Abstract
Background and aims
Higher interannual precipitation variability is predicted for Southern California’s shrub-dominated systems, promoting soil moisture variation and changing community composition. We asked if soil microbial responses to rainfall regime will depend on litter inputs; showing direct effects of altered precipitation through soil moisture and indirect effects resulting from shifting litter inputs.
Methods
Soils were collected from a 2-year field rainfall manipulation experiment. Under lab conditions soils were subjected to high or low moisture pulses with litter amendments from native and exotic species in all combinations.
Results
Soil respiration was higher with larger water pulses, but rose over time in low pulse treatments (direct response). Litter additions from exotic species promoted greater respiration, and results were stronger under higher soil moisture (indirect response). Extracellular enzyme activities generally were higher with exotic litter and under high moisture pulses. Those involved in N-cycling had much larger increases activity for the exotic litter addition - high moisture pulse scenarios compared to other treatments.
Conclusions
Our results indicate the potential for microbial acclimation to drought conditions over short timescales and that below-ground processes are sensitive to direct and indirect effects of shifting rainfall regimes, especially where invasion is promoted by future climate change.
Similar content being viewed by others
Abbreviations
- NAG:
-
β-1,4-N-acetylglucosaminidase
- BGLUC:
-
β-Glucosidase
- CBH:
-
Cellobiohydrolase
- EEA:
-
Extracellular enzyme activity
- LAP:
-
L-leucine aminopeptidase
- MBM:
-
Microbial biomass
- PHOS:
-
Phosphatase
References
Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37:937–944. doi:10.1016/J.Soilbio.2004.09.014
American Public Health Association (1994) Water Environment Federation (1998) Standard methods for the examination of water and wastewater. Washington, DC, USA
Ashbacher AC, Cleland EE (2015) Native and exotic plant species show differential growth but similar functional trait responses to experimental rainfall. Ecosphere 6. doi:10.1890/Es15-00059.1
Austin AT (2011) Has water limited our imagination for aridland biogeochemistry? Trends Ecol Evol 26:229–235. doi:10.1016/J.Tree.2011.02.003
Austin AT et al. (2004) Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141:221–235. doi:10.1007/S00442-004-1519-1
Beck T, Joergensen RG, Kandeler E, Makeschin F, Nuss E, Oberholzer HR, Scheu S (1997) An inter-laboratory comparison of ten different ways of measuring soil microbial biomass C. Soil Biol Biochem 29:1023–1032. doi:10.1016/S0038-0717(97)00030-8
Berg N, Hall A (2015) Increased interannual precipitation extremes over California under climate change. J Clim 28:6324–6334. doi:10.1175/Jcli-D-14-00624.1
Birch H (1958) The effect of soil drying on humus decomposition and nitrogen availability. Plant and soil 10:9–31
Blazewicz SJ, Schwartz E, Firestone MK (2014) Growth and death of bacteria and fungi underlie rainfall-induced carbon dioxide pulses from seasonally dried soil. Ecology 95:1162–1172. doi:10.1890/13-1031.1
Borken W, Matzner E (2009) Reappraisal of drying and wetting effects on C and N mineralization and fluxes in soils. Glob Chang Biol 15:808–824. doi:10.1111/J.1365-2486.2008.01681.X
Brando PM, Nepstad DC, Davidson EA, Trumbore SE, Ray D, Camargo P (2008) Drought effects on litterfall, wood production and belowground carbon cycling in an Amazon forest: results of a throughfall reduction experiment. Philos T R Soc B 363:1839–1848. doi:10.1098/Rstb.2007.0031
Bray SR, Kitajima K, Mack MC (2012) Temporal dynamics of microbial communities on decomposing leaf litter of 10 plant species in relation to decomposition rate. Soil Biol Biochem 49:30–37. doi:10.1016/J.Soilbio.2012.02.009
Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil-nitrogen - a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842. doi:10.1016/0038-0717(85)90144-0
Castro-Diez P, Godoy O, Alonso A, Gallardo A, Saldana A (2014) What explains variation in the impacts of exotic plant invasions on the nitrogen cycle? A meta-analysis. Ecol Lett 17:1–12. doi:10.1111/Ele.12197
Cayan D et al. (2009) Climate change scenarios and sea level rise estimates for the California 2008 climate change scenarios assessment California Climate Change Center CEC-500-2009-014-D doi:http://www.energy.ca.gov/2009publications/CEC-500-2009-014/CEC-500-2009-014-D.PDF
Charlotte J Alster, Donovan P German, Ying Lu, Steven D Allison (2013) Microbial enzymatic responses to drought and to nitrogen addition in a southern California grassland. Soil Biology and Biochemistry 64:68–79
