Abstract
Background and Aims
Feedbacks between plants and soil microbes can play an important role in competition between potential invaders and the resident community. However, the role of saprophytic soil microbes is poorly understood because research largely focuses on the role of specific soil-borne pathogens. Our aim was to examine the role of plant-saprophyte feedbacks in soil processes (decomposition and enzyme activities) and plant competition.
Methods
We preconditioned a common soil in microcosms by decomposing litter of four species; two exotic invasive species (Microstegium vimineum and Berberis thunbergii) and two native species (Viburnum acerifolium and Vaccinium corymbosum). We then replaced the litter with either the same species’ litter or a different species’ litter on the preconditioned soil. We measured the effect of preconditioning on subsequent litter decomposition, microbial community structure (phospholipid fatty acids) and function (soil enzyme activities and decomposition). We then grew Berberis and Viburnum seedlings in preconditioned soils under intraspecific and interspecific competition to determine whether litter preconditioning had a feedback effect on competition.
Results
Changes in microbial community structure during preconditioning persisted through time and altered subsequent soil enzyme activities and litter decomposition. These changes also affected the growth rate of two shrub species, but because both shrubs grew best in soil that previously contained Berberis litter, competition between these species was not directly affected.
Conclusions
Plant litter creates a legacy that influences the future structure of the microbial community even after that litter is gone. This legacy effect has functional consequences on decomposition and plant growth, and could be an important but under-appreciated factor in soil and plant community ecology. Further study is needed to determine how these consequences affect plant community composition and invasibility.
Similar content being viewed by others
Abbreviations
- ANOVA:
-
Analysis of variance
- FAME:
-
Fatty acid methyl ester
- L-DOPA:
-
L-dihydroxy-phenylalanine
- MANOVA:
-
Multivariate analysis of variance
- PCA:
-
Principal components analysis
- PLFA:
-
Phospholipid fatty acids
- pNP:
-
p-nitrophenyl
References
Aerts R (1997) Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79:439–449
Augspurger CK, Wilkinson HT (2007) Host specificity of pathogenic Pythium species: implications for tree species diversity. Biotropica 37:702–708
Ayers E, Steltzer H, Berg S, Wall DH (2009) Soil biota accelerate decomposition in high-elevation forests by specializing in the breakdown of litter produced by the plant species above them. J Ecol 97:901–912
Bardgett RD, Wardle DA (2010) Aboveground-belowground linkages. Oxford University Press, Oxford, p 301
Berendse F (1994) Litter decomposability - a neglected component of plant fitness. J Ecol 82:187–190
Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos JN, Moora M, Rillig MC, Stock WD, Tibbett M, Zobel M (2010) Rooting theories of plant community ecology in microbial interactions. Trends in Ecol & Evol 25:468–478
Brant JB, Myrold DD, Sulzman EW (2006) Root controls on soil microbial community structure in forest soils. Oecologia 148:650–659
Casper B, Cahill JF, Hyatt LA (1998) Above-ground competition does not alter biomass allocated to roots in Abutilon theophrasti. New Phytologist 140:231–238
Casper B, Castelli J (2007) Evaluating plant-soil feedback together with competition in a serpentine grassland. Ecol Lett 10:394–400
Chapman S, Langley J, Hart SC, Koch G (2006) Plants actively control nitrogen cycling: uncorking the microbial bottleneck. New Phytologist 169:27–34
Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner V, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Pérez-Harguindeguy N, Quested HM, Santiago LS, Wardle DA, Wright IJ, Aerts R, Allison SD, Van Bodegom PM, Brovkin V, Chatain A, Callaghan E, Gurvich DE, Kazakou E, Klein JA, Read J, Reich PB, Soudzilovskaia NA, Vaieretti MV, Westoby M (2008) Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol Lett 11:1065–1071
DeGasperis BG, Motzkin G (2007) Windows of opportunity: historical and ecological controls on Berberis thunbergii invasions. Ecol 88:3115–3125
