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Reduction in primary production followed by rapid recovery of plant biomass in response to repeated mid-season droughts in a semiarid shrubland

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Abstract

The frequency and severity of extreme weather events, including droughts, are expected to increase due to the climate change. Climate manipulation field experiments are widely used tools to study the response of key parameters like primary production to the treatments. Our study aimed to detect the effect of drought on the aboveground biomass and primary production both during the treatments as well as during the whole growing seasons in semiarid vegetation. We estimated aboveground green biomass of vascular plants in a Pannonian sand forest-steppe ecosystem in Hungary. We applied non-destructive field remote sensing method in control and drought treatments. Drought treatment was carried out by precipitation exclusion in May and June, and was repeated in each year from 2002. We measured NDVI before the drought treatment, right after the treatment, and at the end of the summer in 2011 and 2013. We found that the yearly biomass peaks, measured in control plots after the treatment periods, were decreased or absent in drought treatment plots, and consequently, the aboveground net primary production was smaller than in the control plots. At the same time, we did not find general drought effects on all biomass data. The studied ecosystem proved resilient, as the biomass in the drought-treated plots recovered by the next drought treatment. We conclude that the effect of drought treatment can be overestimated with only one measurement at the time of the peak biomass, while multiple within-year measurements better describe the response of biomass.

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References

  • Bartholy J, Pongrácz R (2007) Regional analysis of extreme temperature and precipitation indices for the Carpathian Basin from 1946 to 2001. Glob Planet Chang 57:83–95

    Article  Google Scholar 

  • Bartholy J, Pongrácz R, Matyasovszky I, Schlanger V (2003) 4.7 Expected regional variations and changes of mean and extreme climatology of Eastern/Central Europe. In: Proceedings of the Combined Preprints CD-ROM of the 83rd AMS Annual Meeting. American Meteorological Society, Boston, p 10

  • Beier C, Emmett B, Gundersen P, Tietema A, Penuelas J, Estiarte M, Gordon C, Gorissen A, Llorens L, Roda F et al (2004) Novel approaches to study climate change effects on terrestrial ecosystems in the field: drought and passive nighttime warming. Ecosystems 7:583–597

    Article  Google Scholar 

  • Beier C, Beierkuhnlein C, Wohlgemuth T, Penuelas J, Emmett B, Körner C, Boeck H, Christensen JH, Leuzinger S, Janssens IA et al (2012) Precipitation manipulation experiments–challenges and recommendations for the future. Ecol Lett 15:899–911

    Article  PubMed  Google Scholar 

  • Boelman NT, Stieglitz M, Griffin KL, Shaver GR (2005) Inter-annual variability of NDVI in response to long-term warming and fertilization in wet sedge and tussock tundra. Oecologia 143:588–597. https://doi.org/10.1007/s00442-005-0012-9

    Article  PubMed  Google Scholar 

  • Brancaleoni L, Gualmini M, Tomaselli M, Gerdol R (2007) Responses of subalpine dwarf-shrub heath to irrigation and fertilization. J Veg Sci 18:337. https://doi.org/10.1658/1100-9233(2007)18[337:ROSDHT]2.0.CO;2

    Article  Google Scholar 

  • Byrne KM, Lauenroth WK, Adler PB (2013) Contrasting effects of precipitation manipulations on production in two sites within the central grassland region, USA. Ecosystems 16:1039–1051. https://doi.org/10.1007/s10021-013-9666-z

    Article  Google Scholar 

  • Ciais P, Reichstein M, Viovy N, Granier A, Ogée J, Allard V, Aubinet M, Buchmann N, Bernhofer C, Carrara A, Chevallier F, De Noblet N, Friend AD, Friedlingstein P, Grünwald T, Heinesch B, Keronen P, Knohl A, Krinner G, Loustau D, Manca G, Matteucci G, Miglietta F, Ourcival JM, Papale D, Pilegaard K, Rambal S, Seufert G, Soussana JF, Sanz MJ, Schulze ED, Vesala T, Valentini R (2005) Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437:529–533. https://doi.org/10.1038/nature03972

    Article  CAS  PubMed  Google Scholar 

  • Colegrave N, Ruxton GD (2018) Using biological insight and pragmatism when thinking about pseudoreplication. Trends Ecol Evol 33:28–35. https://doi.org/10.1016/j.tree.2017.10.007

    Article  PubMed  Google Scholar 

  • Cornic G, Massacci A (1996) Leaf photosynthesis under drought stress. In: Baker NR (ed) Photosynthesis and the environment. Springer, Dordrecht, pp 347–366

