Abstract
Recent research indicates that the soil microbial community, particularly arbuscular mycorrhizal fungi (AMF), can influence plant invasion in several ways. We tested if 1) invasive species are colonised by AMF to a lower degree than resident native species, and 2) AMF colonisation of native plants is lower in a community inhabited by an invasive species than in an uninvaded resident community. The two tests were run in semiarid temperate grasslands on grass (Poaceae) species, and the frequency and intensity of mycorrhizal colonisation, and the proportion of arbuscules and vesicles in plant roots have been measured. In the first test, grasses representing three classes of invasiveness were included: invasive species, resident species becoming abundant upon disturbance, and non-invasive native species. Each class contained one C3 and one C4 species. The AMF colonisation of the invasive Calamagrostis epigejos and Cynodon dactylon was consistently lower than that of the non-invasive native Chrysopogon gryllus and Bromus inermis, and contained fewer arbuscules than the post-disturbance dominant resident grasses Bothriochloa ischaemum andBrachypodiumpinnatum. The C3 and C4 grasses behaved alike despite their displaced phenologies in these habitats. The second test compared AMF colonisation for sand grassland dominant grasses Festuca vaginata and Stipa borysthenica in stands invaded by either C. epigejos or C. dactylon, and in the uninvaded natural community. Resident grasses showed lower degree of AMF colonisation in the invaded stand compared to the uninvaded natural community with F. vaginata responding so to both invaders, while S. borysthenica responding to C. dactylon only. These results indicate that invasive grasses supposedly less reliant on AMF symbionts have the capacity of altering the soil mycorrhizal community in such a way that resident native species can establish a considerably reduced extent of the beneficial AMF associations, hence their growth, reproduction and ultimately abundance may decline. Accumulating evidence suggests that such indirect influences of invasive alien plants on resident native species mediated by AMF or other members of the soil biota is probably more the rule than the exception.
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Abbreviations
- AMF:
-
Arbuscular Mycorrhizal Fungi
- a%:
-
percentage arbuscule occurrence of the AMF colonised root section
- A%:
-
percentage arbuscule occurrence of the whole root
- F%:
-
frequency of root segments colonised by AMF
- M%:
-
intensity of mycorrhizal colonisation
- v%:
-
percentage vesicle occurrence of the AMF colonised root section
- V%:
-
percentage vesicle occurrence of the whole root
References
Barto, K., C. Friese and D. Cipollini. 2010. Arbuscular mycorrhizal fungi protect a native plant from allelopathic effects of an invader. J. Chem. Ecol. 36: 351–360.
Batten, K.M., K.M. Scow, K.F. Davies and S.P. Harrison. 2006. Two invasive plants alter soil microbial community composition in serpentine grasslands. Biol. Invasions 8: 217–230.
Bever, J.D. 2002a. Host-specificity of AM fungal population growth rates can generate feedback on plant growth. Plant and Soil 244: 281–290.
Bever, J.D. 2002b. Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Proc. Royal Soc., Lond., Ser. B 269: 2595–2601.
Bever, J.D., I.A. Dickie, E. Facelli, J.M. Facelli, J. Klironomos, M. Moora, M.C. Rillig, W.D. Stock, M. Tibbett, and M. Zobel. 2010. Rooting theoriesof plant community ecology in microbial interactions. Trends Ecol. Evol. 25(8):468–478.
Blossey, B. and R. Nötzold. 1995. Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J. Ecol. 83: 887–889.
Bossdorf, O., H. Auge, L. Lafuma, W.E. Rogers, E. Siemann and D. Prati. 2005. Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144: 1–11.
Bray, S. and K. Kitajima. 2003. Mycorrhizae differentially alter growth, physiology, and competitive ability of an invasive shrub. Ecol. Appl. 13: 565–574.
Brundrett, M. 1991. Mycorrhizas in natural ecosystems. Adv. Ecol. Res. 21: 171–313.
Busby, R.R, M. W. Paschke, M.E. Stromberger and D. L. Gebhart. 2012. Seasonal variation in arbuscular mycorrhizal fungi root colonization of cheatgrass (Bromus tectorum), an invasive winter annual. J. Ecosyst. Ecogr. S8: 001.
