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Variation in root:shoot ratios induced the differences between above and belowground mass–density relationships along an aridity gradient
Acta Oecologica 36 (2010) 393e395
Contents lists available at ScienceDirect
Acta Oecologica journal homepage: www.elsevier.com/locate/actoec
Original article
Variation in root:shoot ratios induced the differences between above and belowground massedensity relationships along an aridity gradient Yanyuan Bai, Weiping Zhang, Xin Jia, Nan Wang, Lei Zhou, Shanshan Xu, Genxuan Wang* The State Key Laboratory of Plant Physiology and Biochemistry, Institute of Agroecology and Ecoengineering, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang Province 310058, China
a r t i c l e i n f o
a b s t r a c t
Article history: Received 18 November 2009 Accepted 26 March 2010 Published online 21 April 2010
Despite the importance of root density regulation, this has received little attention compared with density regulation of aboveground plant parts and there is a similar lack of comparisons between above and belowground massedensity relationships. Here we report on field investigations in three sites to study these two aspects. We found that the belowground massedensity exponents (a) were closer to 4/ 3 and they varied less than the aboveground a along an aridity gradient. These differences arose because of variation in root:shoot ratios. Ó 2010 Elsevier Masson SAS. All rights reserved.
Keywords: Abiotic stress Optimal partitioning theory Water availability gradient Vegetation density regulation Variation
1. Introduction Two scaling exponents (a), 3/2 and 4/3, have long been applied by plant ecologists to studies of vegetation ecology. However, the generality of either of them has been called into question (Lonsdale, 1990; Dewar, 1999; Magnani, 1999; Dodds et al., 2001; Darveau et al., 2002; White and Seymour, 2003; Kozlowski and Konarzewski, 2004; Makarieva et al., 2005). Recent studies have demonstrated that a can vary under different stressful conditions, e.g., arid, nutrient-limited or shady environments (Morris, 2002; Deng et al., 2006; Chu et al., 2008). Based on previous work of our team and new field data, we also found that a increased with drought stress, deviating from 3/2 or 4/3 due to allometric growth and open canopy (Dai et al., 2009). All the studies mentioned above, except for Morris’s (2002) and Deng et al.’s (2006), mainly involved aboveground plant parts. Although the secrets of the underworld of vegetation, especially trees, are hard to disclose, understanding their dynamics is necessary for understanding changes in population or community density over time because roots (or belowground stems) play an indispensable role in vascular plants (Trumbore and Gaudinski, 2003). In fact, Morris (1999, 2003), Morris and Myerscough (1991) had conducted a series of experiments and found that roots contributed much to vegetation regulation along a fertility
* Corresponding author. Tel./fax: þ86 0571 88206590. E-mail address: [email protected] (G.X. Wang). 1146-609X/$ e see front matter Ó 2010 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.actao.2010.03.007
gradient. In addition, Deng et al. (2006) found that root massedensity exponents varied little along a moisture gradient. However, despite the progress made by these authors we still know little about belowground massedensity relationships. Since roots play so important a role in vegetation regulation, we needed to learn more about their density regulation. In this paper, we investigated: (1) what rule belowground massedensity relationships would observe along an aridity gradient; (2) what differences may exist between above and belowground masse density relationships along the aridity gradient. To reach our goal, we conducted field experiments on both above and belowground massedensity relationships along an aridity gradient from eastern to western China. 2. Materials and methods 2.1. Field investigation In 2008 and 2009, we carried out field studies at three sites (Tianmushan Mountain, Dengfeng City and Guazhou County), whose geographic and climatic information can be found in Dai et al. (2009). Since we were working on self-thinning, we needed to test whether the vegatation we investigated were under selfthinning or not. To ensure the quality of the samples, we selected mature vegetation. We judged maturity by the overlapping degree of crowns in benign environments and by plant age in arid conditions. The procedure of our studies on aboveground plant parts within each site was the same as in Dai et al.’s (2009). As for the
