Abstract
Both Impatiens glandulifera and Fallopia japonica are highly invasive plant species that have detrimental impacts on native biodiversity in areas where they invade and form dense monocultures. Both species are weakly dependent on arbuscular mycorrhizal fungi (AMF) for their growth and, therefore, under monotypic stands, the AMF network can become depauperate. We evaluated the impact of I. glandulifera and F. japonica on the performance (expressed as shoot biomass) of three UK native species (Plantago lanceolata, Lotus corniculatus and Trifolium pratense) grown in soil collected from under stands of both invasive plants and compared to plants grown in soil from under stands of the corresponding native vegetation. All native species had a higher percentage colonisation of AMF when grown in uninvaded soil compared to the corresponding invaded soil. P. lanceolata and L. corniculatus had a higher biomass when grown in uninvaded soil compared to corresponding invaded soil indicating an indirect impact from the non-native species. However, for T. pratense there was no difference in biomass between soil types related to I. glandulifera, suggesting that the species is more reliant on rhizobial bacteria. We conclude that simply managing invasive populations of non-native species that are weakly, or non-dependent, on AMF is inadequate for habitat restoration as native plant colonisation and establishment may be hindered by the depleted levels of AMF in the soil below invaded monocultures. We suggest that the reintroduction of native plants to promote AMF proliferation should be incorporated into future management plans for habitats degraded by non-native plant species.
Similar content being viewed by others
References
Allen MF, Allen EB, Gomez-Pompa A (2005) Effects of mycorrhizae and nontarget organisms on restoration of seasonal tropical forest in Quintana Roo, Mexico: factors limiting tree establishment. Restor Ecol 13:325–333
Beerling DJ, Perrins JM (1993) Impatiens glandulifera Royle (Impatiens roylei Walp.). J Ecol 81:367–382
Beerling DJ, Bailey JP, Conolly AP (1994) Fallopia japonica (Houtt.) Ronse Decraene. J Ecol 82:959–979
Bever JD, Morton JB, Antonovics J, Schultz PA (1996) Host-dependent sporulation and species diversity of arbuscular fungi in a mown grassland. J Ecol 84:71–82
Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154:275–304
Caravaca F, Barea JM, Palenzuela J, Figueroa D, Alguacil MM, Roldan A (2003) Establishment of shrub species in a degraded semiarid site after inoculation with native or allochthonous arbuscular mycorrhizal fungi. Appl Soil Ecol 22:103–111
Chittka L, Schürkens S (2001) Successful invasion of a floral market. Nature 411:653
Clements DR, Feenstra KR, Jones K, Staniforth R (2008) The biology of invasive alien plants in Canada. 9. Impatiens glandulifera Royle. Can J Plant Sci 88:403–417
Cockel CP, Tanner RA (2011) Impatiens glandulifera Royle (Himalayan balsam). A handbook of global freshwater invasive species. Earthscan, London, pp 67–77
Corbin EJ, Brockwell J, Gault RR (1977) Nodulation studies on chickpea (Cicer arietinum). Aust J Exp Agric Anim Husb 17:126–134
Curaqueo G, Barea JM, Acevedo E, Rubio R, Cornejo P, Borie F (2011) Effects of different tillage system on arbuscular mycorrhizal fungal propagules and physical properties in a Mediterranean agroecosystem in central Chile. Soil Tillage Res 113:11–18
Denison RF, Kiers ET (2011) Life histories of symbiotic rhizobia and mycorrhizal fungi. Curr Biol 21:775–785
Douds DD, Millner PD (1999) Biodiversity of arbuscular mycorrhizal fungi in agroecosystems. Agric Ecosyst Environ 74:77–93
Fansler VA, Mangold JM (2011) Restoring native plants to create wheatgrass stands. Restor Ecol 19:16–23
Frostegård A, Tunlid A, Bååth E (2011) Use and misuse of PLFA measurements in soils. Soil Biol Biochem 43(8):1621–1625
Gange AC, Ayres RL (1999) On the relation between arbuscular mycorrhizal colonization and plant ‘benefit’. Oikos 87:615–621
Gange AC, Brown VK, Farmer LM (1990) A test of mycorrhizal benefit in an early successional plant community. New Phytol 115:85–91
Gange AC, Brown VK, Sinclair GS (1993) Vesicular-arbuscular mycorrhizal fungi: a determinant of plant community structure in early succession. Funct Ecol 7:616–622
Geddes JS, Shaw RG, Tiffin P (2012) Interactions between soil habitats and geographic range location affect plant fitness. PLoS One 7(5):e36015. doi:10.1371/journal.pone.0036015
Gerber E, Krebs C, Murrell C, Moretti M, Rocklin R, Schaffner U (2008) Exotic invasive knotweeds (Fallopia spp.) negatively affect native plant and invertebrate assemblages in European riparian habitats. Biol Conserv 141:646–654
Giovannetti M, Avio L, Sbrana C (2010) Fungal spore germination and presymbiotic mycelial growth- physiological and genetic aspects. Arbuscular mycorrhizas: physiology and Function. Springer, Dordrecht, pp 3–32
Grman E, Suding KN (2010) Within-year soil legacies contribute to strong priority effects of exotics on native California grassland communities. Restor Ecol 18:664–670
