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.
Similar content being viewed by others
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
Agrios G (2005) Plant Pathology, 5th edn. Academic Press, New York
Augspurger CK (1984) Seedling survival of tropical tree species—interactions of dispersal distance, light-gaps, and pathogens. Ecology 65(6):1705–1712
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
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
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
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
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
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
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
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
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
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
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
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
Daubenmire R (1970) Steppe vegetation of Washington. Washington Agric Exp Station Tech Bull 62:1–131
Daubenmire R, Daubenmire J (1968) Forest vegetation of Eastern Washington and Northern Idaho. Washington Agric Exp Station Tech Bull 60:1–104
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
Elton C (1958) The ecology of invasions by animals and plants. University of Chicago Press, Chicago
Flory SL, Clay K (2013) Pathogen accumulation and long-term dynamics of plant invasions. J Ecol 101(3):607–613
Harley JL, Waid JS (1955) The effect of light upon the roots of beech and its surface population. Plant Soil 7(1):96–112
Harper JL (1977) Population Biology of Plants. University College of North Wales, Bagnor
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
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
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
Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7(10):975–989
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
Mack RN (1981) Invasions of Bromus tectorum L. into western North America: an ecological chronicle. Agro-Ecosyst 7:145–165
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
Mack RN (1991) The commercial seed trade: an early disperser of weeds in the United States. Econ Bot 45(2):257–273
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
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
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
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
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
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
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
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
Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421(6923):625–627
Mordecai EA (2013) Despite spillover, a shared pathogen promotes native plant persistence in a cheatgrass-invaded grassland. Ecology 94(12):2744–2753
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
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
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
Packer A, Clay K (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404(6775):278–281
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
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
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
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
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
Power AG, Mitchell CE (2004) Pathogen spillover in disease epidemics. Am Nat 164(S5):S79–S89
Reichard S, White P (2001) Horticulture as a pathway of invasive plant introductions in the United States. Bioscience 51(2):103–113
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
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
Richardson DM, Pyšek P (2012) Naturalization of introduced plants: ecological drivers of biogeographical patterns. New Phytol 196(2):383–396
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
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
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
Schafer M, Kotanen PM (2004) Impacts of naturally-occurring soil fungi on seeds of meadow plants. Plant Ecol 175:19–35
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
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
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
Trevors JT (1996) Sterilization and inhibition of microbial activity in soil. J Microbiol Methods 26(1–2):53–59
Vaartaja O (1962) The relationship of fungi to survival of shaded tree seedlings. Ecology 43(3):547–549
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
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
Vandenkoornhuyse P, Baldauf SL, Leyval C, Straczek J, Young JPW (2002) Extensive fungal diversity in plant roots. Science 295:2051
Wearing A, Burgess L (1979) Water potential and the saprophytic growth of Fusarium roseum “Graminearum”. Soil Biol Biochem 11(6):661–667
Zenni RD, Nunez MA (2013) The elephant in the room: the role of failed invasions in understanding invasion biology. Oikos 122(6):801–815
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Thomas A. Nagel.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-018-0800-z