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Anatomy and Morphology |
Department of Biological Sciences, Butler University, Indianapolis, Indiana 46208 USA
Received for publication October 9, 2006. Accepted for publication May 11, 2007.
ABSTRACT
Lily pads (Nymphaea odorata) exhibit heterophylly where a single plant may have leaves that are submerged, floating, or above (aerial) the surface of the water. Lily pads are placed in a unique situation because each leaf form is exposed to a distinctly different set of mechanical demands. While surface petioles may be loaded in tension under conditions of wind or waves, aerial petioles are loaded in compression because they must support the weight of the lamina. Using standard techniques, we compared the mechanical and morphological properties of both surface and aerial leaf petioles. Structural stiffness (EI) and the second moment of area (I) were higher in aerial petioles, although we detected no differences in other mechanical values (elastic modulus [E], extension ratio, and breaking strength). Morphologically, aerial petioles had a thicker rind, with increased collenchyma tissue and sclereid cell frequency. Aerial petioles also had a larger cross-sectional area and were more elliptical. Thus, subtle changes in the distribution of materials, rather than differences in their makeup, differentiate petiole forms. We suggest that the growth of aerial petioles may be an adaptive response to shading, allowing aerial leaves to rise above a crowded water surface.
Key Words: amphibious • biomechanics • heterophylly • Indiana • lily pad • Nymphaeaceae • petiole • plasticity
Heterophylly, or the presence of two or more leaf forms on a single plant, is a common phenomenon (Arber, 1920
; Sculthorpe, 1967
). Some of the more pronounced examples of heterophylly occur in the amphibious aquatic plants (Schmidt and Millington, 1968
; Cook, 1969
) where a single plant may have leaves that are submerged, floating, or above (aerial) the surface of the water. As the aquatic environment changes (e.g., water depth, light quality, water clarity), the ability to position leaves in different areas about the environment allows the plant to maintain photosynthetic ability. Amphibious aquatic plants are unique because they produce leaves in different physical environments. Thus, these distinct leaf forms are exposed to a different set of mechanical demands (for reviews see Koehl, 1986
; Denny et al., 1989
). Amphibious aquatic plants provide a unique situation for studying how a single plant can alter internal factors to change its biomechanical properties to match the environment.
The leaves of the American white water lily [Nymphaea odorata Ait. subsp. Tuberosa (Paine) Wiersm & Hellquist] have marked heterophylly, providing an opportunity to compare the biomechanical properties of distinctly different leaf forms. Lily pads are a common floating aquatic plant in still and slow-flowing freshwater in the northeastern parts of North America (Gleason and Cronquist, 1991
). Plants primarily produce two distinct mature leaf forms (Sculthorpe, 1967
). These different forms do not reflect a growth continuum of a single leaf but rather distinct leaf forms that may be a response to environmental factors. Early in the growing season, most leaves float on the surface of the pond. These surface leaves have a flexible petiole that cannot support the weight of the lamina (S. A. Etnier and P. J. Villani, personal observation). Because petiole length typically exceeds water depth, the petiole is subject to tensile loads only under conditions of wind or water movement (Sculthorpe, 1967
). Later in the season, aerial leaves, in which the lamina is held above the surface of the water, become the dominant leaf form (Fig. 1). The petiole of an aerial leaf supports the weight of the lamina, loading the petiole in compression (Biehle et al., 1998
). Thus, surface and aerial petioles experience very different physical demands which must be met by differences in the mechanical behavior of the petioles.
|
). Structural stiffness is a measure of the resistance of a beam to bending under a given load. Structural stiffness is a composite variable (EI: E, elastic modulus; I, second moment of area) determined both by material composition and the distribution of those materials (Wainwright et al., 1976
). The material property of importance is the elastic modulus (E), which describes how a sample of material deforms when a load is applied in simple tension or compression (Roark, 1943
; Vincent, 1990
). The distribution of material is described by the second moment of area (I), which reflects the cross-sectional geometry (size and shape) of the beam (Roark, 1943
; Vincent, 1990
). Because structural stiffness is a composite variable, a beam's stiffness can be altered by changing either its material makeup and/or the distribution of that material. Material differences may reflect changes in the composition of individual components making up the petiole, such as cell wall chemistry (Vicre et al., 1999
), cell anatomy (Balsamo et al., 2003
), or lignin content (Kohler, 2000
; Niklas et al., 2000
). Structural differences may involve combined changes in the size and shape of the petiole, or they may occur on a finer scale and involve the distribution of support tissues, changes in cell wall thickness, or changes in cell size (Balsamo et al., 2003
). This paper has two distinct goals: First, to quantify the mechanical differences between aerial and surface petioles; and second, to determine whether these differences are due to changes in material composition and/or the distribution of those materials. Specifically, we measured both material and structural properties from a mechanical and morphological perspective. Thus, this study provides insight into how subtle changes in leaf growth dramatically alter the biomechanical properties of the petioles. We propose that the biomechanical properties that differentiate the heterophyllic leaves of the lily pad are an adaptive response to environmental cues that alter the developmental pathway of a maturing leaf. By doing so, the plant is able to elevate the lamina out of the water to an unobstructed position for maximizing light interception.
