The developmental ecology of mycorrhizal associations in mayapple, Podophyllum peltatum, Berberidaceae

  • Maxine A. Watson
  • Kristin Scott
  • Jon Griffith
  • Stephanie Dieter
  • Cynthia S. Jones
  • Sunita Nanda


Associations between plants and arbuscular mycorrhizal (AM) fungi are widespread and well-studied. Yet little is known about the pattern of association between clonal plants and AM fungi. Here we report on the pattern of mycorrhizal association within the rhizome systems of mayapple, Podophyllum peltatum. Mayapple is a long-lived understory clonal herb that is classified as obligately mycorrhizal. We found that while all mayapple rhizome systems maintained mycorrhizal associations, the percent colonization of roots by AM fungi differed among ramets of different age. The highest concentrations of AM fungi were in the roots of intermediate-aged ramets, while roots beneath the youngest ramet were not colonized. This pattern of ramet age or position-dependent colonization was observed in two separate studies; each conducted in a different year and at a different site. The pattern of AM fungal colonization of mayapple rhizome systems suggests that the mycorrhizal relationship is facultative at the ramet level. This conclusion is reinforced by our observation that augmentation of soil phosphate lowers root colonization by AM fungi. We also found that soil phosphate concentrations were depleted by ca. 1% under the same ramet positions where roots bore the highest AM fungal loads. Three non-exclusive hypotheses are proposed regarding the mechanisms that might cause this developmentally dependent pattern of mycorrhizal association.

Key words

arbuscular mycorrhizal fungi developmental ecology developmental phenology facultative symbiosis mycorrhizal associations Podophyllum peltatum roots 


