treated in the same way: the measurements corresponding to flow velocities below 0.35 m s–1 were excluded from the model. To test the validity of the Cdmin estimation (i.e. the reality of a threshold value of Cd under the highest velocity conditions used here), for each individual the difference between the Cd values measured at the two highest experimental velocities were calculated. As this difference was, on average, below 5% (5.00% and 4.72% on average for B. erecta and M. aquatica, respectively), it was considered that the threshold value of Cd was almost attained and that the Cdmin (estimated for a flow velocity of 1.15 m s–1) was a reliable estimator of the Cd value reached by each plant at the highest velocity obtained in the water flume.
The E-value is a measurement of plant reconfiguration when water velocity increases (Vogel, 1984, 1989). It indicates how drag varies with flow velocity, but is independent of the absolute drag value. The lower the E value, the more the plant reconfigures. The E-value was calculated as the slope of a double logarithmic plot of speed-specific drag (D/U2) against speed (U), for regions of curves without inflection points (following Vogel, 1984). Note that E is equal to exponent b in the equation Cd=aUb applied to these regions of the curves.
Extrapolated plant drag along the velocity gradient:
The drag values that a given individual would have if placed in the different patches can be extrapolated from the experimental drag measurements. For each individual, plots of drag values against velocity were fitted by second order polynomial regression. Fitted curves were next used to calculate, for each plant, the drag it would face if placed in the median velocity of each of the five flow-patches (cf Table 1). Such an estimation should allow the hydrodynamic (dis)advantage of the morphology found in a given patch to be compared to those of the alternative morphologies.
Morphometry
The morphological traits measured on each plant were as follows: (i) plant height (m), defined for M. aquatica as the maximum length of the shoot and for B. erecta, as the height of the plant above ground; (ii) number of branches for M. aquatica and of interconnected stolons for B. erecta; (iii) plant mass (g): plants were divided into roots, stems, leaves for M. aquatica and into roots, stems, petioles, and leaflets for B. erecta. The different parts were weighed to obtain fresh and dry mass (measured after 48 h at 85 °C). (iv) Leaf area (cm2): leaves were scanned (150 dpi, Epson Expression 1680 scanner) and the images were analysed with WinFolia 2001 image analysis software (Regent Instrument Inc., Quebec, Canada). These values were used to calculate two sets of traits.
The first set (five traits) was used to assess the morphological determinants of Cdmin and E-values. These traits were selected for their potential relevance in explaining plant hydrodynamics.
(i) Plant height, total leaf area, and above-ground biomass were highly correlated (for B. erecta, r2=0.59, P <0.001, and r2=0.84, P <0.001 for correlations between above-ground biomass, plant height, and total leaf area, respectively; for M. aquatica, r2=0.55, P <0.001, and r2=0.86, P <0.001 for the same correlations). Consequently, above-ground biomass (stem and leaves for M. aquatica and petioles and leaflets for B. erecta) was used as a measurement of plant size and energetic investment in tissue production (Dudgeon and Johnson, 1992; Schutten and Davy, 2000).
(ii) Water content of ‘axes’ (i.e. stem for M. aquatica and petiole for B. erecta) and ‘photosynthetic surfaces’ (i.e. leaves for M. aquatica and leaflets for B. erecta) were measured for analogous structures that play the same functional role, rather than homologous structures less relevant for contrasting growth forms (rosette with reduced, buried stems for B. erecta and large, erect stem for M. aquatica). Water content (=1–(dry mass/fresh mass)) should correlate with the proportion of different types of tissues and tends to be negatively correlated with density (Garnier and Laurent, 1994; Pyankov et al., 1999).
(iii) Specific leaf area, SLA=leaf area/leaf dry mass (cm2 g–1), correlates with leaf thickness (Garnier and Laurent, 1994; Pyankov et al., 1999) and was used to assess anatomical variation unrelated to water content.
