Ecological variations of woody species along an altitudinal gradient in the Qinling Mountains of Central China: area-based versus mass-based expression of leaf traits

Abstract

Leaf trait-based research has become the preferred method to understand the ecological strategies of plants. However, there is still a debate on whether area-based or mass-based traits provide different insights into environmental adaptations and responses. In this study, seven key leaf traits (maximum net photosynthetic rate, dark respiration rate, nitrogen content, photosynthetic nitrogen use efficiency, leaf mass per area, leaf dry matter contents and leaf area) of 43 woody species were quantified on the basis of both area and mass along an altitudinal gradient (1100–2700 m) in the Qinling Mountains of China. Differences in leaf traits and bivariate correlations between the two expressions were compared. By considering different expressions, the strengths and directions of the responses of leaf traits to the altitudinal gradient were determined. Leaf traits showed large variations; interspecific variations contributed more to total variance than intraspecific variations. Bivariate correlations between photosynthetic traits and structural traits (mass per area, dry matter content, and area) were weaker on a mass basis than those on an area basis. Most traits exhibited quadratic trends along the altitudinal gradient, and these patterns were more noticeable for area-based than mass-based traits. Area-based traits were more sensitive to changes in temperature and precipitation associated with altitude. These results provide evidence that mass- versus area-based traits show different ecological responses to environmental conditions associated with altitude, even if they do not contain very broad spatial scales. Our results also indicate distinction of photosynthetic acclimation among the two expressions along an altitudinal gradient, reflecting trade-offs among leaf structure and physiological traits.

Keywords

Altitude modulation / Bivariate relationship / Leaf trait / Qinling Mountains

References

[1] Adler PB, Fajardo A, Kleinhesselink AR, Kraft NJB. Trait-based tests of coexistence mechanisms. Ecol Lett, 2013, 16: 1294-1306.

[2] Almeida JP, Montúfar R, Anthelme F. Patterns and origin of intraspecific functional variability in a tropical alpine species along an altitudinal gradient. Plant Ecol Divers, 2013, 6: 423-433.

[3] Bassman JH, Zwier JC. Gas exchange characteristics of Populus trichocarpa, Populus deltoides and Populus trichocarpa ×  P. deltoides clones. Tree Physiol, 1991, 8: 145-159.

[4] Berli FJ, Alonso R, Bressan-Smith R, Bottini R. UV-B impairs growth and gas exchange in grapevines grown in high altitude. Physiol Plantarum, 2013, 149: 127-140.

[5] Blonder B, Violle C, Bentley LP, Enquist BJ. Venation networks and the origin of the leaf economics spectrum. Ecol Lett, 2011, 14: 91-100.

[6] Bloomfield KJ, Cernusak LA, Eamus D, Ellsworth DS, Prentice IC, Wright IJ, Boer MM, Bradford MG, Cale P, Cleverly J, Egerton JJG, Evans BJ, Hayes LS, Hutchinson MF, Liddell MJ, Macfarlane C, Meyer WS, Prober SM, Togashi HF, Wardlaw T, Zhu L, Atkin OK. A continental-scale assessment of variability in leaf traits: within species, across sites and between seasons. Funct Ecol, 2018

[7] Bu HY, Jia P, Qi W, Liu K, Xu DH, Ge WJ, Wang XJ. The effects of phylogeny, life-history traits and altitude on the carbon, nitrogen, and phosphorus contents of seeds across 203 species from an alpine meadow. Plant Ecol, 2018, 219: 737-748.

[8] Chai YF, Zhang XF, Yue M, Liu X, Li Q, Shang HL, Meng QC, Zhang RC. Leaf traits suggest different ecological strategies for two Quercus species along an altitudinal gradient in the Qinling Mountains. J Forest Res, 2015, 20: 501-513.

[9] Dubuis A, Rossier L, Pottier J, Pellissier L, Vittoz P, Guisan A. Predicting current and future spatial community patterns of plant functional traits. Ecography, 2013, 36: 1158-1168.

[10] Dunne JA, Harte J, Taylor KJ. Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecol Monogr, 2003, 73: 69-86.

[11] Fujii S, Cornelissen JHC, Berg MP, Mori AS. Tree leaf and root traits mediate soil faunal contribution to litter decomposition across an elevational gradient. Funct Ecol, 2018, 32: 840-852.

