Skip to main content
Log in

Does An Asexual Endophyte Symbiont Alter Life Stage and Long-Term Survival in a Perennial Host Grass?

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Asexual, seedborne endophytic fungi in perennial grasses are often viewed as strong mutualists because fitness of the symbiont and host grass are closely coupled. However, at least for some native grasses, the asexual endophyte, Neotyphodium, acts parasitically, yet remains at high frequencies in natural populations. Most previous studies of Neotyphodium effects on host survival have been short term relative to the long life span of the perennial grass host. We therefore tested the hypothesis that Neotyphodium alters the survival in various life stages and long-term survival of adult native Arizona fescue (Festuca arizonica). To test the former, we planted 40 infected (E+) and 40 uninfected (E−, endophyte removed) seeds from four different maternal plants in the field under ambient conditions. We followed survival of seeds, seedlings, and adult plants over a 5-year period. To test the latter, we determined the infection of 1633 adult plants and followed their survival over the next 5–7 years. E+ seeds did not differ from uninfected seeds in terms of overall survival from seed germination to seedling to adult. However, the shape of the survival curve differed, with E+ plants showing higher mortality in early life stages. E+ adult plants did not differ from E− plants in long-term survival. Survival was generally very high during the study, which included a severe and prolonged drought. Infection by asexual Neotyphodium does not increase survival in early life stages or that of adult plants. Because asexual, vertically transmitted symbionts are predicted by evolutionary theory to be strong mutualists, the persistence of high infection frequencies in natural populations without long-term benefits to the host remains enigmatic. One possible explanation is that the long life span of the perennial host and low seedling recruitment may obscure either the costs or benefits of endophyte infection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2

Similar content being viewed by others

References

  1. 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 Univ Press, Cambridge, pp 89–123

    Google Scholar 

  2. Arnold, AE, Maynard, Z, Gilbert, GS, Coley, PD, Kursar, TA (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3: 267–274

    Article  Google Scholar 

  3. Clay, K (1990) Fungal endophytes of grasses. Annu Rev Ecol Syst 21: 275–297

    Article  Google Scholar 

  4. Clay K (1990) Comparative demography of three graminoids infected by systemic, clavicipitaceous fungi. Ecology 71:558–570

    Article  Google Scholar 

  5. Schardl, CL, Clay, K (1997) Evolution of mutualistic endophytes from plant pathogens. In: Carroll, GC, Tudzynski, P (eds.) The Mycota. V. Plant Relationships. Part B. Springer-Verlag, Berlin, pp 221–238

    Google Scholar 

  6. Saikkonen, K, Faeth, SH, Helander, M, Sullivan, TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Ann Rev Ecol Syst 29: 319–343

    Article  Google Scholar 

  7. Clay, K, Schardl, C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160: S99–S127

    Google Scholar 

  8. Law, R (1985) Evolution in a mutualistic environment. In: Boucher, DH (ed.) The Biology of Mutualisms. Croom Helm, London, pp 145–170

    Google Scholar 

  9. Massad, E (1987) Transmission rates and the evolution of pathogenicity. Evolution 41: 1127–1130

    Article  Google Scholar 

  10. Ewald, PW (1994) Evolution of Infectious Disease. Oxford University Press, Oxford, UK

    Google Scholar 

  11. Frank, SA (1994) Genetics of mutualisms: the evolution of altruism between species. J Theor Biol 170: 393–400

    Article  CAS  PubMed  Google Scholar 

  12. Saikkonen, K, Wali, P, Helander, M, Faeth, SH (2004) Evolution of endophyte plant symbioses. Trends Plant Sci 9: 275–280

    Article  CAS  PubMed  Google Scholar 

  13. Müller, CB, Krauss, J (2005) Symbiosis between grasses and asexual endophytes. Curr Opin Plant Biol 8: 450–456

    Article  PubMed  CAS  Google Scholar 

  14. Bazely, DR, Vicari, M, Emmerich, S, Filip, L, Lin, D, Inman, AI (1997) Interactions between herbivores and endophyte-infected Festuca rubra from the Scottish islands of St. Kilda, Benbecul and Rum. J Appl Ecol 34: 847–861

