Evaluating physiological changes of grass and semishrub species with seasonality for understanding the process of shrub encroachment in semiarid grasslands
Liu Yang A B , Jihua Zhou A , Liming Lai A , Qinglin Sun A B , Sangui Yi A B , Lianhe Jiang A and Yuanrun Zheng A CA Key Laboratory of Resource Plants, West China Subalpine Botanical Garden, Institute of Botany, Chinese Academy of Sciences, Xiangshan, Beijing, China.
B University of Chinese Academy of Sciences, Beijing, China.
C Corresponding author. Email: zhengyr@ibcas.ac.cn
Functional Plant Biology 47(7) 628-638 https://doi.org/10.1071/FP19194
Submitted: 9 July 2019 Accepted: 18 February 2020 Published: 15 May 2020
Abstract
Shrub encroachment occurs worldwide, especially in arid and semiarid grasslands. Changes in soil water in different layers affect the process of shrub encroachment. Understanding the biological and physiological responses of plant species to shrub encroachment is essential for explaining shrub encroachment. The dominant species in six typical plant communities changed from Stipa bungeana Trin. to Artemisia ordosica Krasch., representing different shrub-encroached grasslands. The gravimetric soil water content (SWC) and enzyme and osmotic adjustment compounds of the dominant species across shrub encroachment stages and growing seasons were measured to explain the shrub encroachment. Results showed that SWC decreased and then increased during the growing seasons. With the process of shrub encroachment, SWC first increased, then decreased. With increasing soil depth, SWC increased or decreased. Across seasons with decreasing SWC, enzyme activity decreased and then increased, and malondialdehyde content and osmotic adjustment compounds increased. With the process of shrub encroachment, enzyme activity, malondialdehyde content and osmotic adjustment compounds increased or decreased. The two dominant species (S. bungeana and A. ordosica) enhanced their drought resistance abilities by regulating their antioxidant systems and osmotic adjustment compounds when soil water in a specific layer was not over the threshold. We recommend increasing the clay content to increase the water holding capacity in the surface soil layer to restore the zonal vegetation of S. bungeana.
Additional keywords: antioxidant enzyme activity, osmotic adjustment compounds.
References
Ansari WA, Atri N, Singh B, Kumar P, Pandey S (2018) Morpho-physiological and biochemical responses of muskmelon genotypes to different degree of water deficit. Photosynthetica 56, 1019–1030.| Morpho-physiological and biochemical responses of muskmelon genotypes to different degree of water deficit.Crossref | GoogleScholarGoogle Scholar |
Belayneh A, Tessema ZK (2017) Mechanisms of bush encroachment and its inter-connection with rangeland degradation in semi-arid African ecosystems: a review. Journal of Arid Land 9, 299–312.
| Mechanisms of bush encroachment and its inter-connection with rangeland degradation in semi-arid African ecosystems: a review.Crossref | GoogleScholarGoogle Scholar |
Cai WT, Guan TY, Li HY, Lai LM, Zhang XL, Zhou JH, Jiang LH, Zheng YR (2018) Vegetation succession of abandoned croplands in Ruanliang and Yingliang in the Ordos Plateau. Acta Ecologica Sinica 38, 21–28.
| Vegetation succession of abandoned croplands in Ruanliang and Yingliang in the Ordos Plateau.Crossref | GoogleScholarGoogle Scholar |
Caracciolo D, Istanbulluoglu E, Noto LV, Collins SL (2016) Mechanisms of shrub encroachment into Northern Chihuahuan Desert grasslands and impacts of climate change investigated using a cellular automata model. Advances in Water Resources 91, 46–62.
| Mechanisms of shrub encroachment into Northern Chihuahuan Desert grasslands and impacts of climate change investigated using a cellular automata model.Crossref | GoogleScholarGoogle Scholar |
Case MF, Staver AC (2017) Fire prevents woody encroachment only at higher-than-historical frequencies in a South African savanna. Journal of Applied Ecology 54, 955–962.
| Fire prevents woody encroachment only at higher-than-historical frequencies in a South African savanna.Crossref | GoogleScholarGoogle Scholar |
Chakhchar A, Wahbi S, Lamaoui M, Ferradous A, El Mousadik A, Ibnsouda-Koraichi S, Filali-MaltoufEl A, El Modafar C (2015) Physiological and biochemical traits of drought tolerance in Argania spinosa. Journal of Plant Interactions 10, 252–261.
