| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Ecology |
2Organization for Tropical Studies, La Selva Biological Station, Interlink 341, P.O. Box 02-5635, Miami, Florida 33102-5635 USA; 3Department of Organismal Biology, Ecology and Evolution, University of California, Los Angeles, California 90095 USA
Received for publication June 5, 2003. Accepted for publication November 7, 2003.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
max), Young's modulus of elasticity (E), and flexural stiffness (F) of stems and petioles in 14 monocot species from six families. These biomechanical properties were evaluated with respect to habitat, rates of leaf production, clonality, and growth form. Species with higher E and max, indicating greater resistance per unit area to bending and breaking, respectively, tended to be shade-tolerant, slow growing, and nonclonal. This result is consistent with an increase in carbon allocation to structural tissue in shade-tolerant species at the expense of photosynthetic tissue and growth. Forest- edge species were weaker per unit area (had a lower E), but had higher flexural stiffness due to increases in stem and petiole diameter. While this is inefficient in requiring more carbon per unit of structural support, it may enable forest-edge species to support larger and heavier leaves. Our results emphasize the degree to which biomechanical traits vary with ecological niche and illustrate suites of characteristics associated with different carbon allocation strategies.
Key Words: biomechanics • herb • modulus of elasticity • modulus of rupture • monocot • petiole • stem • understory
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
). However, because structural tissues must be reinforced to avoid toppling as plant height increases, a trade-off in carbon allocation between height and support is created. Indeed, patterns of carbon allocation have been shown to change as a function of light availability (Givnish and Vermeij, 1976
), plant age (Steele et al., 1989
), and plant size (King, 1999
). Another trade-off exists between structural tissues and photosynthetic surface area (PSA). This trade-off is particularly critical in low-light understory environments where the benefit of a greater PSA is at odds with the cost of carbon investment in structures to support that amount of biomass. Such trade-offs between PSA and reinforcement of support tissues have been recorded in tropical understory palms, where support tissues are thought to increase plant resilience to damage from falling debris (Chazdon, 1986
).
Broad-leaved herbs of the tropical understory exemplify the conflict between safety and light-harvesting efficiency. They occupy environments where typical light levels are routinely as low as 1–2% of that in clearings (Chazdon and Fetcher, 1984
). Herbs with relatively greater PSA are likely to fix more carbon per unit biomass and thus be more likely to survive in heavily shaded sites. However, these same plants, living in the forest understory, are also subject to periodically falling canopy debris, ranging from leaf litter and small branches to whole trees and liana networks. Falling debris is a major cause of mortality in tropical understory plants including tree seedlings (Clark and Clark, 1989
), saplings (Hartshorn, 1972
; Uhl, 1982
; Aide, 1987
), and understory herbs (Gartner, 1989
; Sharpe, 1993
).
The combination of light limitation with a high risk of physical damage creates a resource allocation dilemma. Plants with light-limited growth rates cannot quickly replace lost or broken tissues. Avoiding damage in the first place should therefore be advantageous, and slow-growing plants might be expected to exhibit extensive investment in structural support. Conversely, fast-growing plants replace tissue more quickly and should thus be able to afford to allocate proportionally fewer resources to structural support.
Although this trade-off has been addressed for tropical understory palms (Chazdon, 1986
, 1991
), it has not been examined in their herbaceous monocot counterparts. Broad- leaved herbs are an important component of low cover in wet tropical forests, competing directly with understory palms of similar heights. Despite their ecological significance, however, little is known about the ecology of these herbs. Most broad- leaved herbs lack the stiff petioles and support structures characteristic of palms, the other major monocot group of the rainforest understory. Indeed, most herbs are fragile, with leaf support structures that readily undergo structural failure when struck by falling debris.
