Abstract
Background and aims
Plant-soil feedbacks may determine the long-term success of introduced species. Here we examined plant-soil feedbacks of a globally invasive shrub, Cytisus scoparius (hereafter Cytisus), which associates with multiple guilds of microbial mutualists and dominates harvested Douglas-fir forests in the Pacific Northwest.
Methods
We studied Cytisus root nodulation, mycorrhizal colonization, and growth in two greenhouse experiments. First, we compared invaded to uninvaded field soils. Then we did a soil conditioning experiment with Cytisus (in both invaded and uninvaded field soil) compared to soil conditioned by Douglas-fir.
Results
Cytisus grown in invaded soils had 67% more root nodules and 72% more AMF colonization than uninvaded soil. Conditioning uninvaded soil with Cytisus increased root nodules by 14% and mycorrhizal colonization by 55%, compared to Douglas-fir conditioned soil. Despite the increased abundance of mutualists, Cytisus grown in Cytisus-conditioned soils were 41% smaller than in uninvaded soil.
Conclusions
Cytisus increased the abundance of its microbial mutualists in soils, but overall plant-soil feedback was still negative, likely driven by soilborne pathogens, nutrient depletion, and/ or reduced benefits of mutualists. Our results do not support the idea that the high densities reached by Cytisus in its invaded range are caused by positive plant-soil feedbacks.
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References
Agrawal AA, Kotanen PM, Mitchell CE, Power AG, Godsoe W, Klironomos J (2005) Enemy release? An experiment with congeneric plant pairs and diverse above- and belowground enemies. Ecology 86:2979–2989. https://doi.org/10.1890/05-0219
Anacker BL, Klironomos JN, Maherali H, Reinhart KO, Strauss SY (2014) Phylogenetic conservatism in plant-soil feedback and its implications for plant abundance. Ecol Lett 17:1613–1621. https://doi.org/10.1111/ele.12378
Barrett LG, Broadhurst LM, Thrall PH (2012) Geographic adaptation in plant–soil mutualisms: tests using Acacia spp. and rhizobial bacteria. Funct Ecol 26:457–468. https://doi.org/10.1111/j.1365-2435.2011.01940.x
Bates DM, Machler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Beckstead J, Parker IM (2003) Invasiveness of Ammophila arenaria: release from soil-borne pathogens? Ecology 84:2824–2831
Bennett JA, Klironomos J (2019) Mechanisms of plant–soil feedback: interactions among biotic and abiotic drivers. New Phytol 222:91–96. https://doi.org/10.1111/nph.15603
Bever JD (2002) Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Proc Biol Sci 269:2595–2601. https://doi.org/10.1098/rspb.2002.2162
Bever JD (2003) Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol 157:465–473. https://doi.org/10.1046/j.1469-8137.2003.00714.x
Bever JD, Westover KM, Antonovics J (1997) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J Ecol 85:561–573. https://doi.org/10.2307/2960528
Birnbaum C, Bissett A, Thrall PH, Leishman MR (2016) Nitrogen-fixing bacterial communities in invasive legume nodules and associated soils are similar across introduced and native range populations in Australia. J Biogeogr 43:1631–1644. https://doi.org/10.1111/jbi.12752
Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77. https://doi.org/10.1007/s11104-008-9877-9
Bunn RA, Ramsey PW, Lekberg Y (2015) Do native and invasive plants differ in their interactions with arbuscular mycorrhizal fungi? A meta-analysis. J Ecol 103:1547–1556. https://doi.org/10.1111/1365-2745.12456
Caldwell BA (2006) Effects of invasive scotch broom on soil properties in a Pacific coastal prairie soil. Appl Soil Ecol 32:149–152. https://doi.org/10.1016/j.apsoil.2004.11.008
Callaway RM, Thelen GC, Barth S, Ramsey PW, Gannon JE (2004) Soil Fungi Alter interactions between the invader Centaurea Maculosa and north American natives. Ecology 85:1062–1071. https://doi.org/10.1890/02-0775