(iv) The bending angle (°) of the plant in flow is an important determinant of plant drag (Sand-Jensen, 2003). It represents the way the plant reconfigures and bends under increasing flow velocity and can be viewed as a synthetic variable expressing flexibility and bending capacity. Two different bending angles were used to explain Cdmin and E-value. As Cdmin corresponds to the lowest Cd under experimental flow conditions, the lowest angle (min) reached by the plant (i.e. highest bending) was used as an explanatory variable of Cdmin. The E-value measures the change of drag with flow velocity. Consequently, the difference between bending angles at the lowest and highest flow velocities (
) was used as an explanatory variable of the E-value. A mixed stepwise multiple regression between bending angles (min and ) and the four other morphological traits was performed to check that these angles were not redundant when compared with other traits. Morphological traits explained 31.2% (above-ground biomass) and 27.9% (SLA and above-ground biomass) of the variability of min for B. erecta and M. aquatica, respectively. No morphological trait was significantly correlated with , neither for B. erecta nor for M. aquatica.
The second set of traits (three traits) was used to compare the fitness of individuals growing in the different flow-patches.
(i) Total dry mass (g) of the ramet (Liao et al., 2003; Pilon and Santamaria, 2002).
(ii) Clonal multiplication: as growth forms of both species differ, the number of stolons connected to the main ramet was used for B. erecta (stoloniferous growth) and the number of terminal buds of the ramet (i.e. number of branches potentially able to become an independent ramet) was used for M. aquatica.
(iii) Dry mass allocation to storage organs (root and stems) (Storage Organs Ratio=dry mass of storage organs/total dry mass) (Cornelissen et al., 2003).
Finally, as anchorage strength affects the ability of the plant to resist the flow, but was considered as unrelated to the hydrodynamic ability of the above-ground part of the plant, it was felt necessary to measure an anchorage trait as well. Above-ground fresh mass/total fresh mass (above-ground ratio) measures the plant investment in its above-ground biomass, directly submitted to flow stress, compared with total plant biomass, including below-ground biomass participating in plant anchorage.
Statistical analysis
Within-species variations of morphological traits and hydrodynamic parameters along the gradient were assessed through a one-way ANOVA, conducted after tests of normality and homoscedasticity (Kolmogorov-Smirnov and Bartlett's tests) and where necessary, log-transformation of data (Sokal and Rohlf, 1995). The non-parametric Kruskal–Wallis test was used when data did not meet the assumption of normality or equality of variance after being transformed. Spearman's test was used to test the variation tendency of the different variables along the flow velocity gradient. A sequential Bonferroni correction was applied for multiple tests to control a type I error rate (Sokal and Rohlf, 1995).
To evaluate the causal relationship between morphology and hydrodynamic performance, the first set of morphological traits was used in a mixed stepwise multiple regression on both Cdmin and E-value. The criterion for entry of a trait and for keeping it in the final model was P <0.05.
R-Software (R development Core Team 2003) was used for all statistical calculations.
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Morphological variations along the flow velocity gradient
All morphological traits differed significantly between the five flow-patches, except
(for both species) and water content of axes and photosynthetic surface for M. aquatica (Tables 2, 3). The above-ground biomass (i.e. size) of B. erecta, decreased significantly and min increased along the gradient (Spearman test, P <0.01 and P <0.001, respectively). In M. aquatica, SLA decreased significantly and above-ground biomass increased (Spearman test, P <0.05 and P <0.001, respectively).
|
|
Concerning fitness-related traits, total dry mass increased by a factor of 2.8 between flow-patches 1 and 5 for M. aquatica (P <0.01, Spearman test) (Table 3). The other traits did not differ significantly between patches (number of terminal buds) or differed between patches but without significant tendency (storage organ ratio, Spearman test, P=0.07, Fig. 3). For B. erecta, fitness-related traits varied inversely (Table 2), since total dry mass decreased along the gradient by a factor of 2.8, while the number of stolons and the storage organ ratio increased (Spearman test, P <0.001, P <0.01, P <0.001 for these three traits, respectively).
|
The above-ground ratio differed significantly between flow-patches for both species (Tables 2, 3), but with opposite variation trends along the gradient (negative, P <0.001 for B. erecta and positive, P <0.001 for M. aquatica, Spearman test).
