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Mycorrhiza

pp 1–13 | Cite as

AM fungi facilitate the competitive growth of two invasive plant species, Ambrosia artemisiifolia and Bidens pilosa

  • Fengjuan Zhang
  • Qiao Li
  • Ellen Heininger Yerger
  • Xue Chen
  • Qing Shi
  • Fanghao Wan
Original Article
  • 18 Downloads

Abstract

Invasive species often cause enormous economic and ecological damage, and this is especially true for invasive plants in the Asteraceae family. Arbuscular mycorrhizal fungi (AMF) play an important role in the successful invasion by exotic plant species because of their ability to promote growth and influence interspecific competition. However, few studies have evaluated the effects of invasive Asteraceae species on AMF diversity and how feedback mechanisms during competition with native species subsequently affect the accumulation of nutrient resources. Two exotic Asteraceae, Ambrosia artemisiifolia and Bidens pilosa, were monitored during competition with a native grass species, Setaria viridis, which is being replaced by these exotic species in natural areas around the study site. From these species continuously maintained in a field plot for 5 years, we collected the rhizosphere soil and cloned and identified soil AMF. Furthermore, AM fungal spores were isolated from rhizosphere soil of the two invasive species and used as inoculum in greenhouse experiments, to compare growth and nutrient accumulation during competition. The results indicate that although the AMF diversity in the rhizosphere soil of A. artemisiifolia and B. pilosa differed, the three most abundant species (Septoglomus viscosum, Septoglomus constrictum, Glomus perpusillum) were identical. The addition of AMF inoculum changed the competition between the plants, increasing the competitive ability of the invasives and decreasing that of the native. The results show a similar AMF community composition between A. artemisiifolia and B. pilosa, increased AMF root colonization of the invasive species during competition, AMF-enhanced N accumulation, and AMF-facilitated competitive growth of the invasive species.

Keywords

Arbuscular mycorrhizal fungi Asteraceae Interspecific competition Invasive species Soil nutrients 

Notes

Acknowledgements

We thank two anonymous reviewers for helpful comments on the manuscript.

Funding information

This research was funded by the National Natural Science Foundation of China, Grant No. 31372000 and No. 31171906; Hebei National Natural Science Foundation, Grant No. C2015201021 and C2015201241; and Department of Education Project, Grant No. ZD2016039.

Supplementary material

572_2018_866_MOESM1_ESM.pdf (349 kb)
ESM 1 (PPTX 348 kb)

