Fungal Diversity

, Volume 41, Issue 1, pp 101–113 | Cite as

Defensive mutualism between plants and endophytic fungi?

  • Kari SaikkonenEmail author
  • S. Saari
  • M. Helander


Endophyte-grass symbiosis is generally considered to be a classic example of microbe-plant symbiosis in which the fitness of the microbial symbiont and its host plant is closely linked, and thus, presumed to align the interests of partners toward mutually beneficial cooperation. Accumulating evidence seems to suggest that defensive mutualism provides the best framework for understanding plant-endophyte interactions in general. We conducted a meta-analysis of 99 published studies on 36 plant (inc. both grass and tree species), 62 herbivore and 17 predator or parasitoid taxons to test the importance of defensive mutualism in multitrophic interactions. In general, statistical perusal revealed that we still know little about these seemingly well-studied biological interactions. The conceptual framework for endophyte-grass interactions has largely been based on endophyte-plant-herbivore studies of two, economically important, artificially selected and introduced agricultural grass species, tall fescue and perennial ryegrass, and two generalist invertebrate pests. Only 10 original publications provided data of higher trophic levels. Consistent with the defensive mutualism hypothesis, the meta-analysis indicates that endophytes slightly increase grass resistance to herbivores, and the defensive mutualism appears to be most commonly detected in systemic and vertically transmitted grass endophytes compared to horizontally transmitted tree endophytes. However, variation appears to increase when higher trophic levels are considered. In addition to taxonomical bias, the literature is strongly biased toward short-term laboratory and greenhouse experiments rather than field conditions. Thus, current literature is insufficient to capture the breadth of variability inherent in the wild grass-endophyte populations and communities, and the general importance of defensive mutualism remains to be solved in future studies.


Defensive mutualism Endophytes Grass tree Vertical transmission Horizontal transmission Neotyphodium Epichloë Meta-analysis Publication bias 



This study was funded by the Academy of Finland (Project no. 110658).


  1. Ahlholm J, Helander M, Elamo P, Saloniemi I, Neuvonen S, Hanhimäki S, Saikkonen K (2002a) Micro-fungi and invertebrate herbivores on birch trees: fungal mediated plant-herbivore interactions or responses to host quality? Ecol Lett 5:648–655Google Scholar
  2. Ahlholm JU, Helander M, Lehtimaki S, Wäli P, Saikkonen K (2002b) Vertically transmitted fungal endophytes: different responses of host-parasite systems to environmental conditions. Oikos 99:173–183Google Scholar
  3. Ahmad S, Govindarajan S, Funk CR, Johnson-Cicalese JM (1985) Fatality of house crickets on perennial ryegrasses infected with a fungal endophyte. Entomol Exp Appl 39:183–190Google Scholar
  4. Ahmad S, Johnson-Cicalese JM, Dickson WK, Funk CR (1986) Endophyte-enhanced resistance in perennial ryegrass to the bluegrass billbug, Sphenophorus parvulus. Entomol Exp Appl 41:3–10Google Scholar
  5. Arnold AE (2007) Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers. Fungal Biol Rev 21:51–66Google Scholar
  6. Arnold AE, Maynard Z, Gilbert GS, Coley PD, Kursar TA (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3:267–274Google Scholar
  7. Arnold AE, Mejia LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci USA 100:15649–15654PubMedGoogle Scholar
  8. Bacon CW, Porter JK, Robbins JD, Luttrell ES (1977) Epichloë typhina from toxic tall fescue grasses. Appl Environ Microbiol 34:576–581PubMedGoogle Scholar
  9. Ball OJ-P, Bernard EC, Gwinn KD (1997) Effect of selected Neotyphodium lolii isolates on root-knot nematode (Meloidogyne marylandi) numbers in perennial ryegrass. Proceedings of the 50th New Zealand Plant Protection Conference 50: 65–68Google Scholar
  10. Barger JL, Tannenbaum MG (1998) Consumption of endophyte-infected fescue seeds and osmoregulation in white-footed mice. Journal of Mammal 79:464–474Google Scholar
  11. Barker GM (2008) Mollusc herbivory influenced by endophytic clavicipitaceous fungal infections in grasses. Ann Appl Biol 153:381–393Google Scholar
  12. Bazely DR, Vicari M, Emmerich S, Filip L, Lin D, Inman A (1997) Interactions between herbivores and endophyte-infected Festuca rubra from the Scottish islands of St. Kilda, Benbecula and Rum. J Appl Ecol 34:847–860Google Scholar
  13. Berryman AA (2002) Population: a central concept for ecology? Oikos 97:439–442Google Scholar
  14. Bluett SJ, Thom ER, Clark DA, Waugh CD (2005) Effects of a novel ryegrass endophyte on pasture production, dairy cow milk production and calf liveweight gain. Aust J Exp Agric 45:11–19Google Scholar
  15. Boning RA, Bultman TL (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 136:328–335Google Scholar
  16. Bourassa S, Brodeur J, Carriere Y (2007) Endophyte-grass complexes and the relationship between feeding preference and performance in a grass herbivore. Entomol Exp Appl 124:221–228Google Scholar
