Plant Ecology

, Volume 219, Issue 4, pp 359–368 | Cite as

Soil-borne seed pathogens: contributors to the naturalization gauntlet in Pacific Northwest (USA) forest and steppe communities?

  • B. M. Connolly
  • L. M. Carris
  • R. N. Mack


Soil-borne seed pathogens are omnipresent but are often overlooked components of a community’s biotic resistance to plant naturalization and invasion. Using multi-year greenhouse experiments, we compared the seed mortality of single invasive, naturalized, and native grass species in sterilized and unsterilized soils collected from Pacific Northwest (USA) steppe and forest communities. Native Pseudoroegneria spicata displayed the greatest seed mortality, naturalized Secale cereale displayed intermediate seed mortality, and invasive Bromus tectorum was least affected by soil pathogens. Seed mortality across all three species was consistently greater in soils collected from steppe than soils collected from forest; seeds sown into sterilized steppe soil experienced half the overall seed mortality compared to seeds sown into unsterilized steppe soil. Soil sterilization did not affect grass seed mortality in forest soils. We conclude that (1) removing soil-borne pathogens with sterilization does increase native and non-native grass seed survival, and (2) soil-borne pathogens may influence whether an introduced species becomes invasive or naturalized within these Pacific Northwest communities as a result of differential seed survival. Soil-borne pathogens in these communities, however, have the greatest negative effect on the survival of native grass seeds, suggesting that the native microbial soil flora more effectively attack seeds of native plants than seeds of non-native species.


Biotic resistance Bluebunch wheatgrass Cereal rye Cheatgrass Invasibility Soil pathogens 



We thank S. Porter, D.E. Pearson and M.F. Dybdahl and two anonymous reviewers for helpful comments on earlier versions of the manuscript. J. L. Richards, J. Harris and C. Cody provided field assistance, sample and data collection, and greenhouse maintenance, respectively. We thank M. Rule for assistance with site identification and permit preparation at the Turnbull National Wildlife Refuge sites. Funds from the Betty Higinbotham Trust at Washington State University provided financial support for this research. A USDA-NIFA Fellowship (Grant #2014-02074; awarded to B.M.C.), Michael Guyer Fellowship funding (UW-Madison, Department of Integrative Biology), and the Dean’s Office at EMU provided financial support to B.M.C. while writing this manuscript.