394
Y. Bai et al. / Acta Oecologica 36 (2010) 393e395
belowground parts, we dug out the roots of 7 sample shrubs, sent them to the laboratory and weighed their dry mass after drying them at 80 C for 48 h. Then we estimated the root mass of other shrubs by the allometric relationships between the dry weight of roots and that of shoots of sample plants (y ¼ 1.029 x1.1559, R2 ¼ 0.98). Since the collection of tree roots was laborious and timeconsuming, we estimated tree root mass from empirical equations instead of actually measuring it (Niklas, 2005; Mokany et al., 2006). 2.2. Statistical analysis Using the reduced major axis (RMA) regression of log10-transformed data, we estimated the scaling exponents and intercepts of both above and belowground massedensity relationships. Then we conducted regression analyses for both the above and belowground scaling exponents against the aridity indexes. In addition, we combined the related results of Deng et al. (2006) with our results to further analyze the differences between the below and aboveground massedensity relationships. 3. Results Table 1 lists the average root:shoot ratios, aboveground massedensity scaling exponents and belowground massedensity scaling exponents from the three sites. We found that average root: shoot ratios increased with aridity. As demonstrated in Fig. 1, both the above and belowground massedensity scaling exponents showed a decelerating relationship with drought stress (indicated by aridity index). From the figure, we could see that the exponent of belowground aearidity index relationships was smaller than that of aboveground aearidity index relationships, meaning the belowground massedensity relationships varied less than the aboveground ones. 4. Discussion 4.1. Belowground massedensity relationships along the aridity gradient Deng et al. (2006) showed that little variation existed among the belowground massedensity exponents, which could also be seen in Fig. 1. However, all their research was conducted in arid areas, with no information on vegetation in semi-arid or moist areas. By contrast, vegetation in our study areas mainly consisted of trees from moist and semi-arid areas and shrubs from deserts. We could see that the belowground massedensity exponents did vary. This variation may be due to the wide range of aridity between those areas which resulted in discrepancies among root:shoot ratios of the vegetation (See Table 1). Though there was variation among the belowground massedensity exponents, we still noticed that compared with the aboveground exponents, these exponents were closer to 4/3, implying that, the belowground parts of vegetations were more likely to follow the metabolic theory (Deng et al., 2006).
Table 1 Mean root:shoot ratios (R/S), aboveground massedensity scaling exponents (aboveground a) and belowground massedensity scaling exponents (belowground a) of three sites. a was obtained by doing RMA regression of log10-transformed data. Sites
Mean R/S
n
Aboveground a
R2
Belowground a
R2
Tianmu Dengfeng Guazhou
0.19 0.37 2.51
42 25 32
1.71 1.31 1.19
0.88 0.95 0.69
1.53 1.30 1.38
0.88 0.94 0.69
Fig. 1. Relationships between the scaling exponents (including above and belowground parts) and the aridity index for six sites (half from our studies and the rest from Deng et al. (2006)). : and ; were respectively above and belowground parts from our studies, D and V were respectively above and belowground parts from Deng et al. (2006). Formulae were y ¼ 1.65043 þ 0.83485x0.31915x2 (R2 ¼ 0.95, P < 0.01) and y ¼ 1.47821 þ 0.33746e0.15911x2 (R2 ¼ 0.76, P < 0.01) respectively for the aboveground line the belowground line.
