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Tansley Review Biological Stoichiometry of Plant Production: Metabolism, Scaling and Ecological Response to Global Change

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Tansley Review Biological Stoichiometry of Plant Production: Metabolism, Scaling and Ecological Response to Global Change New Phytologist Review Tansley review Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change Author for correspondence: J. J. Elser1, W. F. Fagan2, A. J. Kerkhoff3, N. G. Swenson4 J. J. Elser 5,6,7 Tel: +1 480 965 9747 and B. J. Enquist Email: [email protected] 1School of Life Sciences, Arizona State University, Tempe, AZ 85287, USA; 2Department of Biology, 3 Received: 19 May 2009 University of Maryland, College Park, MD 20742, USA; Department of Biology and Department of Accepted: 4 January 2010 Mathematics, Kenyon College, Gambier, OH 43022, USA; 4Department of Plant Biology, Michigan State University, East Lansing, MI 48824, USA; 5Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA; 6The Santa Fe Institute, Santa Fe, NM 87501, USA; 7Center for Applied Biodiversity Science, Conservation International, Arlington, VA 22202, USA Contents Summary 1 V. Applications: large-scale patterns and processes 9 associated with plant stoichiometry I. Introduction 2 VI. Global change and plants: a stoichiometric scaling 11 II. Variation in plant C : N : P ratios: how much and what are 3 perspective the sources? VII. Synthesis and summary 12 III. The growth rate hypothesis in terrestrial plants and the 5 scaling of whole-plant N : P stoichiometry Acknowledgements 13 and production References 13 IV. Scaling from tissues to whole plants 7 Summary New Phytologist (2010) Biological stoichiometry theory considers the balance of multiple chemical ele- doi: 10.1111/j.1469-8137.2010.03214.x ments in living systems, whereas metabolic scaling theory considers how size affects metabolic properties from cells to ecosystems. We review recent develop- ments integrating biological stoichiometry and metabolic scaling theories in the Key words: biological stoichiometry, carbon, global change, growth rate, metabolic context of plant ecology and global change. Although vascular plants exhibit wide scaling, nitrogen, phosphorus, plant size. variation in foliar carbon : nitrogen : phosphorus ratios, they exhibit a higher degree of ‘stoichiometric homeostasis’ than previously appreciated. Thus, terres- trial carbon : nitrogen : phosphorus stoichiometry will reflect the effects of adjust- ment to local growth conditions as well as species’ replacements. Plant stoichiometry exhibits size scaling, as foliar nutrient concentration decreases with increasing plant size, especially for phosphorus. Thus, small plants have lower nitrogen : phosphorus ratios. Furthermore, foliar nutrient concentration is reflected in other tissues (root, reproductive, support), permitting the development of empirical models of production that scale from tissue to whole-plant levels. Plant stoichiometry exhibits large-scale macroecological patterns, including stronger latitudinal trends and environmental correlations for phosphorus concentration Ó The Authors (2010) New Phytologist (2010) 1 Journal compilation Ó New Phytologist Trust (2010) www.newphytologist.com New 2 Review Tansley review Phytologist (relative to nitrogen) and a positive correlation between nutrient concentrations and geographic range size. Given this emerging knowledge of how plant nutrients respond to environmental variables and are connected to size, the effects of global change factors (such as carbon dioxide, temperature, nitrogen deposition) can be better understood. I. Introduction hierarchical branching of vascular networks that distribute energy and materials in organisms, including plants Plant ecophysiologists and terrestrial ecosystem ecologists (Niklas, 1994; West et al., 1997; Enquist et al., 1999; En- are confronted with the challenge of connecting simulta- quist, 2002; Price et al., 2007). West et al. (1997) showed neous changes in multiple biogeochemical cycles (e.g. rising that, based on the geometric consequences of the underly- CO2, enhanced nitrogen (N) deposition) with alterations in ing assumptions of MST, for a volume-filling network a climate (temperature, rainfall) and land use to make useful measure of total metabolic rate (Y) should scale exponen- 3 predictions about the future of plant communities and their tially with body mass (M) with an exponent of =4. functional characteristics. Many of the pieces of knowledge Although evidence for the generality of this exponent is needed for this effort are already in hand. For example, we equivocal (Muller-Landau et al., 2006; Reich et al., 2006c; know that climatic variables, such as water availability, have Enquist et al., 2007a, 2009), there is little dispute that major impacts on key traits, such as plant size and stature plant size is a key