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  1. Abbot, L.K. and Gazey, C. (1994) An ecological view of the formation of VA mycorrhizas. Plant Soil 159, 69–78.Google Scholar
  2. Allen, M.F. (1983) Formation of vesicular-arbuscular mycorrhizae in Atriplex gardneri (Chenopodiaceae): seasonal response in cold desert. Mycologia 75, 773–776.CrossRefGoogle Scholar
  3. Allen, M.F. (1991) The Ecology of Mycorrhizae. Cambridge University Press, Cambridge. 184 pp.Google Scholar
  4. Allen, M.F. (1996) The ecology of arbuscular mycorrhizas: a look back into the 20th century and a peek into the 21st. Mycol. Res. 100, 769–782.CrossRefGoogle Scholar
  5. Allsop, N. (1998) Effect of defoliation on the arbuscular mycorrhizas of three perennial pasture and rangeland grasses. Plant Soil 202, 117–124.CrossRefGoogle Scholar
  6. Alpert, P. and Stuefer, J.F. (1997) Division of labor in clonal plants. In H. de Kroon and J. van Groenendael, (eds) The Ecology and Evolution of Clonal Plants. Backhuys Academic Publishers, Leiden, pp. 137–154.Google Scholar
  7. An, Z.Q., Guo, B.Z. and Hendrix, J.W. (1993) Populations of spores and propagules of mycorrhizal fungi in relation to the life cycles of tall fescue and tobacco. Soil Biol Biochem 25, 813–817.CrossRefGoogle Scholar
  8. Bates, T.E. (1993) Soil handling and preparation. In M.R. Carter (ed.) Soil Sampl Meth. Anal. Lewis, Ann Arbor, pp. 19–23.Google Scholar
  9. Benner, B. and Watson, M. (1989) Developmental ecology of mayapple: seasonal patterns of resource distribution in sexual and vegetative rhizome systems. Func. Ecol. 3, 539–547.CrossRefGoogle Scholar
  10. Binkley, D. and Vitousek, P. (1994) Soil nutrient availability. In R.W Pearcy, et al. (eds) Plant Physiological Ecology. - Field Methods and Instrumentation. Chapman and Hall, New York, pp. 75–83.Google Scholar
  11. Boerner, R.E.J. (1986) Seasonal nutrient dynamics, nutrient resorption, and mycorrhizal infection intensity of two perennial forest herbs. Amer. J. Bot. 73, 1249–1257.CrossRefGoogle Scholar
  12. Brundrett, M.C. (1996) Mycorrhizas in natural ecosystems. Adv. Ecol. Res. 21, 171–313.CrossRefGoogle Scholar
  13. Brundrett, M.C. and Kendrick, B. (1988) The mycorrhizal status, root anatomy and phenology of plants in a sugar maple forest. Can. J. Bot. 66, 1153–1173.CrossRefGoogle Scholar
  14. Brundrett, M.C. and Kendrick, B. (1990a) The roots and mycorrhizas of herbaceous woodland plants. I. Quantitative aspects of morphology. New Phytol. 114, 457–468.CrossRefGoogle Scholar
  15. Brundrett, M.C. and Kendrick, B. (1990b) The roots and mycorrhizas of herbaceous woodland plants. II. Structural aspects of morphology. New Phytol. 114, 479–486.Google Scholar
  16. Brundrett, M., Melville, L. and Peterson, L. (1994) Practical Methods in Mycorrhiza Research. Mycologue Publications, Guelph, Ontario. 161 pp.Google Scholar
  17. Brundrett, M.C., Piche, Y. and Peterson, R.L. (1984) A new method for observing the morphology of vescicular-arbuscular mycorrhizae. Can. J. Bot. 62, 2128–2134.CrossRefGoogle Scholar
  18. Caldwell, M.M. and Pearcy, R.W. (1994) Exploitation of Environmental Heterogeneity by Plants. Academic Press, New York. 429 pp.Google Scholar
  19. Callaghan, T.V. (1984) Growth and translocation in a clonal southern hemisphere sedge–Uncinia meridensis. J. Ecol. 72, 529–546.CrossRefGoogle Scholar
  20. Cooke, R. (1977) The Biology of Symbiotic Fungi. John Wiley and Sons Ltd., London. 282 pp.Google Scholar
  21. Cox, G., Sanders, F.E., Tinker, P.B. and Wild, J.A. (1975) Ultrastructural evidence relating to host endophyte transfer in a vesicular-arbuscular mycorrhiza. In F.E. Sanders, B. Mosse and P.B. Tinker (eds) Mycorrhizas. Academic Press, New York, pp. 297 312.Google Scholar
  22. DeMars, B.G. and Boerner, R.E.J. (1995) Mycorrhizal dynamics of three woodland herbs of contrasting phenology along topographic gradients. Amer. J. Bot. 82, 1426–1431.CrossRefGoogle Scholar
