Skip to main content
SpringerLink
Log in

Arbuscular mycorrhizal fungi protect native woody species from novel weapons

Plant and Soil volume 440, pages 39–52 (2019)Cite this article

Abstract

Background and aims

Arbuscular mycorrhizal fungi (AMF) play important roles in plant community structure and ecosystem functioning. The allelopathic disruption of arbuscular mycorrhizal mutualism is a potentially powerful mechanism by which non-native species can negatively impact native plant diversity. However, there is limited understanding of this mechanism on woody species in forest ecosystems. In this study, we carried out a set of experiments to explore the allelopathy of Eucalyptus urophylla on mycorrhizal mutualists.

Methods

First, we examined allelopathic effects on the mycorrhizal growth responses of woody species by collecting leachates from the understory of an E. urophylla plantation. Second, we examined if AMF could counteract the allelopathy of E. urophylla by treating the target species with and without aqueous extract of E. urophylla and AMF inoculum. We conducted a third in vitro experiment to characterize the effects of identified putative allelochemicals (IPAs) of E. urophylla on AMF spore germination, namely Glomus mosseae, Claroideoglomus etunicatum and mixed spores extracted from field soil.

Results

There was a positive correlation between the stimulatory effects of natural leachates of E. urophylla and the mycorrhizal growth responses of target woody species. AMF could counteract the negative impact of E. urophylla allelopathy at a relatively low concentration. The IPAs of E. urophylla had variable effects on germination of AMF spores, from stimulatory to inhibitory, depending on chemical types and AMF species. Moreover, the AMF G. mosseae was the least sensitive to allelopathic inhibition of E. urophylla IPAs.

Conclusions

This study does not support the hypothesis that allelopathy degrades mycorrhizal symbioses. Our study first provides preliminary evidence for a positive correlation between allelopathy and mycorrhizal growth responses and suggests that higher mycorrhizal growth responses could better protect woody species from allelopathic inhibition in E. urophylla plantations.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Aschehoug ET, Callaway RM, Newcombe G, Tharayil N, Chen S (2014) Fungal endophyte increases the allelopathic effects of an invasive forb. Oecologia 175:285–291

    Article  PubMed  Google Scholar 

  • Bajwa R, Naz I (2005) Allelopathic effects of Eucalyptus citriodora on growth, nodulation and AM colonization of Vigna radiata (L) Wilczek. Allelopath J 15:237–246

    Google Scholar 

  • Barto K, Friese C, Cipollini D (2010) Arbuscular mycorrhizal fungi protect a native plant from allelopathic effects of an invader. J Chem Ecol 36:351–360

    Article  CAS  PubMed  Google Scholar 

  • Beauchamp VB, Stromberg JC, Stutz JC (2005) Interactions between Tamarix ramosissima (saltcedar), Populus fremontii (cottonwood), and mycorrhizal fungi: effects on seedling growth and plant species coexistence. Plant Soil 275:221–231

    Article  CAS  Google Scholar 

  • Bever JD, Richardson SC, Lawrence BM, Holmes J, Watson M (2009) Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism. Ecol Lett 12:13–21

    Article  PubMed  Google Scholar 

  • Bidartondo MI, Redecker D, Hijri I, Wiemken A, Bruns TD (2002) Epiparasitic plants specialized on arbuscular mycorrhizal fungi. Nature 419:387–392

    Article  CAS  Google Scholar 

  • Biermann B, Linderman RG (2006) Quatifying vesicular-arbuscular mycorrhizae: a proposed method towads standardization. New Phytol 87:63–67

    Article  Google Scholar 

  • Blum U (2011) Plant-plant allelopathic interactions: phenolic acids, cover crops and weed emergence. Springer Dordrecht, Heidelberg, London, New York, pp 1–200

    Book  Google Scholar 

  • Blum U, Staman KL, Flint LJ, Shafer SR (2000) Induction and/or selection of phenolic acid-utilizing bulk-soil andrhizosphere bacteria and their influence on phenolic acid phytotoxicity. J Chem Ecol 26:2059–2078

