Model systems in ecology: dissecting the endophyte–grass literature

Online Supplementary Material Model systems in ecology: dissecting the endophyte–grass literature Kari Saikkonen1, Päivi Lehtonen2, Marjo Helander2, Julia Koricheva3 and Stanley H. Faeth4 1 MTT Agrifood Research Finland, Plant Production Research, Karilantie 2 A, FI-50600 Mikkeli, Finland 2 Section of Ecology, Department of Biology, University of Turku, 20014 Turku, Finland 3 School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK 4 School of Life Sciences, Arizona State University, Tempe, AZ 85287-4501, USA Corresponding author: Saikkonen, K. (kari.saikkonen@mtt.fi). Survey of grass endophyte literature We used a dataset of 164 titles comprising 146 primary publications, 16 congress proceedings and 2 unpublished studies on grass endophytes published or conducted between 1982–2004. We compiled the reference database from narrative reviews of the topic, keyword searches in the Web of Science, reference sections of published papers and information gathered by networking with our colleagues over the past 15 years. To be included in the statistical synthesis of original data analyses (i.e. the meta-analysis), a study had to provide results as either (i) means, some measure of variance, and sample sizes of endophyte-free control and endophyte-infected groups in numerical or graphical form, (ii) correlation coefficients, (iii) two × two contingency tables, or (iv) F-, chi-square-, or t tests statistics and df. Only 56% of the titles presented sufficient data for the meta-analysis. Thus, we used two approaches to examine trends in grass endophyte literature in this study: (i) qualitative vote-counting-based approaches in all primary studies to assess the direction of endophyte effects on host plants and (ii) meta-analysis of studies that provided sufficient data to allow assessment of the magnitude of the endophyte effect on the host plant. In both approaches, we classified the studies in three categories: studies focusing on endophyte-mediated plant competition, plant performance or plant resistance to herbivores. In vote-counting, the outcome of each study was classified as either positive (endophytes benefit host plant), neutral (non-significant effect) or negative (endophytes decrease host plant performance, resistance to herbivores and/or competitive ability). We conducted the analyses in three steps. First, to examine temporal changes and the importance of individual publications on temporal trends in the endophyte literature, we carried out cumulative meta-analyses (using means of effect sizes from the primary publication) separately for the studies focusing on endophyte-mediated plant competition, plant performance or plant resistance to herbivores. In cumulative meta-analysis, studies are successively added to the analysis in a predetermined (in our case chronological) order, and the summary statistics are recalculated at each step [S1,S2]. Second, we examined sources of variation (including plant species, plant genotype and nutrient availability in soils) to assess the effects of endophytes on the host plants. Third, we examined possible publication bias in the endophyte literature associated with the quality of the journal, which was interpreted as the impact factor of the journal [obtained from the Journal Citation Reports of the Institute for Scientific Information (ISI)]. Meta-analysis Meta-analyses were conducted using the MetaWin, v. 2.0 statistical software [S3]. We used Fisher’s z-transformed correlation coefficients as a measure of effect size in analyses [S3] allowing us to combine the data from the primary studies presented in different forms. Another metric of effect size, Hedges’ d, which represents standardized mean difference [S4], was calculated if the means, sample sizes and standard deviations for both endophyte-infected (experimental group) and endophyte-free (control group) plants were available. Hedges’ d was then converted into correlation coefficient (r) by the function ( r = d2 d2 +4 ) [S5, S6], and then r was converted into Fisher’s z-transformed correlation coefficients using MetaWin Statistical Calculator [S3]. When the statistical summary information of the primary study was insufficient for calculating Hedges’ d, Fisher’s z-transformed correlation coefficients were calculated from summary statistics (e.g. F- or