Skip to main content
Log in

An invasive aster (Ageratina adenophora) invades and dominates forest understories in China: altered soil microbial communities facilitate the invader and inhibit natives

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Exotic plant invasion may alter underground microbial communities, and invasion-induced changes of soil biota may also affect the interaction between invasive plants and resident native species. Increasing evidence suggests that feedback of soil biota to invasive and native plants leads to successful exotic plant invasion. To examine this possible underlying invasion mechanism, soil microbial communities were studied where Ageratina adenophora was invading a native forest community. The plant–soil biota feedback experiments were designed to assess the effect of invasion-induced changes of soil biota on plant growth, and interactions between A. adenophora and three native plant species. Soil analysis showed that nitrate nitrogen (NO 3 -N), ammonium nitrogen (NH +4 -N), and available P and K content were significantly higher in a heavily invaded site than in a newly invaded site. The structure of the soil microbial community was clearly different in all four sites. Ageratina adenophora invasion strongly increased the abundance of soil VAM (vesicular-arbuscular mycorrhizal fungi) and the fungi/bacteria ratio. A greenhouse experiment indicated that the soil biota in the heavily invaded site had a greater inhibitory effect on native plant species than on A. adenophora and that soil biota in the native plant site inhibited the growth of native plant species, but not of A. adenophora. Soil biota in all four sites increased A. adenophora relative dominance compared with each of the three native plant species and soil biota in the heavily invaded site had greater beneficial effects on A. adenophora relative dominance index (20% higher on average) than soil biota in the non-invaded site. Our results suggest that A. adenophora is more positively affected by the soil community associated with native communities than are resident natives, and once the invader becomes established it further alters the soil community in a way that favors itself and inhibits natives, helping to promote the invasion. Soil biota alteration after A. adenophora establishment may be an important part of its invasion process to facilitate itself and inhibit native plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Allen EB, Allen MF (1984) Competition between plants of different successional stages: mycorrhizae as regulators. Can J Bot 62:2625–2629

    Article  Google Scholar 

  • Augspurger CK, Kelly CK (1984) Pathogen mortality of tropical tree seedlings: experimental studies of the effects of dispersal distance, seedling density, and light conditions. Oecologia 61:211–217

    Article  Google Scholar 

  • Bååth E, Diaz-Ravińa M, Frostegård Å, Campbell CD (1998) Effect of metal-rich sludge amendments on the soil microbial community. Appl Environ Microb 64:238–245

    Google Scholar 

  • Bao SD (2000) Soil and agricultural chemistry analysis. Chinese Agricultural Press, Beijing, pp 100–109

    Google Scholar 

  • Bardgett RD, Hobbs PJ, Frostegård Å (1996) Changes in soil fungal:bacterial ratios following reductions in the intensity of management of an upland grassland. Biol Fertil Soils 22:261–264

    Google Scholar 

  • Beckstead J, Parker IM (2003) Invasiveness of Ammophila arenaria: release from soil-borne pathogens? Ecology 84:2824–2831

    Article  Google Scholar 

  • Bever JD (2002) Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Pro R Soc Lond B 269:2595–2601

    Article  Google Scholar 

  • Bever JD (2003) Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol 157:465–473

    Article  Google Scholar 

  • Bever JD, Westover KM, Antonovics J (1997) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J Ecol 85:561–573

    Article  Google Scholar 

  • Borga P, Nilsson M, Tunlid A (1994) Bacterial communities in peat in relation to botanical composition as revealed by phospholipid fatty acid analysis. Soil Biol Biochem 7:841–848

    Article  Google Scholar 

  • Brown VK, Gange AC (1989) Herbivory by soil-dwelling insects depresses plant species richness. Funct Ecol 3:667–671

    Article  Google Scholar 

  • Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521–523

    Article  PubMed  CAS  Google Scholar 

  • Callaway RM, Newingham B, Zabinski CA, Mahall BE (2001) Compensatory growth and competitive ability of an invasive weed are enhanced by soil fungi and native neighbors. Ecol Lett 4:429–433

    Article  Google Scholar 

  • Callaway RM, Thelen GC, Barth S, Ramsey PW, Gannon JE (2004a) Soil fungi alter interactions between the invader Centaurea maculosa and north American natives. Ecology 85:1062–1071

    Article  Google Scholar 

  • Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004b) Soil biota and exotic plant invasion. Nature 427:731–733

    Article  CAS  Google Scholar 

  • De Deyn GB, Raaijmakers CE, Van Der Putten WH (2004) Plant community development is affected by nutrients and soil biota. J Ecol 92:824–834

    Article  Google Scholar 

  • Dewalt SJ, Denslow JS, Ickes K (2004) Natural-enemy release facilitates habitat expansion of the invasive tropical shrub Clidemia hirta. Ecology 85:471–483

    Article  Google Scholar 

  • Drijber RA, Doran JW, Parkhurst AM, Lyond DJ (2000) Changes in soil microbial community structure with tillage under long-term wheat-fallow management. Soil Biol Biochem 32:1419–1430

