Abstract
Background and aims
The occurrence of drought-induced forest die-off events is projected to increase in the future, but we still lack complete understanding of its impact on plant-soil interactions, soil microbial diversity and function. We investigated the effects of holm oak (Quercus ilex) decline (HOD) on soil microbial community and functioning, and how these effects relate to changes in the herbaceous community.
Methods
We selected 30 holm oak trees with different defoliation degrees (healthy, affected and dead) and analyzed soil samples collected under the canopy (holm oak ecotype) and out of the influence (grassland ecotype) of each tree.
Results
HOD increased potential nitrogen (N) mineralization and decreased inorganic N concentrations. These results could be partially explained by changes in the herbaceous composition, an increased herbaceous abundance and changes in soil microbial functional diversity and structure, with HOD favoring bacteria against fungi. Moreover, herbaceous abundance and microbial functional diversity of holm oak and grassland ecotypes converged with HOD.
Conclusions
Our results show that HOD triggers a cascade effect on plant understory and soil microbial communities, as well as a plant succession (savannization) process, where understory species colonize the gaps left by dead holm oaks, with important implications for ecosystem C and N budgets.
Similar content being viewed by others
References
Allen CD, Breshears DD, McDowell NG (2015) On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere 6:1–55. doi:10.1890/ES15-00203.1
Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim JH, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684. doi:10.1016/j.foreco.2009.09.001
Allison SD, Martiny JBH (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci U S A 105:11512–11519. doi:10.1073/pnas.0801925105
Anderegg WRL, Anderegg LDL, Sherman C, Karp DS (2012) Effects of widespread drought-induced aspen mortality on understory plants. Conserv Biol 26:1082–1090. doi:10.1111/j.1523-1739.2012.01913.x
Anderegg WRL, Kane JM, Anderegg LDL (2013) Consequences of widespread tree mortality triggered by drought and temperature stress. Nat Clim Chang 3:30–36. doi:10.1038/nclimate1635
Anderson JPE, Domsch KH (1978) A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol Biochem 10:215–221. doi:10.1016/0038-0717(78)90099-8
Anderson MJ, Ellingsen KE, McArdle BH (2006) Multivariate dispersion as a measure of beta diversity. Ecol Lett 9:683–693. doi:10.1111/j.1461-0248.2006.00926.x
Baldocchi D, Tang J, Xu L (2006) How switches and lags in biophysical regulators affect spatial-temporal variation of soil respiration in an oak-grass savanna. J Geophys Res Biogeosci 111:G02008. doi:10.1029/2005JG000063
Barba J, Curiel Yuste J, Martínez-Vilalta J, Lloret F (2013) Drought-induced tree species replacement is reflected in the spatial variability of soil respiration in a mixed Mediterranean forest. For Ecol Manag 306:79–87. doi:10.1016/j.foreco.2013.06.025
Barba J, Curiel Yuste J, Poyatos R, Janssens IA, Lloret F (2016) Strong resilience of soil respiration components to drought-induced die-off resulting in forest secondary succession. Oecologia:1–15. doi:10.1007/s00442-016-3567-8
Barba J, Lloret F, Curiel Yuste J (2015) Effects of drought-induced forest die-off on litter decomposition. Plant Soil 402:91–101. doi:10.1007/s11104-015-2762-4
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 61:1–48. doi:10.18637/jss.v067.i01
Burnham KP, Anderson DR (2010) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York
Carnicer J, Coll M, Ninyerola M, Pons X, Sánchez G, Peñuelas J (2011) Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought. Proc Natl Acad Sci U S A 108:1474–1478. doi:10.1073/pnas.1010070108