4.2. Differences between above and belowground massedensity relationships Fig. 1 indicates that scaling exponents of massedensity relationships for belowground parts of vegetation varied less than those for their aboveground along an aridity gradient. In the following, we argue about the potential causes for this phenomenon. First, compared to the air, soil is a relatively stable medium for plants. For example, Morecroft et al. (1998) found that under forest cover soil temperature varied less than air temperature under the canopy; they also discovered that no significant correlation existed between soil water content and soil temperature. High temperature can promote plant development, so it is reasonable to think that roots may grow less than shoots in any given habitat since soil temperature is invariably lower than air temperature during daytime in the growing season. Here we consider plants growing under normal temperatures only, without taking those under lowtemperature stress into account because under such conditions root growth may be greater than shoot growth (Lambers et al., 1995; Li et al., 1994). Second, in our field investigation, we found that root crowns were closed in benign environments and near to closure under arid conditions while the aboveground crown was never closed in arid environments (data not showed), suggesting that the variation of belowground parts was probably less than that of aboveground parts. Third, according to optimal partitioning theory, plant organs in need of the most limiting resource will preferentially receive the allocation of photosynthetic production (Thornley, 1972; Bloom et al., 1985). Consistent with this theory, the drier the site, the higher the root:shoot ratios of its plants (Chapin, 1980; Axelsson, 1981; Deng et al., 2006; Keyes and Grier, 1981; Brown and Lugo, 1982; Nadelhoffer et al., 1985; Murphy and Lugo, 1986). In other words, the aboveground biomass of populations/communities is relatively larger compared with the belowground biomass when water availability is high but relatively smaller under water-limited condition. Therefore, from M ¼ k Na, here M is average dry mass, k is a constant, N is density and a is the scaling exponent, we can deduce that a for aboveground mass is more negative than that for
Y. Bai et al. / Acta Oecologica 36 (2010) 393e395
belowground mass in benign environments while under waterstressed condition the former is less negative. Based on these and the findings of Dai et al. (2009), we can infer that scaling exponents of massedensity relationships for belowground parts of vegetations vary less than those for the aboveground counterparts along an aridity gradient. In sum, the belowground massedensity exponents were much closer to 4/3, suggesting that the belowground parts of vegetation were more likely than the aboveground parts to comply with the metabolic theory. Furthermore, due to the differences in root:shoot ratios, scaling exponents of massedensity relationships for belowground parts of vegetations varied less than those for the aboveground counterparts along an aridity gradient. Since roots and shoots are integrated for plants, we should pay attention to the dynamics of both of them. Acknowledgements Our gratitude goes to the handling editor Ms Shykoff for her help in improving the language and to two anonymous reviewers for their instructive comments. This study was supported by the Natural Science Foundation of China (30730020) and Hi-Tech Research and Development (863) Program of China (2006AA100202). References Axelsson, B., 1981. Site Differences in Yield-differences in Biological Production or in Redistribution of Carbon Within Trees. Dept. Ecol. Environ. Res. Rep. 9. Swed. Univ. Agr. Sci., pp. 1e11. Bloom, A.J., Chapin, F.S., Mooney, H.A., 1985. Resource limitations in plants e an economic analogy. Annu. Rev. Ecol. Syst 16, 363e392. Brown, S., Lugo, A.E., 1982. The storage and production of organic matter in tropical forests and their role in the global carboncycle. Biotropica 14, 161e187. Chapin III, F.S., 1980. The mineral nutrition of wild plants. Annu. Rev. Ecol. Syst. 11, 233e260. Chu, C.J., Maestre, F.T., Xiao, S., Weiner, J., Wang, Y.S., Duan, Z.H., Wang, G., 2008. Balance between facilitation and resource competition determines biomassedensity relationships in plant populations. Ecol. Lett. 11, 1e9. Dai, X.F., Jia, X., Zhang, W.P., Bai, Y.Y., Zhang, J.Y., Wang, Y., Wang, G.X., 2009. Plant height-crown radius and canopy coverage-density relationships determines above-ground biomassedensity relationship in stressful environments. Biol. Lett. 5, 571e573.
395