X2-statistics) if available using the MetaWin Statistical Calculator [S3]. The bias-corrected 95% bootstrap confidence intervals were generated from 4999 iterations. A relationship was considered significant if the confidence interval did not include zero. To test whether the effects of explanatory variables differ from each other, within and between-group heterogeneity was examined using a chi-square test statistic, Q. Because different response variables might indicate opposite effects on the plant (e.g. higher growth rate and mortality of herbivores, indicating higher and lower susceptibility of the host plant to the herbivores respectively), the sign of the effect size was adjusted so that positive effect sizes indicated benefits from the endophyte to the host plant compared with the endophyte-free host plant in terms of enhanced growth, reproduction, competitive abilities or resistance to herbivores. Primary publications commonly included several separate experiments (e.g. bioassays with different species and/or parallel experiments conducted in laboratory, greenhouse or common garden), which we considered as independent observations (see Table 1 in the main text). Some of the studies included variables that can be classified into two or all three of the categories (e.g. plant growth can indicate the performance or competitive ability of a plant). However, in these cases, the ambiguous variable was classified according to the focus of the study. When several estimates of effect size were available from a study, we pooled the data and calculated an overall effect for the study to avoid pseudoreplication. If responses were measured multiple times during the experiment, the last measurement was selected. References S1 Leimu, R. and Koricheva, J. (2004) Cumulative meta-analysis: a new tool for detection of temporal trends and publication bias in ecology. Proc. R. Soc. London Ser. B 271, 1961–1966 S2 Nykänen, H. and Koricheva, J. (2004) Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis. Oikos 104, 247–268 S3 Rosenberg, M.S. et al., eds (2000) MetaWin: Statistical Software for Meta–Analysis. Version 2.0., Sinauer Associates, Sunderland, MA, USA S4 Gurevitch, J. and Hedges, L.V. (1999) Statistical issue in ecological meta-analyses. Ecology 80, 1142–1149 S5 Koricheva, J. (2002) Meta-analysis of sources of variation in fitness costs of plant antiherbivore defenses. Ecology 83, 176– 190 S6 Rosenthal, R. (1994) Parametric measures of effect size. In The Handbook of Research Synthesis (Cooper, H. and Hedges, L.V., eds), pp. 231–244, Russell Sage Foundation, New York, NY, USA The dataset of the 164 titles used in the meta-analysis 1 2 3 4 5 6 7 8 9 10 11 12 13 14 Ahmad, S. et al. (1985) Fatality of house crickets on perennial ryegrasses infected with a fungal endophyte. Entomol. Exp. Appl. 39, 183–190 Ahmad, S. et al. (1986) Endophyte-enhanced resistance in perennial ryegrass to the bluegrass billbug, Sphenophorus parvulus. Entomol. Exp. Appl. 41, 3–10 Arachevaleta, M. et al. (1989) Effect of the tall fescue endophyte on plant-response to environmental-stress. Agron. J. 81, 83–90 Ball, O-J. et al. (1994) Effect of selected isolates of Acremonium endophytes on adult black beetle (Heteronychus arator) feeding. Proc. 47th N. Z. Plant Protect. Conf. 47, 227–231 Ball, O-J. et al. (1997) Effect of selected Neotyphodium lolii isolates on root-knot nematode (Meloidogyne marylandi) numbers in perennial ryegrass. Proc. 50th N. Z. Plant Prot. Conf. 50, 65–68 Barger, J.L. and Tannenbaum, M.G. (1998) Consumption of endophyte-infected fescue seeds and osmoregulation in whitefooted mice. J. Mammal. 79, 464–474 Bazely, D.R. et al. (1997) Interactions between herbivores and endophyte-infected Festuca rubra from the Scottish islands of St. Kilda, Benbecula and Rum. J. Appl. Ecol. 34, 847–860 Belesky, D.P. and Fedders, J.M. (1995) Tall fescue development in response to Acremonium coenophialum and soil acidity. Crop Sci. 35, 529–533 Boning, R.A. and Bultman, T.L. (1996) A test for constitutive and induced resistance by tall fescue (Festuca arundinacea) to an insect herbivore: impact of the fungal endophyte, Acremonium coenophialum. Am. Midl. Nat. 136, 328–335 Braman, S.K. et al. (2002) Grass species and endophyte effects on survival and development of fall armyworm (Lepidoptera : Noctuidae). J. Econ. Entomol. 