  23. Douds, D.D. Jr., Johnson, C.R. and Koch, K.E. (1988) Carbon costs of the fungal symbiont relative to net leaf P accumulation in a split-root VA mycorrhizal symbiosis. Plant Physiol. 86, 491–496.PubMedCrossRefGoogle Scholar
  24. Duke, S.E., Jackson, R.B. and Caldwell, M.M. (1994) Local reduction of mycorrhizal arbuscule frequency in enriched soil microsites. Can. J. Bot. 72, 998–1001.CrossRefGoogle Scholar
  25. Gay, P.E., Grubb, P.J. and Hudson, H.J. (1982) Seasonal changes in the concentrations of nitrogen, phosphorus and potassium, and in the density of mycorrhiza, in biennial and matrix-forming perennial species of closed chalkland turf. J. Ecol. 70, 571–593.CrossRefGoogle Scholar
  26. Geber, M.A., de Kroon, H. and Watson, M.A. (1997a) Organ preformation in mayapple as a mechanism for historical effects on demography. J. Ecol. 85, 211–223.CrossRefGoogle Scholar
  27. Geber, M.A., Watson, M.A. and de Kroon, H. (1997b) Development and resource allocation in perennial plants: The significance of organ preformation. In F.A Bazzaz and J. Grace (eds.) Plant Resource Allocation. Academic Press, London, pp. 113–141.CrossRefGoogle Scholar
  28. Gehring, C.A. and Whitham, T.G. (1992) Reduced mycorhizzae on Juniperus monosperma with mistletoe: the influence of environmental stress and tree gender on a plant parasite and plant-fungal mutualism. Oecologia 89, 298–303.Google Scholar
  29. Giovanetti, M. (1985) Seasonal variations of vesicular-arbuscular mycorrhizas and endogenous spores in a maritime sand dune. Trans. Brit. Mycol. Soc. 84, 679–684.CrossRefGoogle Scholar
  30. Giovannetti, M. and Mosse, B. (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol. 84, 489–500.CrossRefGoogle Scholar
  31. Graham, J.H. and Eissenstat, D.M. (1994) Host genotype and the formation and function of VA mycorrhizae. Plant Soil 159, 179–185.Google Scholar
  32. Graham, J.H., Eissenstat, D.M. and Drouillard, D.L. (1991) On the relationship between a plant’s mycorrhizal dependency and rate of vesicular-arbuscular mycorrhizal colonization. Func. Ecol. 5, 773–779.CrossRefGoogle Scholar
  33. Harley, J.L. and Smith, S.E. (1983) Mycorrhizal Symbiosis. Academic Press, London. 483 pp. Hendrix, J.W. (1993) Glomales mycorrhizal fungi as pathogens. Mycorrhiza News 5, 1–6.Google Scholar
  34. Jackson, R.B. and Caldwell, M.M. (1993) The scale of nutrient heterogeneity around individual plants and its quantification with geostatistics. Ecology 74, 612–614.CrossRefGoogle Scholar
  35. Jakobsen, I. (1998) Transport of phosphorus and carbon in arbuscular mycorrhizas. In A. Varma and B. Hock (eds.), Mycorrhiza: Structure, Function, Molecular Biology and Biotechnology. 2nd ed. Springer, pp. 305–332.Google Scholar
  36. Jakobsen, 1., Abbot, L.K. and Robson, A.D. (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L.1. Spread of hyphae and phosphorus inflow into roots. New Phytol. 120, 371–380.CrossRefGoogle Scholar
  37. Jónsdóttir, I.S. and Callaghan, T.V. (1990) Intraclonal translocation of ammonium and nitrate nitrogen in Carex bigelowii Torr. Ex Schwein. using ‘5N and nitrate reductase assays. New Phytol. 114, 419–428.CrossRefGoogle Scholar
  38. Jónsdóttir, I.S and Watson, M.A. (1997) Ecological significance of physiological integration in plants. In H. de Kroon and J. van Groenendael (eds) The Ecology and Evolution of Clonal Plants. Backhuys Academic Publishers, Leiden, pp. 109–136.Google Scholar
  39. Jónsdóttir, I.S., Callaghan, T.V. and Headley, A.D. (1996) Resource dynamics within arctic clonal plants. Ecol. Bull. 45, 53–64.Google Scholar
  40. Jones, C.S. and Watson, M.A. (2001) Heteroblasty and preformation in mayapple, Podophyllum peltatum (Berberidaceae): developmental flexibility and morphological constraint. Am. J. Bot. 88, 1340–1358.PubMedCrossRefGoogle Scholar
