Advertisement

Plant and Soil

, Volume 294, Issue 1–2, pp 73–85 | Cite as

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

  • Hong-bang Niu
  • Wan-xue Liu
  • Fang-hao Wan
  • Bo Liu
Regular Article

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.

Keywords

Ageratina adenophora Feedback of soil biota Exotic plant invasion Facilitation Mutualisms Underground invasion mechanism 

Notes

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).

References

  1. Allen EB, Allen MF (1984) Competition between plants of different successional stages: mycorrhizae as regulators. Can J Bot 62:2625–2629CrossRefGoogle Scholar
  2. 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 61:211–217CrossRefGoogle Scholar
  3. Bååth E, Diaz-Ravińa M, Frostegård Å, Campbell CD (1998) Effect of metal-rich sludge amendments on the soil microbial community. Appl Environ Microb 64:238–245Google Scholar
  4. Bao SD (2000) Soil and agricultural chemistry analysis. Chinese Agricultural Press, Beijing, pp 100–109Google Scholar
  5. 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 22:261–264Google Scholar
  6. Beckstead J, Parker IM (2003) Invasiveness of Ammophila arenaria: release from soil-borne pathogens? Ecology 84:2824–2831CrossRefGoogle Scholar
  7. Bever JD (2002) Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Pro R Soc Lond B 269:2595–2601CrossRefGoogle Scholar
  8. Bever JD (2003) Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol 157:465–473CrossRefGoogle Scholar
  9. Bever JD, Westover KM, Antonovics J (1997) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J Ecol 85:561–573CrossRefGoogle Scholar
  10. 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 7:841–848CrossRefGoogle Scholar
  11. Brown VK, Gange AC (1989) Herbivory by soil-dwelling insects depresses plant species richness. Funct Ecol 3:667–671CrossRefGoogle Scholar
  12. Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521–523PubMedCrossRefGoogle Scholar
  13. 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 4:429–433CrossRefGoogle Scholar
  14. 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 85:1062–1071CrossRefGoogle Scholar
  15. Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004b) Soil biota and exotic plant invasion. Nature 427:731–733CrossRefGoogle Scholar
  16. De Deyn GB, Raaijmakers CE, Van Der Putten WH (2004) Plant community development is affected by nutrients and soil biota. J Ecol 92:824–834CrossRefGoogle Scholar
  17. Dewalt SJ, Denslow JS, Ickes K (2004) Natural-enemy release facilitates habitat expansion of the invasive tropical shrub Clidemia hirta. Ecology 85:471–483CrossRefGoogle Scholar
  18. 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 32:1419–1430CrossRefGoogle Scholar
  19. 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 38:72–77CrossRefGoogle Scholar
  20. Frostegård Å, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65Google Scholar
  21. 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 25:723–730CrossRefGoogle Scholar
  22. 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 59:3605–3617Google Scholar
  23. Garbaye J (1994) Tansley review no. 76 helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210CrossRefGoogle Scholar
  24. 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 33:533–551CrossRefGoogle Scholar
  25. Hawkes CV, Wren IF, Herman DJ, Firestone MK (2005) Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol Lett 8:976–985CrossRefGoogle Scholar
  26. 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 93:5–15CrossRefGoogle Scholar
  27. 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 15:25–36CrossRefGoogle Scholar
  28. Horiuchi J, Prithiviraj B, Kimball BA, Vivanco JM (2005) Soil nematodes mediate positive interactions between legume plants and Rhizobium bacteria. Planta 222:848–857PubMedCrossRefGoogle Scholar
  29. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70PubMedCrossRefGoogle Scholar
  30. 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 141:502–510PubMedCrossRefGoogle Scholar
  31. 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 35:895–905CrossRefGoogle Scholar
  32. Kourtev PS, Ehrenfeld JG, Häggblom M (2002) Exotic plant species alter the microbial community structure and function in the soil. Ecology 83:3152–3166Google Scholar
  33. 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 105:493–501CrossRefGoogle Scholar
  34. 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 281:309–324CrossRefGoogle Scholar
  35. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710Google Scholar
  36. Marler MJ, Zabinski CA, Callaway RM (1999) Mycorrhizae indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology 80:1180–1186Google Scholar
  37. Mills KE, Bever JD (1998) Maintenance of diversity within plant communities: soil pathogens as agents of negative feedback. Ecology 79:1595–1601CrossRefGoogle Scholar
