Plant’s gypsum affinity shapes responses to specific edaphic constraints without limiting responses to other general constraints

Abstract

Aims

Harsh edaphic environments harbor species with different soil affinities. Plant’s responses to specific edaphic constraints may be compromised against responses to prevalent stresses shared with other semi-arid environments. We expect that species with high edaphic affinity may show traits to overcome harsh soil properties, while species with low affinity may respond to environmental constraints shared with arid environments.

Methods

We quantified the edaphic affinity of 12 plant species co-occurring in gypsum outcrops and measured traits related to plant responses to specific gypsum constraints (rooting and water uptake depth, foliar accumulation of Ca, S and Mg), and traits related to common constraints of arid environments (water use efficiency, macronutrients foliar content).

Results

Plants in gypsum outcrops differed in their strategies to face edaphic limitations. A phylogenetic informed PCA segregated species based on their foliar Ca and S accumulation and greater water uptake depths, associated with plant responses to specific gypsum limitations. Species’ gypsum affinity explained this segregation, but traits related to water or nutrient use efficiency did not contribute substantially to this axis.

Conclusions

Plant’s specializations to respond to specific edaphic constraints of gypsum soils do not limit their ability to deal with other non-specific environmental constraints.

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Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  1. Ajmal Khan M, Ungar IA, Showalter AM (2000) Effects of salinity on growth, water relations and ion accumulation of the subtropical perennial halophyte, Atriplex griffithii var. stocksii. Ann Bot 85:225–232. https://doi.org/10.1006/anbo.1999.1022

    CAS  Article  Google Scholar 

  2. Allison GB, Barnes CJ, Hughes MW (1983) The distribution of deuterium and 18O in dry soils 2. Exp J Hydrol 64:377–397. https://doi.org/10.1016/0022-1694(83)90078-1

    CAS  Article  Google Scholar 

  3. Aston MJ, Lawlor DW (1979) The relationship between transpiration, root water uptake, and leaf water potential. J Exp Bot 30:169–181

    Article  Google Scholar 

  4. Barbeta A, Peñuelas J (2017) Relative contribution of groundwater to plant transpiration estimated with stable isotopes. Sci Rep 7. https://doi.org/10.1038/s41598-017-09643-x

  5. Barbeta A, Jones SP, Clavé L et al (2019) Unexplained hydrogen isotope offsets complicate the identification and quantification of tree water sources in a riparian forest. Hydrol Earth Syst Sci 23:2129–2146. https://doi.org/10.5194/hess-23-2129-2019

    CAS  Article  Google Scholar 

  6. Barbour MM (2007) Stable oxygen isotope composition of plant tissue: a review. Funct Plant Biol 34:83–94. https://doi.org/10.1071/FP06228

    CAS  Article  PubMed  Google Scholar 

  7. Barbour MM, Fischer RA, Sayre KD, Farquhar GD (2000) Oxygen isotope ratio of leaf and grain material correlates with stomatal conductance and grain yield in irrigated wheat. Funct Plant Biol 27:625. https://doi.org/10.1071/PP99041

    CAS  Article  Google Scholar 

  8. Bridges EM, Burnham CP (1980) Soils of the state of Bahrain. J Soil Sci 31:689–707. https://doi.org/10.1111/j.1365-2389.1980.tb02115.x

    Article  Google Scholar 

  9. Brooks JR, Flanagan LB, Buchmann N, Ehleringer JR (1997) Carbon isotope composition of boreal plants: functional grouping of life forms. Oecologia 110:301–311. https://doi.org/10.2307/4221610

    CAS  Article  PubMed  Google Scholar 

  10. Brunel JP, Walker GR, Kennett-Smith AK (1995) Field validation of isotopic procedures for determining sources of water used by plants in a semi-arid environment. J Hydrol 167:351–368. https://doi.org/10.1016/0022-1694(94)02575-V

    CAS  Article  Google Scholar 

  11. Büchi L, Vuilleumier S (2014) Coexistence of specialist and generalist species is shaped by dispersal and environmental factors. Am Nat 183:612–624. https://doi.org/10.1086/675756

