Testing the Growth Rate Hypothesis in Vascular Plants with Above-And

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Testing the Growth Rate Hypothesis in Vascular Plants with Above-And Testing the Growth Rate Hypothesis in Vascular Plants with Above- and Below-Ground Biomass Qiang Yu1,2*, Honghui Wu1,2, Nianpeng He3, Xiaotao Lu¨ 1,2, Zhiping Wang2, James J. Elser4, Jianguo Wu4,5, Xingguo Han1,2* 1 State Key Laboratory of Forest and Soil Ecology, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, China, 2 State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing, China, 3 Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing, China, 4 School of Life Sciences, Arizona State University, Tempe, Arizona, United States of America, 5 Sino-US Center for Conservation, Energy and Sustainability Science (SUCCESS), Inner Mongolia University, Hohhot, Inner Mongolia, China Abstract The growth rate hypothesis (GRH) proposes that higher growth rate (the rate of change in biomass per unit biomass, m)is associated with higher P concentration and lower C:P and N:P ratios. However, the applicability of the GRH to vascular plants is not well-studied and few studies have been done on belowground biomass. Here we showed that, for aboveground, belowground and total biomass of three study species, m was positively correlated with N:C under N limitation and positively correlated with P:C under P limitation. However, the N:P ratio was a unimodal function of m, increasing for small values of m, reaching a maximum, and then decreasing. The range of variations in m was positively correlated with variation in C:N:P stoichiometry. Furthermore, m and C:N:P ranges for aboveground biomass were negatively correlated with those for belowground. Our results confirm the well-known association of growth rate with tissue concentration of the limiting nutrient and provide empirical support for recent theoretical formulations. Citation: Yu Q, Wu H, He N, Lu¨ X, Wang Z, et al. (2012) Testing the Growth Rate Hypothesis in Vascular Plants with Above- and Below-Ground Biomass. PLoS ONE 7(3): e32162. doi:10.1371/journal.pone.0032162 Editor: Dorian Q. Fuller, University College London, United Kingdom Received September 15, 2011; Accepted January 21, 2012; Published March 13, 2012 Copyright: ß 2012 Yu et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported by the National Natural Science Foundation of China (NSFC, 31170434) and the Key Project of NSFC (30830026). N. He acknowledges support from the Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering (K0802). J. Elser and J. Wu acknowledge support from the National Science Foundation (DEB-0618193). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] (QY); [email protected] (XH) Introduction stoichiometric concept in evolutionary studies [3,15,16], providing a unifying thread connecting genes to ecosystems. The GRH has Carbon (C), nitrogen (N) and phosphorus (P) are very important been intensively tested and generally supported via both elements for living organisms [1]. Their relative use in biomass (i.e. theoretical and empirical analysis in zooplankton, arthropods, their C:N:P stoichiometry) reflects a complex interplay of and bacteria [3,16–20]. However, the applicability of the evolutionary processes [2] coupled to phenotypic plasticity that is driven by patterns of element supply from the environment or hypothesis to photoautotrophs is not entirely clear, especially diet. Thus, it is increasingly recognized that the values and ranges given the fact that storage materials in plants may obscure the of C:N:P ratios in an organism are important determinants of the associations between C:N:P stoichiometry and growth rate ecological niche. Indeed, C:N:P stoichiometry, and especially N:P [1,21,22]. So, it is not clear whether the relationships between ratio, is a powerful factor underlying diverse ecological processes growth rate and C:N:P observed in the world of bacteria and [3], such as population stability [4], competitive interactions [5], zooplankton would also be observed for plants. community organization [6], trophic dynamics [7], litter decom- Diverse comprehensive reviews have shown that foliar N position [8,9], nutrient limitation [10,11], and biogeochemical content in vascular plants tends to increase less than proportion- cycling [12]. Thus, it is important to understand the underlying ately with P content [23–27]; thus, nutrient-rich foliage tends to biological factors that drive observed variation in C:N:P ratios in have low N:P ratio, suggesting that the GRH has validity in the organisms. realm of vascular plants. However, not all studies in plants provide Considerable recent work has proposed specific connections consistent support for the GRH. For example, Matzek and between C:N:P stoichiometry and growth