  41. Koide, R. (1985) The nature of growth depressions in sunflower caused by vesicular-arbuscular mycorrhizal infection. New Phytol. 99, 449–462.CrossRefGoogle Scholar
  42. Landa, K., Benner, B., Watson, M.A. and Gartner, J. (1992) Physiological integration for carbon in mayapple (Podophyllum peltatum), a clonal perennial herb. Oikos 63, 348–356.Google Scholar
  43. Mayr, R. and Goday, R. (1989) Seasonal patterns in vesicular-arbuscular mycorrhiza in a mesic beech forest. Agric. Ecosyst. Envir. 29, 281–288.Google Scholar
  44. Marshall, C. and Price, E.A.C. (1997) Sectoriality and its implications for physiological integration. In H. de Kroon and J. van Groenendael (eds) The Ecology and Evolution of Clonal Plants. Backhuys Academic Publishers, Leiden, pp. 79–108.Google Scholar
  45. Newsham, K.K., Fitter, A.H. and Watkinson, A.R. (1995) Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol. Evol. 10, 408–411.CrossRefGoogle Scholar
  46. Policansky, D. (1987) Sex choice and reproductive costs in jack-in-the-pulpit. Size determines a plant’s sexual state. Bioscience 37, 476–481.CrossRefGoogle Scholar
  47. Read, D.J. (1998) Mycorrhiza–the state of the art. In A. Varma and B. Hock (eds) Mycorrhiza: Structure, Function, Molecular Biology and Biotechnology. 2nd ed. Springer, pp. 3–36.Google Scholar
  48. Sanders, I.R. and Fitter, A.H. (1992) The ecology and functioning of vesicular-arbuscular mycorrhizae in co-existing grassland species. I. Seasonal patterns of mycorrihizal occurrence and morphology. New Phytol. 120, 517–524.CrossRefGoogle Scholar
  49. SAS (1988) SAS/STAT User’s Guide. Release 6. 03. SAS Institute Inc., Cary, N.C.Google Scholar
  50. Schemer, S.M. and Gurevitch, J. (ed) (2000) Design and Analysis of Ecological Experiments. 2nd ed. Oxford University Press, New York, 415 pp.Google Scholar
  51. Schoenau, J.J. and Karamanos, R.E. (1993) Sodium bicarbonate-extractable P, K and N. In M.R. Carter (ed.) Soil Sampling and Methods of Analysis, Lewis Publ., Ann Arbor, pp. 51–58.Google Scholar
  52. Smith, S.E. and Read, D.J. (1997) Mycorrhizal Symbioses. Academic Press, San Diego, 605 pp.Google Scholar
  53. Smith, F.A. and Smith, S.E. (1996) Mutualism and parasitism: diversity in function and structure in the `arbuscular’ (VA) mycorrizal symbiosis. Adv. Bot. Res. 22, 1–43.CrossRefGoogle Scholar
  54. Sohn, J.J. and Policansky, D. (1977) The costs of reproduction in the mayapple Podophyllum peltatum (Berberidaceae). Ecology 58, 1366–1374.CrossRefGoogle Scholar
  55. St. John, T.V. and Coleman, D.C. (1983) The role of mycorrhizae in plant ecology. Can. J. Bot. 61, 1005–1014.Google Scholar
  56. Streitwolf-Engel, R., Boller, T., Wiemken, A. and Sanders, I.R. (1997) Clonal growth traits of two Prunella species are determined by co-occurring arbuscular mycorrhizal fungi from a calcareous grassland. J. Ecol. 85, 181–191.CrossRefGoogle Scholar
  57. Streitwolf-Engel, R., van der Heijden, M.G.A., Wiemken, A. and Sanders, I.R. (2001) The ecological significance of arbuscular mycorrhizal fungal effects on clonal reproduction in plants. Ecology 82 (10), 2846–2859.CrossRefGoogle Scholar
  58. Watson, M.A. and Lu, Y. (1999) Timing of shoot senescence and demographic expression in the clonal perennial Podophyllum Peltatum (Berberidaceae). Oikos 86, 67–78.CrossRefGoogle Scholar
  59. Zobel, M., Moora, M. and Haukioja, E. (1997) Plant coexistence in the interactive environment: arbuscular mycorrhiza should not be out of mind. Oikos 78, 202–208.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2002

Authors and Affiliations

  • Maxine A. Watson
    • 1
  • Kristin Scott
    • 1
  • Jon Griffith
    • 1
  • Stephanie Dieter
    • 1
    • 2
  • Cynthia S. Jones
    • 2
  • Sunita Nanda
    • 1
  1. 1.Department of BiologyIndiana University BloomingtonUSA
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of ConnecticutStorrsUSA

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