    Article  CAS  Google Scholar 

  • Duda JJ, Freeman DC, Emlen JM, Belnap J, Kitchen SG, Zak JC, Sobek E, Tracy M, Montante J (2003) Difference in native soil ecology associated with invasion of exotic annual chenopod, Halogeton glomeratus. Biol Fertil Soils 38:72–77

    Article  CAS  Google Scholar 

  • Frostegård Å, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65

    Google Scholar 

  • Frostegård Å, Bååth E, Tunlid A 1993a Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty acid analysis. Soil Biol Biochem 25:723–730

    Article  Google Scholar 

  • Frostegård Å, Tunlid A, Bååth E 1993b Phospholipid fatty acid composition, biomass, and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Appl Environ Microb 59:3605–3617

    Google Scholar 

  • Garbaye J (1994) Tansley review no. 76 helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210

    Article  Google Scholar 

  • Grayston SJ, Griffth GS, Mawdsley JL, Campbell C D, Bardgett RD (2001) Accounting for variability in soil microbial communities of temperate upland grassland ecosystems. Soil Biol Biochem 33:533–551

    Article  CAS  Google Scholar 

  • Hawkes CV, Wren IF, Herman DJ, Firestone MK (2005) Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol Lett 8:976–985

    Article  Google Scholar 

  • Hierro JL, Maron JL, Callaway RM (2005) A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. J Ecol 93:5–15

    Article  Google Scholar 

  • Hill GT, Mitkowski NA, Aldrich-Wolfe L, Emele LR, Jurkonie DD, Ficke A, Maldonado-Ramirez, Lynch ST, Nelson EB (2000) Methods for assessing the composition and diversity of soil microbial communities. Appl Soil Ecol 15:25–36

    Article  Google Scholar 

  • Horiuchi J, Prithiviraj B, Kimball BA, Vivanco JM (2005) Soil nematodes mediate positive interactions between legume plants and Rhizobium bacteria. Planta 222:848–857

    Article  PubMed  CAS  Google Scholar 

  • Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70

    Article  PubMed  CAS  Google Scholar 

  • Knevel IC, Lans T, Menting FBJ, Hertling UM, van der Putten WH (2004). Release from native root herbivores and biotic resistance by soil pathogens in a new habitat both affect the alien Ammophila arenaria in South Africa. Oecologia 141:502–510

    Article  PubMed  Google Scholar 

  • Kourtev PS, Ehrenfeld JG, Häggblom M (2003) Experimental analysis of the effect of exotic and native plant species on the structure and function of soil microbial communities. Soil Biol Biochem 35:895–905

    Article  CAS  Google Scholar 

  • Kourtev PS, Ehrenfeld JG, Häggblom M (2002) Exotic plant species alter the microbial community structure and function in the soil. Ecology 83:3152–3166

    Google Scholar 

  • Kourtev PS, Ehrenfeld JG, Huang WZ (1998) Effects of exotic plant species on soil properties in hardwood forests of New Jersey. Water Air Soil Poll 105:493–501

    Article  CAS  Google Scholar 

  • Li WH, Zhang CB, Jiang HB, Xin GR, Yang ZY (2006) Changes in soil microbial community associated with invasion of the exotic weed, Mikania micrantha H.B.K. Plant Soil 281:309–324

    Article  CAS  Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Google Scholar 

  • Marler MJ, Zabinski CA, Callaway RM (1999) Mycorrhizae indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology 80:1180–1186

    Google Scholar 

  • Mills KE, Bever JD (1998) Maintenance of diversity within plant communities: soil pathogens as agents of negative feedback. Ecology 79:1595–1601

    Article  Google Scholar 

  • Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627

    Article  PubMed  CAS  Google Scholar 

  • Myers J H, Bazely R (2003) Appendix-Some tools for studying plant populations. In Ecology and control of introduced plants. Cambridge University Press, pp 255

  • Olsen S R, Sommers L E (1982) Phosphorus. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, Part 2. Am Soc Agron, Soil Sci. Soc. Am, Madison, Wisconsin, pp 403–430

  • Olsson S, Alström S (2000) Characterization of bacteria in soils under barley monoculture and crop rotation. Soil Biol Biochem 32:1443–1451

    Article  CAS  Google Scholar 

  • Packer A, Clay K (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404:278–281

    Article  PubMed  CAS  Google Scholar 

  • Packer A, Clay K (2002) Soil pathogens and Prunus serotina seedlings and sapling growth near conspecific trees. Ecology 84:108–119

    Article  Google Scholar 

  • Qiang S (1998) The history and status of the study on Crofton weed (Eupatorium Spreng.): A worst worldwide weed. J Wuhan Botl Res 16(4):366–372

    Google Scholar 

  • Reinhart KO, Callaway RM (2004) Soil biota facilitate exotic Acer invasions in Europe and north America. Ecol Appl 14:1737–1745

    Article  Google Scholar 

  • Reinhart KO, Callaway RM (2006) Soil biota and invasive plants. New Phytol 170:445–457

    Article  PubMed  Google Scholar 

  • Reinhart KO, Packer A, van der Putten WH, Clay K (2003) plant–soil biota interactions and spatial distribution of black cherry in its native and invasive ranges. Ecol Lett 6:1046–1050