95, 487–492 Breen, J.P. (1992) Temperature and seasonal effects on expression of Acremonium endophyte-enhanced resistance to Schizaphis graminum (Homoptera, Aphididae). Environ. Entomol. 21, 68–74 Breen, J.P. (1993) Enhanced resistance to fall armyworm (Lepidoptera, Noctudiae) in Acremonium endophyte-infected turfgrasses. J. Econ. Entomol. 86, 621–629 Breen, J.P. (1993) Enhanced resistance to 3 species of aphids (Homoptera, Aphididae) in Acremonium endophyte-infected turfgrasses. J. Econ. Entomol. 86, 1279–1286 Brem, D. and Leuchtmann, A. (2001) Epichloë grass endophytes increase herbivore resistance in the woodland grass Brachypodium sylvaticum. Oecologia 126, 522–530 15 Brem, D. and Leuchtmann, A. (2002) Intraspecific competition of endophyte infected vs uninfected plants of two woodland grass species. Oikos 96, 281–290 16 Bultman, T.L. and Bell, G.D. (2003) Interaction between fungal endophytes and environmental stressors influences plant resistance to insects. Oikos 103, 182–190 17 Bultman, T.L. and Conard, N.J. (1998) Effects of endophytic fungus, nutrient level, and plant damage on performance of fall armyworm (Lepidoptera : Noctuidae). Environ. Entomol. 27, 631–635 18 Bultman, T.L. and Ganey, D.T. (1995) Induced resistance to fall armyworm (Lepidoptera, Noctuidae) mediated by a fungal endophyte. Environ. Entomol. 24, 1196–1200 19 Carriere, Y. et al. (1998) Effect of endophyte incidence in perennial ryegrass on distribution, host-choice, and performance of the hairy chinch bug (Hemiptera : Lygaeidae). J. Econ. Entomol. 91, 324–328 20 Cheplick, G.P. (1997) Effects of endophytic fungi on the phenotypic plasticity of Lolium perenne (Poaceae). Am. J. Bot. 84, 34–40 21 Cheplick, G.P. and Clay, K. (1988) Acquired chemical defenses in grasses – the role of fungal endophytes. Oikos 52, 309–318 22 Cheplick, G.P. et al. (1989) Interactions between infection by endophytic fungi and nutrient limitation in the grasses Lolium perenne and Festuca arundinacea. New Phytol. 111, 89–97 23 Cheplick, G.P. et al. (2000) Effect of drought on the growth of Lolium perenne genotypes with and without fungal endophytes. Funct. Ecol. 14, 657–667 24 Clark, D.A. et al. (1996) Milk production and pasture silage with different levels of endophyte infection. Proc. NZ Soc. Anim. Prod. 56, 292–296 25 Clay, K. (1984) The effect of the fungus Atkinsonella hypoxylon (Clavicipitaceae) on the reproductive-system and demography of the grass Danthonia spicata. New Phytol. 98, 165–175 26 Clay, K. (1987) Effects of fungal endophytes on the seed and seedling biology of Lolium perenne and Festuca arundinacea. Oecologia 73, 358–362 27 Clay, K. (1990) Comparative demography of 3 graminoids infected by systemic, clavicipitaceous fungi. Ecology 71, 558–570 28 Clay, K. and Brown, V.K. (1997) Infection of Holcus lanatus and H. mollis by Epichloë in experimental grasslands. Oikos 79, 363–370 29 Clay, K. and Holah, J. (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285, 1742–1744 30 Clay, K. et al. (1985) Fungal endophytes of grasses and their effects on an insect herbivore. Oecologia 66, 1–5 31 Clay, K. et al. (1985) Fungal endophytes of Cyperus and their effect on an insect herbivore. Am. J. Bot. 72, 1284–1289 32 Clay, K. et al. (1989) Impact of the fungus Balansia henningsiana on Panicum agrostoides – frequency of infection, plantgrowth and reproduction, and resistance to pests. Oecologia 80, 374–380 33 Clay, K. et al. (1993) Effects of insect herbivory and fungal endophyte infection on competitive interactions among grasses. Ecology 74, 1767–1777 34 Clement, S.L. (1991) Field evaluation of wild barley accessions against Russian wheat aphid. Arthr. Manag. Tests 24, 409 35 Clement, S.L. et al. (1992) Behavior and performance of Diuraphis noxia (Homoptera, Aphididae) on fungal endophyteinfected and uninfected perennial ryegrass. J. Econ. Entomol. 85, 583–588 36 Clement, S.L. et al. (1996) Expression of Russian wheat aphid (Homoptera: Aphididae) resistance in genotypes of tall fescue harboring different isolates of Acremonium endophyte. J. Econ. Entomol. 89, 766–770 37 Clement, S.L. et al. (1997) Fungal endophytes of wild barley and their effects on Diuraphis noxia population development. Entomol. Exp. Appl. 82, 275–281 38 Clement, S.L. et al. (2001) Incidence and diversity of Neotyphodium fungal endophytes in tall fescue from Morocco, Tunisia, and Sardinia. Crop Sci. 41, 570–576 39 Clement, S.L. et al. (2005) Detrimental and neutral effects of wild barley – Neotyphodium fungal endophyte associations on insect survival. Entomol. Exp. Appl. 114, 119–125 40 Conover, M.R. (1998) Impact of consuming tall fescue leaves with the endophytic fungus, Acremonium coenophialum, on meadow voles. J. Mammal. 