Soil patch heterogeneity improves plant productivity and nutrients regulated by arbuscular mycorrhizal fungi
Tingting Xia
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorYun Guo
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
College of Eco-Environmental Engineering, Guizhou Minzu University, Guiyang, China
Search for more papers by this authorPan Wu
Key Laboratory of Karst Georesources and Environment, Ministry of Education, Guizhou University, Guiyang, China
Search for more papers by this authorYing Zhao
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorXinyang Xu
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorXu Han
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorKaiping Shen
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorBangli Wu
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorYan Sun
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorWenda Ren
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorQing Li
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorJinting Li
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorXiaorun Hu
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorLi Wang
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorCorresponding Author
Yuejun He
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Correspondence
Yuejun He, Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang 550025, China.
Email: [email protected]
Search for more papers by this authorTingting Xia
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorYun Guo
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
College of Eco-Environmental Engineering, Guizhou Minzu University, Guiyang, China
Search for more papers by this authorPan Wu
Key Laboratory of Karst Georesources and Environment, Ministry of Education, Guizhou University, Guiyang, China
Search for more papers by this authorYing Zhao
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorXinyang Xu
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorXu Han
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorKaiping Shen
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorBangli Wu
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorYan Sun
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorWenda Ren
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorQing Li
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorJinting Li
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorXiaorun Hu
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorLi Wang
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Search for more papers by this authorCorresponding Author
Yuejun He
Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang, China
Correspondence
Yuejun He, Forestry College, Research Center of Forest Ecology, Guizhou University, Guiyang 550025, China.
Email: [email protected]
Search for more papers by this authorAbstract
The interlacing and mosaic distribution of karst soil and rock result in the high spatial heterogeneity of the natural karst habitat. Karst plants are suffered from spatially heterogeneous microhabitats with different-sized patches. Arbuscular mycorrhizal (AM) fungi are crucial in regulating plant productivity and nutrients in heterogeneous karst environments. However, how spatial patch heterogeneity influences plant productivity and nutrient utilization by AM fungi regulation in karst soil remains unclear. A simulated heterogeneity experiment regarding soil grid patches was conducted by planting Bidens pilosa into a microcosm of a square device. Experimental treatments included the mycorrhizal fungus treatments inoculation with (M+) or non-inoculation with (M−) Glomus etunicatum fungus, and the spatial heterogeneity treatments involved homogeneous patches (HO), heterogeneity-small patches (HS), and heterogeneity-large patches (HL). The growth and nutritional traits of plants were analyzed. The results showed that AM fungus promoted the productivity and nutrient uptake of B. pilosa by substantial increases in biomass, nitrogen (N) accumulation, phosphorus (P) accumulation, and N/P ratio. The spatial heterogeneity promoted the biomass and N and P accumulations of B. pilosa when inoculating with AM fungus. The mycorrhizal colonization rate and hyphae length were greater in HS than in HO and HL under the M+ treatment, with a greater response ratio of biomass, N and P under HS conditions. These indicated that the heterogeneous small patches had a greater promotion of the biomass production and nutrients of B. pilosa with inoculation of AM fungus because extensive fungal hyphae can acquire soil resources in more distant patches outside the root zone with more economical metabolic costs compared to roots. We thus conclude that patch heterogeneity contributes to plant productivity and nutrient utilization regulated by AM fungi in karst soil, and the broader nutrient capture induced by extraradical hyphae of AM fungi may be an adaptive mechanism for karst plants to cope with heterogeneous environmental conditions.
CONFLICT OF INTEREST STATEMENT
The authors do not have a conflict of interest to declare.
Open Research
DATA AVAILABILITY STATEMENT
Research data are not shared.
REFERENCES
- Adomako, M. O., Roiloa, S., & Yu, F. H. (2022). Potential roles of soil microorganisms in regulating the effect of soil nutrient heterogeneity on plant performance. Microorganisms, 10, 1–17. https://doi.org/10.3390/microorganisms10122399
- Adomako, M. O., Wei, X., Lin, D. D., & Hai, Y. F. (2021). Soil biota and soil substrates influence responses of the rhizomatous clonal grass Leymus chinensis to nutrient heterogeneity. Plant and Soil, 465, 19–29. https://doi.org/10.1007/s11104-021-04967-0
- Bao, S. D. (2000). Soil and agricultural chemistry analysis. China Agriculture Press.