    Google Scholar 

  • Erdős L, Tölgyesi C, Horzse M, Tolnay D, Hurton Á, Schulcz N, Körmöczi L, Lengyel A, Bátori Z (2014) Habitat complexity of the Pannonian forest-steppe zone and its nature conservation implications. Ecol Complex 17:107–118. https://doi.org/10.1016/j.ecocom.2013.11.004

    Article  Google Scholar 

  • Estiarte M, Vicca S, Peñuelas J, Bahn M, Beier C, Emmett BA, Fay PA, Hanson PJ, Hasibeder R, Kigel J, Kröel-Dulay G, Larsen KS, Lellei-Kovács E, Limousin J-M, Ogaya R, Ourcival J-M, Reinsch S, Sala OE, Schmidt IK, Sternberg M, Tielbörger K, Tietema A, Janssens IA (2016) Few multiyear precipitation-reduction experiments find a shift in the productivity-precipitation relationship. Glob Chang Biol 22:2570–2581. https://doi.org/10.1111/gcb.13269

    Article  PubMed  Google Scholar 

  • Fekete G, Molnár Z, Kun A, Botta-Dukát Z (2002) On the structure of the Pannonian forest steppe: grasslands on sand. Acta Zool Hung 48:137–150

    Google Scholar 

  • Filella I, Penuelas J, Llorens L, Estiarte M (2004) Reflectance assessment of seasonal and annual changes in biomass and CO2 uptake of a Mediterranean shrubland submitted to experimental warming and drought. Remote Sens Environ 90:308–318. https://doi.org/10.1016/j.rse.2004.01.010

    Article  Google Scholar 

  • Gamon JA, Field CB, Goulden ML, Griffin KL, Hartley AE, Joel G, Penuelas J, Valentini R (1995) Relationships between NDVI, canopy structure, and photosynthesis in three Californian vegetation types. Ecol Appl 5:28–41. https://doi.org/10.2307/1942049

    Article  Google Scholar 

  • Goodin DG, Henebry GM (1997) A technique for monitoring ecological disturbance in tallgrass prairie using seasonal NDVI trajectories and a discriminant function mixture model. Remote Sens Environ 61:270–278. https://doi.org/10.1016/S0034-4257(97)00043-6

    Article  Google Scholar 

  • Hoover DL, Knapp AK, Smith MD (2014) Resistance and resilience of a grassland ecosystem to climate extremes. Ecology 95:2646–2656. https://doi.org/10.1890/13-2186.1

    Article  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363

    Article  PubMed  Google Scholar 

  • 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. Cambridge University Press, New York, NY

  • Köchy M, Wilson SD (2004) Semiarid grassland responses to short-term variation in water availability. Plant Ecol 174:197–203. https://doi.org/10.1023/B:VEGE.0000049098.74147.57

    Article  Google Scholar 

  • Kovács-Láng E (1974) Examination of dynamics of organic matter in a perennial open sandy steppe-meadow (Festucetum vaginatae danubiale) at the Csévharaszt IBP sample area (Hungary). Acta Bot Acad Sci Hung 20:309–326

    Google Scholar 

  • Kovács-Láng E, Kröel-Dulay G, Kertész M, Fekete G, Bartha S, Mika J, Dobi-Wantuch I, Rédei T, Rajkai K, Hahn I et al (2000) Changes in the composition of sand grasslands along a climatic gradient in Hungary and implications for climate change. Phytocoenologia 30(3):385–407

    Article  Google Scholar 

  • Kröel-Dulay G, Ransijn J, Schmidt IK, Beier C, De Angelis P, de Dato G, Dukes JS, Emmett B, Estiarte M, Garadnai J, Kongstad J, Kovács-Láng E, Larsen KS, Liberati D, Ogaya R, Riis-Nielsen T, Smith AR, Sowerby A, Tietema A, Penuelas J (2015) Increased sensitivity to climate change in disturbed ecosystems. Nat Commun 6:6682. https://doi.org/10.1038/ncomms7682

    Article  PubMed  Google Scholar 

  • Lellei-Kovács E, Kovács-Láng E, Kalapos T, Botta-Dukat Z (2008a) Soil respiration and its main limiting factors in a semiarid sand forest-steppe ecosystem-results of a climate simulation experiment. Cereal Res Commun 36:1223–1226

    Google Scholar 

  • Lellei-Kovács E, Kovács-Láng E, Kalapos T, Botta-Dukát Z, Barabás S, Beier C (2008b) Experimental warming does not enhance soil respiration in a semiarid temperate forest-steppe ecosystem. Commun Ecol 9:29–37

    Article  Google Scholar 

  • Lenth RV (2016) Least-squares means: the R package {lsmeans}. J Stat Softw 69:1–33. https://doi.org/10.18637/jss.v069.i01

