Article

Universal scaling of respiratory metabolism, size and nitrogen in plants

Department of Biology, Swarthmore College, Swarthmore, Pennsylvania, United States
Nature (Impact Factor: 41.46). 02/2006; 439(7075):457-61. DOI: 10.1038/nature04282
Source: PubMed

ABSTRACT

The scaling of respiratory metabolism to body size in animals is considered to be a fundamental law of nature, and there is substantial evidence for an approximate (3/4)-power relation. Studies suggest that plant respiratory metabolism also scales as the (3/4)-power of mass, and that higher plant and animal scaling follow similar rules owing to the predominance of fractal-like transport networks and associated allometric scaling. Here, however, using data obtained from about 500 laboratory and field-grown plants from 43 species and four experiments, we show that whole-plant respiration rate scales approximately isometrically (scaling exponent approximately 1) with total plant mass in individual experiments and has no common relation across all data. Moreover, consistent with theories about biochemically based physiological scaling, isometric scaling of whole-plant respiration rate to total nitrogen content is observed within and across all data sets, with a single relation common to all data. This isometric scaling is unaffected by growth conditions including variation in light, nitrogen availability, temperature and atmospheric CO2 concentration, and is similar within or among species or functional groups. These findings suggest that plants and animals follow different metabolic scaling relations, driven by distinct mechanisms.

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    • "To date, many empirical and field monitoring studies have been conducted to determine the environmental and biological controls on the NPP/GPP ratio, including temperature, precipitation , CO 2 level and plant age (Ryan, 1991; Cheng et al., 2000; Van Iersel, 2003; Reich et al., 2006; Metcalfe et al., 2010). Most studies have concluded that the NPP/GPP ratio is a fixed value independent of ecosystem type (Gifford, 1994, 1995, 2003; Ryan et al., 1994; Landsberg & Gower, 1997; Dewar et al., 1998; Waring et al., 1998) and is constant across various CO2 and temperature levels for herbaceous and woody plants (Gifford, 1994, 1995; Dewar et al., 1999; Tjoelker et al., 1999; Cheng et al., 2000). "

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    • "Additionally, some previous work (Givnish 1988; Lusk et al. 2011) initially assumed that leaf and stem gas exchange rates do not vary with tree size, but several studies have shown that this is not the case. For instance, stem-specific nitrogen concentrations and respiration rates have been shown to decline with size in seedlings and saplings (Walters et al. 1993; Tjoelker et al. 1999; Reich et al. 2006), as well as in larger trees (Sendall and Reich 2013), congruent with decreasing proportional biomass in leaves and increasing proportional biomass in wood (Reich et al. 2014). Thus, as individuals grow larger, the proportion of tissues with high respiration rates (e.g., leaves and fine twigs) declines in favor of structural support tissues with low respiration rates (e.g., coarse twigs, branches, and boles), potentially causing a decline in stem respiration rates per gram tissue and thus reducing per gram respiration rates at the whole-plant level. "
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    ABSTRACT: Although shade tolerance is often assumed to be a fixed trait, recent work suggests ontogenetic changes in the light requirements of tree species. We determined the influence of gas exchange, biomass distribution, and self-shading on ontogenetic variation in the instantaneous aboveground carbon balance of Acer saccharum. We quantified the aboveground biomass distributions of 18 juveniles varying in height and growing in low light in a temperate forest understory in Minnesota, USA. Gas exchange rates of leaf and stem tissues were measured, and the crown architecture of each individual was quantified. The YPLANT program was used to estimate the self-shaded fraction of each crown and to model net leaf-level carbon gain. Leaf respiration and photosynthesis per gram of leaf tissue increased with plant size. In contrast, stem respiration rates per gram of stem tissue declined, reflecting a shift in the distribution of stem diameter sizes from smaller (with higher respiration) to larger diameter classes. However, these trends were outweighed by ontogenetic increases in self-shading (which reduces the net photosynthesis realized) and stem mass fraction (which increases the proportion of purely respiratory tissue) in terms of influence on net carbon exchange. As a result, net carbon gain per gram of aboveground plant tissue declined with increasing plant size, and the instantaneous aboveground light compensation point increased. When estimates of root respiration were included to model whole-plant carbon gain and light compensation points, relationships with plant size were even more pronounced. Our findings show how an interplay of gas exchange, self-shading, and biomass distribution shapes ontogenetic changes in shade tolerance.
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