References

  1. Bajpai D, Inderjit (2013) Impact of nitrogen availability and soil communities on biomass accumulation of an invasive species. AoB Plants 5:490–552CrossRefGoogle Scholar
  2. Biermann B, Linderman RG (1981) Quantifying vesicular-arbuscular mycorrhizas: a proposed method towards standardization. New Phytol 87:63–67CrossRefGoogle Scholar
  3. Bunn RA, Ramsey PW, Lekberg Y (2015) Do native and invasive plants differ in their interactions with arbuscular mycorrhizal fungi? A meta-analysis. J Ecol 103:1547–1556CrossRefGoogle Scholar
  4. Chen XW, Liu YX, Liu HM, Wang H, Yang DL, Huangfu CH (2015) Impacts of four invasive Asteraceae on soil physico-chemical properties and AM Fungi community. AJPS 6:2734–2743CrossRefGoogle Scholar
  5. Chen XW, Wei ZS, Liu HM, Yang DL, Wang H, Huangfu CH (2016) Comparison of photosynthetic characteristics between invasive and co-occurring native Asteraceae plants in Yunnan Province, China. Res Environ Sci 29:538–546Google Scholar
  6. Connelly P (2009) Horrible weed or miracle herb? A review of Bidens pilosa. J Aust Tradit-Med So 15:77–79Google Scholar
  7. Cortois R, Schroder-Georgi T, Weigelt A, van der Putten WH, De Deyn GB (2016) Plant-soil feedbacks: role of plant functional group and plant traits. J Ecol 104:1608–1617CrossRefGoogle Scholar
  8. Daniels BA, Skipper HA (1982) Methods for the recovery and quantitative estimation of propagules from soil. In: Schenck NC (ed) Methods and principles of mycorrhizal research. American Phytopathological Society, St. Paul, pp 29–35Google Scholar
  9. Day NJ, Antunes PM, Dunfield KE (2015) Changes in arbuscular mycorrhizal fungal communities during invasion by an exotic invasive plant. Acta Oecol 67:66–74CrossRefGoogle Scholar
  10. De Muth, James E (2006) Basic statistics and pharmaceutical statistical applications (2nd ed.). Boca Raton: Chapman and Hall/CRC. pp. 229–259. ISBN 0-8493-3799-2 Google Scholar
  11. Fischer NH, Quijano L (1985) Allelopathic agents from common weeds Amaranthus palmeri, Ambrosia artemisiifolia, and related weeds. In: The chemistry of allelopathy biochemical interactions among plant ACS symposium series, vol 268. pp 133–147Google Scholar
  12. Fischer NH, Williamson GB, Weidenhamer JD, Richardson DR (1994) In search of allelopathy in the Florida scrub: the role of terpenoids. J Chem Ecol 20:1355–1380CrossRefGoogle Scholar
  13. Fumanal B, Plenchette C, Chauvel B, Bretagnolle F (2006) Which role can arbuscular mycorrhizal fungi play in the facilitation of Ambrosia artemisiifolia L. invasion in France? Mycorrhiza 17:25–35CrossRefGoogle Scholar
  14. Fumanal B, Girod C, Fried G, Bretagnolle F, Chauvel B (2008) Can the large ecological amplitude of Ambrosia artemisiifolia explain its invasive success in France? Weed Res 48:349–359CrossRefGoogle Scholar
  15. Gallagher RV, Randall RP, Leishman MR (2014) Trait differences between naturalized and invasive plant species independent of residence time and phylogeny. Conserv Biol 29:360–369CrossRefGoogle Scholar
  16. Ghiani A, Aina R, Asero R, Bellotto E, Citterio S (2012) Ragweed pollen collected along high-traffic roads shows a higher allergenicity than pollen sampled in vegetated areas. Allergy 67:887–894CrossRefGoogle Scholar
  17. Grilli G, Urcelay C, Longo MS, Galetto L (2014) Mycorrhizal fungi affect plant growth: experimental evidence comparing native and invasive hosts in the context of forest fragmentation. Plant Ecol 215:1513–1525CrossRefGoogle Scholar
  18. Güsewell S, Koerselman W, Verhoeven JTA (2003) Biomass N:P ratios as indicators of nutrient limitation for plant populations in wetlands. Ecol Appl 13:372–384CrossRefGoogle Scholar
  19. Hawkes CV, Belnap J, D’Antonio C, Firestone MK (2006) Arbuscular mycorrhizal assemblages in native plant roots change in the presence of invasive exotic grasses. Plant Soil 281:369–380CrossRefGoogle Scholar
