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Biomechanics of the Columnar Cactus Pachycereus Pringlei1

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Biomechanics of the Columnar Cactus Pachycereus Pringlei1 American Journal of Botany 86(6): 767±775. 1999. BIOMECHANICS OF THE COLUMNAR CACTUS PACHYCEREUS PRINGLEI1 KARL J. NIKLAS,2 FRANCISCO MOLINA-FREANER,3 AND CLARA TINOCO-OJANGUREN3 2Section of Plant Biology, Cornell University, Ithaca, New York 14853; and 3Instituto de Ecologia UNAM, Apartado Postal 1354, Hermosillo, Sonora CP 83000, Mexico We report the longitudinal variations in stiffness and bulk density of tissue samples drawn from along the length of two Pachycereus pringlei plants measuring 3.69 and 5.9 m in height to determine how different tissues contribute to the me- chanical stability of these massive vertical organs. Each of the two stems was cut into segments of uniform length and subsequently dissected to obtain and mechanically test portions of xylem strands, stem ribs, and a limited number of pith and cortex samples. In each case, morphometric measurements were taken to determine the geometric contribution each tissue likely made to the ability of whole stems to resist bending forces. The stiffness of each xylem strand increased basipetally toward the base of each plant where stiffness sharply decreased, reaching a magnitude comparable to that of strands 1 m beneath the stem apex. The xylem was anisotropic in behavior, i.e., its stiffness measured in the radial and in the tangential directions differed signi®cantly. Despite the abrupt decrease in xylem strand stiffness at the stem base, the contribution made by this tissue to resist bending forces increased exponentially from the tip to the base of each plant due to the accumulation of wood. A basipetal increase in the stiffness of the pith (and, to limited extent, that of the cortex) was also observed. In contrast, the stiffness of stem rib tissues varied little as a function of stem length. These tissues were stiffer than the xylem in the corresponding portions of the stem along the upper two-®fths of the length of either plant. Tissue stiffness and bulk density were not signi®cantly correlated within or across tissue types. However, a weak inverse relationship was observed for these properties in the case of the xylem and stem rib tissues. We present a simple formula that predicts when stem ribs rather than the xylem strands serve as the principal stiffening agents in stems. This formula successfully predicted the observed aspect ratio of the stem ribs (the average quotient of the radial and tangential dimensions of rib transections), and thus provided circumstantial evidence that the ribs are important for mechanical stability for the distal and younger regions of the stems examined. Key words: biomechanics; Cactaceae; mechanical stability; plants; stems; tissue density; tissue stiffness; wood; Young's modulus. The relationship between the mechanical and anatom- The stems of columnar cacti are ideal organs with ical properties of plant tissues has been the subject of which to empirically study the relationship between anat- considerable speculation because it is evident that, aside omy and tissue stiffness because of their tall, compara- from their physiological functions, every tissue type con- tively sparsely branched and woody growth habit, the tributes in some way to the mechanical behavior of or- persistence of pith and cortex in older portions of stems, gans (Schwendener, 1874; Carlquist, 1961, 1969, 1975; and the presence of vascular strands that, despite the ac- Wainwright et al., 1976; Niklas, 1992; Speck, 1994; cumulation of secondary tissues, remain slender and Spatz et al., 1995). A number of factors in¯uence the largely unconnected to neighboring strands (Gibson, mechanical properties of each tissue type, but prior stud- 1978; Mauseth, 1988; Mauseth and Plemons, 1995; Mau- ies suggest that stiffness is positively correlated with the seth et al., 1995). These and other features provide an volume fraction of cell wall materials (and thus speci®c opportunity to remove nearly untapered cylindrical sam- gravity and density), especially among the secondary tis- ples of xylem and other tissue types from different lo- sues (Forsaith, 1926; Record, 1934; Seibt, 1964; see cations along the length of stems, test these samples in Esau, 1967), and with water content and thus turgor, es- bending to determine their stiffness, assess whether lon- pecially among the primary tissues (Falk, Hertz, and Vir- gitudinal gradients in this property exist, and evaluate gin, 1958; Niklas, 1992). However, comparatively few whether observed gradients correlate with anatomical studies have addressed these relationships experimentally variations. in quantitative terms. In this paper we present the ®rst phase of this research agenda by reporting the longitudinal variations in the 1 Manuscript received 21 August 1998; revision accepted 21 Decem- stiffness of tissue types surgically removed from different ber 1998. The