  17. Braman SK, Duncan RR, Engelke MC, Hanna WW, Hignight K, Rush D (2002) Grass species and endophyte effects on survival and development of fall armyworm (Lepidoptera: Noctuidae). J Econ Entomol 95:487–492PubMedGoogle Scholar
  18. Breen JP (1993a) Enhanced resistance to fall armyworm (Lepidoptera, Noctudiae) in Acremonium endophyte-infected turfgrasses. J Econ Entomol 86:621–629Google Scholar
  19. Breen JP (1993b) Enhanced resistance to 3 species of aphids (Homoptera, Aphididae) in Acremonium endophyte-infected turfgrasses. J Econ Entomol 86:1279–1286Google Scholar
  20. Brem D, Leuchtmann A (2001) Epichloë grass endophytes increase herbivore resistance in the woodland grass Brachypodium sylvaticum. Oecologia 126:522–530Google Scholar
  21. Bultman TL, Bell GD (2003) Interaction between fungal endophytes and environmental stressors influences plant resistance to insects. Oikos 103:182–190Google Scholar
  22. Bultman TL, Conard NJ (1998) Effects of endophytic fungus, nutrient level, and plant damage on performance of fall armyworm (Lepidoptera: Noctuidae). Environ Entomol 27:631–635Google Scholar
  23. Bultman TL, Ganey DT (1995) Induced resistance to fall armyworm (Lepidoptera, Noctuidae) mediated by a fungal endophyte. Environ Entomol 24:1196–1200Google Scholar
  24. Bultman TL, McNeill MR, Goldson SL (2003) Isolate-dependent impacts of fungal endophytes in a multitrophic interaction. Oikos 102:491–496Google Scholar
  25. Bultman TL, Pulas C, Grant L, Bell G, Sullivan TJ (2006) Effects of fungal endophyte isolate on performance and preference of bird cherry-oat aphid. Environ Entomol 35:1690–1695Google Scholar
  26. Bultman TL, Rodstrom JL, Radabaugh KR, VanDop JD, Librizzi JM, Longwell LL, Pulas C, Grant L, Sullivan TJ (2009) Influence of genetic variation in the fungal endophyte of a grass on an herbivore and its parasitoid. Entomol Exp Appl 130:173–180Google Scholar
  27. Butin H (1992) Effect of endophytic fungi from oak (Quercus robur L.) on mortality of leaf inhabiting gall insects. Eur J For Pathol 22:237–246Google Scholar
  28. Calhoun LA, Findlay JA, Miller JD, Whitney NJ (1992) Metabolites toxic to spruce budworm from balsam fir needle endophytes. Mycol Res 96:281–286Google Scholar
  29. Carriere Y, Bouchard A, Bourassa S, Brodeur J (1998) Effect of endophyte incidence in perennial ryegrass on distribution, host-choice, and performance of the hairy chinch bug (Hemiptera: Lygaeidae). J Econ Entomol 91:324–328Google Scholar
  30. Carroll G (1988) Fungal endophytes in stems and leaves - from latent pathogen to mutualistic symbiont. Ecology 69:2–9Google Scholar
  31. Carroll GC (1991) Beyond pest deterrence. Alternative strategies and hidden costs of endophytic mutualisms in vascular plants. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Springer, New York, pp 358–375Google Scholar
  32. Cheplick GP, Clay K (1988) Acquired chemical defenses in grasses - the role of fungal endophytes. Oikos 52:309–318Google Scholar
  33. Cheplick GP, Faeth S (2009) Ecology and evolution of the grass-endophyte symbiosis. Oxford University Press, New YorkGoogle Scholar
  34. Clark CL, Miller JD, Whitney NJ (1989) Toxicity of conifer needle endophytes to spruce budworm. Mycol Res 93:508–512Google Scholar
  35. Clark DA, Thom ER, Waugh CD (1996) Milk production and pasture silage with different levels of endophyte infection. Proc N Z Soc Anim Prod 56:292–296Google Scholar
  36. Clay K (1984) The effect of the fungus Atkinsonella hypoxylon (Clavicipitaceae) on the reproductive-system and demography of the grass Danthonia spicata. New Phytol 98:165–175Google Scholar
  37. Clay K (1988a) Clavicipitaceous fungal endophytes of grasses: coevolution and the change from parasitism to mutualism. In: Pirozynski K, Hawksworth DL (eds), Co-evolution of fungi with plants and animals. Academic Press, pp 79–105Google Scholar
  38. Clay K (1988b) Fungal endophytes of grasses - a defensive mutualism between plants and fungi. Ecology 69:10–16Google Scholar
  39. Clay K (2009) Defensive mutualism and grass endophytes: still valid after all these years? In: Torres M, White JF Jr (eds) Defensive mutualism in symbiotic association. Taylor and Francis Publications, pp 9–20Google Scholar
  40. Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:99–127Google Scholar
  41. Clay K, Hardy TN, Hammond AM (1985a) Fungal endophytes of grasses and their effects on an insect herbivore. Oecologia 66:1–5Google Scholar
  42. Clay K, Hardy TN, Hammond AM (1985b) Fungal endophytes of Cyperus and their effect on an insect herbivore. Am J Bot 72:1284–1289Google Scholar
  43. Clay K, Cheplick GP, Marks S (1989) Impact of the fungus Balansia henningsiana on Panicum agrostoides - frequency of infection, plant-growth and reproduction, and resistance to pests. Oecologia 80:374–380Google Scholar
  44. Clay K, Marks S, Cheplick GP (1993) Effects of insect herbivory and fungal endophyte infection on competitive interactions among grasses. Ecology 74:1767–1777Google Scholar
  45. Clement SL (1991) Field evaluation of wild barley accessions against Russian wheat aphid. Arthropod Management Tests 24:409Google Scholar