Darveau, C.A., Suarez, R.K., Andrews, R.D., Hochachka, P.W., 2002. Allometric cascade as a unifying principle of body mass effects on metabolism. Nature 417, 166e170. Deng, J.M., Wang, G.X., Morris, E.C., Wei, X.P., Li, D.X., Chen, B.M., Zhao, C.M., Liu, J., Wang, Y., 2006. Plant massedensity relationship along a moisture gradient in north-west China. J. Ecol. 94, 953e958. Dewar, R.C., 1999. Plant energetics and population density. Nature 398, 572. Dodds, P.S., Rothman, D.H., Weitz, J.S., 2001. Re-examination of the ‘3/4-law’ of metabolism. J. Theor. Biol. 209, 9e27. Keyes, M.R., Grier, C.C., 1981. Above- and belowground net production in 40-yearold Douglas-fir stands on low and high productivity sites. Can. J. For. Res. 11, 599e605. Kozlowski, J., Konarzewski, M., 2004. Is West, Brown and Enquist’s model of allometric scaling mathematically correct and biologically relevant? Funct. Ecol. 18, 283e289. Lambers, H., van den Boogaard, R., Veneklaas, E.J., Villar, R., 1995. Effects of global environmental change on carbon partitioning in vegetative plants of Triticum aestivum and closely related Aegilops species. Glob. Change Biol. 1, 397e406. Li, X., Feng, Y., Boersma, L., 1994. Partition of photosynthates between shoot and root in spring wheat (Triticum aestivum L.) as a function of soil water potential and root temperature. Plant Soil 164, 43e50. Lonsdale, W.N., 1990. The self-thinning rule: dead or alive? Ecol. 71, 1373e1388. Magnani, F., 1999. Plant energetics and population density: comment. Nature 398, 572. Makarieva, A.M., Gorshkov, V.G., Li, B.L., 2005. Biochemical universality of living matter and its metabolic implications. Funct. Ecol. 19, 547e557. Mokany, K., Raison, R.J., Prokushkin, A.S., 2006. Critical analysis of root: shoot ratios in terrestrial biomes. Glob. Change Biol. 12, 84e96. Morecroft, M.D., Taylor, M.E., Oliver, H.R., 1998. Air and soil microclimates of deciduous woodland compared to an open site. Agri. For. Meteor. 90, 141e156. Morris, E.C., Myerscough, P.J., 1991. Self-thinning and competition intensity over a gradient of nutrient availability. J. Ecol. 79, 903e923. Morris, E.C., 1999. Density-dependent mortality induced by low nutrient status of the substrate. Ann. Bot. 84, 95e107. Morris, E.C., 2002. Self-thinning lines differ with fertility level. Ecol. Res. 17, 17e28. Morris, E.C., 2003. How does fertility of the substrate affect intraspecific competition? Evidence and synthesis from self-thinning. Ecol. Res. 18, 287e305. Murphy, P.G., Lugo, A.E., 1986. Structure and biomass of a subtropical dry forest in Puerto Rico. Biotropica 18, 89e96. Nadelhoffer, K.J., Aber, J.D., Melillo, J.M., 1985. Fine roots, net primary production, and soil nitrogen availability: a new hypothesis. Ecol. 66, 1377e1390. Niklas, K.J., 2005. Modelling below- and above-ground biomass for non-woody and woody plants. Ann. Bot. 95, 315e321. Thornley, J.H.M., 1972. A balanced quantitative model for root: shoot ratios in vegetative plants. Ann. Bot. 36, 431e441. Trumbore, S.E., Gaudinski, J.B., 2003. The secret lives of roots. Science 302, 1344e1345. White, C.R., Seymour, R.S., 2003. Mammalian basal metabolic rate is proportional to body mass (2/3). Proc. Natl. Acad. Sci. 100, 4046e4049.
Contents lists available at ScienceDirect
Acta Oecologica journal homepage: www.elsevier.com/locate/actoec
Original article
Variation in root:shoot ratios induced the differences between above and belowground massedensity relationships along an aridity gradient Yanyuan Bai, Weiping Zhang, Xin Jia, Nan Wang, Lei Zhou, Shanshan Xu, Genxuan Wang* The State Key Laboratory of Plant Physiology and Biochemistry, Institute of Agroecology and Ecoengineering, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang Province 310058, China
a r t i c l e i n f o
a b s t r a c t
Article history: Received 18 November 2009 Accepted 26 March 2010 Published online 21 April 2010
Despite the importance of root density regulation, this has received little attention compared with density regulation of aboveground plant parts and there is a similar lack of comparisons between above and belowground massedensity relationships. Here we report on field investigations in three sites to study these two aspects. We found that the belowground massedensity exponents (a) were closer to 4/ 3 and they varied less than the aboveground a along an aridity gradient. These differences arose because of variation in root:shoot ratios. Ó 2010 Elsevier Masson SAS. All rights reserved.