    Article  CAS  Google Scholar 

  • Bronstein JL (1994) Conditional outcomes in mutualistic interactions. Trends Ecol Evol 9:214–217

    Article  CAS  PubMed  Google Scholar 

  • Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–463

    Article  Google Scholar 

  • Callaway RM, Cipollini D, Barto K, Thelen GC, Hallett SG, Prati D, Stinson K, Klironomos J (2008) Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native europe. Ecology 89:1043–1055

    Article  PubMed  Google Scholar 

  • Cameron DD, Neal AL, van Wees SCM, Ton J (2013) Mycorrhiza-induced resistance: more than the sum of its parts? Trends Plant Sci 18:539–545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cantor A, Hale A, Aaron J, Traw MB, Kalisz S (2011) Low allelochemical concentrations detected in garlic mustard-invaded forest soils inhibit fungal growth and AMF spore germination. Biol Invasions 13:3015–3025

    Article  Google Scholar 

  • Carvalho FP, Melo CAD, Machado MS, Dias DCFS, Alvarenga EM (2015) The allelopathic effect of Eucalyptus leaf extract on grass forage seed. Planta Daninha 33:193–201

    Article  Google Scholar 

  • Chen YL, Brundrett MC, Dell B (2000) Effects of ectomycorrhizas and vesicular-arbuscular mycorrhizas, alone or in competition, on root colonization and growth of Eucalyptus globulus and E. urophylla. New Phytol 146:545–556

    Article  Google Scholar 

  • Cipollini D, Rigsby CM, Barto EK (2012) Microbes as targets and mediators of allelopathy in plants. J Chem Ecol 38:714–727

    Article  CAS  PubMed  Google Scholar 

  • Cossalter C, Pye-Smith C (2003) Fast-wood forestry: myths and realities. Center for International Forestry Research, Bogor

    Google Scholar 

  • de Mendonça Bellei M, Garbaye J, Gil M (1992) Mycorrhizal succession in young Eucalyptus viminalis plantations in Santa Catarina (southern Brazil). For Ecol Manag 54:205–213

    Article  Google Scholar 

  • Duke SO, Dayan FE (2006) Modes of action of phytotoxins from plants. In: Reigosa MJ, Pedrol N, González L (eds) Allelopathy: a physiological process with ecological implications. Springer, Netherlands, pp 511–536

    Google Scholar 

  • Džafić E, Pongrac P, Likar M, Regvar M, Vogel-Mikuš K (2013) The arbuscular mycorrhizal fungus Glomus mosseae alleviates autotoxic effects in maize (Zea mays L.). Eur J Soil Biol 58:59–65

    Article  CAS  Google Scholar 

  • El-Khawas SA, Shehata MM (2005) The allelopathic potentialities of Acacia nilotica and Eucalyptus rostrata on monocot (Zea mays L.) and dicot (Phaseolus vulgaris L.) plants. Biotechnology 4:23–34

    Article  CAS  Google Scholar 

  • Ellers J, Kiers ET, Currie CR, McDonald BR, Visser B (2012) Ecological interactions drive evolutionary loss of traits. Ecol Lett 15:1071–1082

    Article  PubMed  Google Scholar 

  • Fang B, Yu S, Wang Y, Qiu X, Cai C, Liu S (2009) Allelopathic effects of Eucalyptus urophylla on ten tree species in South China. Agrofor Syst 76:401–408

    Article  Google Scholar 

  • Fernandez C, Monnier Y, Santonja M, Gallet C, Weston LA, Prévosto B, Saunier A, Baldy V, Bousquet-Mélou A (2016) The impact of competition and allelopathy on the trade-off between plant defense and growth in two contrasting tree species. Front Plant Sci 7:594

    PubMed  PubMed Central  Google Scholar 

  • Ferreira MC, Souza JRP, Faria TJ (2007) Potenciação alelopática de extratos vegetais na germinação e no crescimento inicial de picão-preto e alface. Ciência e Agrotecnologia 31:1054–1060

    Article  Google Scholar 

  • Feyera S, Beck E, Lüttge U (2002) Exotic trees as nurse-trees for the regeneration of natural tropical forests. Trees 16:245–249