MATERIALS AND METHODS
Plant material
A population of Nymphaea odorata subsp. tuberosa growing in a 2000 m2 ice skating pond at Eagle Creek City Park, Indianapolis, Indiana, was used for all measurements in this study. The subspecies tuberosa has characteristic knotty, tuberous rhizomes; long, striped petioles; and large, green, orbicular leaves (Gleason and Cronquist, 1991
). Except where noted, all petioles were collected from May through July 2005.
Mechanical tests
Petioles collected for mechanical measurements were immediately placed in an insulated cooler with cool pond water and tested within 3 h of collection. Petioles remained in the cooler until just before testing, with each test taking no more than 5 min.
Structural stiffness
Structural stiffness was measured on surface and aerial petioles using standard three-point bending tests. Each petiole was placed horizontally between a pair of supports 4–5 cm apart. Because petioles were positioned without reference to shape, values should be considered as overall measures of stiffness, due to the radial asymmetry of some petioles. The stem was loaded midway between the supports with standard weights, causing the petiole to deform. A millimeter ruler mounted 1 cm behind the petiole was used to measure deformation, approximately 30 s after load application. A Coolpix 5400 digital camera (Nikon, Tokyo, Japan), mounted 25 cm in front of the sample, was used to record an image of the deformation following each load. All length measurements were made from digital images with a precision of 0.01 mm using the Motic imaging system (Motic Instruments, Richmond, British Columbia, Canada) and were calibrated with a known standard. In terms of applied weight (F), distance between supports (s), and deflection (d), structural stiffness (EI) was calculated as:
|
| (1) |
). Deflections were less than 5% of beam length, ensuring that measurements reflected bending rather than shearing. Specimens were tested with three loads of different magnitude, and these deformations were used to calculate the mean value for structural stiffness. This protocol assumes that structural stiffness is a linear function of load.
Material properties
Standard uniaxial force-extension tests (Koehl and Wainwright, 1973
) were used to measure the elastic modulus (E), breaking strength (both force per cross-sectional area), and maximum extension ratio or strain (l/lo, dimensionless). The extension ratio was calculated as the length following load application (l) divided by the original length (lo). Petioles were hung vertically and marked with two lines approximately midway along the length. A known load was applied to the free end, causing the petiole to extend. The amount of extension was measured between the two marked lines approximately 30 s after load application. In practice, approximately 25 cm of petiole from an underwater portion was mounted in the test apparatus. Weights were added until the petiole broke or the grips failed. Image acquisition and calibration were completed as described previously. The effective elastic modulus (E) was determined from the slope of the straight portion of the stress–strain curve (Vincent, 1990
). Breaking strength and maximum measured extension ratios (extension ratio at which breakage or failure occurred) were determined by petiole breakage, when possible.
During summer 2005, the majority of laboratory breaking tests were unusable because the grips failed before the petiole did. In June 2006, field tests were done to calculate breaking strength of surface and aerial petioles. A 20-kg Pesola scale (Pesola AG, Baar, Switzerland) was connected to a loop of string tied around the petiole 4–6 cm below the lamina. A vertical force was applied until the petiole broke. In general, the breakage was perpendicular to the long axis, near the distal end.
Distribution of materials
A razor blade was used to cut cross sections of petioles for calculating the second moment of area (I). Each cross section was imaged using the Motic imaging system. Values of I for bending about the long and short axis were calculated by hand, using the standard equation (Gere and Timoshenko, 1984
):
|
| (2) |
Morphology
Thirty-five petioles of each leaf form (surface and aerial) were collected during the growing season for morphological measurements. A cross section, approximately 1 mm thick, was taken from the midpoint of a fresh petiole and photographed with the Motic imaging system attached to a standard dissecting microscope. Morphological measurements were made from digital micrographs using the Motic imaging system . The following characteristics were measured for each petiole: (1) total cross-sectional area, (2) maximal and minimal diameter (x/y), (3) number of internal lacunae greater than 0.5 mm in diameter, (4) total cross-sectional area of lacunae, and (5) the percentage of lacunae cross-sectional area compared with total cross-sectional area of the petiole.