Chen SP, Lin GH, Huang JH, Jenerette GD (2009) Dependence of carbon sequestration on the differential responses of ecosystem photosynthesis and respiration to rain pulses in a semiarid steppe. Glob Chang Biol 15:2450–2461. doi:10.1111/J.1365-2486.2009.01879.X
Cleland EE et al. (2013) Sensitivity of grassland plant community composition to spatial vs. temporal variation in precipitation. Ecology 94:1687–1696. doi:10.1890/12-1006.1
Collins SL, Sinsabaugh RL, Crenshaw C, Green L, Porras-Alfaro A, Stursova M, Zeglin LH (2008) Pulse dynamics and microbial processes in aridland ecosystems. J Ecol 96:413–420. doi:10.1111/J.1365-2745.2008.01362.X
Collins M et al. (2013) Long-term climate change: projections, commitments and irreversibility. In: Stocker TF et al. (eds) Climate Change 2013: The Physical Science Basis. Contribution of Working Group 1 to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambrige, pp. 1029–1136. doi:10.1017/CBO9781107415324.024
Cook FJ, Orchard VA (2008) Relationships between soil respiration and soil moisture. Soil Biol Biochem 40:1013–1018. doi:10.1016/J.Soilbio.2007.12.012
D’Antonio CM (2000) Fire, plant invasions, and global changes. In: Mooney HA, Hobbs RJ (eds) Invasive species in a changing world. Island Press, Washington, D.C., pp. 65–94
de Vries FT, Shade A (2013) Controls on soil microbial community stability under climate change. Front Microbiol 4. doi:10.3389/fmicb.2013.00265
Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523. doi:10.1007/S10021-002-0151-3
Esch EH, Hernandez DL, Pasari JR, Kantor RSG, Selmants PC (2013) Response of soil microbial activity to grazing, nitrogen deposition, and exotic cover in a serpentine grassland. Plant Soil 366:671–682. doi:10.1007/S11104-012-1463-5
Evans SE, Burke IC (2013) Carbon and nitrogen decoupling under an 11-year drought in the shortgrass steppe. Ecosystems 16:20–33. doi:10.1007/S10021-012-9593-4
Evans SE, Wallenstein MD (2012) Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter? Biogeochemistry 109:101–116. doi:10.1007/S10533-011-9638-3
Evans SE, Wallenstein MD (2014) Climate change alters ecological strategies of soil bacteria. Ecol Lett 17:155–164. doi:10.1111/ele.12206
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
Fox J, Weisberg S (2011) An R companion to applied regression, Second edn. Sage, Thousand Oaks
Gorissen A et al. (2004) Climate change affects carbon allocation to the soil in shrublands. Ecosystems 7:650–661. doi:10.1007/S10021-004-0218-4
Hawkes CV, Keitt TH (2015) Resilience vs. historical contingency in microbial responses to environmental change. Ecol Lett 18:612–625. doi:10.1111/ele.12451
Hobbs RJ, Mooney HA (1991) Effects of rainfall variability and gopher disturbance on serpentine annual grassland dynamics. Ecology 72:59–68. doi:10.2307/1938902
Hobbs RJ, Mooney HA (2005) Invasive species in a changing world: the interactions between global change and invasives. In: Mooney HA (ed) Invasive alien species: a new synthesis. Island Press, Washington, DC
Hugh AL, Henry, John D Juarez, Christopher B Field, Peter M Vitousek (2005) Interactive effects of elevated CO2, N deposition and climate change on extracellular enzyme activity and soil density fractionation in a California annual grassland. Global Change Biology 11 (10):1808–1815
IPCC (2012) Managing the risks of extreme events and disasters to advance climate change adaptation. Cambridge University Press, Cambridge
Kempf B, Bremer E (1998) Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch Microbiol 170:319–330. doi:10.1007/S002030050649
KR Saiya-Cork, RL Sinsabaugh, DR Zak (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biology and Biochemistry 34 (9):1309–1315
Kramer S, Green DM (2000) Acid and alkaline phosphatase dynamics and their relationship to soil microclimate in a semiarid woodland. Soil Biol Biochem 32:179–188. doi:10.1016/S0038-0717(99)00140-6
Lennon JT, Aanderud ZT, Lehmkuhl BK, Schoolmaster DR (2012) Mapping the niche space of soil microorganisms using taxonomy and traits. Ecology 93:1867–1879
Li XZ, Sarah P (2003) Enzyme activities along a climatic transect in the Judean Desert. Catena 53:349–363. doi:10.1016/S0341-8162(03)00087-0
Liao CZ et al. (2008) Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytol 177:706–714. doi:10.1111/J.1469-8137.2007.02290.X
Meisner A, Rousk J, Bååth E (2015) Prolonged drought changes the bacterial growth response to rewetting. Soil Biol Biochem 88:314–322
Mikha MM, Rice CW, Milliken GA (2005) Carbon and nitrogen mineralization as affected by drying and wetting cycles. Soil Biol Biochem 37:339–347. doi:10.1016/J.Soilbio.2004.08.003
Ng EL, Patti AF, Rose MT, Schefe CR, Smernik RJ, Cavagnaro TR (2015) Do organic inputs alter resistance and resilience of soil microbial community to drying? Soil Biol Biochem 81:58–66. doi:10.1016/j.soilbio.2014.10.028