| Physiological and biochemical traits of drought tolerance in Argania spinosa.Crossref | GoogleScholarGoogle Scholar |
Chen LY, Li H, Zhang PJ, Zhao X, Zhou LH, Liu TY, Hu HF, Bai YF, Shen HH, Fang JY (2015) Climate and native grassland vegetation as drivers of the community structures of shrub-encroached grasslands in Inner Mongolia, China. Landscape Ecology 30, 1627–1641.
| Climate and native grassland vegetation as drivers of the community structures of shrub-encroached grasslands in Inner Mongolia, China.Crossref | GoogleScholarGoogle Scholar |
Cipriotti PA, Aguiar MR, Wiegand T, Paruelo JM (2014) A complex network of interactions controls coexistence and relative abundances in Patagonian grass-shrub steppes. Journal of Ecology 102, 776–788.
| A complex network of interactions controls coexistence and relative abundances in Patagonian grass-shrub steppes.Crossref | GoogleScholarGoogle Scholar |
D’Odorico P, Okin GS, Bestelmeyer BT (2012) A synthetic review of feedbacks and drivers of shrub encroachment in arid grasslands. Ecohydrology 5, 520–530.
| A synthetic review of feedbacks and drivers of shrub encroachment in arid grasslands.Crossref | GoogleScholarGoogle Scholar |
Donovan LA, Ehleringer JR (1994) Water stress and use of summer precipitation in a Great Basin shrub community. Functional Ecology 8, 289–297.
| Water stress and use of summer precipitation in a Great Basin shrub community.Crossref | GoogleScholarGoogle Scholar |
Fan Y, Li XY, Huang H, Wu XC, Yu KL, Wei JQ, Zhang CC, Wang P, Hu X, D’Odorico P (2019) Does phenology play a role in the feedbacks underlying shrub encroachment? Science of the Total Environment 657, 1064–1073.
| Does phenology play a role in the feedbacks underlying shrub encroachment?Crossref | GoogleScholarGoogle Scholar | 30677874PubMed |
Fort F, Volaire F, Guilioni L, Barkaoui K, Navas ML, Roumet C (2017) Root traits are related to plant water-use among rangeland Mediterranean species. Functional Ecology 31, 1700–1709.
| Root traits are related to plant water-use among rangeland Mediterranean species.Crossref | GoogleScholarGoogle Scholar |
Ge YJ, He XY, Wang JF, Jiang B, Ye RH, Lin XC (2014) Physiological and biochemical responses of Phoebe bournei seedlings to water stress and recovery. Acta Physiologiae Plantarum 36, 1241–1250.
| Physiological and biochemical responses of Phoebe bournei seedlings to water stress and recovery.Crossref | GoogleScholarGoogle Scholar |
Germino MJ, Reinhardt K (2014) Desert shrub responses to experimental modification of precipitation seasonality and soil depth: relationship to the two-layer hypothesis and ecohydrological niche. Journal of Ecology 102, 989–997.
| Desert shrub responses to experimental modification of precipitation seasonality and soil depth: relationship to the two-layer hypothesis and ecohydrological niche.Crossref | GoogleScholarGoogle Scholar |
Haider MS, Kurjogi MM, Khalil-ur-Rehman M, Pervez T, Songtao J, Fiaz M, Jogaiah S, Wang C, Fang JG (2018) Drought stress revealed physiological, biochemical and gene-expressional variations in ‘“Yoshihime”‘ peach (Prunus Persica L) cultivar. Journal of Plant Interactions 13, 83–90.
| Drought stress revealed physiological, biochemical and gene-expressional variations in ‘“Yoshihime”‘ peach (Prunus Persica L) cultivar.Crossref | GoogleScholarGoogle Scholar |
Jia X, Sun CS, Li GY, Li GB, Chen GL (2015) Effects of progressive drought stress on the physiology, antioxidative enzymes and secondary metabolites of Radix astragali. Acta Physiologiae Plantarum 37, 262
| Effects of progressive drought stress on the physiology, antioxidative enzymes and secondary metabolites of Radix astragali.Crossref | GoogleScholarGoogle Scholar |
Kaur G, Asthir B (2017) Molecular responses to drought stress in plants. Biologia Plantarum 61, 201–209.
| Molecular responses to drought stress in plants.Crossref | GoogleScholarGoogle Scholar |
Kulmatiski A, Beard KH (2013) Woody plant encroachment facilitated by increased precipitation intensity. Nature Climate Change 3, 833–837.