    Article  Google Scholar 

  • Florentine SK, Fox JED (2003) Allelopathic effects of Eucalyptus victrix L. on Eucalyptus species and grasses. Allelopath J 11:77–83

    Google Scholar 

  • Forrester DI, Bauhus J, Cowie AL, Vanclay JK (2006) Mixed-species plantations of Eucalyptus with nitrogen-fixing trees: a review. For Ecol Manag 233:211–230

    Article  Google Scholar 

  • Forsyth GG, Richardson DM, Brown PJ, Van Wilgen BW (2004) A rapid assessment of the invasive status of Eucalyptus species in two South African provinces. S Afr J Sci 100:75–77

    Google Scholar 

  • Fox J, Weisberg S (2011) An R companion to applied regression. SAGE, Thousand Oaks

    Google Scholar 

  • Gaertner M, Richardson DM, Privett SDJ (2011) Effects of alien plants on ecosystem structure and functioning and implications for restoration: insights from three degraded sites in south African fynbos. Environ Manag 48:57–69

    Article  Google Scholar 

  • Gardner RAW (2007) Investigating the environmental adaptability of promising subtropical and cold-tolerant eucalypt species in the warm temperate climate zone of KwaZulu-Natal, South Africa. South Africa South Hemisp For J 69:27–38

    Google Scholar 

  • Grbović S, Orčić D, Couladis M, Jovin E, Bugarin D, Balog K, Mimica-Dukić N (2010) Variation of essential oil composition of Eucalyptus camaldulensis (myrtaceae) from the Montengero coastline. Acta Period Technol 41:151–158

    Article  CAS  Google Scholar 

  • Greipsson S, DiTommaso A (2006) Invasive non-native plants alter the occurrence of arbuscular mycorrhizal fungi and benefit fromthis association. Ecol Restor 24:236–241

    Article  Google Scholar 

  • Grove S, Haubensak KA, Gehring C, Parker IM (2017) Mycorrhizae, invasions, and the temporal dynamics of mutualism disruption. J Ecol 105:1496–1508

    Article  Google Scholar 

  • Gruntman M, Zieger S, Tielbörger K (2016) Invasive success and the evolution of enhanced weaponry. Oikos 125:59–65

    Article  Google Scholar 

  • Gustafson DJ, Casper BB (2005) Differential host plant performance as a function of soil arbuscular mycorrhizal fungal communities: experimentally manipulating co-occurring Glomus species. Plant Ecol 183:257–263

    Article  Google Scholar 

  • Hale AN, Kalisz S (2012) Perspectives on allelopathic disruption of plant mutualisms: a framework for individual- and population-level fitness consequences. Plant Ecol 213:1991–2006

    Article  Google Scholar 

  • Hale AN, Tonsor SJ, Kalisz S (2011) Testing the mutualism disruption hypothesis: physiological mechanisms for invasion of intact perennial plant communities. Ecosphere 2:art110

    Article  Google Scholar 

  • Hartnett DC, Wilson GWT (2002) The role of mycorrhizas in plant community structure and dynamics: lessons from grasslands. Plant Soil 244:319–331

    Article  CAS  Google Scholar 

  • He H, Song Q, Wang Y, Yu S (2014) Phytotoxic effects of volatile organic compounds in soil water taken from a Eucalyptus urophylla plantation. Plant Soil 377:203–215

    Article  CAS  Google Scholar 

  • Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GW, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407

    Article  PubMed  Google Scholar 

  • Hunter I (2001) Above ground biomass and nutrient uptake of three tree species (Eucalyptus camaldulensis, Eucalyptus grandis and Dalbergia sissoo) as affected by irrigation and fertiliser, at 3 years of age, in southern India. For Ecol Manag 144:189–200

    Article  Google Scholar 

  • Ibanez SG, Medina MI, Agostini E (2011) Phenol tolerance, changes of antioxidative enzymes and cellular damage in transgenic tobacco hairy roots colonized by arbuscular mycorrhizal fungi. Chemosphere 83:700–705

    Article  CAS  PubMed  Google Scholar 

  • Inderjit (2005) Soil microorganisms: an important determinant of allelopathic activity. Plant Soil 274:227–236