- Cahill, J. F., Jr., & McNickle, G. G. (2011). The behavioral ecology of nutrient foraging by plants. Annual Review of Ecology Evolution and Systematics, 42, 289–311. https://doi.org/10.1146/annurev-ecolsys-102710-145006
- Carter, M. R., & Gregorich, E. G. (2007). Soil sampling and methods of analysis. CRC press.
10.1201/9781420005271 Google Scholar
- Chen, D., Ali, A., Yong, X. H., Lin, C. G., Niu, X. H., Cai, A. M., Dong, B. C., Zhou, Z. X., Wang, Y. J., & Yu, F. H. (2019). A multi-species comparison of selective placement patterns of ramets in invasive alien and native clonal plants to light, soil nutrient and water heterogeneity. Science of the Total Environment, 657, 1568–1577. https://doi.org/10.1016/j.scitotenv.2018.12.099
- Chen, H., Nie, Y., & Wang, K. (2013). Spatio-temporal heterogeneity of water and plant adaptation mechanisms in karst regions: A review. Acta Ecologica Sinica, 33, 317–326. https://doi.org/10.5846/stxb201112011836
10.5846/stxb201112011836 Google Scholar
- Chen, W., Koide, R. T., & Eissenstat, D. M. (2018). Nutrient foraging by mycorrhizas: From species functional traits to ecosystem processes. Functional Ecology, 32, 858–869. https://doi.org/10.1111/1365-2435.13041
- Coleman, M. C. S. (1999). Biomass allocation in plants: Ontogeny or optimality? A test along three resource gradients. Ecology, 80, 2581–2593. https://doi.org/10.1890/0012-9658(1999)080[2581:BAIPOO]2.0.CO;2
- Croft, S. A., Hodge, A., & Pitchford, J. W. (2012). Optimal root proliferation strategies: The roles of nutrient heterogeneity, competition and mycorrhizal networks. Plant and Soil, 351, 191–206. https://doi.org/10.1007/s11104-011-0943-3
- Day, K., Hutchings, M., & John, E. (2003). The effects of spatial pattern of nutrient supply on the early stages of growth in plant populations. Journal of Ecology, 91, 305–315. https://doi.org/10.1046/j.1365-2745.2003.00763.x
- Dong, B., Wang, J., Liu, R., Zhang, M., Luo, F., & Yu, F. (2015). Soil heterogeneity affects ramet placement of Hydrocotyle vulgaris. Journal of Plant Ecology, 8, 91–100. https://doi.org/10.1093/jpe/rtu003
- Facelli, E., & Facelli, J. M. (2002). Soil phosphorus heterogeneity and mycorrhizal symbiosis regulate plant intra-specific competition and size distribution. Oecologia, 133, 54–61. https://doi.org/10.1007/s00442-002-1022-5
- Felderer, B., Jansa, J., & Schulin, R. (2013). Interaction between root growth allocation and mycorrhizal fungi in soil with patchy P distribution. Plant and Soil, 373, 569–582. https://doi.org/10.1007/s11104-013-1818-6
- Frew, A., Powell, J. R., & Johnson, S. N. (2020). Aboveground resource allocation in response to root herbivory as affected by the arbuscular mycorrhizal symbiosis. Plant and Soil, 447, 463–473. https://doi.org/10.1007/s11104-019-04399-x
- Fridley, J. D., Grime, J. P., Askew, A. P., Moser, B., & Stevens, C. (2011). Soil heterogeneity buffers community response to climate change in species-rich grassland. Global Change Biology, 17, 2002–2011. https://doi.org/10.1111/j.1365-2486.2010.02347.x
- Gazol, A., Tamme, R., Price, J. N., Hiiesalu, I., Laanisto, L., & Pärtel, M. (2013). A negative heterogeneity–diversity relationship found in experimental grassland communities. Oecologia, 173, 545–555. https://doi.org/10.1007/s00442-013-2623-x
- Giovannetti, M., & Mosse, B. (1980). An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. The New Phytologist, 84, 489–500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x