    Article  Google Scholar 

  • Reinhart KO, Royo AA, van der Patten WH, Clay K (2005) Soil feedback and pathogen activity in Prunus serotina throughout its native range. J Ecol 93:890–898

    Article  Google Scholar 

  • Reynolds HL, Packer A, Bever JD, Clay K (2003) Plant–microbe–soil interactions as drivers of plant community structure and dynamics. Ecology 84:2281–2291

    Article  Google Scholar 

  • Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmanek M (2000) Plant invasions-the role of mutualisms. Biol Rev Camb Philos Soc 75:65–93

    Article  PubMed  CAS  Google Scholar 

  • Roberts KJ, Anderson RC (2001) Effect of garlic mustard (Alliaria petiolata) extracts on plants and arbuscular mycorrhizal (AM) fungi. Am Midl Nat 146:146–152

    Article  Google Scholar 

  • Suding KN, LeJeune KD, Seastedt TR (2004) Competitive impacts and responses of an invasive weed: dependencies on nitrogen and phosphorus availability. Oecologia 141:526–535

    Article  PubMed  Google Scholar 

  • Sun XY, Lu ZH, Sang WG (2004) Review on studies of Eupatorium adenophorum—an important invasive species in China. J Fore Rese l5:319–322

    Google Scholar 

  • van der Putten WH (2001) Interactions of plants, soil pathogens and their antagonists in natural ecosystems. In: Jeger MJ, Spence NJ (eds) Biotic interactions in plant-pathogen associations. CAB International, New York, USA, pp 285–305

    Google Scholar 

  • van der Putten WH, Dijk CV, Peters AM (1993) Host-specific soil-borne diseases contribute to succession in foredune vegetation. Nature 362:53–56

    Article  Google Scholar 

  • Vaughn SF, Berhow MA (1999) Allelochemicals isolated from tissues of the invasive weed garlic mustard (Alliaria petiolata). J Chem Ecol 25:2495–2504

    Article  CAS  Google Scholar 

  • Vestal JR, White DC (1989) Lipid analysis in microbial ecology. BioScience 39:535–541

    Article  PubMed  CAS  Google Scholar 

  • Vitousek PM, Walker LR, Whiteaker LD, Mueller-Dombois D, Matson PA (1987) Biological invasion by Myrica faya alters ecosystem development in Hawaii. Science 238:802–804

    Article  PubMed  Google Scholar 

  • Vivanco JM, Bais HP, Stermitz FR, Thelen GC, Callaway RM (2004) Biogeographical variation in community response to root allelochemistry: novel weapons and exotic invasion. Ecol. Lett. 285–292

  • Waldrop MP, Balser TC, Firestone MK (2000) Linking microbial community composition to function in a tropical soil. Soil Biol Biochem 32:1837–1846

    Article  CAS  Google Scholar 

  • Wang JJ (2005) Ageratina adenophora (Spreng.). In: Wan FH, Zheng XB, Guo JY (eds) Biology and management of invasive alien species in agriculture and forestry. Science Press, Beijing, pp 651–661

    Google Scholar 

  • Westover KM, Bever JD (2001) Mechanisms of plant species coexistence: complementary roles of rhizosphere bacteria and root fungal pathogens. Ecology 82:3285–3294

    Google Scholar 

  • White DC, Davis WM, Nickels JS, King JD, Bobbie RJ (1979) Determination of the sedimentary microbial biomass by extractible lipid phosphate. Oecologia 40:51–62

    Article  Google Scholar 

  • Wolfe BE, Klironoms JN (2005) Breaking new ground: soil communities and exotic plant invasion. BioScience 55:477–493

    Article  Google Scholar 

  • Yang GQ, Wan FH, Liu WX, Zhang XW (2006) Physiological effects of allelochemicals from leachates of Ageratina adenophora (Spreng.) on rice seedlings. Allelopathy J 18:237–246

    Google Scholar 

  • Yao H, He Z, Wilson MJ, Campbell CD (2000) Microbial biomass and community structure in a sequence of soils with increasing fertility and changing land use. Microbial Ecol 40:223–237

    CAS  Google Scholar 

  • Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities: a review. Biol Fertil Soils 29:111–129

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Dr Li Yan-shan, Yunnan Agricultural University, for assistance with measurement of soil characteristics and our colleague Jiang Zhi-lin for finding experimental sites and for field work. We also thank Dr Jiang Ling-Huo and Dr Imtiaz Khan, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, for reviewing this manuscript. This study was funded by the National Basic Research and Development Programme, China. (2002CB111400) and International Science and Technology Cooperation Programme (2005DFA31090).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fang-hao Wan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Niu, Hb., Liu, Wx., Wan, Fh. et al. An invasive aster (Ageratina adenophora) invades and dominates forest understories in China: altered soil microbial communities facilitate the invader and inhibit natives. Plant Soil 294, 73–85 (2007). https://doi.org/10.1007/s11104-007-9230-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-007-9230-8

Keywords

Navigation