    Article  PubMed  Google Scholar 

  12. Cera A, Montserrat-Martí G, Ferrio JP et al (2020) Gypsum-exclusive plants accumulate more leaf S than non-exclusive species both in and off gypsum. Environ Exp Bot 182:104294. https://doi.org/10.1016/j.envexpbot.2020.104294

    CAS  Article  Google Scholar 

  13. Chen H, Jiang JG (2010) Osmotic adjustment and plant adaptation to environmental changes related to drought and salinity. Environ Rev 18:309–319

    Article  Google Scholar 

  14. Chesson P (2000) Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31:343–366. https://doi.org/10.1146/annurev.ecolsys.31.1.343

    Article  Google Scholar 

  15. Cienciala E, Lindroth A, Čermák J et al (1994) The effects of water availability on transpiration, water potential and growth of Picea abies during a growing season. J Hydrol 155:57–71. https://doi.org/10.1016/0022-1694(94)90158-9

    Article  Google Scholar 

  16. Damschen EI, Harrison S, Ackerly DD et al (2012) Endemic plant communities on special soils: early victims or hardy survivors of climate change? J Ecol 100:1122–1130. https://doi.org/10.1111/j.1365-2745.2012.01986.x

    Article  Google Scholar 

  17. Dansgaard W (1964) Stable isotopes in precipitation. Tellus 16:436–468. https://doi.org/10.1111/j.2153-3490.1964.tb00181.x

    Article  Google Scholar 

  18. Dawson TE, Mambelli S, Plamboeck AH et al (2002) Stable isotopes in plant ecology. Annu Rev Ecol Syst 33:507–559. https://doi.org/10.1146/annurev.ecolsys.33.020602.095451

    Article  Google Scholar 

  19. Duvigneaud P, Denaeyer-de Smet S (1966) Accumulation du soufre dans quelques espèces gypsophiles d’Espagne. Bull la Société R Bot Belgique 99:263–269

    Google Scholar 

  20. Ehleringer JR, Dawson TE (1992) Water uptake by plants: perspectives from stable isotope composition. Plant Cell Environ 15:1073–1082. https://doi.org/10.1111/j.1365-3040.1992.tb01657.x

    CAS  Article  Google Scholar 

  21. Ehleringer JR, Osmond CB (1989) Stable isotopes. In: Pearcy RW, Ehleringer JR, Mooney HA, Rundel PW (eds) Plant Physiological Ecology. Kluwer Academic Publishers, London, pp 281–300

    Google Scholar 

  22. Ellsworth PZ, Williams DG (2007) Hydrogen isotope fractionation during water uptake by woody xerophytes. Plant Soil 291:93–107. https://doi.org/10.1007/s11104-006-9177-1

    CAS  Article  Google Scholar 

  23. Escudero PS, Maestre F, Luzuriaga A (2015) Plant life on gypsum: a review of its multiple facets. Biol Rev 90:1–18. https://doi.org/10.1111/brv.12092

    Article  PubMed  Google Scholar 

  24. Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Funct Plant Biol 11:539. https://doi.org/10.1071/PP9840539

    CAS  Article  Google Scholar 

  25. Farquhar GD, Cernusak LA, Barnes B (2007) Heavy water fractionation during transpiration. Plant Physiol 143:11–18. https://doi.org/10.1104/pp.106.093278

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. Flowers TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Annu Rev Plant Physiol 28:89–121. https://doi.org/10.1146/annurev.pp.28.060177.000513

    CAS  Article  Google Scholar 

  27. Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–233. https://doi.org/10.1146/annurev.es.19.110188.001231

    Article  Google Scholar 

  28. Guerrero Campo J, Alberto F, Hodgson J et al (1999a) Plant community patterns in a gypsum area of NE Spain. I. Interactions with topographic factors and soil erosion. J Arid Environ 41:401–410. https://doi.org/10.1006/JARE.1999.0492

    Article  Google Scholar 

  29. Guerrero Campo J, Alberto F, Maestro M et al (1999b) Plant community patterns in a gypsum area of NE Spain. II. Effects of ion washing on topographic distribution of vegetation. J Arid Environ 41:411–419. https://doi.org/10.1006/jare.1999.0493