Dorrepaal E, Cornelissen JHC, Aerts R (2007) Changing leaf litter feedbacks on plant production across contrasting sub-arctic peatland species and growth forms. Oecologia 151:251–261
Ehrenfeld J (1999) Structure and dynamics of populations of Japanese barberry (Berberis thunbergii DC.) in deciduous forests of New Jersey. Biol Invasions 1:203–213
Ehrenfeld J, Ravit B, Elgersma K (2005) Feedback in the plant-soil system. Ann Rev Environ & Resour 30:75–115
Elgersma KJ, Ehrenfeld JG, Yu S, Vor T (2011) Legacy effects overwhelm the short-term effects of exotic plant invasion and restoration on soil microbial community structure, enzyme activities, and nitrogen cycling. Oecologia 167:733–745
Elgersma KJ, Ehrenfeld JG (2011) Linear and non-linear impacts of a non-native plant invasion on soil microbial community structure and function. Biol Invasions 13:757–768
Fan FL, Zhang FS, Lu YH (2011) Linking plant identity and interspecific competition to soil nitrogen cycling through ammonia oxidizer communities. Soil Biol & Biochem 43:46–54
Fierer N, Morse JL, Berthrong S, Bernhardt ES, Jackson RB (2007) Environmental controls on the landscape-scale biogeography of stream bacterial communities. Ecol 88:2162–2173
Frostegård A, Tunlid A, Bååth E (2011) Use and misuse of PLFA measurements in soils. Soil Biol & Biochem 43:1621–1625
García-Guzmán G, Benítez-Malvido J (2003) Effect of litter on the incidence of leaf-fungal pathogens and herbivory in seedlings of the tropical tree Nectandra ambigens. J Tropi Ecol 19:171–177
Gartner TB, Cardon ZG (2004) Decomposition dynamics in mixed-species leaf litter. Oikos 104:230–246
Geng Y-P, Pan X-Y, Xu C-Y, Zhang WJ, Li B, Chen JK (2007) Plasticity and ontogenetic drift of biomass allocation in response to above- and below-ground resource availabilities in perennial herbs: a case study of Alternanthera philoxeroides. Ecol Res 22:1440–1703
Hobbie SE (1992) Effects of plant species on nutrient cycling. Trends Ecol & Evolut 7:336–339
Janvier C, Villeneuve F, Alabouvette C, Edel-Hermann V, Mateille T, Steinberg C (2007) Soil health through soil disease suppression: which strategy from descriptors to indicators? Soil Biol & Biochem 39:1–23
Jenny H (1941) Factors of soil formation. McGraw-Hill, New York
Kardol P, Bezemer TM, van der Putten WH (2006) Temporal variation in plant-soil feedback controls succession. Ecol Lett 9:1080–1088
Kardol P, Cornips NJ, van Kempen MML, Bakx-Schotman JMT, van der Putten WH (2007) Microbe-mediated plant-soil feedback causes historical contingency effects in plant community assembly. Ecol Monogr 77:147–162
Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70
Knops JMH, Bradley KL, Wedin DA (2002) Mechanisms of plant species impacts on ecosystem nitrogen cycling. Ecol Lett 5:454–466
Kourtev P, Ehrenfeld J, Häggblom M (2003) Experimental analysis of the effect of exotic and native plant species on the structure and function of soil microbial communities. Soil Biol & Biochem 35:895–905
Kourtev PS, Ehrenfeld JG, Huang WZ (1998) Effects of exotic plant species on soil properties in hardwood forests of New Jersey. Water Air & Soil Pollut 105:493–501
Kuhman TR, Pearson SM, Turner MG (2010) Effects of land-use history and the contemporary landscape on non-native plant invasion at local and regional scales in the forest-dominated southern Appalachians. Landsc Ecol 25:1433–1445
Kulmatiski A, Beard KH (2011) Long-term plant growth legacies overwhelm short-term plant growth effects on soil microbial community structure. Soil Biol & Biochem 43:823–830
Kulmatiski A, Beard KH, Stevens JR, Cobbold SM (2008) Plant–soil feedbacks: a meta-analytical review. Ecol Lett 11:980–992
Lauber C, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol & Biochem 40:2407–2415
McCarthy-Neumann S, Kobe RK (2010) Conspecific and heterospecific plant-soil feedbacks influence survivorship and growth of temperate tree seedlings. J Ecol 98:408–418
Meier CL, Keyserling K, Bowman WD (2009) Fine root inputs to soil reduce growth of a neighbouring plant via distinct mechanisms dependent on root carbon chemistry. J Ecol 97:941–949