Placella SA, Brodie EL, Firestone MK (2012) Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups. P Natl Acad Sci USA 109:10931–10936. doi:10.1073/pnas.1204306109
Pysek P, Jarosik V, Hulme PE, Pergl J, Hejda M, Schaffner U, Vila M (2012) A global assessment of invasive plant impacts on resident species, communities and ecosystems: the interaction of impact measures, invading species’ traits and environment. Glob Chang Biol 18:1725–1737. doi:10.1111/J.1365-2486.2011.02636.X
R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Rao LE, Allen EB (2010) Combined effects of precipitation and nitrogen deposition on native and invasive winter annual production in California deserts. Oecologia 162:1035–1046
Robert L Sinsabaugh, Christian L Lauber, Michael N Weintraub, Bony Ahmed, Steven D Allison, Chelsea Crenshaw, Alexandra R Contosta, Daniela Cusack, Serita Frey, Marcy E Gallo, Tracy B Gartner, Sarah E Hobbie, Keri Holland, Bonnie L Keeler, Jennifer S Powers, Martina Stursova, Cristina Takacs-Vesbach, Mark P Waldrop, Matthew D Wallenstein, Donald R Zak, Lydia H Zeglin, (2008) Stoichiometry of soil enzyme activity at global scale. Ecology Letters
Sandel B, Dangremond EM (2012) Climate change and the invasion of California by grasses. Glob Chang Biol 18:277–289. doi:10.1111/J.1365-2486.2011.02480.X
Sardans J, Penuelas J (2005) Drought decreases soil enzyme activity in a Mediterranean Quercus ilex L. Forest. Soil Biol Biochem 37:455–461. doi:10.1016/J.Soilbio.2004.08.004
Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394. doi:10.1890/06-0219
Schwinning S, Sala OE (2004) Hierarchy of responses to resource pulses in and and semi-arid ecosystems. Oecologia 141:211–220. doi:10.1007/S00442-004-1520-8
Shi AD, Marschner P (2014) Drying and rewetting frequency influences cumulative respiration and its distribution over time in two soils with contrasting management. Soil Biol Biochem 72:172–179. doi:10.1016/J.Soilbio.2014.02.001
Sinsabaugh RL (1994) Enzymatic analysis of microbial pattern and process Biol Fert. Soils 17:69–74
Sinsabaugh RL, Hill BH, Shah JJF (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–U117. doi:10.1038/Nature08632
Smith MD, Knapp AK, Collins SL (2009) A framework for assessing ecosystem dynamics in response to chronic resource alterations induced by global change. Ecology 90:3279–3289
Stevenson, FJ, Cole, MA (1999) Cycles of soils: carbon, nitrogen, phosphorus, sulfur, micronutrients. Wiley
Tiemann LK, Billings SA (2011) Changes in variability of soil moisture alter microbial community C and N resource use. Soil Biol Biochem 43:1837–1847. doi:10.1016/J.Soilbio.2011.04.020
Vangestel M, Merckx R, Vlassak K (1993) Microbial biomass responses to soil drying and rewetting - the fate of fast-growing and slow-growing microorganisms in soils from different climates. Soil Biol Biochem 25:109–123. doi:10.1016/0038-0717(93)90249-B
Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633
Wolkovich EM, Lipson DA, Virginia RA, Cottingham KL, Bolger DT (2010) Grass invasion causes rapid increases in ecosystem carbon and nitrogen storage in a semiarid shrubland. Glob Chang Biol 16:1351–1365. doi:10.1111/J.1365-2486.2009.02001.X
Xiang SR, Doyle A, Holden PA, Schimel JP (2008) Drying and rewetting effects on C and N mineralization and microbial activity in surface and subsurface California grassland soils. Soil Biol Biochem 40:2281–2289. doi:10.1016/j.soilbio.2008.05.004
Yu ZH, Wang GH, Marsthner P (2014) Drying and rewetting - effect of frequency of cycles and length of moist period on soil respiration and microbial biomass. Eur J Soil Biol 62:132–137. doi:10.1016/J.Ejsobi.2014.03.007
Acknowledgments
We thank Rachel Abbott, Angie Ashbacher, and Christopher Kopp for maintaining the field experiment along with Rochelle Aran and Magali Porrachia for their laboratory assistance. This work was performed at the University of California Natural Reserve System and supported by a Mildred E. Mathias Graduate Student Research Grant from the University of California Natural Reserve System. This material is based upon work supported by the National Science Foundation Graduate Research Fellowship under Grant No. (DGE-1144086) and also a National Science Foundation Division of Environmental Biology grant (DEB 1154082). Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Sven Marhan.
Appendices
Appendix 1
Appendix 2
Rights and permissions
About this article
Cite this article
Esch, E.H., Lipson, D. & Cleland, E.E. Direct and indirect effects of shifting rainfall on soil microbial respiration and enzyme activity in a semi-arid system. Plant Soil 411, 333–346 (2017). https://doi.org/10.1007/s11104-016-3027-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-016-3027-6