[12] Funk JL, Cornwell WK. Leaf traits within communities: context may affect the mapping of traits to function. Ecology, 2013, 94: 1893-1897.

[13] Gong Y, Ling H, Lv G, Chen Y, Guo Z, Cao J. Disentangling the influence of aridity and salinity on community functional and phylogenetic diversity in local dryland vegetation. Sci Total Environ, 2019, 653: 409-422.

[14] Guo Z, Lin H, Chen S, Yang Q. Altitudinal patterns of leaf traits and leaf allometry in bamboo Pleioblastus amarus. Front Plant Sci, 2018

[15] Hikosaka K. Interspecific difference in the photosynthesis–nitrogen relationship: patterns, physiological causes, and ecological importance. J Plant Res, 2004, 117: 481-494.

[16] Hu YB, Bellaloui N, Sun GY, Tigabu M, Wang JH. Exogenous sodium sulfide improves morphological and physiological responses of a hybrid Populus species to nitrogen dioxide. J Plant Physiol, 2014, 171(10): 868-875.

[17] Kenzo T, Inoue Y, Yoshimura M, Yamashita M, Tanaka-Oda A, Ichie T. Height-related changes in leaf photosynthetic traits in diverse Bornean tropical rain forest trees. Oecologia, 2015, 177: 191-202.

[18] Kraft NJB, Valencia R, Ackerly DD. Functional traits and niche-based tree community assembly in an Amazonian forest. Science, 2008, 322: 580-582.

[19] Krix DW, Murray BR. Landscape variation in plant leaf flammability is driven by leaf traits responding to environmental gradients. Ecosphere, 2018, 9: e02093.

[20] Li DW, Wang ZQ, Tian HX, He WX, Geng ZC. Carbon, nitrogen and phosphorus contents in soils on Taibai Mountain and their ecological stoichiometry relative to elevation. Acta Pedol Sin, 2017, 54: 160-170.

[21] Lloyd J, Bloomfield K, Domingues TF, Farquhar GD. Photosynthetically relevant foliar traits correlating better on a mass versus an area basis: of ecophysiological relevance or just a case of mathematical imperatives and statistical quicksand?. New Phytol, 2013, 199: 311-321.

[22] Malhi Y, Silman M, Salinas N, Bush M, Meir P, Saatchi S. Introduction: elevation gradients in the tropics: laboratories for ecosystem ecology and global change research. Glob Change Biol, 2010, 16: 3171-3175.

[23] Niinemets Ü. Stomatal conductance alone does not explain the decline in foliar photosynthetic rate with increasing tree age and size in Picea abies and Pinus sylvestris. Tree Physiol, 2002, 22: 515-535.

[24] Niinemets Ü, Keenan TF, Hallik L. A worldwide analysis of within-canopy variations in leaf structural, chemical and physiological traits across plant functional types. New Phytol, 2014, 205: 973-993.

[25] Onoda Y, Wright IJ, Evans JR, Hikosaka K, Kitajima K, Niinemets Ü. Physiological and structural tradeoffs underlying the leaf economics spectrum. New Phytol, 2017, 214: 1447.

[26] Osnas JLD, Lichstein JW, Reich PB, Pacala SW. Global leaf trait relationships: mass, area, and the leaf economics spectrum. Science, 2013, 340: 741-744.

[27] Poorter HNU, Poorter L, Wright IJ, Villar R. Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol, 2009, 182: 565-588.

[28] Poorter H, Lambers H, Evans JR. Trait correlation networks: a whole-plant perspective on the recently criticized leaf economic spectrum. New Phytol, 2014, 201: 378-382.

[29] Read QD, Moorhead LC, Swenson NG, Bailey JK, Sanders NJ. Convergent effects of elevation on functional leaf traits within and among species. Funct Ecol, 2014, 28: 37-45.

[30] Rijkers T, Pons TL, Bongers F. The effect of tree height and light availability on photosynthetic leaf traits of four neotropical species differing in shade tolerance. Funct Ecol, 2000, 14: 77-86.

[31] Rose L, Rubarth MC, Hertel D, Leuschner C. Management alters interspecific leaf trait relationships and trait-based species rankings in permanent meadows. J Veg Sci, 2013, 24: 239-250.

