增温对林木细根物候影响的研究进展
收稿日期: 2022-08-11
录用日期: 2023-03-13
网络出版日期: 2023-03-16
基金资助
国家自然科学基金(32071743);国家自然科学基金(32192433);福建省科技厅公益类项目(2022R1002004)
Effects of warming on fine root phenology of forests: a review
Received date: 2022-08-11
Accepted date: 2023-03-13
Online published: 2023-03-16
Supported by
National Natural Science Foundation of China(32071743);National Natural Science Foundation of China(32192433);Public Welfare Projects of Science and Technology Department of Fujian Province(2022R1002004)
林木细根物候是观测全球变暖影响的重要指标。全球变化背景下, 细根物候不仅反映林木的生长状况变化, 也揭示着陆地生态系统碳循环和地下碳分配动态。林木细根物候对气候变化的响应是全球变化研究的热点和难点, 国内外已开展了大量研究工作, 目前部分研究认为土壤增温将延长林木细根的物候期, 并且北半球一些地区春季物候期、生长高峰期均提前, 而大气增温有可能抑制细根生长, 推迟其物候期, 此外还有研究发现表层土壤中的根系物候受增温的影响可能比深层根系更大。同时, 一些学者将细根物候与根际土壤环境、微生物和地上物候几个方面相联系以研究其响应机制, 但细根物候如何响应气候变暖以及这些响应可能的机制仍未有定论。为此, 该文系统阐述了全球变暖背景下林木细根物候的研究进展, 以期为地下物候学研究以及林木对全球变化的响应和适应机制研究提供参考, 并认为今后还需加强以下几个方面的研究: 1)改进和探索更精确的模拟增温方式并开展更长时间尺度的量化研究; 2)探究变化环境下林木根系不同功能模块(如吸收根/运输根, 纤维根/先锋根)与其物候的联系, 即将“环境-性状-物候”相关联; 3)综合考虑根系物候的控制因素在不同地下物候相(根系生长开始、生长峰值、生长停止)、物种、土层的差异性; 4)关注地下、地上物候相互关联及其对植物生产力影响的研究; 5)增温与其他环境因子(CO2浓度、氮沉降等)综合作用下的林木地下物候与生态系统功能变化(如碳汇、养分循环等)间联系应是未来研究的重点方向。
陈心怡, 吴晨, 黄锦学, 熊德成 . 增温对林木细根物候影响的研究进展[J]. 植物生态学报, 2023 , 47(11) : 1471 -1482 . DOI: 10.17521/cjpe.2022.0326
The fine root phenology of forests is an important indicator to observe the impact of global warming. It can reflect not only the growth status of forests under the background of global change but also the dynamics of the carbon cycle and below-ground carbon distribution of terrestrial ecosystems. Meanwhile, the response of forest fine root phenology to climate change is considered a hotspot and challenge in the field of global change effects, and thus has been studied extensively. Recent studies claim that soil warming will prolong the growing season of fine roots in forests as the spring phenology and growth peak will begin earlier in some areas of the northern hemisphere, however, atmospheric warming may inhibit the growth of fine roots and delay the phenological events. In addition, some studies found that the root phenology in the surface soil may be more affected by warming than that in the deep layer. Concurrently, some researchers associated fine root phenology with rhizosphere soil environment, microorganisms and above-ground phenology to reveal the response mechanism. However, the response of fine root phenology to climate warming and its underlying mechanisms have not been fully explained. This paper systematically reviewed changes in fine root phenology in forests under global warming, and aimed to provide references for the research on below-ground phenology, and the response and adaptation mechanism of forests to global changes. Future studies should enhance the research on the following aspects: 1) improving and exploring more accurate simulation warming devices and carrying out long-term quantitative research; 2) exploring the relationship between different functional modules of roots (such as absorbing root/transporting root, fibrous root/pioneering root) and their phenology under changing environments, i.e. “environment-traits- phenology”; 3) considering variations of the control factors of root phenology under different below-ground phenological phases (the beginning, peak and end of root growth), species and soil layers; 4) focusing on the relationship between below- and above-ground phenology, and its impacts on plant productivity; 5) focus on the changes of forest below-ground phenology and ecosystem functions (such as carbon sinks, nutrient cycling, etc.) under the combined effect of warming and other environmental factors (CO2 concentration, nitrogen deposition, etc.).