    Article  Google Scholar 

  • Mänd P, Hallik L, Peñuelas J, Nilson T, Duce P, Emmett BA, Beier C, Estiarte M, Garadnai J, Kalapos T (2010) Responses of the reflectance indices PRI and NDVI to experimental warming and drought in European shrublands along a north–south climatic gradient. Remote Sens Environ 114:626–636. https://doi.org/10.1016/j.rse.2009.11.003

    Article  Google Scholar 

  • Miranda JD, Armas C, Padilla FM, Pugnaire FI (2011) Climatic change and rainfall patterns: effects on semi-arid plant communities of the Iberian Southeast. J Arid Environ 75:1302–1309. https://doi.org/10.1016/j.jaridenv.2011.04.022

    Article  Google Scholar 

  • Molnár Z, Biró M, Bartha S, Fekete G, Dúbravková D, Hajnalová M (2012) Eurasian steppes. In: Werger JAM, van Staalduinen AM (eds) Ecological problems and livelihoods in a changing world. Springer, Dordrecht

    Google Scholar 

  • Mulla DJ (2013) Twenty five years of remote sensing in precision agriculture: key advances and remaining knowledge gaps. Biosyst Eng 114:358–371. https://doi.org/10.1016/j.biosystemseng.2012.08.009

    Article  Google Scholar 

  • Nagy Z, Pintér K, Czóbel S, Balogh J, Horváth L, Fóti S, Barcza Z, Weidinger T, Csintalan Z, Dinh NQ, Grosz B, Tuba Z (2007) The carbon budget of semi-arid grassland in a wet and a dry year in Hungary. Agric Ecosyst Environ 121:21–29. https://doi.org/10.1016/j.agee.2006.12.003

    Article  CAS  Google Scholar 

  • Nestola E, Calfapietra C, Emmerton C, Wong C, Thayer D, Gamon J (2016) Monitoring grassland seasonal carbon dynamics, by integrating MODIS NDVI, proximal optical sampling, and eddy covariance measurements. Remote Sens 8:260. https://doi.org/10.3390/rs8030260

    Article  Google Scholar 

  • Ónodi G, Kertész M, Kovács-Láng E, Ódor P, Botta-Dukát Z, Lhotsky B, Barabás S, Mojzes A, Kröel-Dulay G (2017a) Estimating aboveground herbaceous plant biomass via proxies: the confounding effects of sampling year and precipitation. Ecol Indic 79:355–360. https://doi.org/10.1016/j.ecolind.2017.04.011

    Article  Google Scholar 

  • Ónodi G, Kröel-Dulay G, Kovács-Láng E, Ódor P, Botta-Dukat Z, Lhotsky B, Barabás S, Garadnai J, Kertész M (2017b) Comparing the accuracy of three non-destructive methods in estimating aboveground plant biomass. Commun Ecol 18:56–62. https://doi.org/10.1556/168.2017.18.1.7

    Article  Google Scholar 

  • Peñuelas J, Prieto P, Beier C, Cesaraccio C, De Angelis P, de Dato G, Emmett BA, Estiarte M, Garadnai J, Gorissen A et al (2007) Response of plant species richness and primary productivity in shrublands along a north–south gradient in Europe to seven years of experimental warming and drought: reductions in primary productivity in the heat and drought year of 2003. Glob Chang Biol 13:2563–2581

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2017) nlme: Linear and nonlinear mixed effects models. Retrieved from https://CRAN.R-project.org/package=nlme

  • Pintér K, Barcza Z, Balogh J, Czóbel S, Csintalan Z, Tuba Z, Nagy Z (2008) Interannual variability of grasslands’ carbon balance depends on soil type. Commun Ecol 9:43–48. https://doi.org/10.1556/ComEc.9.2008.S.7

    Article  Google Scholar 

  • Pontailler J-Y, Hymus GJ, Drake BG (2003) Estimation of leaf area index using ground-based remote sensed NDVI measurements: validation and comparison with two indirect techniques. Can J Remote Sens 29:381–387. https://doi.org/10.5589/m03-009

    Article  Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing

  • Reinsch S, Koller E, Sowerby A, de Dato G, Estiarte M, Guidolotti G, Kovács-Láng E, Kröel-Dulay G, Lellei-Kovács E, Larsen KS, Liberati D, Peñuelas J, Ransijn J, Robinson DA, Schmidt IK, Smith AR, Tietema A, Dukes JS, Beier C, Emmett BA (2017) Shrubland primary production and soil respiration diverge along European climate gradient. Sci Rep 7:43952. https://doi.org/10.1038/srep43952

