Response of plant, litter, and soil C:N:P stoichiometry to growth stages in Quercus secondary forests on the Loess Plateau, China

doi:10.1007/s11676-022-01512-2

Abstract

Abstract:

Ecological stoichiometry is an important indicator of biogeochemical cycles and nutrient limitations in terrestrial ecosystems. However, little is known about the response of ecological stoichiometry to plant growth. In this study, carbon (C), nitrogen (N), and phosphorus (P) concentrations were evaluated in plant tissues (trees, shrubs, and herbs), litter, and soil of young (≤ 40-year-old), middle-aged (41–60-year-old), near-mature (61–80-year-old), and mature (81–120-year-old) Quercus secondary forests on the Loess Plateau, China. Vegetation composition, plant biomass, and C stock were determined to illustrate their interaction with stoichiometry. Only tree biomass C significantly increased with stand development. Leaf N and trunk P concentrations generally increased, but branch P decreased with growth stage. Fine roots had the highest C and P concentrations at the middle-aged stage. In contrast, shrubs, herbs, litter, and soil C:N:P stoichiometry did not change significantly during stand development. Leaf N and P were positively correlated with soil C, N, P, and their ratios. However, there was no significant correlation between litter and leaves in terms of C:N:P stoichiometry. A redundancy analysis showed that soil N best explained leaf N and P variance, and tree biomass and C stock were related to biotic factors such as tree age and shrub biomass. Hierarchical partitioning analysis indicated that, compared with soil or litter variables, stand age only accounted for a relatively small proportion of leaf C, N, and P variation. Thus, secondary Quercus ecosystems might have inherent ability to maintain sensitive responses of metabolically active organs to environmental factors during stand aging. The results of this work help to elucidate the biogeochemical cycling of secondary forest ecosystems in tree development, provide novel insights into the adaptation strategies of plants in different organs and growth stages, and could be used to guide fertilization programs and optimize forest structure.

Key words: Ecological stoichiometry, Tree biomass C stock, Understory plant, Age, Stand development

Juanjuan Zhang, Xinyang Li, Meng Chen, Linjia Huang, Ming Li, Xu Zhang, Yang Cao. Response of plant, litter, and soil C:N:P stoichiometry to growth stages in Quercus secondary forests on the Loess Plateau, China[J]. JOURNAL OF FORESTRY RESEARCH, 2023, 34(3): 595-607.

Juanjuan Zhang, Xinyang Li, Meng Chen, Linjia Huang, Ming Li, Xu Zhang, Yang Cao. [J]. 林业研究(英文版), 2023, 34(3): 595-607.