We selected a group of broad-leaved herbs having a diverse array of ecological properties. The study group contains examples of species with both musoid growth forms, where the petiole is the leaf support structure, and zingiberoid growth form species in which the stem is the primary support structure with lateral leaves borne on short petioles (Fig. 1). To our knowledge, no other studies have reported biomechanical properties of monocot herbs, or of any understory plants aside from the three palm species investigated by Chazdon (1986)
. Here we describe three measures of biomechanical support— the modulus of rupture, Young's modulus of elasticity, and flexural stiffness—of the leaf support tissues in 14 species of herbaceous understory monocots from six families.
|
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
). Adult plants of each study species were selected from natural populations growing in or near primary forest at La Selva. The taxa selected represent a variety of ecological characteristics, differing in aspects such as plant size and architecture, habitat type, and degree of clonal reproduction (Table 1). Ten of the species used (Calathea lasiostachya, Ischnosiphon inflatus, Asplundia uncinata, Cyclanthus bipartitus, Heliconia irrasa, H. umbrophila, Spathiphyllum fulvovirens, Philodendron grandipes, Costus scaber, and Renealmia pluriplicata) are found almost exclusively in the heavily shaded understory of the biological station's primary forest. The remaining four (Calathea marantifolia, Heliconia latispatha, H. mathiasiae, and Costus malortieanus) occur along trails and forest edges where light levels are higher. Although species found in the two habitats were morphologically comparable, leaf surface area and dry mass were significantly higher in forest-edge than in primary-forest species (A. M. Cooley and J. Sun, unpublished data).
|
max) represents the maximum stress per unit area that a structure can support without mechanical failure. The modulus of elasticity (E) is a measure of a material's resistance to bending per unit area; higher E indicates greater stiffness. Flexural stiffness is dependent on the cross-sectional dimensions as well as the elasticity of a material and describes total resistance to bending. Each stem and petiole tested was collected from a different adult plant. To avoid potential ontogenetic effects, such as reduced lignification associated with juvenile or senescent tissue, stems and petioles of the youngest fully mature tissues were selected. Segments 5–15 cm in length were cut from the center of each stem or petiole and were returned to the laboratory for biomechanical testing within 4 h of collection.
The basal end of each petiole or stem segment was tightly secured in a rubber stopper, which was fixed in a block of plaster of paris for stability (Fig. 2). Mass was added incrementally (1, 2, or 5 g at a time) to a preweighed plastic cup suspended from the distal end of the segment. With each added mass, the end of the segment bent slightly downward and then stopped. Mass was added until the point of mechanical failure, defined as the point at which the segment continued to sag downwards rather than stopping. A needle inserted at the distal end of the segment was used to measure vertical deflection with the addition of each mass increment. Vertical deflection, relative to the segment's unweighted position, was recorded.
|
max. E was determined using the mass and vertical deflection at one-half of the failure mass. Both max and E were calculated in grams per square centimeter and then converted to megaPascals.
Modulus of rupture
The equation for modulus of rupture is:
 | (1) |
, we evaluated max at the bottom of the petiole cross-section because petioles consistently failed under compression.
Second moment of area
The second moment of area (I) describes mass distribution around a given center of mass. Equations are available for calculating I for standard geometric shapes (Niklas, 1992
). Petioles and stems of most species had elliptical cross-sections, in which case the second moment of area was calculated as:
 | (2) |
 | (3) |
 | (4) |
 | (5) |
).
Modulus of elasticity
Young's modulus of elasticity was calculated using a standard equation, modified by Chazdon (1986)
to account for the slight linear taper of the petiole segments:
 | (7) |
); L is the distance between the fixed end of the petiole and the point of mass addition; t0 and tL are the segment thicknesses at the fixed end and the point of mass addition, respectively; and I0 is the second moment of area of a cross-section at the fixed end of the petiole.
Flexural stiffness
The flexural stiffness (F) of a segment is simply the product of the segment's modulus of elasticity and second moment of area, in units of newton square centimeters (N · cm2):
 | (8) |
Habitat, clonality, and leaf support
Species were considered primary- forest or forest-edge species, as described previously (Table 1). There was very little habitat overlap; primary-forest species were virtually never encountered on forest edges and vice versa.
Clonality was included as a factor in this study because we were interested in its potential "buffering effect" via nutrient translocation amongst individual ramets of a clonal genet. Species in which plants always occurred as isolated individuals were considered nonclonal for purposes of this study, although they may in fact be capable of reproducing vegetatively. Species were characterized as clonal if individuals routinely comprised two or more ramets connected by underground or aboveground rhizomes. Nondestructive root excavations were performed on multiple individuals of each species to determine whether or not such rhizomes were present.