Cabello, M.M. 1997. Hydrocarbon pollution: its effect on native ar-buscular mycorrhizal fungi (AMF). FEMS Microbiol. Ecol. 22: 233–236.
Callaway, R.M., D. Cippolini, K. Barto, G.C. Thelen, S.G. Hallett, D. Prati, K. Stinson and J.N. Klironomos. 2008. Novel weapons: invasive plant supresses fungal mutualists in America but not in its native Europe. Ecology 89: 1043–1055.
Callaway, R.M. and W. Ridenour. 2004. Novel weapons: invasive success and the evolution of increased competitive ability. Frontiers in Ecol. Env. 2: 436–443.
Carey, J.R., M.J. Marler and R.M. Callaway. 2004. Mycorrhizae transfer carbon from a native grass to an invasive weed: evidence from stable isotopes and physiology. Plant Ecol. 172: 133–141.
Davis, M.A., J.P. Grime and K. Thompson. 2000. Fluctuating resources in plant communities: a general theory of invasibility. J. Ecol. 88: 528–534.
Davison, J., M. Öpik, M. Zobel, M. Vasar, M. Metsis, and M. Moora. 2012. Communities of arbuscular mycorrhizal fungi detected in forest soil are spatially heterogeneous but do not vary throughout the growing season. PLoS ONE 7(8): e41938.
Douds, D.D., C.R. Johnson and K.E. Koch. 1988. Carbon cost of the fungal symbiont relative to net leaf P accumulation in a split-root VA mycorrhizal symbiosis. Plant Physiol. 86: 491–496.
Emery, S.M. and J.A. Rudgers. 2012. Impact of competition and my-corrhizal fungi on growth of Centaurea stoebe, an invasive plant of sand dunes. Amer. Midland Nat. 167: 213–222.
Endresz, G., Á. Zöld-Balogh, and T. Kalapos. 2005. Local distribution pattern of Brachypodium pinnatum (Poaceae) - Field experiments in xeric loess grassland in N. Hungary. Phyton 45(2):249–265.
Faraway, J.J. 2002. Linear Models With R. Texts in Statistical Science. Chapman & Hall/CRC, New York.
Fitter, A. 2005. Darkness visible: reflections on underground ecology. J. Ecol. 93: 231–243.
Fox, J. and S. Weisberg. 2011. An {R} Companion to Applied Regression. Second Edition. Thousand Oaks CA: Sage. URL: http://socserv.socsci.mcmaster.ca/jfox/Books/Companion
Fumanal, B., C. Plenchette, B. Chauvel, and F. Bretagnolle. 2006. Which role can arbuscular mycorrhizal fungi play in the facilitation of Ambrosia artemisiifolia L. invasion in France? Mycor-rhiza 17: 25–35.
Goodwin, J. 1992. The role of mycorrhizal fungi in competitive interactions among native bunchgrasses and alien weeds: A review and synthesis. Northwest Sci. 66: 251–260.
Grace, C. and D.P. Stribley. 1991. A safer procedure for routine staining of vesicular arbuscular mycorrhizal fungi. Mycol. Res. 95: 1160–1162.
Graphpad Prism v.5.04 2007. GraphPad Software, San Diego California USA, www.graphpad.com.
Greipsson, S. and A. DiTommaso. 2006. Invasive non-native plants alter the occurrence of arbuscular mycorrhizal fungi and benefit from this association. Ecol. Restoration 24: 236–241.
Hale, A., S.J. Tonsor and S. Kalisz. 2011. Testing the mutualism disruption hypothesis: physiological mechanisms for invasion of intact perennial plant communities. Ecosphere 2: 110.
Hawkes, C.W., J. Belnap, C. D’Antonio and M.K. Firestone. 2006. Arbuscular mycorrhizal assemblages in native plant roots change in the presence of invasive exotic grasses. Plant and Soil 281: 369–380.
Hierro, J.L., J.L. Maron and R.M. Callaway. 2005. A biogeographi-cal approach to plant invasions: the importance of studying exotics in their introduced and native range. J. Ecol. 93: 5–15.
