Abstract
Recent work suggests that soil nutrient heterogeneity may modulate plant responses to drivers of global change, but interactions between N heterogeneity and changes in rainfall regime remain poorly understood. We used a model grassland system to investigate the interactive effects of N application pattern (homogeneous, heterogeneous) and precipitation-magnitude manipulation during the growing season (control, +50 % rainfall, −50 % rainfall) on aboveground biomass and plant community dominance patterns. Our study resulted in four major findings: patchy N addition increased within-plot variability in plant size structure at the species level, but did not alter total aboveground biomass; patchy N addition increased community dominance and caused a shift in the ranking of subordinate plant species; unlike community-level biomass, plant species differed in their biomass response to the rainfall treatments; and neither aboveground biomass nor community dominance showed significant interactions between N pattern and rainfall manipulation, suggesting that grassland responses to patchy N inputs are insensitive to water addition or rainfall reduction in our temperate study system. Overall, our results indicate that the spatial pattern of N inputs has greater effects on species biomass variability and community dominance than on aboveground production. These short-term changes in plant community structure may have significant implications for longer-term patterns of vegetation dynamics and plant-soil feedbacks. Moreover our results suggest that the magnitude of precipitation during the growing season plays a limited role in grassland responses to heterogeneous organic N inputs, emphasizing the need to consider other components of precipitation change in future heterogeneity studies.
Similar content being viewed by others
References
Adamcczyk B, Godlewski M, Smolander A, Kitunen V (2009) Degradation of proteins by enzymes exuded by Allium porrum roots—a potentially important strategy for acquiring organic nitrogen by plants. Plant Physiol Biochem 47:919–925
Bloor JMG, Bardgett RD (2012) Stability of above-ground and below-ground processes to extreme drought in model grassland ecosystems: interactions with plant species diversity and soil nitrogen availability. Perspect Plant Ecol 14:193–204. doi:10.1016/j.ppees.2011.12.001
Bloor JMG, Pottier J (2014) Grazing and spatial heterogeneity: implications for grassland structure and function. In: Mariotte P, Kardol P (eds) Grassland biodiversity and conservation in a changing world. Nova, Hauppage, pp 135–162
Borken W, Matzner E (2009) Reappraisal of drying and wetting effects on C and N mineralization and fluxes in soils. Glob Change Biol 15:808–824. doi:10.1111/j.1365-2486.2008.01681.x
Caldwell MM, Pearcy RW (1994) Exploitation of environmental heterogeneity by plants: ecophysiological processes above-and belowground. Academic Press, San Diego
Callaway RM, Pennings SC, Richards CL (2003) Phenotypic plasticity and interactions among plants. Ecology 84:1115–1128
Campbell BD, Grime JP, Mackey JML (1991) A trade-off between scale and precision in resource foraging. Oecologia 87:532–538
Casper BB, Cahill JF (1996) Limited effects of soil nutrient heterogeneity on populations of Abutilon theophrasti (Malvaceae). Am J Bot 83:333–341. doi:10.2307/2446168
Chesson PL, Warner RR (1981) Environmental variability promotes coexistence in lottery competitive systems. Am Nat 117:923–943
Clair SB, Sudderth EA, Castanha C, Torn MS, Ackerly DD (2009) Plant responsiveness to variation in precipitation and nitrogen is consistent across the compositional diversity of a California annual grassland. J Veg Sci 20:860–870
Collins B, Wein G (1998) Soil resource heterogeneity effects on early succession. Oikos 82:238–245. doi:10.2307/3546963
