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Department of Organismic Biology, Ecology and Evolution, University of California, Los Angeles, California 90095-1606 USA
Received for publication January 4, 2000. Accepted for publication June 8, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: biomechanics • Cactaceae • cladode • cladode junction • hybrid • libriform fibers • Opuntia • vascular tracheids • vessel elements
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). In the Cactaceae, prominent examples of sympodial axes are found in the genus Opuntia, for which photosynthetic branch units are either cylindrical (cylindropuntias) or flattened (platyopuntias; Gibson and Nobel, 1986
). A common characteristic of both cylindrical and flattened stem segments, referred to as joints and cladodes, respectively, is that they are smaller in cross section at their bases (Gibson and Nobel, 1986
; Nobel and Meyer, 1991
). For instance, junctions between cladodes along a branch of Opuntia ficus-indica have a cross-sectional area equal to 22% of the area at mid- cladode (Nobel and Meyer, 1991
).
A woody dicotyledon branch can resemble a tapered cantilever, with a greater cross-sectional area at the fixed end of the branch compensating for the local increase of tensile and compressive forces when the branch is subjected to applied forces (Mosbrugger, 1990
; Niklas, 1992
). In platyopuntias, forces due to applied loads are concentrated in relatively small cross-sectional areas of the cladode junctions, which could contribute to a local mechanical weakness and possibly lead to stem failure (Gibson and Nobel, 1986
; Nobel and Meyer, 1991
). Therefore, the ability of cladode junctions to resist mechanical failure was hypothesized to depend on the cross-sectional area of the junctions. Because detached Opuntia stems have the ability to root (Gibson and Nobel, 1986
), such mechanical failure of the cladode junctions could facilitate vegetative reproduction (Grant and Grant, 1980
; Mandujano, Montaña, and Eguiarte, 1996
; Mandujano et al., 1998
).
Platyopuntia wood is generally composed of fibrous axial regions produced by fascicular vascular cambium and poorly lignified, or unlignified, vascular rays produced by interfascicular cambium (Gibson, 1976, 1978
; Gibson and Nobel, 1986
). However, variation occurs in wood characteristics among platyopuntias, especially for the amount of fibers in the axial regions (Gibson, 1978
). Furthermore, wood composition in the Cactaceae can change during development (Gibson, 1973
; Mauseth and Plemons, 1995
), e.g., trunks of Browningia candelaris have fibrous wood at maturity while its branches have fibrous wood early in development and nonfibrous wood at maturity (Mauseth, 1993
). Preliminary observations have revealed that only wood, pith, and phloem of cladode junctions directly connect the older cladodes to the younger cladodes for Opuntia ficus-indica. The preponderance of wood in the cladode junction led to the hypothesis that the constituents of such wood affect branch deflection and the ability of the cladode junctions to resist mechanical failure.
Hybridization has long been recognized among platyopuntias in southern California (Philbrick, 1963
; Benson and Walkington, 1965
; Goeden, Fleschner, and Ricker, 1967
). An interesting case involves the introduced, arborescent, agricultural species Opuntia ficus-indica and the native, low, shrubby species Opuntia littoralis. Progeny of this hybridization can vary morphologically between putative F1 hybrids and O. littoralis backcrosses and are referred to as Opuntia "occidentalis" (Benson and Walkington, 1965
; Benson, 1982
). In the southern California chaparral where platyopuntias occur, the fire frequency has changed due to human disturbances and the arrival of Mediterranean grasses (Mensing, 1998
; Keeley, Fotheringham, and Morais, 1999
). Although fire is detrimental to most cacti (Nobel, 1988
), populations of O. "occidentalis" are often able to survive fires because it forms large thickets due to vegetative reproduction, unlike its putative parents, and only the outer plants are damaged (Gibson and Nobel, 1986
). Cladode detachment caused by failure at cladode junctions and leading to vegetative reproduction may be caused by passing animals, extreme environmental conditions, or extensive self- loading due to biomass accumulation. The greater ability of O. "occidentalis" to reproduce vegetatively compared with O. ficus-indica and O. littoralis was hypothesized to reflect the biomechanical and anatomical properties of the cladode junctions of the three taxa. Also, because different Opuntia growth forms have different types of wood and wood development (Gibson, 1978