    Article  Google Scholar 

  15. Tibbets, TM, Faeth, SH (1999) Neotyphodium endophytes in grasses: deterrents or promoters of herbivory by leaf-cutting ants? Oecologia 118: 297–305

    Article  Google Scholar 

  16. Faeth, SH (2002) Are endophytic fungi generally plant mutualists? Oikos 98: 25–36

    Article  Google Scholar 

  17. Clement, SL, Elbersen, LR, Bosque-Pérez, NA, Schotzko, DJ (2005) Detrimental and neutral effects of wild barley–Neotyphodium fungal endophyte associations on insect survival. Entomol Exp Appl 114: 19–125

    Article  Google Scholar 

  18. Ahlhom, JU, Helander, M, Lehtimaki, S, Wäli, P, Saikkonen, K (2002). Benefits of seed-borne endophytes: effects of host species, life stage and environmental conditions. Oikos 99: 173–183

    Article  Google Scholar 

  19. Faeth, SH, Sullivan, TJ (2003) Mutualistic, asexual endophytes in a native grass are usually parasitic. Am Nat 161: 310–325

    Article  PubMed  Google Scholar 

  20. Morse, LJ, Day, TA, Faeth, SH (2002) Effect of Neotyphodium endophyte infection on growth and leaf gas exchange of Arizona fescue under contrasting water availability regimes. Environ Exp Bot 48: 257–268

    Article  Google Scholar 

  21. Lewis, GC, Ravel, C, Naffaa, W, Astier, C, Charmet, G (1997) Occurrence of Acremonium-endophytes of wild populations of Lolium spp. in European countries and a relationship between level of infection and climate in France. Ann Appl Biol 130: 227–238

    Article  Google Scholar 

  22. Schulthess, F, Faeth, SH (1998) Distribution, abundances, and associations of the endophytic fungal community of Arizona fescue (Festuca arizonica). Mycologia 90: 569–578

    Google Scholar 

  23. Clement, SL, Elberson, LR, Youssef, NN, Davitt, CM, Ross, RP (2001) Incidence and diversity of Neotyphodium fungal endophytes in tall fescue from Morroco, Tunisia and Sardinia. Crop Sci 41: 570–576

    Article  Google Scholar 

  24. Vinton, MA, Kathol, ES, Vogel, KP, Hopkins, AA (2001) Endophytic fungi in Canada wild rye: widespread occurrence in natural grasslands in the central United States. J Range Manag 54: 390–395

    Google Scholar 

  25. Clay K (1998) Fungal endophyte infection and the population biology of grasses. In: Cheplick, GP (ed.) The Population Biology of Grasses. Cambridge Univ Press, Cambridge, pp 255–285

    Google Scholar 

  26. Fowler, NL, Clay, K (1995). Environmental heterogeneity, fungal parasitism and the demography of the grass Stipa leucotricha. Oecologia 103: 55–62

    Article  Google Scholar 

  27. Saikkonen, K, Lehtonen, P, Helander, ML, Koricheva J, Faeth, SH (2006). Conventional wisdom and model systems in ecology: dissecting the grass-endophyte literature. Trends Plant Sci (in press)

  28. Harberd, DJ (1961) Observations on population structure and longevity of Festuca rubra L. New Phytol 60: 184–206

    Article  Google Scholar 

  29. Harberd, DJ (1962) Some observations on natural clones in Festuca ovina L. New Phytol 61: 85–100

    Article  Google Scholar 

  30. Antonovics, J (1972) Population dynamics of the grass Anthoxanthum odoratum on a zinc mine. J Ecol 60: 351–365

    Article  Google Scholar 

  31. Williams, OB (1970) Population dynamics of two perennial grasses in Australian semi-arid grassland. J Ecol 58: 869–875