The majority of the herbs used in this study had either musoid or zingiberoid growth forms. The "banana-like" musoids comprise clusters of petioles originating from a basal pseudostem, whereas "ginger-like" zingiberoids have alternating horizontal leaves attached to a central stem (Fig. 1). Petioles of musoid plants are highly elongated and can be easily snapped or broken by falling debris. In the zingiberoids, the petioles are quite short, and the stem to which they are attached is at a greater risk of breaking. To maintain functional equivalence in our comparisons, we examined the biomechanical properties of petioles in musoids and stems in zingiberoids. Ischnosiphon inflatus is neither musoid nor zingiberoid; rather, it is erect with tree-like branching. Since the petioles of I. inflatus are extremely short whereas the stems are long and slender, stems were considered to be most subject to physical damage and were selected as the unit of study.
Leaf production
Leaf production rates were monitored for eight species (Calathea lasiostachya, C. marantifolia, A. uncinata, Costus scaber, C. malortieanus, H. irrasa, H. latispatha, and S. fulvovirens). Fifteen adults of each species were selected haphazardly from natural populations at La Selva, distributed roughly 5–15 m from trails and transect lines. Individuals of the same species were separated by a minimum of 2 m. The number of new leaves produced was recorded every other week for 12 wk. Leaf production rates were expressed relative to each plant's initial number of leaves to standardize for differences in leaf number among individuals.
Data analysis
The mean modulus of rupture, modulus of elasticity, and flexural stiffness were calculated for each species individually. Differences among species were tested with a one-way ANOVA and the Tukey-Kramer pairwise comparison. Simple linear regressions were used to compare biomechanical properties for each individual.
Species were also grouped by three ecological characteristics: habitat type (primary forest vs. forest edge), clonal vs. nonclonal growth, and the functional unit of leaf support (stem vs. petiole). One-way ANOVAs were used to analyze differences within each set of ecological characteristics.
Flexural stiffness and the moduli of rupture and elasticity were plotted against rates of leaf production for eight species: Calathea lasiostachya, C. marantifolia, A. uncinata, Costus scaber, C. malortieanus, H. irrasa, H. latispatha, S. fulvovirens. All data were analyzed with JMP 4.0 (SAS Institute, Cary, North Carolina, USA).
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
max (r2 = 0.713, P < 0.001) and E (r2 = 0.677, P < 0.001). Mean values for the 14 species ranged widely, with a five-fold difference between the highest (0.326 ± 0.019 MPa; S. fulvovirens) and lowest (0.0657 ± 0.0059 MPa; Calathea marantifolia) mean max and a 12-fold difference between the highest (20.5 ± 2.8 MPa; S. fulvovirens) and lowest (1.67 ± 0.29 MPa; Costus malortieanus) mean E (Table 2). There was a positive correlation (r2 = 0.560, P < 0.0001) between max and E (Fig. 3A). For both biomechanical properties, S. fulvovirens scored the highest, indicating a greater resistance to both breaking (max) and bending (E), per unit of cross-sectional area, than any of the other species. Petioles of S. fulvovirens, with a mean midpoint diameter of just 0.33 ± 0.01 cm (N = 15), are the thinnest of any of the other nine musoid herbs in this study (data not shown). Mean midpoint petiole diameters of the other nine musoids range from 0.37 ± 0.03 cm (Calathea lasiostachya; N = 30) to 0.74 ± 0.06 cm (H. latispatha; N = 14).
|
|
max, it was not linearly correlated with E (r2 = 0.034, P > 0.05; Fig. 3B). The nonlinearity reflects variation in the other component of flexural stiffness, the second moment of area (I).
Habitat, clonality, and leaf support
The mean max (± SE) across primary-forest species was 0.155 ± 0.012 MPa, significantly higher than the 0.101 ± 0.013 MPa of forest- edge species (Fig. 4A). The mean E across primary-forest species was 8.24 ± 0.98 MPa, nearly three times the mean of 3.04 ± 0.29 MPa for forest-edge species (Fig. 4B). Flexural stiffness, in contrast, was significantly lower in primary-forest than in forest-edge species (3.84 ± 0.37 vs. 6.60 ± 0.70 MN · cm2; Fig. 4C).
|
max (0.161 ± 0.012 MPa) and a higher mean E (8.14 ± 0.88 MPa) than did clonal species (0.101 ± 0.015 and 4.31 ± 1.18 MPa, respectively), but did not differ in flexural stiffness (4.69 ± 0.43 vs. 4.51 ± 0.67 MN · cm2).