Supplementary material

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  1. Agrawal AA, Kotanen PM, Mitchell CE, Power AG, Godsoe W, Klironomos JN (2005) Enemy release? An experiment with congeneric plant pairs and diverse above- and belowground enemies. Ecology 86(11):2979–2989CrossRefGoogle Scholar
  2. Agrios G (2005) Plant Pathology, 5th edn. Academic Press, New YorkGoogle Scholar
  3. Augspurger CK (1984) Seedling survival of tropical tree species—interactions of dispersal distance, light-gaps, and pathogens. Ecology 65(6):1705–1712CrossRefGoogle Scholar
  4. Baker HG (1986) Patterns of plant invasion in North America. In: Mooney HA, Drake JA (eds) Ecology of Biological Invasions of North America and Hawaii. Springer, New York, pp 44–57CrossRefGoogle Scholar
  5. Baynes M, Newcombe G, Dixon L, Castlebury L, O’Donnell K (2012) A novel plant-fungal mutualism associated with fire. Fungal Biology 116(1):133–144CrossRefPubMedGoogle Scholar
  6. Beckstead J, Meyer SE, Molder CJ, Smith C (2007) A race for survival: can Bromus tectorum seeds escape Pyrenophora semeniperda-caused mortality by germinating quickly? Ann Bot 99:907–914CrossRefPubMedPubMedCentralGoogle Scholar
  7. Beckstead J, Meyer SE, Connolly BM, Huck MB, Street LE (2010) Cheatgrass facilitates spillover of a seed bank pathogen onto native grass species. J Ecol 98(1):168–177CrossRefGoogle Scholar
  8. Bennett JA, Maherali H, Reinhart KO, Lekberg Y, Hart MM, Klironomos J (2017) Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355:181–184CrossRefPubMedGoogle Scholar
  9. Blaney CS, Kotanen PM (2001) Effects of fungal pathogens on seeds of native and exotic plants: a test using congeneric pairs. J Appl Ecol 38(5):1104–1113CrossRefGoogle Scholar
  10. Borza JK, Westerman PR, Liebman M (2007) Comparing estimates of seed viability in three Foxtail (Setaria) species using the imbibed seed crush test with and without additional tetrazolium testing. Weed Technol 21:5118–5222CrossRefGoogle Scholar
  11. Connolly, BM. 2013. Comparing biotic resistance between Pacific Northwest steppe and coniferous forest: The role of predation, competition, and parasitism. Ph.D. diss., Washington State UniversityGoogle Scholar
  12. Connolly BM, Orrock JL (2015) Climatic variation and seed persistence: freeze-thaw cycles lower survival via the joint action of abiotic stress and fungal pathogens. Oecologia 179:609–619CrossRefPubMedGoogle Scholar
  13. Connolly BM, Pearson DE, Mack RN (2014) Granivory of invasive, naturalized, and native plants in communities differentially susceptible to invasion. Ecology 95(7):1759–1769CrossRefPubMedGoogle Scholar
  14. Connolly BM, Orrock JL, Witter MS (2016) Soil conditions moderate the effects of herbivores, but mycorrhizae, on a native bunchgrass. Acta Oecologica 77:100–108CrossRefGoogle Scholar
  15. Connolly BM, Powers J, Mack RN (2017) Biotic constraints on the establishment and performance of native, naturalized, and invasive plants in Pacific Northwest (USA) steppe and forest. Neobiota 34:21–40CrossRefGoogle Scholar
  16. Crist TO, Friese CF (1993) The impact of fungi on soil seeds—implications for plants and granivores in a semiarid shrub-steppe. Ecology 74(8):2231–2239CrossRefGoogle Scholar
  17. Daubenmire R (1970) Steppe vegetation of Washington. Washington Agric Exp Station Tech Bull 62:1–131Google Scholar
  18. Daubenmire R, Daubenmire J (1968) Forest vegetation of Eastern Washington and Northern Idaho. Washington Agric Exp Station Tech Bull 60:1–104Google Scholar
  19. Domsch KH, Gams W, Anderson T (1993) Compendium of Soil Fungi. Eching. IHW-Verlag; reprint. vol 1 and 2Google Scholar
  20. Dostál P (2010) Post-dispersal seed mortality of exotic and native species: effects of fungal pathogens and seed predators. Basic Appl Ecol 11(8):676–684CrossRefGoogle Scholar
  21. Elton C (1958) The ecology of invasions by animals and plants. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  22. Flory SL, Clay K (2013) Pathogen accumulation and long-term dynamics of plant invasions. J Ecol 101(3):607–613CrossRefGoogle Scholar
  23. Harley JL, Waid JS (1955) The effect of light upon the roots of beech and its surface population. Plant Soil 7(1):96–112CrossRefGoogle Scholar
  24. Harper JL (1977) Population Biology of Plants. University College of North Wales, BagnorGoogle Scholar
  25. Howell CR (2003) Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87:4–10CrossRefGoogle Scholar
  26. Kirkpatrick BL, Bazzaz FA (1979) Influence of certain fungi on seed germination and seedling survival of four colonizing annuals. J Appl Ecol 16(2):515–527CrossRefGoogle Scholar