Hydrodynamic abilities
Drag coefficients and E-values:
The Cdmin of B. erecta differed significantly between patches (P <0.01, ANOVA) and consistently increased as the average velocity in the corresponding flow-patches increased (Spearman test, P <0.001, Fig. 4), indicating that plants experiencing high current speed had higher drag relative to leaf area under high velocity conditions. The Cdmin of M. aquatica did not differ significantly between the five flow-patches of the gradient (P=0.1, ANOVA), even though it decreased significantly between flow-patches 2 and 5 (Spearman test, P <0.05, Fig. 4).
|
E-values did not differ significantly along the gradient for B. erecta (P=0.3, ANOVA, Fig. 4). They differed significantly for M. aquatica (P <0.05, ANOVA), but without any apparent trend (Fig. 4).
Extrapolated plant drag along the velocity gradient:
For both species, individual plant drag consistently increased with increasing flow velocity (Fig. 5), in accordance with theoretical expectations that higher flow velocity induces higher drag.
|
For both species (except the null velocity patch), the drag of plants originating from different flow-patches differed significantly under the flow velocity conditions of a given patch (P <0.001, ANOVA) (Fig. 5). Plant drag rankings, according to the patch where they originated are preserved for the four non-null velocities of the gradient, but varied in the opposite way for the two species. For a given flow velocity (except 0), plant drag is significantly negatively correlated with the flow-patch of origin for B. erecta (P <0.01 for all non-null flow velocities, Spearman test): plants from high velocity patches have at least half the drag values of plants from low velocity patches (Fig. 5). For M. aquatica, at a given flow velocity (except 0), plant drag is significantly positively correlated with the flow-patch of origin: plants of more exposed flow-patches have higher drag values than plants of less exposed flow-patches (P <0.001 for all non-null flow velocities, Spearman test) (Fig. 5).
Relationships between morphology and hydrodynamics: morphological determinants of Cdmin and E-values
For both species, the minimal bending angle is the only significant trait explaining Cdmin. This morphological trait explained 49.1% of the variability of Cdmin for B. erecta (P <0.001) and 14% for M. aquatica (P <0.05).
For both species, no morphological traits correlated with the E-value.
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Morphological and hydrodynamic differences along the flow-velocity gradient
Both species exhibited significant morphological differences along the flow velocity gradient. The sharp size reduction of B. erecta with increasing flow velocities is a very frequent response for individuals of a given species exposed to mechanical stresses (Jaffe, 1973
; Gaylord et al., 1994; Idestam-Almquist and Kautsky, 1995; Blanchette, 1997). The size increase of M. aquatica constitutes a rarely observed response for higher plants (Jaffe, 1973; Coops and Van der Velde, 1996).
Increased allocation to below-ground biomass observed for B. erecta has been demonstrated to increase anchorage strength (Crook and Ennos, 1996; Goodman and Ennos, 1996). Surprisingly, biomass root allocation decreased along the gradient for M. aquatica, suggesting lower anchorage strength for high flow velocity and therefore an increased uprooting risk. Such a strategy may increase the dispersal ability of this species in a high flow habitat.
For both species, the only trait explaining Cdmin is the minimal bending angle of the plant. This is consistent with previous studies demonstrating that flexible organisms have lower drag because they bend and reconfigure into more streamlined shapes (Koehl, 1977; Vogel, 1994, Usherwood et al., 1997). Bending angle depends not only on flexibility but also on the force exerted on the plant, which causes bending (Sand-Jensen, 2003). Bending places the plant closer to the substrate in a zone of lower flow velocity, which decreases plant drag (Koehl, 1977; Vogel, 1994; Sand-Jensen, 2003).
