Abstract
Background and aims
Native shrub species of southern California have a long history of displacement by exotic annual herbs and forbs. Such invasions may be mediated by interactions with the microbial community and changes in the N cycle as a result of N pollution. However, the simultaneous effects of the soil microbial community status and N fertilization on dominant native and exotic plant species growth have not been thoroughly explored in this ecosystem.
Methods
Three species of native shrubs and of exotic annuals were grown in an orthogonal two-factor greenhouse experiment. To assess the importance of the soil microbial community pre-sterilized soils were inoculated with sterilized or non-sterilized field soil; to assess the importance of N type pots were fertilized with nitrate, ammonium or glycine solutions. Plant shoot and root biomass was measured after harvesting.
Results
The natives Artemisia californica and Eriogonum fasciculatum had lower growth in sterilized soil, suggesting microbial facilitation of these species, and E. fasciculatum higher growth with ammonia than either nitrate or glycine. Salvia apiana had equal growth under all conditions. The exotics Brassica nigra and Bromus madritensis grew equally in sterilized and unsterilized soil, and B. madritensis greater growth with ammonia fertilizer. Centaurea melitensis had greater growth in sterilized soil, and with either form of inorganic N.
Conclusions
These results highlight the importance of the soil microbial community in contributing to relative success of native vs. exotic species, and could inform restoration approaches for these species.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11104-013-1668-2/MediaObjects/11104_2013_1668_Fig1_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11104-013-1668-2/MediaObjects/11104_2013_1668_Fig2_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11104-013-1668-2/MediaObjects/11104_2013_1668_Fig3_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11104-013-1668-2/MediaObjects/11104_2013_1668_Fig4_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11104-013-1668-2/MediaObjects/11104_2013_1668_Fig5_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11104-013-1668-2/MediaObjects/11104_2013_1668_Fig6_HTML.gif)
Similar content being viewed by others
References
Allen EB, Padgett PE, Bytnerowicz A, Minnich R (1996) Nitrogen deposition effects on coastal sage vegetation of Southern California. In: Bytnerowicz A, Arbaugh M, Schilling S (eds) Proceedings of the International Symposium on Air Pollution and Climate Change Effects on Forest Ecosystems. Pacific Southwest Research Station, USDA Forest Service, Riverside, California, Albany, pp 131–139
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
Bottomley PJ (1994) Light microscopic methods for studying soil microorganisms. Methods of soil analysis: part 2—Microbiological and biochemical properties SSSA book series, 81-105
Bowler PA (2000) Ecological restoration of coastal sage scrub and its potential role in habitat conservation plans. Environ Manag 26:S85–S96
Bozzolo F (2012) Nitrogen relations among plant species in a semi-arid shrubland: impacts of invasion and plant-soil feedbacks. Dissertation, San Diego State University, San Diego, CA, USA
Callaway R, Newingham B, Zabinski CA, Mahall BE (2001) Compensatory growth and competitive ability of an invasive weed are enhanced by soil fungi and native neighbours. Ecol Lett 4:429–433
Callaway RM, Mahall BE, Wicks C, Pankey J, Zabinski C (2003) Soil fungi and the effects of an invasive forb on grasses: neighbor identity matters. Ecology 84:129–135
Callaway RM, Thelen G, Rodriguez A, Holben W (2004) Soil biota and exotic plant invasion. Nature 427:731–733
Camprubí A, Estaun V, Calvet C, Pera J (1990) Infectivity and effectivity of Glomus mosseae mycorrhizae in four different species of medicinal plants. Symbiosis (Rehovot) 9:305–307
Costacurta A, Vanderleyden J (1995) Synthesis of phytohormones by plant-associated bacteria. Crit Rev Microbiol 21:1–18
Daehler CC (2003) Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restoration. Annu Rev Ecol Evol Syst 34:183–211
Diffenbaugh NS, Giorgi F, Pal JS (2008) Climate change hotspots in the United States. Geophys Res Lett 35:L16709
Dobson AP, Rodriguez JP, Roberts WM, Wilcove DS (1997) Geographic distribution of endangered species in the United States. Science 275:550–553
Drew MC (1975) Comparison of the effects of a localized pupply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytol 75:479–490
Egerton-Warburton LM, Allen EB (2000) Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient. Ecol Appl 10:484–496
Egerton-Warburton LM, Querejeta JI, Allen MF (2007) Common mycorrhizal networks provide a potential pathway for the transfer of hydraulically lifted water between plants. J Exp Bot 58:1473–1483
Ehrenfeld JG, Scott N (2001) Invasive species and the soil: effects on organisms and ecosystem processes. Ecol Appl 11:1259–1260