  20. He B, Li RY, Luo MY, Wei HM, Zhang H, Ma DW (2013) Effects of Bidens pilosa of invasive plant on soil ecological system at different developmental stages. Southwest China J Agric Sci 26:1953–1956Google Scholar
  21. Hidaka A, Kitayama K (2009) Divergent patterns of photosynthetic phosphorus-use efficiency versus nitrogen-use efficiency of tree leaves along nutrient-availability gradients. J Ecol 97:984–991CrossRefGoogle Scholar
  22. Hiiesalu I, Pärtel M, Davison J, Gerhold P, Metsis M, Moora M, Wilson SD (2014) Species richness of arbuscular mycorrhizal fungi: associations with grassland plant richness and biomass. New Phytol 203:233–244CrossRefGoogle Scholar
  23. Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soil. Calif Agric Exp Stn Circ 347:357–359Google Scholar
  24. Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407CrossRefGoogle Scholar
  25. Huber P (1981) Robust statistics. Wiley, New YorkCrossRefGoogle Scholar
  26. Isaac RA, Johnson WC (1983) High speed analysis of agricultural samples using inductively coupled plasma-atomic emission spectroscopy. Spectrochim Acta B 38:277–282CrossRefGoogle Scholar
  27. Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882CrossRefGoogle Scholar
  28. Klironomos JN (2002) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301CrossRefGoogle Scholar
  29. Lankau RA, Nodurft RN (2013) An exotic invader drives the evolution of plant traits that determine mycorrhizal fungal diversity in a native competitor. Mol Ecol 22:5472–5485CrossRefGoogle Scholar
  30. Leigh J, Hodge A, Fitter AH (2009) Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol 181:199–207CrossRefGoogle Scholar
  31. Lekberg Y, Koide RT (2005) Is plant performance limited by abundance of arbuscular mycorrhizal fungi? A meta-analysis of studies published between 1988 and 2003. New Phytol 168(1):89–204CrossRefGoogle Scholar
  32. Lekberg Y, Gibbons SM, Rosendahl S, Ramsey PW (2013) Severe plant invasions can increase mycorrhizal fungal abundance and diversity. ISME J 7:1424–1433CrossRefGoogle Scholar
  33. Li ZY, Xie Y (2002) Invasive alien species in China. China Forestry Publishing House, Beijing, p 162Google Scholar
  34. Liang C, Huina L, Minhe Y, Fanghao W (2011) The influence of invasion of Mikania micrantha and Bidens pilosa to the bacterial community in the root soils. Chin Agric Bull 27:63–68Google Scholar
  35. Liu RJ, Chen YL (2007) Mycorrhizology (1st ed.). Science Press, BeijingGoogle Scholar
  36. Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228CrossRefGoogle Scholar
  37. Lu GY, Wang JP, Sang WG (2012) Effects of nitrogen deposition on invasive and competitive abilities of an alien plant Ambrosia artemisiifolia. J Northeast Fore Univ 40:60–66Google Scholar
  38. Marler MJ, Zabinski CA, Callaway RM (1999) Mycorrhizae indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology 80:1180–1186.  https://doi.org/10.2307/177065 CrossRefGoogle Scholar
  39. Meisner A, Hol WHG, de Boer W, Krumins JA, Wardle DA, van der Putten W (2014) Plant soil feedbacks of exotic plant species across life forms: a metaanalysis. Biol Invasions 16:2551–2561CrossRefGoogle Scholar
  40. Menzel A, Hempel S, Klot S, Moora M, Pyšek P, Rillig M, Zobel M, Kühn I (2017) Mycorrhizal status helps explain invasion success of alien plant species. Ecology 98:92–102CrossRefGoogle Scholar
  41. Moeller HV, Dickie IA, Peltzer DA, Fukami T (2015) Mycorrhizal co-invasion and novel interactions depend on neighborhood context. Ecology 96:2336–2347CrossRefGoogle Scholar
  42. Mummey DL, Rillig MC (2006) The invasive plant species Centaurea maculosa alters arbuscular mycorrhizal fungal communities in the field. Plant Soil 288:81–90CrossRefGoogle Scholar