79, 457–463 41 Conover, M.R. (2003) Impact of the consumption of endophyte-infected perennial ryegrass by meadow voles. Agr. Ecosyst. Environ. 97, 199–203 42 Conover, M.R. and Messmer, T.A. (1996) Feeding preferences and changes in mass of Canada geese grazing endophyteinfected tall fescue. Condor 98, 859–862 43 Conover, M.R. and Messmer, T.A. (1996) Consequences for captive zebra finches of consuming tall fescue seeds infected with the endophytic fungus Acremonium coenophialum. Auk 113, 492–495 44 Cook, R. et al. (1991) Effects on plant-parasitic nematodes of infection of perennial ryegrass, Lolium perenne, by the endophytic fungus, Acremonium lolii. Crop Prot. 10, 403–407 45 Crutchfield, B.A. and Potter, D.A. (1994) Preferences of Japanese beetle and southern masked chafer (Coleoptera, Scarabaeidae) grubs among cool-season turfgrasses. J. Entomol. Sci. 29, 398–406 46 Crutchfield, B.A. and Potter, D.A. (1995) Damage relationships of Japanese beetle and southern masked chafer (Coleoptera, Scarabaeidae) grubs in cool-season turfgrasses. J. Econ. Entomol. 88, 1049–1056 47 Davidson, A.W. and Potter, D.A. (1995) Response of plant-feeding, predatory, and soil-inhabiting invertebrates to Acremonium endophyte and nitrogen-fertilization in tall fescue turf. J. Econ. Entomol. 88, 367–379 48 DeBattista, J.P. et al. (1990) Rhizome and herbage production of endophyte-removed tall fescue clones and populations. Agron. J. 82, 651–654 49 Durham, W.F. and Tannenbaum, M.G. (1998) Effects of endophyte consumption on food intake, growth, and reproduction in prairie voles. Can. J. Zool. 76, 960–969 50 Easton, H.S. et al. (2001) Selected endophyte and plant variation. In Proc. 4th Int. Neotyphodium/Grass Interactions Symposium (Paul, V.H. and Dapprich, P.D., eds), pp. 351–356 51 Eerens, J.P.J. et al. (1992) The ryegrass endophyte in a cool moist environment. Proc. NZ Grassl. Assoc. 54, 157–160 52 Eerens, J.P.J. et al. (1994) Ryegrass endophyte and sheep production. Proc. NZ Grassl. Assoc. 56, 255–258 53 Eerens, J.P.J. et al. (1998) Influence of the ryegrass endophyte (Neotyphodium lolii) in a cool-moist environment II. Sheep production. N. Z. J. Agric. Res. 41, 191–199 54 Eerens, J.P.J. et al. (1998) Influence of the ryegrass endophyte (Neotyphodium lolii) in a cool moist environment IV. Plant parasitic nematodes. N. Z. J. Agric. Res. 41, 209–217 55 Eerens, J.P.J. et al. (1998) Influence of the endophyte (Neotyphodium lolii) on morphology, physiology, and alkaloid synthesis of perennial ryegrass during high temperature and water stress. N. Z. J. Agric. Res. 41, 219–226 56 Eichenseer, H. and Dahlman, D.L. (1992) Antibiotic and deterrent qualities of endophyte-infected tall fescue to 2 aphid species (homoptera, aphidiae). Environ. Entomol. 21, 1046–1051 57 Eichenseer, H. and Dahlman, D.L. (1993) Survival and development of the true armyworm Pseudaletia unipuncta (Haworth) (Lepidoptera, Noctuidae), on endophyte-infected and endophyte-free tall fescue. J. Entomol. Sci. 28, 462–467 58 Eichenseer, H. et al. (1991) Influence of endophyte infection, plant-age and harvest interval on Rhopalosipum padi survival and its relation to quantity of N-formyl and N-acetyl loline in tall fescue. Entomol. Exp. Appl. 60, 29–38 59 Elbersen, H.W. and West, C.P. (1996) Growth and water relations of field-grown tall fescue as influenced by drought and endophyte. Grass Forage Sci. 51, 333–342 60 Elmi, A.A. et al. (2000) Endophyte effects on reproduction of a root-knot nematode (Meloidogyne marylandi) and osmotic adjustment in tall fescue. Grass Forage Sci. 55, 166–172 61 Faeth, S.H. et al. (2004) Asexual Neotyphodium endophytes in a native grass reduce competitive abilities. Ecol. Lett. 7, 304– 313 62 Filipov, N.M. et al. (1998) Vaccination against ergot alkaloids and the effect of endophyte-infected fescue seed-based diets on rabbits. J. Anim. Sci. 76, 2456–2463 63 Ford, V.L. and Kirkpatrik, T.L. (1989) Effects of Acremonium coenophialum in tall fescue on host disease and insect resistance and allelopathy to Pinus taeda seedlings. Arkansas Experiment Station Special Report 140, 29–34 64 Fortier, G.M. et al. (2000) Effects of tall fescue endophyte infection and population density on growth and reproduction in prairie voles. J. Wildl. Manage. 