Da Silveria Pontes L, Louault F, Carrère P, Maire V, Andueza D, Soussana J-F (2010) The role of plant traits and their plasticity in the response of pasture grasses to nutrients and cutting frequency. Ann Bot 105:957–965. doi:10.1093/aob/mcq066
Day KJ, Hutchings MJ, John EA (2003a) The effects of spatial pattern of nutrient supply on the early stages of growth in plant populations. J Ecol 91:305–315
Day KJ, Hutchings MJ, John EA (2003b) The effects of spatial pattern of nutrient supply on yield, structure and mortality in plant populations. J Ecol 91:541–553
De Deyn GB, Shiel RS, Ostle NJ, McNamara NP, Oakley S, Young I, Freeman C, Fenner N, Quirk H, Bardgett R (2011) Additional carbon sequestration benefits for grassland diversity restoration. J Appl Ecol 48:600–608
de Kroon H, Hendriks M, van Ruijven J, Ravenek J, Padilla FM, Jongejans E, Visser EJW, Mommer L (2012) Root responses to nutrients and soil biota: drivers of species coexistence and ecosystem productivity. J Ecol 100:6–15
Eilts JA, Mittelbach GG, Reynolds HL, Gross KL (2011) Resource heterogeneity, soil fertility, and species diversity: effects of clonal species on plant communities. Am Nat 177:574–588. doi:10.1086/659633
Einsmann JC, Jones RH, Pu M, Mitchell RJ (1999) Nutrient foraging traits in 10 co-occurring plant species of contrasting life forms. J Ecol 87:609–619
Farley RA, Fitter AH (1999) The responses of seven co-occurring woodland herbaceous perennials to localized nutrient-rich patches. J Ecol 87:849–859. doi:10.1046/j.1365-2745.1999.00396.x
Farrell M, Hill PW, Farrar J, Bardgett RD, Jones DL (2011) Seasonal variation in soluble soil carbon and nitrogen across a grassland productivity gradient. Soil Biol Biochem 43:835–844
Fiala K, Tuma I, Holub P (2009) Effect of manipulated rainfall on root production and plant belowground dry mass of different grassland ecosystems. Ecosystems 12:906–914. doi:10.1007/s10021-009-9264-2
Fierer N, Schimel JP (2002) Effects of drying-rewetting frequency on soil carbon and nitrogen transformations. Soil Biol Biochem 34:777–787. doi:10.1016/s0038-0717(02)00007-x
Fridley JD, Grime JP, Askew AP, Moser B, Stevens CJ (2011) Soil heterogeneity buffers community response to climate change in species-rich grassland. Glob Change Biol 17:2002–2011. doi:10.1111/j.1365-2486.2010.02347.x
García-Palacios P, Maestre FT, Gallardo A (2011) Soil nutrient heterogeneity modulates ecosystem responses to changes in the identity and richness of plant functional groups. J Ecol 99:551–562. doi:10.1111/j.1365-2745.2010.01765.x
García-Palacios P, Maestre FT, Bardgett RD, de Kroon H (2012) Plant responses to soil heterogeneity and global environmental change. J Ecol 100:1303–1314. doi:10.1111/j.1365-2745.2012.02014.x
Gazol A, Tamme R, Price JN, Hiiesalu I, Laanisto L, Partel M (2013) A negative heterogeneity-diversity relationship found in experimental grassland communities. Oecologia 173:545–555. doi:10.1007/s00442-013-2623-x
Gilgen AK, Buchmann N (2009) Response of temperate grasslands at different altitudes to simulated summer drought differed but scaled with annual precipitation. Biogeosciences 6:2525–2539
Gordon H, Haygarth PM, Bardgett RD (2008) Drying and rewetting effects on soil microbial community composition and nutrient leaching. Soil Biol Biochem 40:302–311. doi:10.1016/j.soilbio.2007.08.008
Grigulis K et al (2013) Relative contributions of plant traits and soil microbial properties to mountain grassland ecosystem services. J Ecol 101:47–57. doi:10.1111/1365-2745.12014
Grime JP (1998) Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J Ecol 86:902–910. doi:10.1046/j.1365-2745.1998.00306.x
Grime JP, Mackey JML (2002) The role of plasticity in resource capture by plants. Evol Ecol 16:299–307