Petioles did not differ from stems with respect to max (0.142 ± 0.012 MPa in petioles; 0.132 ± 0.019 MPa in stems). They had a higher mean E (0.811 ± 0.084 MPa in petioles; 0.387 ± 0.133 MPa in stems), but a lower mean flexural stiffness (3.96 ± 0.40 MN · cm2 in petioles; 7.07 ± 0.46 MN · cm2 in stems).
Leaf production
Production of new leaves varied by species, from a mean of 8.1 ± 5.6% of initial leaf number in A. uncinata to 53.1 ± 6.0% in Calathea marantifolia (Table 3). Rates of leaf production were uniformly and significantly higher in forest-edge than old-growth plants (df = 114, t = 7.82, P < 0.001). Fast growth was associated with reduced biomechanical investment. Species with low moduli of rupture and elasticity—that is, little resistance per unit area to breaking or bending, respectively—tended to have higher rates of leaf production (Fig. 5). That trend did not hold for flexural stiffness, which covered a nearly equal range for forest-edge and primary-forest species (Fig. 5C).
|
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
max) and elasticity (E), respectively, varied widely across 14 species of broad-leaf monocot herbs. Species with greater resistance to bending and breaking tended to be shade tolerant, slow growing, and nonclonal. Petioles had higher E, on average, than stems, but the two leaf support types did not differ with respect to max.
The range of values of E is similar to that reported previously for 76 other herbaceous species (Niklas, 1995
). Of the 65 that were angiosperms, the lowest E was 0.090 GN, corresponding to 90 MPa, and the highest was 1.96 GN or 1960 MPa. Values obtained in the present study were comparable, ranging from 168 to 2048 MPa.
Variation in E reflects intrinsic anatomical changes, such as cell wall chemistry (Vicre et al., 1999
), cell anatomy (Balsamo et al., 2003
), or lignin content (Kohler, 2000
; Niklas et al., 2000
). The second moment of area (I), in contrast, is dependent on morphological variables, namely the diameter and shape of petiole cross sections. The second moment of area (I) has been shown to vary over ontogeny (Gallenmuller et al., 2001
; Isnard et al., 2003
), within species due to mechanical stress (Cordero, 1999
; Hepworth and Vincent, 1999
), and between closely related species that have different growth forms (Usherwood et al., 1997
; Isnard et al., 2003
). As might be expected, the species in this study that had thicker petioles also had higher second moments of area.
Flexural stiffness, that is, a petiole's total mass-bearing capacity, can be increased by increasing either E or I. Although the forest-edge species had uniformly lower E than primary- forest species, they tended to have much thicker stems and petioles. This increased I and thus flexural stiffness in forest- edge species. Size increase is generally not efficient with respect to carbon use, since the costs of biomechanical support increase disproportionately with plant height (Givnish, 1986
; King, 1999
; Hogan and Niklas, 2003
). The relatively low strength and stiffness of forest-edge plants per unit area reflects that inefficiency. Presumably, the high light conditions to which they are adapted permit this strategy of a low modulus of elasticity, compensated for by increased stem and petiole thickness.
Phenotypic plasticity could potentially contribute to the observed differences. Environmental variables such as light availability or exposure to mechanical stress may cause some degree of plasticity in biomechanical traits (Ashby et al., 1979
; Cordero, 1999
; Hepworth and Vincent, 1999
; Henry and Thomas, 2002
). Future studies should include reciprocal transplants to determine the extent to which the biomechanical properties reported here are influenced by environmental factors.
Habitat, clonality, and leaf support
Habitat (primary forest or forest edge) was the single most influential variable included in this study. Shade tolerance and slow growth rate are, not surprisingly, closely related features that appear to characterize a particular adaptive strategy of herb species common to the deeply shaded understory of primary forest. Given the extreme light limitation of the rainforest understory (Chazdon and Fetcher, 1984
), primary-forest herbs might be expected to have larger leaves than forest-edge herbs, in order to maximize light interception. In fact, as noted earlier (A. M. Cooley and J. Sun, unpublished data), mean leaf surface area is actually smaller in primary-forest herbs.