  46. Clement SL, Lester DG, Wilson AD, Pike KS (1992) Behavior and performance of Diuraphis noxia (Homoptera: Aphididae) on fungal endophyte-infected and uninfected perennial ryegrass. J Econ Entomol 85:583–588Google Scholar
  47. Clement SL, Lester DG, Wilson AD, Johnson RC, Bouton JH (1996) Expression of russian wheat aphid (Homoptera: Aphididae) resistance in genotypes of tall fescue harboring different isolates of Acremonium endophyte. J Econ Entomol 89:766–770Google Scholar
  48. Clement SL, Wilson AD, Lester DG, Davitt CM (1997) Fungal endophytes of wild barley and their effects on Diuraphis noxia population development. Entomol Exp Appl 82:275–281Google Scholar
  49. Clement SL, Elberson LR, Youssef NN, Davitt CM, Doss RP (2001) Incidence and diversity of Neotyphodium fungal endophytes in tall fescue from Morocco, Tunisia, and Sardinia. Crop Sci 41:570–576Google Scholar
  50. Clement SL, Elberson LR, Bosque-Perez NA, Schotzko DJ (2005) Detrimental and neutral effects of wild barley - Neotyphodium fungal endophyte associations on insect survival. Entomol Exp Appl 114:119–125Google Scholar
  51. Conover MR (1998) Impact of consuming tall fescue leaves with the endophytic fungus, Acremonium coenophialum, on meadow voles. J Mammal 79:457–463Google Scholar
  52. Conover MR (2003) Impact of the consumption of endophyte-infected perennial ryegrass by meadow voles. Agric Ecosyst Environ 97:199–203Google Scholar
  53. Conover MR, Messmer TA (1996a) Feeding preferences and changes in mass of Canada geese grazing endophyte-infected tall fescue. Condor 98:859–862Google Scholar
  54. Conover MR, Messmer TA (1996b) Consequences for captive zebra finches of consuming tall fescue seeds infected with the endophytic fungus Acremonium coenophialum. Auk 113:492–495Google Scholar
  55. Cook R, Lewis GC, Mizen KA (1991) Effects on plant-parasitic nematodes of infection of perennial ryegrass, Lolium perenne, by the endophytic fungus, Acremonium lolii. Crop Prot 10:403–407Google Scholar
  56. Crutchfield BA, Potter DA (1994) Preferences of Japanese beetle and southern masked chafer (Coleoptera, Scarabaeidae) grubs among cool-season turfgrasses. J Entomol Sci 29:398–406Google Scholar
  57. Davidson AW, Potter DA (1995) Response of plant-feeding, predatory, and soil-inhabiting invertebrates to Acremonium endophyte and nitrogen-fertilization in tall fescue turf. J Econ Entomol 88:367–379Google Scholar
  58. de Sassi C, Müller CB, Krauss J (2006) Fungal plant endosymbionts alter life history and reproductive success of aphid predators. Proc R Soc B 273:1301–1306PubMedGoogle Scholar
  59. Durham WF, Tannenbaum MG (1998) Effects of endophyte consumption on food intake, growth, and reproduction in prairie voles. Can J Zool 76:960–969Google Scholar
  60. Eerens JPJ, Miller KB, White JGH, Easton HS, Lucas RJ (1994) Ryegrass endophyte and sheep production. Proc N Z Grassl Assoc 56:255–258Google Scholar
  61. Eerens JPJ, Lucas RJ, Easton HS, White JGH (1998a) Influence of the ryegrass endophyte (Neotyphodium lolii) in a cool-moist environment II. Sheep production. N Z J Agric Res 41:191–199Google Scholar
  62. Eerens JPJ, Visker MHPW, Lucas RJ, Easton HS, White JGH (1998b) Influence of the ryegrass endophyte (Neotyphodium lolii) in a cool-moist environment IV. Plant parasitic nematodes. N Z J Agric Res 41:209–217Google Scholar
  63. Eichenseer H, Dahlman DL (1992) Antibiotic and deterrent qualities of endophyte-infected tall fescue to 2 aphid species (Homoptera, Aphidiae). Environ Entomol 21:1046–1051. 57Google Scholar
  64. Eichenseer H, Dahlman DL (1993) Survival and development of the true armyworm Pseudaletia unipunctata (Haworth) (Lepidoptera: Noctuidae), on endophyte-infected and endophyte-free tall fescue. J Entomol Sci 28:462–467Google Scholar
  65. Eichenseer H, Dahlman DL, Bush LP (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 60:29–38Google Scholar
  66. Elmi AA, West CP, Robbins RT, Kirkpatrick TL (2000) Endophyte effects on reproduction of a root-knot nematode (Meloidogyne marylandi) and osmotic adjustment in tall fescue. Grass Forage Sci 55:166–172Google Scholar
  67. Ewald PW (1987) Transmission modes and evolution of the parasitism-mutualism continuum. Ann N Y Acad Sci 503:295–306PubMedGoogle Scholar
  68. Faeth SH (2002) Are endophytic fungi defensive plant mutualists? Oikos 99:200–200Google Scholar
  69. Faeth SH (2009) Asexual fungal symbionts alter reproductive allocation and herbivory over time in their native perennial grass hosts. Am Nat 173:554–565PubMedGoogle Scholar
  70. Faeth SH, Hammon KE (1996) Fungal endophytes and phytochemistry of oak foliage: determinants of oviposition preference of leafminers? Oecologia 108:728–736Google Scholar
  71. Faeth SH, Hammon KE (1997a) Fungal endophytes in oak trees: long-term patterns of abundance and associations with leafminers. Ecology 78:810–819CrossRefGoogle Scholar
  72. Faeth SH, Hammon KE (1997b) Fungal endophytes in oak trees: experimental analyses of interactions with leafminers. Ecology 78:820–827Google Scholar