- Guo, Y., Wang, B., Li, D., Mallik, A. U., Xiang, W., Ding, T., Wen, S., Lu, S., Huang, F., & He, Y. (2017). Effects of topography and spatial processes on structuring tree species composition in a diverse heterogeneous tropical karst seasonal rainforest. Flora, 231, 21–28. https://doi.org/10.1016/j.flora.2017.04.002
- He, Y., Cornelissen, J. H., Wang, P., Dong, M., & Ou, J. (2019). Nitrogen transfer from one plant to another depends on plant biomass production between conspecific and heterospecific species via a common arbuscular mycorrhizal network. Environemental Science and Pollution Research, 26, 8828–8837. https://doi.org/10.1007/s11356-019-04385-x
- He, Y., Jiang, C., Yang, H., Wang, Y., & Zhong, Z. (2017). Arbuscular mycorrhizal fungal composition affects the growth and nutrient acquisition of two plants from a karst area. Sains Malays, 46, 1701–1708. https://doi.org/10.17576/jsm-2017-4610-05
- Heck, C., Kuhn, H., Heidt, S., Walter, S., Rieger, N., & Requena, N. (2016). Symbiotic fungi control plant root cortex development through the novel GRAS transcription factor MIG1. Current Biology, 26, 2770–2778. https://doi.org/10.1016/j.cub.2016.07.059
- Hedges, L. V., & Curtis, G. (1999). The meta-analysis of response ratios in experimental ecology. Ecology, 80, 1150–1156. https://doi.org/10.2307/177062
- Heijden, M., Wiemken, A., & Sanders, I. R. (2010). Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occurring plant. The New Phytologist, 157, 569–578. https://doi.org/10.1046/j.1469-8137.2003.00688.x
10.1046/j.1469-8137.2003.00688.x Google Scholar
- Hodge, A. (2004). The plastic plant: Root responses to heterogeneous supplies of nutrients. The New Phytologist, 162, 9–24. https://doi.org/10.1111/j.1469-8137.2004.01015.x
- Hodge, A., Berta, G., Doussan, C., Merchan, F., & Crespi, M. (2009). Plant root growth, architecture and function. Plant and Soil, 321, 153–187. https://doi.org/10.1007/s11104-009-9929-9
- Hutchings, M. J., John, E. A., & Wijesinghe, D. K. (2003). Toward understanding the consequences of soil heterogeneity for plant populations and communities. Ecology, 84, 2322–2334. https://doi.org/10.1890/02-0290
- Hutchings, M. J., & Wijesinghe, D. K. (1997). Patchy habitats, division of labour and growth dividends in clonal plants. Trends in Ecology & Evolution, 12, 390–394. https://doi.org/10.1016/S0169-5347(97)87382-X
- Jiang, Z., Lian, Y., & Qin, X. (2014). Rocky desertification in Southwest China: Impacts, causes, and restoration. Earth Science Reviews, 132, 1–12. https://doi.org/10.1016/j.earscirev.2014.01.005
- Koerselman, W., & Meuleman, F. M. A. (1996). The vegetation N:P ratio: A new tool to detect the nature of nutrient limitation. Journal of Applied Ecology, 33, 1441–1450. https://doi.org/10.2307/2404783
- Kume, T., Sekiya, N., & Yano, K. (2006). Heterogeneity in spatial P-distribution and foraging capability by Zea mays: Effects of patch size and barriers to restrict root proliferation within a patch. Annals of Botany, 98, 1271–1277. https://doi.org/10.1093/aob/mcl216
- Li, H., Wang, X., Rengel, Z., Ma, Q., Zhang, F., & Shen, J. (2016). Root over-production in heterogeneous nutrient environment has no negative effects on Zea mays shoot growth in the field. Plant and Soil, 409, 405–417. https://doi.org/10.1007/s11104-016-2963-5
