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Ecology |
UMR CNRS 5023, "Ecology of Fluvial Hydrosystems," Université Claude Bernard Lyon 1, 43 Boulevard du 11 novembre 1918, F-69622 Villeurbanne Cedex, France
Received for publication October 20, 2005. Accepted for publication May 18, 2006.
ABSTRACT
Mechanical stresses from wind, current or wave action can strongly affect plant growth and survival. Survival and distribution of species often depend on the plant's capacity to adapt to such stresses, particularly when amplified by climatic variations. Few studies have dealt with plastic adjustments in response to mechanical stress compared to resource stress. We hypothesized that mechanical stress should favor plastic adjustments that result in increased biomass production in zones protected from the stress and that altered growth patterns should be reversible after mechanical stress removal. Here we measured plastic adjustments in morphological traits and clonal architecture for an aquatic clonal species (Berula erecta) under two contrasting mechanical stresses in the field—standing vs. running water. Reversion of the morphological changes was then assessed using transplants in standing water. In the case of mechanical stress, size reduction, biomass reallocation within clones (higher allocations to clonal growth and to belowground organs), and a more compact growth form (reduced spacer lengths) contributed to reducing the damage risk. The removal of mechanical stress induced compensatory growth, probably linked to the production of low density tissues. However, most patterns of dry mass partitioning induced by current stress were not reversed after stress removal.
Key Words: Berula erecta • clonal plant • clone architecture • hydraulic stress • morphology • submerged aquatic vegetation • stress recovery
Many plant species exposed to environmental stresses display plastic responses in their developmental, morphological, physiological, anatomical, or reproductive traits that can support functional adjustments, possibly compensating for the detrimental effect of stress (e.g., reviewed by Sultan, 2000
, 2003
). Phenotypic plasticity elicited by stresses has been widely studied, but mainly in regard to resource stresses (e.g., light, nutrients, water availability, or inorganic carbon). This body of work has resulted in several theories or models that explain plastic responses to those stresses (e.g., optimal resource use or optimal foraging, Chapin, 1991
; Gleeson and Tilman, 1992
; Hutchings and de Kroon, 1994
; Hutchings and John, 2004
). However, under natural conditions, plants are also subjected to stresses that do not directly limit resource availability (e.g., flooding, mineral toxicity). Plant responses to those stresses cannot be simply predicted by models linked to resource use (Chapin, 1991
). Mechanical stresses from wind, current or wave action affect plants mechanically and act on the plant's spatial organization rather than directly on resource acquisition (e.g., many plants escape from the stress through a prostrate growth form). Such stresses are widely encountered by plants and are ecologically very important because they act on plant growth and survival, diaspore survival or recruitment, and species distribution (Foote and Kadlec, 1988
; Ennos, 1997
; Hudon et al., 2000
; Gantes and Caro, 2001
). Moreover, these stresses could become more critical for communities and ecosystems in the future, due to changes in natural regimes (e.g., flow regimes) linked to climate change (Lytle and Poff, 2003
). In this framework, in order to predict future distribution of a species, we need to elucidate how mechanical stresses act on plants in order to determine (1) how far models proposed for resource stresses could apply to other kinds of stress and (2) how plants tolerate and adapt to those stresses.
Mechanical stress results mainly from forces exerted directly on plants (drag, lift, and acceleration reaction), that tend to break and dislodge them (Vogel, 1994
; Schutten et al., 2005
). Permanent exposure to mechanical stress also leads to altered morphologies in plants, involving many morphological, architectural, and allocation features of individual ramets (Strand and Weisner, 2001
; Jaffe et al., 2002
; Boeger and Poulson, 2003
). Permanently exposed plants are usually reduced in size (height, leaf area, biomass, but also petiole length or leaf size; see Biddington and Dearman, 1985
; Niklas, 1998
; Henry and Thomas, 2002
; Boeger and Poulson, 2003
; Hik et al., 2003
), generally resulting in a reduced drag (Puijalon et al., 2005
). The aero- and hydrodynamic forces exerted on plants exposed to moving fluids are indeed proportional to plant size (Vogel, 1994
). Moreover, increases in root allocation and stem diameter are often observed, possibly resulting in higher uprooting and breaking strengths (Niklas, 1998
; Retuerto and Woodward, 2001
; Henry and Thomas, 2002
; Puijalon and Bornette, 2004
). A lower allocation to sexual reproduction or delayed flowering can also be observed (Niklas, 1998
; Retuerto and Woodward, 2001
; Hodges et al., 2004
). Little information exists concerning the way clonal growth is affected by mechanical stress (Idestam-Almquist and Kautsky, 1995
), even if it could be hypothesized to affect clonal pattern and biomass allocation within clones (a clone refers here to the whole set of interconnected ramets produced by a single plant). Indeed, any reallocation of biomass to more protected locations (e.g., the production of greater biomass belowground or of numerous small ramets growing in areas with a lower risk of damage instead of one tall individual) should be favored in mechanically stressful conditions.