Clark JS, Iverson L, Woodall CW, Allen CD, Bell DM, Bragg DC, D’Amato AW, Davis FW, Hersh MH, Ibanez I, Jackson ST, Matthews S, Pederson N, Peters M, Schwartz MW, Waring KM, Zimmermann NE (2016) The impacts of increasing drought on forest dynamics, structure, and biodiversity in the United States. Glob Chang Biol. doi:10.1111/gcb.13160
Classen AT, Boyle SI, Haskins KE, Overby ST, Hart SC (2003) Community-level physiological profiles of bacteria and fungi: plate type and incubation temperature influences on contrasting soils. FEMS Microbiol Ecol 44:319–328. doi:10.1016/S0168-6496(03)00068-0
Coleman DC, Whitman WB (2005) Linking species richness, biodiversity and ecosystem function in soil systems. Pedobiologia 49:479–497. doi:10.1016/j.pedobi.2005.05.006
Crowther TW, Thomas SM, Maynard DS, Baldrian P, Covey K, Frey SD, van Diepen LTA, Bradford MA (2015) Biotic interactions mediate soil microbial feedbacks to climate change. Proc Natl Acad Sci U S A 112:7033–7038. doi:10.1073/pnas.1502956112
Curiel Yuste J, Barba J, Fernandez-Gonzalez AJ, Fernandez-Lopez M, Mattana S, Martinez-Vilalta J, Nolis P, Lloret F (2012) Changes in soil bacterial community triggered by drought-induced gap succession preceded changes in soil C stocks and quality. Ecol Evol 2:3016–3031. doi:10.1002/ece3.409
Curiel Yuste J, Peñuelas J, Estiarte M, Garcia-Mas J, Mattana S, Ogaya R, Pujol M, Sardans J (2011) Drought-resistant fungi control soil organic matter decomposition and its response to temperature. Glob Chang Biol 17:1475–1486. doi:10.1111/j.1365-2486.2010.02300.x
De Frenne P, Brunet J, Shevtsova A, Kolb A, Graae BJ, Chabrerie O, Cousins SA, Decocq G, De Schrijver A, Diekmann M, Gruwez R, Heinken T, Hermy M, Nilsson C, Stanton S, Tack W, Willaert J, Verheyen K (2011) Temperature effects on forest herbs assessed by warming and transplant experiments along a latitudinal gradient. Glob Chang Biol 17:3240–3253. doi:10.1111/j.1365-2486.2011.02449.x
Delgado-Baquerizo M, Maestre FT, Reich PB, Jeffries TC, Gaitan JJ, Encinar D, Berdugo M, Campbell CD, Singh BK (2016) Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun 7:10541. doi:10.1038/ncomms10541
Durán J, Rodríguez A, Fernández-Palacios JM, Gallardo A (2009) Changes in net N mineralization rates and soil N and P pools in a pine forest wildfire chronosequence. Biol Fertil Soils 45:781–788. doi:10.1007/s00374-009-0389-4
Durán J, Rodríguez A, Morse JL, Groffman PM (2013) Winter climate change effects on soil C and N cycles in urban grasslands. Glob Chang Biol 19:2826–2837. doi:10.1111/gcb.12238
Edburg S, Hicke J, Brooks P, Pendall E, Ewars B, Norton U, Gochis D, Guttman E, Meddens A (2012) Cascading impacts of bark beetle-caused tree mortality on coupled biogeophysical and biogeochemical processes. Front Ecol Environ 10:416–424. doi:10.1890/110173
European Environment Agency (2008) Impacts of Europe’s changing climate - 2008 indicator-based assessment. European environment agency summary, report No 4. European Environment Agency, Copenhagen, Denmark
Evans SE, Burke IC (2012) Carbon and nitrogen decoupling under an 11-year drought in the shortgrass steppe. Ecosystems 16:20–33. doi:10.1007/s10021-012-9593-4
Fernández-Martínez M, Vicca S, Janssens IA, Sardans J, Luyssaert S, Campioli M, Chapin FS III, Ciais P, Malhi Y, Obersteiner M, Papale D, Piao SL, Reichstein M, Rodà F, Peñuelas J (2014) Nutrient availability as the key regulator of global forest carbon balance. Nat Clim Chang 4:471–476. doi:10.1038/nclimate2177
Finzi AC, Austin AT, Cleland EE, Frey SD, Houlton BZ, Wallenstein MD (2011) Responses and feedbacks of coupled biogeochemical cycles to climate change: examples from terrestrial ecosystems. Front Ecol Environ 9:61–67. doi:10.1890/100001