| Woody plant encroachment facilitated by increased precipitation intensity.Crossref | GoogleScholarGoogle Scholar |
Luvuno L, Biggs R, Stevens N, Esler K (2018) Woody encroachment as a social-ecological regime shift. Sustainability 10, 2221
| Woody encroachment as a social-ecological regime shift.Crossref | GoogleScholarGoogle Scholar |
Marjanović Ž, Glišić A, Mutavdžić D, Saljnikov E, Bragato G (2015) Ecosystems supporting Tuber magnatum Pico production in Serbia experience specific soil environment seasonality that may facilitate truffle lifecycle completion. Applied Soil Ecology 95, 179–190.
| Ecosystems supporting Tuber magnatum Pico production in Serbia experience specific soil environment seasonality that may facilitate truffle lifecycle completion.Crossref | GoogleScholarGoogle Scholar |
Rao DE, Chaitanya KV (2016) Photosynthesis and antioxidative defense mechanisms in deciphering drought stress tolerance of crop plants. Biologia Plantarum 60, 201–218.
| Photosynthesis and antioxidative defense mechanisms in deciphering drought stress tolerance of crop plants.Crossref | GoogleScholarGoogle Scholar |
Reynolds JF, Smith DMS, Lambin EF, Turner BL, Mortimore M, Batterbury SPJ, Downing TE, Dowlatabadi H, Fernández RJ, Herrick JE, Huber-Sannwald E, Jiang H, Leemans R, Lynam T, Maestre FT, Ayarza M, Brian Walker B (2007) Global desertification: building a science for dryland development. Science 316, 847–851.
| Global desertification: building a science for dryland development.Crossref | GoogleScholarGoogle Scholar | 17495163PubMed |
Silvertown J, Araya Y, Gowing D (2015) Hydrological niches in terrestrial plant communities: a review. Journal of Ecology 103, 93–108.
| Hydrological niches in terrestrial plant communities: a review.Crossref | GoogleScholarGoogle Scholar |
Skowno AL, Thompson MW, Hiestermann J, Ripley B, West AG, Bond WJ (2017) Woodland expansion in South African grassy biomes based on satellite observations (1990–2013): general patterns and potential drivers. Global Change Biology 23, 2358–2369.
| Woodland expansion in South African grassy biomes based on satellite observations (1990–2013): general patterns and potential drivers.Crossref | GoogleScholarGoogle Scholar | 27732761PubMed |
Stevens N, Erasmus BFN, Archibald S, Bond WJ (2016) Woody encroachment over 70 years in South African savannahs: overgrazing, global change or extinction aftershock? Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 371, 20150437
| Woody encroachment over 70 years in South African savannahs: overgrazing, global change or extinction aftershock?Crossref | GoogleScholarGoogle Scholar | 27502384PubMed |
Thomas AD, Elliott DR, Dougill AJ, Stringer LC, Hoon SR, Sen R (2018) The influence of trees, shrubs, and grasses on microclimate, soil carbon, nitrogen, and CO2 efflux: potential implications of shrub encroachment for Kalahari rangelands. Land Degradation & Development 29, 1306–1316.
| The influence of trees, shrubs, and grasses on microclimate, soil carbon, nitrogen, and CO2 efflux: potential implications of shrub encroachment for Kalahari rangelands.Crossref | GoogleScholarGoogle Scholar |
Thompson JA, Zinnert JC, Young DR (2017) Immediate effects of microclimate modification enhance native shrub encroachment. Ecosphere 8, e01687
| Immediate effects of microclimate modification enhance native shrub encroachment.Crossref | GoogleScholarGoogle Scholar |
Toscano S, Farieri E, Ferrante A, Romano D (2016) Physiological and biochemical responses in two ornamental shrubs to drought stress. Frontiers of Plant Science 7, 645
| Physiological and biochemical responses in two ornamental shrubs to drought stress.Crossref | GoogleScholarGoogle Scholar |
Van Auken OW (2000) Shrub invasions of North American semiarid grasslands. Annual Review of Ecology and Systematics 31, 197–215.
| Shrub invasions of North American semiarid grasslands.Crossref | GoogleScholarGoogle Scholar |
Van Auken OW (2009) Causes and consequences of woody plant encroachment into western North American grasslands. Journal of Environmental Management 90, 2931–2942.
| Causes and consequences of woody plant encroachment into western North American grasslands.Crossref | GoogleScholarGoogle Scholar | 19501450PubMed |
Venter ZS, Cramer MD, Hawkins HJ (2018) Drivers of woody plant encroachment over Africa. Nature Communications 9, 2272
| Drivers of woody plant encroachment over Africa.Crossref | GoogleScholarGoogle Scholar | 29891933PubMed |
Wang YQ, Hu W, Zhu YJ, Shao MA, Xiao S, Zhang CC (2015) Vertical distribution and temporal stability of soil water in 21-m profiles under different land uses on the Loess Plateau in China. Journal of Hydrology 527, 543–554.