Cappuccino N (2004) Allee effect in an invasive alien plant, pale swallow-wort Vincetoxicum rossicum (Asclepiadaceae). Oikos 106:3–8. https://doi.org/10.1111/j.0030-1299.2004.12863.x
Chen L, Zheng Y, Gao C, Mi XC, Ma KP, Wubet T, Guo LD (2017) Phylogenetic relatedness explains highly interconnected and nested symbiotic networks of woody plants and arbuscular mycorrhizal fungi in a Chinese subtropical forest. Mol Ecol 26:2563–2575. https://doi.org/10.1111/mec.14061
Crawford KM, Bauer JT, Comita LS, Eppinga MB, Johnson DJ, Mangan SA, Queenborough SA, Strand AE, Suding KN, Umbanhowar J, Bever JD (2019) When and where plant-soil feedback may promote plant coexistence: a meta-analysis. Ecol Lett 22:1274–1284. https://doi.org/10.1111/ele.13278
Davison J, Öpik M, Daniell TJ, Moora M, Zobel M (2011) Arbuscular mycorrhizal fungal communities in plant roots are not random assemblages. FEMS Microbiol Ecol 78:103–115. https://doi.org/10.1111/j.1574-6941.2011.01103.x
Davison J, Moora M, Öpik M et al (2015) Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349:970–973. https://doi.org/10.1126/science.aab1161
Diez JM, Dickie I, Edwards G, Hulme PE, Sullivan JJ, Duncan RP (2010) Negative soil feedbacks accumulate over time for non-native plant species. Ecol Lett 13:803–809. https://doi.org/10.1111/j.1461-0248.2010.01474.x
Ehrenfeld JG, Ravit B, Elgersma K (2005) Feedback in the plant-soil system. Annu Rev Environ Resour 30:75–115. https://doi.org/10.1146/annurev.energy.30.050504.144212
Elton CS (2000) The ecology of invasions by animals and plants. University of Chicago Press
Farr DF, Bills GF, Chamuris GP, Rossman AY (1989) Fungi on plants and plant products in the United States. Fungi Plants Plant Prod U S
Flory SL, Clay K (2013) Pathogen accumulation and long-term dynamics of plant invasions. J Ecol 101:607–613. https://doi.org/10.1111/1365-2745.12078
Goss EM, Kendig AE, Adhikari A et al (2020) Disease in invasive plant populations. Annual review of phytopathology 58:null. https://doi.org/10.1146/annurev-phyto-010820-012757
Grove S, Haubensak KA, Parker IM (2012) Direct and indirect effects of allelopathy in the soil legacy of an exotic plant invasion. Plant Ecol 213:1869–1882
Grove S, Parker IM, Haubensak KA (2015) Persistence of a soil legacy following removal of a nitrogen-fixing invader. Biol Invasions 17:2621–2631. https://doi.org/10.1007/s10530-015-0900-9
Grove S, Parker IM, Haubensak KA (2017) Do impacts of an invasive nitrogen-fixing shrub on Douglas-fir and its ectomycorrhizal mutualism change over time following invasion? J Ecol 105:1687–1697. https://doi.org/10.1111/1365-2745.12764
Grove S, Saarman NP, Gilbert GS, Faircloth B, Haubensak KA, Parker IM (2019) Ectomycorrhizas and tree seedling establishment are strongly influenced by forest edge proximity but not soil inoculum. Ecol Appl 29:e01867. https://doi.org/10.1002/eap.1867
Gustafson DJ, Casper BB (2004) Nutrient addition affects AM fungal performance and expression of plant/fungal feedback in three serpentine grasses. Plant Soil 259:9–17. https://doi.org/10.1023/B:PLSO.0000020936.56786.a4
Halekoh U, Højsgaard S (2014) A Kenward-Roger approximation and parametric bootstrap methods for tests in linear mixed models – the R package pbkrtest. Journal of Statistical Software 59:1–32. https://doi.org/10.18637/jss.v059.i09
Harley JL, Harley EL (1987) A check-list of Mycorrhiza in the British Flora—addenda, errata and index. New Phytol 107:741–749. https://doi.org/10.1111/j.1469-8137.1987.tb00912.x
Harrison TL, Simonsen AK, Stinchcombe JR, Frederickson ME (2018) More partners, more ranges: generalist legumes spread more easily around the globe. Biol Lett 14:20180616. https://doi.org/10.1098/rsbl.2018.0616
Haubensak KA, Parker IM (2004) Soil changes accompanying invasion of the exotic shrub Cytisus scoparius in glacial outwash prairies of Western Washington [USA]. Plant Ecol 175:71–79