- Li, S., Liu, J., Li, J., Deng, Y., Chen, J., Wang, J., Song, H., Zhang, J., Tao, J., & Liu, J. (2021). Reproductive strategies involving biomass allocation, reproductive phenology and seed production in two Asteraceae herbs growing in karst soil varying in depth and water availability. Plant Ecology, 222, 737–747. https://doi.org/10.1007/s11258-021-01141-5
- Li, S., Ren, H., Xue, L., Chang, J., & Yao, X. (2014). Influence of bare rocks on surrounding soil moisture in the karst rocky desertification regions under drought conditions. Catena, 116, 157–162. https://doi.org/10.1016/j.catena.2013.12.013
- Liang, Y. M., Pan, F., Jiang, Z. C., Li, Q., Pu, J. B., & Liu, K. P. (2022). Accumulation in nutrient acquisition strategies of arbuscular mycorrhizal fungi and plant roots in poor and heterogeneous soils of karst shrub ecosystems. BMC Plant Biology, 22, 188. https://doi.org/10.1186/s12870-022-03514-y
- Linderman, R. G., & Brenda, B. (1981). Quantifying vesicular-arbuscular mycorrhizae: A proposed method towards standardization. The New Phytologist, 87, 63–67. https://doi.org/10.2307/2485121
- Liu, L., Alpert, P., Dong, B. C., Li, J. M., & Yu, F. H. (2017). Combined effects of soil heterogeneity, herbivory and detritivory on growth of the clonal plant Hydrocotyle vulgaris. Plant and Soil, 421, 429–437. https://doi.org/10.1007/s11104-017-3476-6
- Liu, X., Peng, Y., Li, J., & Peng, P. (2018). Enhanced shoot investment makes invasive plants exhibit growth advantages in high nitrogen conditions. Brazilian Journal of Biology, 79, 15–21. https://doi.org/10.1590/1519-6984.169578
- Liu, Y., Li, G., Wang, M., Yan, W., & Hou, F. (2021). Effects of three-dimensional soil heterogeneity and species composition on plant biomass and biomass allocation of grass-mixtures. AoB Plants, 13, plab033. https://doi.org/10.1093/aobpla/plab033
- Luo, Y., Peng, Q., Li, K., Gong, Y., & Han, W. (2021). Patterns of nitrogen and phosphorus stoichiometry among leaf, stem and root of desert plants and responses to climate and soil factors in Xinjiang, China. Catena, 199, 105100. https://doi.org/10.1016/j.catena.2020.105100
- Miransari, M. (2011). Arbuscular mycorrhizal fungi and nitrogen uptake. Archives of Microbiology, 193, 77–81. https://doi.org/10.1007/s00203-010-0657-6
- Orwin, K. H., Bertram, J., Clough, T., Condron, L., Sherlock, R., & O'Callaghan, M. (2009). Short-term consequences of spatial heterogeneity in soil nitrogen concentrations caused by urine patches of different sizes. Applied Soil Ecology, 42, 271–278. https://doi.org/10.1016/j.apsoil.2009.05.002
- Qian, Y. Q., Luo, D., Gong, G., & Han, L. (2014). Effects of spatial scale of soil heterogeneity on the growth of a clonal plant producing both spreading and clumping ramets. Journal of Plant Growth Regulation, 33, 214–221. https://doi.org/10.1007/s00344-013-9365-1
- Reynolds, H. L., Mittelbach, G. G., Darcy-Hall, T. L., Houseman, G. R., & Gross, K. L. (2007). No effect of varying soil resource heterogeneity on plant species richness in a low fertility grassland. Journal of Ecology, 95, 723–733. https://doi.org/10.1111/j.1365-2745.2007.01252.x
- Rillig, M. C., Wright, S. F., Shaw, M. R., & Field, C. B. (2002). Artificial climate warming positively affects arbuscular mycorrhizae but decreases soil aggregate water stability in an annual grassland. Oikos, 97, 52–58. https://doi.org/10.1034/j.1600-0706.2002.970105.x
- Roiloa, S. R., & Hutchings, M. J. (2013). The effects of physiological integration on biomass partitioning in plant modules: An experimental study with the stoloniferous herb Glechoma hederacea. Plant Ecology, 214, 521–530. https://doi.org/10.1007/s11258-013-0186-x