Unexpectedly, morphological traits were not correlated with Cdmin and E-values (Schutten and Davy, 2000). The bending angle only explained less than half of the Cdmin variability. Carrington (1990) previously demonstrated that Cd mainly correlated with the algal surface exposed to flow and not to morphology per se. However, the anatomical complexity of higher plants suggests that tissues characteristics (proportion and deformation ability) should be considered for an accurate description of plant biomechanics (Patterson, 1992; Usherwood et al., 1997).
For B. erecta, minimization of plant drag results from a size reduction, without particular shape streamlining (higher Cdmin) probably because of the lower bending ability of small plants compared with larger ones. However, the sharp size-reduction leads to a reduction in overall drag forces on plants and places them partly within the boundary layer where flow velocity is reduced (Koehl, 1977, 1982; Sheath and Hambrook, 1988). This flow stress ‘avoiding strategy’ has already been described between species (animals, algae or macrophytes; Koehl, 1977; Denny et al., 1985; Sheath and Hambrook, 1988), but also within species, with dwarfing of more exposed individuals (Idestam-Almquist and Kautsky, 1995; Blanchette, 1997). The apparent decrease in plant performance (drag increase and decrease of allocation to roots) observed for M. aquatica is an uncommon response to mechanical constraint. Taller plants are more likely to be damaged under high flow conditions (as demonstrated for macroalgae, Gaylord et al., 1994; Blanchette, 1997). However, the high stem breaking force (>8.8 N by pulling along the stem, preliminary results) probably preserves M. aquatica from breaking in high flow velocity patches (where it faces 0.3 N only, Fig. 5). Anchorage allocation decreased along the gradient suggesting an increased uprooting risk and subsequent increase of plant dispersal. However, a very high density of strongly anchored runners has been observed for individuals colonizing high velocity patches, suggesting a higher number of anchorage points relative to the number of erect ramets within the same individual. Changes in anchorage efficiency could be quantified more accurately through calculating, for each plant, the ratio of the uprooting force to the drag force (Crook and Ennos, 1996; Pratt and Johnson, 2002).
Adaptive value of morphological changes and maintenance strategies of both species
Size-limitation of the above-ground part of B. erecta could at first be considered as an important reduction in plant fitness. However, the close relationship between size and drag makes it necessary to consider other fitness-related traits. Plant investment in clonal reproduction and storage increased with current velocity (Table 2), suggesting that plants would maintain their fitness, at least in part, through a spatial biomass reallocation at the whole individual level, when velocity increases. Biomass did indeed appear reorganized, from a vertical organization in low flow-velocity patches (one tall ramet), to a horizontal organization with the biomass concentrated close to the substrate (shorter individual avoiding high flow velocities, divided into many interconnected ramets, with higher storage) in high velocity patches. Horizontal reorganization of biomass would, if this hypothesis is verified, be a way of partly reducing the detrimental effect of a reduction in ramet size.
Trends observed for M. aquatica (drag increase, decrease of root biomass) probably do not affect its survival ability, because of its very strong stem resistance and the probable underestimation of anchorage strength. The size increase combined with the decrease of drag coefficient (for high velocities) could indicate an increase of plant performance and fitness. However, the size increase could result from indirect effects: (i) increased current velocity could reduce boundary layer thickness at the plant surface (Westlake, 1967; Madsen and Sondergaard, 1983), thus favouring plant growth; (ii) under high flow velocities, foliated shoots of M. aquatica are brought closer to the substrate, where flow stress is lower, thus favouring their growth, and the growth of new anchorage points along the ramet; (iii) reconfiguration of leaves occurred below 20 cm s–1 in the flume (S Puijalon, personal observation). When a plant reconfigures, leaves stack up on the stem, inducing self-shading, and probably reducing their photosynthetic efficiency (as only the lower face of leaves remains exposed to light) (Koehl and Alberte, 1988). For patches 2 to 5, light stress could, consequently, also promote stem elongation (Pilon and Santamaria, 2002). Finally, the fitness-related traits that were measured did not permit the conclusion that the morphological changes occurring along the gradient, even when they are not directed towards greater hydrodynamic performance, decrease plant fitness.