  43. Murrell C, Gerber E, Krebs C, Parepa M, Schaffner U, Bossdorf O (2011) Invasive knotweed affects native plants through allelopathy. Am J Bot 98:38–43CrossRefGoogle Scholar
  44. Nelson DW, Sommers LE (1973) Determination of total nitrogen in plant material. Agron J 65:109–112CrossRefGoogle Scholar
  45. Oksanen L, Sammul M, Mägi M (2006) On the indices of plant–plant competition and their pitfalls. Oikos 112:149–155CrossRefGoogle Scholar
  46. Ozaslan C, Onen H, Farooq S, Gunal H, Akyol N (2016) Common ragweed: an emerging threat for sunflower production and human health in Turkey. Weed Biol Manag 16:42–55.  https://doi.org/10.1111/wbm.12093 CrossRefGoogle Scholar
  47. Richardson DM, Allsopp N, D'Antonio CM, Milton SJ, Rejmánek M (2000) Plant invasions-the role of mutualisms. Biol Rev 75:65–93CrossRefGoogle Scholar
  48. Rúa MA, Antoninka A, Antunes PM, Chaudhary VB, Gehring C, Lamit L, Lajeunesse MJ (2016) Home-field advantage? Evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis. BMC Evol Biol 16:122CrossRefGoogle Scholar
  49. Schwarzott D, Schüßler AA (2001) Simple and reliable method for SSU rRNA gene DNA extraction, amplification, and cloning from single AM fungal spores. Mycorrhiza 10:203–207CrossRefGoogle Scholar
  50. Shah MA, Reshi ZA, Khasa DP (2009) Arbuscular mycorrhizas: drivers or passengers of alien plant invasion. Bot Rev 75:397–417CrossRefGoogle Scholar
  51. Simon L, Lalonde M, Bruns TD (1992) Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Appl Environ Microb 58:291–295Google Scholar
  52. Smith SE, Read DJ (2008) Mycorrhizal symbiosis. 3rd ed. 3rd ed. London: AcademicCrossRefGoogle Scholar
  53. Smith FA, Jakobsen I, Smith SE (2000) Spatial differences in acquisition of soil phosphate between two arbuscular mycorrhizal fungi in symbiosis with Medicago truncatula. New Phytol 147:357–366CrossRefGoogle Scholar
  54. Spence LA, Dickie IA, Coomes DA (2011) Arbuscular mycorrhizal inoculum potential: a mechanism promoting positive diversity–invasibility relationships in mountain beech forests in New Zealand? Mycorrhiza 21:309–314CrossRefGoogle Scholar
  55. Stinson KA, Campbell SA, Powell JR, Wolfe BE, Callaway RM, Thelen GC, Klironomos JN (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4:e140CrossRefGoogle Scholar
  56. Sun ZK, He WM (2010) Evidence for enhanced mutualism hypothesis: Solidago canadensis plants from regular soils perform better. PLoS One 5:e15418CrossRefGoogle Scholar
  57. Sun X, Gao C, Guo LD (2013) Changes in arbuscular mycorrhizal fungus community along an exotic plant Eupatorium adenophorum invasion in a Chinese secondary forest. J Microbiol 51:295–300CrossRefGoogle Scholar
  58. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729.  https://doi.org/10.1093/molbev/mst197 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Torrez V, Ceulemans T, Mergeay J, Meester L, Honnay O (2016) Effects of adding an arbuscular mycorrhizal fungi inoculum and of distance to donor sites on plant species recolonization following topsoil removal. Appl Veg Sci 19:7–19CrossRefGoogle Scholar
  60. Van Aarle IM, Rouhier H, Saito M (2002) Phosphatase activities of arbuscular mycorrhizal intraradical and extraradical mycelium, and their relation to phosphorus availability. Mycol Res 106:1224–1229CrossRefGoogle Scholar
  61. Van Der Heijden MG, Wiemken A, Sanders IR (2003) Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occurring plants. New Phytol 157:569–578CrossRefGoogle Scholar
  62. Van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245CrossRefGoogle Scholar
  63. Wagg C, Jansan J, Schmid B, Van der Heijden MGA (2011) Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecol Lett 14:1001–1009CrossRefGoogle Scholar