- Rugemalila, D. M., Cory, S. T., Smith, W. K., & Anderson, T. M. (2020). The role of microsite sunlight environment on growth, architecture, and resource allocation in dominant Acacia tree seedlings, in Serengeti, East Africa. Plant Ecology, 221, 1187–1199. https://doi.org/10.1007/s11258-020-01074-5
- Saia, S., Benítez, E., García-Garrido, J. M., Settanni, L., Amato, G., & Giambalvo, D. (2014). The effect of arbuscular mycorrhizal fungi on total plant nitrogen uptake and nitrogen recovery from soil organic material. The Journal of Agricultural Science, 152, 370–378. https://doi.org/10.1017/S002185961300004X
- Shen, J., Yuan, L., Zhang, J., Li, H., Bai, Z., Chen, X., Zhang, W., & Zhang, F. (2011). Phosphorus dynamics: From soil to plant. Plant Physiology, 156, 997–1005. https://doi.org/10.1104/PP.111.175232
- Shen, K., Cornelissen, J. H. C., Wang, Y., Wu, C., He, Y., Ou, J., Tan, Q., Xia, T., Kang, L., & Guo, Y. (2020). AM fungi alleviate phosphorus limitation and enhance nutrient competitiveness of invasive plants via mycorrhizal networks in karst areas. Frontiers in Ecology and Evolution, 8, 125. https://doi.org/10.3389/fevo.2020.00125
- Shen, N., Yu, H., Yu, S., Yu, D., & Liu, C. (2019). Does soil nutrient heterogeneity improve the growth performance and intraspecific competition of the invasive plant Myriophyllum aquaticum? Frontiers in Plant Science, 10, 723. https://doi.org/10.3389/fpls.2019.00723
- Shi, Z., Wang, F., Zhang, C., & Yang, Z. (2011). Exploitation of phosphorus patches with different phosphorus enrichment by three arbuscular mycorrhizal fungi. Journal of Plant Nutrition, 34, 1096–1106. https://doi.org/10.1080/01904167.2011.558154
- Si, C., Xue, W., Guo, Z. W., Zhang, J. F., & Yu, F. H. (2021). Soil heterogeneity and earthworms independently promote growth of two bamboo species. Ecological Indicators, 130, 108068. https://doi.org/10.1016/j.ecolind.2021.108068
- Simard, S. W., Beiler, K. J., Bingham, M. A., Deslippe, J. R., Philip, L. J., & Teste, F. P. (2012). Mycorrhizal networks: Mechanisms, ecology and modelling. Fungal Biology Reviews, 26, 39–60. https://doi.org/10.1016/j.fbr.2012.01.001
10.1016/j.fbr.2012.01.001 Google Scholar
- Smith, S. E., & David Read, F. (2008). Mycorrhizal symbiosis ( Third ed.). Academic Press.
- Tedersoo, L., Bahram, M., & Zobel, M. (2020). How mycorrhizal associations drive plant population and community biology. Science, 367, p.eaba1223. https://doi.org/10.1126/science.aba1223
- Veresoglou, S. D., Menexes, G., & Rillig, M. C. (2012). Do arbuscular mycorrhizal fungi affect the allometric partition of host plant biomass to shoots and roots? A meta-analysis of studies from 1990 to 2010. Mycorrhiza, 22, 227–235. https://doi.org/10.1007/s00572-011-0398-7
- Vitousek, P. M., Porder, S., Houlton, B. Z., & Chadwick, O. A. (2010). Terrestrial phosphorus limitation: Mechanisms, implications, and nitrogen–phosphorus interactions. Ecological Applications, 20, 5–15. https://doi.org/10.1890/08-0127.1
- Walder, F., Niemann, H., Natarajan, M., Lehmann, M. F., Boller, T., & Wiemken, A. (2012). Mycorrhizal networks: Common goods of plants shared under unequal terms of trade. Plant Physiology, 159, 789–797. https://doi.org/10.1104/pp.112.195727
- Wang, B., & Qiu, Y. (2006). Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza, 16, 299–363. https://doi.org/10.1007/s00572-005-0033-6