), it is further hypothesized that the hybridization of O. ficus-indica and O. littoralis may have led to different wood characteristics in O. "occidentalis." The present study therefore investigated biomechanical properties and cellular anatomy of the cladode junctions for O. ficus-indica, O. littoralis, and O. "occidentalis." Cellular wood composition, wood development, and measurements of wood elements with secondary cell walls were interpreted with respect to biomechanics and vegetative reproduction for each taxon.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Biomechanical and morphological measurements
Deflections caused by incrementally increased masses applied perpendicularly to the face of the younger cladode of each cladode junction were determined for seven branches of each taxon analyzed in the order of terminal, subterminal, and then sub- subterminal junction. The masses that caused failure of each of the junctions were determined. Branches were held in place using two wooden clamps bolted to a rigid scaffold and covered with 10 mm of rubber foam to prevent damaging the cladodes (Fig. 1). The upper clamp was placed 10 mm below the cladode junction being analyzed, with the younger cladode oriented vertically, and the lower clamp was used to help immobilize the branch (Nobel and Meyer, 1991
). Forces were applied to the upper cladode using a steel wire attached to a 7-mm-diameter j-bolt that was placed through the cladode center of mass and secured with nuts, washers, and rubber foam padding (Nobel and Meyer, 1991
; Fig. 1). Preliminary measurements indicated that the center of mass of the upper cladodes for all three taxa was 40% of the distance from the base to the tip of a cladode. The steel wire passed over a low-friction pulley adjusted so that the applied forces were always perpendicular to the face of the upper cladode (Fig. 1). Linear deflections were read on a scale with millimetre gradations mounted directly above the upper cladode, which had a fine steel needle inserted into its apex (Fig. 1). The deflection angle was calculated as sin-1 (linear deflection/cladode length; Nobel and Meyer, 1991
).
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; Niklas, 1992
), was calculated from the semi- minor axis (a, in direction of applied bending moment) and the semi-major axis (b) of the junction area that included the wood, pith, and phloem, using the following equation: I/a = 
a2b/4, where I is the second moment of area.
Tissue preparation and cell measurements
Samples for sectioning were taken from the terminal and the sub-subterminal cladode junctions of four branches for each taxon. After the epidermis, hypodermis, and areoles had been removed with a razor blade, terminal and sub-subterminal junctions were cut into four 90° sectors and eight 45° sectors, respectively. The sectors were then fixed in formalin, acetic acid, and ethyl alcohol (FAA) and dehydrated through a tertiary butanol series (Jensen, 1962
). Once embedded in Paraplast Plus (Oxford Labware, St. Louis, Missouri, USA), sections 
15 µm thick were prepared using a rotary microtome with a 12-cm blade (Leica Instruments, Heidelberg, Germany). The sections were stained using safranin as the primary stain and fast green as the counter stain (Jensen, 1962
).
Digital images of the cross-sections at 200x were obtained using an Olympus BH-2 light microscope (Lake Success, New York, USA) and a digital image analysis system (Pixera Corporation, Los Gatos, California, USA). Measurements of cell wall thickness and the cross-sectional area of cells with secondary cell walls were recorded from the images using Image Pro Plus (Media Cybernetics, Silver Spring, Maryland, USA). Mean external cell diameter was calculated for vessels, libriform fibers, and vascular (wide-band) tracheids (Gibson, 1973, 1978
; Mauseth, 1995
) from the cell cross-sectional area of 150 cells for each junction; mean cell wall thicknesses of these cells were determined from the average of three measurements per cell. The numbers of vessels, libriform fibers, and vascular tracheids per unit area were determined for two entire sectors of terminal junctions and for four entire sectors of sub-subterminal junctions.
The lengths of vessel elements, libriform fibers, and vascular tracheids were determined from macerations of 5-mm-thick tissue samples from four sub- subterminal cladode junctions of each taxon. Tissue samples were immersed in Jeffrey's solution (10% chromic acid and 10% nitric acid) at 40°C (Berlyn and Miksche, 1976
). After 24 h, a sample was removed, washed with distilled water, affixed to slides, and stained with safranin. Cell lengths were measured from digital images taken at 30x for libriform fibers or at 100x for vessel elements and vascular tracheids and recorded using Image Pro Plus.
