Skip to main content

Advertisement

SpringerLink
Log in

Plant mortality on ultramafic soils after an extreme heat and drought event in the Mediterranean area

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

Plant mortality associated with the growing frequency and intensity of heatwaves and dry spells is increasingly occurring in various ecosystems worldwide. However, the impacts of extreme events on plant communities of ultramafic soils are still unknown. Here, we describe a first case of plant mortality on serpentine outcrops in Italy following a heat and drought event that occurred between autumn 2016 and summer 2017.

Methods

Mortality of perennial plants was assessed in thirty plots representing ten major serpentine areas along a SW-NE gradient, with the sparse vegetation of ultramafic soils. Statistical modelling was based on temperature and precipitation data and local site conditions.

Results

Responses of single species were largely different and not related to their taxonomic position, growth form or level of edaphic specialization for serpentine soils. Notably, obligate serpentine endemics were not less impacted than non-endemics. As expected, species mortality decreased with increasing chromosome number, suggesting higher tolerance and adaptive capacity in taxa of likely polyploid origin. Mortality increased with decreasing number of rainy days and duration of the heatwave and decreased with increasing distance from the Tyrrhenian coastline, reaching 60% in the southern and western areas with a Mediterranean climate. Local site conditions such as increasing soil depth and north-facing aspect significantly increased plant survivorship.

Conclusions

Our findings show that extreme drought and heat can have a previously unrealized impact on ultramafic plant communities in the short term. Further studies should examine the recovery capacity and resilience of serpentine plants, together with the long term effects.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH, Gonzalez P, Fensham R (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684

    Google Scholar 

  • Appels R, Morris R, Gill BS, May CE (1998) Chromosome Biology, pp. 67–84. Springer

  • Baldi M, Dalu G, Maracchi G, Pasqui M, Cesarone F (2006) Heat waves in the Mediterranean: a local feature or a larger-scale effect? Int. J. Climatol. 26(11):1477–1487

    Google Scholar 

  • Barton K (2019) MuMIn: Multi-Model Inference. R package version 1(43):15

    Google Scholar 

  • Blasi C (2010) La vegetazione d’Italia. Palombi Ed, Roma

    Google Scholar 

  • Boulding EG (2009) Genetic Diversity, Adaptive Potential, and Population Viability in Changing Environments. In: Carroll SP, Fox CW (Eds), Conservation Biology. Evolution in Action, 1° Ed., chapter 13. Oxford University Press pp 199

  • Bristiel P, Roumet C, Violle C, Volaire F (2019) Coping with drought: root trait variability within the perennial grass Dactylis glomerata captures a trade-off between dehydration avoidance and dehydration tolerance. Plant Soil 434: 327–342. doi: 10.1007

  • Brooks RR (1987) Serpentine and its Vegetation. Dioscorides Press, Portland, Oregon

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Second edition. Springer-Verlag, New York, pp 528

  • Cacho NI, Strauss SY (2014) Occupation of bare habitats, an evolutionary precursor to soil specialization in plants. Proc Nat Acad Sci USA 111:15132–15137

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chiarucci A (2003) Vegetation ecology and conservation on Tuscan ultramafic soils. Bot Rev 69(3):252–268

    Google Scholar 

  • Chiarucci A, Foggi B, Selvi F (1995) Garrigue plant communities of ultramafic outcrops of Tuscany (Central Italy). Webbia 49:179–192

    Google Scholar 

  • Chiarucci A, Robinson BH, Bonini I, Petit D, Brooks RR, De Dominicis V (1998) Vegetation of Tuscan ultramafic soils in relation to edaphic and physical factors. Folia Geobot 33(2):113–131

    Google Scholar 

  • Copeland SM, Harrison SP, Latimer AM, Damschen EI, Eskelinen AM, Fernandez-Going B, Spasojevic MJ, Anacker BL, Thorne JH (2016) Ecological effects of extreme drought on Californian herbaceous plant communities. Ecol Monogr 86:295–311

    Google Scholar 

  • Corlett RT, Tomlinson KW (2020) Climate Change and Edaphic Specialists: Irresistible Force Meets Immovable Objects ? Trends Ecol Evol 35:367–376

    PubMed  Google Scholar 

  • Crouchet SE, Jensen J, Schwartz BF, Schwinning S (2019) Tree mortality after a hot drought: distinguishing density-dependent and -independent drivers and why it matters. Front For Glob Change 2:1–21