Harley JL, Harley EL (1987) A check-list of mycorrhiza in the British flora—addenda, errata and index. New Phytol 107:741–749
Harner MJ, Mummey DL, Stanford JA, Rillig MC (2010) Arbuscular mycorrhizal fungi enhance spotted knapweed growth across a riparian chronosequence. Biol Invasions 12:1481–1490
Harris JA (2003) Measurements of the soil microbial community for estimating the success of restoration. Eur J Soil Sci 54:801–808
Hulme PE, Bremner ET (2006) Assessing the impact of Impatiens glandulifera on riparian habitats: partitioning diversity components following species removal. J Appl Ecol 43:43–50
Jansa J, Mozafar A, Kuhn G, Anken T, Ruh R, Sanders R, Frossard E (2003) Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecol Appl 13:1164–1176
Jeffries PS, Gianninazzi S, Perotto KK, Barea JM (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils 37:1–16
Ji B, Bentivenga SP, Casper BB (2010) Evidence for ecological matching of whole AM fungal communities to the local plant-host environment. Ecology 91:3037–3046
Klironomos JN, McCune L, Hart M, Neville J (2001) The influence of arbuscular mycorrhizae on the relationship between plant diversity and productivity. Ecol Lett 3:137–141
Lobstein A, Brenne X, Feist E, Metz N, Weniger B, Anton R (2001) Quantitative determination of naphthoquinones of Impatiens species. Phytochem Anal 12:202–205
Marler MJ, Zabinski CA, Callaway RM (1999) Mycorrhizae indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology 80:1180–1186
Maule H, Andrews M, Watson C, Cherrill A (2000) Distribution, biomass and effect on native species of Impatiens glandulifera in a deciduous woodland in northeast England. Asp Appl Biol 58:31–38
McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular–arbuscular mycorrhizal fungi. New Phytol 115:495–501
Miller RM, Jastrow JD (1992) The application of VA mycorrhizae to ecosystem restoration and reclamation. Mycorrhizal functioning: an integrative plant-fungal process. Chapman and Hall, New York, pp 438–467
Mirás-Avalos JM, Antunes PM, Koch A, Khosla K, Klironomos JN, Dunfield KE (2011) The influence of tillage on the structure of rhizosphere and root-associated arbuscular mycorrhizal fungal communities. Pedobiologia 54:235–241
Murrell C, Gerber E, Krebs C, Parepra M, Schaffner U, Bossdorf O (2011) Invasive knotweed affects native plants through allelopathy. Am J Bot 98:38–43
Ohsowski BM, Klironomos JN, Dunfield KE, Hart MM (2012) The potential of soil amendments for restoring severely disturbed grasslands. Appl Soil Ecol 60:77–83
Olsson PA, Rahm J, Aliasgharzad N (2010) Carbon dynamics in mycorrhizal symbioses is linked to carbon costs and phosphorus benefits. FEMS Microbiol Ecol 72:123–131
Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endo-symbioses. Nat Rev Microbiol 6:755–763
Perkins LB, Nowak RS (2012) Native and non-native grasses generate common types of plant-soil feedbacks by altering soil nutrients and microbial communities. Oikos. doi:10.1111/j.1600-0706.2012.20592.x
R Development Core Team (2011) R: a language and environment for statistical computing. R foundation for statistical computing. Vienna, Austria. ISBN: 3-900051-07-01
Reinhart KO, Callaway KM (2006) Tansley review: soil biota and invasive plants. New Phytol 170:445–457
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
Stinson KA, Campbell SA, Powell JR, Wolf BE, Callaway RM, Thelen GC, Hallett SG, Prati D, Kilronomos JN (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4(5):e140. doi:10.1371/journal.pbio.0040140
Thiet RK, Boerner REJ (2007) Spatial patterns of ectomycorrhizal fungal inoculum in arbuscular mycorrhizal barrens communities: implications for controlling invasion by Pinus virginiana. Mycorrhiza 17(6):507–517
van der Heijden MGA, Boller T, Wiemken A, Sanders IR (1998) Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79:2082–2091
van der Putten WH, Ruiter PC, Hol WHG, Mever KM, Bezemer TM, Bradford MA, Christensen S, Eppinga MB, Fukami T, Hemerik L, Molofsky J, Schädler M, Scherber C, Strauss SY, Vos M, Wardle DA (2009) Empirical and theoretical challenges in aboveground–belowground ecology. Oecologia 161:1–14
Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink and vinegar, a simple staining technique for arbuscular–mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007
Vogelsang KM, Reynolds HL, Bever JD (2006) Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol 172:554–562
Acknowledgments
We would like to thank Alex Lee and Oliver Kerr for assisting in the experimental recording for this experiment. We would also like to thank British Airways and the rangers at Harmondsworth Moor for allowing access to their land to collect soil samples. We are very grateful to René Eschen (CABI) for constructive comments on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Tanner, R.A., Gange, A.C. The impact of two non-native plant species on native flora performance: potential implications for habitat restoration. Plant Ecol 214, 423–432 (2013). https://doi.org/10.1007/s11258-013-0179-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-013-0179-9