Holm, L.G., D.L. Plucknett, J.V. Pancho and J.P. Herberger. 1977. The World’s Worst Weeds. Distribution and Biology. Univ. Press of Hawaii, Honolulu, Hawaii.
Kalapos, T. 1991. C3 and C4 grasses of Hungary: environmental requirements, phenology and role in the vegetation. Abstracta Bot. 15: 83–88.
Keane, R.M. and M.J. Crawley. 2002. Exotic plant invasions and the enemy release hypothesis. Trends Ecol. Evol. 17: 164–170.
Klironomos, J. 2000. Host-specificity and functional diversity among arbuscular mycorrhizal fungi. In: Bell, C.R., M. Brylin-ski and P. Johnson-Green. (eds.) Microbial Biosystems: New Frontiers. Proceedings of the 8th International Symposium of Microbial Ecology, Halifax, NS, Canada. Atlantic Canada Society for Microbial Ecology. pp. 845–851.
Klironomos, J.N. 2002. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417: 67–70.
Klironomos, J. 2003. Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84: 2292–2301.
Kourtev, P., J. Ehrenfeld and M. Häggblom. 2002. Exotic plant species alter the microbial community structure and function in the soil. Ecology 83: 3152–3166.
Kovács, M.G. and I. Bagi. 2001. Mycorrhizal status of plants in a mixed deciduous forest from the Great Hungarian Plain with special emphasis on the potential mycorrhizal partners of Ter-fezia terfezioides (Matt.) Trappe (Pezizales). Phyton 161–168.
Kovács, M.G. and Cs. Szigetvári. 2002. Mycorrhizae and other root-associated fungal structures of the plants of a sandy grassland on the Great Hungarian Plain. Phyton 42: 211–223.
Kovács-Láng, E. 1970. Fractional humus investigation of soils under sward communities (Festucetum vaginatae danubiale, Fes-tucetum wagneri) growing on sandy sites. Annales Universitatis Scientiarum Budapestiensis, Sectio Biologica 12: 163–170.
Lingfei, L., Y. Anna and Z. Zhiwei. 2005. Seasonality of arbuscular mycorrhizal symbiosis and dark septate endophytes in a grassland site in southwest China. FEMS Microbiol. Ecol. 54: 367–373.
Lugo, M.A, M.E. González Maza and M.N. Cabello. 2003. Arbus-cular mycorrhizal fungi in a mountain grassland II: Seasonal variation of colonization studied, along with its relation to grazing and metabolic host type. Mycologia 95: 407–415.
Marler, M.J., C.A. Zabinski and R.M. Callaway. 1999. Mycorrhizae indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology 80: 1180–1186.
Meinhardt, K.A. and C.A. Gehring. 2012. Disrupting mycorrhizal mutualisms: a potential mechanism by which exotic tamarisk outcompetes native cottonwoods. Ecol. Appl. 22: 532–549.
Merryweather, J. and A.H. Fitter. 1998. The arbuscular mycorrhizal fungi of Hyacinthoides non-scripta II. Seasonal and spatial patterns of fungal populations. New Phytol. 138: 131–142.
Mitchell, C.E., A.A. Agrawal, J.D. Bever, G.S. Gilbert, R.A. Huf-bauer, J.N. Klironomos, J.L. Maron, W.F. Morris, I.M. Parker, A.G. Power, E.W. Seabloom, M.E. Torchin and D.P. Vázquez 2006. Biotic interactions and plant invasions. Ecol. Lett. 9: 726–740.
Mihály, B. and A. Demeter. 2003. Invasive Alien Species in Hungary. National Ecological Network Vol. 6. Authority for Nature Conservation, Ministry of Environment and Water, Budapest.
Moles, A., M. Gruber and S. Bonser. 2008. A new framework for predicting invasive plant species. J. Ecol. 96: 13–17.
Molnár, Zs., M. Bíró, S. Bartha and G. Fekete. 2012. Past trends, present state and future prospects of Hungarian forest-steppes. In: Werger, M.J.A. and M.A. van Staalduinen (eds.) Eurasian Steppes. Ecological Problems and Livelihoods in a Changing World. Plant and Vegetation, vol. 6. Springer, Dordrecht. pp. 209–252.