Despite having relatively small leaves, primary-forest species had stiffer and stronger leaf support structures than the forest-edge species, as indicated by their higher moduli of elasticity and rupture, respectively. This suggests that the former are slow growing not only because of light limitation but also because they allocate a larger fraction of their already slender carbon budget to nonphotosynthetic support tissues and is consistent with a strategy of increased investment in biomechanical support at the expense of photosynthetic surface area. The high risk of damage by falling debris compounds the difficulty of persisting in the light-limited understory. Selection for extensive structural reinforcement appears to further slow the growth rate realized by shade-tolerant herbs.
Within any given habitat, variation in carbon allocation is undoubtedly influenced by a complex and interacting set of species-specific characteristics. Successional stage, competitive ability, moisture or nutrient requirements, and reproductive strategies are all important aspects of plant ecology that could influence carbon allocation strategies and biomechanical properties. Our data indicate an effect of another ecological feature, namely degree of clonality. Nonclonal species were significantly stronger and stiffer than clonal species in our study.
An important advantage of clonality is that it reduces the risk of mortality due to ramet damage (i.e., by falling debris). A single catastrophic event, such as windfall, lightning strike, or tree- or branch-fall, is much more likely to obliterate a single, isolated individual than a spatially dispersed clonal cluster. Clonality spreads the risk of mortality among multiple copies of the same genotype.
Nonlethal damage can also be ameliorated by clonality. Many clonal plants are known to share water and nutrients among their ramets (Tissue and Nobel, 1990
; Alpert, 1996
; deKroon et al., 1996
), potentially enabling the rescue of a damaged ramet by other ramets whose photosynthetic surface area remains relatively intact. These forms of risk reduction associated with clonality imply that clonal plants can afford to invest less carbon in damage resistance because they have more effective mechanisms of damage recovery. Indeed, Chazdon (1991)
proposed that translocation of resources to artificially defoliated ramets in a clonal palm may have helped the damaged ramets maintain steady rates of growth. The data we present are consistent with this proposed benefit of clonality, with lower moduli of elasticity and rupture in clonal herbs than in their nonclonal counterparts.
Petioles and stems were similar with respect to max. Stems had a lower E, but because they were thicker than petioles they had a higher flexural stiffness. As in the comparison between primary-forest and forest-edge species, the larger size of stems relative to petioles compensates for reduced biomechanical efficiency (that is, less stiffness per unit area of support structure).
Leaf production
The inverse relationships of leaf production rate with the moduli of elasticity and rupture are consistent with a carbon allocation trade-off between "speed" and "safety." However, the pattern is observed only when both forest-edge and primary-forest plants are included. No trade- off between leaf production rate and biomechanical support per unit area was observed within either of these two habitats. Strategies of structural investment, then, appear to vary across broad habitat categories. Forest-edge species had low, nearly constant E and max and high, variable rates of leaf production, consistent with a "speed" strategy of minimal structural reinforcement and more or less rapid growth. The converse was true of primary-forest species: they had high E and max and low, constant rates of leaf production, consistent with a strategy of maximizing safety at the expense of growth rate. No trade-off was evident with respect to flexural stiffness. Although one of its components, E, decreased with rates of leaf production, the other component, I, did not.
Differences between herbaceous monocots and palms
The values of elasticity and rupture reported for the 10 primary-forest herbs are generally lower than values reported for the palms G. congesta, G. cuneata, and A. martiana (Table 4). The reduced strength and stiffness of herb stems and petioles compared to palms is consistent with the subjective impression that they are fleshier and more easily broken. The observed disparity may lead to important differences in growth strategy between these two sets of taxa and suggests that they should perhaps not be grouped together into a general "understory monocots" category of plant growth form.
|
Despite obvious morphological similarities, Asplundia uncinata and the palms with which it co-occurs have fundamental biomechanical differences. The morphology and distribution patterns of Asplundia uncinata are deceptively similar to those of several common understory palms, and yet it falls squarely with the assemblage of other primary-forest herbs in terms of flexibility and strength. Its petioles are much weaker and more flexible than the palm petioles and are in fact very near the median moduli of elasticity and rupture for the primary-forest herbs in this study.
The contrasts between Asplundia uncinata and the palms mentioned earlier may reflect important differences in growth strategies that enable their continued coexistence. The mechanism for this has yet to be determined. Root storage capacity, leaf production rates, and responses to defoliation all appear to be comparable amongst the three.