Keywords: Abiotic stress Optimal partitioning theory Water availability gradient Vegetation density regulation Variation
1. Introduction Two scaling exponents (a), 3/2 and 4/3, have long been applied by plant ecologists to studies of vegetation ecology. However, the generality of either of them has been called into question (Lonsdale, 1990; Dewar, 1999; Magnani, 1999; Dodds et al., 2001; Darveau et al., 2002; White and Seymour, 2003; Kozlowski and Konarzewski, 2004; Makarieva et al., 2005). Recent studies have demonstrated that a can vary under different stressful conditions, e.g., arid, nutrient-limited or shady environments (Morris, 2002; Deng et al., 2006; Chu et al., 2008). Based on previous work of our team and new field data, we also found that a increased with drought stress, deviating from 3/2 or 4/3 due to allometric growth and open canopy (Dai et al., 2009). All the studies mentioned above, except for Morris’s (2002) and Deng et al.’s (2006), mainly involved aboveground plant parts. Although the secrets of the underworld of vegetation, especially trees, are hard to disclose, understanding their dynamics is necessary for understanding changes in population or community density over time because roots (or belowground stems) play an indispensable role in vascular plants (Trumbore and Gaudinski, 2003). In fact, Morris (1999, 2003), Morris and Myerscough (1991) had conducted a series of experiments and found that roots contributed much to vegetation regulation along a fertility
* Corresponding author. Tel./fax: þ86 0571 88206590. E-mail address: [email protected] (G.X. Wang). 1146-609X/$ e see front matter Ó 2010 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.actao.2010.03.007
gradient. In addition, Deng et al. (2006) found that root massedensity exponents varied little along a moisture gradient. However, despite the progress made by these authors we still know little about belowground massedensity relationships. Since roots play so important a role in vegetation regulation, we needed to learn more about their density regulation. In this paper, we investigated: (1) what rule belowground massedensity relationships would observe along an aridity gradient; (2) what differences may exist between above and belowground masse density relationships along the aridity gradient. To reach our goal, we conducted field experiments on both above and belowground massedensity relationships along an aridity gradient from eastern to western China. 2. Materials and methods 2.1. Field investigation In 2008 and 2009, we carried out field studies at three sites (Tianmushan Mountain, Dengfeng City and Guazhou County), whose geographic and climatic information can be found in Dai et al. (2009). Since we were working on self-thinning, we needed to test whether the vegatation we investigated were under selfthinning or not. To ensure the quality of the samples, we selected mature vegetation. We judged maturity by the overlapping degree of crowns in benign environments and by plant age in arid conditions. The procedure of our studies on aboveground plant parts within each site was the same as in Dai et al.’s (2009). As for the
394
Y. Bai et al. / Acta Oecologica 36 (2010) 393e395
belowground parts, we dug out the roots of 7 sample shrubs, sent them to the laboratory and weighed their dry mass after drying them at 80 C for 48 h. Then we estimated the root mass of other shrubs by the allometric relationships between the dry weight of roots and that of shoots of sample plants (y ¼ 1.029 x1.1559, R2 ¼ 0.98). Since the collection of tree roots was laborious and timeconsuming, we estimated tree root mass from empirical equations instead of actually measuring it (Niklas, 2005; Mokany et al., 2006). 2.2. Statistical analysis Using the reduced major axis (RMA) regression of log10-transformed data, we estimated the scaling exponents and intercepts of both above and belowground massedensity relationships. Then we conducted regression analyses for both the above and belowground scaling exponents against the aridity indexes. In addition, we combined the related results of Deng et al. (2006) with our results to further analyze the differences between the below and aboveground massedensity relationships. 3. Results Table 1 lists the average root:shoot ratios, aboveground massedensity scaling exponents and belowground massedensity scaling exponents from the three sites. We found that average root: shoot ratios increased with aridity. As demonstrated in Fig. 1, both the above and belowground massedensity scaling exponents showed a decelerating relationship with drought stress (indicated by aridity index). From the figure, we could see that the exponent of belowground aearidity index relationships was smaller than that of aboveground aearidity index relationships, meaning the belowground massedensity relationships varied less than the aboveground ones. 4. Discussion 4.1. Belowground massedensity relationships along the aridity gradient Deng et al. (2006) showed that little variation existed among the belowground massedensity exponents, which could also be seen in Fig. 1. However, all their research was conducted in arid areas, with no information on vegetation in semi-arid or moist areas. By contrast, vegetation in our study areas mainly consisted of trees from moist and semi-arid areas and shrubs from deserts. We could see that the belowground massedensity exponents did vary. This variation may be due to the wide range of aridity between those areas which resulted in discrepancies among root:shoot ratios of the vegetation (See Table 1). Though there was variation among the belowground massedensity exponents, we still noticed that compared with the aboveground exponents, these exponents were closer to 4/3, implying that, the belowground parts of vegetations were more likely to follow the metabolic theory (Deng et al., 2006).