Mummey, D.L., M.C. Rillig and W.E. Holben. 2005. Neighboring plant influences on arbuscular mycorrhizal fungal community composition as assessed by T-RFLP analysis. Plant and Soil 271: 83–90.
Niu, H.-b., W.-X. Liu, F.-H. Wan and B. Liu. 2007. An invasive aster (Ageratina adenophora) invades and dominates forest un-derstories in China: altered soil microbial communities facilitate the invader and inhibit natives. Plant and Soil 294: 73–85.
Pringle, A., J.D. Bever, M. Gardes, J.L. Parrent, M.C. Rillig and J.N. Klironomos. 2009. Mycorrhizal symbioses and plant invasions. Annu. Rev. Ecol. Syst. 40: 699–715.
Quinn, G.P. and J.M. Keough. 2002. Experimental Design and Data Analysis for Biologists. Cambridge University Press, New York.
R Development Core Team 2009. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org.
Reinhart, K.O. and R.M. Callaway. 2006. Soil biota and invasive plants. New Phytol. 170: 445–457.
Richardson, D.M., N. Allsopp, C.M. D’Antonio, S.J. Milton and M. Rejmánek. 2000. Plant invasions - the role of mutualism. Biol. Rev. 75: 65–93.
Roberts, K.J. and R.C. Anderson. 2001. Effect of garlic mustard [Al-liaria petiolata (Beib. Cavara & Grande)] extracts on plants and arbuscular mycorrhizal (AM) fungi. Amer. Midland Nat. 146: 146–152.
Rydlová, J. and M. Vosátka. 2001. Associations of dominant plant species with arbuscular mycorrhizal fungi during vegetation development on coal mine spoil banks. Folia Geobot. 36: 85–97.
Sanon, A., Beguiristain, T., Cébron, A., J. Berthelin, S.N. Sylla and R. Duponnois. 2012. Differencesinnutrient availability and my-corrhizal infectivity in soils invaded by an exotic plant negatively influence the development of indigenous Acacia species. J. Env. Manage. 95: S275–S279.
Sánchez-Castro, I., N. Ferrol, P. Cornejo and J.-M. Barea. 2012. Temporal dynamics of arbuscular mycorrhizal fungi colonizing roots of representative shrub species in a semi-arid Mediterranean ecosystem. Mycorrhiza 22: 449–460.
Seifert, E.K., J.D. Bever and J.L. Maron. 2009. Evidence for the evolution of reduced mycorrhizal dependence during plant invasion. Ecology 90: 1055–1062.
Shah, M.A., Z.A. Reshi and D. Khasa. 2009a. Arbuscular mycorrhi-zal status of some Kashmir Himalayan alien invasive plants. Mycorrhiza 20: 67–72.
Shah, M.A., Z.A. Reshi and D.P. Khasa. 2009b. Arbuscular mycor-rhizas: drivers or passengers of alien plant invasion. Bot. Rev. 75: 397–417.
Simberloff, D. and B.V. Holle. 1999. Positive interactions of nonin-digenous species: invasional meltdown? Biol. Conserv. 1: 21–32.
Somodi, I., K. Virágh and J. Podani. 2008. The effect of the expansion of the clonal grass Calamagrostis epigejos on the species turnover of a semi-arid grassland. Appl. Veg. Sci. 11: 187–192.
Stampe, E.D. and C. Daehler. 2003. Mycorrhizal species identity affects plant community structure and invasion: a microcosm study. Oikos 100: 362–372.
Stinson, K.A., S.A. Campbell, J.R. Powell, B.E. Wolfe, R.M. Cal-laway, G.C. Thelen, S.G. Hallett, D. Prati and J.N. Klironomos. 2006. Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol. 4: e140.