This study has emphasized the importance of size in mechanically stressful habitats, with both species exhibiting completely opposed responses. Changes in terms of morphology or size, exhibited by a given species exposed to flow, are probably restricted by: (i) developmental constraints linked to plant morphology and (ii) trade-offs between major plant functions (e.g. light capture, nutrient acquisition), which require the efficiency of the organs that carry out these functions. The response in terms of trait variations and hydrodynamic performance observed for M. aquatica could be due to the necessary trade-off between a morphology that maximizes light interception and one minimizing drag (Koehl and Alberte, 1988; Vogel, 1989). For B. erecta, rosette growth form does not allow the plant to adapt through stem morphological variation (e.g. stem length or flexibility), but enables the plant to produce a constant leaf number, whatever its size. On the other hand, an erect stem (in the case of M. aquatica) probably offers better opportunities for the reorganization of leaves along the axis.
|
Acknowledgements |
|---|
We thank R Morel and J-Y Champagne from the Fluid Mechanics and Acoustics Laboratory of INSA-Lyon (Institut National des Sciences Appliquées) for providing the water flume. N Lamouroux and B Statzner are gratefully acknowledged for previous discussions on methodological measurements and analyses of plant hydrodynamics and P Joly for valuable comments and suggestions on a previous version of the paper. We thank D Reynaud and E Malet for technical assistance. This study was partly funded by the ‘ACI Ecologie Quantitative’ of the MENRT (Ministère de l'Education Nationale, de la Recherche et de la Technologie), and was carried out under the aegis of the long-term ecological research programme on the Rhône River Basin (Zone Atelier Bassin du Rhône).
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Armstrong SL. 1989. The behavior in flow of the morphologically variable seaweed Hedophyllum sessile (C. Ag.) Setchell. Hydrobiologia 183, 115–122.[CrossRef]
Arnold SJ. 1983. Morphology, performance and fitness. American Zoologist 23, 347–361.
Barrat-Segretain MH, Elger A, Sagnes P, Puijalon S. 2002. Comparison of three life-history traits of invasive Elodea canadensis Michx. and Elodea nuttallii (Planch.) H. St. John. Aquatic Botany 74, 299–313.[CrossRef]
Bell EC. 1999. Applying flow tank measurements to the surf zone: predicting dislodgment of the Gigartinaceae. Phycological Research 47, 159–166.
Biehle G, Speck T, Spatz HC. 1998. Hydrodynamics and biomechanics of the submerged water moss Fontinalis antipyretica: a comparison of specimens from habitats with different flow velocities. Botanica Acta 111, 42–50.[ISI]
Blanchette CA. 1997. Size and survival of intertidal plants in response to wave action: a case study with Fucus gardneri. Ecology 78, 1563–1578.[CrossRef]
Boeger MRT, Poulson ME. 2003. Morphological adaptations and photosynthetic rates of amphibious Veronica anagallis-aquatica L. (Scrophulariaceae) under different flow regimes. Aquatic Botany 75, 123–135.[CrossRef][ISI]
Carbiener R, Trémolières M, Mercier JL, Ortscheit A. 1990. Aquatic macrophyte communities as bioindicators of eutrophication in calcareous oligosaprobe stream waters (Upper Rhine plain, Alsace). Vegetatio 86, 71–88.[CrossRef][ISI]
Carrington E. 1990. Drag and dislodgement of an intertidal macroalga: consequences of morphological variation in Mastocarpus papillatus kützing. Journal of Experimental Marine Biology and Ecology 139, 185–200.[CrossRef]
Coops H, Van der Velde G. 1996. Effects of waves on helophyte stands: mechanical characteristics of stems of Phragmites australis and Scirpus lacustris. Aquatic Botany 53, 175–185.[CrossRef]
Cornelissen JHC, Lavorel S, Garnier E, et al. 2003. A handbook of protocols for standardized and easy measurement of plant functional traits worldwide. Australian Journal of Botany 51, 335–380.[CrossRef]
Crook MJ, Ennos AR. 1996. Mechanical differences between free-standing and supported wheat plants Triticum aestivum L. Annals of Botany 77, 197–202.