Haubensak KA, Grove S, Foster J, Parker IM (2020) Chemical and mechanical control of the invasive shrub Cytisus scoparius in forest clearings in western Washington, USA. Invasive Plant Science and Management 13:30–36. https://doi.org/10.1017/inp.2020.1
Hooper DU, Vitousek PM (1998) Effects of plant composition and diversity on nutrient cycling. Ecol Monogr 68:121–149. https://doi.org/10.1890/0012-9615(1998)068[0121:EOPCAD]2.0.CO;2
Horn K, Parker IM, Malek W, Rodríguez-Echeverría S, Parker MA (2014) Disparate origins of Bradyrhizobium symbionts for invasive populations of Cytisus scoparius (Leguminosae) in North America. FEMS Microbiol Ecol 89:89–98. https://doi.org/10.1111/1574-6941.12335
Inderjit, Cahill JF (2015) Linkages of plant–soil feedbacks and underlying invasion mechanisms. AoB PLANTS 7. https://doi.org/10.1093/aobpla/plv022
Inderjit, van der Putten WH (2010) Impacts of soil microbial communities on exotic plant invasions. Trends Ecol Evol 25:512–519. https://doi.org/10.1016/j.tree.2010.06.006
Johnson NC, Graham JH, Smith FA (1997) Functioning of Mycorrhizal associations along the mutualism-parasitism continuum. The New Phyt 135:575–586. https://doi.org/10.1046/j.1469-8137.1997.00729.x
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170. https://doi.org/10.1016/S0169-5347(02)02499-0
Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70. https://doi.org/10.1038/417067a
Kulmatiski A, Kardol P (2008) Getting plant—soil feedbacks out of the greenhouse: experimental and conceptual approaches. In: Lüttge U, Beyschlag W, Murata J (eds) Progress in botany. Springer, Berlin Heidelberg, Berlin, Heidelberg, pp 449–472
Kulmatiski A, Beard KH, Stevens JR, Cobbold SM (2008) Plant-soil feedbacks: a meta-analytical review. Ecol Lett 11:980–992. https://doi.org/10.1111/j.1461-0248.2008.01209.x
Lafay B, Burdon JJ (2006) Molecular diversity of rhizobia nodulating the invasive legume Cytisus scoparius in Australia. J Appl Microbiol 100:1228–1238. https://doi.org/10.1111/j.1365-2672.2006.02902.x
Lau JA, Suwa T (2016) The changing nature of plant–microbe interactions during a biological invasion. Biol Invasions 18:3527–3534. https://doi.org/10.1007/s10530-016-1245-8
Leary JK, Singleton PW, Scowcroft PG, Borthakur D (2006) Symbiotic diversity in the cosmopolitan genus Acacia Symbiosis 4 107-117 4:117
Lekberg Y, Bever JD, Bunn RA, Callaway RM, Hart MM, Kivlin SN, Klironomos J, Larkin BG, Maron JL, Reinhart KO, Remke M, van der Putten WH (2018) Relative importance of competition and plant-soil feedback, their synergy, context dependency and implications for coexistence. Ecol Lett 21:1268–1281. https://doi.org/10.1111/ele.13093
Lenth R (2018) Least-squares means. Comprehensive R Archive Network
LeRoux JJ, Ellis AG, van Zyl L-M et al (2018) Importance of soil legacy effects and successful mutualistic interactions during Australian acacia invasions in nutrient-poor environments. J Ecol 106:2071–2081. https://doi.org/10.1111/1365-2745.12965
Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989. https://doi.org/10.1111/j.1461-0248.2004.00657.x
Liang M, Liu X, Etienne RS, Huang F, Wang Y, Yu S (2015) Arbuscular mycorrhizal fungi counteract the Janzen-Connell effect of soil pathogens. Ecology 96:562–574. https://doi.org/10.1890/14-0871.1
Liang M, Liu X, Gilbert GS, Zheng Y, Luo S, Huang F, Yu S (2016) Adult trees cause density-dependent mortality in conspecific seedlings by regulating the frequency of pathogenic soil fungi. Ecol Lett 19:1448–1456. https://doi.org/10.1111/ele.12694
Lucero JE, Schaffner U, Asadi G, Bagheri A, Rajabov T, Callaway RM (2019) Enemy release from the effects of generalist granivores can facilitate Bromus tectorum invasion in the Great Basin desert. Ecology and Evolution 9:8490–8499. https://doi.org/10.1002/ece3.5314
Manning P, Morrison SA, Bonkowski M, Bardgett RD (2008) Nitrogen enrichment modifies plant community structure via changes to plant–soil feedback. Oecologia 157:661–673. https://doi.org/10.1007/s00442-008-1104-0