    Article  CAS  Google Scholar 

  • Inderjit, Duke SO (2003) Ecophysiological aspects of allelopathy. Planta 217:529–539

    Article  CAS  PubMed  Google Scholar 

  • Inderjit, Streibig JC, Olofsdotter M (2002) Joint action of phenolic acid mixtures and its significance in allelopathy research. Physiol Plant 114:422–428

    Article  CAS  Google Scholar 

  • Inderjit, Wardle DA, Karban R, Callaway RM (2011) The ecosystem and evolutionary contexts of allelopathy. Trends Ecol Evol 26:655–662

    Article  CAS  PubMed  Google Scholar 

  • Jansa J, Smith FA, Smith Sally E (2007) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol 177:779–789

    Article  CAS  PubMed  Google Scholar 

  • Javaid A (2007) Allelopathic interactions in mycorrhizal associations. Allelopath J 20:29–42

    Google Scholar 

  • Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–586

    Article  Google Scholar 

  • Jones MD, Smith SE (2004) Exploring functional definitions of mycorrhizas: are mycorrhizas always mutualisms? Can J Bot 82:1089–1109

    Article  Google Scholar 

  • Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–664

    Article  CAS  PubMed  Google Scholar 

  • Kaur H, Kaur R, Kaur S, Baldwin IT, Inderjit (2009) Taking ecological function seriously: soil microbial communities can obviate allelopathic effects of released metabolites. PLoS One 4:e4700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan MA, Hussain I, Khan EA (2008) Allelopathic effects of eucalyptus (Eucalyptus camaldulensis L.) on germination and seedling growth of wheat (Triticum aestivum L.). Pakistan J Weed Sci Res 14:9–18

    Google Scholar 

  • 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 333:880–882

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Koch AM, Antunes PM, Barto KE, Cipollini D, Mummey DL, Klironomos JN (2010) The effects of arbuscular mycorrhizal (AM) fungal and garlic mustard introductions on native AM fungal diversity. Biol Invasions 13:1627–1639

    Article  Google Scholar 

  • Koide RT (2000) Functional complementarity in the arbuscular mycorrhizal symbiosis. New Phytol 147:233–235

    Article  Google Scholar 

  • Kulmatiski A, Beard KH, Stevens JR, Cobbold SM (2008) Plant-soil feedbacks: a meta-analytical review. Ecol Lett 11:980–992

    Article  PubMed  Google Scholar 

  • Lankau RA (2011) Intraspecific variation in allelochemistry determines an invasive species' impact on soil microbial communities. Oecologia 165:453–463

    Article  PubMed  Google Scholar 

  • Lankau RA (2013) Species invasion alters local adaptation to soil communities in a native plant. Ecology 94:32–40

    Article  PubMed  Google Scholar 

  • Li YP, Feng YL, Chen YJ, Tian YH (2015) Soil microbes alleviate allelopathy of invasive plants. Sci Bull 60:1083–1091

    Article  Google Scholar 

  • Liu S, Qin F, Yu S (2018) Eucalyptus urophylla root-associated fungi can counteract the negative influence of phenolic acid allelochemicals. Appl Soil Ecol 127:1–7

    Article  Google Scholar 

  • Lorenzo P, Palomera-Pérez A, Reigosa MJ, González L (2011) Allelopathic interference of invasive Acacia dealbata link on the physiological parameters of native understory species. Plant Ecol 212:403–412

    Article  Google Scholar 

  • Lorenzo P, Pereira CS, Rodríguez-Echeverría S (2013a) Differential impact on soil microbes of allelopathic compounds released by the invasive Acacia dealbata link. Soil Biol Biochem 57:156–163

    Article  CAS  Google Scholar 

  • Lorenzo P, Rodríguez-Echeverría S, Freitas H (2013b) No allelopathic effect of the invader Acacia dealbata on the potential infectivity of arbuscular mycorrhizal fungi from native soils. Eur J Soil Biol 58:42–44

