Abstract
Plants infected with vertically transmitted fungal endophytes carry their microbial symbionts with them during dispersal into new areas. Yet, whether seed-borne endophytes enhance the host plant’s ability to overcome colonisation barriers and to regenerate within invaded sites remains poorly understood. We examined how symbiosis with asexual endophytic fungi (Neotyphodium) affected establishment and seed loss to predators in the invasive annual grass Lolium multiflorum (Italian ryegrass) across contrasting successional plots. Italian ryegrass seeds with high and low endophyte incidence were sown into three communities: a 1-year-old fallow field, a 15-year-old grassland, and a 24-year-old forest, which conformed to an old-field chronosequence in the eastern Inland Pampa, Argentina. We found that endophyte infection consistently increased host population recruitment and reproductive output. Endophyte presence also enhanced aerial biomass production of ryegrass in a low recruitment year but not in a high recruitment year, suggesting that symbiotic effects on growth performance are density dependent. Endophyte presence reduced seed removal by rodents, although differential predation may not account for the increased success of infected grass populations. Overall, there was no statistical evidence for an endophyte-by-site interaction, indicating that the fungal endosymbiont benefitted host establishment regardless of large differences in biotic and abiotic environment among communities. Our results imply that hereditary endophytes may increase the chances for host grass species to pass various ecological filters associated with invasion resistance across a broad range of successional habitats.
Similar content being viewed by others
References
Ahlholm JU, Helander M, Lehtimäki S, Wäli P, Saikkonen K (2002) Vertically transmitted fungal endophytes: different responses of host-parasite systems to environmental conditions. Oikos 99:173–183
Arnold AE (2008) Endophytic fungi: hidden components of tropical community ecology. In: Carson WP, Schnitzer SA (eds) Tropical forest community ecology. Wiley, Chichester, pp 254–272
Borer ET, Hosseini PR, Seabloom EW, Dobson AP (2007) Pathogen-induced reversal of native dominance in a grassland community. Proc Natl Acad Sci USA 104:5473–5478
Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125
Bush LP, Wilkinson HH, Schardl C (1997) Bioprotective alkaloids of grass–funga1 endophyte symbioses. Plant Physiol 114:1-7
Callaway RM, Thelen GC, Barth S, Ramsey PW, Gannon JE (2004) Soil fungi alter interactions between the invader Centaurea maculosa and North American natives. Ecology 85:1062–1071
Chaneton EJ, Omacini M, Trebino HJ, León RJC (2001) Disturbios, dominancia y diversidad de especies nativas y exóticas en pastizales pampeanos húmedos. An Acad Nac Cs Ex Fis Nat 53:121–140
Cheplick GP, Faeth SH (2009) Ecology and evolution of the grass–endophyte symbiosis. Oxford University Press, Oxford
Cheplick GP, Perera A, Koulouris K (2000) Effect of drought on the growth of Lolium perenne genotypes with and without fungal endophytes. Funct Ecol 14:657–667
Clay K (1987) Effects of fungal endophytes on seed and seedling biology of Lolium perenne and Festuca arundinaceae. Oecologia 73:358–362
Clay K (2001) Symbiosis and the regulation of communities. Am Zool 41:810–824
Clay K, Schardl CP (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:99–127
Clay K, Marks S, Cheplick GP (1993) Effects of insect herbivory and fungal endophyte infection on competitive interactions among grasses. Ecology 74:1767–1777
Clay K, Holah J, Rudgers JA (2005) Herbivores cause a rapid increase in hereditary symbiosis and alter plant community composition. Proc Natl Acad Sci USA 102:12465–12470
Crawley MJ (1993) GLIM for ecologists. Blackwell, Oxford
Desprez-Loustau JM, Robin C, Buée M, Courtecuisse R, Garbaye J, Suffert F, et al. (2007) The fungal dimension of biological invasions. Trends Ecol Evol 22:472–480
Douglas AE (1994) Symbiotic interactions. Oxford University Press, Oxford
Eerens JPJ, Lucas RJ, Easton HS, White JGH (1998) Influence of the ryegrass endophyte (Neotyphodium lolii) in a cool moist environment. I. Pasture production. N Z J Agric Res 41:39–48