Flores-Rentería D, Curiel Yuste J, Rincón A, Brearley FQ, García-Gil JC, Valladares F (2015) Habitat fragmentation can modulate drought effects on the plant-soil-microbial system in Mediterranean holm oak (Quercus ilex) forests. Microb Ecol 69:798–812. doi:10.1007/s00248-015-0584-9
Flores-Rentería D, Rincón A, Valladares F, Curiel Yuste J (2016) Agricultural matrix affects differently the alpha and beta structural and functional diversity of soil microbial communities in a fragmented Mediterranean holm oak forest. Soil Biol Biochem 92:79–90. doi:10.1016/j.soilbio.2015.09.015
Fontaine S, Barot S, Barré P, Bdioui N, Mary B, Rumpel C (2007) Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450:277–280. doi:10.1038/nature06275
Gallardo A, Rodríguez-Saucedo JJ, Covelo F, Fernández-Alés R (2000) Soil nitrogen heterogeneity in a Dehesa ecosystem. Plant Soil 222:71–82. doi:10.1023/A:1004725927358
García LV, Maltez-Mouro S, Pérez-Ramos IM, Freitas H, Marañón T (2006) Counteracting gradients of light and soil nutrients in the understorey of Mediterranean oak forests. Web Ecol 6:67–74
Graham EB, Knelman JE, Schindlbacher A, Siciliano S, Breulmann M, Yannarell A, Beman JM, Abell G, Philippot L, Prosser J, Foulquier A, Yuste JC, Glanville HC, Jones DL, Angel R, Salminen J, Newton RJ, Bürgmann H, Ingram LJ, Hamer U, Siljanen HMP, Peltoniemi K, Potthast K, Bañeras L, Hartmann M, Banerjee S, Yu R-Q, Nogaro G, Richter A, Koranda M, Castle SC, Goberna M, Song B, Chatterjee A, Nunes OC, Lopes AR, Cao Y, Kaisermann A, Hallin S, Strickland MS, Garcia-Pausas J, Barba J, Kang H, Isobe K, Papaspyrou S, Pastorelli R, Lagomarsino A, Lindström ES, Basiliko N, Nemergut DR (2016) Microbes as engines of ecosystem function: when does community structure enhance predictions of ecosystem processes? Front Microbiol. doi:10.3389/fmicb.2016.00214
Hegyi F (1974) A simulation model for managing jack-pine stands. In: Fries J (ed) International union of forestry research organizations. Working party S4.01, Growth models for tree and stand simulation. Royal College of Forestry, Stockholm, pp. 74–90
Ibáñez B, Gómez-Aparicio L, Stoll P, Ávila JM, Pérez-Ramos IM, Marañón T (2015) A neighborhood analysis of the consequences of Quercus suber decline for regeneration dynamics in Mediterranean forests. PLoS One 10:e0117827. doi:10.1371/journal.pone.0117827
IPCC (2013) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change
Jenkins JC, Aber JD, Canham CD (1999) Hemlock woolly adelgid impacts on community structure and N cycling rates in eastern hemlock forests. Can J For Res 29:630–645
Lloret F, Escudero A, Iriondo JM, Martínez-Vilalta J, Valladares F (2012) Extreme climatic events and vegetation: the role of stabilizing processes. Glob Chang Biol 18:797–805. doi:10.1111/j.1365-2486.2011.02624.x
Lloret F, Mattana S, Curiel Yuste J (2014) Climate-induced die-off affects plant–soil–microbe ecological relationship and functioning. FEMS Microbiol Ecol. doi:10.1093/femsec/fiu014
Lloret F, Siscart D, Dalmases C (2004) Canopy recovery after drought dieback in holm-oak Mediterranean forests of Catalonia (NE Spain). Glob Chang Biol 10:2092–2099. doi:10.1111/j.1365-2486.2004.00870.x
Maaß S, Migliorini M, Rillig MC, Caruso T (2014) Disturbance, neutral theory, and patterns of beta diversity in soil communities. Ecol Evol 4:4766–4774. doi:10.1002/ece3.1313
Martínez-Vilalta J, Lloret F, Breshears DD (2012) Drought-induced forest decline: causes, scope and implications. Biol Lett 8:689–691. doi:10.1098/rsbl.2011.1059
McDowell NG (2011) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 155:1051–1059. doi:10.1104/pp.110.170704
Monturiol F, Alcalá del Olmo L (1990) Mapa de asociaciones de suelos de la Comunidad de Madrid. Comunidad de Madrid, Consejería de Agricultura y Cooperación: Consejo Superior de Investigaciones Científicas, Madrid, Spain