  38. Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627PubMedCrossRefGoogle Scholar
  39. Myers J H, Bazely R (2003) Appendix-Some tools for studying plant populations. In Ecology and control of introduced plants. Cambridge University Press, pp 255Google Scholar
  40. 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 403–430Google Scholar
  41. Olsson S, Alström S (2000) Characterization of bacteria in soils under barley monoculture and crop rotation. Soil Biol Biochem 32:1443–1451CrossRefGoogle Scholar
  42. Packer A, Clay K (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404:278–281PubMedCrossRefGoogle Scholar
  43. Packer A, Clay K (2002) Soil pathogens and Prunus serotina seedlings and sapling growth near conspecific trees. Ecology 84:108–119CrossRefGoogle Scholar
  44. 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):366–372Google Scholar
  45. Reinhart KO, Callaway RM (2004) Soil biota facilitate exotic Acer invasions in Europe and north America. Ecol Appl 14:1737–1745CrossRefGoogle Scholar
  46. Reinhart KO, Callaway RM (2006) Soil biota and invasive plants. New Phytol 170:445–457PubMedCrossRefGoogle Scholar
  47. 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 6:1046–1050CrossRefGoogle Scholar
  48. 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 93:890–898CrossRefGoogle Scholar
  49. Reynolds HL, Packer A, Bever JD, Clay K (2003) Plant–microbe–soil interactions as drivers of plant community structure and dynamics. Ecology 84:2281–2291CrossRefGoogle Scholar
  50. Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmanek M (2000) Plant invasions-the role of mutualisms. Biol Rev Camb Philos Soc 75:65–93PubMedCrossRefGoogle Scholar
  51. Roberts KJ, Anderson RC (2001) Effect of garlic mustard (Alliaria petiolata) extracts on plants and arbuscular mycorrhizal (AM) fungi. Am Midl Nat 146:146–152CrossRefGoogle Scholar
  52. Suding KN, LeJeune KD, Seastedt TR (2004) Competitive impacts and responses of an invasive weed: dependencies on nitrogen and phosphorus availability. Oecologia 141:526–535PubMedCrossRefGoogle Scholar
  53. Sun XY, Lu ZH, Sang WG (2004) Review on studies of Eupatorium adenophorum—an important invasive species in China. J Fore Rese l5:319–322Google Scholar
  54. 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 285–305Google Scholar
  55. van der Putten WH, Dijk CV, Peters AM (1993) Host-specific soil-borne diseases contribute to succession in foredune vegetation. Nature 362:53–56CrossRefGoogle Scholar
  56. Vaughn SF, Berhow MA (1999) Allelochemicals isolated from tissues of the invasive weed garlic mustard (Alliaria petiolata). J Chem Ecol 25:2495–2504CrossRefGoogle Scholar
  57. Vestal JR, White DC (1989) Lipid analysis in microbial ecology. BioScience 39:535–541PubMedCrossRefGoogle Scholar
  58. Vitousek PM, Walker LR, Whiteaker LD, Mueller-Dombois D, Matson PA (1987) Biological invasion by Myrica faya alters ecosystem development in Hawaii. Science 238:802–804CrossRefPubMedGoogle Scholar
  59. 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. 285–292Google Scholar
  60. Waldrop MP, Balser TC, Firestone MK (2000) Linking microbial community composition to function in a tropical soil. Soil Biol Biochem 32:1837–1846CrossRefGoogle Scholar
  61. 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 651–661Google Scholar
  62. Westover KM, Bever JD (2001) Mechanisms of plant species coexistence: complementary roles of rhizosphere bacteria and root fungal pathogens. Ecology 82:3285–3294Google Scholar
  63. White DC, Davis WM, Nickels JS, King JD, Bobbie RJ (1979) Determination of the sedimentary microbial biomass by extractible lipid phosphate. Oecologia 40:51–62CrossRefGoogle Scholar
  64. Wolfe BE, Klironoms JN (2005) Breaking new ground: soil communities and exotic plant invasion. BioScience 55:477–493CrossRefGoogle Scholar
  65. Yang GQ, Wan FH, Liu WX, Zhang XW (2006) Physiological effects of allelochemicals from leachates of Ageratina adenophora (Spreng.) on rice seedlings. Allelopathy J 18:237–246Google Scholar
  66. 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 40:223–237Google Scholar
  67. Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities: a review. Biol Fertil Soils 29:111–129CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Hong-bang Niu
    • 1
    • 2
  • Wan-xue Liu
    • 1
    • 2
  • Fang-hao Wan
    • 1
    • 2
  • Bo Liu
    • 3
  1. 1.The State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant ProtectionChinese Academy of Agricultural SciencesBeijingP.R. China
  2. 2.Center for Management of Invasive Alien SpeciesMinistry of AgricultureBeijingP.R. China
  3. 3.Biotechnology Research InstituteFujian Academy of Agricultural SciencesFuzhouP.R. China

Personalised recommendations