| [1] | Abramoff RZ, Finzi AC (2015). Are above- and below-ground phenology in sync? New Phytologist, 205, 1054-1061. |
| [2] | Adamczyk B, Sieti? OM, Straková P, Prommer J, Wild B, Hagner M, Pihlatie M, Fritze H, Richter A, Heinonsalo J (2019). Plant roots increase both decomposition and stable organic matter formation in boreal forest soil. Nature Communications, 10, 104-108. |
| [3] | Allison SD, Treseder KK (2008). Warming and drying suppress microbial activity and carbon cycling in boreal forest soils. Global Change Biology, 14, 2898-2909. |
| [4] | Alvarez-Uria P, K?rner C (2007). Low temperature limits of root growth in deciduous and evergreen temperate tree species. Functional Ecology, 21, 211-218. |
| [5] | Antonino DI, Valentino G, Donato C (2016). Acclimation of fine root respiration to soil warming involves starch deposition in very fine and fine roots: a case study in Fagus sylvatica saplings. Physiologia Plantarum, 165, 294-310. |
| [6] | Canham CA, Froend RH, Stock WD, Davies M (2012). Dynamics of phreatophyte root growth relative to a seasonally fluctuating water table in a Mediterranean-type environment. Oecologia, 170, 909-916. |
| [7] | Chen HYH, Brassard BW (2013). Intrinsic and extrinsic controls of fine root life span. Critical Reviews in Plant Sciences, 32, 151-161. |
| [8] | Chen XL, Wang GX, Yang Y, Yang Y (2015). Response of soil surface enzyme activities to short-term warming and litter decomposition in a mountain forest. Acta Ecologica Sinica, 35, 7071-7079. |
| [8] | [陈晓丽, 王根绪, 杨燕, 杨阳 (2015). 山地森林表层土壤酶活性对短期增温及凋落物分解的响应. 生态学报, 35, 7071-7079.] |
| [9] | Chmielewski FM, R?tzer T (2001). Response of tree phenology to climate change across Europe. Agricultural and Forest Meteorology, 108, 101-112. |
| [10] | Danjon F, Reubens B (2008). Assessing and analyzing 3D architecture of woody root systems, a review of methods and applications in tree and soil stability, resource acquisition and allocation. Plant and Soil, 303, 1-34. |
| [11] | Dawes MA, Schleppi P, H?ttenschwiler S, Rixen C, Hagedorn F (2017). Soil warming opens the nitrogen cycle at the alpine treeline. Global Change Biology, 23, 421-434. |
| [12] | Downie HF, Adu MO, Schmidt S, Otten W, Dupuy LX, White PJ, Valentine TA (2015). Challenges and opportunities for quantifying roots and rhizosphere interactions through imaging and image analysis. Plant, Cell & Environment, 38, 1213-1232. |
| [13] | Du EZ, Fang JY (2014). Linking belowground and aboveground phenology in two boreal forests in Northeast China. Oecologia, 176, 883-892. |
| [14] | Fuchslueger L, Bahn M, Fritz K, Hasibeder R, Richter A (2014). Experimental drought reduces the transfer of recently fixed plant carbon to soil microbes and alters the bacterial community composition in a mountain meadow. New Phytologist, 201, 916-927. |
| [15] | Han MG, Sun LJ, Gan DY, Fu LC, Zhu B (2020). Root functional traits are key determinants of the rhizosphere effect on soil organic matter decomposition across 14 temperate hardwood species. Soil Biology & Biochemistry, 151, 108019. DOI: 10.1016/j.soilbio.2020.108019. |
| [16] | Hasibeder R, Fuchslueger L, Richter A, Bahn M (2015). Summer drought alters carbon allocation to roots and root respiration in mountain grassland. New Phytologist, 205, 1117-1127. |
| [17] | Helmut LPD (1975). Phenology and Seasonality Modeling. Springer, Berlin. |
| [18] | Hertel D, Leuschner C (2006). The in situ root chamber: a novel tool for the experimental analysis of root competition in forest soils. Pedobiologia, 50, 217-224. |
| [19] | Hishi T, Takeda H (2005). Dynamics of heterorhizic root systems: protoxylem groups within the fine-root system of Chamaecyparis obtusa . New Phytologist, 167, 509-521. |
