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T ECHNICAL C OMMENTS ly ontogeny, such that our model obtains inac- curate estimates of above-ground . Global Allocation Rules for We agree that SLA is an important factor in ecophysiology. However, the scaling Patterns of Biomass Partitioning differences noted by Sack et al. can be ex- plained in other, equally effective ways. For Enquist and Niklas proposed global rules for Consejo Superior example, our theory (1, 2) assumes that plant biomass allocation allometry (1). How- de Investigaciones are mature and that are the sole pho- ever, early plant ontogeny (from emergence Cientı´ficas tosynthetic organs. For most of the data we to ϳ5 g plant dry mass) follows different Post Office Box 1052 analyzed, that assumption is reasonably ac- rules than they propose, and this early stage Sevilla 41080, Spain curate; however, it is often violated during constitutes a crucial period for establishment, E-mail: [email protected] early ontogeny, when stem tissues may sig- with plant size ranging across six orders of nificantly contribute to . If magnitude. At this crucial stage, their model Peter J. Grubb stems do contribute significantly to photosyn- falls short in a number of important respects. Department of Plant Sciences thesis, our model predicts that the sum of Enquist and Niklas first suggested that total Cambridge University and stem biomass will scale in a near-isomet- ϰ ϰ 3⁄4 leaf area ML MT , where ML is standing Downing Street ric way with respect to biomass, as noted leaf dry mass and MT is total plant dry mass. In Cambridge CB2 3EA, UK by Sack et al. other words, specific leaf area (SLA), defined as E-mail: [email protected] Similarly, as we stated (1), our model as-

total lamina area/ML, remains constant. After sumes that maternal effects (such as metabolites producing their first true leaves, however, stored in endosperm or megagametophytes and References and Notes plants commonly decline dramatically in SLA 1. B. J. Enquist, K. J. Niklas, Science 295, 1517 (2002). used in early ) are negligible. (2–4). For juveniles of seven woody species 2. G. C. Evans, The Quantitative Analysis of Plant Growth If this assumption is violated, as it may be in the (Blackwell, Oxford, 1972). ranging in MT from 9 mg to 27 g, we found that case of seedling or juvenile establishment, ob- SLA ϰ M Ϫ0.22 (4). This scaling may change in 3. E. J. Veneklaas, L. Poorter, in Inherent Variation in served standing biomass relations will differ on June 4, 2016 T Plant Growth: Physiological Mechanisms and Ecolog- later ontogeny, but SLA declines further from ical Consequences, H. Lambers, H. Poorter, M. M. I. from those predicted by our model. Therefore, a saplings to trees (5, 6). Van Vuuren, Eds. (Backhuys, Leiden, Netherlands, variety of factors other than changes in SLA can Enquist and Niklas also proposed that M 1998), pp. 337-361. account for the differences in juvenile versus L 4. For seven species of woody broad-leaved evergreens, ϰ 3⁄4 ϰ 3⁄4 MS MR , where MS is stem dry mass we excavated plants in a range of sizes in the under- mature plant biomass partitioning patterns ob- and MR is root dry mass (1). For small plants, stories of three forests in southern Spain (for six of served by Sack et al. That these differences however, their model produces up to a tenfold the species, n ϭ 20 to 40; for the seventh, n ϭ 10). evoke a “tenfold error” in the predictions of our We determined allometries relating variables x and y error. The data for early ontogeny actually (i.e., log y ϭ␣log x ϩ␤), with ␣ calculated as the model for extremely small, juvenile plants is ϩ ϰ support ML MS MR—a constant shoot- reduced major axis slope (16). For each allometry, hardly surprising, but it is also somewhat mis- to-root ratio (2, 4, 7, 8)—as is predicted by different species typically had the same slope with leading. Our model identifies the functional different intercepts; we calculated common slopes. the coordinated growth of shoot and root 95% confidence intervals and R2 values were deter- allometric relations among standing leaf, stem,

ϰ http://science.sciencemag.org/ meristems (7, 9). Given MS MR, the typical mined as for least-squares regression (16). SLA scaled and root biomass (across rather than within ϰ with M , ␣ϭ-0.22 Ϯ 0.024 (R2 ϭ 0.66); shoot dry pattern is ML MT in early ontogeny (2, 4, T species) based on Model Type II regression mass scaled with root dry mass, ␣ϭ1.02 Ϯ 0.078 10, 11). 2 ϭ ␣ϭ Ϯ 2 analyses. Therefore, the magnitude of “error” in (R 0.83); MS scaled with MR, 1.10 0.085 (R Finally, Enquist and Niklas assumed that ϭ ␣ϭ Ϯ 2 ϭ one variable must be placed in the context of 0.83); ML scaled with MT, 0.97 0.052 (R ϰ 3⁄4 0.92) (17). gross photosynthesis, B, MT —an analogy the magnitude of “error” in the other variable with Kleiber’s Law—but data are insufficient 5. S. C. Thomas, F. A. Bazzaz, Ecology 80, 1607 (1999). against which it is regressed. In this regard, 6. J. Cavender-Bares, F. A. Bazzaz, Oecologia 124,8 to support this assumption for early ontoge- (2000). the “errors” referred to by Sack et al. are