[32] Ryser P, Bernardi J, Merla A. Determination of leaf fresh mass after storage between moist paper towels: constraints and reliability of the method. J Exp Bot, 2008, 59: 2461-2467.

[33] Santiago LS, Wright SJ. Leaf functional traits of tropical forest plants in relation to growth form. Funct Ecol, 2007, 21: 19-27.

[34] Saura-Mas S, Shipley B, Lioret F. Relationship between post-fire regeneration and leaf economics spectrum in Mediterranean woody species. Funct Ecol, 2009, 23: 103-110.

[35] Sessa EB, Givnish TJ. Leaf form and photosynthetic physiology of Dryopteris species distributed along light gradients in eastern North America. Funct Ecol, 2014, 28: 108-123.

[36] Takashima T, Hikosaka K, Hirose T. Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant, Cell Environ, 2004, 27: 1047-1054.

[37] Tan Q, Wang G. Decoupling of nutrient element cycles in soil and plants across an altitude gradient. Sci Rep, 2016, 6: 34875.

[38] Tang ZY, Fang JY. Temperature variation along the northern and southern slopes of Mt. Taibai, China. Agric For Meteorol, 2006, 139: 200-207.

[39] van de Weg MJ, Meir P, Grace J, Atkin OK. Altitudinal variation in leaf mass per unit area, leaf tissue density and foliar nitrogen and phosphorus content along an Amazon-Andes gradient in Peru. Plant Ecol Divers, 2009, 2: 243-254.

[40] Villar R, Ruiz-Robleto J, Ubera JL, Poorter H. Exploring variation in leaf mass per area (LMA) from leaf to cell: an anatomical analysis of 26 woody species. Am J Bot, 2013, 100: 1969-1980.

[41] Vitória AP, Alves LF, Santiago LS. Atlantic forest and leaf traits: an overview. Trees, 2019

[42] Wang Z, Liu X, Bao WK. Higher photosynthetic capacity and different functional trait scaling relationships in erect bryophytes compared with prostrate species. Oecologia, 2016, 180: 359-369.

[43] Wang X, Wiegand T, Anderson-Teixeira KJ, Bourg NA, Hao Z, Howe R, Jin G, Orwig DA, Spasojevic MJ, Wang S, Wolf A, Myers JA. Ecological drivers of spatial community dissimilarity, species replacement and species nestedness across temperate forests. Glob Ecol Biogeogr, 2018, 27: 581-592.

[44] Warton DI, Wright IJ, Falster DS, Westoby M. Bivariate line-fitting methods for allometry. Biol Rev, 2006, 81: 259-291.

[45] Westoby M, Reich PB, Wright IJ. Understanding ecological variation across species: area-based versus mass-based expression of leaf traits. New Phytol, 2013, 199: 322-323.

[46] Wright IJ, Groom PK, Lamont BB, Poot P, Prior LD, Reich PB, Schulze ED, Veneklaas EJ, Westoby M. Leaf traits relationships in Australian plant species. Func Plant Biol, 2004, 31: 551-558.

[47] Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin FS, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R. The world-wide leaf economics spectrum. Nature, 2004, 428: 821-827.

[48] Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Groom PK, Hikosaka K, Lee W, Lusk CH, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Warton DI, Westoby M. Modulation of leaf economic traits and trait relationships by climate. Glob Ecol Biogeogr, 2005, 14: 411-421.

[49] Xiang S, Reich PB, Sun SC, Atkin OK. Contrasting leaf trait scaling relationships in tropical and temperate wet forest species. Funct Ecol, 2013, 27: 522-534.

[50] Xu DQ. Some noteworthy problems in measurement and investigation of photosynthesis. Plant Physiol Commun, 2006, 42: 1163-1167.

[51] Yue M, Zhou H. Diversity of higher plants in deciduous broadleaved forests on the northern slope of Taibai Mountain. Acta Bot Yunnanica, 1997, 19: 171-176. (in Chinese with English abstract)

[52] Zhang SB, Zhou ZK, Hu H, Xu K, Yan N, Li SY. Photosynthetic performances of Quercus pannosa vary with altitude in the Hengduan Mountains, southwest China. Forest Ecol Manag, 2005, 212: 291-301.

[53] Zheng SX, Shangguan ZP. Spatial patterns of photosynthetic characteristics and leaf physical traits of plants in the Loess Plateau of China. Plant Ecol, 2007, 191: 279-293.