Marler MJ, Zabinski CA, Callaway RM (1999) Mycorrhizae indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology 80:1180–1186. https://doi.org/10.1890/0012-9658(1999)080[1180:MIECEO]2.0.CO;2
Meisner A, Gera Hol WH, de Boer W, Krumins JA, Wardle DA, van der Putten WH (2014) Plant–soil feedbacks of exotic plant species across life forms: a meta-analysis. Biol Invasions 16:2551–2561. https://doi.org/10.1007/s10530-014-0685-2
Miller EC, Perron GG, Collins CD (2019) Plant-driven changes in soil microbial communities influence seed germination through negative feedbacks. Ecol Evol 9:9298–9311. https://doi.org/10.1002/ece3.5476
Mills KE, Bever JD (1998) Maintenance of diversity within plant communities: soil pathogens as agents of negative feedback. Ecology 79:1595–1601. https://doi.org/10.1890/0012-9658(1998)079[1595:MODWPC]2.0.CO;2
Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627. https://doi.org/10.1038/nature01317
Mitchell CE, Agrawal AA, Bever JD et al (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740. https://doi.org/10.1111/j.1461-0248.2006.00908.x
Moora M, Berger S, Davison J, Öpik M, Bommarco R, Bruelheide H, Kühn I, Kunin WE, Metsis M, Rortais A, Vanatoa A, Vanatoa E, Stout JC, Truusa M, Westphal C, Zobel M, Walther GR (2011) Alien plants associate with widespread generalist arbuscular mycorrhizal fungal taxa: evidence from a continental-scale study using massively parallel 454 sequencing. J Biogeogr 38:1305–1317. https://doi.org/10.1111/j.1365-2699.2011.02478.x
Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142. https://doi.org/10.1111/j.2041-210x.2012.00261.x
Ndlovu J, Richardson DM, Wilson JRU, Roux JJL (2013) Co-invasion of south African ecosystems by an Australian legume and its rhizobial symbionts. J Biogeogr 40:1240–1251. https://doi.org/10.1111/jbi.12091
Nijjer S, Rogers WE, Siemann E (2007) Negative plant–soil feedbacks may limit persistence of an invasive tree due to rapid accumulation of soil pathogens. Proc R Soc B Biol Sci 274:2621–2627. https://doi.org/10.1098/rspb.2007.0804
Nuñez MA, Dickie IA (2014) Invasive belowground mutualists of woody plants. Biol Invasions 16:645–661. https://doi.org/10.1007/s10530-013-0612-y
Nuñez MA, Horton TR, Simberloff D (2009) Lack of belowground mutualisms hinders Pinaceae invasions. Ecology 90:2352–2359. https://doi.org/10.1890/08-2139.1
Parker IM (2000) Invasion dynamics of Cytisus Scoparius: a matrix model approach. Ecol Appl 10:726–743. https://doi.org/10.1890/1051-0761(2000)010[0726:IDOCSA]2.0.CO;2
Parker IM, Gilbert GS (2007) When there is no escape: the effects of natural enemies on native, invasive, and noninvasive plants. Ecology 88:1210–1224. https://doi.org/10.1890/06-1377
Parker IM, Simberloff D, Lonsdale WM, Goodell K, Wonham M, Kareiva PM, Williamson MH, von Holle B, Moyle PB, Byers JE, Goldwasser L (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biol Invasions 1:3–19. https://doi.org/10.1023/A:1010034312781
Parker MA, Malek W, Parker IM (2006) Growth of an invasive legume is symbiont limited in newly occupied habitats. Divers Distrib 12:563–571. https://doi.org/10.1111/j.1366-9516.2006.00255.x
Paynter Q, Csurhes SM, Heard TA, Ireson J, Julien MH, Lloyd J, Lonsdale WM, Palmer WA, Sheppard AW, Klinken RD (2003) Worth the risk? Introduction of legumes can cause more harm than good: an Australian perspective. Aust Syst Bot 16:81–88. https://doi.org/10.1071/sb01025
Petermann JS, Fergus AJF, Turnbull LA, Schmid B (2008) Janzen-Connell effects are widespread and strong enough to maintain diversity in grasslands. Ecology 89:2399–2406. https://doi.org/10.1890/07-2056.1
Peterson DJ, Prasad R (1998) The biology of Canadian weeds. 109. Cytisus scoparius (L.) link. Can J Plant Sci 78:497–504. https://doi.org/10.4141/P97-079
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–IN18. https://doi.org/10.1016/S0007-1536(70)80110-3
Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN (2009) Mycorrhizal symbioses and plant invasions. Annu Rev Ecol Evol Syst 40:699–715. https://doi.org/10.1146/annurev.ecolsys.39.110707.173454
R Core Team (2018) R: language and environment for statsitical computing. R foundation for Statistical Computing, Vienna, Austria http://www.R-project.org/
Rapparini F, Peñuelas J (2014) Mycorrhizal fungi to alleviate drought stress on plant growth. In Use of Microbes for the Alleviation of Soil Stresses, Volume 1 (pp. 21-42). Springer, New York, NY
Reinhart KO, Callaway RM (2004) Soil biota facilitate exotic Acer invasions in Europe and North America. Ecol Appl 14:1737–1745. https://doi.org/10.1890/03-5204
Reinhart KO, Callaway RM (2006) Soil biota and invasive plants. New Phytol 170:445–457. https://doi.org/10.1111/j.1469-8137.2006.01715.x
Reinhart KO, Tytgat T, der Putten WHV, Clay K (2010) Virulence of soil-borne pathogens and invasion by Prunus serotina. New Phytol 186:484–495. https://doi.org/10.1111/j.1469-8137.2009.03159.x
Richardson DM, Allsopp N, D’antonio CM et al (2000) Plant invasions – the role of mutualisms. Biol Rev 75:65–93. https://doi.org/10.1017/S0006323199005435
Richardson DM, Carruthers J, Hui C, Impson FAC, Miller JT, Robertson MP, Rouget M, le Roux JJ, Wilson JRU (2011) Human-mediated introductions of Australian acacias – a global experiment in biogeography. Divers Distrib 17:771–787. https://doi.org/10.1111/j.1472-4642.2011.00824.x
Rodríguez-Echeverría S, Crisóstomo JA, Freitas H (2007) Genetic diversity of rhizobia associated with Acacia longifolia in two stages of invasion of coastal sand dunes. Appl Environ Microbiol 73:5066–5070. https://doi.org/10.1128/AEM.00613-07
Sajnaga E, Małek W, Łotocka B, Stepkowski T, Legocki A (2001) The root-nodule symbiosis between Sarothamnus scoparius L. and its microsymbionts. Antonie Van Leeuwenhoek 79:385–391. https://doi.org/10.1023/A:1012010328061
Schnitzer SA, Klironomos JN, HilleRisLambers J, Kinkel LL, Reich PB, Xiao K, Rillig MC, Sikes BA, Callaway RM, Mangan SA, van Nes EH, Scheffer M (2011) Soil microbes drive the classic plant diversity–productivity pattern. Ecology 92:296–303. https://doi.org/10.1890/10-0773.1
Schroeder JW, Martin JT, Angulo DF (2019) Host plant phylogeny and abundance predict root-associated fungal community composition and diversity of mutualists and pathogens. J Ecol 107:1557–1566. https://doi.org/10.1111/1365-2745.13166
Schulze J (2004) How are nitrogen fixation rates regulated in legumes? J Plant Nutr Soil Sci 167:125–137. https://doi.org/10.1002/jpln.200320358
Seifert EK, Bever JD, Maron JL (2009) Evidence for the evolution of reduced mycorrhizal dependence during plant invasion. Ecology 90:1055–1062. https://doi.org/10.1890/08-0419.1
Shaben J, Myers JH (2010) Relationships between scotch broom (Cytisus scoparius), soil nutrients, and plant diversity in the Garry oak savannah ecosystem. Plant Ecol 207:81–91. https://doi.org/10.1007/s11258-009-9655-7
Shah MA, Reshi ZA, Khasa DP (2009) Arbuscular Mycorrhizas: drivers or passengers of alien plant invasion. Bot Rev 75:397–417. https://doi.org/10.1007/s12229-009-9039-7
Simonsen AK, Dinnage R, Barrett LG, Prober SM, Thrall PH (2017) Symbiosis limits establishment of legumes outside their native range at a global scale. Nat Commun 8:14790. https://doi.org/10.1038/ncomms14790
Slabbert E, Jacobs SM, Jacobs K (2014) The soil bacterial communities of south African Fynbos riparian ecosystems invaded by Australian Acacia species. PLoS One 9:e86560. https://doi.org/10.1371/journal.pone.0086560
Smith SE, Read DJ (2010) Mycorrhizal Symbiosis. Academic Press
Sofaer HR, Jarnevich CS, Pearse IS (2018) The relationship between invader abundance and impact. Ecosphere 9:e02415. https://doi.org/10.1002/ecs2.2415
Stark JM, Norton JM (2015) The invasive annual cheatgrass increases nitrogen availability in 24-year-old replicated field plots. Oecologia 177:799–809. https://doi.org/10.1007/s00442-014-3093-5