Statistical analyses were performed using SigmaStat (Jandel Corporation, San Rafael, California, USA). All means are presented with standard errors.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Vascular tracheids occurred only in the wood of O. littoralis and O. "occidentalis." These cells were fusiform, having two to six annular secondary thickenings along their length, and were arranged in radial files bordering the metaxylem, in the axial xylem, and adjacent to the axial xylem in the rays (Fig. 7). The vascular tracheids in the rays had a greater diameter than did those of the axial xylem. Adjacent vascular tracheids often had an interlocking appearance due to the positions of the annular bands, which usually alternated (Fig. 10).
The average number of cell types per square millimetre differed between terminal and sub-subterminal cladode junction wood. Vessel frequencies in junction wood decreased 30–45% from terminal to sub-subterminal junctions (Table 2). Libriform fibers were absent in terminal junction wood for O. ficus- indica and nearly absent for O. littoralis and O. "occidentalis" (Table 2). The libriform fiber frequency in sub-subterminal junction wood was 5 times greater than the vessel frequency for O. ficus-indica, about the same for O. littoralis, but only one-third as much for O. "occidentalis" (Table 2). Vascular tracheids were absent from terminal and sub-subterminal junctions of O. ficus-indica (Table 2). Vascular tracheid frequency increased 114% from terminal to sub-subterminal junction wood for O. littoralis but decreased 62% for O. "occidentalis," reflecting the lack of vascular tracheids in the outer half of sub-subterminal junctions of O. "occidentalis." Comparisons among the three taxa showed that O. ficus-indica averaged only 42% as many vessels per square millimetre in terminal and sub-subterminal junctions as the other two taxa (Table 2). However, libriform fibers in sub-subterminal junctions of O. ficus-indica were 2.0 times more frequent than for O. littoralis and 7.0 times more frequent than for O. "occidentalis" (Table 2). Vascular tracheids in terminal junctions and sub-subterminal junctions were common only for O. littoralis (Table 2).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Molina-Freaner, Tinoco- Ojanguren, and Niklas, 1998
), any increases in cladode junction wood production should increase the section modulus, and, consequently, the junction strength for O. ficus-indica, O. littoralis, and their hybrid O. "occidentalis." Cladode mass, junction cross-sectional area, the wood cross-sectional area, and the section modulus of such junctions were greater for the arborescent O. ficus-indica than for the frutescent O. littoralis and O. "occidentalis." This is consistent with the trend for platyopuntias that plant height is proportional to wood accumulation (Gibson, 1978
). Although cladode mass and junction area did not differ between O. littoralis and O. "occidentalis," the junction wood area averaged 70% greater and the section modulus averaged 210% greater for O. littoralis than those for O. "occidentalis." Also, the ratios of wood area to junction area for O. ficus-indica and O. littoralis, while similar to each other, were greater than the ratios for O. "occidentalis," again indicating that the hybrid produced less junction wood and thus had a smaller region resisting bending moments.
Many allometric relationships describing plant structure are logarithmic (Niklas and Buchman, 1994
; Niklas, 1997
), as are the relationships between the applied breaking mass of cladode junctions and the junction wood area, and the critical bending moment and the section modulus for the three platyopuntias considered. The increase for log (breaking mass) with log (wood area) averaged 54% greater for O. ficus-indica than for O. littoralis and O. "occidentalis"; the increase for log (critical bending moment) with log (section modulus) for O. ficus- indica averaged 29% greater than for O. littoralis and 78% greater than for O. "occidentalis." Not only was the resistance to junction failure correlated with plant height but also the junction of the hybrid did not increase in strength as much with age as did the junctions of its parents. The resistance to angular deflection of cladodes depended on junction wood area, with O. ficus-indica deflecting the least per applied mass and per bending moment, and O. "occidentalis" deflecting the most. Increases in junction wood area and, consequently, section modulus from terminal to sub-subterminal junctions influenced the angle of cladode deflection prior to junction failure for O. littoralis and O. "occidentalis" but not for O. ficus- indica.
Cellular contributions to stem strength can change with the age of the wood, especially for polymorphic woods in the Cactaceae (Gibson, 1973, 1978
; Mauseth and Plemons, 1995
). The wood of terminal, subterminal, and sub-subterminal cladode junctions for the three taxa consisted mostly of parenchyma, suggesting that the strength of the junctions depended on the hydrostatic pressure of the parenchyma cells (Niklas, 1992
). The contribution of the parenchyma apparently decreased from terminal junctions to sub-subterminal junctions because the proportion of cells with secondary cell wall thickenings increased with junction age, especially for O. ficus- indica and O. littoralis. A similar cellular phenomenon may explain the stiffening of wood in Carnegiea gigantea as plants increase in height (Niklas and Buchman, 1994
). The ability to resist junction failure appeared to correlate with wood type, with the diffuse-porous wood of O. ficus-indica being more resistant than the ring-porous woods of O. littoralis and O. "occidentalis." However, these differences are more likely dependent on the properties of the cell types present rather than on the size and distribution of the vessels in the wood.