In contrast to A. uncinata, S. fulvovirens does not appear to have many ecological "safety mechanisms" to protect against genet destruction by falling debris: in addition to its slender petioles, it does not occur in clonal stands and its root systems are fairly small, thus limiting the amount of carbohydrate it can store for emergency tissue regeneration. Nonetheless, S. fulvovirens is one of the most abundant of the understory herbs at La Selva (A. M. Cooley, unpublished data). Its success in surviving the rain of debris suffered by understory plants is more comprehensible in light of its biomechanical strength and resilience, reflected in its high E and max.
Variability within families
The study taxa include four species from the Heliconiaceae and three species from the Marantaceae, thus giving some illustration of the potential for variation within and among families. The four Heliconiaceae were grouped around the median for both E and max. In both cases, the species order from highest to lowest average value was: H. mathiasiae > H. umbrophila > H. irrasa > H. latispatha. In the case of the Marantaceae, effects of habitat overwhelm effects of phylogenetic relatedness. Both Calathea lasiostachya and I. inflatus had among the highest values for modulus of elasticity and modulus of rupture. In contrast, the forest-edge Marantaceae, C. marantifolia, had the third lowest modulus of elasticity and the lowest modulus of rupture.
Other ecological variables besides habitat may contribute to large within-family differences in biomechanical properties. Of the primary-forest Araceae, for example, Spathiphyllum fulvovirens had the highest modulus of elasticity and modulus of rupture, whereas P. grandipes was in the lower 50th percentile for both properties. In sum, habitat and other ecological factors may be better predictors of biomechanical properties than phylogeny.
Conclusion
Biomechanical properties are intimately related to plant form and function and may influence key life history characteristics such as leaf turnover, growth rates, longevity, or resilience to damage. Our results emphasize the degree to which biomechanical traits vary with ecological niche and suggest that selective forces have acted, directly or perhaps indirectly via correlated traits, on the degree of investment in structural support. Multiple successful strategies exist, as with the compensation between E and I in influencing flexural stiffness.
|
FOOTNOTES |
|---|
4 Present address: Department of Biology, Duke University, Durham, North Carolina 27708 USA. E-mail: amc34{at}duke.edu
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Alpert P. 1996 Nutrient sharing in natural clonal fragments of Fragaria chiloensis. Journal of Ecology 84: 395-406[CrossRef][ISI]
Ashby W. C. A. Kolar T. R. Hendricks R. E. Phares 1979 Effects of shaking and shading on growth of three hardwood species. Forest Science 25: 212-216[ISI]
Balsamo R. A. A. M. Bauer S. D. Davis B. M. Rice 2003 Leaf biomechanics, morphology, and anatomy of the deciduous mesophyte Prunus serrulata (Rosaceae) and the evergreen sclerophyllous shrub Heteromeles arbutifolia (Rosaceae). American Journal of Botany 90: 72-77
Chazdon R. L. 1986 The costs of leaf support in understory palms: economy versus safety. American Naturalist 127: 9-30[CrossRef][ISI]
Chazdon R. L. 1991 Effects of leaf and ramet removal on growth and reproduction of Geonoma congesta, a clonal understorey palm. Journal of Ecology 79: 1137-1146[CrossRef]
Chazdon R. L. N. Fetcher 1984 Photosynthetic light environments in a lowland tropical rain-forest in Costa Rica. Journal of Ecology 72: 553-564[CrossRef]
Clark D. B. D. A. Clark 1989 The role of physical damage in the seedling mortality regime of a neotropical rain-forest. Oikos 55: 225-230[CrossRef][ISI]
Cordero R. A. 1999 Ecophysiology of Cecropia schreberiana saplings in two wind regimes in an elfin cloud forest: growth, gas exchange, architecture and stem biomechanics. Tree Physiology 19: 153-163[ISI][Medline]
deKroon H. B. Fransen J. W. A. vanRheenen A. vanDijk R. Kreulen 1996 High levels of inter-ramet water translocation in two rhizomatous Carex species, as quantified by deuterium labelling. Oecologia 106: 73-84