In this framework, the aim of the present paper was to measure patterns of clonal growth and biomass allocation within natural populations of an aquatic plant species, Berula erecta (Hudson) Coville, in response to hydraulic stress (permanent exposure to current). In a second step, we aimed to determine whether the patterns observed under stressful conditions are reversed after the stress is removed.
We explicitly tested two hypotheses. (1) Under water current stress situations, the architectural, morphological, and clonal pattern should result in (a) a morphological organisation that tends to locate plant biomass in protected zones (e.g., through the production of many small ramets close to the substrate or through higher allocation to the belowground biomass), (b) decreased hydraulic roughness at the clone level (e.g., through decreased ramet size and leaf number), and (c) a tendency to escape from unfavorable conditions (e.g., through increased spacer length). (2) If these altered patterns of biomass allocation and clonal growth result from phenotypic plasticity, they should be, at least partly, reversible after removal of the stressing current.
MATERIALS AND METHODS
The experiments were conducted on the clonal aquatic plant species Berula erecta (Hudson) Coville. Differences in clonal growth and biomass allocation within the clones were investigated by measuring the traits of individuals sampled in the field under two different hydraulic conditions (standing vs. running water). For the study of the growth patterns of plants following removal of the current, individuals originating from the two sampling patches were transplanted to a favorable standing habitat for 4 months.
Species and study sites
Berula erecta (Apiaceae) is a perennial stoloniferous species, consisting of a rosette of petiolated-dissected leaves. It colonizes calcareous nutrient-poor flowing habitats.
Plants were collected from a groundwater-supplied channel of the Rhône River, including riffles, with a permanent, relatively steady flow. Two patches (1 m2) were selected for plant sampling. The first patch was defined as a zone of zero velocity (standing patch), and the other one as a patch where the highest flow velocity in the riffle was measured (running patch).
Flow velocity
The channel drains water from the river, and the channel discharge is related to the river discharge. To describe flow velocity encountered by plants, taking into account all discharge variations, we established a regression between the daily Rhône river discharge and flow velocity in the patches. We then used this regression to predict flow velocity encountered by plants on the patches during the whole experimental period. To establish the regression, four flow velocities were measured at random at each patch while avoiding hydraulic shelters (big cobbles, tall plants), on 17 dates with contrasting river discharges. Flow velocity was measured with a propeller (C2 current meter, OTT Messtechnik GmbH. KG, Kempten, Germany) at a water depth 40% above the substrate, which gives a good estimate of average flow velocity in the water column (Dingman, 1984
).
Flow velocity in patches was predicted for two periods: (1) 4 months before transplantation, in order to describe the constraints encountered by plants collected in situ before the beginning of the experiment; and (2) 4 months after transplantation, to measure flow velocity encountered by plants still in their habitats during the experiment. Average flow velocity was 0 and 0.52 ± 0.05 m · s–1 during the first period and 0 and 0.53 ± 0.04 m · s–1 during the period of transplantation, for standing and running patches, respectively.
Substrate (coarse grain size: gravels, cobbles) did not differ between patches. Water depth was 0.10 and 0.70 m on average for running and standing patches, respectively.
Transplantation experiment
Individuals originating from standing and running patches were transplanted to a common site characterised by stress-free growth conditions (i.e., zero velocity and protected from any human or animal disturbance). The transplantation site was located in a private protected zone, in a small manmade experimental canal.
All the transplantation was carried out within 2 days in April 2002; plants were therefore held for no more than 24 h after collection prior to transplantation.