| [20] | Hou YH, Zhou GS, Xu ZZ (2013). An overview of research progress on responses of grassland ecosystems to global warming based on infrared heating experiments. Chinese Journal of Plant Ecology, 37, 1153-1167. |
| [20] | [侯彦会, 周广胜, 许振柱 (2013). 基于红外增温的草地生态系统响应全球变暖的研究进展. 植物生态学报, 37, 1153-1167.] |
| [21] | Hu QJ, Wang LJ, Sheng MY (2019). Research progress of plant fine root production and turnover. World Forestry Research, 32(2), 29-34. |
| [21] | [胡琪娟, 王霖娇, 盛茂银 (2019). 植物细根生产和周转研究进展. 世界林业研究, 32(2), 29-34.] |
| [22] | IPCC (2021). Climate Change 2021: the Physical Science. Cambridge University Press, Cambridge, UK. |
| [23] | Jarvi MP, Burton AJ (2013). Acclimation and soil moisture constrain sugar maple root respiration in experimentally warmed soil. Tree Physiology, 33, 949-959. |
| [24] | Jia LQ (2021). Effects of Soil Warming on Fine Root Turnover and Its Mechanism in a Chinese Fir (Cunninghamia lanceolata) Plantation. Master degree dissertation, Fujian Normal University, Fuzhou. |
| [24] | [贾林巧 (2021). 土壤增温对杉木幼龄林细根生产量的影响. 硕士学位论文, 福建师范大学, 福州.] |
| [25] | Jiang HY, Gu JC, Qiu J, Wang ZQ (2010). Seasonal variations of fine root production and mortality in Larix gmelinii plantation in 2004-2008. Chinese Journal of Applied Ecology, 21, 2465-2471. |
| [25] | [姜红英, 谷加存, 邱俊, 王政权 (2010). 2004-2008年落叶松人工林细根生产和死亡的季节动态. 应用生态学报, 21, 2465-2471.] |
| [26] | Johnson MG, Rygiewicz PT, Tingey DT, Phillips DL (2006). Elevated CO2 and elevated temperature have no effect on Douglas-fir fine-root dynamics in nitrogen-poor soil. New Phytologist, 170, 345-356. |
| [27] | Johnson MG, Tingey DT, Phillips DL, Storm MJ (2001). Advancing fine root research with minirhizotrons. Environmental and Experimental Botany, 45, 263-289. |
| [28] | Keel SG, Campbell CD, H?gberg MN, Richter A, Wild B, Zhou XH, Hurry V, Linder S, N?sholm T, H?gberg P (2012). Allocation of carbon to fine root compounds and their residence times in a boreal forest depend on root size class and season. New Phytologist, 194, 972-981. |
| [29] | King J, Pregitzer K, Zak D, Sober J, Isebrands J, Dickson R, Hendrey G, Karnosky D (2001). Fine-root biomass and fluxes of soil carbon in young stands of paper birch and trembling aspen as affected by elevated atmospheric CO2 and tropospheric O3. Oecologia, 128, 237-250. |
| [30] | Lahti M, Aphalo PJ, Finér L, Ryypp? A, Lehto T, Mannerkoski H (2005). Effects of soil temperature on shoot and root growth and nutrient uptake of 5-year-old Norway spruce seedlings. Tree Physiology, 25, 115-122. |
| [31] | Laskin DN, McDermid GJ, Nielsen SE, Marshall SJ, Roberts DR, Montaghi A (2019). Advances in phenology are conserved across scale in present and future climates. Nature Climate Change, 9, 419-425. |
| [32] | Lepp?lammi-Kujansuu J, Salemaa M, Kleja DB, Linder S, Helmisaari HS (2014). Fine root turnover and litter production of Norway spruce in a long-term temperature and nutrient manipulation experiment. Plant and Soil, 374, 73-88. |
| [33] | Liu HY, Lu CY, Wang SD, Ren F, Wang H (2021). Climate warming extends growing season but not reproductive phase of terrestrial plants. Global Ecology and Biogeography, 30, 950-960. |
| [34] | Liu HY, Wang H, Li N, Shao JJ, Zhou XH, van Groenigen KJ, Thakur MP (2022). Phenological mismatches between above- and belowground plant responses to climate warming. Nature Climate Change, 12, 97-102. |
| [35] | Liu YC, Liu SR, Wan SQ, Wang JX, Wang H, Liu K (2017). Effects of experimental throughfall reduction and soil warming on fine root biomass and its decomposition in a warm temperate oak forest. Science of the Total Environment, 574, 1448-1455. |
| [36] | Liu YJ, Ge QS, Dai JH (2020). Research progress in crop phenology under global climate change. Acta Geographica Sinica, 75, 14-24. |