Microscopy
Ten petioles from each leaf form were collected for histological studies. A cross section approximately 4 mm thick was taken from the midpoint of the petiole and fixed overnight in 2% glutaraldehyde in a 50 mM phosphate buffer (pH 7.2), dehydrated in a graded ethanol series, and embedded in JB-4 plastic (Polysciences, Warrington, Pennsylvania, USA). Sections were cut at 4 µm on a Sorvall (Newtown, Connecticut, USA) JB-4A microtome and stained with 0.05% toluidine blue in benzoate buffer at pH 4.4. The petiole cross section was divided into two regions based on histology. The rind was defined as the epidermis and the collenchyma tissue adjacent to the epidermis. The core was defined as all tissues internal to the rind, including the lacunae. The following histological measurements were recorded: (1) number of subepidermal collenchyma layers, (2) rind thickness, and (3) mean spacing between subepidermal sclereids. This final parameter was determined by choosing 10 sclereids per petiole and measuring the distance from each to its nearest neighbor.
Stereology
The frequency of sclereids within a cross section of the petiole was determined using the disector principle (Mouton, 2002
). A segment of petiole approximately 3 cm long was taken from the midpoint of five fresh surface and aerial petioles. Cross sections (1 mm thick) were removed from five different locations within each segment and prepared for light microscopy as described previously. A Leica (Wetzlar, Germany) DMLB Microscope with an attached SPOT imaging system (Diagnostic Instruments, Sterling Heights, Michigan, USA) was used to take micrographs of a reference space within each of the five cross sections. The reference space was defined as starting at a point on the epidermis and extending to the center of the petiole. A transparent grid was placed over a micrograph that was printed on a standard laser printer. For each cross section, 35 disector frames were observed for the presence or absence of sclerenchyma tissue. Frames were selected using a random number generator. Sclerenchyma frequency, the mean number of sclereid cells per millimeter squared, was determined by calculating mean sclereid frequency for the five sections taken from each petiole, and then calculating the mean for the five petioles of each leaf form (surface and aerial). Note that this measurement represents the frequency of sclereid cells across the entire petiole cross section (rind and core), while the nearest neighbor measurement reflects how closely spaced sclereids are within the rind only.
Statistical analysis
Arithmetic means were calculated for all measured values. Differences between leaf forms were tested with one-way ANOVAs (Sokal and Rohlf, 1981
). Simple linear regressions were used to calculate the elastic modulus. All statistical tests were completed using Microsoft (Redmond, Washington, USA) Excel 2002 SP-1.
RESULTS
Mechanical measures
The mechanical behavior of the surface and aerial petioles was highly variable, as is common in many biological structures (Etnier and Vogel, 2000
; Etnier, 2001
; Vogel, 2003
). The structural stiffness (EI) of aerial petioles was significantly greater (F = 4.56, P < 0.05) than that of surface petioles (Table 1), indicating that aerial petioles deform less under a given load than surface petioles. These results are consistent with observations of lily pad petioles in nature.
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Morphology
Compared to petioles of surface leaves, petioles of aerial leaves were more elliptical (F = 6.78, P < 0.05), with a larger cross-sectional petiole area (F = 62, P < 0.01), and more lacunae (F = 7.3, P < 0.01), which were also larger in cross-sectional area (F = 18.5, P < 0.01) and relative area (F = 2.67, P < 0.01) (Table 2, Fig. 2A, B).
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Lily pad plants have a number of specialized adaptations that allow them to grow in an aquatic environment. These adaptations include a thick cuticle on the lamina, stomata limited to the adaxial surface of the lamina, large internal lacunae in most organs, lacunose parenchyma tissue throughout the plant, scattered and scant supportive tissues, and highly reduced or absent water-conducting tissues. These characteristics are not peculiar to lily pads; they are commonly present on other aquatic plants (Daubenmire, 1947
; Sculthorpe, 1967
). In addition, the core/rind arrangement of tissues seen within the petioles of lily pad leaves is a common feature of both aquatic and terrestrial plants (Niklas, 1991
, 1992
, 1995
). While the basic structure of lily pad petioles is not unusual, our results indicate that minor modifications to anatomy and/or morphology greatly change their mechanical properties, permitting them to exist in both aquatic and aerial environments.
As anticipated from field observations, the structural stiffness of aerial petioles was greater than that of surface petioles, allowing them to hold their laminae above the surface of the water. Values for both forms were within the range of values seen for other herbaceous stems (Vogel, 1992
; Ennos, 1993
; Usherwood et al., 1997
; Etnier and Vogel, 2000
; Cooley et al., 2004
; Stewart, 2004
). Both our mechanical and morphological results suggest that differences in structural stiffness are not due to differences in material properties. Nor do the materials appear to be exceptional in any way (Holbrook et al., 1991
; Niklas, 1992
; Usherwood et al., 1997
; Vogel, 2003
). Rather, differences in structural stiffness are due to differences in the distribution of materials in aerial and surface petioles, as reflected in the second moment of area. Aerial petioles are larger in diameter, with a thicker rind. In addition, aerial petioles have more subepidermal collenchyma layers and more sclereids within the rind than do surface petioles. According to beam theory (Roark, 1943
), materials that are farthest from the axis of bending will contribute the most to structural stiffness, with EI being nearly proportional to the fourth power of the average radius (Vogel, 2003
). Thus, a larger petiole, or one in which structural materials are located on the periphery, will have a greater structural stiffness (Usherwood et al., 1997
).