Ehrenfeld JG, Ravit B, Elgersma K (2005) Feedback in the plant-soil system. Annu Rev Environ Resour 30:75–115
Frank DA, Groffman PM (2009) Plant rhizospheric N processes: what we don’t know and why we should care. Ecology 90:1512–1519
Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–233
Gai J, Christie P, Feng G, Li X (2006) Twenty years of research on community composition and species distribution of arbuscular mycorrhizal fungi in China: a review. Mycorrhiza 16:229–239
Geneva MP, Stancheva IV, Boychinova MM, Mincheva NH, Yonova PA (2010) Effects of foliar fertilization and arbuscular mycorrhizal colonization on Salvia officinalis L. growth, antioxidant capacity, and essential oil composition. J Sci Food Agric 90:696–702
Glenn MG, Chew FS, Williams PH (1985) Hyphal penetration of Brassica (Cruciferae) roots by a vesicular-arbuscular mycorrhizal fungus. New Phytol 99:463–472
Glenn MG, Chew FS, Williams PH (1988) Influence of glucosinolate content of Brassica (Cruciferae) roots on growth of vesicular-arbuscular mycorrhizal fungi. New Phytol 110:217–225
Glick BR (1995) The enhancement of plant growth by free-living bacteria. Rev Can Microbiol 41:109–117
Gordon DR (1998) Effects of invasive, non-indigenous plant species on ecosystem processes: lessons from Florida. Ecol Appl 8:975–989
Guo Q (2001) Early post-fire succession in California chaparral: changes in diversity, density, cover and biomass. Ecol Res 16:471–485
Haichar FZ, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230
James JJ, Davies KW, Sheley RL, Aanderud ZT (2008) Linking nitrogen partitioning and species abundance to invasion resistance in the Great Basin. Oecologia 156:637–648
Keeley JE, Keeley SC (1984) Postfire recovery of California coastal sage scrub. Am Midl Nat 111:105–117
Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70
Lake JC, Leishman MR (2004) Invasion success of exotic plants in natural ecosystems: the role of disturbance, plant attributes and freedom from herbivores. Biol Conserv 117:215–226
Lea PJ, Azevedo RA (2006) Nitrogen use efficiency. 1. Uptake of nitrogen from the soil. Ann Appl Biol 149:243–247
Lundgren DG, Silver M (1980) Ore leaching by bacteria. Annu Rev Microbiol 34:263–283
Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710
Matson PA, Vitousek PM (1981) Nitrogen mineralization and nitrification potentials following clearcutting in the Hoosier National Forest, Indiana. For Sci 27:781–791
Minnich RA, Dezzani RJ (1998) Historical decline of coastal sage scrub in the Riverside-Perris Plain, California. West Birds 29:366–391
Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytol 182:31–48
Nord EA, Lynch JP (2009) Plant phenology: a critical controller of soil resource acquisition. J Exp Bot 60:1927–1937
Norton J, Monaco T, Norton U (2007) Mediterranean annual grasses in western North America: kids in a candy store. Plant Soil 298:1–5
O’Connor PJ, Smith SE, Smith FA (2002) Arbuscular mycorrhizas influence plant diversity and community structure in a semiarid herbland. New Phytol 154:209–218
Öpik M, Moora M, Liira J, Kõljalg U, Zobel M, Sen R (2003) Divergent arbuscular mycorrhizal fungal communities colonize roots of Pulsatilla spp. in boreal Scots pine forest and grassland soils. New Phytol 160:581–593
Padgett PE, Allen EB (1999) Differential responses to nitrogen fertilization in native shrubs and exotic annuals common to mediterranean coastal sage scrub of California. Plant Ecol 144:93–101
Quantin C, Becquer T, Rouiller JH, Berthelin J (2001) Oxide weathering and trace metal release by bacterial reduction in a New Caledonia Ferralsol. Biogeochemistry 53:323–340
Reasoner DJ, Geldreich EE (1985) A new medium for the enumeration and subculture of bacteria from potable water. Appl Environ Microbiol 49:1–7
Requena N, Perez-Solis E, Azcon-Aguilar C, Jeffries P, Barea J-M (2001) Management of indigenous plant-microbe symbioses aids restoration of desertified ecosystems. Appl Environ Microbiol 67:495–498
Richter BS, Stutz JC (2002) Mycorrhizal inoculation of big sacaton: implications for grassland restoration of abandoned agricultural fields. Restor Ecol 10:607–616
Rinaldi MG (1982) Use of potato flakes agar in clinical mycology. J Clin Microbiol 15:1159–1160
Schmidt SK, Lipson DA, Ley RE, Fisk MC, West AE (2004) Impacts of chronic nitrogen additions vary seasonally and by microbial functional group in tundra soils. Biogeochemistry 69:1–17
Schreiner RP, Koide RT (1993) Mustards, mustard oils and mycorrhizas. New Phytol 123:107–113
Seifert EK, Bever JD, Maron JL (2009) Evidence for the evolution of reduced mycorrhizal dependence during plant invasion. Ecology 90:1055–1062
Sigüenza C, Corkidi L, Allen E (2006a) Feedbacks of soil inoculum of mycorrhizal fungi altered by N deposition on the growth of a native shrub and an invasive annual grass. Plant Soil 286:153–165