    Article  Google Scholar 

  32. Faeth, SH, Saikkonen, K, Helander, M (2004) Asexual Neotyphodium endophytes in a native grass reduce competitive abilities. Ecol Let 7: 304–313

    Article  Google Scholar 

  33. Wilkinson, HH, Schardl, CL (1997) The evolution of mutualism in grass–endophyte associations. In: Bacon, CW, Hill, NS (eds) Neotyphodium/Grass Interactions. Plenum Press, New York, NY, pp 13–26

    Google Scholar 

  34. Faeth, SH, Haase, SH, Sackett, SS, Sullivan, TJ, Keithley, RK, Hamilton, CE (2002) Does fire maintain systemic endophyte infections in native grasses? Symbiosis 32: 211–228

    Google Scholar 

  35. An, Z-Q, Liu, J-S, Siegel, MR, Bunge, G, Schardl, CL (1992) Diversity and origins of endophytic fungal symbionts of the North American grass Festuca arizonica. Theor Appl Genet 85: 366–371

    Article  CAS  Google Scholar 

  36. Sullivan, TJ, Faeth, SH (2001) Genetic variation of Neotyphodium in native grass populations. In: Paul, VH, Dapprich, PD (eds.) Proceedings of the 4th International Neotyphodium/Grass Interactions Symposium. Fachbereich Agrarwirtschaft, Soest, Germany, pp 283–288

    Google Scholar 

  37. Sullivan, TJ, Faeth, SH (2004) Gene flow in the endophyte Neotyphodium and implications for coevolution with Festuca arizonica. Mol Ecol 13: 649–656

    Article  CAS  PubMed  Google Scholar 

  38. United States Department of Agriculture (1988) Range Plant Handbook. Dover Publications, New York, NY

    Google Scholar 

  39. Sackett, SS, Haase, SM, Harrington, MG (1995) Lessons learned from fire use for Restoring southwestern Ponderosa pine ecosystems. USDA-Forest Service General Tech Report RM 278

  40. Cooper, CE (1960) Changes in vegetation, structure and growth of southwestern pine forest since white settlement. Ecol Monogr 30: 129–164

    Article  Google Scholar 

  41. Covington, WW, Moore, MM (1994) Southwestern ponderosa forest structure: changes since Euro-American settlement. J For 92: 39–47

    Google Scholar 

  42. Saikkonen, K, Helander, M, Faeth, SH, Schulthess, F, Wilson, D (1999) Neotyphodium endophytes in native grass populations: against herbivory-based defensive mutualism. Oecologia 121: 411–420

    Article  Google Scholar 

  43. Gwinn, KD, Collins-Shephard, MH, Reddick, BB (1991) Tissue-print immunoblots: an accurate method for the detection of Acremonium coenophialum in tall fescue. Phytopathology 81: 747–748

    Google Scholar 

  44. Saha, DC, Jackson, MA, Johonson-Cicalese, JM (1988) A rapid staining method for detection of endophytic fungi in turf and forage grasses. Phytopathology 78: 237–239

    CAS  Google Scholar 

  45. Pyke, DA, Thompson, JN (1986) Statistical analyses of survival and removal rate experiments. Ecology 67: 240–245

    Article  Google Scholar 

  46. Kalbfleisch, JD, Prentice, RL (1980) The Statistical Analyses of Time Failure Data. Wiley, New York, NY, USA

    Google Scholar 

  47. Allen, MF (1991) The Ecology of Mycorrhizae. Cambridge University Press, Cambridge, UK

    Google Scholar 

  48. Siegel, MR, Bush, LP (1996) Defensive chemicals in grass–fungal endophyte associations. Rec Adv Phytochem 30: 81–118

    CAS  Google Scholar 

  49. Bacon, CW, White, JF Jr (eds) (1994) Biotechnology of endophytic fungi of grasses. CRC Press, Boca Raton, FL, US

  50. Malinowski, D, Belesky, DP (1999) Neotyphodium coenophialum-infection affects the ability of tall fescue to use sparingly available phosphorous. J Plant Nutr 22:835–853