64, 122–128 65 Fortier, G.M. et al. (2001) Are female voles food limited? Effects of endophyte-infected tall fescue on home range size in female prairie voles (Microtus ochrogaster). Am. Midl. Nat. 146, 63–71 66 Gaynor, D.L. and Hunt, W.F. (1983) The relationship between nitrogen supply, endophytic fungus, and Argentine stem weevil resistance in ryegrasses. Proc. NZ Grassl. Assoc. 44, 257–263 67 Groppe, K. et al. (1999) Interaction between the endophytic fungus Epichloë bromicola and the grass Bromus erectus: effects of endophyte infection, fungal concentration and environment on grass growth and flowering. Mol. Ecol. 8, 1827–1835 68 Gwinn, K.D. and Gavin, A.M. (1992) Relationship between endophyte infestation level of tall fescue seed lots and Rhizoctonia zeae seedling disease. Plant Dis. 76, 911–914 69 Hardy, T.N. et al. (1985) Fall armyworm (Lepidoptera, Noctuidae) – a laboratory bioassay and larval preference study for the fungal endophyte of perennial ryegrass. J. Econ. Entomol. 78, 571–575 70 Hardy, T.N. et al. (1986) Leaf age and related factors affecting endophyte-mediated resistance to fall armyworm (Lepidoptera, Noctuidae) in tall fescue. Environ. Entomol. 15, 1083–1089 71 Hayes, C. and Faeth, S.H. Unpublished data. 72 Hesse, U. and Latch, G.C.M. (1999) Influence of Neotyphodium lolii and barley yellow dwarf virus, individually and combined, on the growth of Lolium perenne. Australas. Plant Pathol. 28, 240–247 73 Hill, N.S. et al. (1990) Growth, morphological, and chemical-component responses of tall fescue to Acremonium coenophialum. Crop Sci. 30, 156–161 74 Hill, N.S. et al. (1991) Competitiveness of tall fescue as influenced by Acremonium coenophialum. Crop Sci. 31, 185–190 75 Hill, N.S. et al. (1998) Encroachment of endophyte-infected on endophyte-free tall fescue. Ann. Bot. 81, 483–488 76 Hoveland, C.S. et al. (1980) Association of Epichloë typhina fungus and steer performance on tall fescue pasture. Agron. J. 72, 1064–1065 77 Hoveland, C.S. et al. (1983) Steer performance and association of Acremonium coenophialum fungal endophyte on tall fescue pasture. Agron. J. 75, 821–824 78 Hoveland, C.S. et al. (1997) Tall fescue response to clipping and competition with no-till seeded alfalfa as affected by fungal endophyte. Agron. J. 89, 119–125 79 Hoveland, C.S. et al. (1999) Fungal endophyte effects on production of legumes in association with tall fescue. Agron. J. 91, 897–902 80 Humphries, S.S. et al. (2001) Effects of endophyte status of tall fescue tissues on the earthworm (Eisenia fetida). Environ. Toxicol. Chem. 20, 1346–1350 81 Jackson, J.A. et al. (1997) Effect of dietary supplementation with vitamin E for lactating dairy cows fed tall fescue hay infected with endophyte. J. Dairy Sci. 80, 569–572 82 Jensen, J.G. and Popay, A.J. (2004) Perennial ryegrass infected with AR37 endophyte reduces survival of porina larvae. Proc. 57th N. Z. Plant Prot. Conf. 57, 323–328 83 Johnson, M.C. et al. (1985) Insect feeding deterrents in endophyte-infected tall fescue. Appl. Environ. Microbiol. 49, 568–571 84 Johnson-Cicalese, J.M. and White, R.H. (1990) Effect of Acremonium endophytes on 4 species of billbug found on New Jersey turfgrasses. J. Am. Soc. Hort. Sci. 115, 602–604 85 Kimmons, C.A. et al. (1990) Nematode reproduction on endophyte-infected and endophyte-free tall fescue. Plant Dis. 74, 757–761 86 Kindler, S.D. et al. (1991) Reproduction and damage by Russian wheat aphid (Homoptera, Aphididae) as influenced by fungal endophytes and cool-season turfgrasses. J. Econ. Entomol. 84, 685–692 87 Knoch, T.R. et al. (1993) Endophytic fungi alter foraging and dispersal by desert seed-harvesting ants. Oecologia 95, 470– 473 88 Koga, H. et al. (1997) Successive transmission of resistance to bluegrass webworm to perennial ryegrass and tall fescue plants by artificial inoculation with acremonium endophytes. JARQ 31, 109–115 89 Koppenhöfer, A.M. et al. (2003) Effects of turfgrass endophytes (Clavicipitaceae : Ascomycetes) on white grub (Coleoptera : Scarabaeidae) larval development and field populations. Environ. Entomol. 