Facelli JM, León RJC (1986) El establecimiento espontáneo de árboles en la Pampa—un enfoque experimental. Phytocoenology 14:263–274
Facelli JM, D’Angela E, León RJC (1987) Diversity changes during pioneer stages in a subhumid pampean grassland succession. Am Midl Nat 117:17–25
Faeth SH, Bultman TL (2002) Endophytic fungi and interactions among host plants, herbivores, and natural enemies. In: Tscharntke T, Hawkins BA (eds) Multitrophic level interactions. Cambridge University Press, Cambridge, pp 89–123
Faeth SH, Hamilton CE (2006) Does an asexual endophyte symbiont alter life stage and long-term survival in a perennial host grass? Microbial Ecol 52:748–755
Faeth SH, Helander ML, Saikkonen KT (2004) Asexual Neotyphodium endophytes in a native grass reduce competitive abilities. Ecol Lett 7:304–313
Fenner M (1987) Seedlings. New Phytol (Suppl) 106:35–47
Ghersa CM, León RJC (1999) Successional changes in agroecosystems of the Rolling Pampa. In: Walker LR (ed) Ecosystems of disturbed ground. Ecosystems of the world, vol 16. Elsevier, Amsterdam, pp 487–502
Grime JP (2001) Plant strategies, vegetation processes and ecosystem properties. Wiley, Chichester
Gundel PE, Maseda P, Vila Aiub MM, Ghersa CM, Benech-Arnold RL (2006) Effects of Neotyphodium fungi on Lolium multiflorum seed germination in relation to water availability. Ann Bot 97:571–577
Gundel PE, Batista WB, Texeira M, Martinez-Ghersa MA, Omacini M, Ghersa CM (2008) Neotyphodium endophyte infection frequency in annual grass populations: relative importance of mutualism and transmission efficiency. Proc R Soc B 275:897–905
Gundel PE, Garibaldi LA, Tognetti PM, Aragón R, Ghersa CM, Omacini M (2009) Imperfect vertical transmission of the endophyte Neotyphodium in exotic grasses in grasslands of the flooding pampa. Microb Ecol 57:740–748
Herre EA, Knowlton N, Mueller UG, Rehner SA (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14:49–53
Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70
Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989
Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494
Malinowski DA, Belesky DP (2000) Adaptations of endophyte cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940
Mangla S, Inderjit, Callaway RM (2008) Exotic invasive plant accumulates native soil patthogens which inhibit native plants. J Ecol 96:58–67
McKell CM, Duncan C, Muller CH (1969) Competitive relationships of annual ryegrass (Lolium multiflorum Lam.). Ecology 50:653–657
Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN et al (2006) Biotic interactions and plant invasion. Ecol Lett 9:726–740
Moon CD, Scott B, Schardl CL, Christensen MJ (2000) Evolutionary origins of Epichloë endophytes from annual ryegrasses. Mycologia 92:1103–1108
Morris WF, Hufbauer RA, Agrawal AA, Bever JD, Borowicz VA, Gilbert GS et al (2007) Direct and interactive effects of enemies and mutualists on plant performance: a meta-analysis. Ecology 88:1021–1029
Nuñez MA, Horton TR, Simberloff D (2009) Lack of belowground mutualisms hinders Pinaceae invasions. Ecology 90:2352–2359
Omacini M, Chaneton EJ, León RJC, Batista WB (1995) Old-field successional dynamics on the Inland Pampa, Argentina. J Veg Sci 6:309–316
Omacini M, Chaneton EJ, Ghersa CM, Müller CB (2001) Symbiotic fungal endophytes control insect host–parasite interaction webs. Nature 409:78–81
Omacini M, Chaneton EJ, Ghersa CM (2005) A hierarchical framework for understanding the ecosystem consequences of endophyte–grass symbioses. In: Roberts CA, West CP, Spiers DE (eds) Neotyphodium in cool-season grasses. Blackwell, Ames, pp 141–162
Omacini M, Eggers T, Bonkowski M, Jones TH (2006) Leaf endophytes affect mycorrhizal status and growth of co-infected and neighbouring plants. Funct Ecol 20:226–232
Omacini M, Chaneton EJ, Bush L, Ghersa CM (2009) A fungal endosymbiont affects host plant recruitment through seed- and litter-mediated mechanisms. Funct Ecol 23:1148–1156
Parker MA (2001) Mutualism as a constrain on invasion success for legumes and rhizobia. Div Distrib 7:125–136