    Google Scholar 

  • Damschen EI, Harrison S, Ackerly DD, Fernandez-Going B, Anacker BL (2012) Endemic plant communities on special soils: early victims or hardy survivors of climate change? J Ecol 100:1112–1130

    Google Scholar 

  • Fan Y, Miguez-Macho G, Jobbágy EG, Jackson RB, Otero-Casal C (2017) Hydrologic regulation of plant rooting depth. Proc Nat Acad Sci USA 114:10572–10577

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandez-Going BM, Anacker BL, Harrison SP (2012) Temporal variability in California grasslands: soil type and species functional traits mediate response to precipitation. Ecology 93:2104–2114

    CAS  PubMed  Google Scholar 

  • Fernandez-Going BM, Harrison S (2013) Effects of experimental water addition depend on grassland community characteristics. Plant Ecol 214:777–786. https://doi.org/10.1007/s11258-013-0207-9

    Article  Google Scholar 

  • Ghasemi R, Chavoshi ZZ, Boyd RS, Rajakaruna ND (2015) Calcium:magnesium ratio affects environmental stress sensitivity in the serpentine-endemic Alyssum inflatum (Brassicaceae). Austral J Bot 63:39–46

    CAS  Google Scholar 

  • Gitlin AR, Sthultz CM, Bowker MA, Stumpf PKL, Kennedy K, Munoz A, Bailey JK, Whitham TG (2006) Mortality gradients within and among dominant plant populations as barometers of ecosystem change during extreme drought. Conserv Biol 20:1477–1486

    PubMed  Google Scholar 

  • Godfree RC, Marshall DJ, Young AG, Miller CH, Mathews S (2017) Empirical evidence of fixed and homeostatic patterns of polyploid advantage in a keystone grass exposed to drought and heat stress. R Soc Open Sci 4:170934

    PubMed  PubMed Central  Google Scholar 

  • Hall AE (2001) Crop Responses to Environment. CRC Press LLC, Boca Raton, Florida

    Google Scholar 

  • Hao G-Y, Lucero ME, Sanderson SC, Zacharias EH, Holbrook NM (2013) Polyploidy enhances the occupation of heterogeneous environments through hydraulic related trade-offs in Atriplex canescens (Chenopodiaceae). New Phytol 197:970–978

    PubMed  Google Scholar 

  • Hare RC (1961) Heat effects on living plants. US Dep Agr Occas Pap 183:1–32

    Google Scholar 

  • Harrison SP, Damschen EI, Fernandez-Going B (2009) Climate Gradients, Climate Change, and Special Edaphic Floras. Northeastern Naturalist 16:121–130

    Google Scholar 

  • Harrison SP, Damschen EI, Fernandez-Going B, Eskelinen AM, Copeland S (2015) Plant communities on infertile soils are less sensitive to climate change. Ann Bot 116:1017–1022

    PubMed  Google Scholar 

  • Hidalgo-Triana N, Pérez Latorre AV (2018) Thorne JH (2018) Plant functional traits and groups in a Californian serpentine chaparral. Ecol Res 33:525–535. https://doi.org/10.1007/s11284-017-1532-6

  • IPCC (2018) Global Warming of 1.5°C. An IPCC Special Report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty [Masson-Delmotte, V., P. Zhai, H.-O. Pörtner, D. Roberts, J. Skea, P.R. Shukla, A. Pirani, W. Moufouma-Okia, C. Péan, R. Pidcock, S. Connors, J.B.R. Matthews, Y. Chen, X. Zhou, M.I. Gomis, E. Lonnoy, T. Maycock, M. Tignor, and T. Waterfield (eds.)]. In Press. Available at  https://www.ipcc.ch/sr15/. Accessed 24 Sep 2021

  • IPCC (2019) Climate Change and Land: an IPCC special report on climate change, desertification, land degradation, sustainable land management, food security, and greenhouse gas fluxes in terrestrial ecosystems [P.R. Shukla, J. Skea, E. Calvo Buendia, V. Masson-Delmotte, H.-O. Pörtner, D. C. Roberts, P. Zhai, R. Slade, S. Connors, R. van Diemen, M. Ferrat, E. Haughey, S. Luz, S. Neogi, M. Pathak, J. Petzold, J. Portugal Pereira, P. Vyas, E. Huntley, K. Kissick, M. Belkacemi, J. Malley, (eds.)]. In press. Available at https://www.ipcc.ch/srccl/. Accessed 24 Sep 2021