    Article  PubMed  PubMed Central  Google Scholar 

  • Rouse JW, Haas RH, Deering DW, Schell JA, Harlan JC (1974) Monitoring the vernal advancement and retrogradation (green wave effect) of natural vegetation. NASA/GSFCT Type III Final Report, Greenbelt, MD, USA

  • Sala OE, Austin AT (2000) Methods of estimating aboveground net primary productivity. In: Sala OE, Jackson RB, Mooney HA, Howarth RH (eds) Methods in ecosystem science. Springer, Dordrecht, pp 31–43

    Chapter  Google Scholar 

  • Scurlock JMO, Johnson K, Olson RJ (2002) Estimating net primary productivity from grassland biomass dynamics measurements. Glob Chang Biol 8:736–753. https://doi.org/10.1046/j.1365-2486.2002.00512.x

    Article  Google Scholar 

  • Shinoda M, Nachinshonhor GU, Nemoto M (2010) Impact of drought on vegetation dynamics of the Mongolian steppe: a field experiment. J Arid Environ 74:63–69. https://doi.org/10.1016/j.jaridenv.2009.07.004

    Article  Google Scholar 

  • Tielbörger K, Bilton MC, Metz J, Kigel J, Holzapfel C, Lebrija-Trejos E, Konsens I, Parag HA, Sternberg M (2014) Middle-Eastern plant communities tolerate 9 years of drought in a multi-site climate manipulation experiment. Nat Commun 5:5102. https://doi.org/10.1038/ncomms6102

    Article  PubMed  PubMed Central  Google Scholar 

  • Vicente-Serrano SM, Gouveia C, Camarero JJ, Beguería S, Trigo R, López-Moreno JI, Azorín-Molina C, Pasho E, Lorenzo-Lacruz J, Revuelto J, Morán-Tejeda E, Sanchez-Lorenzo A (2013) Response of vegetation to drought time-scales across global land biomes. Proc Natl Acad Sci USA 110:52–57. https://doi.org/10.1073/pnas.1207068110

    Article  CAS  PubMed  Google Scholar 

  • Wang R, Gamon J, Montgomery R, Townsend P, Zygielbaum A, Bitan K, Tilman D, Cavender-Bares J (2016) Seasonal variation in the NDVI–species richness relationship in a prairie grassland experiment (Cedar Creek). Remote Sens 8:1–15. https://doi.org/10.3390/rs8020128

    Google Scholar 

  • Wu Z, Dijkstra P, Koch GW, Peñuelas J, Hungate BAR (2011) Responses of terrestrial ecosystems to temperature and precipitation change: a meta-analysis of experimental manipulation. Glob Chang Biol 17:927–942. https://doi.org/10.1111/j.1365-2486.2010.02302.x

    Article  Google Scholar 

  • Zhao M, Running SW (2010) Drought-induced reduction in global terrestrial net primary production from 2000 through 2009. Science 80(329):940–943

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects modelling for nested data. In: Zuur AF (ed) Mixed effects models and extensions in ecology with R. Springer, Dordrecht, pp 101–142

    Chapter  Google Scholar 

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Acknowledgements

This study was funded by the VULCAN project (EU FP5 Grant EVK2-CT-2000-00094), the INCREASE project (EU FP7 Grant 227628), the Hungarian Scientific Research Fund (OTKA K112576), and the National Research, Development and Innovation Office (GINOP 2.3.3-15-2016-00019). We are grateful to the Kiskunság National Park (Hungary) for the support of our field work. The authors thank the anonymous reviewers of this manuscript for their valuable comments which have helped us to improve the quality of the paper.

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Authors and Affiliations

  1. MTA Centre for Ecological Research, Institute of Ecology and Botany, Alkotmány 2-4, 2163, Vácrátót, Hungary

    G. Ónodi, Z. Botta-Dukát, Gy. Kröel-Dulay, E. Lellei-Kovács & M. Kertész

  2. MTA Centre for Ecological Research, GINOP Sustainable Ecosystems Group, Klebelsberg Kuno 3, 8237, Tihany, Hungary

    G. Ónodi, Z. Botta-Dukát, Gy. Kröel-Dulay & M. Kertész

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  1. G. Ónodi
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  2. Z. Botta-Dukát
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  3. Gy. Kröel-Dulay
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  4. E. Lellei-Kovács
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Correspondence to G. Ónodi.

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Communicated by Julie C. Zinnert.

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Ónodi, G., Botta-Dukát, Z., Kröel-Dulay, G. et al. Reduction in primary production followed by rapid recovery of plant biomass in response to repeated mid-season droughts in a semiarid shrubland. Plant Ecol 219, 517–526 (2018). https://doi.org/10.1007/s11258-018-0814-6

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