Sigüenza C, Crowley DE, Allen EB (2006b) Soil microorganisms of a native shrub and exotic grasses along a nitrogen deposition gradient in southern California. Appl Soil Ecol 32:13–26
Silvertown J (2004) Plant coexistence and the niche. Trends Ecol Evol 19:605–611
Sims GK, Wander MM (2002) Proteolytic activity under nitrogen or sulfur limitation. Appl Soil Ecol 19:217–221
Smith MR, Charvat I, Jacobson RL (1998) Arbuscular mycorrhizae promote establishment of prairie species in a tallgrass prairie restoration. Can J Bot 76:1947–1954
Stylinski CD, Allen EB (1999) Lack of native species recovery following severe exotic disturbance in southern Californian shrublands. J Appl Ecol 36:544–554
Suding KN, Gross KL, Houseman GR (2004) Alternative states and positive feedbacks in restoration ecology. Trends Ecol Evol 19:46–53
Swenson JJ, Franklin J (2000) The effects of future urban development on habitat fragmentation in the Santa Monica Mountains. Landsc Ecol 15:713–730
Trevors JT (1996) Sterilization and inhibition of microbial activity in soil. J Microbiol Methods 26:53–59
Uroz S, Buée M, Murat C, Frey-Klett P, Martin F (2010) Pyrosequencing reveals a contrasted bacterial diversity between oak rhizosphere and surrounding soil. Environ Microbiol Rep 2:281–288
van der Putten WH, Klironomos JN, Wardle DA (2007) Microbial ecology of biological invasions. ISME J 1:28–37
van Grunsven RHA, van der Putten WH, Bezemer TM, Tamis WLM, Berendse F, Veenendaal EM (2007) Reduced plant–soil feedback of plant species expanding their range as compared to natives. J Ecol 95:1050–1057
Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115
Vitousek PM, Matson PA (1985) Disturbance, nitrogen availability, and nitrogen losses in an intensively managed loblolly pine plantation. Ecology 66:1360–1376
Vitousek PM, Gosz JR, Grier CC, Melillo JM, Reiners WA, Todd RL (1979) Nitrate losses from disturbed ecosystems. Science 204:469–474
Vitousek PM, D’Antonio CM, Loope LL, Rejmánek M, Westbrooks R (1997) Introduced species: a significant component of human-caused global change. N Z J Ecol 21:1–16
Vogelsang KM, Bever JD, Griswold M, Schultz PA (2004) The use of mycorrhizal fungi in erosion control applications. Final Report for Caltrans. Contract number 65A0070. California Department of Transportation, Sacramento, CA
Walch-Liu P, Liu L-H, Remans T, Tester M, Forde BG (2006) Evidence that L-glutamate can act as an exogenous signal to modulate root growth and branching in Arabidopsis thaliana. Plant Cell Physiol 47:1045–1057
Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633
Westman WE (1981) Diversity relations and succession in Californian coastal sage scrub. Ecology 62:170–184
Wilson GWT, Hartnett DC, Smith MD, Kobbeman K (2001) Effects of mycorrhizae on growth and demography of tallgrass prairie forbs. Am J Bot 88:1452–1457
Wolfe BE, Klironomos JN (2005) Breaking new ground: soil communities and exotic plant invasion. Bioscience 55:477–487
Wolkovich EM, Cleland EE (2010) The phenology of plant invasions: a community ecology perspective. Front Ecol Environ 9:287–294
Yoshida LC, Allen EB (2001) Response to ammonium and nitrate by a mycorrhizal annual invasive grass and native shrub in southern California. Am J Bot 88:1430–1436
Yoshida LC, Allen EB (2004) 15N uptake by mycorrhizal native and invasive plants from a N-eutrophied shrubland: a greenhouse experiment. Biol Fertil Soils 39:243–248
Zachara JM, Fredrickson JK, Smith SC, Gassman PL (2001) Solubilization of Fe(III) oxide-bound trace metals by a dissimilatory Fe(III) reducing bacterium. Geochim Cosmochim Acta 65:75–93
Zak DR, Groffman PM, Pregitzer KS, Christensen S, Tiedje JM (1990) The vernal dam: plant-microbe competition for nitrogen in northern hardwood forests. Ecology 71:651–656
Zedler JB, Kercher S (2004) Causes and consequences of invasive plants in wetlands: opportunities, opportunists, and outcomes. Crit Rev Plant Sci 23:431–452
Zink TA, Allen MF, Heindl-Tenhunen B, Allen EB (1995) The effect of a disturbance corridor on an ecological reserve. Restor Ecol 3:304–310
Acknowledgments
We thank J. Franklin for much valuable support and feedback; the Soil Ecology and Restoration Group for assistance and the use of their greenhouse facilities; R. Smith for assistance harvesting plants; M. Mauritz, I. Hale, K. Reasor, J. Zlamal for assistance processing samples; T.P. Young for many valuable comments. This research was funded by the National Science Foundation Biological Invasions Integrative Graduate Education and Research Traineeship (NSF-IGERT DGE 0114432), and by the San Diego State University Department of Biology.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Jeff R. Powell.
Rights and permissions
About this article
Cite this article
Bozzolo, F.H., Lipson, D.A. Differential responses of native and exotic coastal sage scrub plant species to N additions and the soil microbial community. Plant Soil 371, 37–51 (2013). https://doi.org/10.1007/s11104-013-1668-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-013-1668-2