| [36] | [刘玉洁, 葛全胜, 戴君虎 (2020). 全球变化下作物物候研究进展. 地理学报, 75, 14-24.] |
| [37] | Lucas M, Schlüter S, Vogel HJ, Vetterlein D (2019). Roots compact the surrounding soil depending on the structures they encounter. Scientific Reports, 9, 16236. DOI: 10.1038/s41598-019-52665-w. |
| [38] | Ma ZL, Zhao WQ, Liu M, Liu Q (2019). Effects of warming on microbial biomass carbon and nitrogen in the rhizosphere and bulk soil in an alpine scrub ecosystem. Chinese Journal of Applied Ecology, 30, 1893-1900. |
| [38] | [马志良, 赵文强, 刘美, 刘庆 (2019). 增温对高寒灌丛根际和非根际土壤微生物生物量碳氮的影响. 应用生态学报, 30, 1893-1900.] |
| [39] | Majdi H, ?hrvik J (2004). Interactive effects of soil warming and fertilization on root production, mortality, and longevity in a Norway spruce stand in Northern Sweden. Global Change Biology, 10, 182-188. |
| [40] | Malhotra A, Brice DJ, Childs J, Graham JD, Hobbie EA, Vander Stel H, Feron SC, Hanson PJ, Iversen CM (2020). Peatland warming strongly increases fine-root growth. Proceedings of the National Academy of Sciences of the United States of America, 117, 17627-17634. |
| [41] | Manzoni S, Vico G, Porporato A, Katul G (2013). Biological constraints on water transport in thesoil-plant-atmosphere system. Advances in Water Resources, 51, 292-304. |
| [42] | McCormack ML, Adams TS, Smithwick EAH, Eissenstat DM (2014). Variability in root production, phenology, and turnover rate among 12 temperate tree species. Ecology, 95, 2224-2235. |
| [43] | Piao SL, Liu Q, Chen AP, Janssens IA, Fu YS, Dai JH, Liu LL, Lian X, Shen MG, Zhu XL (2019). Plant phenology and global climate change: current progresses and challenges. Global Change Biology, 25, 1922-1940. |
| [44] | Pregitzer KS, King JS, Burton AJ, Brown SE (2000). Responses of tree fine roots to temperature. New Phytologist, 147, 105-115. |
| [45] | Pregitzer KS, Kubiske ME, Yu CK, Hendrick RL (1997). Relationships among root branch order, carbon, and nitrogen in four temperate species. Oecologia, 111, 302-308. |
| [46] | Rachmilevitch S, Lambers H, Huang BR (2006). Root respiratory characteristics associated with plant adaptation to high soil temperature for geothermal and turf-type Agrostis species. Journal of Experimental Botany, 57, 623-631. |
| [47] | Radville L, McCormack ML, Post E, Eissenstat DM (2016). Root phenology in a changing climate. Journal of Experimental Botany, 67, 3617-3628. |
| [48] | Sadans J, Peuelas J, Esltiate M (2008). Changes in soil enzymes related to C and N cycle and in soil C and N content under prolonged warming and drought in a Mediterranean shrubland. Applied Soil Ecology, 39, 223-235. |
| [49] | Steinaker DF, Wilson SD, Peltzer DA (2009). Asynchronicity in root and shoot phenology in grasses and woody plants. Global Change Biology, 16, 2241-2251. |
| [50] | Svane SF, Dam EB, Carstensen JM, Thorup-Kristensen K (2019). A multispectral camera system for automated minirhizotron image analysis. Plant and Soil, 441, 657-672. |
| [51] | Thomas SM, Whitehead D, Adams JA, Reid JB, Sherlock RR, Leckie AC (1996). Seasonal root distribution and soil surface carbon fluxes for one-year-old Pinus radiata trees growing at ambient and elevated carbon dioxide concentration. Tree Physiology, 16, 1015-1021. |
| [52] | Vogt KA, Grier CC, Vogt DJ (1986). Production, turnover, and nutrient dynamics of above- and belowground detritus of world forests. Advances in Ecological Research, 15, 303-377. |
| [53] | Wang WL, Kong WD, Zeng H (2015). A meta-analysis of responses of soil microbes to warming. Journal of Agro-Environment Science, 34, 2169-2175. |
| [53] | [王文立, 孔维栋, 曾辉 (2015). 土壤微生物对增温响应的Meta分析. 农业环境科学学报, 34, 2169-2175.] |
| [54] | Weger HG, Guy RD (1991). Cytochrome and alternative pathway respiration in white spruce (Picea glauca) roots. Effects of growth and measurement temperature. Physiologia Plantarum, 83, 675-681. |