Libriform fibers contribute to support and resist bending moments (Fahn, 1990
). Although libriform fibers were virtually absent from terminal junctions of O. ficus-indica, O. littoralis, and O. "occidentalis," additional biomass due to the production of daughter cladodes probably was a signal for fiber production (Gibson, 1978
), explaining the occurrence of the fibers in their sub-subterminal junctions. Sclerenchyma, which often includes libriform fibers, is more resistant to elastic deformation than is parenchyma (Niklas, 1993
). Thus libriform fibers in sub-subterminal junctions can support the mass of the cladodes distal to the junction with a smaller amount of area than would parenchyma. As in other platyopuntias, libriform fibers for O. ficus-indica, O. littoralis, and O. "occidentalis" were longer than the two other cell types investigated (vessel elements and vascular tracheids). The greater length of libriform fibers is due to intrusive growth (Gibson, 1978
), which creates extra contact between cell walls in the clusters of fibers. This cell wall contact, along with the lignification of the middle lamellae, prevents the fibers from shearing past each other, making the clusters of fibers act as a unit when resisting bending moments. Moreover, secondary cell walls of libriform fibers were thickened along the length of a cell, indicating that fiber cell walls were more resistant to deformation due to tensile or compressive forces than if the walls were reticulately, helically, or annularly thickened (Carlquist, 1975
). Therefore, the properties of libriform fibers indicate that the greater their frequency in the junction wood, the stronger the wood, as is shown by the greater resistance of O. ficus-indica and O. littoralis compared with O. "occidentalis."
Reaction wood in stems forms in response to a gravitational stimulus and acts to orient them vertically (Fahn, 1990
; Gartner, 1995
). A distinguishing feature of reaction wood in dicotyledons, which is referred to as tension wood, is the presence of gelatinous fibers, which have an inner gelatinous layer in the secondary cell wall that has little or no lignin and that often separates from the rest of the wall during sectioning (Satiat-Jeunemaitre, 1986
; Fahn, 1990
). Because the libriform fibers in the junction wood of the three taxa investigated had these characteristics and cladodes are rarely perfectly vertical, the libriform fibers most likely aid in orienting cladodes vertically and the junction wood of these three taxa is apparently tension wood. However, further research is necessary to describe the development of reaction wood in cladode junctions of platyopuntias.
The contributions of vessel elements and vascular tracheids to junction strength are less apparent than the contributions of libriform fibers. The strength of vessel elements usually increases with increasing secondary cell wall thickening (Carlquist, 1975
). Thus the vessel elements of O. ficus-indica, which were larger and had greater thickening of the secondary cell walls, should be stronger than those of O. littoralis and O. "occidentalis." However, vessel elements are probably weaker than libriform fibers because the amount of cell wall thickening per lumen area for vessel elements is less than that of libriform fibers.
Vascular tracheids are common in shrubby and caespitose forms of the Cactaceae, but are absent in taller growth forms (Gibson, 1973, 1978
). In polymorphic woods they are seldom produced after the appearance of fibers (Gibson, 1978
; Mauseth and Plemons, 1995
), suggesting that they do not provide much support. Because vascular tracheids interlock due to their annular secondary thickenings, they may provide resistance against shearing stresses resulting from bending forces in the junction, preventing vascular tracheids and adjacent parenchyma from sliding past each other. Vascular tracheids are also located close to the center of the junction where shearing stresses are maximal (Niklas, 1992
). The greater frequency of vascular tracheids in the junction wood of O. littoralis than in that of O. "occidentalis" may then explain why, along with greater wood area, O. littoralis cladodes showed greater resistance to angular deflection about their respective junctions than did those of O. "occidentalis."