References 69

1	Ågren GI. Stoichiometry and nutrition of plant growth in natural communities. Ann Rev Ecol Evol S, 2008, 39: 153-170, DOI
2	Agren GI, Weih M. Plant stoichiometry at different scales: element concentration patterns reflect environment more than genotype. New Phytol, 2012, 194: 944-952, DOI
3	Ahirwal JA, Nath B, Brahma S, Deb UK, Sahoo A, Nath J. Patterns and driving factors of biomass carbon and soil organic carbon stock in the Indian Himalayan region. Sci Total Environ, 2021, 770, DOI
4	Bai X, Wang B, An S, Zeng Q, Zhang H. Response of forest species to C:N: P in the plant-litter-soil system and stoichiometric homeostasis of plant tissues during afforestation on the Loess Plateau. China Catena, 2019, 183, DOI
5	Bardgett R, Bowman R, Kaufmann S, Schmidt K. A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evol, 2005, 20: 634-641, DOI
6	Bell C, Carrillo Y, Boot CM, Rocca JD, Pendall E, Wallenstein MD. Rhizosphere stoichiometry: are C:N: P ratios of plants, soils, and enzymes conserved at the plant species-level?. New Phytol, 2014, 201: 505-517, DOI
7	Boyden S, Binkley D, Senock R. Competition and facilitation between eucalyptus and nitrogen-fixing falcataria in relation to soil fertility. Ecology, 2005, 86: 992-1001, DOI
8	Cao Y, Chen YM. Ecosystem C:N: P stoichiometry and carbon storage in plantations and a secondary forest on the Loess Plateau, China. Ecol Eng, 2017, 105: 125-132, DOI
9	Cao Y, Chen Y. Coupling of plant and soil C:N: P stoichiometry in black locust (Robinia pseudoacacia) plantations on the Loess Plateau, China. Trees, 2017, 31: 1559-1570, DOI
10	Cao Y, Li Y, Zhang G, Zhang J, Chen M. Fine root C:N: P stoichiometry and its driving factors across forest ecosystems in northwestern China. Sci Total Environ, 2020, 737, DOI
11	Chen L, Deng Q, Yuan Z, Mu X, Kallenbach RL. Age-related C:N: P stoichiometry in two plantation forests in the Loess Plateau of China. Ecol Eng, 2018, 120: 14-22, DOI
12	Chen M, Zhang X, Li M, Zhang JJ, Cao Y. Climate-growth pattern of Pinus tabulaeformis plantations and their resilience to drought events in the Loess Plateau. For Ecol Manag, 2021, 499, DOI
13	Cleveland CC, Liptzin D. C:N: P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass?. Biogeochemistry, 2007, 85: 235-252, DOI
14	De Groote SRE, Vanhellemont M, Baeten L, De Schrijver A, Martel A, Bonte D, Lens L, Verheyen K. Tree species diversity indirectly affects nutrient cycling through the shrub layer and its high-quality litter. Plant Soil, 2018, 427: 335-350, DOI
15	Delgado-Baquerizo M, Reich PB, Bardgett RD, Eldridge DJ, Lambers H, Wardle DA, Reed SC, Plaza C, Png GK, Neuhauser S, Berhe AA, Hart SC, Hu HW, He JZ, Bastida F, Abades S, Alfaro FD, Cutler NA, Gallardo A, Garcia-Velazquez L, Hayes PE, Hseu ZY, Perez CA, Santos F, Siebe C, Trivedi P, Sullivan BW, Weber-Grullon L, Williams MA, Fierer N. The influence of soil age on ecosystem structure and function across biomes. Nat Commun, 2020, 11: 4721, DOI
16	Di Palo F, Fornara DA. Plant and soil nutrient stoichiometry along primary ecological successions: Is there any link?. PLoS ONE, 2017, 12, DOI
17	Du E, Terrer C, Pellegrini AFA, Ahlström A, van Lissa CJ, Zhao X, Xia N, Wu X, Jackson RB. Global patterns of terrestrial nitrogen and phosphorus limitation. Nat Geosci, 2020, 13: 221-226, DOI
18	Ellison AM. Nutrient limitation and stoichiometry of carnivorous plants. Plant Mol Biol, 2006, 8: 740-747, DOI
19	Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotner JB, Harrison JF, Hobbie SE, Odell GM, Weider LJ. Biological stoichiometry from genes to ecosystems. Ecol Lett, 2000, 3: 540-550, DOI
20	Fan H, Wu J, Liu W, Yuan Y, Hu L, Cai Q. Linkages of plant and soil C:N: P stoichiometry and their relationships to forest growth in subtropical plantations. Plant Soil, 2015, 392: 127-138, DOI
21	FAO (2020) Global forest resources assessment 2020. Food and Agriculture Organization of the United Nations
22	Feng ZW, Wang XK, Wu G. Biomass and productivity in forest ecosystem of China, 1999 Beijing Science Press 41-45
23	Fisher JAD, Frank KT, Leggett WC. Dynamic macroecology on ecological time-scales. Global Ecol Biogeogr, 2010, 19: 1-15, DOI
24	Grau O, Penuelas J, Ferry B, Freycon V, Blanc L, Desprez M, Baraloto C, Chave J, Descroix L, Dourdain A, Guitet S, Janssens IA, Sardans J, Herault B. Nutrient-cycling mechanisms other than the direct absorption from soil may control forest structure and dynamics in poor Amazonian soils. Sci Rep, 2017, 7: 45017, DOI