Twenty-five and 30 submerged individual plants (ramets) were collected from distinct clones in standing and running patches, respectively. We defined a ramet as a single rooted rosette. To standardize transplants, all horizontal stolons growing from the main ramet were removed. Ramets were planted in plastic containers (18 x 24 x 10 cm) filled to the brim with river sand (0–5 mm). Five or six ramets were planted in each container, depending on initial plant size. The containers were randomly positioned within the transplantation site. The water depth was about 40 cm above the top of the containers. Plants living in the reference patches were referred to as "residents," as opposed to those that were transplanted ("transplants"). Plants transplanted from the standing patch were used as controls for the transplantation experiment. This experimental design allowed the following comparisons to be made: residents of standing patch vs. residents of running patch, effect of hydraulic stress; resident of standing patch vs. transplants of standing patch, effect of transplantation (control); resident of running patch vs. transplants of running patch, effect of transplantation and stress removal; transplants of standing patch vs. transplants of running patch, expected morphological convergence (i.e., similar trait values at the end of the experiment).
Harvest and morphometry
At the end of the experiment (18 weeks after transplantation in September 2002), all transplanted individuals were harvested. At the same time, 15 resident plants were collected from both standing and running patches. The start date and duration of the experiment were designed to enable transplants to grow under stress-free conditions for a period long enough to allow for the turn-over of plant tissues and to harvest fully developed plants at the end of the vegetative growth period, but before autumnal decay or reduced growth. Transplants and residents were harvested on the same dates, thus avoiding a possible phenological effect.
All plants were stored in aerated tap water at 16°C for a maximum of 2 days until measurements were made. Transplanted ramets and the main ramet of a clone for resident plants were referred to as "mother ramets." New ramets produced vegetatively by mother ramets were referred to as "daughter ramets" and stolons and daughter ramets together were referred to as "juveniles."
Traits were measured for the ramet, the whole clone, and the juveniles. The following traits were measured for mother ramets: (1) plant height (cm); (2) number of leaves; (3) plant mass (g), plants were divided into roots, stems, and leaves, then the different parts were weighed to obtain fresh and dry mass after drying for 48 h at 85°C; (4) number of stolons produced and (5) leaf area (cm2), leaves were scanned (150 dpi, Epson Expression 1680 scanner; Epson America, Long Beach, California, USA) and the resultant images analyzed with WinFolia 2001 image analysis software (Regent Instruments, Quebec City, Quebec, Canada).
For each stolon, the following traits were measured: (1) stolon length (cm), (2) number of leaves carried by stolons (i.e., of daughter ramets or growing directly on stolon nodes), (3) number of daughter ramets, (4) the fresh and dry mass of the different sections (stolons, roots, stems, and leaves), and (5) spacer length between consecutive rooted ramets (mother or daughter).
These measurements were used to calculate the following traits grouped into four sets:
) and is linked to their biomechanical properties (e.g., stiffness and flexibility) and therefore to their adaptation to moving fluid (Niklas, 1996
; Usherwood et al., 1997
). Water content was considered here as the fresh mass of an organ regressed on the dry mass of the same organ. (A) Mother ramet: root, stem, and leaf water content. (B) Juveniles: stolon, root, stem, and leaf water content.
Statistical analysis
Mechanically stressed plants often display important size reductions, making it necessary to consider plant size when studying variations in morphological traits. Because of ontogenetic drift, some traits (e.g. biomass allocations) depend on plant size and growth stage (Gedroc et al., 1996
; McConnaughay and Coleman, 1998
, 1999
). Moreover, the comparison of some architectural traits (e.g., spacer length) is irrelevant if not corrected for size. In order to (1) express the biomass allocation of one organ relative to another (e.g., dry mass allocation to root relative to total dry mass), (2) calculate water content (fresh mass expressed relative to dry mass), and (3) standardize plant size, we calculated residuals of linear regression for the whole set of individuals and used them for comparison between treatments. This method was used, because the data set did not meet all the assumptions for an analysis of covariance. The residual distance (i.e., difference between the measured value of a trait for a given individual and its estimation provided by the regression) was used to estimate the allocation trait or the size-corrected trait. Variables that did not meet assumptions of linear regressions (normality and/or homogeneity of variances) were loge-transformed before regression to make the data closer to a normal distribution and to improve homogeneity of variances.