Table 1 Mean root:shoot ratios (R/S), aboveground massedensity scaling exponents (aboveground a) and belowground massedensity scaling exponents (belowground a) of three sites. a was obtained by doing RMA regression of log10-transformed data. Sites
Mean R/S
n
Aboveground a
R2
Belowground a
R2
Tianmu Dengfeng Guazhou
0.19 0.37 2.51
42 25 32
1.71 1.31 1.19
0.88 0.95 0.69
1.53 1.30 1.38
0.88 0.94 0.69
Fig. 1. Relationships between the scaling exponents (including above and belowground parts) and the aridity index for six sites (half from our studies and the rest from Deng et al. (2006)). : and ; were respectively above and belowground parts from our studies, D and V were respectively above and belowground parts from Deng et al. (2006). Formulae were y ¼ 1.65043 þ 0.83485x0.31915x2 (R2 ¼ 0.95, P < 0.01) and y ¼ 1.47821 þ 0.33746e0.15911x2 (R2 ¼ 0.76, P < 0.01) respectively for the aboveground line the belowground line.
4.2. Differences between above and belowground massedensity relationships Fig. 1 indicates that scaling exponents of massedensity relationships for belowground parts of vegetation varied less than those for their aboveground along an aridity gradient. In the following, we argue about the potential causes for this phenomenon. First, compared to the air, soil is a relatively stable medium for plants. For example, Morecroft et al. (1998) found that under forest cover soil temperature varied less than air temperature under the canopy; they also discovered that no significant correlation existed between soil water content and soil temperature. High temperature can promote plant development, so it is reasonable to think that roots may grow less than shoots in any given habitat since soil temperature is invariably lower than air temperature during daytime in the growing season. Here we consider plants growing under normal temperatures only, without taking those under lowtemperature stress into account because under such conditions root growth may be greater than shoot growth (Lambers et al., 1995; Li et al., 1994). Second, in our field investigation, we found that root crowns were closed in benign environments and near to closure under arid conditions while the aboveground crown was never closed in arid environments (data not showed), suggesting that the variation of belowground parts was probably less than that of aboveground parts. Third, according to optimal partitioning theory, plant organs in need of the most limiting resource will preferentially receive the allocation of photosynthetic production (Thornley, 1972; Bloom et al., 1985). Consistent with this theory, the drier the site, the higher the root:shoot ratios of its plants (Chapin, 1980; Axelsson, 1981; Deng et al., 2006; Keyes and Grier, 1981; Brown and Lugo, 1982; Nadelhoffer et al., 1985; Murphy and Lugo, 1986). In other words, the aboveground biomass of populations/communities is relatively larger compared with the belowground biomass when water availability is high but relatively smaller under water-limited condition. Therefore, from M ¼ k Na, here M is average dry mass, k is a constant, N is density and a is the scaling exponent, we can deduce that a for aboveground mass is more negative than that for
Y. Bai et al. / Acta Oecologica 36 (2010) 393e395
belowground mass in benign environments while under waterstressed condition the former is less negative. Based on these and the findings of Dai et al. (2009), we can infer that scaling exponents of massedensity relationships for belowground parts of vegetations vary less than those for the aboveground counterparts along an aridity gradient. In sum, the belowground massedensity exponents were much closer to 4/3, suggesting that the belowground parts of vegetation were more likely than the aboveground parts to comply with the metabolic theory. Furthermore, due to the differences in root:shoot ratios, scaling exponents of massedensity relationships for belowground parts of vegetations varied less than those for the aboveground counterparts along an aridity gradient. Since roots and shoots are integrated for plants, we should pay attention to the dynamics of both of them. Acknowledgements Our gratitude goes to the handling editor Ms Shykoff for her help in improving the language and to two anonymous reviewers for their instructive comments. This study was supported by the Natural Science Foundation of China (30730020) and Hi-Tech Research and Development (863) Program of China (2006AA100202). References Axelsson, B., 1981. Site Differences in Yield-differences in Biological Production or in Redistribution of Carbon Within Trees. Dept. Ecol. Environ. Res. Rep. 9. Swed. Univ. Agr. Sci., pp. 1e11. Bloom, A.J., Chapin, F.S., Mooney, H.A., 1985. Resource limitations in plants e an economic analogy. Annu. Rev. Ecol. Syst 16, 363e392. Brown, S., Lugo, A.E., 1982. The storage and production of organic matter in tropical forests and their role in the global carboncycle. Biotropica 14, 161e187. Chapin III, F.S., 1980. The mineral nutrition of wild plants. Annu. Rev. Ecol. Syst. 11, 233e260. Chu, C.J., Maestre, F.T., Xiao, S., Weiner, J., Wang, Y.S., Duan, Z.H., Wang, G., 2008. Balance between facilitation and resource competition determines biomassedensity relationships in plant populations. Ecol. Lett. 11, 1e9. Dai, X.F., Jia, X., Zhang, W.P., Bai, Y.Y., Zhang, J.Y., Wang, Y., Wang, G.X., 2009. Plant height-crown radius and canopy coverage-density relationships determines above-ground biomassedensity relationship in stressful environments. Biol. Lett. 5, 571e573.