    Article  Google Scholar 

  • Lüttge U, Berg A, Fetene M, Nauke P, Peter D, Beck E (2003) Comparative characterization of photosynthetic performance and water relations of native trees and exotic plantation trees in an Ethiopian forest. Trees 17:40–50

    Article  CAS  Google Scholar 

  • Martinez-Garcia LB, Pugnaire FI (2011) Arbuscular mycorrhizal fungi host preference and site effects in two plant species in a semiarid environment. Appl Soil Ecol 48:313–317

    Article  Google Scholar 

  • Meiners SJ, Phipps KK, Pendergast TH, Canam T, Carson WP (2017) Soil microbial communities alter leaf chemistry and influence allelopathic potential among coexisting plant species. Oecologia 183:1155–1165

    Article  PubMed  Google Scholar 

  • Meinhardt KA, Gehring CA (2012) Disrupting mycorrhizal mutualisms: a potential mechanism by which exotic tamarisk outcompetes native cottonwoods. Ecol Appl 22:532–549

    Article  PubMed  Google Scholar 

  • Mummey DL, Rillig MC (2006) The invasive plant species Centaurea maculosa alters arbuscular mycorrhizal fungal communities in the field. Plant Soil 288:81–90

    Article  CAS  Google Scholar 

  • Natel P, Neumann P (1992) Ecology of ectomycorrhizal-basidiomycete communities on a local vegetation gradient. Ecology 73:99–117

    Article  Google Scholar 

  • Ou YD, Wang CB (2015) Comparative analysis of the diversity of undergrowth plants in secondary forest and Eucalyptus plantations. Eucalypt Sci Technol 32:21–25

    Google Scholar 

  • Pellissier F (1993) Allelopathic effect of phenolic acids from humic solutions on two spruce mycorrhizal fungi: Cenococcum graniforme and Laccaria laccata. J Chem Ecol 19:2105–2114

    Article  CAS  PubMed  Google Scholar 

  • Pellissier F, Souto XC (1999) Allelopathy in northern temperate and boreal semi-natural woodland. Crit Rev Plant Sci 18:637–652

    Article  Google Scholar 

  • Pinzone P, Potts D, Pettibone G, Warren R (2018) Do novel weapons that degrade mycorrhizal mutualisms promote species invasion? Plant Ecol 219:539–548

    Article  Google Scholar 

  • Pringle A, Bever JD (2008) Analogous effects of arbuscular mycorrhizal fungi in the laboratory and a North Carolina field. New Phytol 180:162–175

    Article  PubMed  Google Scholar 

  • Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN (2009) Mycorrhizal symbioses and plant invasions. Annu Rev Ecol Evol Syst 40:699–715

    Article  Google Scholar 

  • Qin FC, Liu S, Yu SX (2018) Effects of allelopathy and competition for water and nutrients on survival and growth of tree species in Eucalyptus urophylla plantations. For Ecol Manag 424:387–395

    Article  Google Scholar 

  • R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Reigosa MJ, Souto XC, Gonz’lez L (1999) Effect of phenolic compounds on the germination of six weeds species. Plant Growth Regul 28:83–88

    Article  CAS  Google Scholar 

  • Renne IJ, Rios BG, Fehmi JS, Tracy BF (2004) Low allelopathic potential of an invasive forage grass on native grassland plants: a cause for encouragement? Basic Appl Ecol 5:261–269

    Article  Google Scholar 

  • Rice EL (1984) Allelopathy, 2nd edn. Academic Press, Inc, Orlando

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ridenour WM, Callaway RM (2001) The relative importance of allelopathy in interference: the effects of an invasive weed on a native bunchgrass. Oecologia 126:444–450

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Ruwanza S, Gaertner M, Esler KJ, Richardson DM (2014) Allelopathic effects of invasive Eucalyptus camaldulensis on germination and early growth of four native species in the Western Cape, South Africa. Southern Forests 77:91–105

    Article  Google Scholar 

  • Sanders IR (2003) Preference, specificity and cheating in the arbuscular mycorrhizal symbiosis. Trends Plant Sci 8:143–145