Variations in morphological traits between treatments (e.g., standing vs. running water, residents vs. transplants) were assessed through t tests, after normality and homoscedasticity tests carried out either on the measured traits, or on the residuals of the regression (Shapiro-Wilk and Bartlett's tests, respectively). The nonparametric Wilcoxon two-sample test was used when data did not meet the assumption of normality, and Welch's approximate t was used when data met normality assumptions, but variances were unequal (Zar, 1998
). We applied a sequential Bonferroni correction for multiple tests to control type I error rates (Sokal and Rohlf, 1995
). The Bonferroni correction was applied per hypothesis tested.
All statistical analyses were performed using JMP 5.1 statistical software (SAS Institute, Cary, North Carolina, USA)
RESULTS
Trait variations induced by current stress
Growth and biomass production: all growth-related traits of mother ramets (total dry mass, plant height, and total leaf area) and the total dry mass of the whole clone were significantly lower for plants exposed to current stress (Table 1, Figs. 1, 2). Individuals from the running patch had more stolons (not significant after Bonferroni correction), but total juvenile dry mass and total stolon length did not differ significantly. These three traits were significantly higher in the running patch, when expressed relative to total mother dry mass (Table 1, Fig. 2).
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Dry mass partitioning: mother ramets exhibited a higher relative allocation to roots (only before Bonferroni correction) and stems in the running patch, and a lower relative allocation to leaves (Table 2, Fig. 1). For juveniles, only the relative allocation to roots was significantly higher in the running patch, other traits exhibiting no significant trend (Table 2, Fig. 1). The relative allocation to belowground organs was significantly higher for whole clones in the running patch (Table 2). Dry mass allocation to mother leaves relative to total leaf dry mass of the clone was significantly lower (before Bonferroni correction) for plants originating from running patches (Table 2, Fig. 2).
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Trait variations after transplantation
Twenty-five and 23 transplants originating from standing and running patches, respectively, survived until the harvest date. Five individuals originating from running patch failed to establish at the beginning of the transplantation experiment, probably because of their small size and relatively insufficient anchorage strength.
Comparison of residents and transplants originating from the standing patch
Growth and biomass production: height was the only mother trait that differed significantly between residents and transplants (transplants exhibiting a significantly lower height, Table 3, Fig. 2). Transplants produced more stolons and a higher juvenile dry mass (still consistent after correction for mother plant size). Total stolon length was also higher, but only when corrected for mother plant size (Table 3). Total clone dry mass did not differ significantly (Table 3, Fig. 1).
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Dry mass partitioning: no trait, but leaf dry mass of the mother ramets relative to total leaf clone dry mass differed significantly (Table 4, Figs. 1, 2).
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Comparison of residents and transplants originating from the running patch
Growth and biomass production: all traits were significantly higher for transplants compared to residents (Table 3, Figs. 1, 2). Juvenile traits remained significantly higher for transplants after correction for mother ramet dry mass (but not after Bonferroni correction for total juvenile dry mass, Table 3).
Architecture and morphology: leaf number in mother ramets did not differ significantly. Stolons of transplants were longer, with higher spacer length, and more leaves, but with fewer daughter ramets than residents (Table 3, Fig. 2). However, only the length of the longest stolon remained significantly higher when corrected for total juvenile dry mass.
Dry mass partitioning: only the relative allocation to roots was significantly higher for transplanted mother ramets (before Bonferroni correction, Table 4, Fig. 1).
Water content: all but one trait (juvenile roots) were significantly higher for transplants (Table 4).
Comparison of transplants originating from standing and running patches
Growth and biomass production: all traits were significantly higher for transplants originating from the running patch compared to those of the standing one (not significant after Bonferroni correction for total mother and clone dry mass, Table 3, Figs. 1, 2). This pattern was also consistent for juvenile traits relative to total mother dry mass (but not significant after Bonferroni correction for total juvenile dry mass, Table 3, Figs. 1, 2).