    Article  CAS  Google Scholar 

  51. Cheplick, GP, Perera, P, Koulouris, K (2002) Effects of drought on the growth of Lolium perenne genotypes with and without endophytes. Funct Ecol 14: 657–667

    Article  Google Scholar 

  52. Siegel, MR, Varney, DR, Johnson, MC, Nesmith, WC, Buckner, RC, Bush, LP, Burris, PB, II, Hardison, JR (1984) A fungal endophyte of tall fescue: evaluation of control methods. Phytopathology 74: 937–941

    CAS  Google Scholar 

  53. Ravel, C, Michalakis, Y, Charmet, G (1997) The effect of imperfect transmission on the frequency of mutualistic seed-borne endophytes in natural populations of grasses. Oikos 80: 18–24

    Article  Google Scholar 

  54. Buck, GW, Elbersen, HW, West, CP, Sleper, DA (1994) Endophyte enhances drought survival of Moroccan fescues. Ark Farm Res 43: 6–7

    Google Scholar 

  55. Lopez, JE, Faeth, SH, Miller, M (1995) The effect of endophytic fungi on herbivory by red-legged grasshoppers (Orthoptera: Acrididae) on Arizona fescue. Environ Entomol 24: 1576–1580

    Google Scholar 

  56. Hamilton, CE, Faeth, SH (2005) Asexual, systemic endophytes in grasses: a test of the seed germination and pathogen resistance hypothesis. Symbiosis 38: 69–86

    Google Scholar 

  57. Knoch, TR, Faeth, SH, Arnott, DL (1993) Endophytic fungi alter foraging and dispersal by desert seed-harvesting ants. Oecologia 95: 470–475

    Google Scholar 

  58. Neil, KL, Tiller, RL, Faeth, SH (2003) Germination of big Sacaton and endophyte-infected Arizona fescue under water stress. J Range Manag 56: 616–622

    Google Scholar 

  59. White, JF Jr, Martin, TI, Cabral, D (1996) Endophyte–host associations in grasses. 22. Conidia formation by Acremonium endophytes on the phylloplanes of Agrostis hiemalis and Poa rigidifolia. Mycologia 88: 174–178

    Google Scholar 

  60. Schardl, CL, Leuchtmann, A, Spiering, MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55: 315–340

    Article  CAS  PubMed  Google Scholar 

  61. Sackett, SS (1994) Observations on natural regeneration in Ponderosa pine following a prescribed fire in Arizona. USDA-Forest Service General Tech Report RM 435

Download references

Acknowledgments

We thank Laura Beard, Natalie Fuller, Hilary Gan, Cinnamon Hayes, Jean Horne, Andrea Jani, Morgan MacCallum, Wendy Marussich, Vivian Miller, Jennie Rambo, Stephanie Steele, Phil Steiner, T.J. Sullivan and Sally Wittlinger for assistance in the field and in the laboratory. Jesse Brunner provided statistical advice. We are also grateful to the Sally Haase and Steve Sackett of USDA Forest Service–Fire Research Lab, Riverside, CA, for their generous help in accessing the experimental fire rotation sites, and the Arboretum of Flagstaff for use of experimental plots. We are especially grateful to Dr. and Mrs. Meyer for use of their cabin during field observations. This research was supported by NSF grants DEB 9727020 and 0128343 to S.H.F.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stanley H. Faeth.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Faeth, S.H., Hamilton, C.E. Does An Asexual Endophyte Symbiont Alter Life Stage and Long-Term Survival in a Perennial Host Grass?. Microb Ecol 52, 748–755 (2006). https://doi.org/10.1007/s00248-006-9123-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-006-9123-z

Keywords

Navigation