Scaling of growth: plants and animals are not so different.

T relationship of body size to the anatomical, physiological, behavioral, and ecological characteristics of animals has long been a focus of interest in zoology. As one considers animal species of different sizes, regular, predictable changes are seen in the relative proportions of the body’s organs and the relative rates of physiological processes such as metabolism and growth. Students of zoology are familiar with these scaling relationships (also called allometries) and many of their ecological and adaptive implications (1–3). For example, the relative scaling of metabolism versus that of the volume of the digestive tract affects the potential diets of herbivorous mammals, which in turn influences their social behavior (4, 5). Plant biology, on the other hand, does not have a long history of investigation of issues involving the scaling of physiological processes versus body-size, despite a wealth of detailed data on plant morphology and function. This situation is perhaps because plants are seen to exhibit degrees of modular construction, indeterminate growth, and variety of form greater than those shown by animals, so the idea of a plant species even having a ‘‘body size’’ strikes some as problematical. Nevertheless, plant species do have characteristic shapes and sizes and span 20 orders of magnitude in body mass. Niklas’s 1994 book on plant allometry (6) has been described fairly as the first attempt to provide a unified treatment of plant form and function from an allometric perspective. However, until even more recently, the scaling of such basic processes as metabolism and growth had remained undocumented for a representative sample of plant species. In this issue of PNAS, Niklas and Enquist (7) present empirical scaling relationships involving the rates of plant growth in species ranging from unicellular algae to large trees. These new analyses reveal that growth scales among plants in the same way that it does among animals, and further underscores the growing realization that the same scaling rules may apply to both animals and plants, and for much the same reasons. Growth rates, or rates of production of new biomass, are of fundamental importance in linking physiological processes to adaptively important features such as reproductive rates and other life history variables (8). Among animal species, rates of biomass production and growth are proportional to metabolic rate, which scales as the 3y4 power of body mass (M; refs. 1 and 3). This proportionality, where organismal growth rate scales as M0.75, makes intuitive sense. Cells should divide or otherwise do work at rates roughly proportional to the rates at which they are supplied with energy. Across different species, these rates should be the rates of metabolism, less the energy used for physiological maintenance and ecological demands, and energy lost as heat. Previous work (9) has strongly suggested that plant nutrient f lux used for photosynthesis scales as M0.75. This result implies that plant growth rates should also scale as M0.75, a value that is confirmed by Niklas and Enquist (7). Further emphasizing this connection between plant metabolic processes and growth rates is the additional demonstration that the anatomical measures of an individual’s photosynthetic pigment volume (and thus its presumed ability to obtain energy) also scale as M0.75. It is interesting to compare the rates of growth of animals and plants over size ranges that they have in common (Fig. 1). In the Niklas and Enquist study, only the trees represent a sufficient diversity of species to permit comparison with a wide range of animal species, so only a portion of the overall body size range is shown. Although there is insufficient information here to discuss the relative efficiency of plants and animals in the conversion of energy to growth, it is clear that the realized somatic growth rates of both plants and animals of comparable body mass are remarkably similar. This finding suggests that the cells of both plants and animals are similarly limited in the rates by which they can effectuate growth, just as the abilities of different-sized plants and animals to deliver energy to their cells are similarly constrained by scaling relationships. Niklas and Enquist point out that a single linear relationship characterizes the growth allometry of all plants over the 20 orders of magnitude in plant size that they studied. True, among plants, there is no equivalent to the distinction among animal taxonomic groups between ‘‘warmblooded’’ (endothermic) and ‘‘coldblooded’’ (ectothermic) metabolic regimes. The tendency toward higher growth rates of endothermic vertebrates is evident in Fig. 1. One should not conclude, however, that variation in growth rates among plants of a similar size is either small or without biological significance. Note that the range of variation in growth rates of trees at some sizes is greater than that found among either ectothermic or endothermic vertebrates taken alone. In fact, there is some reason to believe that the full range of variation in tree growth rates is somewhat underestimated in the Niklas and Enquist dataset