Architecture and morphology: leaf number in mother ramets was significantly lower for transplants originating from the running patch (Table 3, Fig. 2). Stolons from the running patch were shorter relatively to total juvenile dry mass and carried significantly more leaves (even when corrected for total juvenile dry mass), but fewer daughter ramets with shorter stolons (before Bonferroni correction) (Table 3). Other traits did not differ significantly between transplants (Table 3).
Dry mass partitioning: relative dry mass allocations were higher for roots and stems and lower for leaves in mother ramets originating from the running patch (Table 4, Fig. 1). The dry mass allocation of juveniles did not differ significantly between transplants according to the patch of origin (Table 4, Fig. 1). At the clone level, belowground dry mass relative to total dry mass was significantly higher and the allocation to mother leaf dry mass relative to total clone dry mass was significantly lower (before Bonferroni correction), for plants originating from the running patch (Table 4, Fig. 2).
Water content: the water content was significantly higher for plants originating from the running patch (not significant after Bonferroni correction for juvenile roots and leaves, Table 4).
DISCUSSION
Growth patterns induced by current stress
The very small size of mother ramets (dry mass reduced by a factor of 15) and whole clones in the running patch are related to the strong current stress exerted on resident plants, their small size reducing the risk of damage by partly escaping the mechanical constraint (Puijalon et al., 2005
). The higher relative investment in clonal growth, together with a size reduction is rarely observed in response to stress. Indeed, clonal growth is usually positively related to plant size (Dong and de Kroon, 1994
; Verburg et al., 1996
). In the case of resource stress, small-sized mother ramets are usually associated with low clonal growth (Dong et al., 1996
; Clevering, 1998
; Stuefer and Huber, 1998
). For mechanical stress, increased clonal growth could reduce the detrimental effects of physical stress (vertical growth reduction) at the clone scale. This reallocation of biomass towards juveniles was possibly due to the plants not being resource limited.
The lower relative allocation to leaves in mother ramets within the clones growing in the running patch suggests a switch of photosynthesis from mother to juvenile leaves within the clone. This may indicate an altered pattern of physiological integration within the clone, particularly for the translocation of assimilates (e.g., increased basipetal translocation from younger to older ramets).
In accordance with the hypothesis, the relative allocation to belowground dry mass for the whole clone was higher in the running patch. This corresponded to a biomass accumulation in zones protected from the current and was considered to improve anchorage efficiency (Crook and Ennos, 1996
). More generally, observed patterns of dry mass allocation agreed with patterns observed in other studies concerning mechanical stress (Biddington and Dearman, 1985
; Crook and Ennos, 1996
; Niklas, 1998
).
Contrary to what we hypothesized, stolons were shorter and had shorter spacer lengths in the running patch. Plants did not escape unfavorable patches by producing longer spacers (as suggested by the optimal foraging model in the case of resource stress, de Kroon and Hutchings, 1995
) but, on the contrary, tended to present a more compact clonal growth form. Such a pattern could improve the reciprocal sheltering of ramets, thus decreasing the mechanical forces exerted on individuals (Koehl, 1982
; Peterson and Jones, 1997
).
Growth pattern of transplants
Transplantation per se did not strongly modify the traits of control plants, because only a few traits differed significantly between residents and transplants originating from the standing patch. The most noteworthy effect of transplantation was the increase in clonal growth. Stolon removal carried out before transplantation could have stimulated the production of new meristems, thus favoring clonal growth.
As hypothesized, all the growth-related traits of transplants originating from the running patch were much higher than those of residents of the same patch (e.g., by a factor of 1.5 for dry mass). Growth following stress removal was so significant that, at the end of the growing season, all the growth-related traits of previously stressed mother ramets were significantly higher than those of transplants originating from the standing patch. Compensatory growth leading to higher productivity by previously stressed plants compared to unstressed ones (i.e., "overcompensation" according to Belsky, 1986
) has already been observed for a terrestrial species submitted to mechanical stress (Retuerto and Woodward, 2001
). The high growth rate probably relied on the production of low-density tissues (Garnier, 1992
; Weiher et al., 1999
). Indeed, the water content increased very significantly for transplants (except for one organ) when compared to residents (both originating from the running patch).