25	Gusewell S. N: P ratios in terrestrial plants: variation and functional significance. New Phytol, 2004, 164: 243-266, DOI
26	Han W, Fang J, Guo D, Zhang Y. Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. New Phytol, 2005, 168: 377-385, DOI
27	Hooker TD, Compton JE. Forest ecosystem carbon and nitrogen accumulation during the first century after agricultural abandonment. Ecol Appl, 2003, 13: 299-313, DOI
28	Hou E, Wen D, Jiang L, Luo X, Kuang Y, Lu X, Chen C, Allen KT, He X, Huang X, Luo Y. Latitudinal patterns of terrestrial phosphorus limitation over the globe. Ecol Lett, 2021, 24: 1420-1431, DOI
29	Hu Q, Sheng M, Bai Y, Jie Y, Xiao H. Response of C, N, and P stoichiometry characteristics of Broussonetia papyrifera to altitude gradients and soil nutrients in the karst rocky ecosystem, SW China. Plant Soil, 2020, DOI
30	Jones ILSJ, DeWalt OR, Lopez L, Bunnefeld Z, Pattison D, Dent H. Above- and belowground carbon stocks are decoupled in secondary tropical forests and are positively related to forest age and soil nutrients respectively. Sci Total Environ, 2019, 697: 1-10, DOI
31	Keeton WS, Chernyavskyy M, Gratzer G, Main-Knorn M, Shpylchak M, Bihun Y. Structural characteristics and aboveground biomass of old-growth spruce-fir stands in the eastern Carpathian mountains, Ukraine. Plant Biosyst, 2010, 144: 148-159, DOI
32	Kerkhoff AJ, Fagan WF, Elser JJ, Enquist BJ. Phylogenetic and growth form variation in the scaling of nitrogen and phosphorus in the seed plants. Am Nat, 2006, 168: 103-122, DOI
33	Koerselman W, Afm M. The vegetation N: P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol, 1996, 33: 1441-1450, DOI
34	Lai J, Peres-Neto P (2021) rdacca.hp: Hierarchical and variation partitioning for canonical analysis. R package version 0.5-6. https://CRAN.R-project.org/package=rdacca.hp
35	Liang X, Liu S, Wang H, Wang J. Variation of carbon and nitrogen stoichiometry along a chronosequence of natural temperate forest in northeastern China. J Plant Ecol, 2018, 11: 339-350, DOI
36	Liu W, Fu S, Wu S, Zhong Z, Xu Y, Deng J, Ren C, Han X, Zhang Q, Su Y. Nutrient limitations for overstory and understory plants during Robinia pseudoacacia afforestation in the Loess Plateau, China. Soil Sci Soc Am J, 2020, 84: 888-900, DOI
37	Liu Y, Fang Y, An S. How C:N: P stoichiometry in soils and plants responds to succession in Robinia pseudoacacia forests on the Loess Plateau. China for Ecol Manag, 2020, 475, DOI
38	Massmann A, Cavaleri MA, Oberbauer SF, Olivas PC, Porder S. Foliar stoichiometry is marginally sensitive to soil phosphorus across a lowland tropical rainforest. Ecosystems, 2021, DOI
39	Peichl M, Leava NA, Kiely G. Above- and belowground ecosystem biomass, carbon and nitrogen allocation in recently afforested grassland and adjacent intensively managed grassland. Plant Soil, 2011, 350: 281-296, DOI
40	Powers J, Peréz-Aviles SD. Edaphic factors are a more important control on surface fine roots than stand age in secondary tropical dry forests. Biotropica, 2013, 45: 1-9, DOI
41	Prescott CE. The influence of the forest canopy on nutrient cycling. Tree Physiol, 2002, 22: 1193, DOI
42	Reich PB, Oleksyn J. Global patterns of plant leaf N and P in relation to temperature and latitude. PNAS, 2004, 101: 11001-11006, DOI
43	Sardans J, Peñuelas J. Tree growth changes with climate and forest type are associated with relative allocation of nutrients, especially phosphorus, to leaves and wood. Global Ecol Biogeogr, 2013, 22: 494-507, DOI
44	Sardans J, Penuelas J. Trees increase their P: N ratio with size. Glob Ecol Biogeogr, 2015, 24: 147-156, DOI
45	Sterner RW, Elser JJ. Ecological stoichiometry: the biology of elements from molecules to the biosphere. J Plankton Res, 2002, 25: 1183
46	Su B, Shangguan Z. Response of water use efficiency and plant-soil C:N: P stoichiometry to stand quality in Robinia pseudoacacia on the Loess Plateau of China. CATENA, 2021, 206, DOI
47	Sun T, Dong L, Mao Z, Li Y. Fine root dynamics of trees and understory vegetation in a chronosequence of Betula platyphylla stands. Forest Ecol Manag, 2015, 346: 1-9, DOI
48	Tang Z, Xu W, Zhou G, Bai Y, Li J, Tang X, Chen D, Liu Q, Ma W, Xiong G, He H, He N, Guo Y, Guo Q, Zhu J, Han W, Hu H, Fang J, Xie Z. Correction for Tang et al., Patterns of plant carbon, nitrogen, and phosphorus concentration in relation to productivity in China's terrestrial ecosystems. PNAS, 2018, 115: E6095-E6096, DOI