Harpole WS, Potts DL, Suding KN (2007) Ecosystem responses to water and nitrogen amendment in a California grassland. Glob Change Biol 13:2341–2348. doi:10.1111/j.1365-2486.2007.01447.x
Hartmann AA, Barnard RL, Marhan S, Niklaus PA (2013) Effects of drought and N-fertilization on N cycling in two grassland soils. Oecologia 171:705–717. doi:10.1007/s00442-012-2578-3
Haynes RJ, Williams PH (1993) Nutrient cycling and soil fertility in the grazed pasture ecosystem. Adv Agron 49:119–199
Hillebrand H, Bennett DM, Cadotte MW (2008) Consequences of dominance: a review of evenness effects on local and regional ecosystem processes. Ecology 89:1510–1520. doi:10.1890/07-1053.1
Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24. doi:10.1111/j.1469-8137.2004.01015.x
Hovenden MJ, Newton PCD, Wills KE (2014) Seasonal not annual rainfall determines grassland biomass response to carbon dioxide. Nature 511:583–586
Hulin S, Carrère P, Chabalier C, Farruggia A, Landriaux J, Orth D, Piquet M, Rivière J, Seytre L (2011) Diagnostic prairial en zone fromagère AOP Massif Central—typologie multifonctionnelle des prairies. Pôle fromager AOP, Massif Central, France
Hutchings MJ, John EA, Wijesinghe DK (2003) Toward understanding the consequences of soil heterogeneity for plant populations and communities. Ecology 84:2322–2334
IPCC (2007) Summary for policymakers. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate Change 2007: the physical science basis. Contribution of Working Group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge
Jung V, Albert CH, Violle C, Kunstler G, Loucougaray G, Spiegelberger T (2014) Intraspecific trait variability mediates the response of subalpine grassland communities to extreme drought events. J Ecol 102:45–53. doi:10.1111/1365-2745.12177
Kembel SW, De Kroon H, Cahill JF, Mommer L (2008) Improving the scale and precision of hypotheses to explain root foraging ability. Ann Bot 101:1295–1301. doi:10.1093/aob/mcn044
Knapp AK et al (2002) Rainfall variability, carbon cycling, and plant species diversity in a mesic grassland. Science 298:2202–2205. doi:10.1126/science.1076347
Kong DL, Lu XT, Jiang LL, Wu HF, Miao Y, Kardol P (2013) Extreme rainfall events can alter inter-annual biomass responses to water and N enrichment. Biogeosciences 10:8129–8138. doi:10.5194/bg-10-8129-2013
Koopmans LH, Owen DB, Rosenblatt JI (1964) Confidence intervals for the coefficient of variation for the normal and log normal distributions. Biometrika 51:25–32
Lauenroth WK, Sala OE (1992) Long-term forage production of North American shortgrass steppe. Ecol Appl 2:397–403. doi:10.2307/1941874
Lin Y, Han GD, Zhao ML, Chang SX (2010) Spatial vegetation patterns as early signs of desertification: a case study of a desert steppe in Inner Mongolia, China. Landsc Ecol 25:1519–1527. doi:10.1007/s10980-010-9520-z
Maestre FT, Reynolds JF (2006) Spatial heterogeneity in soil nutrient supply modulates nutrient and biomass responses to multiple global change drivers in model grassland communities. Glob Change Biol 12:2431–2441
Maestre FT, Reynolds JF (2007) Amount or pattern? Grassland responses to the heterogeneity and availability of two key resources. Ecology 88:501–511
Maestre FT, Bradford MA, Reynolds JF (2005) Soil nutrient heterogeneity interacts with elevated CO2 and nutrient availability to determine species and assemblage responses in a model grassland community. New Phytol 168:637–649. doi:10.1111/j.1469-8137.2005.01547.x
Magurran AE (2004) Measuring biological diversity. Blackwell, Oxford
Mariotte P (2014) Do subordinate species punch above their weight? Evidence from above- and below-ground. New Phytol 203:16–21
Mokany K, Ash J, Roxburgh S (2008) Functional identity is more important than diversity in influencing ecosystem processes in a temperate native grassland. J Ecol 96:884–893. doi:10.1111/j.1365-2745.2008.01395.x