The lack of convergence (i.e., maintenance of differences between plants originating from both patches) observed for the dry mass partitioning and architecture traits of mother ramets could be due to the transplantation period (18 weeks) being too short to enable plants to display significant changes in dry mass partitioning. Furthermore, adjustments in biomass allocation probably depended on the ontogenetic stage of the mother ramets. It could have been too late in ontogeny in this case for them to exhibit plastic responses. Previous studies have demonstrated that switches in nutrient availability have not systematically affected biomass partitioning (Gedroc et al., 1996
; McConnaughay and Coleman, 1998
).
More surprising was the lack of convergence observed for the dry mass partitioning and architecture traits of the juveniles growing under stress-free conditions (but produced by previously stressed vs. unstressed plants). This lack of convergence is due to the absence of significant variations or to the reinforcement of patterns observed in the reference patches. This result suggests a carryover effect (Schwaegerle et al., 2000
) or the storage and translocation of morphogenetic information from mother ramets to juveniles, occurring on the time scale of our experiment (Thellier et al., 2000
). However, the high variability of juvenile trait values resulting from the variability in size and age of the different stolons within a clone could also hide variation tendencies.
In the present work, we cannot exclude the possibility of a genetic difference between patches, which could explain some of the patterns observed. However, it is unlikely that plants of both patches were genetically differentiated because the patches were small and close to each other (only a few meters) and neither sexual reproduction, nor recruitment from seeds or drifting individuals could occur in patches with such fast-flowing water. Consequently, the running patch was probably colonized by a border effect from the less stressful upstream reaches.
Concluding remarks
This study demonstrates that mechanical stress induces changes in plant traits that differ from those observed under resource stress. In the latter case, growth patterns and biomass partitioning tend to maximize the use of the limiting resource (Chapin et al., 1987
; Gleeson and Tilman, 1992
). Mechanical stress exerts physical constraints on plants. In this case, modifications in the shape, lateral spreading, and spatial organization of plant biomass decrease the risk of the clone being damaged by flow forces. Altered clonal growth and stable offspring production under stressful conditions probably minimize extinction risk for the genet under fast flowing conditions, where sexual reproduction is frequently impeded.
The growth responses to stress observed for B. erecta probably differ from those of aquatic species with contrasting growth forms. Indeed, these growth patterns are ruled by the location of plant meristems (e.g., located in a basal position for rosette growth form or in an apical position for erect stems), but probably also by the whole set of architectural constraints that characterize each species (e.g., the preformation and dormancy of meristems, de Kroon and van Groenendael, 1990
; Hutchings and Mogie, 1990
; Watson et al., 1997
).
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1 The authors thank P. Robinot (Poissons Sauvages Production) for providing the experimental canal and D. Reynaud and E. Malet for technical assistance. This study was partly funded by the "Thématiques Prioritaires" of the Rhône-Alpes region, and was carried out under the aegis of the long-term ecological research program on the Rhône River Basin (Zone Atelier Bassin du Rhône). 
2 Author for correspondence (sara.puijalon{at}univ-lyon1.fr
)
LITERATURE CITED
Belsky A. J.. 1986. Does herbivory benefit plants? A review of the evidence. American Naturalist 127: 870-892.[CrossRef][Web of Science]
Biddington N. L. Dearman A. S.. 1985. The effect of mechanically induced stress on the growth of cauliflower, lettuce and celery seedlings. Annals of Botany 55: 109-119.
Boeger M. R. T. Poulson M. E.. 2003. Morphological adaptations and photosynthetic rates of amphibious Veronica anagallis-aquatica L. (Scrophulariaceae) under different flow regimes. Aquatic Botany 75: 123-135.[CrossRef][Web of Science]
Chapin F. S. III. 1991. Effects of multiple environmental stresses on nutrient availability and use. In H. A. Mooney, W. E. Winner and E. J. Pell [eds.] Responses of plants to multiple stresses 67-88 Academic Press, New York, New York, USA.
Chapin F. S. III Bloom A. J. Field C. B. Waring R. H.. 1987. Plant responses to multiple environmental factors. Bioscience 37: 49-57.