    Article  CAS  PubMed  Google Scholar 

  • Santos SAO, Villaverde JJ, Freire CSR, Domingues MRM, Neto CP, Silvestre AJD (2012) Phenolic composition and antioxidant activity of Eucalyptus grandis, E. urograndis (E. grandis×E. urophylla) and E. maidenii bark extracts. Ind Crop Prod 39:120–127

    Article  CAS  Google Scholar 

  • Sasikumar K, Vijayalakshmi C, Parthiban KT (2001) Allelopathic effects of four Eucalyptus species on redgram (Cajanus cajan L.). J Trop Agric 39:134–138

    Google Scholar 

  • Sides CB, Enquist BJ, Ebersole JJ, Smith MN, Henderson AN, Sloat LL (2014) Revisiting Darwin’s hypothesis: does greater intraspecific variability increase species’ ecological breadth? Am J Bot 101:56–62

    Article  PubMed  Google Scholar 

  • Sikes BA, Cottenie K, Klironomos JN (2009) Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas. J Ecol 97:1274–1280

    Article  Google Scholar 

  • Sikes BA, Maherali H, Klironomos JN (2014) Mycorrhizal fungal growth responds to soil characteristics, but not host plant identity, during a primary lacustrine dune succession. Mycorrhiza 24:219–226

    Article  PubMed  Google Scholar 

  • Sinkkonen A (2006) Ecological relationships and allelopathy. In: Reigosa MJ, Pedrol N, González L (eds) Allelopathy: a physiological process with ecological implications. Springer, Netherlands, pp 373–393

    Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, Inc, San Diego

    Google Scholar 

  • Smith FA, Smith SE (2013) How useful is the mutualism-parasitism continuum of arbuscular mycorrhizal functioning? Plant Soil 363:7–18

    Article  CAS  Google Scholar 

  • Sodaeizadeh H, Rafieiolhossaini M, Havlík J, Van Damme P (2009) Allelopathic activity of different plant parts of Peganum harmala L. and identification of their growth inhibitors substances. Plant Growth Regul 59:227–236

    Article  CAS  Google Scholar 

  • Souto C, Pellissier F, Chiapusio G (2000) Allelopathic effects of humus phenolics on growth and respiration of mycorrhizal fungi. J Chem Ecol 26:2015–2023

    Article  CAS  Google Scholar 

  • Stampe ED, Daehler CC (2003) Mycorrhizal species identity affects plant community structure and invasion: a microcosm study. Oikos 100:362–372

    Article  Google Scholar 

  • Stone R (2009) Nursing China's ailing forests back to health. Science 325:556–558

    Article  PubMed  Google Scholar 

  • Tererai F, Gaertner M, Jacobs SM, Richardson DM (2013) Eucalyptus invasions in riparian forests: effects on native vegetation community diversity, stand structure and composition. For Ecol Manag 297:84–93

    Article  Google Scholar 

  • van der Heijden MGA (2002) Arbuscular mycorrhizal fungi as a determinant of plant diversity: in search of underlying mechanisms and general principles. In: Ecology M (ed) M G A van der Heijden and I R Sanders. Springer, Berlin, Heidelberg, pp 243–265

    Google Scholar 

  • van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72

    Article  CAS  Google Scholar 

  • van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, Van de Voorde TFJ, Wardle DA, Hutchings M (2013) Plant-soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276

    Article  Google Scholar 

  • Veiga RSL, Howard K, van der Heijden MGA (2012) No evidence for allelopathic effects of arbuscular mycorrhizal fungi on the non-host plant Stellaria media. Plant Soil 360:319–331

    Article  CAS  Google Scholar 

  • Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vogelsang KM, Bever JD (2009) Mycorrhizal densities decline in association with normative plants and contribute to plant invasion. Ecology 90:399–407

    Article  PubMed  Google Scholar 

  • Waller LP, Callaway RM, Klironomos JN, Ortega YK, Maron JL, Shefferson R (2016) Reduced mycorrhizal responsiveness leads to increased competitive tolerance in an invasive exotic plant. J Ecol 104:1599–1607

    Article  Google Scholar 

  • Wardle DA, Zackrisson O (2005) Effects of species and functional group loss on island ecosystem properties. Nature 435:806–810