  • Loarie SR, Carter BE, Hayhoe K, McMahon S, Moe R, Knight CA, Ackerly DD (2008) Climate Change and the Future of California's Endemic Flora. PLoS ONE 3(6):e2502. https://doi.org/10.1371/journal.pone.0002502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krause W (1958) Andere Bodenspezialisten. In: Handbuch der Pflanzenphysiologie v. 4. Springer Berlin, 755–806

  • Kruckeberg AR (2002) Geology and Plant Life. University of Washington Press

  • Lazzarotto A (1993) Elementi di Geologia. In: Giusti F (ed) La storia naturale della Toscana meridionale. Pizzi, Siena, pp 19–87

    Google Scholar 

  • Levin DA (2019) Plant speciation in the age of climate change. Ann Bot 124:769–775

    PubMed  PubMed Central  Google Scholar 

  • Magno R, De Filippis T, Di Giuseppe E, Pasqui M, Rocchi L, Gozzini B (2018) Semi-Automatic operational service for drought monitoring and forecasting in the Tuscany region. Geosciences 8:49. https://doi.org/10.3390/geosciences8020049

    Article  Google Scholar 

  • Maherali H, Walden AE, Husband BC (2009) Genome duplication and the evolution of physiological responses to water stress. New Phytol 184:721–731

    CAS  PubMed  Google Scholar 

  • Malpas J (1992) Serpentine and geology of serpentinised rocks. In: Roberts BA, Proctor J (eds) The ecology of areas with serpentinized rocks – a world view. Kluwer Academic Publishers, Dordrecht, pp 7–30

    Google Scholar 

  • McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739

    PubMed  Google Scholar 

  • Meehl GA, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305:994–997

    CAS  PubMed  Google Scholar 

  • Onyekachi OG, Boniface OO, Gemlack NF, Nicholas N (2019) The effect of climate change on abiotic plant stress: A review. Abiotic and Biotic Stress in Plants. https://doi.org/10.5772/intechopen.82681

  • Padilla FM, Pugnaire FI (2007) Rooting depth and soil moisture control Mediterranean woody seedling survival during drought. Funct Ecol 21:489–495

    Google Scholar 

  • Perkins SE, Alexander LV, Nairn JR (2012) Increasing frequency, intensity and duration of observed global heatwaves and warm spells. Geophys Res Lett 39:L20714

    Google Scholar 

  • Pignatti S (2005) Valori di Bioindicazione delle piante vascolari della Flora d'Italia. Braun-Blanquetia 39:1–97

    Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D (2019) nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-143. https://CRAN.R-project.org/package=nlme. Accessed 18 Dec 2019

  • Pollastrini M, Puletti N, Selvi F, Iacopetti G, Bussotti F (2019) Widespread crown defoliation after a drought and heat wave in the forests of Tuscany (Central Italy) and their recovery—A case study from summer 2017. Front For Glob Change 2:1–8

    Google Scholar 

  • R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/. Accessed 18 Dec 2019

  • Rao S, Tian Y, Xia X, Li Y, Chen J (2020) Chromosome doubling mediates superior drought tolerance in Lycium ruthenicum via abscisic acid signaling. Hortic Res 7:40

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rajakaruna N (2017) Lessons on evolution from the study of edaphic specialization. Bot Rev 84:39–78

    Google Scholar 

  • Richards SA (2008) Dealing with overdispersed count data in applied ecology. J Appl Ecol 45:218–227

    Google Scholar 

  • Sade N, Gebremedhin A, Moshelion M (2012) Risk-taking plants: anisohydric behavior as a stress-resistance trait. Pl Signal Behav 7(7):767–770

    CAS  Google Scholar 

  • Selvi F (2007) Diversity, geographic variation and conservation of the serpentine flora of Tuscany (Italy). Biodiv Cons 16:1423–1439

    Google Scholar 

  • Selvi F, Carrari E, Colzi I, Coppi A, Gonnelli C (2017) Responses of serpentine plants to pine invasion: Vegetation diversity and nickel accumulation in species with contrasting adaptive strategies. Sci Tot Environ 595:72–80