| Vertical distribution and temporal stability of soil water in 21-m profiles under different land uses on the Loess Plateau in China.Crossref | GoogleScholarGoogle Scholar |
Wang P, Li XY, Wang LX, Wu XC, Hu X, Fan Y, Tong YQ (2018) Divergent evapotranspiration partition dynamics between shrubs and grasses in a shrub-encroached steppe ecosystem. New Phytologist 219, 1325–1337.
| Divergent evapotranspiration partition dynamics between shrubs and grasses in a shrub-encroached steppe ecosystem.Crossref | GoogleScholarGoogle Scholar | 29862515PubMed |
Weng MY, Cui LR, Liu FL, Zhang M, Shan L, Yang SS, Deng XP (2015) Effects of drought stress on antioxidant enzymes in seedlings of different wheat genotypes. Pakistan Journal of Botany 47, 49–56.
Wilcox BP, Birt A, Fuhlendorf SD, Archer SR (2018) Emerging frameworks for understanding and mitigating woody plant encroachment in grassy biomes. Current Opinion in Environmental Sustainability 32, 46–52.
| Emerging frameworks for understanding and mitigating woody plant encroachment in grassy biomes.Crossref | GoogleScholarGoogle Scholar |
Yang L, Lai LM, Zhou JH, Yi SG, Sun QL, Li HY, Jiang LH, Zheng YR (2019) Enzyme and osmotic adjustment compounds of key species can help explain shrub encroachment in a semiarid sandy grassland. Ecological Indicators 101, 541–551.
| Enzyme and osmotic adjustment compounds of key species can help explain shrub encroachment in a semiarid sandy grassland.Crossref | GoogleScholarGoogle Scholar |
Yu K, D’Odorico P (2014) An ecohydrological framework for grass displacement by woody plants in savannas. Journal of Geophysical Research. Biogeosciences 119, 192–206.
| An ecohydrological framework for grass displacement by woody plants in savannas.Crossref | GoogleScholarGoogle Scholar |
Yu K, Saha MV, D’Odorico P (2017) The Effects of interannual rainfall variability on tree-grass composition along Kalahari rainfall gradient. Ecosystems 20, 975–988.
| The Effects of interannual rainfall variability on tree-grass composition along Kalahari rainfall gradient.Crossref | GoogleScholarGoogle Scholar |
Yuan XK, Yang ZQ, Li YX, Liu Q, Han W (2016) Effects of different levels of water stress on leaf photosynthetic characteristics and antioxidant enzyme activities of greenhouse tomato. Photosynthetica 54, 28–39.
| Effects of different levels of water stress on leaf photosynthetic characteristics and antioxidant enzyme activities of greenhouse tomato.Crossref | GoogleScholarGoogle Scholar |
Zhang Z, Wang SP, Nyren P, Jiang JM (2006) Morphological and reproductive response of Caragana microphylla to different stocking rates. Journal of Arid Environments 67, 671–677.
| Morphological and reproductive response of Caragana microphylla to different stocking rates.Crossref | GoogleScholarGoogle Scholar |
Zhang M, Jin ZQ, Zhao J, Zhang GP, Wu FB (2015) Physiological and biochemical responses to drought stress in cultivated and Tibetan wild barley. Plant Growth Regulation 75, 567–574.
| Physiological and biochemical responses to drought stress in cultivated and Tibetan wild barley.Crossref | GoogleScholarGoogle Scholar |
Zhang CM, Shi SL, Wang BW, Zhao JF (2018) Physiological and biochemical changes in different drought-tolerant alfalfa (Medicago sativa L.) varieties under PEG-induced drought stress. Acta Physiologiae Plantarum 40, 25
| Physiological and biochemical changes in different drought-tolerant alfalfa (Medicago sativa L.) varieties under PEG-induced drought stress.Crossref | GoogleScholarGoogle Scholar |
Zhou Y, Boutton TW, Wu XB (2018) Woody plant encroachment amplifies spatial heterogeneity of soil phosphorus to considerable depth. Ecology 99, 136–147.
| Woody plant encroachment amplifies spatial heterogeneity of soil phosphorus to considerable depth.Crossref | GoogleScholarGoogle Scholar | 29030983PubMed |