ny. That pattern does fit realistic ontogenetic 7. W. H. Pearsall, Ann. Bot. 41, 549 (1927). comparable across 12 orders of magnitude Downloaded from allometries, however, if the leaf-area-based 8. C. Monk, Bull. Torrey Bot. Club 93, 402 (1966). of body size. 9. G. I. Ågren, T. Ingestad, Plant Cell Environ. 10, 579 photosynthetic rate (Parea) is stable. Parea (1987). Sack et al. also attribute to us statements that sometimes increases ontogenetically with 10. M. B. Walters, E. L. Kruger, P. B. Reich, Oecologia 96, we did not make. We explicitly stated that ac- plant size, but only slightly, as the leaf me- 219 (1993). cording to allometric theory, “the surface areas sophyll thickens (5, 6), because fewer pho- 11. D. R. Causton, J. C. Venus, The Biometry of Plant over which resources are exchanged with the Growth (Edward Arnold, London, 1981). tons penetrate additional mesophyll layers 12. T. C. Vogelmann, J. N. Nishio, W. K. Smith, Trends environment (e.g., leaf surface area, which cor- Ϫ1 ϰ ⁄4 ϰ (12). If SLA MT and ML MT, then leaf Plant Sci. 1, 65 (1996). relates with ML) are proportional to the 3/4 area ϰ M 3⁄4 and B ϰ M 3⁄4. Here, as in so 13. T. Maran˜o´n, P. J. Grubb, Funct. Ecol. 7, 591 (1993). power of the total plant biomass” [see also (3)]. T T 14. B. Shipley, R. H. Peters, Funct. Ecol. 4, 523 (1990). many processes in early establishment, SLA 15. L. Sack, P. J. Grubb, Funct. Ecol. 15, 145 (2001). It cannot escape attention that the resource ex- plays a fundamental role (13–15). 16. K. J. Niklas, Plant Allometry (Univ. of Chicago Press, change “surface areas” of leaves include inter- Lawren Sack Chicago, 1994). nalized mesophyll surface areas in contact with Department of Organismic 17. L. Sack, P. J. Grubb, T. Maran˜o´n, Plant Ecol., in press. the air. Further, as noted above, these exchange and Evolutionary Biology 11 March 2002; accepted 13 May 2002 surfaces might also include stems during early Biological Laboratories ontogeny. Thus, total exchange surface areas Harvard University Response: Sack et al. draw much-needed atten- may not be equivalent to total leaf surface area 16 Divinity Avenue tion to the difference between the allometry of as defined by Sack et al. Unfortunately, these Cambridge, MA 02138, USA early plant ontogeny and the allometry of inter- and other inaccurate statements detract from E-mail: [email protected] specific comparisons using data from mature many of the valuable points that Sack et al. individuals. Using intraspecific data for a few make. Teodoro Maran˜o´n species from closed canopy forests, where light We are nonetheless gratified that Sack et Instituto de Recursos is likely limiting, Sack et al. claim that leaf al. agree that the 3/4 scaling relation we Naturales y Agrobiologı´a properties (specifically SLA) change during ear- proposed for gross photosynthesis and total

www.sciencemag.org SCIENCE VOL 296 14 JUNE 2002 1923a T ECHNICAL C OMMENTS plant body mass fits “realistic ontogenetic less, our model accurately predicts the scal- Karl J. Niklas allometries. . .if the area-based photosynthet- ing relations among standing leaf, stem, and Department of Plant Biology ic rate. . .is stable,” noting that such rates root biomass across 12 orders of magnitude Cornell University sometimes increase “ontogenetically with of body size for monocot, dicot, and conifer Ithaca, NY 14853, USA plant size, but only slightly.” Clearly, these species growing under remarkably different observations only bolster the predictions of environmental conditions. To our knowledge, References our model. Indeed, our recent data compila- no other analytically based treatment of veg- 1. B. J. Enquist, K. J. Niklas, Science 295, 1517 (2002). 2. K. J. Niklas, B. J. Enquist, Am. Nat., in press. tions support a 3/4 scaling of whole plant etative biomass partitioning is as statistically, 3. G. B. West, J. H. Brown, B. J. Enquist, Science 284, resource use for both adult and juvenile conceptually, or mechanistically robust. 1677 (1999). plants (4, 5). Brian J. Enquist 4. B. J. Enquist, G. B. West, E. L. Charnov, J. H. Brown, Nature 401, 907 (1999). We agree with Sack et al. that allometric Department of Ecology and 5. K. J. Niklas, B. J. Enquist, Proc. Natl. Acad. Sci. U.S.A. relationships for early ontogeny may be very Evolutionary Biology 98, 2922 (2001). different as a result of a variety of factors, University of Arizona some of which we outlined in (1). Neverthe- Tucson, AZ 85721, USA 1 April 2002; accepted 13 May 2002 on June 4, 2016 http://science.sciencemag.org/ Downloaded from

1923a 14 JUNE 2002 VOL 296 SCIENCE www.sciencemag.org Global Allocation Rules for Patterns of Biomass Partitioning Lawren Sack, Teodoro Marañón and Peter J. Grubb (June 14, 2002) Science 296 (5575), 1923. [doi: 10.1126/science.296.5575.1923a]

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