Abstract
Fungal endophytes in cool-season grasses may affect communities at multiple trophic levels. However, it is unclear whether community-scale endophyte effects arise due to the endophyte itself or as a result of unique, endophyte–host interactions. We used a long-term field experiment to test whether common-toxic (CT) and non-ergot alkaloid-producing (novel) endophytes in Schedonorus arundinaceus (tall fescue) forage cultivars consistently affect communities across tall fescue hosts. Tilled plots (2 × 2 m; Guelph, ON) were seeded with Georgia 5 and Jesup cultivars containing either the CT or AR542 (novel) endophyte and allowed to be re-colonized by plant species from the local propagule pool. Non-seeded control plots were included to assess effects of seeding the non-native grass. We assessed plant, invertebrate, soil moisture, and soil nutrient responses to the endophyte–cultivar treatments after four growing seasons. Seeding tall fescue affected plant species abundances, but not richness, and did not consistently alter soil moisture and nutrient pools. Endophyte identity in the tall fescue cultivars affected the communities, but effects were not consistent between cultivars. Within Georgia 5, the AR542 endophyte reduced tall fescue abundance and altered the invertebrate community relative to CT plots. Within Jesup, the AR542 endophyte reduced species evenness and decreased soil moisture during dry periods relative to CT plots. Endophyte effects were not consistent between cultivars, and it is probable that the community-scale effects of endophyte infection in tall fescue cultivars arise due to unique interactions between cultivar and endophyte.
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References
Antunes PM, Miller J, Carvalho LM, Klironomos JN, Newman JA (2008) Even after death the endophytic fungus of Schedonorus phoenix reduces the arbuscular mycorrhizas of other plants. Funct Ecol 22:912–918
Armas C, Kim J, Bleby T, Jackson R (2012) The effect of hydraulic lift on organic matter decomposition, soil nitrogen cycling, and nitrogen acquisition by a grass species. Oecologia 168:11–22
Assuero SG, Matthew C, Kemp PD, Latch GCM, Barker DJ et al (2000) Morphological and physiological effects of water deficit and endophyte infection on contrasting tall fescue cultivars. N Z J Agric Res 43:49–61
Belesky DP, Burner DM, Ruckle JM (2008) Does endophyte influence resource acquisition and allocation in defoliated tall fescue as a function of microsite conditions? Environ Exp Bot 63:368–377
Bouton JH, Gates RN, Hill GM, Owsley M, Wood DT (1993) Registration of ‘Georgia 5’ tall fescue. Crop Sci 33:1405
Bouton JH, Duncan RR, Gates RN, Hoveland CS, Wood DT (1997) Registration of ‘Jesup’ tall fescue. Crop Sci 37:1011–1012
Bouton JH, Latch GCM, Hill NS, Hoveland CS, McCann MA et al (2002) Reinfection of tall fescue cultivars with non-ergot alkaloid producing endophytes. Agron J 94:567–574
Brathen KA, Hagberg O (2004) More efficient estimation of plant biomass. J Veg Sci 15:653–660
Bultman TL, Rodstrom JL, Radabaugh KR, VanDop JD, Librizzi JM et al (2009) Influence of genetic variation in the fungal endophyte of a grass on an herbivore and its parasitoid. Entomol Exp Appl 130:173–180
Cheplick GP (2008) Host genotype overrides fungal endophyte infection in influencing tiller and spike production of Lolium perenne (Poaceae) in a common garden experiment. Am J Bot 95:1063–1071
Christensen MJ, Latch GCM (1991) Variation among isolates of Acremonium endophytes (A. coenophialum and possibly A. typhinum) from tall fescue (Festuca arundinacea). Mycol Res 95:1123–1126
Clay K, Holah J (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285:1742
Cully AC, Cully JF, Hiebert RD (2003) Invasion of exotic plant species in tallgrass prairie fragments. Conserv Biol 17:990–998
Daly HV, Doyen JT, Purcell AH (1998) Introduction to insect biology and diversity. Oxford University Press, Oxford
De Battista JP, Bouton JH, Bacon CW, Siegel MR (1990) Rhizome and herbage production of endophyte-removed tall fescue clones and populations. Agron J 82:651–654
Fribourg HA, Hannaway DB, West CP (2009) Tall fescue for the twenty-first century. American Society of Agronomy, Madison
Funk CR, White RH, Breen JP (1993) Importance of Acremonium endophytes in turf-grass breeding and management. Agric Ecosyst Environ 44:215–232
Garrison MA, Stier JC (2010) Cool-season turfgrass colony and seed survival in a restored prairie. Crop Sci 50:12
Gundel PE, Perez LI, Helander M, Saikkonen K (2013) Symbiotically modified organisms: nontoxic fungal endophytes in grasses. Trends Plant Sci 18:420–427
Hesse U, Schoberlein W, Wittenmayer L, Forster K, Warnstorff K et al (2003) Effects of Neotyphodium endophytes on growth, reproduction and drought-stress tolerance of three Lolium perenne L. genotypes. Grass Forage Sci 58:407–415
Hunt MG, Newman JA (2005) Reduced herbivore resistance from a novel grass–endophyte association. J Appl Ecol 42:762–769
Iqbal J, Nelson J, McCulley R (2013) Fungal endophyte presence and genotype affect plant diversity and soil-to-atmosphere trace gas fluxes. Plant Soil 364:15–27
Jonasson S (1988) Evaluation of the point intercept method for the estimation of plant biomass. Oikos 52:101–106