Orwin KH, Buckland SM, Johnson D, Turner BL, Smart S, Oakley S, Bardgett RD (2010) Linkages of plant traits to soil properties and the functioning of temperate grassland. J Ecol 98:1074–1083
Orwin KH, Wardle DA (2005) Plant species composition effects on belowground properties and the resistance and resilience of the soil microflora to a drying disturbance. Plant and Soil 278:205–221
Packer A, Clay K (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404:278–281
Peay KG, Bruns TD, Kennedy PG, Bergemann SE, Garbelotto M (2007) A strong species-area relationship for eukaryotic soil microbes: island size matters for ectomycorrhizal fungi. Ecol Lett 10:470–480
Petermann JS, Fergus AJF, Turnbull LA, Schmid B (2008) Janzen-Connell effects are widespread and strong enough to maintain diversity in grasslands. Ecol 89:2399–2406
R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org
Ramette A, Tiedje JM (2007) Biogeography: an emerging cornerstone for understanding prokaryotic diversity, ecology, and evolution. Microbial Ecol 53:197–207
Reinhart KO, Callaway RM (2006) Soil biota and invasive plants. New Phytologist 170:445–457
Scherer-Lorenzen M (2008) Functional diversity affects decomposition processes in experimental grasslands. Funct Ecol 22:547–555
Schimel J, Bennet J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecol 85:591–602
Sinsabaugh RL, Reynolds H, Long TM (2000) Rapid assay for amidohydrolase (urease) activity in environmental samples. Soil Biol & Biochem 32:2095–2097
Strickland MS, Lauber C, Fierer N, Bradford MA (2009) Testing the functional significance of microbial community composition. Ecol 90:441–451
Suding KN, Larson JR, Thorsos E, Steltzer H, Bowman WD (2004) Species effects on resource supply rates: do they influence competitive interactions? Plant Ecol 175:47–58
van der Putten WH, Klironomos JN, Wardle DA (2007a) Microbial ecology of biological invasions. Int Soc Microbial Ecol J 1:28–37
van der Putten WH, Kowalchuck GA, Brinkman EP, Doodeman GTA, van der Kaaij RM, Kamp AFD, Menting FBJ, Veenendaal EM (2007b) Soil feedback of exotic savanna grass relates to pathogen absence and mycorrhizal selectivity. Ecol 88:978–988
Vivanco L, Austin AT (2008) Tree species identity alters forest litter decomposition through long-term plant and soil interactions in Patagonia, Argentina. J Ecol 96:727–736
Vogelsang KM, Bever JD (2009) Mycorrhizal densities decline in assocation with nonnative plants and contribute to plant invasion. Ecol 90:399–407
Waldrop MP, Balser TC, Firestone MK (2000) Linking microbial community composition to function in a tropical soil. Soil Biol & Biochem 32:1837–1846
Wardle DA (2006) The influence of biotic interactions on soil biodiversity. Ecol Lett 9:870–886
Wedin DA, Tilman D (1993) Competition among grasses along a nitrogen gradient: initial conditions and mechanisms of competition. Ecol Monogr 63:199–229
White DC, Davis WM, Nickels JS, King JD, Bobbie RJ (1979) Determination of the sedimentary microbial biomass by extractible lipid phosphate. Oecologia 40:51–62
Wilson SD, Tilman D (1991) Components of plant competition along an experimental gradient of nitrogen availability. Ecol 72:1050–1065
Zhang D, Hui D, Luo YQ, Zhou G (2008) Rates of litter decomposition in terrestrial ecosystems: global patterns and controlling factors. J Plant Ecol 1:85–93
Acknowledgements
I dedicate this article to the memory of my mentor and friend, Joan Ehrenfeld. Jodi Messina provided lab and field assistance, Michael Murillo at the Rutgers University High-Throughput Screening Lab helped with enzyme analyses and Cathleen McFadden conducted plant tissue analyses. This manuscript was improved by helpful comments from Brenda Casper, members of the Ehrenfeld lab, and five anonymous referees. Funding was provided by a National Science Foundation Graduate Research Fellowship to K.J.E. and an NSF grant (DEB-0309047) to J.G.E.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Hans Lambers.
Joan G. Ehrenfeld is deceased.
Rights and permissions
About this article
Cite this article
Elgersma, K.J., Yu, S., Vor, T. et al. Microbial-mediated feedbacks of leaf litter on invasive plant growth and interspecific competition. Plant Soil 356, 341–355 (2012). https://doi.org/10.1007/s11104-011-1117-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-011-1117-z