  73. Filipov NM, Thompson FN, Hill NS, Dawe DL, Stuedemann JA, Price JC, Smith CK (1998) Vaccination against ergot alkaloids and the effect of endophyte-infected fescue seed-based diets on rabbits. J Anim Sci 76:2456–2463PubMedGoogle Scholar
  74. Findlay JA, Buthelezi S, Lavoie R, Peña-Rodriguez L, Miller JD (1995a) Bioactive isocoumarins and related metabolites from conifer endophytes. J Nat Prod 58:1759–1766PubMedGoogle Scholar
  75. Findlay JA, Li GQ, Penner PE, Miller JD (1995b) Novel diterpenoid insect toxins from a conifer endophyte. J Nat Prod 58:197–200Google Scholar
  76. Findlay JA, Buthelezi S, Li GQ, Seveck M, Miller JD (1997a) Insect toxins from an endophytic fungus from wintergreen. J Nat Prod 60:1214–1215Google Scholar
  77. Findlay JA, Li GQ, Johnson JA (1997b) Bioactive compounds from an endophytic fungus from eastern larch (Larix laricina) needles. Can J Chem 75:716–719Google Scholar
  78. Findlay JA, Li GQ, Miller JD, Womiloju TO (2003) Insect toxins from spruce endophytes. Can J Chem 81:284–292Google Scholar
  79. Fine FEM (1975) Vectors and vertical transmission: an epidemiological perspective. Ann N Y Acad Sci 266:173–194PubMedGoogle Scholar
  80. Finkes LK, Cady AB, Mulroy JC, Clay K, Rudgers JA (2006) Plant-fungus mutualism affects spider composition in successional fields. Ecol Lett 9:344–353Google Scholar
  81. Fisher DS, Burns JC (2008) Testing for variation in animal preference for “Jesup” tall fescue hays with wild-type, novel, or no fungal endophyte. Crop Sci 48:2026–2032Google Scholar
  82. Ford VL, Kirkpatrik TL (1989) Effects of Acremonium coenophialum in tall fescue on host disease and insect resistance and allelopathy to Pinus taeda seedlings. Ark Exp Stat Spec Rep 140:29–34Google Scholar
  83. Fortier GM, Bard N, Jansen M, Clay K (2000) Effects of tall fescue endophyte infection and population density on growth and reproduction in prairie voles. J Wildl Manage 64:122–128Google Scholar
  84. Fortier GM, Osmon MA, Roach M, Clay K (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 146:63–71Google Scholar
  85. Gaylord ES, Preszler RW, Boecklen WJ (1996) Interactions between host plants, endophytic fungi, and a phytophagous insect in an oak (Quercus grisea x Q. gambelii) hybrid zone. Oecologia 105:336–342Google Scholar
  86. Gaynor DL, Hunt WF (1983) The relationship between nitrogen supply, endophytic fungus, and argentine stem weevil resistance in ryegrass. Proc N Z Grassl Assoc 44:257–263Google Scholar
  87. Gurevitch J, Hedges LV (1999) Statistical issues in ecological meta-analyses. Ecology 80:1142–1149CrossRefGoogle Scholar
  88. Gwinn KD, Gavin AM (1992) Relationship between endophyte infestation level of tall fescue seed lots and Rhizoctonia zeae seedling disease. Plant Dis 76:911–914Google Scholar
  89. Hardy TN, Clay K, Hammond AM (1985) Fall armyworm (Lepidoptera, Noctuidae) - a laboratory bioassay and larval preference study for the fungal endophyte of perennial ryegrass. J Econ Entomol 78:571–575Google Scholar
  90. Hardy TN, Clay K, Hammond AM (1986) Leaf age and related factors affecting endophyte-mediated resistance to fall armyworm (Lepidoptera, Noctuidae) in tall fescue. Environ Entomol 15:1083–1089Google Scholar
  91. Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu Rev Entomol 54:323–342PubMedGoogle Scholar
  92. Härri SA, Krauss J, Müller CB (2008a) Natural enemies act faster than endophytic fungi in population control of cereal aphids. J Anim Ecol 77:605–611PubMedGoogle Scholar
  93. Härri SA, Krauss J, Müller CB (2008b) Trophic cascades initiated by fungal plant endosymbionts impair reproductive performance of parasitoids in the second generation. Oecologia 157:399–407PubMedGoogle Scholar
  94. Härri SA, Krauss J, Müller CB (2008c) Fungal endosymbionts of plants reduce lifespan of an aphid secondary parasitoid and influence host selection. Proc R Soc Lond B 275:2627–2632Google Scholar
  95. Härri SA, Krauss J, Müller CB (2009) Extended larval development time for aphid parasitoids in the presence of plant endosymbionts. Ecol Entomol 34:20–25Google Scholar
  96. Hol WHG, de la Pena E, Moens M, Cook R (2007) Interaction between a fungal endophyte and root herbivores of Ammophila arenaria. Basic Appl Ecol 8:500–509Google Scholar
  97. Holdenrieder O, Pautasso M, Weisberg PJ, Lonsdale D (2004) Tree diseases and landscape processes: the challenge of landscape pathology. Trends Ecol Evol 19:446–452PubMedGoogle Scholar
  98. Hoveland CS, Haaland RL, King CC, Anthony WB, Clark EM, McGuire JA, Smith LA, Grimes HW, Holliman JL (1980) Association of Epichloë typhina fungus and steer performance on tall fescue pasture. Agron J 72:1064–1065CrossRefGoogle Scholar
  99. Hoveland CS, Schmidt SP, King CC, Odom JW, Clark EM, McGuire JA, Smith LA, Grimes HW, Holliman JL (1983) Steer performance and association of Acremonium coenophialum fungal endophyte on tall fescue pasture. Agron J 75:821–824CrossRefGoogle Scholar
  100. Huitu O, Helander M, Lehtonen P, Saikkonen K (2008) Consumption of grass endophytes alters the ultraviolet spectrum of vole urine. Oecologia 156:333–340PubMedGoogle Scholar