    CAS  Google Scholar 

  • Senf C, Pflugmacher D, Zhiqiang Y, Sebald J, Knorn J, Neumann M, Hostert P, Seidl R (2018) Canopy mortality has doubled in Europe’s temperate forests over the last three decades. Nat Commun 9:4978. https://doi.org/10.1038/s41467-018-07539-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sessa EB (2019) Polyploidy as a mechanism for surviving global change. New Phytol 221:5–6

    PubMed  Google Scholar 

  • Sianta SA, Kay KM (2019) Adaptation and divergence in edaphic specialists and generalists: serpentine soil endemics in the California flora occur in barer serpentine habitats with lower soil calcium levels than serpentine tolerators. Am J Bot 106(5):690–703

    PubMed  Google Scholar 

  • Van de Peer Y, Mizrachi E, Marchal K (2017) The evolutionary significance of polyploidy. Nat Rev Genet 18:411–424

    PubMed  Google Scholar 

  • Thuiller W, Lavorel S, Araújo MB, Sykes MT, Prentice IC (2005) Climate change threats to plant diversity in Europe. Proc Natl Acad Sci USA 102: 8245–8250.Vergnano Gambi O (1992) The distribution and ecology of the vegetation of ultramafic soils in Italy. In: Roberts BA, Proctor J (eds) The Ecology of Areas with Serpentinized Rocks-A World View. Kluwer Academic Publishers, Dordrecht, pp 217–247

    Google Scholar 

  • Vogel J, Paton E, Aich V, Bronstert A (2021) Increasing compound warm spells and droughts in the Mediterranean Basin. Weather Clim. Extrem 32:100312

    Google Scholar 

  • Whiting SN, Reeves RD, Richards D, Johnson MS, Cooke JA, Malaisse F, Paton A, Smith JAC, Angle JS, Chaney RL, Ginocchio R, Jaffré T, Johns R, McIntyre T, Purvis OW, Salt DE, Schat H, Zhao FJ, Baker AJM (2004) Research priorities for conservation of metallophyte biodiversity and their potential for restoration and site remediation. Restor Ecol 12:106–116

    Google Scholar 

  • Wójcik M, Gonnelli C, Selvi F, Dresler S, Rostański A, Vangronsveld J (2017) Metallophytes of serpentine and calamine soils –their unique ecophysiology and potential for phytoremediation. Adv Bot Res 83:1–42

    Google Scholar 

  • Wright HA (1970) A Method to Determine Heat-Caused Mortality in Bunchgrasses. Ecology 51:582–587

    Google Scholar 

Download references

Acknowledgments

Authors wish to acknowledge Isabella Bettarini for valuable help during field work, Filippo Bussotti and Martina Pollastrini for useful discussion on plant mortality associated with climate extremes. We would also like to thank Ilaria Colzi for critical reading our manuscript and providing valuable comments. We finally wish to thank three anonymous reviewers whose comments/suggestions helped to improve the first version of our manuscript.

Availability of data and material

All data are provided as supplementary materials

Funding

Research funds to FS from the Italian Ministry for University and Research and University of Firenze are acknowledged.

Author information

Authors and Affiliations

  1. Department of Biology, University of Firenze, Via P.A. Micheli 1, I-50121, Florence, Italy

    Andrea Coppi

  2. Department of Biology, University of Firenze, Via G. La Pira 4, I-50121, Florence, Italy

    Lorenzo Lazzaro

  3. Department of Agriculture, Food, Environment and Forestry, Laboratories of Botany, University of Firenze, Piazzale delle Cascine 28, I-50144, Florence, Italy

    Federico Selvi

Authors
  1. Andrea Coppi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lorenzo Lazzaro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Federico Selvi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

FS conceived the ideas and designed the methodology and collected the data. LL and FS analysed and interpreted the data. AC, FS and LL led the writing of the manuscript and contributed critically to the drafts and gave final approval for publication.

Corresponding author

Correspondence to Lorenzo Lazzaro.

Ethics declarations

Conflicts of interest/Competing interests (include appropriate disclosures)

The authors declare no competing interests.

Code availability

'Not applicable'

Additional information

Responsible Editor: Susan Schwinning

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(DOCX 710 kb)

ESM 2

(XLSX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Coppi, A., Lazzaro, L. & Selvi, F. Plant mortality on ultramafic soils after an extreme heat and drought event in the Mediterranean area. Plant Soil 471, 123–139 (2022). https://doi.org/10.1007/s11104-021-05179-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-021-05179-2

Keywords

Search

Navigation