395
Darveau, C.A., Suarez, R.K., Andrews, R.D., Hochachka, P.W., 2002. Allometric cascade as a unifying principle of body mass effects on metabolism. Nature 417, 166e170. Deng, J.M., Wang, G.X., Morris, E.C., Wei, X.P., Li, D.X., Chen, B.M., Zhao, C.M., Liu, J., Wang, Y., 2006. Plant massedensity relationship along a moisture gradient in north-west China. J. Ecol. 94, 953e958. Dewar, R.C., 1999. Plant energetics and population density. Nature 398, 572. Dodds, P.S., Rothman, D.H., Weitz, J.S., 2001. Re-examination of the ‘3/4-law’ of metabolism. J. Theor. Biol. 209, 9e27. Keyes, M.R., Grier, C.C., 1981. Above- and belowground net production in 40-yearold Douglas-fir stands on low and high productivity sites. Can. J. For. Res. 11, 599e605. Kozlowski, J., Konarzewski, M., 2004. Is West, Brown and Enquist’s model of allometric scaling mathematically correct and biologically relevant? Funct. Ecol. 18, 283e289. Lambers, H., van den Boogaard, R., Veneklaas, E.J., Villar, R., 1995. Effects of global environmental change on carbon partitioning in vegetative plants of Triticum aestivum and closely related Aegilops species. Glob. Change Biol. 1, 397e406. Li, X., Feng, Y., Boersma, L., 1994. Partition of photosynthates between shoot and root in spring wheat (Triticum aestivum L.) as a function of soil water potential and root temperature. Plant Soil 164, 43e50. Lonsdale, W.N., 1990. The self-thinning rule: dead or alive? Ecol. 71, 1373e1388. Magnani, F., 1999. Plant energetics and population density: comment. Nature 398, 572. Makarieva, A.M., Gorshkov, V.G., Li, B.L., 2005. Biochemical universality of living matter and its metabolic implications. Funct. Ecol. 19, 547e557. Mokany, K., Raison, R.J., Prokushkin, A.S., 2006. Critical analysis of root: shoot ratios in terrestrial biomes. Glob. Change Biol. 12, 84e96. Morecroft, M.D., Taylor, M.E., Oliver, H.R., 1998. Air and soil microclimates of deciduous woodland compared to an open site. Agri. For. Meteor. 90, 141e156. Morris, E.C., Myerscough, P.J., 1991. Self-thinning and competition intensity over a gradient of nutrient availability. J. Ecol. 79, 903e923. Morris, E.C., 1999. Density-dependent mortality induced by low nutrient status of the substrate. Ann. Bot. 84, 95e107. Morris, E.C., 2002. Self-thinning lines differ with fertility level. Ecol. Res. 17, 17e28. Morris, E.C., 2003. How does fertility of the substrate affect intraspecific competition? Evidence and synthesis from self-thinning. Ecol. Res. 18, 287e305. Murphy, P.G., Lugo, A.E., 1986. Structure and biomass of a subtropical dry forest in Puerto Rico. Biotropica 18, 89e96. Nadelhoffer, K.J., Aber, J.D., Melillo, J.M., 1985. Fine roots, net primary production, and soil nitrogen availability: a new hypothesis. Ecol. 66, 1377e1390. Niklas, K.J., 2005. Modelling below- and above-ground biomass for non-woody and woody plants. Ann. Bot. 95, 315e321. Thornley, J.H.M., 1972. A balanced quantitative model for root: shoot ratios in vegetative plants. Ann. Bot. 36, 431e441. Trumbore, S.E., Gaudinski, J.B., 2003. The secret lives of roots. Science 302, 1344e1345. White, C.R., Seymour, R.S., 2003. Mammalian basal metabolic rate is proportional to body mass (2/3). Proc. Natl. Acad. Sci. 100, 4046e4049.