Moore JC, McCann K, de Ruiter PC (2005) Modeling trophic pathways, nutrient cycling, and dynamic stability in soils. Pedobiologia 49:499–510. doi:10.1016/j.pedobi.2005.05.008
Morillas L, Durán J, Rodríguez A, Roales J, Gallardo A, Lovett GM, Groffman PM (2015) Nitrogen supply modulates the effect of changes in drying–rewetting frequency on soil C and N cycling and greenhouse gas exchange. Glob Chang Biol 21:3854–3863. doi:10.1111/gcb.12956
Nave LE, Gough CM, Maurer KD, Bohrer G, Hardiman BS, Le Moine J, Munoz AB, Nadelhoffer KJ, Sparks JP, Strahm BD, Vogel CS, Curtis PS (2011) Disturbance and the resilience of coupled carbon and nitrogen cycling in a north temperate forest. J Geophys Res Biogeosci 116:G04016. doi:10.1029/2011JG001758
Nielsen UN, Ayres E, Wall DH, Bardgett RD (2011) Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity–function relationships. Eur J Soil Sci 62:105–116. doi:10.1111/j.1365-2389.2010.01314.x
Ninyerola M, Pons X, Roure J (2005) Atlas climático digital de la Península Ibérica. Metodología y aplicaciones en bioclimatología y geobotánica. Universidad Autónoma de Barcelona, Barcelona
Prescott CE (2010) Litter decomposition: what controls it and how can we alter it to sequester more carbon in forest soils? Biogeochemistry 101:133–149. doi:10.1007/s10533-010-9439-0
R Core Team (2014) R: a language and environment for statistical computing. Vienna, Austria
Rangel TF, Diniz-Filho JAF, Bini LM (2010) SAM: a comprehensive application for spatial analysis in Macroecology. Ecography 33:46–50. doi:10.1111/j.1600-0587.2009.06299.x
Rey A, Pegoraro E, Tedeschi V, De Parri I, Jarvis PG, Valentini R (2002) Annual variation in soil respiration and its components in a coppice oak forest in Central Italy. Glob Chang Biol 8:851–866. doi:10.1046/j.1365-2486.2002.00521.x
Rodríguez A, Durán J, Covelo F, Fernández-Palacios JM, Gallardo A (2011) Spatial pattern and variability in soil N and P availability under the influence of two dominant species in a pine forest. Plant Soil 345:211–221. doi:10.1007/s11104-011-0772-4
Rodríguez A, Lovett GM, Weathers KC, Arthur MA, Templer PH, Goodale CL, Christenson LM (2014) Lability of C in temperate forest soils: assessing the role of nitrogen addition and tree species composition. Soil Biol Biochem 77:129–140. doi:10.1016/j.soilbio.2014.06.025
Royer PD, Cobb NS, Clifford MJ, Huang C-Y, Breshears DD, Adams HD, Villegas JC (2011) Extreme climatic event-triggered overstorey vegetation loss increases understorey solar input regionally: primary and secondary ecological implications. J Ecol 99:714–723. doi:10.1111/j.1365-2745.2011.01804.x
Saura-Mas S, Bonas A, Lloret F (2014) Plant community response to drought-induced canopy defoliation in a Mediterranean Quercus ilex forest. Eur J For Res 134:261–272. doi:10.1007/s10342-014-0848-9
Tang J, Baldocchi DD (2005) Spatial–temporal variation in soil respiration in an oak–grass savanna ecosystem in California and its partitioning into autotrophic and heterotrophic components. Biogeochemistry 73:183–207. doi:10.1007/s10533-004-5889-6
Valladares F, Benavides R, Rabasa SG, Díaz M, Pausas J, Paula S, Simonson W (2014) Global change and Mediterranean forests: current impacts and potential responses. In: Coomes DA, Burslem DFRP, Simonson WD (eds) Forests and global change. Cambridge University Press, Cambridge, pp. 47–75
van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310. doi:10.1111/j.1461-0248.2007.01139.x