Parker IM, Gilbert GS (2007) When there is no escape: the effects of natural enemies on native, invasive, and noninvasive plants. Ecology 88:1210–1224
Parodi LR (1930) Ensayo fitosociológico sobre el Partido de Pergamino. Rev Fac Agron Vet B Aires 7:65–271
Rejmánek M (1989) Invasibility of plant communities. In: Drake JA et al (eds) Biological invasions: a global perspective. Wiley, Chichester, pp 369–388
Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmánek M (2000) Plant invasions—the role of mutualisms. Biol Rev 75:65–93
Rudgers JA, Mattingly WB, Koslow JM (2005) Mutualistic fungus promotes plant invasion into diverse communities. Oecologia 144:463–471
Rudgers JA, Holah J, Orr SP, Clay K (2007) Forest succession suppressed by an introduced plant–fungal symbiosis. Ecology 88:18–25
Rudgers JA, Afkhami ME, Rúa MA, Davitt AJ, Hammer S, Huguet VM (2009) A fungus among us: broad patterns of endophyte distribution in the grasses. Ecology 90:1531–1539
Saikkonen K, Wali P, Helander M, Faeth SH (2004) Evolution of endophyte–plant symbioses. Trends Plant Sci 9:275–280
SAS Institute (1996) SAS system for Windows, release 6.12. User’s guide. SAS Institute, Cary
Schardl CL, Leutchmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340
Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176
Soriano A (1992) Río de la Plata grasslands. In: Coupland RT (ed) Natural grasslands: introduction, western hemisphere. Ecosystems of the world 8A. Elsevier, Amsterdam, pp 367–407
Söyrinki N (2001) On the alien flora of the province of Buenos Aires, Argentina. Ann Bot Fenn 28:59–79
Stachowicz JJ (2001) Mutualism, facilitation, and the structure of ecological communities. Bioscience 51:235–246
Steel RGD, Torrie JH (1980) Principles and procedures of statistics: a biometrical approach, 2nd edn. McGraw-Hill, Tokyo
Stinson KA, Campbell SA, Powell JR, Wolfe BE, Callaway RM et al (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PloS Biol 4:727–731
Sugawara K, Inoue T, Yamashita M, Ohkubo H (2006) Distribution of the endophytic fungus, Neotyphodium occultans in naturalized Italian ryegrass in western Japan and its production of bioactive alkaloids known to repel insect pests. Grassl Sci 52:147–154
TePaske M, Powell R, Clement S (1993) Analyses of selected endophyte-infected grasses for the presence of loline-type and ergot-type alkaloids. J Agric Food Chem 41:2299–2303
Tibbets TM, Faeth SH (1999) Neotyphodium endophytes in grasses: deterrernts or promoters of herbivory by leaf-cutting ants. Oecologia 118:297–305
Tognetti PM, Chaneton EJ, Omacini M, Trebino HJ, León RJC (2010) Exotic versus native plant dominance over 20 years of old-field succession on set-aside farmland in Argentina. Biol Conserv: doi:10.1016/j.biocon.2010.06.016
Turnbull LA, Crawley MJ, Rees M (2000) Are plant populations seed-limited: a review of seed sowing experiments. Oikos 88:225–238
Van der Putten WH, Klironomos JN, Wardle DA (2007) Microbial ecology of biological invasions. ISME 1:28–37
Vila-Aiub MM, Gundel PE, Ghersa CM (2005) Fungal endophyte infection changes growth attributes in Lolium multiflorum Lam. Aust Ecol 30:49–57
Wolfe BE, Klironomos JN (2005) Breaking new ground: soil communities and exotic plant invasion. Bioscience 55:477–487
Acknowledgments
We thank P. Tognetti and I. Miranda for field assistance, and the Administración de Campos (UBA) for lodging and logistic support at Estancia San Claudio, and Stan Faeth for comments on the manuscript. The study was partly funded by Consejo Nacional de Investigaciones Científicas, Agencia Nacional de Promoción Científica, Universidad de Buenos Aires and Fundación Antorchas. A U. was supported by a CONICET doctoral fellowship. The reported experiments comply with the current laws of Argentina.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Melinda Smith.
Rights and permissions
About this article
Cite this article
Uchitel, A., Omacini, M. & Chaneton, E.J. Inherited fungal symbionts enhance establishment of an invasive annual grass across successional habitats. Oecologia 165, 465–475 (2011). https://doi.org/10.1007/s00442-010-1740-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-010-1740-z