Gallenmuller F. U. Muller N. Rowe T. Speck 2001 The growth form of Croton pullei (Euphorbiaceae): functional morphology and biomechanics of a neotropical liana. Plant Biology 3: 50-61[CrossRef][ISI]
Gartner B. L. 1989 Breakage and regrowth of Piper species in rain-forest understory. Biotropica 21: 303-307[CrossRef][ISI]
Givnish T. J. 1982 On the adaptive significance of leaf height in forest herbs. American Naturalist 120: 353-381[CrossRef][ISI]
Givnish T. J. 1986 Biomechanical constraints on crown geometry in forest herbs. In T. J. Givnish [ed.], On the economy of plant form and function, 525–583. Cambridge University Press, Cambridge, UK
Givnish T. J. J. G. Vermeij 1976 Sizes and shapes of liana leaves. American Naturalist 110: 743-778[CrossRef][ISI]
Hartshorn G. S. 1972 The ecological life history and population dynamics of Pentaclethra macroloba, a tropical wet forest dominant, and Stryphnodendron excelsum, an occasional associate. Thesis, University of Washington, Seattle, Washinton, USA
Henry H. A. L. S. C. Thomas 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
Hepworth D. G. J. F. V. Vincent 1999 The growth response of the stems of genetically modified tobacco plants (Nicotiana tabacum ‘Samsun’) to flexural stimulation. Annals of Botany—London 83: 39-43
Hogan C. J. K. J. Niklas 2003 On the economy and safety of hollow non-septate peduncles. American Journal of Botany 90: 356-363
Isnard S. T. Speck N. P. Rowe 2003 Mechanical architecture and development in clematis: implications for canalised evolution of growth forms. New Phytologist 158: 543-559[CrossRef][ISI]
King D. A. 1999 Juvenile foliage and the scaling of tree proportions, with emphasis on Eucalyptus. Ecology 80: 1944-1954[ISI]
Kohler L. 2000 Biphasic mechanical behaviour of plant tissues. Materials Science and Engineering C: Biomimetic and Supramolecular Systems 11: 51-56
Niklas K. J. 1992 Plant biomechanics: an engineering approach to plant form and function. University of Chicago Press, Chicago, Illinois, USA
Niklas K. J. 1995 Plant height and the properties of some herbaceous stems. Annals of Botany 75: 133-142
Niklas K. J. F. Molina-Freaner C. Tinoco-Ojanguren D. J. Paolillo 2000 Wood biomechanics and anatomy of Pachycereus pringlei. American Journal of Botany 87: 469-481
Sanford R. L. P. Paaby J. Luvall E. Phillips 1994 Climate, geomorphology and aquatic systems. In L. McDade [ed.], La Selva: ecology and natural history of a neotropical rainforest, 19–33. University of Chicago Press, Chicago, Illinois, USA
Sharpe J. M. 1993 Plant growth and demography of the neotropical herbaceous fern Danaea wendlandii (Marattiaceae) in a Costa Rican rain forest. Biotropica 25: 85-94[CrossRef][ISI]
Steele M. J. M. P. Coutts M. M. Yeoman 1989 Developmental changes in Sitka spruce as indexes of physiological age. 1. Changes in needle morphology. New Phytologist 113: 367-375[CrossRef][ISI]
Tissue D. T. P. S. Nobel 1990 Carbon translocation between parents and ramets of a desert perennial. Annals of Botany 66: 551-557
Uhl C. 1982 Tree dynamics in a species rich tierra firme forest in Amazonia, Venezuela. Acta Cientifica Venezolana 33: 72-77
Usherwood J. R. A. R. Ennos D. J. Ball 1997 Mechanical and anatomical adaptations in terrestrial and aquatic buttercups to their respective environments. Journal of Experimental Botany 48: 1469-1475
Vicre M. H. W. Sherwin A. Driouich M. A. Jaffer J. M. Farrant 1999 Cell wall characteristics of hydrated and dry leaves of the resurrection plant Craterostigma wilmsii, a microscopical study. Journal of Plant Physiology 155: 719-726[ISI]
This article has been cited by other articles:
|
|
 |
|
  S. A. Etnier and P. J. Villani Differences in mechanical and structural properties of surface and aerial petioles of the aquatic plant Nymphaea odorata subsp. tuberosa (Nymphaeaceae) Am. J. Botany, July 1, 2007; 94(7): 1067 - 1072. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. M. Bruna and M. B. N. Ribeiro The compensatory responses of an understory herb to experimental damage are habitat-dependent Am. J. Botany, December 1, 2005; 92(12): 2101 - 2106. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