  27. Kotanen PM (2007) Effects of fungal seed pathogens under conspecific and heterospecific trees in a temperate forest. Canadian J Bot-Revue Canadienne De Botanique 85(10):918–925Google Scholar
  28. Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7(10):975–989CrossRefGoogle Scholar
  29. Littell RC, Stroup WW, Milliken GA, Wolfinger RD, Schabenberger O (2006) SAS for mixed models. SAS instituteGoogle Scholar
  30. Liu Y, Yu SX, Xie ZP, Staehelin C (2012) Analysis of a negative plant-soil feedback in a subtropical monsoon forest. J Ecol 100(4):1019–1028CrossRefGoogle Scholar
  31. Mack RN (1981) Invasions of Bromus tectorum L. into western North America: an ecological chronicle. Agro-Ecosyst 7:145–165CrossRefGoogle Scholar
  32. Mack RN (1986) Alien plant invasion into the Intermountain West: a case history. In: Mooney HA, Drake JA (eds) Ecology of biological invasions of North America and Hawaii. Springer, New York, pp 191–213CrossRefGoogle Scholar
  33. Mack RN (1991) The commercial seed trade: an early disperser of weeds in the United States. Econ Bot 45(2):257–273CrossRefGoogle Scholar
  34. Mack RN (1996) Biotic barriers to plant naturalization. Proceedings of the IX International Symposium on Biological Control of Weeds, pp 39–46Google Scholar
  35. Mack RN, Pyke DA (1984) The demography of Bromus tectorum: the role of microclimate, grazing and disease. J Ecol 72(3):731–748CrossRefGoogle Scholar
  36. Malmstrom CM, McCullough AJ, Johnson HA, Newton LA, Borer ET (2005) Invasive annual grasses indirectly increase virus incidence in California native perennial bunchgrasses. Oecologia 145(1):153–164CrossRefPubMedGoogle Scholar
  37. Mangan SA, Schnitzer SA, Herre EA, Mack KM, Valencia MC, Sanchez EI, Bever JD (2010) Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466(7307):752–755CrossRefPubMedGoogle Scholar
  38. Maron JL, Pearson DE, Potter T, Ortega YK (2012) Seed size and provenance mediate the joint effects of disturbance and seed predation on community assembly. J Ecol 100(6):1492–1500CrossRefGoogle Scholar
  39. Maron JL, Waller LP, Hahn MA, Diaconu A, Pal RW, Muller-Scharer H, Klironomos JN, Callaway RM (2013) Effects of soil fungi, disturbance and propagule pressure on exotic plant recruitment and establishment at home and abroad. J Ecol 101(4):924–932CrossRefGoogle Scholar
  40. Maron JL, Smith AL, Ortega YK, Pearson DE, Callaway RM (2016) Negative plant-soil feedbacks increase with plant abundance, and are unchanged by competition. Ecology 97(8):2055–2063CrossRefPubMedGoogle Scholar
  41. Meyer SE, Franke JL, Baughman OW, Beckstead J, Geary B, Bailey K (2014) Does Fusarium-caused seed mortality contribute to Bromus tectorum stand failure in the Great Basin? Weed Res 54(5):511–519CrossRefGoogle Scholar
  42. Milbau A, Nijs I, Van Peer L, Reheul D, De Cauwer B (2003) Disentangling invasiveness and invasibility during invasion in synthesized grassland communities. New Phytol 159(3):657–667CrossRefGoogle Scholar
  43. Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421(6923):625–627CrossRefPubMedGoogle Scholar
  44. Mordecai EA (2013) Despite spillover, a shared pathogen promotes native plant persistence in a cheatgrass-invaded grassland. Ecology 94(12):2744–2753CrossRefPubMedGoogle Scholar
  45. O’Hanlon-Manners DL, Kotanen PM (2006) Losses of seeds of temperate trees to soil fungi: effects of habitat and host ecology. Plant Ecol 187(1):49–58CrossRefGoogle Scholar
  46. Olff H, Hoorens B, de Goede RGM, van der Putten WH, Gleichman JM (2000) Small-scale shifting mosaics of two dominant grassland species: the possible role of soil-borne pathogens. Oecologia 125(1):45–54CrossRefPubMedGoogle Scholar
  47. Orrock JL, Christopher CC, Dutra HP (2012) Seed bank survival of an invasive species, but not of two native species, declines with invasion. Oecologia 168(4):1103–1110CrossRefPubMedGoogle Scholar
  48. Packer A, Clay K (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404(6775):278–281CrossRefPubMedGoogle Scholar
  49. Parker IM, Gilbert GS (2007) When there is no escape: the effects of natural enemies on native, invasive, and noninvasive plants. Ecology 88(5):1210–1224CrossRefPubMedGoogle Scholar
  50. Parks C, Radosevich S, Endress B, Naylor B, Anzinger D, Maxwell B, Dwire K (2005) Natural and land-use history of the Northwest mountain ecoregions (USA) in relating to patterns of plant invasions. Perspect Plant Ecol Evol Syst 7:137–158CrossRefGoogle Scholar
  51. Pearson DE, Potter T, Maron JL (2012) Biotic resistance: exclusion of native rodent consumers releases populations of a weak invader. J Ecol 100:1383–1390CrossRefGoogle Scholar