32, 895–906 90 Latch, G.C.M. et al. (1985) Aphid detection of endophyte infection in tall fescue. N. Z. J. Agric. Res. 28, 129–132 91 Latch, G.C.M. et al. (1985) Endophytic fungi affect growth of perennial ryegrass. N. Z. J. Agric. Res. 28, 165–168 92 Lehtonen, P. et al. (2005) Are endophyte-mediated effects on herbivores conditional on soil nutrients? Oecologia 142, 38–45 93 Lehtonen, P. et al. (2005) Transfer of endophyte-origin defensive alkaloids from a grass to a hemiparasitic plant. Ecol. Lett. 8, 1256–1263 94 Lewis, G.C. and Clements, R.O. (1986) A survey of ryegrass endophyte (Acremonium loliae) in the UK and its apparent ineffectuality on a seedling pest. J. Agric. Sci. 107, 633–638 95 Lewis, G.C. et al. (1993) Evaluation of grasses infected with fungal endophytes against locusts. Ann. Appl. Biol. S122, 142– 143 96 Lewis, G.C. et al. (1996) Effect of infection by the endophytic fungus Acremonium lolii on growth and nitrogen uptake by perennial ryegrass (Lolium perenne) in flowing solution culture. Ann. Appl. Biol. 129, 451–460 97 Lopez, J.E. et al. (1995) Effect of endophytic fungi on herbivory by redlegged grasshoppers (Orthoptera: Acrididae) on Arizona fescue. Environ. Entomol. 24, 1576–1580 98 Madej, C.W. and Clay, K. (1991) Avian seed preference and weight-loss experiments – the effect of fungal endophyteinfected tall fescue seeds. Oecologia 88, 296–302 99 Malinowski, D. et al. (1997) Growth and water status in meadow fescue is affected by Neotyphodium and Phialophora species endophytes. Agron. J. 89, 673–678 100 Malinowski, D. et al. (1997) Symbiosis with Neotyphodium uncinatum endophyte may increase the competitive ability of meadow fescue. Agron. J. 89, 833–839 101 Malinowski, D.P. et al. (1998) Influence of phosphorus on the growth and ergot alkaloid content of Neotyphodium coenophialum-infected tall fescue (Festuca arundinacea Schreb.). Plant Soil 198, 53–61 102 Malinowski, D.P. et al. (1999) Endophyte infection may affect the competitive ability of tall fescue grown with red clover. J. Agron. Crop Sci. 183, 91–101 103 Marks, S. and Clay, K. (1990) Effects of CO2 enrichment, nutrient addition, and fungal endophyte-infection on the growth of 2 grasses. Oecologia 84, 207–214 104 Marks, S. and Lincoln, D.E. (1996) Antiherbivore defense mutualism under elevated carbon dioxide levels: A fungal endophyte and grass. Environ. Entomol. 25, 618–623 105 Marks, S. et al. (1991) Effects of fungal endophytes on interspecific and intraspecific competition in the grasses Festuca arundinacea and Lolium perenne. J. Appl. Ecol. 28, 194–204 106 Mathias, J.K. et al. (1990) Association of an endophytic fungus in perennial ryegrass and resistance to the hairy chinch bug (Hemiptera, Lygaeidae). J. Econ. Entomol. 83, 1640–1646 107 Matthews, J.W. and Clay, K. (2001) Influence of fungal endophyte infection on plant-soil feedback and community interactions. Ecology 82, 500–509 108 McCormick, M.K. et al. (2001) Danthonia spicata (Poaceae) and Atkinsonella hypoxylon (Balansiae): environmental dependence of a symbiosis. Am. J. Bot. 88, 903–909 109 McLeod, A.R. et al. (2001) Effects of elevated ultraviolet radiation and endophytic fungi on plant growth and insect feeding in Lolium perenne, Festuca rubra, F. arundinacea and F. pratensis. J. Photochem. Photobiol. B: Biology 62, 97–107 110 Meijer, G. and Leuchtmann, A. (2000) The effects of genetic and environmental factors on disease expression (stroma formation) and plant growth in Brachypodium sylvaticum infected by Epichloë sylvatica. Oikos 91, 446–458 111 Meister, B. (2003) Symbiosis between fungal endophytes and grasses: effects of endophytic fungi on the life history of plants and herbivores. Master’s Thesis. pp.1–92 112 Miles, C.O. et al. (1998) Endophytic fungi in indigenous Australasian grasses associated with toxicity to livestock. Appl. Environ. Microbiol. 64, 601–606 113 Muegge, M.A. et al. (1991) Influence of Acremonium infection and pesticide use on seasonal abundance of leafhoppers and froghoppers (Homoptera, Cicadellidae, Cercopidae) in tall fescue. Environ. Entomol. 20, 1531–1536 114 Murphy, J.A. et al. (1993) Endophyte-enhanced resistance to billbug (Coleoptera, Curculionidae), sod webworm (Lepidoptera, Pyralidae), and white grub (Coleoptera, Scarabeidae) in tall fescue. Environ. Entomol. 