- Wang, Y. J., Shi, X. P., Meng, X. F., Wu, X. J., Luo, F. L., & Yu, F. H. (2016). Effects of spatial patch arrangement and scale of covarying resources on growth and intraspecific competition of a clonal plant. Frontiers in Plant Science, 7, 753. https://doi.org/10.3389/fpls.2016.00753
- Xia, T., Wang, Y. J., He, Y. J., Wu, C. B., & Han, X. (2020). An invasive plant experiences greater benefits of root morphology from enhancing nutrient competition associated with arbuscular mycorrhizae in karst soil than a native plant. PLoS ONE, 15, e0234410. https://doi.org/10.1371/journal.pone.0234410
- Xia, Z., He, Y., Yu, L., Lv, R., Korpelainen, H., & Li, C. (2020). Sex-specific strategies of phosphorus (P) acquisition in Populus cathayana as affected by soil P availability and distribution. The New Phytologist, 225, 782–792. https://doi.org/10.1111/nph.16170
- Xing, D., Wang, Z. H., Xiao, J. J., Han, S. Y., Luo, C. B., Zhang, A. M., Song, L. L., & Gao, X. B. (2018). The composition and diversity of arbuscular mycorrhizal fungi in karst soils and roots collected from mulberry of different ages. Ciencia Rural, 48, 1–14. https://doi.org/10.1590/0103-8478cr20180361
- Yamato, M., Suzuki, T., Matsumoto, M., Shiraishi, T., & Yukawa, T. (2021). Mycoheterotrophic seedling growth of Gentiana zollingeri, a photosynthetic Gentianaceae plant species, in symbioses with arbuscular mycorrhizal fungi. Journal of Plant Research, 134, 921–931. https://doi.org/10.1007/s10265-021-01311-6
- Yan, X. L., Wang, C., Ma, X., & Wu, P. (2019). Root morphology and seedling growth of three tree species in southern China in response to homogeneous and heterogeneous phosphorus supplies. Trees-Structure and Function, 33, 1283–1297. https://doi.org/10.1007/s00468-019-01858-x
- Yang, Z., & Midmore, D. J. (2005). Modelling plant resource allocation and growth partitioning in response to environmental heterogeneity. Ecological Modelling, 181, 59–77. https://doi.org/10.1016/j.ecolmodel.2004.06.023
- Zhang, Q., Xiong, G., Li, J., Lu, Z., Li, Y., Xu, W., Wang, Y., Zhao, C., Tang, Z., & Xie, Z. (2018). Nitrogen and phosphorus concentrations and allocation strategies among shrub organs: The effects of plant growth forms and nitrogen-fixation types. Plant and Soil, 427, 305–319. https://doi.org/10.1007/s11104-018-3655-0
- Zhang, W., Zhao, J., Pan, F., Li, D., Chen, H., & Wang, K. (2015). Changes in nitrogen and phosphorus limitation during secondary succession in a karst region in Southwest China. Plant and Soil, 391, 77–91. https://doi.org/10.1007/s11104-015-2406-8
- Zhang, Z., Zhang, J., Xu, G., Zhou, L., & Li, Y. (2019). Arbuscular mycorrhizal fungi improve the growth and drought tolerance of Zenia insignis seedlings under drought stress. New Forest, 50, 593–604. https://doi.org/10.1007/s11056-018-9681-1
- Zhao, N., Yu, G., He, N., Xia, F., Wang, Q., Wang, R., Xu, Z., & Jia, Y. (2016). Invariant allometric scaling of nitrogen and phosphorus in leaves, stems, and fine roots of woody plants along an altitudinal gradient. Journal of Plant Research, 129, 647–657. https://doi.org/10.1007/s10265-016-0805-4
- Zhao, W., Liu, T., Liu, Y., Wang, H., Wang, R., Ma, Q., Dong, H., & Bi, X. (2021). The significance of biomass allocation to population growth of the invasive species Ambrosia artemisiifolia and Ambrosia trifida with different densities. BMC Ecology and Evolution, 21, 1–13. https://doi.org/10.1186/s12862-021-01908-4