van der Plas F, Manning P, Soliveres S, Allan E, Scherer-Lorenzen M, Verheyen K, Wirth C, Zavala MA, Ampoorter E, Baeten L, Barbaro L, Bauhus J, Benavides R, Benneter A, Bonal D, Bouriaud O, Bruelheide H, Bussotti F, Carnol M, Castagneyrol B, Charbonnier Y, Coomes DA, Coppi A, Bestias CC, Dawud SM, De Wandeler H, Domisch T, Finér L, Gessler A, Granier A, Grossiord C, Guyot V, Hättenschwiler S, Jactel H, Jaroszewicz B, Joly F-X, Jucker T, Koricheva J, Milligan H, Mueller S, Muys B, Nguyen D, Pollastrini M, Ratcliffe S, Raulund-Rasmussen K, Selvi F, Stenlid J, Valladares F, Vesterdal L, Zielínski D, Fischer M (2016) Biotic homogenization can decrease landscape-scale forest multifunctionality. Proc Natl Acad Sci U S A 113:3557–3562. doi:10.1073/pnas.1517903113
Vitousek PM, Gosz JR, Grier CC, Melillo JM, Reiners WA, Todd RL (1979) Nitrate losses from disturbed ecosystems. Science 204:469–474. doi:10.1126/science.204.4392.469
Wagg C, Bender SF, Widmer F, van der Heijden MGA (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci U S A 111:5266–5270. doi:10.1073/pnas.1320054111
Wardle DA (1998) Controls of temporal variability of the soil microbial biomass: a global-scale synthesis. Soil Biol Biochem 30:1627–1637. doi:10.1016/S0038-0717(97)00201-0
Warton DI, Wright ST, Wang Y (2012) Distance-based multivariate analyses confound location and dispersion effects. Methods Ecol Evol 3:89–101. doi:10.1111/j.2041-210X.2011.00127.x
Xiong Y, D’Atri JJ, Fu S, Xia H, Seastedt TR (2011) Rapid soil organic matter loss from forest dieback in a subalpine coniferous ecosystem. Soil Biol Biochem 43:2450–2456. doi:10.1016/j.soilbio.2011.08.013
Acknowledgements
This study was supported by the International Laboratory of Global Change (LINCGlobal), the Spanish Ministry of Economy and Competitiveness grant VERONICA (CGL2013-42271-P), the Community of Madrid grant REMEDINAL3-CM (S2013/MAE-2719) and the FCT/MEC through national funds and the co-funding by the FEDER, within the PT2020 Partnership Agreement and COMPETE 2020 (UID/BIA/04004/2013). The authors are especially grateful to David López-Quiroga, Ioanna Boudouris, Elizabeth Turcotte and Ana Prado Comesaña for their excellent help in the field and laboratory, to Dulce Flores, Teresa Morán and Aldo Barreiro for their assistance with data and statistical analysis, to Raquel Benavides for providing valuable study site information, and to Jennifer L. Morse and two anonymous reviewers for their comments on the manuscript. Meteorological data for the reference stations were provided by the Spanish Meteorological Agency (AEMET). AR was supported by the Spanish National Research Council (CSIC) in the JAE-doc modality co-financed by the European Social Fund (ESF) and by a Postdoctoral Grant of the Portuguese Science and Technology Foundation (SFRH/BDP/108913/2015).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Jeff R. Powell .
Electronic supplementary material
Table S1
(DOCX 19 kb)
Table S2
(DOCX 28 kb)
Table S3
(DOCX 27 kb)
Table S4
(DOCX 26 kb)
Table S5
(DOCX 26 kb)
Table S6
(DOCX 20 kb)
Fig. S1
Three-dimensional non-metric multidimensional scaling (NMDS) ordination, shown as 2D plot, of (a) soil bacteria and (b) soil fungi community-level physiological profiles (CLPP) and (c) herbaceous composition data for all defoliation degrees and ecotypes (n = 5). Vectors on figure (c) show grass species that strongly contributed (correlation higher than 0.6) to the NMDS ordination of the different defoliation degree and ecotype levels. Distance between points shows dissimilarity in CLPP [(a) and (b)] and species composition [(c)]. P def , P eco and P int show the significant level of the defoliation degree, the ecotype and the interaction of both, respectively (PERMANOVA). (JPEG 703 kb)
Rights and permissions
About this article
Cite this article
Rodríguez, A., Curiel Yuste, J., Rey, A. et al. Holm oak decline triggers changes in plant succession and microbial communities, with implications for ecosystem C and N cycling. Plant Soil 414, 247–263 (2017). https://doi.org/10.1007/s11104-016-3118-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-016-3118-4