Kardol P, Cornips NJ, van Kempen MML, Bakx-Schotman JMT, van der Putten WH (2007) Microbe-mediated plant-soil feedback causes historical contingency effects in plant community assembly. Ecol Monogr 77:147–162
Keathley CP, Potter DA (2012) Arthropod abundance in tall fescue, Lolium arundinaceum, pastures containing novel ‘safe’ endophytes. J Appl Entomol 136:576–587
Kuldau G, Bacon C (2008) Clavicipitaceous endophytes: their ability to enhance resistance of grasses to multiple stresses. Biol Control 46:57–71
Latch GCM, Christensen MJ, Tapper BA, Easton HS, Hume DE et al (2000) Tall fescue endophytes. United States Patent No. 6,111,170, Washington, DC
Leahy M, Robinson S (eds) (2000) Pasture production. Ontario Ministry of Agriculture, Food and Rural Affairs [Publication 19], Toronto
MacDougall AS, Turkington R (2005) Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86:42–55
Malinowski DP, Belesky DP (2006) Ecological importance of Neotyphodium spp. grass endophytes in agroecosystems. Grassl Sci 52:1–14
Malinowski DP, Zuo H, Belesky DP, Alloush GA (2005) Evidence for copper binding by extracellular root exudates of tall fescue but not perennial ryegrass infected with Neotyphodium spp. endophytes. Plant Soil 267:1–12
Marshall SA (2006) Insects: their natural history and diversity. Firefly, Buffalo
Matthews JW, Clay K (2001) Influence of fungal endophyte infection on plant-soil feedback and community interactions. Ecology 82:500–509
Mian MAR, Hopkins AA, Zwonitzer JC (2002) Determination of genetic diversity in tall fescue with AFLP markers. Crop Sci 42:944–950
Omacini M, Semmartin M, Perez LI, Gundel PE (2012) Grass-endophyte symbiosis: a neglected aboveground interaction with multiple belowground consequences. Appl Soil Ecol 61:273–279
Popay AJ, Jensen JG (2005) Soil biota associated with endophyte-infected tall fescue in the field. N Z Plant Prot 58:117
Rasmussen S, Parsons A, Newman J (2009) Metabolomics analysis of the Lolium perenne—Neotyphodium lolii symbiosis: more than just alkaloids? Phytochem Rev 8:535–550
Ratliff LF, Ritchie JT, Cassel DK (1983) Field-measured limits of soil water availability as related to laboratory-measured properties. Soil Sci Soc Am J 47:770–775
Rudgers JA, Clay K (2007) Endophyte symbiosis with tall fescue: how strong are the impacts on communities and ecosystems? Fungal Biol Rev 21:107–124
Rudgers JA, Fischer S, Clay K (2010) Managing plant symbiosis: fungal endophyte genotype alters plant community composition. J Appl Ecol 47:468–477
Saikkonen K, Lehtonen P, Helander M, Koricheva J, Faeth SH (2006) Model systems in ecology: dissecting the endophyte-grass literature. Trends Plant Sci 11:428–433
Saikkonen K, Wali PR, Helander M (2011) Genetic compatibility determines endophyte-grass combinations. PLoS ONE 5:e11395
Saikkonen K, Gundel P, Helander M (2013) Chemical ecology mediated by fungal endophytes in grasses. J Chem Ecol 39:962–968
Shortt R, Eng P, Verhallen A, Fisher P (2011) Monitoring soil moisture to improve irrigation decisions. Ontario Ministry of Agriculture, Food and Rural Affairs Factsheet, Toronto
Timper P, Gates RN, Bouton JH (2005) Response of Pratylenchus spp. in tall fescue infected with different strains of the fungal endophyte Neotyphodium coenophialum. Nematology 7:105–110
Tozer KN, Lucas RJ, Edwards GR (2007) Suppression of annual grass weeds by AR542 endophyte infection in dryland tall fescue pastures. N Z Plant Prot 60:164–167
Vaylay R, van Santen E (2002) Application of canonical discriminant analysis for the assessment of genetic variation in tall fescue. Crop Sci 42:534–539
Vellend M, Drummond E, Tomimatsu H (2010) Effects of genotype identity and diversity on the invasiveness and invasibility of plant populations. Oecologia 162:371–381
Vesterlund S-R, Helander M, Faeth S, Hyvonen T, Saikkonen K (2011) Environmental conditions and host plant origin override endophyte effects on invertebrate communities. Fungal Divers 47:109–118
Wei YK, Gao YB, Xu H, Su D, Zhang X et al (2006) Occurrence of endophytes in grasses native to northern China. Grass Forage Sci 61:422–429
Yurkonis KA, Maherali H, Bolton KA, Klironomos JN, Newman JA (2012) Cultivar genotype, application and endophyte history affects community impact of Schedonorus arundinaceus. J Appl Ecol 49:1094–1102
Acknowledgments
P. Purvis, K. Carey, the staff at the Guelph Turfgrass Institute and members of J.A.N’s research group helped to establish, sample, and maintain the study. Invertebrates were identified with the assistance of members of the S. H. Marshall laboratory. Funding for this project was provided by grants from the Canadian Natural Science and Engineering Research Council to J.A.N., the Ontario Ministry of Agriculture, Food and Rural Affairs to J.A.N, H.M. and J.N.K., the Canada Foundation for Innovation/Ontario Innovation Trust to H.M., and the North Dakota Experimental Program to Stimulate Competitive Research to K.A.Y.
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Communicated by Gavin Kernaghan.
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Yurkonis, K.A., Shukla, K., Holdenried, J. et al. Endophytes inconsistently affect plant communities across Schedonorus arundinaceus hosts. Plant Ecol 215, 389–398 (2014). https://doi.org/10.1007/s11258-014-0309-z
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DOI: https://doi.org/10.1007/s11258-014-0309-z