Interestingly, we found that some petioles actually shorten in length when initially loaded. While unusual, this behavior has been noted in abiotic materials (Lakes et al., 2001
). This odd behavior may be associated either with unusual material properties or unusual structural properties. Of note is the fact that the five petioles that behaved in this manner were more elliptical (x/y ratio) than the majority of the other petioles. While our data cannot confirm whether this factor contributed to the negative moduli, elliptical shape may be an important variable to investigate in the future. Perhaps the application of the initial load resulted in a shape change in these elliptical petioles. The biological and mechanical relevance of negative elastic moduli are as yet undetermined but of unquestionable interest.
When the structural stiffness of aerial and surface petioles is known, theoretical models can be used to determine the likelihood that the petiole will buckle under a given compression (Wainwright et al., 1976
; Niklas, 1991
). The resistance of a beam to buckling (sudden rapid deviation from vertical, producing a long-wave deformation) is proportional to structural stiffness (Schulgasser and Witztum, 1992
), so aerial petioles also have a reduced likelihood of buckling under the compressive weight of the laminae or in combination with bending moments due to the wind. Such buckling would reduce height and perhaps photosynthetic ability.
Intertidal organisms appear to take two different approaches to surviving environmental forces. Such organisms may be "strong and rigid" vs. "flexible and extensible" (Koehl, 1984
). In lily pads, both approaches are evident in the two different leaf forms. In the case of surface petioles, their length and flexibility may have several functional consequences to the plant as a whole (Sculthorpe, 1967
). The petioles may never be fully loaded by either the wind or waves, because they deform in response to the load. The long length of the petiole also shifts the lamina away from the rhizome, allowing young leaves an unobstructed route to the water's surface. Finally, the long length of the petiole allows it to remain on the surface in the face of changing water levels or water movements (Sculthorpe, 1967
).
What benefit might a strong, rigid petiole provide to the plant? In the case of aerial leaves, they appear later in the season when most of the water's surface is covered by surface leaves (S. A. Etnier and P. J. Villani, unpublished data), potentially altering the sunlight that penetrates to the submerged parts of the plant. The preponderance of surface petioles early in the season suggests that the short, robust aerial petiole is a response to shading due to overcrowding. During surface leaf maturation, laminae are initially tightly coiled, but began to uncoil and open fully before reaching the water's surface. In contrast, as the stiffer aerial petioles grow toward the surface, their laminae remain tightly coiled, thus allowing them to push past the leaves at the surface as they emerge from the water. If they opened underwater, as the surface leaves do, they would not be able to penetrate the thick mat of surface leaves. Once the leaf emerges through the surface of the water, the lamina will receive sunlight without any shading by the surface leaves.
Many plants demonstrate a shade response typified by decreases in leaf area, reduced branching, and rapid internode and petiole growth, resulting in longer and more slender plants (Holbrook et al., 1991
; Leyser and Day, 2003
). In contrast, lily pad petioles have a distinctly different developmental plasticity in response to changes in light. Aerial petioles are shorter, thicker, and subsequently stiffer in response to shading. This response allows the leaves to extend above the floating canopy of surface leaves with long, slender, and more flexible petioles.
In conclusion, we found that differences in the structure of aerial and surface petioles, rather than changes in their material composition, are responsible for the differences in their mechanical properties. We suggest that these mechanical differences are correlated with changes in the light environment due to self-shading by the surface petioles. The lily pad responds to light limitations by growing short, robust petioles that hold aerial laminae above the water's surface. While the developmental signal is as yet unknown, we suggest that lily pads may be responding to changes in the red:far red ratio, as is seen in many other plants (Smith and Whitelam, 1997
). Of particular interest in this study is that the growth pattern of the aerial form is not the typical response to light limitations, suggesting a novel approach to solving the problem of vegetational shading.
FOOTNOTES
1 The authors thank E. Holm for assistance in data collection in leech-infested waters, Dr. E. Gerecke and E. L. Etnier for critical review of the manuscript, Dr. C. Salsbury for assistance with statistical analysis, and Butler Institute for Research and Scholarship for funding of this project. This paper benefited greatly from the constructive comments of the reviewers. 
2 Author for correspondence (setnier{at}butler.edu
)
3 Authors contributed equally.
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