  64. Waller LP, Callaway RM, Klironomos JN, Ortega YK, Maron JL (2016) Reduced mycorrhizal responsiveness leads to increased competitive tolerance in an invasive exotic plant. J Ecol 104(6):1599–1607CrossRefGoogle Scholar
  65. Wan FH, Zheng XB, Guo JY (2005) Biology and management of invasive alien species in agriculture and forestry. Science Publication, Beijing, pp 774–774Google Scholar
  66. Wan FH, Guo JY, Zhang F et al (2009) Research on biological invasions in China. China Science Press, BeijingGoogle Scholar
  67. Wan FH, Jiang MX, Zhan AB et al (2017) Biological invasions and its management in China. Invading Nature - Springer Series in Invasion Ecology, vol 11.  https://doi.org/10.1007/978-94-024-0948-2 Google Scholar
  68. Willis A, Rodrigues BF, Harris PC (2013) The ecology of arbuscular mycorrhizal fungi. Crit Rev Plant Sci 32:1–20CrossRefGoogle Scholar
  69. Xu HG, Qiang S (2004) Catalog of invasive species in China. China environmental science press, BeijingGoogle Scholar
  70. Yan J, Zhang XY, Chen X, Wang Y, Zhang FJ, Wan FH (2016) Effects of rhizosphere soil microorganisms and soil nutrients on competitiveness of Bidens pilosa with different native plants. Biodivers Sci 24:1381–1389CrossRefGoogle Scholar
  71. Yang FJ, Wang JK, Zhang Y, Zhang ZH, Chen HF (2004) Analysis of the component forestry harmful plant of Ambrosia artemisiifolia essential oil by gas chromatography mass spectrometry. Bull Bot Res 25:457–459Google Scholar
  72. Yin JL, Zhang XY, Yan J, Li Q, Jia YY, Zhang FJ, Wan FH (2015) The feedback of arbuscular mycorrhizal fungi on the competition between Flaveria bidentis and cotton. Ecol Environ 24:1132–1136Google Scholar
  73. Yu WQ, Zhang LL, Liu WX, Wan FH (2010) Soil fungi differentially affect the growth of and interaction between invasive weed Ambrosia artemisiifolia and native plants. Chin J Ecol 29:523–528Google Scholar
  74. Zabinski CA, Quinn L, Callaway RM (2002) Phosphorus uptake, not carbon transfer, explains arbuscular mycorrhizal enhancement of Centaurea maculosa in the presence of native grassland species. Funct Ecol 16:758–765CrossRefGoogle Scholar
  75. Zeng RS, Luo SM (1996) The allelopathic effects of root exudates of Cymbopogon citratus, Ageratum conyzoides and Bidens pilosa. J South Chin Agric Univ 17:119–120Google Scholar
  76. Zhang Q, Yao LJ, Yang RY, Tang JJ, Chen X (2007) Potential allelopathic effects of an invasive species Solidago canadensis in the mycorrhizae of native plant species. Allelopathy J 20:71–77Google Scholar
  77. Zhang FJ, Guo JY, Long R, Wan FH (2010) Allelopathy of different treated residues of Ambrosiaa rtemisiifolia L. on wheat growth. Chin J Ecol 29:669–673Google Scholar
  78. Zhang FJ, Chen FX, Li Q, Xu HY, Jia YY (2015a) Effects of nitrogen addition on the competition between the invasive species Flaveria bidentis and two native species. Russ J Ecol 46:325–331CrossRefGoogle Scholar
  79. Zhang YM, Wang Y, Li Q, Zhang FJ, Wan FH (2015b) Mechanism of AM fungi on competitive growth between invasive plant Flaveria bidentis and native plant Setaria viridis. Acta Bot Bore ali-Occident Sin 35:1215–1221Google Scholar
  80. Zhang FJ, Li Q, Chen FX, Xu HY, Inderjit, Wan FH (2017) Arbuscular mycorrhizal fungi facilitate growth and competitive ability of an exotic species Flaveria bidentis. Soil Biol Biochem 115:275–284CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.College of Life ScienceHebei UniversityBaodingChina
  2. 2.College of Plant ProtectionHunan Agricultural UniversityChangshaChina
  3. 3.State Key Laboratory for Biology of Plant Diseases and Insect PestsInstitute of Plant Protection Chinese Academy of Agricultural SciencesBeijingChina
  4. 4.Department of BiologyIndiana University of PennsylvaniaIndianaUSA
  5. 5.Department of BiologyHuihua College of Hebei Normal UniversityShijiazhuangChina

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