Abstract
The exotic plant, Eupatorium adenophorum, has invaded rapidly across southwest China, damaging native ecosystems and causing great economic losses. Soil microbes, as an important component of belowground community, can drive nutrient cycling and regulate plant competition in terrestrial ecosystems. Therefore, knowledge of the soil microbial community and function will enhance our understanding of the mechanism of exotic plant invasive process in natural ecosystems. In this study, we examined the soil microbial community, soil enzyme activity, soil property and plant community along an invasive gradient of E. adenophorum in a southwest Chinese secondary forest. The soil analysis demonstrated that heavy invasion significantly increased the total P and NO −3 -N contents, whereas it significantly decreased the total N and soil organic matter contents. The available P content was significantly decreased by moderate invasion. The E. adenophorum invasion significantly decreased the biomass of total soil microbes, as well as Gram-negative bacteria, actinomycetes, arbuscular mycorrhizal (AM) fungi and non-AM fungi. However, E. adenophorum invasion significantly increased the activities of soil urease, acid phosphatase, polyphenol oxidase and peroxidase. Non-metric multidimensional scaling showed that soil microbial composition and soil enzyme composition were significantly different in the three E. adenophorum invaded sites. Partial Mantel tests indicated that plant composition was the most important factor for structuring soil microbial and enzyme compositions. The results suggest that changes in soil microbial community structure and enzyme activity may play an important role in the process of E. adenophorum invasion in a Chinese secondary forest ecosystem.
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Moles A T, Flores-Moreno H, Bonser S P, et al. Invasions: The trail behind, the path ahead, and a test of a disturbing idea. J Ecol, 2012, 100:116–127
Pejchar L, Mooney H A. Invasive species, ecosystem services and human well-being. Trends Ecol Evol, 2009, 24:497–504
Levine J M, Vila M, D’Antonio C M, et al. Mechanisms underlying the impacts of exotic plant invasions. Proc R Soc Lond B, 2003, 270:775–781
van der Heijen M G A. The unseen majority: Soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett, 2008, 11:651
Wolfe B E, Klironomos J N. Breaking new ground: Soil communities and exotic plant invasion. Bioscience, 2005, 55:477–487
Callaway R M, Thelen G C, Rodriguez A, et al. Soil biota and exotic plant invasion. Nature, 2004, 427:731–733
Wilson G W T, Hickman K R, Williamson M M. Invasive warm-season grasses reduce mycorrhizal root colonization and biomass production of native prairie grasses. Mycorrhiza, 2012, 22:327–336
Arthur M A, Bray S R, Kuchle C R, et al. The influence of the invasive shrub, Lonicera maackii, on leaf decomposition and microbial community dynamics. Plant Ecol, 2012, 213:1571–1582
Elgersma K J, Ehrenfeld J G. Linear and non-linear impacts of a non-native plant invasion on soil microbial community structure and function. Biol Invasions, 2011, 13:757–768
Kourtev P S, Ehrenfeld J G, Haggblom M. Exotic plant species alter the microbial community structure and function in the soil. Ecology, 2002, 83:3152–3166
Lankau R A. Resistance and recovery of soil microbial communities in the face of Alliaria petiolata invasions. New Phytol, 2011, 189:536–548
Li W H, Zhang C B, Jiang H B, et al. Changes in soil microbial community associated with invasion of the exotic weed, Mikania micrantha H.B.K. Plant Soil, 2006, 281:309–324
Lorenzo P, Rodriguez-Echeverria S, Gonzalez L, et al. Effect of invasive Acacia dealbata Link on soil microorganisms as determined by PCR-DGGE. Appl Soil Ecol, 2010, 44:245–251