  101. Humphries SS, Gwinn KD, Stewart AJ (2001) Effects of endophyte status of tall fescue tissues on the earthworm (Eisenia fetida). Environ Toxicol Chem 20:1346–1350PubMedGoogle Scholar
  102. Hunt MG, Newman JA (2005) Reduced herbivore resistance from a novel grass-endophyte association. J Appl Ecol 42:762–769Google Scholar
  103. Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 33:163–173Google Scholar
  104. Jackson JA, Harmon RJ, Tabeidi Z (1997) Effect of dietary supplementation with vitamin E for lactating dairy cows fed tall fescue hay infected with endophyte. J Dairy Sci 80:569–572PubMedCrossRefGoogle Scholar
  105. Jallow MFA, Dugassa-Gobena D, Vidal S (2008) Influence of an endophytic fungus on host plant selection by a polyphagous moth via volatile spectrum changes. Arthropod-Plant Interact 2:53–62Google Scholar
  106. Johnson JA, Whitney NJ (1994) Cytotoxicity and insecticidal activity of endophytic fungi from black spruce (Picea mariana) needles. Can J Microbiol 40:24–27CrossRefGoogle Scholar
  107. Johnson MC, Dahlman DL, Siegel MR, Bush LP, Latch GCM, Potter DA, Varney DR (1985) Insect feeding deterrents in endophyte-infected tall fescue. Appl Environ Microbiol 49:568–571PubMedGoogle Scholar
  108. Johnson-Cicalese JM, White RH (1990) Effect of Acremonium endophytes on 4 species of billbug found on New Jersey turfgrasses. J Am Soc Hortic Sci 115:602–604Google Scholar
  109. Kimmons CA, Gwinn KD, Bernard EC (1990) Nematode reproduction on endophyte-infected and endophyte-free tall fescue. Plant Dis 74:757–761Google Scholar
  110. Kindler SD, Breen JP, Springer TL (1991) Reproduction and damage by Russian wheat aphid (Homoptera, Aphididae) as influenced by fungal endophytes and cool-season turfgrasses. J Econ Entomol 84:685–692Google Scholar
  111. Knoch TR, Faeth SH, Arnott DL (1993) Endophytic fungi alter foraging and dispersal by desert seed-harvesting ants. Oecologia 95:470–473Google Scholar
  112. Koga H, Hirai Y, Kanda K, Tsukiboshi T, Uematsu T (1997) Successive transmission of resistance to bluegrass webworm to perennial ryegrass and tall fescue plants by artificial inoculation with Acremonium endophytes. Jpn Agric Res Q 31:109–115Google Scholar
  113. Koppenhöfer AM, Cowles RS, Fuzy EM (2003) Effects of turfgrass endophytes (Clavicipitaceae: Ascomycetes) on white grub (Coleoptera: Scarabaeidae) larval development and field populations. Environ Entomol 32:895–906Google Scholar
  114. Koricheva J (2002) Meta-analysis of sources of variation in fitness costs of plant antiherbivore defenses. Ecology 83:176–190CrossRefGoogle Scholar
  115. Kover PX, Clay K (1998) Trade-off between virulence and vertical transmission and the maintenance of a virulent plant pathogen. Am Nat 152:165–175PubMedGoogle Scholar
  116. Krauss J, Härri SA, Bush L, Husi R, Bigler L, Power SA, Müller CB (2007) Effects of fertilizer, fungal endophytes and plant cultivar on the performance of insect herbivores and their natural enemies. Funct Ecol 21:107–116Google Scholar
  117. Kucht S, Gross J, Hussein Y, Grothe T, Keller U, Basar S, Konig WA, Steiner U, Leistner E (2004) Elimination of ergoline alkaloids following treatment of Ipomoea asarifolia (Convolvulaceae) with fungicides. Planta 219:619–625PubMedGoogle Scholar
  118. Kunkel BA, Grewal PS (2003) Endophyte infection in perennial ryegrass reduces the susceptibility of black cutworm to an entomopathogenic nematode. Entomol Exp Appl 107:95–104Google Scholar
  119. Kunkel BA, Grewal PS, Quigley MF (2004) A mechanism of acquired resistance against an entomopathogenic nematode by Agrotis ipsilon feeding on perennial ryegrass harboring a fungal endophyte. Biol Control 29:100–108Google Scholar
  120. Kumaresan V, Suryanarayanan TS (2001) Occurrence and distribution of endophytic fungi in a mangrove community. Mycol Res 105:1388–1391Google Scholar
  121. Kumaresan V, Suryanarayanan TS (2002) Endophyte assemblages in young, mature and senescent leaves of Rhizophora apiculata: evidence for the role of endophytes in mangrove litter degradation. Fungal Divers 9:81–91Google Scholar
  122. Lappalainen JH, Helander ML (1997) The role of foliar microfungi in mountain birch - insect herbivore relationships. Ecography 20:116–122Google Scholar
  123. Lappalainen JH, Koricheva J, Helander ML, Haukioja E (1999) Densities of endophytic fungi and performance of leafminers (Lepidoptera: Eriocraniidae) on birch along a pollution gradient. Environ Pollut 104:99–105Google Scholar
  124. Latch GCM, Christensen MJ, Gaynor DL (1985) Aphid detection of endophyte infection in tall fescue. N Z J Agric Res 28:129–132Google Scholar
  125. Lehtonen P, Helander M, Saikkonen K (2005) Are endophyte-mediated effects on herbivores conditional on soil nutrients? Oecologia 142:38–45PubMedGoogle Scholar
  126. Lewis GC, White JFJ, Bonnefont J (1993) Evaluation of grasses infected with fungal endophytes against locusts. Ann Appl Biol S122:142–143Google Scholar
  127. Lipsitch M, Nowak MA, Ebert D, May RM (1995) The population dynamics of vertically and horizontally transmitted parasites. Proc R Soc Lond Ser B 260:321–327Google Scholar
