Hostname: page-component-7479d7b7d-qlrfm Total loading time: 0 Render date: 2024-07-11T22:48:59.326Z Has data issue: false hasContentIssue false

Direct and indirect effects of plant litter on a seed–pathogen interaction in Bromus tectorum seed banks

Published online by Cambridge University Press:  20 December 2011

Julie Beckstead*
Affiliation:
Department of Biology, Gonzaga University, Spokane, Washington99258, USA
Lauren E. Miller
Affiliation:
Department of Biology, Gonzaga University, Spokane, Washington99258, USA
Brian M. Connolly
Affiliation:
Department of Biology, Gonzaga University, Spokane, Washington99258, USA
*
*Correspondence Fax: (+1) 509-313-5804 Email: beckstead@gonzaga.edu

Abstract

The naturally occurring fungal seed pathogen, Pyrenophora semeniperda, reduces the seed bank of Bromus tectorum but the role of plant litter in this seed–pathogen interaction is unexplored. To investigate the direct and indirect effects of litter on this interaction, we first collected field seed-bank samples from low and high Bromus litter patches. From these data, we explored the relationship between litter depth, seed-bank density and seed mortality from P. semeniperda. Second, we manipulated the fungal stages (conidial spores and mycelium) in/on the litter through sterilization techniques, to measure the direct effect of litter on seed death. Third, for indirect effects, we manipulated litter levels and held seed density and inoculum constant to determine whether Bromus litter could modify the seed zone microsites to favour disease. We found that seed-bank samples from high-litter patches contained higher field-killed seed densities compared with low-litter patches, although the percent difference of disease between litter patch types varied among sites and years (e.g. 80% to 46%). In testing the direct effects of litter on the seed–pathogen interaction, we found that litter can act as a direct inoculum source for the pathogen in the early summer but decreases in disease transmission by the following spring when the litter naturally is in contact with seeds. Investigating indirect effects, we found four times as many pathogen-killed seeds in high-litter treatments as compared with low-litter treatments when inoculum loads and seed densities were held constant. In addition, we found that litter influences the seed–pathogen interaction through density-dependent disease transmission. Our findings demonstrate the ecological importance of litter in semi-arid environments as it influences disease levels of a seed pathogen by direct and indirect means.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Beckstead, J., Meyer, S.E., Molder, C.J. and Smith, C. (2007) A race for survival: can Bromus tectorum seeds escape Pyrenophora semeniperda-caused mortality by germinating quickly? Annals of Botany 99, 907914.Google Scholar
Beckstead, J., Meyer, S.E., Connolly, B.M., Huck, M.B. and Street, L.E. (2010) Cheatgrass facilitates spillover of a seed bank pathogen onto native grass species. Journal of Ecology 98, 168177.CrossRefGoogle Scholar
Bosy, J.L. and Reader, R.J. (1995) Mechanisms underlying the suppression of forb seedling emergence by grass (Poa pratensis) litter. Functional Ecology 9, 635639.Google Scholar
Campbell, M.A., Medd, R.W. and Brown, J.B. (2003) Optimizing conditions for growth and sporulation of Pyrenophora semeniperda. Plant Pathology 52, 448454.Google Scholar
Chambers, J.C. and MacMahon, J.A. (1994) A day in the life of a seed: movements and fates of seeds and their implications for natural and managed systems. Annual Review of Ecology and Systematics 25, 263292.CrossRefGoogle Scholar
Cortesi, P., Gadoury, D.M., Ricciolini, M. and Bisiach, M. (1997) Cleistothecia of Uncinula necator – an additional source of inoculum in Italian vineyards. Plant Disease 81, 922926.Google Scholar
Crist, T.O. and Friese, C.F. (1993) The impact of fungi on soil seeds: implications for plants and granivores in a semiarid shrub–steppe. Ecology 74, 22312239.CrossRefGoogle Scholar
Dalling, J.W., Swaine, M.D. and Garwood, N.C. (1998) Dispersal patterns and seed bank dynamics of pioneer trees in moist tropical forest. Ecology 79, 564578.CrossRefGoogle Scholar
Davidson, J.M., Wickland, A.C., Patterson, H.A., Falk, K.R. and Rizzo, D.M. (2005) Transmission of Phytophthora ramorum in mixed-evergreen forest in California. Phytopathology 95, 587596.Google Scholar
Evans, R.A. and Young, J.A. (1970) Plant litter and establishment of alien annual weed species in rangeland communities. Weed Science 18, 697703.CrossRefGoogle Scholar
Facelli, J.M. (1994) Multiple indirect effects of plant litter affect the establishment of woody seedlings in old fields. Ecology 75, 17271735.CrossRefGoogle Scholar