component of a plant’s life history strat- (Niklas, 1994) and rates of plant production (Huxman egy (Marba et al., 2007) et al., 2004). We know that variations in plant growth rate Connections between BST and MST have been forged in and physiological rates closely track variations in limiting a number of recent publications (Gillooly et al., 2002, nutrients (Lawlor, 1994; Van der Werf et al., 1994), and 2005; Kerkhoff et al., 2005; Niklas et al., 2005; Jeysasingh, that multiple leaf characteristics show close inter-relation- 2007; Allen & Gillooly, 2009). Allen & Gillooly (2009) ships of limiting nutrients with physiological and metabolic pointed out that, although MST and BST have generally functions (Reich et al., 1997; Wright et al., 2004, 2005). emphasized different currencies (energy and elements, Furthermore, we are beginning to gain a larger scale picture respectively), they are closely linked on three levels. First, at of how such traits are distributed in ecological communities the subcellular level, the fundamental ‘machines’ of energy and across broad geographic gradients (Wright et al., 2001; and material capture and transformation (e.g. chloroplasts, Westoby et al., 2002; Swenson & Enquist, 2007; Chave et mitochondria and ribosomes) generally have characteristic al., 2009). However, we do not yet have generalizable theo- elemental compositions. Second, at the level of the whole retical and conceptual frameworks to explicitly interconnect organism, the relationships among size, composition and key ecophysiological and ecological variables with environ- function probably depend on the relative allocation to mental features relevant to global change. In this article, we structural (e.g. bone, sclerenchyma) vs metabolically active attempt to show how recent developments in biological (e.g. muscle, palisade layer) tissues, and their respective stoi- stoichiometry theory (BST) and metabolic scaling theory chiometric compositions. In plants, structural investment is (MST) can contribute to these efforts. likely to be of some considerable importance in understand- BST involves the study of the balance of multiple chemi- ing size-dependent variation in C : nutrient ratios, as cal elements (especially carbon (C), nitrogen (N) and phos- biomechanical support involves the production of C-rich, phorus (P)) in living systems (Elser et al., 2000b; Elser & low-nutrient, low-turnover woody materials. Finally, at the Hamilton, 2007). An extension of the theory of ecological cellular, organismal and even the whole ecosystem level, stoichiometry (Sterner & Elser, 2002), BST attempts to material and energy perspectives are complementary (sensu determine the underlying physiological, cellular and molec- Reiners, 1986) in that the uptake and transformation of ular underpinnings of the organismal processing of chemi- materials and energy require both metabolic energy together cal elements, to understand their evolution and to connect with material substrates and the molecular machinery of both of these to ecosystem material flows. Although much life. By drawing explicit links between energetic and mate- of the work relevant to BST has focused on trophic inter- rial currencies across multiple levels of organization, BST actions and heterotrophic biota (crustacean zooplankton, and MST may provide an integrative framework for under- insects, bacteria), the research approach of BST also has standing how plants and vegetation systems respond to broad relevance for photoautotrophic taxa, whose global change. C : N : P ratios should also reflect their underlying bio- In this article, we attempt to further integrate recent the- chemical allocations and life history strategies (Sterner & oretical, observational and experimental work related to Elser, 2002). MST seeks to explain the observed patterns BST and MST in vascular plants. We first provide a brief of allometric scaling in terms of the geometry of the review of the environmental, size and taxonomic influences New Phytologist (2010) Ó The Authors (2010) www.newphytologist.com Journal compilation Ó New Phytologist Trust (2010) New Phytologist Tansley review Review 3 on plant C : N : P ratios and describe how stoichiometric dent, probably reflecting metabolic activity and ⁄ or invest- traits can be incorporated into MST-based approaches to ment in C-rich structural materials, it remains an open plant performance and productivity. Next, we present an question as to how environmental, developmental, genetic overview of some new and recently published macroecologi- and physiological factors interact to control variation in cal analyses of plant C : N : P stoichiometry at hemispheric plant nutrient concentration. We have identified two scales and as a function of plant dispersal strategy. We end potential contributors to the observed variation. First, by describing how these relationships relate
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