Clevering O. A.. 1998. An investigation into the effects of nitrogen on growth and morphology of stable and die-back populations of Phragmites australis. Aquatic Botany 60: 11-25.[CrossRef]
Crook M. J. Ennos A. R.. 1996. Mechanical differences between free-standing and supported wheat plants Triticum aestivum L. Annals of Botany 77: 197-202.
de Kroon H. van Groenendael J.. 1990. Regulation and function of clonal growth in plants: an evaluation. In J. van Groenendael and H. de Kroon [eds.] Clonal growth in plants: regulation and function SPB Academic Publishing, The Hague, Netherlands.
de Kroon H. Hutchings M. J.. 1995. Morphological plasticity in clonal plants: the foraging concept revisited. Journal of Ecology 83: 143-152.[CrossRef]
Dingman S. L.. 1984. Fluvial hydrology W. H. Freeman, New York, New York, USA.
Dong M. de Kroon H.. 1994. Plasticity in morphology and biomass allocation in Cynodon dactylon, a grass species forming stolons and rhizomes. Oikos 70: 99-106.[CrossRef][Web of Science]
Dong M. During H. J. Werger M. J. A.. 1996. Morphological responses to nutrient availability in four clonal herbs. Vegetatio 123: 183-192.[CrossRef][Web of Science]
Ennos A. R.. 1997. Wind as an ecological factor. Trends in Ecology and Evolution 12: 108-111.[CrossRef]
Foote A. L. Kadlec J. A.. 1988. Effects of wave energy on plant establishment in shallow lacustrine wetlands. Journal of Freshwater Ecology 4: 523-532.[Web of Science]
Gantes H. P. Caro A. S.. 2001. Environmental heterogeneity and spatial distribution of macrophytes in plain streams. Aquatic Botany 70: 225-236.[CrossRef]
Garnier E.. 1992. Growth analysis of congeneric annual and perennial grass species. Journal of Ecology 80: 665-675.[CrossRef][Web of Science]
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][Web of Science]
Gedroc J. J. McConnaughay K. D. M. Coleman J. S.. 1996. Plasticity in root/shoot partitioning: optimal, ontogenetic, or both?. Functional Ecology 10: 44-50.[CrossRef][Web of Science]
Gleeson S. K. Tilman D.. 1992. Plant allocation and the multiple limitation hypothesis. American Naturalist 139: 1322-1343.[CrossRef][Web of Science]
Henry H. A. L. Thomas S. C.. 2002. Interactive effects of lateral shade and wind on stem, allometry, biomass allocation, and mechanical stability in Abutilon theophrasti (Malvaceae). American Journal of Botany 89: 1609-1615.
Hik D. S. Brown M. Dabros A. Weir J. J. Jr Cahill. 2003. Prevalence and predictability of handling effects in field studies: results from field experiments and a meta-analysis. American Journal of Botany 90: 270-277.
Hodges L. Suratman M. N. Brandle J. R. Hubbard K. G.. 2004. Growth and yield of snap beans as affected by wind protection and microclimate changes due to shelterbelts and planting dates. Hortscience 39: 996-1004.[Web of Science]
Hudon C. Lalonde S. Gagnon P.. 2000. Ranking the effects of the site exposure, plant growth form, water depth, and transparency on aquatic plant biomass. Canadian Journal of Fisheries and Aquatic Sciences 57: S31-S42.
Hutchings M. J. Mogie M.. 1990. The spatial structure of clonal plants: control and consequences. In J. van Groenendael and H. de Kroon [eds.] Clonal growth in plants: regulation and function 57-76 SPB Academic Publishing, The Hague, Netherlands.
Hutchings M. J. de Kroon H.. 1994. Foraging in plants: the role of morphological plasticity in resource acquisition. Advances in Ecological Research 25: 159-238.[CrossRef][Web of Science]
Hutchings M. J. John E. A.. 2004. The effects of environmental heterogeneity on root growth and root/shoot partitioning. Annals of Botany 94: 1-8.
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 M. J. Leoplold A. C. Staples R. C.. 2002. Thigmo responses in plants and fungi. American Journal of Botany 89: 375-382.
Koehl M. A. R.. 1982. The interaction of moving water and sessile organisms. Scientific American 247: 110-120.[Web of Science][Medline]
Lytle D. A. Poff N. L.. 2003. Adaptation to natural flow regimes. Trends in Ecology and Evolution 19: 94-100.