Debat V, David P. 2001. Mapping phenotypes: canalization, plasticity and developmental stability. Trends in Ecology and Evolution 16, 555–561.[CrossRef]
Denny MW, Daniel TL, Koehl MAR. 1985. Mechanical limits to size in wave-swept organisms. Ecological Monographs 55, 69–102.[CrossRef]
Dingman SL. 1984. Fluvial hydrology. New York: WH Freeman and Company.
Dudgeon SR, Johnson AS. 1992. Thick versus thin: thallus morphology and tissue mechanics influence differential drag and dislodgement of co-dominant seaweeds. Journal of Experimental Marine Biology and Ecology 165, 23–43.[CrossRef]
Garnier E, Laurent G. 1994. Leaf anatomy, specific mass and water content in congeneric annual and perennial grass species. New Phytologist 128, 725–736.[CrossRef][ISI]
Gaylord B, Blanchette CA, Denny MW. 1994. Mechanical consequences of size in wave-swept algae. Ecological Monographs 64, 287–313.[CrossRef]
Goodman AM, Ennos AR. 1996. A comparative study of the response of the roots and shoots of sunflower and maize to mechanical stimulation. Journal of Experimental Botany 47, 1499–1507.[ISI]
Hawes ID, Smith RA. 1995. Effect of current velocity on the detachment of thalli of Ulva lactuca (Charophyta) in a New Zealand estuary. Journal of Phycology 31, 875–880.[CrossRef][ISI]
Idestam-Almquist J, Kautsky L. 1995. Plastic responses in morphology of Potamogeton pectinatus L. to sediment and above-sediment conditions at two sites in the northern Baltic proper. Aquatic Botany 52, 205–216.[CrossRef]
Jaffe MJ. 1973. Thigmomorphogenesis: the response of plant growth and development to mechanical stimulation. With special reference to Bryonia dioica. Planta 114, 143–157.[CrossRef][ISI]
Koehl MAR. 1977. Effects of sea anemones on the flow forces they encounter. Journal of Experimental Biology 69, 87–105.
Koehl MAR. 1982. The interaction of moving water and sessile organisms. Scientific American 247, 110–120.[ISI][Medline]
Koehl MAR. 1996. When does morphology matter? Annual Review of Ecology and Systematics 27, 501–542.[CrossRef][ISI]
Koehl MAR, Alberte RS. 1988. Flow, flapping, and photosynthesis of Nereocystis luetkeana: a functional comparison of undulate and flat blade morphologies. Marine Biology 99, 435–444.[CrossRef]
Liao M, Yu F, Song M, Zhang S, Zhang J, Dong M. 2003. Plasticity in R/S ratio, morphology and fitness-related traits in response to reciprocal patchiness of light and nutrients in the stoloniferous herb, Glechoma longituba L. Acta Oecologica 24, 231–239.[CrossRef]
Madsen JD, Chambers PA, James WF, Koch EW, Westlake DF. 2001. The interaction between water movement, sediment dynamics and submersed macrophytes. Hydrobiologia 444, 71–84.[CrossRef]
Madsen TV, Sondergaard M. 1983. The effects of current velocity on the photosynthesis of Callitriche stagnalis Scop. Aquatic Botany 15, 187–193.[CrossRef]
Patterson MR. 1992. Role of mechanical loading in growth of sunflower (Helianthus annuus) seedlings. Journal of Experimental Botany 43, 933–939.