Blumenthal D, Mitchell C E, Pysek P, et al. Synergy between pathogen release and resource availability in plant invasion. Proc Natl Acad Sci USA, 2009, 106:7899–7904
Reinhart K O, Packer A, Van der Putten W H, et al. Plant-soil biota interactions and spatial distribution of black cherry in its native and invasive ranges. Ecol Lett, 2003, 6:1046–1050
Beckstead J, Meyer S E, Connolly B M, et al. Cheatgrass facilitates spillover of a seed bank pathogen onto native grass species. J Ecol, 2010, 98:168–177
Mangla S, Inderjit, Callaway R M. Exotic invasive plant accumulates native soil pathogens which inhibit native plants. J Ecol, 2008, 96:58–67
Meinhardt K A, Gehring C A. Disrupting mycorrhizal mutualisms: A potential mechanism by which exotic tamarisk outcompetes native cottonwoods. Ecol Appl, 2012, 22:532–549
Stinson K A, Campbell S A, Powell J R, et al. Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol, 2006, 4:727–731
Vogelsang K M, Bever J D. Mycorrhizal densities decline in association with nonnative plants and contribute to plant invasion. Ecology, 2009, 90:399–407
Sun X Y, Lu Z H, Sang W G. Review on studies of Eupatorium adenophorum - an important invasive species in China. J Forest Res, 2004, 15:319–322
Xie Y, Li Z Y, Gregg W P, et al. Invasive species in China - an overview. Biodivers Conserv, 2001, 10:1317–1341
Wan F H, Liu W X, Guo J Y, et al. Invasive mechanism and control strategy of Ageratina adenophora (Sprengel). Sci China Life Sci, 2010, 53:1291–1298
Li Y P, Feng Y L. Differences in seed morphometric and germination traits of crofton weed (Eupatorium adenophorum) from different elevations. Weed Sci, 2009, 57:26–30
Lu H F, Shen J B, Sang W G, et al. Pollen viability, pollination, seed set, and seed germination of croftonweed (Eupatorium adenophorum) in China. Weed Sci, 2008, 56:42–51
Li H, Qiang S, Qian Y L. Physiological response of different croftonweed (Eupatorium adenophorum) populations to low temperature. Weed Sci, 2008, 56:196–202
Wang J F, Feng Y L, Liang H. Adaptation of Eupatorium adenophorum photosynthetic characteristics to light intensity (in Chinese). Chin J Appl Ecol, 2004, 15:1373–1377
Xie L J, Zeng R S, Bi H H, et al. Allelochemical mediated invasion of exotic plants in China. Allelopathy J, 2010, 25:31–50
Yu X J, Yu D, Ma K P. Relationships between allelophthy and invasiveness by Eupatorium adenophorum at different sites (in Chinese). Acta Phytoecol Sin, 2004, 28:773–780
Zhu X Z, Zhang J T, Ma K P. Soil biota reduce allelopathic effects of the invasive Eupatorium adenophorum. PLoS ONE, 2011, 6:e25393
Yu X J, Yu D, Lu Z J, et al. A new mechanism of invader success: Exotic plant inhibits natural vegetation restoration by changing soil microbe community. Chin Sci Bull, 2005, 50:1105–1112
Xu C W, Yang M Z, Chen Y J, et al. Changes in non-symbiotic nitrogen-fixing bacteria inhabiting rhizosphere soils of an invasive plant Ageratina adenophora. Appl Soil Ecol, 2012, 54:32–38
Nelson D W, Sommers L E. Total carbon, organic carbon, and organic matter. In: Sparks D L, Page A L, Helmke P A, et al. eds. Methods of Soil Analysis. Part 3, Chemical Methods. Madison, WI: SSSA, 1996. 961–1010
Scheiner D. Determination of ammonia and Kjeldahl nitrogen by indophenol method. Water Res, 1976, 10:31–36
Mulvaney R L. Nitrogen-inorganic forms. In: Sparks D L, Page A L, Helmke P A, et al. eds. Methods of Soil Analysis. Part 3, Chemical Methods. Madison, WI: SSSA, 1996. 1123–1184
Kuo S. Phosphorus. In: Sparks D L, Page A L, Helmke P A, et al. eds. Methods of Soil Analysis. Part 3, Chemical Methods. Madison, WI: SSSA, 1996. 869–919
Frostegård A, Tunlid A, Bååth E. Phospholipid fatty acid composition, biomass, and activity of microbial communities from 2 soil types experimentally exposed to different heavy metals. Appl Environ Microbiol, 1993, 59:3605–3617
