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

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Abstract

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.

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References

  • 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):2979–2989

    Article  Google Scholar 

  • Agrios G (2005) Plant Pathology, 5th edn. Academic Press, New York

    Google Scholar 

  • Augspurger CK (1984) Seedling survival of tropical tree species—interactions of dispersal distance, light-gaps, and pathogens. Ecology 65(6):1705–1712

    Article  Google Scholar 

  • 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 44–57

    Chapter  Google Scholar 

  • Baynes M, Newcombe G, Dixon L, Castlebury L, O’Donnell K (2012) A novel plant-fungal mutualism associated with fire. Fungal Biology 116(1):133–144

    Article  PubMed  Google Scholar 

  • 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 99:907–914

    Article  PubMed  PubMed Central  Google Scholar 

  • 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):168–177

    Article  Google Scholar 

  • 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 355:181–184

    Article  CAS  PubMed  Google Scholar 

  • 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):1104–1113

    Article  Google Scholar 

  • 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 21:5118–5222

    Article  Google Scholar 

  • 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 University

  • 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 179:609–619

    Article  PubMed  Google Scholar 

  • Connolly BM, Pearson DE, Mack RN (2014) Granivory of invasive, naturalized, and native plants in communities differentially susceptible to invasion. Ecology 95(7):1759–1769

    Article  CAS  PubMed  Google Scholar 

  • Connolly BM, Orrock JL, Witter MS (2016) Soil conditions moderate the effects of herbivores, but mycorrhizae, on a native bunchgrass. Acta Oecologica 77:100–108

    Article  Google Scholar 

  • 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 34:21–40

    Article  Google Scholar 

  • 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):2231–2239

    Article  Google Scholar 

  • Daubenmire R (1970) Steppe vegetation of Washington. Washington Agric Exp Station Tech Bull 62:1–131

    Google Scholar 

  • Daubenmire R, Daubenmire J (1968) Forest vegetation of Eastern Washington and Northern Idaho. Washington Agric Exp Station Tech Bull 60:1–104

    Google Scholar 

  • Domsch KH, Gams W, Anderson T (1993) Compendium of Soil Fungi. Eching. IHW-Verlag; reprint. vol 1 and 2

  • Dostál P (2010) Post-dispersal seed mortality of exotic and native species: effects of fungal pathogens and seed predators. Basic Appl Ecol 11(8):676–684

    Article  Google Scholar 

  • Elton C (1958) The ecology of invasions by animals and plants. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Flory SL, Clay K (2013) Pathogen accumulation and long-term dynamics of plant invasions. J Ecol 101(3):607–613

    Article  Google Scholar 

  • Harley JL, Waid JS (1955) The effect of light upon the roots of beech and its surface population. Plant Soil 7(1):96–112

    Article  Google Scholar 

  • Harper JL (1977) Population Biology of Plants. University College of North Wales, Bagnor

    Google Scholar 

  • Howell CR (2003) Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87:4–10

    Article  Google Scholar 

  • Kirkpatrick BL, Bazzaz FA (1979) Influence of certain fungi on seed germination and seedling survival of four colonizing annuals. J Appl Ecol 16(2):515–527

    Article  Google Scholar 

  • 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):918–925

    Google Scholar 

  • Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7(10):975–989

    Article  Google Scholar 

  • Littell RC, Stroup WW, Milliken GA, Wolfinger RD, Schabenberger O (2006) SAS for mixed models. SAS institute

  • 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):1019–1028

    Article  Google Scholar 

  • Mack RN (1981) Invasions of Bromus tectorum L. into western North America: an ecological chronicle. Agro-Ecosyst 7:145–165

    Article  Google Scholar 

  • 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 191–213

    Chapter  Google Scholar 

  • Mack RN (1991) The commercial seed trade: an early disperser of weeds in the United States. Econ Bot 45(2):257–273

    Article  Google Scholar 

  • Mack RN (1996) Biotic barriers to plant naturalization. Proceedings of the IX International Symposium on Biological Control of Weeds, pp 39–46

  • Mack RN, Pyke DA (1984) The demography of Bromus tectorum: the role of microclimate, grazing and disease. J Ecol 72(3):731–748

    Article  Google Scholar 

  • 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):153–164

    Article  PubMed  Google Scholar 

  • 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):752–755

    Article  CAS  PubMed  Google Scholar 

  • 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):1492–1500

    Article  Google Scholar 

  • 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):924–932

    Article  Google Scholar 

  • 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):2055–2063

    Article  PubMed  Google Scholar 

  • 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):511–519

    Article  Google Scholar 

  • 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):657–667

    Article  Google Scholar 

  • Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421(6923):625–627

    Article  CAS  PubMed  Google Scholar 

  • Mordecai EA (2013) Despite spillover, a shared pathogen promotes native plant persistence in a cheatgrass-invaded grassland. Ecology 94(12):2744–2753