Facelli, J.M. and Pickett, S.T.A. (1991) Plant litter: light interception and effects on an old-field plant community. Ecology 72, 10241031.CrossRefGoogle Scholar
Facelli, J.M., Williams, R., Fricker, S. and Ladd, B. (1999) Establishment and growth of seedlings of Eucalyptus obliqua: interactive effects of litter, water, and pathogens. Australian Journal of Ecology 24, 484494.Google Scholar
Floyd, M.L., Hanna, D., Romme, W.H. and Crews, T.E. (2006) Predicting and mitigating weed invasions to restore natural post-fire succession in Mesa Verde National Park, Colorado, USA. International Journal of Wildland Fire 15, 247259.Google Scholar
Fowler, N.L. (1986) Microsite requirements for germination and establishment of three grass species. American Midland Naturalist 115, 131145.CrossRefGoogle Scholar
Frey, S.D., Six, J. and Elliott, E.T. (2003) Reciprocal transfer of carbon and nitrogen by decomposer fungi at the soil–litter interface. Soil Biology and Biochemistry 35, 10011004.Google Scholar
Gilbert, G.S. (2002) Evolutionary ecology of plant diseases in natural ecosystems. Annual Review of Phytopathology 40, 1343.Google Scholar
Goldberg, D.E. and Werner, P.A. (1983) The effects of size of opening in vegetation and litter cover on seedling establishment of goldenrods (Solidago spp.). Oecologia 60, 149155.CrossRefGoogle ScholarPubMed
Hamrick, J.L. and Lee, J.M. (1987) Effect of soil surface topography and litter cover on the germination, survival, and growth of musk thistle (Carduus nutans). American Journal of Botany 74, 451457.CrossRefGoogle Scholar
Kelrick, M.I. (1991) Factors affecting seeds in a sagebrush–steppe ecosystem and implications for the dispersion of an annual plant species, cheatgrass (Bromus tectorum). PhD dissertation, Utah State University, Logan, Utah.Google Scholar
Latorre, B.A. and Jones, A.L. (1979) Evaluation of weeds and plant refuse as potential sources of inoculum of Pseudomonas syringae in bacterial canker of cherry. Phytopathology 69, 11221125.CrossRefGoogle Scholar
Mack, R.N. (1981) Invasion of Bromus tectorum L. into western North America: an ecological chronicle. Agro-Ecosystems 7, 145165.CrossRefGoogle Scholar
Medd, R., Murray, G. and Pickering, D. (2003) Review of the epidemiology and economic importance of Pyrenophora semeniperda. Australasian Plant Pathology 32, 539550.Google Scholar
Meyer, S.E., Quinney, D., Nelson, D.L. and Weaver, J. (2007) Impact of the pathogen Pyrenophora semeniperda on Bromus tectorum seedbank dynamics in North American cold deserts. Weed Research 47, 5462.CrossRefGoogle Scholar
Meyer, S.E., Beckstead, J., Allen, P.S. and Smith, D.C. (2008) A seed bank pathogen causes seedborne disease: Pyrenophora semeniperda on undispersed grass seeds in western North America. Canadian Journal of Plant Pathology 30, 525533.CrossRefGoogle Scholar
Moricca, S. and Ragazzi, A. (2008) Fungal endophytes in Mediterranean oak forests: a lesson from Discula quercina. Phytopathology 98, 380386.Google Scholar
Nilsen, E.T., Lei, T.T., Clinton, B.D., Semones, S.W., Walker, J.F. and Miller, O.K. (1999) Inhibition of seedling survival under Rhododendron maximum (Ericaceae): could allelopathy be a cause? American Journal of Botany 86, 15971605.CrossRefGoogle ScholarPubMed
Ooi, M., Aulk, T. and Whelan, R. (2004) Comparison of the cut and tetrazolium tests for assessing seed viability: a study using Australian native Leucopogon species. Ecological Management and Restoration 5, 141143.CrossRefGoogle Scholar
Piotrowski, J.S., Rillig, M.C. and Morford, S.L. (2008) Inhibition of colonization by a native arbuscular mycorrhizal fungal community via Populus trichocarpa litter, litter extract, and soluble phenolic compounds. Soil Biology and Biochemistry 40, 709717.CrossRefGoogle Scholar
Reed, A.W., Kaufman, G.A. and Kaufman, D.W. (2006) Effect of plant litter on seed predation in three prairie types. American Midland Naturalist 155, 278285.Google Scholar
Rotundo, J.L. and Aguiar, M.R. (2005) Litter effects on plant regeneration in arid lands: a complex balance between seed retention, seed longevity and soil–seed contact. Journal of Ecology 93, 829838.Google Scholar
Schafer, M. and Kotanen, P.M. (2004) Impacts of naturally-occurring soil fungi on seeds of meadow plants. Plant Ecology 175, 1935.CrossRefGoogle Scholar
Stewart, T., Meyer, S.E. and Allen, P.S. (2009) First report of Pyrenophora semeniperda in Turkey and Greece. Plant Disease Reporter 93, 1351.Google Scholar
Weaver, J.E. and Rowland, N.W. (1952) Effects of excessive natural mulch on development, yield, and structure of native grassland. Botanical Gazette 114, 119.CrossRefGoogle Scholar