authors thank Prof. James D. Mauseth (University of Texas) who locations along the length of Pachycereus pringlei stems. acted as Editor-in-Chief during the review process; two anonymous re- This species is the most massive plant in the Sonoran viewers who made constructive recommendations to improve an earlier Desert, reaching heights of 15±20 m and producing stems draft; the owners of El Sacri®cio who provided access to their property; up to 1.5 m in diameter (Turner, Bawers, and Burgess, Ivan Romo for logistical support; Conrado Velenzuela, Oscar Gutierrez, 1995). It was selected for study because of the availabil- Mauricio Cervantes, Grethel Ramirez, Martin Villegas, and Daniel Mo- rales for assistance in the ®eld. Field work was supported by funds from ity of specimens differing in size and thus presumably the operating budget of the Instituto de Ecologia UNAM to FMF and age. It was also selected because of its growth habit, CTO. which permits a comparatively straightforward biome- 767 768 AMERICAN JOURNAL OF BOTANY [Vol. 86 chanical interpretation. The cactus ranges from sea level study from this locality because of their size and healthy appearance. to 950 m and grows mainly in areas dominated by warm- These plants measured 3.69 and 5.89 m in height and are denoted season rainfall, with the exception of central Baja Cali- throughout this paper as plants 1 and 2, respectively (Fig. 1A, B). Ad- fornia where it can be found in areas of mainly winter ditional specimens were examined during the course of our ®eld inves- rainfall (Shreve, 1964; Turner, Bowers, and Burgess, tigations to determine patterns of self loading, especially on lateral 1995). Since individual stems are unbranched and since branches. plants are severely damaged or killed by frost, the bio- The stems of plants 1 and 2 were sectioned to obtain representative mechanics of P. pringlei is not likely to be adapted to transections (Fig. 1C) measuring a few centimetres in length and seg- transient snow or ice loadings. Finally, although the xy- ments of equivalent lengths (1.1 and 1.18 m for plants 1 and 2, respec- lem strands of old plants become interconnected near the tively) for mechanical study (Fig. 1D±F). Three segments comprising base of stems, they are only modestly laterally intercon- the stem of plant 1 were designated ``bottom,'' ``middle,'' and ``top''; nected to adjoining strands along much of the length of ®ve segments from plant 2 were assigned letters A to E in an acropetal even very massive and tall stems. These xylem strands direction starting from the base of the stem. In addition to these stems, a representative curved lateral branch on plant 2 measuring 2.12 m in are thus easily removed from ground tissues, and seg- length was studied. This branch was cut into two segments designated ments differing in position with respect to stem height ``B'' and ``T'' (for bottom and top), each measuring ;0.93 m in length. can be tested in bending to determine how stiffness varies Stem segments were dissected either in the ®eld or laboratory to along stem length. remove their xylem strands, which contained secondary tissues in all In this paper we show that the stiffness of the xylem cases, from surrounding ground tissues. During this process, the smaller increases in a basipetal direction toward the base of lateral strands that interconnected the main strands were purposely bro- young and old stems but sharply decreases ;1 m above ken and removed to produce beam-like specimens for mechanical tests ground level to a level comparable to that found just be- (see Fig. 1D±E). On average, 12 of these specimens in excess of 1 m low the stem tip. In terms of their per unit volume con- long were successfully removed from each of the three stem segments tribution to the ability of stems to resist bending forces, of plant 1 and tested in bending. Between 7 and 15 beam-like specimens the xylem strands of P. pringlei are ill equipped to cope in excess of 1 m long were removed from each of the ®ve stem seg- with the potentially large bending forces that can occur ments of plant 2 and tested in bending. A smaller number of vascular in the base of stems. However, we demonstrate that the bundle specimens was sampled from segment A of plant 2 because the geometric contribution made by the xylem to the ability xylem strands in the base of this segment were laterally fused together of stems to resist bending forces increases sharply at the in various combinations such that a beam-like sample for each xylem base of plants. Consequently, the amount of xylem at the strand could not be obtained. Finally, between 9 and 15 xylem strand base of stems more than compensates for its low stiffness. specimens were removed from the lateral branch of plant 2 re¯ecting We also demonstrate that the stem ribs running much of the fact that some of the branch strands broke during the process of the length of even old and tall stems contribute signi®- dislodging the branch from its main stem.
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