    Article  PubMed  Google Scholar 

  • 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):49–58

    Article  Google Scholar 

  • 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):45–54

    Article  CAS  PubMed  Google Scholar 

  • 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):1103–1110

    Article  PubMed  Google Scholar 

  • Packer A, Clay K (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404(6775):278–281

    Article  CAS  PubMed  Google Scholar 

  • Parker IM, Gilbert GS (2007) When there is no escape: the effects of natural enemies on native, invasive, and noninvasive plants. Ecology 88(5):1210–1224

    Article  PubMed  Google Scholar 

  • 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 7:137–158

    Article  Google Scholar 

  • Pearson DE, Potter T, Maron JL (2012) Biotic resistance: exclusion of native rodent consumers releases populations of a weak invader. J Ecol 100:1383–1390

    Article  Google Scholar 

  • 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):526–533

    Article  PubMed  Google Scholar 

  • 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 237–260

    Chapter  Google Scholar 

  • Power AG, Mitchell CE (2004) Pathogen spillover in disease epidemics. Am Nat 164(S5):S79–S89

    Article  PubMed  Google Scholar 

  • Reichard S, White P (2001) Horticulture as a pathway of invasive plant introductions in the United States. Bioscience 51(2):103–113

    Article  Google Scholar 

  • Reinhart KO, Rinella MJ (2016) A common soil handling technique can generate incorrect estimates of soil biota effects on plants. New Phytol 210:786–789

    Article  PubMed  Google Scholar 

  • Reinhart KO, Tytgat T, Van der Putten WH, Clay K (2010) Virulence of soil-borne pathogens and invasion by Prunus serotina. New Phytol 186:484–495

    Article  PubMed  Google Scholar 

  • Richardson DM, Pyšek P (2012) Naturalization of introduced plants: ecological drivers of biogeographical patterns. New Phytol 196(2):383–396

    Article  PubMed  Google Scholar 

  • 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 216:15–17

    Article  PubMed  Google Scholar 

  • 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):273–293

    Google Scholar 

  • 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 92:665–675

    Article  Google Scholar 

  • Schafer M, Kotanen PM (2004) Impacts of naturally-occurring soil fungi on seeds of meadow plants. Plant Ecol 175:19–35

    Article  Google Scholar 

  • Schultheis EH, Berardi AE, Lau JA (2015) No release for the wicked: enemy release is dynamic and not associated with invasiveness. Ecology 96(9):2446–2457

    Article  PubMed  Google Scholar 

  • Schulz B (2006) Mutualistic interactions with fungal root endophytes. Microbial Root Endophytes, Springer Berlin Heidelberg 261–279

  • 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 Netherlands

  • Simberloff D, Gibbons L (2004) Now you see them, now you don’t!—population crashes of established introduced species. Biol Invasions 6:161–172

    Article  Google Scholar 

  • 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, 2011

  • Suwa T, Louda SM (2012) Combined effects of plant competition and insect herbivory hinder invasiveness of an introduced thistle. Oecologia 169(2):467–476

    Article  PubMed  Google Scholar 

  • Trevors JT (1996) Sterilization and inhibition of microbial activity in soil. J Microbiol Methods 26(1–2):53–59

    Article  CAS  Google Scholar 

  • Vaartaja O (1962) The relationship of fungi to survival of shaded tree seedlings. Ecology 43(3):547–549

    Article  Google Scholar 

  • 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 11:296–310

    Article  PubMed  Google Scholar 

  • 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):947–958

    PubMed  Google Scholar 

  • Vandenkoornhuyse P, Baldauf SL, Leyval C, Straczek J, Young JPW (2002) Extensive fungal diversity in plant roots. Science 295:2051

    Article  PubMed  Google Scholar 

  • Wearing A, Burgess L (1979) Water potential and the saprophytic growth of Fusarium roseum “Graminearum”. Soil Biol Biochem 11(6):661–667

    Article  Google Scholar 

  • Zenni RD, Nunez MA (2013) The elephant in the room: the role of failed invasions in understanding invasion biology. Oikos 122(6):801–815

    Article  Google Scholar 

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Acknowledgments

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.

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Correspondence to B. M. Connolly.

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Communicated by Thomas A. Nagel.

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Connolly, B.M., Carris, L.M. & Mack, R.N. Soil-borne seed pathogens: contributors to the naturalization gauntlet in Pacific Northwest (USA) forest and steppe communities?. Plant Ecol 219, 359–368 (2018). https://doi.org/10.1007/s11258-018-0800-z

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