Frostegård A, Bååth E. The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fert Soils, 1996, 22:59–65
Zelles L. Fatty acid patterns of phospholipids and lipopolisaccharides in the characterisation of microbial communities: A review. Biol Fertil Soils, 1999, 29:111–129
Olsson P A. Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol Ecol, 1999, 29:303–310
Kaiser C, Frank A, Wild B, et al. Negligible contribution from roots to soil-borne phospholipid fatty acid fungal biomarkers 18:2ω6,9 and 18:1ω9. Soil Biol Biochem, 2010, 42:1650–1652
Sinsabaugh R L, Antibus R K, Linkins A E, et al. Wood decomposition: Nitrogen and phosphorus dynamics in relation to extracellular enzyme activity. Ecology, 1993, 74:1586–1593
Kandeler E, Gerber H. Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fert Soils, 1988, 6:68–72
Schinner F, von Mersi W. Xylanase-, CM-cellulase- and invertase activity in soil: An improved method. Soil Biol Biochem, 1990, 22:511–515
Zhou L K, Zhang Z M. The determination method of soil enzyme activity (in Chinese). Chin J Soil Sci, 1980, 5:37–49
Frostegård Å, Tunlid A, Bååth E. Use and misuse of PLFA measurements in soils. Soil Biol Biochem, 2011, 43:1621–1625
R Development Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. 2011
Oksanen J, Kindt R, Legendre P, et al. The vegan package. http://vegan.r-forge.r-project.org/.2007
Goslee S C, Urban D L. The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw, 2007, 22:1–19
Broz A K, Manter D K, Vivanco J M. Soil fungal abundance and diversity: Another victim of the invasive plant Centaurea maculosa. ISME J, 2007, 1:763–765
Allison S D, Nielsen C, Hughes R F. Elevated enzyme activities in soils under the invasive nitrogen-fixing tree Falcataria moluccana. Soil Biol Biochem, 2006, 38:1537–1544
Batten K M, Scow K M, Davies K F, et al. Two invasive plants alter soil microbial community composition in serpentine grasslands. Biol Invasions, 2006, 8:217–230
Inderjit, van der Putten W H. Impacts of soil microbial communities on exotic plant invasions. Trends Ecol Evol, 2010, 25:512–519
Arvind N, Amit S. Antimicrobial potential of Eupatorium adenophorum Spreng. Pharmacogn J, 2010, 2:61–64
Eskelinen A, Stark S, Mannisto M. Links between plant community composition, soil organic matter quality and microbial communities in contrasting tundra habitats. Oecologia, 2009, 161:113–123
Hernandez D L, Hobbie S E. The effects of substrate composition, quantity, and diversity on microbial activity. Plant Soil, 2010, 335:397–411
Sinsabaugh R L. Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem, 2010, 42:391–404
Sanon A, Béguiristain T, Cébron A, et al. Changes in soil diversity and global activities following invasions of the exotic invasive plant, Amaranthus viridis L., decrease the growth of native sahelian Acacia species. FEMS Microbiol Ecol, 2009, 70:118–131
Christian J M, Wilson S D. Long-term ecosystem impacts of an introduced grass in the northern Great Plains. Ecology, 1999, 80: 2397–2407
Liao C Z, Peng R H, Luo Y Q, et al. Altered ecosystem carbon and nitrogen cycles by plant invasion: A meta-analysis. New Phytol, 2008, 177:706–714
Bandick A K, Dick R P. Field management effects on soil enzyme activities. Soil Biol Biochem, 1999, 31:1471–1479
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Sun, X., Gao, C. & Guo, L. Changes in soil microbial community and enzyme activity along an exotic plant Eupatorium adenophorum invasion in a Chinese secondary forest. Chin. Sci. Bull. 58, 4101–4108 (2013). https://doi.org/10.1007/s11434-013-5955-3
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DOI: https://doi.org/10.1007/s11434-013-5955-3