| [55] | Wells CE, Eissenstat DM (2001). Marked differences in survivorship among apple roots of different diameters. Ecology, 82, 882-892. |
| [56] | Wilson SD, Kalamees R (2014). Below-ground opportunities in vegetation science. Journal of Vegetation Science, 25, 1117-1125. |
| [57] | Wu WH (2003). Plant Physiology. Science Press, Beijing. |
| [57] | [武维华 (2003). 植物生理学. 科学出版社, 北京.] |
| [58] | Wu YB, Zhang J, Deng YC, Wu J, Wang SP, Tang YH, Cui XY (2014). Effects of warming on root diameter, distribution, and longevity in an alpine meadow. Plant Ecology, 215, 1057-1066. |
| [59] | Xia M, Guo D, Pregitzer KS (2010). Ephemeral root modules in Fraxinus mandshurica. New Phytologist, 188, 1065-1074. |
| [60] | Xiao CW, Yang F, Liu JY, Zhou Y, Su JQ, Liang Y, Pei ZQ (2017). Advances in input and output processes of below-ground carbon of terrestrial ecosystems. Chinese Bulletin of Botany, 52, 652-668. |
| [60] | [肖春旺, 杨帆, 柳隽瑶, 周勇, 苏佳琦, 梁韵, 裴智琴 (2017). 陆地生态系统地下碳输入与输出过程研究进展. 植物学报, 52, 652-668.] |
| [61] | Xiong DC, Yang ZJ, Chen GS, Liu XF, Lin WS, Huang JX, Bowles FP, Lin CF, Xie JS, Li YQ, Yang YS (2018). Interactive effects of warming and nitrogen addition on fine root dynamics of a young subtropical plantation. Soil Biology & Biochemistry, 123, 180-189. |
| [62] | Xu CS (2017). The Effects of Air and Soil Warming on the Production and Phenology of Fine Roots of Cunninghamia lanceolata Seedlings. Master degree dissertation, Fujian Normal University, Fuzhou. |
| [62] | [许辰森 (2017). 大气和土壤增温对杉木幼苗细根物候和生产量的影响. 硕士学位论文, 福建师范大学, 福州.] |
| [63] | Xu MH, Yang XH, Du R, Qin RM, Wen J (2021). Effects of simulated warming on the allometric growth patterns of an alpine meadow community on the Qinghai-Tibet Plateau. Pratacultural Science, 38, 618-629. |
| [63] | [徐满厚, 杨晓辉, 杜荣, 秦瑞敏, 温静 (2021). 增温改变高寒草甸植物群落异速生长关系. 草业科学, 38, 618-629.] |
| [64] | Yin CY, Pu XZ, Xiao QY, Zhao CZ, Liu Q (2014). Effects of night warming on spruce root around non-growing season vary with branch order and month. Plant and Soil, 380, 249-263. |
| [65] | Yuan ZY, Chen HYH (2012). Indirect methods produce higher estimates of fine root production and turnover rates than direct methods. PLoS ONE, 7, e48989. DOI: 10.1371/journal.pone.0048989. |
| [66] | Zhang BW (2017). Plant root research methods and trends. Agricultural Science & Technology, 18, 2295-2298. |
| [67] | Zhang JF, Wu D, Gong XY, He Y, Liu F (2012). Non-destructive detection of plant roots based on magnetic resonance imaging technology. Transactions of the Chinese Society of Agricultural Engineering, 28, 181-185. |
| [67] | [张建锋, 吴迪, 龚向阳, 何勇, 刘飞 (2012). 基于核磁共振成像技术的作物根系无损检测. 农业工程学报, 28, 181-185.] |
| [68] | Zhang W, Parker KM, Luo Y, Wan S, Wallace LL, Hu S (2005). Soil microbial responses to experimental warming and clipping in a tallgrass prairie. Global Change Biology, 11, 266-277. |
| [69] | Zhang XQ, Wu KH, Dieter M (2000). A review of methods for fine-root production and turnover of trees. Acta Ecologica Sinica, 20, 875-883. |
| [69] | [张小全, 吴可红,Dieter M (2000). 树木细根生产与周转研究方法评述. 生态学报, 20, 875-883.] |
| [70] | Zhao HY (2019). Adaptation Strategies of Fine Roots of Chinese Fir Seedlings to Soil Warming and Precipitation Exclusion. PhD dissertation, Fujian Normal University, Fuzhou. |
| [70] | [赵海英 (2019). 杉木幼苗细根对土壤增温和隔离降雨的适应策略. 博士学位论文, 福建师范大学, 福州.] |
| [71] | Zhao HY, Chen YY, Xiong DC, Huang JX, Wang WW, Yang ZJ, Chen GS, Yang YS (2017). Fine root phenology differs among subtropical evergreen broadleaved forests with increasing tree diversities. Plant and Soil, 420, 481-491. |
| [72] | Zhu KZ, Wan MW (1973). Phenology. Science Press, Beijing. |
| [72] | [竺可桢, 宛敏渭 (1973). 物候学. 科学出版社, 北京.] |
/
| 〈 |
|
〉 |