  128. Lopez JE, Faeth SH, Miller M (1995) Effect of endophytic fungi on herbivory by redlegged grasshoppers (Orthoptera: Acrididae) on Arizona fescue. Environ Entomol 24:1576–1580Google Scholar
  129. Madej CW, Clay K (1991) Avian seed preference and weight-loss experiments - the effect of fungal endophyte-infected tall fescue seeds. Oecologia 88:296–302Google Scholar
  130. Marks S, Lincoln DE (1996) Antiherbivore defense mutualism under elevated carbon dioxide levels: a fungal endophyte and grass. Environ Entomol 25:618–623Google Scholar
  131. Mathias JK, Ratcliffe RH, Hellman JL (1990) Association of an endophytic fungus in perennial ryegrass and resistance to the hairy chinch bug (Hemiptera: Lygaeidae). J Econ Entomol 83:1640–1646Google Scholar
  132. McLeod AR, Rey A, Newsham KK, Lewis GC, Wolferstan P (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 62:97–107Google Scholar
  133. Meister B, Krauss J, Härri SA, Schneider MV, Müller CB (2006) Fungal endosymbionts affect aphid population size by reduction of adult life span and fecundity. Basic Appl Ecol 7:244–252Google Scholar
  134. Miles CO, di Menna ME, Jacobs SWL, Garthwaite I, Lane GA, Prestidge RA, Marshall SL, Wilkinson HH, Schardl CL, Ball OJP, Latch GCM (1998) Endophytic fungi in indigenous Australasian grasses associated with toxicity to livestock. Appl Environ Microbiol 64:601–606PubMedGoogle Scholar
  135. Miller JD, Mackenzie S, Foto M, Adams GW, Findlay JA (2002) Needles of white spruce inoculated with rugulosin-producing endophytes contain rugulosin reducing spruce budworm growth rate. Mycol Res 106:471–479Google Scholar
  136. Muegge MA, Quisenberry SS, Bates GE, Joost RE (1991) Influence of Acremonium infection and pesticide use on seasonal abundance of leafhoppers and froghoppers (Homoptera: Cicadellidae, Cercopidae) in tall fescue. Environ Entomol 20:1531–1536Google Scholar
  137. Murali TS, Suryanarayanan TS, Venkatesan G (2007) Fungal endophyte communities in two tropical forests of southern India: diversity and host affiliation. Mycol Prog 6:191–199Google Scholar
  138. Murphy JA, Sun SC, Betts LL (1993) Endophyte-enhanced resistance to billbug (Coleoptera, Curculionidae), sod webworm (Lepidoptera, Pyralidae), and white grub (Coleoptera, Scarabeidae) in tall fescue. Environ Entomol 22:699–703Google Scholar
  139. Ohgushi T (2005) Indirect interaction webs: Herbivore-induced effects through trait change in plants. Ann Rev Ecol Evol Syst 36:81–105Google Scholar
  140. Oliver JW, Schultze AE, Rohrbach BW, Fribourg HA, Ingle T, Waller JC (2000) Alterations in hemograms and serum biochemical analytes of steers after prolonged consumption of endophyte-infected tall fescue. J Anim Sci 78:1029–1035PubMedGoogle Scholar
  141. Omacini M, Chaneton EJ, Ghersa CM, Müller CB (2001) Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 409:78–81PubMedGoogle Scholar
  142. Osborn TG, Schmidt SP, Marple DN, Rahe CH, Steenstra JR (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 70:2501–2509PubMedGoogle Scholar
  143. Panaccione DG, Cipoletti JR, Sedlock AB, Blemings KP, Schardl CL, Machado C, Seidel GE (2006) Effects of ergot alkaloids on food preference and satiety in rabbits, as assessed with gene-knockout endophytes in perennial ryegrass (Lolium perenne). J Agric Food Chem 54:4582–4587PubMedGoogle Scholar
  144. Parker IM, Gilbert GS (2004) The evolutionary ecology of novel plant-pathogen interactions. Ann Rev Ecol Evol Syst 35:675–700Google Scholar
  145. Pavao-Zuckerman MA, Waller JC, Ingle T, Fribourg HA (1999) Methane emissions of beef cattle grazing tall fescue pastures at three levels of endophyte infestation. J Environ Qual 28:1963–1969CrossRefGoogle Scholar
  146. Pedersen JF, Rodriguez-Kabana R, Shelby RA (1988) Ryegrass cultivars and endophyte in tall fescue affect nematodes in grass and succeeding soybean. Agron J 80:811–814CrossRefGoogle Scholar
  147. Pennell CGL, Popay AJ, Ball OJ-P, Hume DE, Baird DB (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 48:329–337Google Scholar
  148. Petrini O (1991) Fungal endophytes of tree laeves. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Springer, New York, pp 179–197Google Scholar
  149. Piano E, Bertoli FB, Romani M, Tava A, Riccioni L, Valvassori M, Carroni AM, Pecetti L (2005) Specificity of host-endophyte association in tall fescue populations from Sardinia, Italy. Crop Sci 45:1456–1463Google Scholar
  150. Popay AJ, Wyatt RT (1995) Resistance to Argentine stem weevil in perennial ryegrass infected with endophytes producing different alkaloids. Proceedings of the 48th New Zealand Plant Protection Conference 48: 229–236Google Scholar
  151. Popay AJ, Hume DE, Mainland RA, Saunders CJ (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 38:519–528Google Scholar
  152. Popay AJ, Townsend RJ, Fletcher LR (2003) The effect of endophyte (Neotyphodium uncinatum) in meadow fescue on grass grub larvae. N Z Plant Prot 56:123–128Google Scholar
  153. Potter DA, Patterson CG, Redmond CT (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 85:900–909Google Scholar