Pilon J, Santamaria L. 2002. Clonal variation in morphological and physiological responses to irradiance and photoperiod for the aquatic angiosperm Potamogeton pectinatus. Journal of Ecolgy 90, 859–870.[CrossRef]
Pratt MC, Johnson AS. 2002. Strength, drag, and dislodgment of two competing intertidal algae from two wave exposures and four seasons. Journal of Experimental Marine Biology and Ecology 272, 71–101.[CrossRef]
Puijalon S, Bornette G. 2004. Morphological variation of two taxonomically distant plant species along a natural flow velocity gradient. New Phytologist 163, 651–660.[CrossRef][ISI]
Pyankov VI, Kondratchuk AV, Shipley B. 1999. Leaf structure and specific leaf mass: the alpine desert plants of the Eastern Pamirs, Tadjikistan. New Phytologist 143, 131–142.[CrossRef][ISI]
Ricklefs RE, Miles DB. 1994. Ecological and evolutionary inferences from morphology: an ecological perspective. In: Wainwright PC, Reilly SM, eds. Ecological morphology: integrative organismal biology. Chicago: University of Chicago Press, 13–41.
Sagnes P, Champagne J-Y, Morel R. 2000. Shifts in drag and swimming potential during grayling ontogenesis: relations with habitat use. Journal of Fish Biology 57, 52–68.
Sand-Jensen K. 2003. Drag and reconfiguration of freshwater macrophytes. Freshwater Biology 48, 271–283.[CrossRef]
Santamaria L, Figuerola J, Pilon JJ, Mjelde M, Green AJ, de Boer T, King RA, Gornall RJ. 2003. Plant performance across latitude: the role of plasticity and local adaptation in an aquatic plant. Ecology 84, 2454–2461.[CrossRef][ISI]
Schutten J, Davy AJ. 2000. Predicting the hydraulic forces on submerged macrophytes from current velocity, biomass and morphology. Oecologia (Berl.) 123, 445–452.[CrossRef]
Sheath RG, Hambrook JA. 1988. Mechanical adaptations to flow in freshwater red algae. Journal of Phycology 24, 107–111.[ISI]
Sokal RR, Rohlf FJ. 1995. Biometry, 3rd edn. New York: WH Freeman and Company.
Statzner B, Arens MF, Champagne JY, Morel R. 1999. Silk-producing stream insects and gravel erosion: significant biological effects on critical shear stress. Water Resources Research 35, 3495–3506.[CrossRef][ISI]
Sultan SE. 1987. Evolutionary implications of phenotypic plasticity in plants. Evolutionary Biology 21, 127–178.[ISI]
Sultan SE. 2000. Phenotypic plasticity for plant development, function and life-history. Trends in Plant Sciences 5, 537–542.
Telewski FW, Jaffe MJ. 1986. Thigmomorphogenesis: field and laboratory studies of Abies fraseri in response to wind or mechanical perturbation. Physiologia Plantarum 66, 211–218.[CrossRef][Medline]
Usherwood JR, Ennos AR, Ball DJ. 1997. Mechanical adaptations in terrestrial and aquatic buttercups to their respective environments. Journal of Experimental Botany 48, 1469–1475.[ISI]
Vogel S. 1984. Drag and flexibility in sessile organisms. American Zoologist 24, 37–44.
Vogel S. 1989. Drag and reconfiguration of broad leaves in high winds. Journal of Experimental Botany 40, 941–948.
Vogel S. 1994. Life in moving fluids: the physical biology of flow, 2nd edn. Princeton NJ: Princeton University Press.
Wainwright PC. 1994. Functional morphology as a tool in ecological research. In: Wainwright PC, Reilly SM, eds. Ecological morphology: integrative organismal biology. Chicago: University of Chicago Press, 42–59.
Westlake DF. 1967. Some effects of low-velocity currents on the metabolism of aquatic macrophytes. Journal of Experimental Botany 55, 187–205.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  S. Puijalon, J.-P. Lena, and G. Bornette Interactive Effects of Nutrient and Mechanical Stresses on Plant Morphology Ann. Bot., November 1, 2007; 100(6): 1297 - 1305. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. W. Telewski A unified hypothesis of mechanoperception in plants Am. J. Botany, October 1, 2006; 93(10): 1466 - 1476. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Puijalon and G. Bornette Phenotypic plasticity and mechanical stress: biomass partitioning and clonal growth of an aquatic plant species Am. J. Botany, August 1, 2006; 93(8): 1090 - 1099. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||