22, 699–703 115 Nan, Z.B. and Li, C.J. Neotyphodium in native grassesin china and observations on endophyte/host interactions in china and observations on endophyte/host interactions. In Proc. 4th Int. Neotyphodium/Grass Interactions Symposium (Paul, V.H. and Dapprich, P.D., eds), pp. 41–50 116 Oliver, J.W. et al. (2000) Alterations in hemograms and serum biochemical analytes of steers after prolonged consumption of endophyte-infected tall fescue. J. Anim. Sci. 78, 1029–1035 117 Osborn, T.G. et al. (1992) Effect of consuming fungus-infected and fungus-free tall fescue and ergotamine tartrate on selected physiological variables of cattle in environmentally controlled conditions. J. Anim. Sci. 70, 2501–2509 118 Overman, A.R. and Wilkinson, S.R. (1993) Modeling tall fescue cultivar response to applied nitrogen. Agron. J. 85, 1156– 1158 119 Pan, J.J. and Clay, K. (2002) Infection by the systemic fungus Epichloë glyceriae and clonal growth of its host grass Glyceria striata. Oikos 98, 37–46 120 Pan, J.J. and Clay, K. (2003) Infection by the systemic fungus Epichloë glyceriae alters clonal growth of its grass host, Glyceria striata. Proc. R. Soc. London B 270, 1585–1591 121 Pavao-Zuckerman, M.A. et al. (1999) Methane emissions of beef cattle grazing tall fescue pastures at three levels of endophyte infestation. J. Environ. Qual. 28, 1963–1969 122 Pedersen, J.F. et al. (1988) Ryegrass cultivars and endophyte in tall fescue affect nematodes in grass and succeeding soybean. Agron. J. 80, 811–814 123 Pennell, C. and Ball, O.J. (1999) The effects of Neotyphodium endophytes in tall fescue on pasture mealy bug (Balanococcus poae). Proc. 52nd N. Z. Plant Prot. Conf. 259–263 124 Pennell, C.G.L. et al. (2005) Occurrence and impact of pasture mealybug (Balanococcus poae) and root aphid (Aploneura lentisci) on ryegrass (Lolium spp.) with and without infection by Neotyphodium fungal endophytes. N. Z. J. Agric. Res. 48, 329–337 125 Popay, A.J. (2004) Response of black beetle (Heteronychus arator), porina (Wiseana cervinata) and grass grub (Costelytra zealandica) to different endophytes in tall fescue. Proc. 8th Australas. Grassl. Invert. Ecol. Conf. 157–163 126 Popay, A.J. and Wyatt, R.T. (1995) Resistance to argentine stem weevil in perennial ryegrass infected with endophytes producing different alkaloids. Proc. 48th N. Z. Plant Protect. Conf. 229–236 127 Popay, A.J. et al. (1995) Field resistance to argentine stem weevil (Listronotus bonariensis) in different ryegrass cultivars infected with an endophyte deficient in lolitrem B. N. Z. J. Agric. Res. 38, 519–528 128 Popay, A.J. et al. (2001) Insect resistance in perennial ryegrass infected with toxin-free Neotyphodium endophytes. In Proc. 4th Int. Neotyphodium/Grass Interactions Symposium (Paul, V.H. and Dapprich, P.D., eds), pp. 187–194 129 Popay, A.J. et al. (2003) The effect of endophyte (Neotyphodium uncinatum) in meadow fescue on grass grub larvae. N. Z. Plant Protect. 56, 123–128 130 Popay, A.J. et al. (2003) Interactions between endophyte (Neotyphodium spp.) and ploidy in hybrid and perennial ryegrass cultivars and their effects on Argentine stem weevil (Listronotus bonariensis). N. Z. J. Agric. Res. 46, 311–319 131 Potter, D.A. et al. (1992) Influence of turfgrass species and tall fescue endophyte on feeding ecology of Japanese beetle and southern masked chafer grubs (Coleoptera, Scarabaeidae). J. Econ. Entomol. 85, 900–909 132 Prestidge, R.A. and Gallagher, R.T. (1988) Endophyte fungus confers resistance to ryegrass – Argentine stem weevil larval studies. Ecol. Entomol. 13, 429–435 133 Quigley, P.E. (1999) Effects of Neotyphodium lolii infection and sowing rate of perennial ryegrass (Lolium perenne) on the dynamics of ryegrass/subterranean clover (Trifolium subterraneum) swards. Aust. J. Agric. Res. 51, 47–56 134 Ravel, C. et al. (1997) Beneficial effects of Neotyphodium lolii on the growth and the water status in perennial ryegrass cultivated under nitrogen deficiency or drought stress. Agronomie 17, 173–181 135 Raymond, B.D.H. and Lewis, G.C. (1995) Evaluation of endophyte infection of Lolium perenne on molluscan herbivory. Ann. Appl. Biol. S126, 104–105. 136 Read, J.C. and Camp, B.J. (1986) The effect of the fungal endophyte Acremonium coenophialum in tall fescue on animal performance, toxicity, and stand maintenance. Agron. J. 78, 848–850 137 Rice, J.S. et al. (1990) Seed production in tall fescue as affected by fungal endophyte. Crop Sci. 30, 1303–1305 138 Rice, J.S. et al. (1994) Alteration of phenotypic variances by the endophyte of tall fescue. Crop Sci. 34, 1487–1489 139 Richardson, M.D. et al. (1999) Nitrogen-form and endophyte-infection effects on growth, nitrogen uptake, and alkaloid content of chewings fescue turfgrass. J. Plant Nutr. 22, 67–79 140 Richmond, D.S. and Shetlar, D.J. (1999) Larval survival and movement of bluegrass webworm in mixed stands of endophytic perennial ryegrass and Kentucky bluegrass. J. Econ. Entomol. 