  52. Pierson EA, Mack RN (1990) The population biology of Bromus tectorum in forests—effect of disturbance, grazing, and litter on seedling establishment and reproduction. Oecologia 84(4):526–533CrossRefPubMedGoogle Scholar
  53. Pons TL (2000) Seed responses to light. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities, 2nd edn. CABI Publishing, Wallingford, pp 237–260CrossRefGoogle Scholar
  54. Power AG, Mitchell CE (2004) Pathogen spillover in disease epidemics. Am Nat 164(S5):S79–S89CrossRefPubMedGoogle Scholar
  55. Reichard S, White P (2001) Horticulture as a pathway of invasive plant introductions in the United States. Bioscience 51(2):103–113CrossRefGoogle Scholar
  56. Reinhart KO, Rinella MJ (2016) A common soil handling technique can generate incorrect estimates of soil biota effects on plants. New Phytol 210:786–789CrossRefPubMedGoogle Scholar
  57. Reinhart KO, Tytgat T, Van der Putten WH, Clay K (2010) Virulence of soil-borne pathogens and invasion by Prunus serotina. New Phytol 186:484–495CrossRefPubMedGoogle Scholar
  58. Richardson DM, Pyšek P (2012) Naturalization of introduced plants: ecological drivers of biogeographical patterns. New Phytol 196(2):383–396CrossRefPubMedGoogle Scholar
  59. Rinella MJ, Reinhart KO (2017) Mixing soil samples across experimental units ignores uncertainty and generates incorrect estimates of soil biota effects on plants. New Phytol 216:15–17CrossRefPubMedGoogle Scholar
  60. Roth LF, Riker AJ (1943) Influence of temperature, moisture, and soil reaction on the damping-off of red pine seedlings by Pythium and Rhizoctonia. J Agric Res 67(7):273–293Google Scholar
  61. Roy BA, Coulson T, Blaser W, Policha T, Stewart JL, Blaisdell GK, Güsewell S (2010) Population regulation by enemies of the grass Brachypodium sylvaticum: demography in native and invaded ranges. Ecology 92:665–675CrossRefGoogle Scholar
  62. Schafer M, Kotanen PM (2004) Impacts of naturally-occurring soil fungi on seeds of meadow plants. Plant Ecol 175:19–35CrossRefGoogle Scholar
  63. Schultheis EH, Berardi AE, Lau JA (2015) No release for the wicked: enemy release is dynamic and not associated with invasiveness. Ecology 96(9):2446–2457CrossRefPubMedGoogle Scholar
  64. Schulz B (2006) Mutualistic interactions with fungal root endophytes. Microbial Root Endophytes, Springer Berlin Heidelberg 261–279Google Scholar
  65. Seifert, K, G Morgan-Jones, W Gams, and B Kendrick. 2011. The Genera of Hyphomycetes. CBS Biodiversity Series 9, CBS-KNAW Fungal Biodiversity Centre, Utrecht, The NetherlandsGoogle Scholar
  66. Simberloff D, Gibbons L (2004) Now you see them, now you don’t!—population crashes of established introduced species. Biol Invasions 6:161–172CrossRefGoogle Scholar
  67. Smith, MC. 2011. Predicting plant naturalizations in the Pacific Northwest: The fate of bamboos in the understory of coniferous forests. Ph.D. diss., Washington State University, 2011Google Scholar
  68. Suwa T, Louda SM (2012) Combined effects of plant competition and insect herbivory hinder invasiveness of an introduced thistle. Oecologia 169(2):467–476CrossRefPubMedGoogle Scholar
  69. Trevors JT (1996) Sterilization and inhibition of microbial activity in soil. J Microbiol Methods 26(1–2):53–59CrossRefGoogle Scholar
  70. Vaartaja O (1962) The relationship of fungi to survival of shaded tree seedlings. Ecology 43(3):547–549CrossRefGoogle Scholar
  71. van der Heijden MG, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310CrossRefPubMedGoogle Scholar
  72. van Kleunen M, Dawson W, Schlaepfer D, Jeschke JM, Fischer M (2010) Are invaders different? A conceptual framework of comparative approaches for assessing determinants of invasiveness. Ecol Lett 13(8):947–958PubMedGoogle Scholar
  73. Vandenkoornhuyse P, Baldauf SL, Leyval C, Straczek J, Young JPW (2002) Extensive fungal diversity in plant roots. Science 295:2051CrossRefPubMedGoogle Scholar
  74. Wearing A, Burgess L (1979) Water potential and the saprophytic growth of Fusarium roseum “Graminearum”. Soil Biol Biochem 11(6):661–667CrossRefGoogle Scholar
  75. Zenni RD, Nunez MA (2013) The elephant in the room: the role of failed invasions in understanding invasion biology. Oikos 122(6):801–815CrossRefGoogle Scholar

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© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BiologyEastern Michigan UniversityYpsilantiUSA
  2. 2.Department of Plant PathologyWashington State UniversityPullmanUSA
  3. 3.School of Biological SciencesWashington State UniversityPullmanUSA
  4. 4.Department of Integrative BiologyUniversity of WisconsinMadisonUSA

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