  154. Potter DA, Stokes JT, Redmond CT, Schardl CL, Panaccione DG (2008) Contribution of ergot alkaloids to suppression of a grass-feeding caterpillar assessed with gene knockout endophytes in perennial ryegrass. Entomol Exp Appl 126:138–147Google Scholar
  155. Prestidge RA, Gallagher RT (1988) Endophyte fungus confers resistance to ryegrass - Argentine stem weevil larval studies. Ecol Entomol 13:429–435Google Scholar
  156. Preszler RW, Gaylord ES, Boecklen WJ (1996) Reduced parasitism of a leaf-mining moth on trees with high infection frequencies of an endophytic fungus. Oecologia 108:159–166Google Scholar
  157. Ralphs MH, Creamer R, Baucom D, Gardner DR, Welsh SL, Graham JD, Hart C, Cook D, Stegelmeier BL (2008) Relationship between the endophyte Embellisia spp. and the toxic alkaloid swainsonine in major locoweed species (Astragalus and Oxytropis). J Chem Ecol 34:32–38PubMedGoogle Scholar
  158. Rasmussen S, Parsons AJ, Fraser K, Xue H, Newman JA (2008) Metabolic profiles of Lolium perenne are differentially affected by nitrogen supply, carbohydrate content, and fungal endophyte infection. Plant Physiol 146:1440–1453PubMedGoogle Scholar
  159. Raymond BH (1995) Evaluation of endophyte infection of Lolium perenne on molluscan herbivory. Ann Appl Biol S126:104–105Google Scholar
  160. Read JC, Camp BJ (1986) The effect of the fungal endophyte Acremonium coenophialum in tall fescue on animal performance, toxicity, and stand maintenance. Agron J 78:848–850CrossRefGoogle Scholar
  161. Richmond DS, Shetlar DJ (1999) Larval survival and movement of bluegrass webworm in mixed stands of endophytic perennial ryegrass and Kentucky bluegrass. J Econ Entomol 92:1329–1334Google Scholar
  162. Richmond DS, Shetlar DJ (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 93:1167–1172PubMedGoogle Scholar
  163. Richmond DS, Grewal PS, Cardina J (2004) Influence of Japanese beetle Popillia japonica larvae and fungal endophyte on competition between turfgrasses and dandelion. Crop Sci 44:600–606Google Scholar
  164. Rosenberg MS, Adams DC, Gurevitch J (2000) MetaWin: statistical software for meta-analysis. Version 2.0Google Scholar
  165. Rosenthal R (1994) Parametric measures of effect size. In: Cooper H, Hedges LV (eds) The handbook of research synthesis. Russell Sage Foundation, New York, pp 231–244Google Scholar
  166. Rowan DD, Gaynor DL (1986) Isolation of feeding deterrents against argentine stem weevil from ryegrass infected with the endophyte Acremonium loliae. J Chem Ecol 12:647–658Google Scholar
  167. Rudgers JA, Clay K (2008) An invasive plant-fungal mutualism reduces arthropod diversity. Ecol Lett 11:831–840PubMedGoogle Scholar
  168. Saari S, Lehtonen P, Helander M, Saikkonen K (2009) High variation in frequency of infection by endophytes in cultivars of meadow fescue in Finland. Grass Forage Sci 64:169–176Google Scholar
  169. Saha DC, Johnson-Cicalese JM, Halisky PM, Van Heemstra MI, Funk CR (1987) Occurrence and significance of endophytic fungi in the fine fescues. Plant Dis 71:1021–1024Google Scholar
  170. Saikkonen K (2007) Forest structure and fungal endophytes. Fungal Biol Rev 21:67–74Google Scholar
  171. Saikkonen K, Helander M, Ranta H, Neuvonen S, Virtanen T, Suomela J, Vuorinen P (1996) Endophyte-mediated interactions between woody plants and insect herbivores? Entomol Exp Appl 80:269–271Google Scholar
  172. Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343Google Scholar
  173. Saikkonen K, Helander M, Faeth SH, Schulthess F, Wilson D (1999) Endophyte-grass-herbivore interactions: the case of Neotyphodium endophytes in Arizona fescue populations. Oecologia 121:411–420Google Scholar
  174. Saikkonen K, Ion D, Gyllenberg M (2002) The persistence of vertically transmitted fungi in grass metapopulations. Proc R Soc Lond Ser B 269:1397–1403Google Scholar
  175. Saikkonen K, Helander M, Faeth SH (2004a) Fungal endophytes: hitch-hikers of the green world. In: Holmes A, Gillings M (eds) Plant microbiology. Garland Science/BIOS Scientific Publishers, Oxford, pp 77–95Google Scholar
  176. Saikkonen K, Wali P, Helander M, Faeth SH (2004b) Evolution of endophyte-plant symbioses. Trends Plant Sci 9:275–280PubMedGoogle Scholar
  177. Saikkonen K, Lehtonen P, Helander M, Koricheva J, Faeth SH (2006) Model systems in ecology: dissecting the endophyte-grass literature. Trends Plant Sci 11:428–433PubMedGoogle Scholar
  178. Salminen SO, Richmond DS, Grewal SK, Grewal PS (2005) Influence of temperature on alkaloid levels and fall armyworm performance in endophytic tall fescue and perennial ryegrass. Entomol Exp Appl 115:417–426Google Scholar
  179. Sánchez-Márquez S, Bills GF, Zabalgogeazcoa I (2007) The endophyte mycobiota of the grass Dactylis glomerata. Fungal Divers 27:171–195Google Scholar
  180. Sánchez-Márquez S, Bills GF, Zabalgogeazcoa I (2008) Diversity and structure of the fungal endophytic assemblages from two sympatric coastal grasses. Fungal Divers 33:87–100Google Scholar
  181. Sieber TN (2007) Endophytic fungi in forest trees: are they mutualists? Fungal Biol Rev 21:75–89Google Scholar
  182. Siegel MR (1990) Fungal endophyte-infected grasses - alkaloid accumulation and aphid response. J Chem Ecol 16:3301–3315Google Scholar