92, 1329–1334 141 Richmond, D.S. and Shetlar, D.J. (2000) Hairy chinch bug (Hemiptera : Lygaeidae) damage, population density, and movement in relation to the incidence of perennial ryegrass infected by Neotyphodium endophytes. J. Econ. Entomol. 93, 1167–1172 142 Richmond, D.S. et al. (2003) Influence of Japanese beetle Popillia japonica larvae and fungal endophytes on competition between turfgrasses and dandelion. Crop Sci. 44, 600–606 143 Rowan, D.D. and Gaynor, D.L. (1986) Isolation of feeding deterrents against Argentine stem weevil from ryegrass infected with the endophyte Acremonium-loliae. J. Chem. Ecol. 12, 647–658 144 Saha, D.C. et al. (1987) Occurrence and significance of endophytic fungi in the fine fescues. Plant Dis. 71, 1021–1024 145 Saikkonen, K. et al. (1999) Endophyte-grass-herbivore interactions: the case of Neotyphodium endophytes in Arizona fescue populations. Oecologia 121, 411–420 146 Shelby, R.A. and Dalrymple, L.W. (1993) Long-term changes of endophyte infection in tall fescue stands. Grass Forage Sci. 48, 356–361 147 Siegel, M.R. et al. (1985) Acremonium fungal endophytes of tall fescue and perennial ryegrass – significance and control. Plant Dis. 69, 179–183 148 Siegel, M.R. et al. (1990) Fungal endophyte-infected grasses – alkaloid accumulation and aphid response. J. Chem. Ecol. 16, 3301–3315 149 Spyreas, G. et al. (2001) Effects of endophyte infection in tall fescue (Festuca arundinacea: Poaceae) on community diversity. Int. J. Plant Sci. 162, 1237–1245 150 Stewart, T.M. et al. (1993) Development of Meloidogyne naasi on endophyte-infected and endophyte-free perennial ryegrass. Australasian Plant Pathology 22, 40 151 Stovall, M.E. and Clay, K. (1988) The effect of the fungus, Balansia cyperi Edg, on growth and reproduction of purple nutsedge, Cyperus rotundus L. New Phytol. 109, 351–359 152 Sutherland, B.L. et al. (1999) Allelopathic effects of endophyte-infected perennial ryegrass extracts on white clover seedlings. N.Z.J. Agric. Res. 42, 19–26 153 Tibbets, T.M. and Faeth, S.H. (1999) Neotyphodium endophytes in grasses: deterrents or promoters of herbivory by leafcutting ants? Oecologia 118, 297–305 154 Timper, P. and Bouton, J. (2004) Effect of endophyte status and tall fescue cultivar on reproduction of lesion and stubby-root nematodes. In Proc. 5th Int. Symposium Neotyphodium/Grass Interactions (Kallenbach, R. et al., eds), #406 155 Trevathan, L.E. (1996) Performance of endophyte-free and endophyte-infected tall fescue seedlings in soil infested with Cochliobolus sativus. Can. J. Plant Pathol. 18, 415–418 156 Vaylay, R. and van Santen, E. (1999) Grazing induces a patterned selection response in tall fescue. Crop Sci. 39, 44–51 157 Vicari, M. et al. (2002) Combined effect of foliar and mycorrhizal endophytes on an insect herbivore. Ecology 83, 2452–2464 158 Walston, A.T. et al. (2001) Absence of interaction between endophytic perennial ryegrass and susceptibility of Japanese beetle (Coleoptera: Scarabaeidae) grubs to Paenibacillus popilliae Dutky. J. Entomol. Sci. 36, 105–108 159 Watson, R.N. et al. (1995) Plant-parasitic nematodes associated with perennial ryegrass and tall fescue with and without Acremonium endophyte. Proc. 48th N. Z. Plant Protect. Conf. 199–203 160 West, C.P. et al. (1988) The effect of Acremonium coenophialum on the growth and nematode infestation of tall fescue. Plant Soil 112, 3–6 161 White, R.H. et al. (1992) Acremonium endophyte effects on tall fescue drought tolerance. Crop Sci. 32, 1392–1396 162 Williamson, R.C. and Potter, D.A. (1997) Turfgrass species and endophyte effects on survival, development, and feeding preference of black cutworms (Lepidoptera: Noctuidae). J. Econ. Entomol. 90, 1290–1299 163 Wilson, A.D. et al. (1991) Survey and detection of endophytic fungi in Lolium germ plasm by direct staining and aphid assays. Plant Dis. 75, 169–173 164 Yue, Q. et al. (2000) Alkaloid production and chinch bug resistance in endophyte-inoculated chewings and strong creeping red fescues. J. Chem. Ecol. 26, 279–292