49	Urbina I, Grau O, Sardans J, Margalef O, Peguero G, Asensio DLLJ, Ogaya R, Gargallo-Garriga A, Van Langenhove L, Verryckt LT, Courtois EA, Stahl C, Soong JL, Chave J, Herault B, Janssens IA, Sayer E, Penuelas J. High foliar K and P resorption efficiencies in old-growth tropical forests growing on nutrient-poor soils. Ecol Evol, 2021, 11: 8969-8982, DOI
50	Wang Z, Zheng F. Ecological stoichiometry of plant leaves, litter and soils in a secondary forest on China's Loess Plateau. Peer J, 2020, 8, DOI
51	Wang W, Qiu Ling Zu, Dong-Xue Y-G, Jing An, Hong-Yan W, Guan-Yu Z, Wei S, Xi-Quan C. Changes in soil organic carbon, nitrogen, pH and bulk density with the development of larch (Larix gmelinii) plantations in China. Global Change Biol, 2011, 17: 2657-2676, DOI
52	Wang Y, Liu L, Yue F, Li D. Dynamics of carbon and nitrogen storage in two typical plantation ecosystems of different stand ages on the Loess Plateau of China. Peer J, 2019, 7, DOI
53	Wang J, Zhao W, Wang G, Yang S, Pereira P. Effects of long-term afforestation and natural grassland recovery on soil properties and quality in Loess Plateau (China). Sci Total Environ, 2021, 770, DOI
54	Wu T, Dong Y, Yu M, Geoff WG, Zeng D-H. Leaf nitrogen and phosphorus stoichiometry of Quercus species across China. Forest Ecol and Manag, 2012, 284: 116-123, DOI
55	Yang Y, Luo Y. Carbon:nitrogen stoichiometry in forest ecosystems during stand development. Global Ecol Biogeogr, 2011, 20: 354-361, DOI
56	Yang Y, Liu B-R, An S-S. Ecological stoichiometry in leaves, roots, litters and soil among different plant communities in a desertified region of Northern China. CATENA, 2018, 166: 328-338, DOI
57	Yang C, Zhang X, Ni H, Gai X, Huang Z, Du X, Zhong Z. Soil carbon and associated bacterial community shifts driven by fine root traits along a chronosequence of Moso bamboo (Phyllostachys edulis) plantations in subtropical China. Sci Total Environ, 2021, 752, DOI
58	Yelenik SG. Linking dominant Hawaiian tree species to understory development in recovering pastures via impacts on soils and litter. Restor Ecol, 2017, 25: 42-52, DOI
59	Zechmeister-Boltenstern S, Keiblinger KM, Mooshammer M, Penuelas J, Richter A, Sardans J, Wanek W. The application of ecological stoichiometry to plant-microbial-soil organic matter transformations. Ecol Monogr, 2015, 85: 133-155, DOI
60	Zeng Q, Lai R, Chen Y, An S. Soil, leaf and root ecological stoichiometry of Caragana korshinskii on the Loess Plateau of China in relation to plantation age. PLoS ONE, 2017, 12, DOI
61	Zhang J, Zhao N, Liu C, Yang H, Li M, Yu G, Wilcox K, Yu Q, He N, Niu S. C:N: P stoichiometry in China's forests: from organs to ecosystems. Funct Ecol, 2017, 32: 50-60, DOI
62	Zhang J, He N, Liu C, Xu L, Yu Q, Yu G. Allocation strategies for nitrogen and phosphorus in forest plants. Oikos, 2018, 127: 1506-1514, DOI
63	Zhang W, Qiao W, Gao D, Dai Y, Deng J, Yang G, Han X, Ren G. Relationship between soil nutrient properties and biological activities along a restoration chronosequence of Pinus tabulaeformis plantation forests in the Ziwuling Mountains, China. CATENA, 2018, 161: 85-95, DOI
64	Zhang W, Ren C, Deng J, Zhao F, Yang G, Han X, Tong X, Feng Y. Plant functional composition and species diversity affect soil C, N, and P during secondary succession of abandoned farmland on the Loess Plateau. Ecol Eng, 2018, 122: 91-99, DOI
65	Zhang Y, Wei L, Wei X, Liu X, Shao M. Long-term afforestation significantly improves the fertility of abandoned farmland along a soil clay gradient on the Chinese Loess Plateau. Land Degrad Dev, 2018, 29: 3521-3534, DOI
66	Zhang W, Liu W, Xu M, Deng J, Han X, Yang G, Feng Y, Ren G. Response of forest growth to C:N: P stoichiometry in plants and soils during Robinia pseudoacacia afforestation on the Loess Plateau, China. Geoderma, 2019, 337: 280-289, DOI
67	Zhang W, Xu Y, Gao D, Wang X, Liu W, Deng J, Han X, Yang G, Feng Y, Ren G. Ecoenzymatic stoichiometry and nutrient dynamics along a revegetation chronosequence in the soils of abandoned land and Robinia pseudoacacia plantation on the Loess Plateau, China. Soil Biol Biochem, 2019, 134: 1-14, DOI
68	Zhang J, Li M, Xu L, Zhu J, Dai G, He N. C:N: P stoichiometry in terrestrial ecosystems in China. Sci Total Environ, 2021, 795, DOI
69	Zhao H, He N, Xu L, Zhang X, Wang Q, Wang B, Yu G. Variation in the nitrogen concentration of the leaf, branch, trunk, and root in vegetation in China. Ecol Indic, 2019, 96: 496-504, DOI