  183. Siegel MR, Bush LP (1997) Toxin production in grass/endophyte associations. In: Carrol GC, Tudzynski P (eds) The mycota V Part A plant relationships. Springer, Berlin, pp 185–207Google Scholar
  184. Siegel MR, Latch GCM, Johnson MC (1985) Acremonium fungal endophytes of tall fescue and perennial ryegrass - significance and control. Plant Dis 69:179–183Google Scholar
  185. Simons L, Bultman TL, Sullivan TJ (2008) Effects of methyl jasmonate and an endophytic fungus on plant resistance to insect herbivores. J Chem Ecol 34:1511–1517PubMedGoogle Scholar
  186. Strauss SY, Irwin E (2004) Ecological and evolutionary consequencies of multispecies plant-animal interactions. Ann Rev Ecol Evol Syst 35:435–466Google Scholar
  187. Sullivan TJ, Rodstrom J, Vandop J, Librizzi J, Graham C, Schardl CL, Bultman TL (2007) Symbiont-mediated changes in Lolium arundinaceum inducible defenses: evidence from changes in gene expression and leaf composition. New Phytol 176:673–679PubMedGoogle Scholar
  188. Sumarah MW, Adams GW, Berghout J, Slack GJ, Wilson AM, Miller JD (2008) Spread and persistence of a rugulosin-producing endophyte in Picea glauca seedlings. Mycol Res 112:731–736PubMedGoogle Scholar
  189. Suryanarayanan TS, Thennarasan S (2004) Temporal variation in endophyte assemblages of Plumeria rubra leaves. Fungal Divers 15:197–204Google Scholar
  190. Suryanarayanan TS, Wittlinger SK, Faeth SH (2005) Endophytic fungi associated with cacti in Arizona. Mycol Res 109:635–639PubMedGoogle Scholar
  191. Tanaka A, Tapper BA, Popay A, Parker EJ, Scott B (2005) A symbiosis expressed non-ribosomal peptide synthetase from a mutualistic fungal endophyte of perennial ryegrass confers protection to the symbiotum from insect herbivory. Mol Microbiol 57:1036–1050PubMedGoogle Scholar
  192. Thompson JN (1994) The coevolutionary process. The University of Chicago Press, LondonGoogle Scholar
  193. Thompson JN (2005) Geographic mosaic of coevolution. University of Chicago Press, ChicagoGoogle Scholar
  194. Tibbets TM, Faeth SH (1999) Neotyphodium endophytes in grasses: deterrents or promoters of herbivory by leaf-cutting ants? Oecologia 118:297–305Google Scholar
  195. Tintjer T, Rudgers JA (2006) Grass-herbivore interactions altered by strains of a native endophyte. New Phytol 170:513–521PubMedGoogle Scholar
  196. Trevathan LE (1996) Performance of endophyte-free and endophyte-infected tall fescue seedlings in soil infested with Cochliobolus sativus. Can J Plant Pathol 18:415–418Google Scholar
  197. Urrutia MA, Wade MR, Phillips CB, Wratten SD (2007) Influence of host diet on parasitoid fitness: unravelling the complexity of a temperate pastoral agroecosystem. Entomol Exp Appl 123:63–71Google Scholar
  198. Van Bael SA, Valencia MC, Rojas EI, Gomez N, Windsor DM, Herre EA (2009) Effects of foliar endophytic fungi on the preference and performance of the leaf beetle Chelymorpha alternans in Panama. Biotropica 41:221–225Google Scholar
  199. Vicari M, Hatcher PE, Ayres PG (2002) Combined effect of foliar and mycorrhizal endophytes on an insect herbivore. Ecology 83:2452–2464CrossRefGoogle Scholar
  200. Walston AT, Held DW, Mason NR, Potter DA (2001) Absence of interaction between endophytic perennial ryegrass and susceptibility of Japanese beetle (Coleoptera: Scarabaeidae) grubs to Paenibacillus popilliae. J Entomol Sci 36:105–108Google Scholar
  201. West CP, Izekor E, Oosterhuis DM, Robbins RT (1988) The effect of Acremonium coenophialum on the growth and nematode infestation of tall fescue. Plant Soil 112:3–6Google Scholar
  202. White JF, Sullivan RF, Balady GA, Gianfagna TJ, Yue Q, Meyer WA, Cabral D (2001) A fungal endosymbiont of the grass Bromus setifolius: distribution in some Andean populations, identification, and examination of beneficial properties. Symbiosis 31:241–257Google Scholar
  203. Williamson RC, Potter DA (1997) Turfgrass species and endophyte effects on survival, development and feeding preference of black cutworms (Lepidoptera: Noctuidae). J Econ Entomol 90:1290–1299Google Scholar
  204. Wilson D (1995) Fungal endophytes which invade insect galls - insect pathogens, benign saprophytes, or fungal inquilines. Oecologia 103:255–260Google Scholar
  205. Wilson D, Carroll GC (1997) Avoidance of high-endophyte space by gall-forming insects. Ecology 78:2153–2163CrossRefGoogle Scholar
  206. Wilson D, Faeth SH (2001) Do fungal endophytes result in selection for leafminer ovipositional preference? Ecology 82:1097–1111CrossRefGoogle Scholar
  207. Wilson AD, Clement SL, Kaiser WJ (1991) Survey and detection of endophytic fungi in Lolium germ plasm by direct staining and aphid assays. Plant Dis 75:169–173Google Scholar
  208. Zust T, Härri SA, Müller CB (2008) Endophytic fungi decrease available resources for the aphid Rhopalosiphum padi and impair their ability to induce defences against predators. Ecol Entomol 33:80–85Google Scholar

Copyright information

© Kevin D Hyde 2010

Authors and Affiliations

  1. 1.MTT Agrifood Research Finland, Plant protectionJokioinenFinland
  2. 2.Section of Ecology, Department of BiologyUniversity of TurkuTurkuFinland

Personalised recommendations