Orwin KH, Bertram JE, Clough TJ, Condron LM, Sherlock RR, O’Callagha M (2009) Short-term consequences of spatial heterogeneity in soil nitrogen concentrations caused by urine patches of different sizes. Appl Soil Ecol 42:271–278
Paungfoo-Lonhienne C, Lonhienne TGA, Rentsch D, Robinson N, Christie M, Webb RI, Gamage HK, Carroll BJ, Schenk PM, Schmidt S (2008) Plants can use protein as a nitrogen source without assistance from other organisms. PNAS 105:4524–4529
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, New York
Rajaniemi TK (2011) Competition for patchy soil resources reduces community evenness. Oecologia 165:169–174
Rajaniemi TK, Reynolds HL (2004) Root foraging for patchy resources in eight herbaceous plant species. Oecologia 141:519–525
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0
Schwinning S, Weiner J (1998) Mechanisms determining the degree of size asymmetry in competition among plants. Oecologia 113:447–455. doi:10.1007/s004420050397
Tilman D (1988) Plant strategies and the dynamics and structure of plant communities. Princeton University Press, Princeton
Warren CR (2014) Organic N molecules in the soil solution: what is known, what is unknown and the path forwards. Plant Soil 375:1–19
Wijesinghe DK, Hutchings MJ (1999) The effects of environmental heterogeneity on the performance of Glechoma hederacea: the interactions between patch contrast and patch scale. J Ecol 87:860–872
Wijesinghe DK, John EA, Beurskens S, Hutchings MJ (2001) Root system size and precision in nutrient foraging: responses to spatial pattern of nutrient supply in six herbaceous species. J Ecol 89:972–983
Wijesinghe DK, John EA, Hutchings MJ (2005) Does pattern of soil resource heterogeneity determine plant community structure? An experimental investigation. J Ecol 93:99–112
Williams BM, Houseman GR (2014) Experimental evidence that soil heterogeneity enhances plant diversity during community assembly. J Plant Ecol 7:461–469. doi:10.1093/jpe/rtt056
Xi N, Carrère P, Bloor JMG (2014) Nitrogen form and spatial pattern promote asynchrony in plant and soil responses to nitrogen inputs in a temperate grassland. Soil Biol Biochem 71:40–47. doi:10.1016/j.soilbio.2014.01.008
Yang LH, Bastow JL, Spence KO, Wright AN (2008) What can we learn from resource pulses? Ecology 89:621–634
Acknowledgments
The authors thank P. Pichon and A. Salcedo for help setting up the experiment. Thanks also to A. Salcedo for assistance with data collection and harvest. This study was supported by a doctoral fellowship from the Chinese Scholarship Council to N. X. The experiment complies with the current laws of the country (France) in which the experiment was performed.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Scott Collins.
This paper is part of the Ph.D. research of the lead author, Nianxun Xi. It addresses an important question in plant community ecology and uses a unique experimental approach to determine how soil heterogeneity interacts with climate change to affect community structure and function in grasslands. A surprising result is that the impacts of resource heterogeneity were not affected by precipitation. Overall, we found that net primary production responses were stable despite spatial variability in resources and changes in species abundances. This is a nice demonstration of how compensation can serve as a stabilizing mechanism for ecosystem processes.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Xi, N., Carrère, P. & Bloor, J.M.G. Plant community responses to precipitation and spatial pattern of nitrogen supply in an experimental grassland ecosystem. Oecologia 178, 329–338 (2015). https://doi.org/10.1007/s00442-015-3289-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-015-3289-3