rate [1]. Growth rate is Vitousek’s data for pine species showed that it was plant a central integrating parameter of overall life history strategy [13] protein:RNA ratio but not foliar N:P ratio that was significantly and is closely linked to fitness [14]. Initiated from the study of correlated (negatively) with growth rate [28]. Thus, the interac- crustacean zooplankton, the growth rate hypothesis (GRH) tions between N:P stoichiometry and growth rate require further proposes that fast-growing organisms have low biomass C:P and study. N:P ratios [1,3] because of differential allocaiton to P-rich A˚ gren proposed to adapt the GRH to plants via a quantitative ribosomal RNA. By integrating ecological consequences with model of relationship between growth rate (m) and N:C (RN:C), P:C cellular and genetic mechanisms, the GRH broadened the use of (RP:C), N:P (RN:P) with the following four equations [21]: PLoS ONE | www.plosone.org 1 March 2012 | Volume 7 | Issue 3 | e32162 C:N:P and Growth Rate of Vascular Plants plants [21]. However, the relationship between N:P and growth m rate is unclear. Only a few experiments have tested the GRH in RN:C ~ zbN ð1Þ hCN vascular plants [21,22,28,29], especially under both N- and P- limited conditions [21,22]. Unfortunately, even among those limited studies, the results are mixed. N:P ratio of birch seedlings m2 decreased with m when P was limiting but increased with m when ~ z RP:C bP ð2Þ N was limiting [21], suggesting the relationship between N:P and hCN hNP m varies considerably under different nutrient conditions. Consistent with A˚ gren’s theory, Cernusak et al. [29] found that mh zb h h seedlings of 13 tropical tree and liana species showed hump- R ~ NP N CN NP N:P 2 ð3Þ shaped relationships between N:P ratio and the relative growth m zbPhCN hNP rate. However, Matzek and Vitousek [28] found no relationship between m and N:P in greenhouse experiments across 14 species. b 1 Furthermore, most studies have focused only on foliage and ~ Nri 2z z or RN:P m m bN ð4Þ above-ground biomass. To our knowledege, no study has been hCN hNP hCN done to test the relationship between root C:N:P stoichiometry ˚ where hCN represents the rate of C assimilated by proteins; hNP and m. Thus, not only the GRH but also Agren’s model need represents the rate of proteins assimilated by ribosomes, please see more comprehensive testing in terestrial vascular plants, espe- more details for these equations in [21]. Equation 1 predicts that cially for belowground tissues. N:C ratio is a linear increasing function of m. Equation 2 predicts To test the GRH and A˚ gren’s theory in vascular plants, here we that P:C changes quadratically with m. Thus, the N:P ratio is conducted a sand culture experiment in the temperate steppe of predicted to be a unimodal function of m, increasing for small Inner Mongolia. Three grassland plants were planted in sand pots values of m, reaching a maximum, and then decreasing. with various N and P levels to examine the relationship between Previous studies have provided considerable evidence for C:N:P and growth rates of aboveground, belowground and total positive relationships between N:C or P:C with growth rate of biomass under the variation of N and P. Figure 1. The comparison of relative growth rate of aboveground (a, b), belowground (c, d) and total biomass (e, f) along N and P enrichment levels across the three species. The three species are: Leymus chinensis (LC), Cleistogenes squarrosa (CS) and Chenopodium glaucum (CG). doi:10.1371/journal.pone.0032162.g001 PLoS ONE | www.plosone.org 2 March 2012 | Volume 7 | Issue 3 | e32162 C:N:P and Growth Rate of Vascular Plants Figure 2. Relationships between relative growth rate and N:C for aboveground, belowground and total biomass. See analysis results in Table 1. doi:10.1371/journal.pone.0032162.g002 Results (Fig. 2 and Table 1). However, when excess N treatments were included, no significant relationships were found for Leymus Comparison of m along N and P enrichment levels across chinensis and Cleistogenes squarrosa. the three species No significant relationships were found between aboveground Relative growth rate of each species increased significantly with and total biomass N:C and m for any of the three species when P increasing N and P availability for aboveground, belowground, was limiting (Fig. 2 and Table 1). For belowground biomass of and total biomass across low N and P fertilization levels (Fig. 1). Cleistogenes squarrosa, no significant correlation between N:C and m However, for aboveground and total biomass at high levels of N was found in the P treatments (Table 1); however, significant and P, relative growth rate did not increase significantly or relationships were found for the other two species.
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