Terpó, A., M. Zajac and A. Zajac. 1999. Provisional list of Hungarian archaeophytes. Thaiszia - Journal of Botany 9: 41–47
Trouvelot, A., J.L. Kough and V. Gianinazzi-Pearson. 1986. Mesure du taux de mycorhization VA d’un systéme radiculare. Recherche de méthodes d’estimation ayant une signification fonc-tionelle. In: Mycorrhizae: Physiology and Genetics - Les mycorhizes: physiologie et génétique. Proceedings of the 1st ESM/1er SEM, Dijon, 1–5 July 1985.-INRA, Paris, pp. 217–221.
Turnau, K., T. Anielska, P. Ryszka, S. Gawronski, B. Ostachowicz and A. Jurkiewicz. 2008. Establishment of arbuscular mycorrhi-zal plants originating from xerothermic grasslands on heavy metal rich industrial wastes–new solution for waste revegeta-tion. Plant and Soil 305: 267–280.
Tutin T.G., V.H. Heywood, N.A. Burges, D.M. Moore, D.H. Valentine, S.M. Walters, and D.A. Webb (eds). 1964–1993. Flora Europaea, Vols. 1–5. Cambridge University Press, Cambridge, UK.
van der Heijden, M., T. Boller and A. Wiemken. 1998. Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79: 2082–2091.
van der Putten, W.H., G.A. Kowalchuk, E.P. Brinkman, G.T.A. Doodeman, R.M. van der Kaaij, A.F.D. Kamp, F.B.J. Menting and E.M. Veenendaal. 2007. Soil feedback of exotic savanna grass relates to pathogen absence and mycorrhizal selectivity. Ecology 88: 978–988.
van der Staaij, J., A. Rozema, A. van Beem and E. Aerts. 2001. Increased solar UV-B radiation may reduce infection by arbuscu-lar mycorrhizal fungi (AMF) in dune grassland plants: evidence from five years of field exposure. Plant Ecol. 154: 171–177.
Vilà M. and J. Weiner. 2004. Are invasive plant species better competitors than native plant species? - evidence from pair-wise experiments. Oikos 105: 229–238.
Vogelsang K.M., J.D. Bever, M.S.P. Griswold and P.A. Schultz. 2004. The Use of Mycorrhizal Fungi in Erosion Control Applications. California Department of Transportation, Sacramento, CA, USA.
Vogelsang, K.M. and J.D. Bever. 2009. Mycorrhizal densities decline in association with nonnative plants and contribute to plant invasion. Ecology 90: 399–407.
Wang, B. and Y.-L. Qiu. 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16: 299–363.
Wilson, G.W., K.R. Hickman and M.M. Williamson. 2012. Invasive warm-season grasses reduce mycorrhizal root colonization and biomass production of native prairie grasses. Mycorrhiza 22: 327–336.
Wolfe, B.E. and J.N. Klironomos. 2005. Breaking new ground: soil communities and exotic plant invasion. BioScience 55: 477–487.
Wolfe, B. E., V.L. Rodgers, K.A. Stinson and A. Pringle. 2008. The invasive plant Alliaria petiolata (garlic mustard) inhibits ec-tomycorrhizal fungi in its introduced range. J. Ecol. 16: 777–783.
Zabinski, C.A., L. Quinn and R.M. Callaway. 2002. Phosphorus uptake, not carbon transfer, explains arbuscular mycorrhizal enhancement of Centaurea maculosa in the presence of native grassland species. Funct. Ecol. 16: 758–765.
Zeileis, A. 2004. Econometric computing with HC and HAC covari-ance matrix estimators. J. Stat. Software 11: 1–17.
Zeileis, A. 2006. Object-oriented computation of sandwich estimators. J. Stat. Software 16: 1–16.
Zhang, Q., L.J. Yao, L.Y. Yang, J.J. Tang and X. Chen. 2007. Potential allelopathic effects of an invasive species Solidago canaden-sis on the mycorrhizae of native plant species. Allelopathy J. 20: 71–78.
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Endresz, G., Somodi, I. & Kalapos, T. Arbuscular mycorrhizal colonisation of roots of grass species differing in invasiveness. COMMUNITY ECOLOGY 14, 67–76 (2013). https://doi.org/10.1556/ComEc.14.2013.1.8
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DOI: https://doi.org/10.1556/ComEc.14.2013.1.8