Suding KN, Harpole WS, Fukami T, Kulmatiski A, MacDougall AS, Stein C, van der Putten WH (2013) Consequences of plant–soil feedbacks in invasion. J Ecol 101:298–308. https://doi.org/10.1111/1365-2745.12057
Sweetingham M (1984) Pleiochaeta setosa — a root pathogen of lupins. Australas Plant Pathol 13:21–22. https://doi.org/10.1071/APP9840021
Taylor CM, Hastings A (2005) Allee effects in biological invasions. Ecol Lett 8:895–908. https://doi.org/10.1111/j.1461-0248.2005.00787.x
terHorst CP, Wirth C, Lau JA (2018) Genetic variation in mutualistic and antagonistic interactions in an invasive legume. Oecologia 188:159–171. https://doi.org/10.1007/s00442-018-4211-6
Thrall PH, Burdon JJ, Woods MJ (2000) Variation in the effectiveness of symbiotic associations between native rhizobia and temperate Australian legumes: interactions within and between genera. J Appl Ecol 37:52–65. https://doi.org/10.1046/j.1365-2664.2000.00470.x
van der Heijden MG, de Bruin S, Luckerhoff L et al (2016) A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment. ISME J 10:389–399. https://doi.org/10.1038/ismej.2015.120
van der Putten WH, Dijk CK, Peters BAM (1993) Plant-specific soil-borne diseases contribute to succession in foredune vegetation. Nature 362:53–56. https://doi.org/10.1038/362053a0
van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, van de Voorde TFJ, Wardle DA (2013) Plant-soil feedbacks: the past, the present and future challenges. J Ecol Oxf 101:265–276
Veresoglou SD, Rillig MC (2012) Suppression of fungal and nematode plant pathogens through arbuscular mycorrhizal fungi. Biol Lett 8:214–217. https://doi.org/10.1098/rsbl.2011.0874
Vitousek PM, Walker LR, Whiteaker LD, Mueller-Dombois D (1987) Biological invasion by Myrica faya alters ecosystem development in Hawaii. Science 238:802–804. https://doi.org/10.1126/science.238.4828.802
Wandrag EM, Sheppard A, Duncan RP, Hulme PE (2013) Reduced availability of rhizobia limits the performance but not invasiveness of introduced Acacia. J Ecol 101:1103–1113. https://doi.org/10.1111/1365-2745.12126
Weir BS, Turner SJ, Silvester WB, Park D, Young JM (2004) Unexpectedly diverse Mesorhizobium strains and rhizobium leguminosarum Nodulate native legume genera of New Zealand, while introduced legume weeds are Nodulated by Bradyrhizobium species. Appl Environ Microbiol 70:5980–5987. https://doi.org/10.1128/AEM.70.10.5980-5987.2004
Westover KM, Bever JD (2001) Mechanisms of plant species coexistence: roles of rhizosphere bacteria and root fungal pathogens. Ecology 82:3285–3294. https://doi.org/10.1890/0012-9658(2001)082[3285:MOPSCR]2.0.CO;2
Wickham, H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag New York. http://ggplot2.org
Zhang Q, Yang R, Tang J, Yang H, Hu S, Chen X (2010) Positive feedback between Mycorrhizal Fungi and plants influences plant invasion success and resistance to invasion. PLoS One 5:e12380. https://doi.org/10.1371/journal.pone.0012380
Zhang P, Li B, Wu J, Hu S (2019) Invasive plants differentially affect soil biota through litter and rhizosphere pathways: a meta-analysis. Ecol Lett 22:200–210. https://doi.org/10.1111/ele.13181
Acknowledgements
We would like to thank Michelle and Dick Grove, Kyle Gern, Gregory Gilbert, and the UCSC greenhouse staff for assistance, Erin Aiello for creating our experimental design schematic, and to Karen Tanner and Zack Shearin for comments on the manuscript. This work was supported by NSF grants DEB 1354985 to KAH, IMP, and SG and DEB 1655896 to IMP.
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Davis, E.J., Grove, S., Haubensak, K.A. et al. A widespread nitrogen-fixing invader experiences negative soil feedbacks despite enhancing the abundance of beneficial soil microbes. Plant Soil 462, 257–271 (2021). https://doi.org/10.1007/s11104-020-04804-w
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DOI: https://doi.org/10.1007/s11104-020-04804-w