Vegetative reproduction by the rooting of detached branches can increase the ground area covered by platyopuntias (Grant and Grant, 1980
; Gibson and Nobel, 1986
; Mandujano et al., 1998
). For O. "occidentalis," detached branches with two to five cladodes rooted more often than single cladodes; the larger branches probably had more water and stored carbohydrates, which could enable them to survive drought better. Only 9% of detached branches had four or more cladodes, indicating that failure for junctions older than sub-subterminal junctions is unlikely. The ability to form large thickets by vegetative reproduction gives O. "occidentalis" a selective advantage over its putative parents, because these thickets are able to survive the fires in the chaparral of southern California (Benson and Walkington, 1965
; Gibson and Nobel, 1986
). Although there are many morphological variants as a result of the repeated hybridization between the introduced arborescent O. ficus-indica and the native shrubby O. littoralis, the hybrid types believed to dominate the chaparral are backcrosses with O. littoralis (Benson and Walkington, 1965
). Because O. littoralis and the O. "occidentalis" of this study were similar in cladode mass and junction area and both taxa had ring-porous wood, this O. "occidentalis" probably represents much of the platyopuntia hybrid population in the local chaparral.
Although morphological and anatomical evidence describes how O. "occidentalis" junctions can fail mechanically, what causes the junction to fail in nature is not fully known. Perturbations by coyotes and small mammals of the region may cause junction failure. Wind has been previously shown to have little effect on the deflection of O. ficus-indica (Nobel and Meyer, 1991
), but wind effects may be different for lower growth forms of platyopuntias that have weaker junction wood. The most likely junction failure may occur when a branch or individual cladode is at a large angle from the vertical, providing a bending moment due to gravity that is large enough to cause stress fractures in the wood, thus gradually weakening the wood until it either fails under its own mass or by other forces.
In summary, the traits of the cladode junction wood of O. "occidentalis" caused their junctions to be weaker than those of O. ficus-indica and O. littoralis. These traits included a decreased amount of wood compared to junctions of O. ficus-indica and O. littoralis. The junction wood of O. "occidentalis" also had fewer libriform fibers, cells that offer the most support and resistance to bending moments, than both parents and fewer vascular tracheids than O. littoralis, which probably decreased the amount of shear between cells in the wood. These traits, which could be deficiencies for the hybrid in another environment, probably have contributed to the enhanced ability of O. "occidentalis" to form dense thickets in the local chaparral compared to its parents, O. ficus-indica and O. littoralis.
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FOOTNOTES |
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2 Author for reprint requests (psnobel{at}biology.ucla.edu
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Benson, L. 1982 The cacti of the United States and Canada. Stanford University Press, Stanford, California, USA
———, and D. L. Walkington. 1965 The southern California prickly- pears—invasion, adulteration, and trial by fire. Annals of the Missouri Botanical Garden 52: 262–273[CrossRef]
Berlyn, G. P., and J. P. Miksche. 1976 Botanical microtechnique and cytochemistry. Iowa State University Press, Ames, Iowa, USA
Carlquist, S. 1975 Ecological strategies of xylem evolution. University of California Press, Berkeley, California, USA
Fahn, A. 1990 Plant anatomy, 4th ed. Pergamom, Elmsford, New York, USA
Gartner, B. L. 1995 Patterns of xylem variation within a tree and their hydraulic and mechanical consequences. In B. L. Gartner [ed.], Plant stems: physiology and functional morphology, 125–149. Academic Press, San Diego, California, USA
Gibson, A. C. 1973 Comparative anatomy of secondary xylem in Cactoideae (Cactaceae). Biotropica 5: 29–65[CrossRef]
———. 1976 Vascular organization in shoots of Cactaceae. I. Development and morphology of primary vasculature in Pereskioideae and Opuntioideae. American Journal of Botany 63: 414–426[CrossRef][ISI]
———. 1978 Wood anatomy of platyopuntias. Aliso 9: 279–303
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Goeden, R. D., C. A. Fleschner, and D. W. Ricker. 1967 Biological control of prickly pear cacti on Santa Cruz Island, California. Hilgardia 38: 579–606[ISI]
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———. 1995 Structural and systematic study of an unusual tracheid type in cacti. Journal of Plant Research 108: 517–526[CrossRef][ISI]
———, and B. J. Plemons. 1995 Developmentally variable, polymorphic woods in cacti. American Journal of Botany 82: 1199–1205[CrossRef][ISI]
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———. 1993 Influence of tissue density-specific mechanical properties on the scaling of plant height. Annals of Botany 72: 173–179
———. 1997 The evolutionary biology of plants. Universtiy of Chicago Press, Chicago, Illinois, USA
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