McConnaughay K. D. M. Coleman J. S.. 1998. Can plants track changes in nutrient availability via changes in biomass partitioning. Plant and Soil 202: 201-209.[CrossRef][Web of Science]
McConnaughay K. D. M. Coleman J. S.. 1999. Biomass allocation in plants: ontogeny or optimality? A test along three resource gradients. Ecology 80: 2581-2593.[CrossRef][Web of Science]
Niklas K. J.. 1996. Differences between Acer saccharum leaves from open and wind-protected sites. Annals of Botany 78: 61-66.
Niklas K. J.. 1998. Effects of vibration on mechanical properties and biomass allocation pattern of Capsella bursa-pastoris (Cruciferae). Annals of Botany 82: 147-156.
Peterson C. J. Jones R. H.. 1997. Clonality in woody plants: a review and comparison with clonal herbs. In H. de Kroon and J. van Groenendael [eds.] The ecology and evolution of clonal plants 263-289 Backhuys, Leiden, Netherlands.
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][Web of Science]
Puijalon S. Bornette G. Sagnes P.. 2005. Adaptations to increasing hydraulic stress: morphology, hydrodynamics and fitness of two higher aquatic plant species. Journal of Experimental Botany 56: 777-786.
Retuerto R. Woodward F. I.. 2001. Compensatory responses in growth and fecundity traits of Sinapis alba L. following release from wind and density stress. International Journal of Plant Sciences 162: 171-179.[CrossRef][Web of Science]
Schutten J. Dainty J. Davy A. J.. 2005. Root anchorage and its significance for submerged plants in shallow lakes. Journal of Ecology 93: 556-571.
Schwaegerle K. E. McIntyre H. Swingley C.. 2000. Quantitative genetics and the persistence of environmental effects in clonally propagated organisms. Evolution 54: 452-461.[Web of Science][Medline]
Sokal R. R. Rohlf F. J.. 1995. Biometry, 3rd ed W. H Freeman, New York, New York, USA.
Strand J. A. Weisner S. E. B.. 2001. Morphological plastic responses to water depth and wave exposure in an aquatic plant (Myriophyllum spicatum). Journal of Ecology 86: 166-175.
Stuefer J. F. Huber H.. 1998. Differential effects of light quantity and spectral light quality on growth, morphology and development of two stoloniferous Potentilla species. Oecologia 117: 1-8.[CrossRef][Web of Science]
Sultan S. E.. 2000. Phenotypic plasticity for plant development, function and life-history. Trends in Plant Science 5: 537-542.[CrossRef][Web of Science][Medline]
Sultan S. E.. 2003. Phenotypic plasticity in plants: a case study in ecological development. Evolution & Development 5: 25-33.
Thellier M. Le Sceller L. Norris V. Verdus M.-C. Ripoll C.. 2000. Long-distance transport, storage and recall of morphogenetic information in plants. The existence of a sort of primitive plant ‘memory.'. Comptes Rendus de l'Academie des Sciences Paris, Sciences de la vie/Life Sciences 323: 81-91.
Usherwood J. R. Ennos A. R. Ball D. J.. 1997. Mechanical adaptations in terrestrial and aquatic buttercups to their respective environments. Journal of Experimental Botany 48: 1469-1475.
Verburg R. W. Kwant R. Werger M. J. A.. 1996. The effect of plant size on vegetative reproduction in a pseudo-annual. Vegetatio 125: 185-192.[CrossRef][Web of Science]
Vogel S.. 1994. Life in moving fluids: the physical biology of flow Princeton University Press, Princeton, New Jersey, USA.
Watson M. A. Hay M. J. M. Newton P. C. D.. 1997. Developmental phenology and the timing of determination of shoot bud fates: ways in which the developmental program modulates fitness in clonal plants. In H. de Kroon and J. van Groenendael [eds.] The ecology and evolution of clonal plants Backhuys, Leiden, Netherlands.
Weiher E. van der Werf A. Thompson K. Roderick M. Garnier E. Eriksson O.. 1999. Challenging Theophrastus: a common core list of plant traits for functional ecology. Journal of Vegetation Science 10: 609-620.[CrossRef][Web of Science]
Zar J. H.. 1998. Biostatistical analysis Prentice Hall International, Upper Saddle River, New Jersey, USA.
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