    Article  CAS  PubMed  Google Scholar 

  • Weidenhamer JD, Romeo JT (2005) Allelopathy as a mechanism for resisting invasion: the case of Polygonella myriophylla. In: Inderjit S (ed) Invasive plants: ecological and agricultural aspects. Birkhäuser, Basel, pp 167–177

    Chapter  Google Scholar 

  • Williams RA (2015) Mitigating biodiversity concerns in Eucalyptus plantations located in South China. J Biosci Med 3:1–8

    Google Scholar 

  • Williamson GB, Richardson D (1988) Bioassays for allelopathy: measuring treatment responses with independent controls. J Chem Ecol 14:181–187

    Article  Google Scholar 

  • Willis RJ (2007) The history of allelopathy. Springer Science & Business Media, Dordrecht

    Google Scholar 

  • Yamagushi MQ, Gusman GS, Vestena S (2011) Allelopathic effect of aqueous extracts of Eucalyptus globulus Labill. and of Casearia sylvestris Sw. on crops. Semin-Cieng Agrar 32:1361–1374

    Article  Google Scholar 

  • Yang H, Jiang L, Li L, Li A, Wu M, Wan S (2012) Diversity-dependent stability under mowing and nutrient addition: evidence from a 7-year grassland experiment. Ecol Lett 15:619–626

    Article  PubMed  Google Scholar 

  • Yuan Y, Tang J, Leng D, Hu S, Yong JW, Chen X (2014) An invasive plant promotes its arbuscular mycorrhizal symbioses and competitiveness through its secondary metabolites: indirect evidence from activated carbon. PLoS One 9:e97163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zahed N, Hosni K, Ben Brahim N, Kallel M, Sebei H (2010) Allelopathic effect of Schinus molle essential oils on wheat germination. Acta Physiol Plant 32:1221–1227

    Article  CAS  Google Scholar 

  • Zhang Q, Yao LJ, Yang RY, Yang XY, Tang JJ, Chen X (2007) Potential allelopathic effects of an invasive species Solidago canadensis on the mycorrhizae of native plant species. Allelopath J 20:71–78

    CAS  Google Scholar 

  • Zhang S, Zhu W, Wang B, Tang J, Chen X (2011) Secondary metabolites from the invasive Solidago canadensis L. accumulation in soil and contribution to inhibition of soil pathogen Pythium ultimum. Appl Soil Ecol 48:280–286

    Article  Google Scholar 

  • Zhang J, An M, Wu H, Liu d L, Stanton R (2014) Phytotoxic activity and chemical composition of aqueous volatile fractions from Eucalyptus species. PLoS One 9:e93189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao YH, Yang YM, Yang SY, Wang J (2007) A review of the biodiversity in Eucalyptus plantation. J Yunnan Agricu Univ 22:741–746

    Google Scholar 

  • Zhao LM, Diao YN, Jin HR (2013) The optimum disinfection method and the optimal culture medium for AMF spores. Hunan Agricu Sci 19:24–27

    Google Scholar 

Download references

Acknowledgments

We are grateful to Yan Xie and Lufeng Zhao for their assistance in the experiments. We also thank Shan Luo for valuable suggestions that improved the manuscript. This research was funded by the National Nature Science Foundation of China (key project 31361140363) and the Zhang-Hongda Science Foundation in Sun Yat-sen University.

Author information

Authors and Affiliations

  1. Department of Ecology, School of Life Sciences /State Key Laboratory of Biocontrol, Sun Yat-sen University, Guangzhou, 510275, China

    Fangcuo Qin & Shixiao Yu

  2. Department of Ecology, School of Life Sciences, Sun Yat-sen University, Guangzhou, 510275, People’s Republic of China

    Shixiao Yu

Authors
  1. Fangcuo Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shixiao Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shixiao Yu.

Additional information

Responsible Editor: François Teste.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 782 kb)

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Qin, F., Yu, S. Arbuscular mycorrhizal fungi protect native woody species from novel weapons. Plant Soil 440, 39–52 (2019). https://doi.org/10.1007/s11104-019-04063-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-019-04063-4

Keywords

search

Navigation