    Article  Google Scholar 

  30. Jasmin J-N, Kassen R (2007) On the experimental evolution of specialization and diversity in heterogeneous environments. Ecol Lett 10:272–281. https://doi.org/10.1111/j.1461-0248.2007.01021.x

    Article  PubMed  Google Scholar 

  31. Levine JM, HilleRisLambers J (2009) The importance of niches for the maintenance of species diversity. Nature 461:254–257. https://doi.org/10.1038/nature08251

    CAS  Article  PubMed  Google Scholar 

  32. Levins R (1968) Evolution in changing environments; some theoretical explorations. Princeton University Press, Princeton

  33. Marschner P (2012) Marschner’s mineral nutrition of higher plants. Elsevier, London

    Google Scholar 

  34. Martín-Gómez P, Barbeta A, Voltas J et al (2015) Isotope-ratio infrared spectroscopy: A reliable tool for the investigation of plant-water sources? New Phytol 207:914–927. https://doi.org/10.1111/nph.13376

    CAS  Article  PubMed  Google Scholar 

  35. Moore MJ, Mota JF, Douglas NA et al (2014) The ecology, assembly, and evolution of gypsophile floras. In: Rajakaruna N, Boyd R, Harris T (eds) Plant ecology and evolution in harsh environments. Nova Science Publisher, Hauppauge, pp 97–128

    Google Scholar 

  36. Moreno-Gutiérrez C, Dawson TE, Nicolás E, Querejeta JI (2012) Isotopes reveal contrasting water use strategies among coexisting plant species in a Mediterranean ecosystem. New Phytol 196:489–496. https://doi.org/10.1111/j.1469-8137.2012.04276.x

    CAS  Article  PubMed  Google Scholar 

  37. Mota JF, Medina Cazorla JM, Navarro FB et al (2008) Dolomite flora of the Baetic Ranges glades (South Spain). Flora - Morphol Distrib Funct Ecol Plants 203:359–375. https://doi.org/10.1016/J.FLORA.2007.06.006

    Article  Google Scholar 

  38. Murdy WH (1968) Plant speciation associated with granite outcrop communities of the southeastern Piedmont. Rhodora 70:394–407. https://doi.org/10.2307/23308624

    Article  Google Scholar 

  39. Pagel M (1997) Inferring evolutionary processes from phylogenies. Zool Scr 26:331–348. https://doi.org/10.1111/j.1463-6409.1997.tb00423.x

    Article  Google Scholar 

  40. Palacio S, Escudero A, Montserrat-Martí G et al (2007) Plants living on gypsum: Beyond the Specialist model. Ann Bot 99:333–343. https://doi.org/10.1093/aob/mcl263

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Palacio S, Aitkenhead M, Escudero A et al (2014a) Gypsophile chemistry unveiled: Fourier Transform Infrared (FTIR) Spectroscopy provides new insight into plant adaptations to gypsum soils. PLoS One 9:e107285. https://doi.org/10.1371/journal.pone.0107285

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. Palacio S, Azorín J, Montserrat-Martí G, Ferrio JP (2014b) The crystallization water of gypsum rocks is a relevant water source for plants. Nat Commun 5:1–7. https://doi.org/10.1038/ncomms5660

    CAS  Article  Google Scholar 

  43. Paradis E, Claude J, Strimmer K (2004) APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290. https://doi.org/10.1093/bioinformatics/btg412

    CAS  Article  Google Scholar 

  44. Parsons RF (1976) Gypsophily in plants-a review. Am Midl Nat 96:1–20. https://doi.org/10.2307/2424564

    Article  Google Scholar 

  45. Pinheiro J, Bates D, DebRoy S et al (2019) nlme: Linear and nonlinear mixed effects models. R Package version 3.1–142, https://CRAN.R-project.org/package=nlme

  46. Qian H, Jin Y (2016) An updated megaphylogeny of plants, a tool for generating plant phylogenies and an analysis of phylogenetic community structure. J Plant Ecol 9:233–239. https://doi.org/10.1093/jpe/rtv047

    Article  Google Scholar 

  47. R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing. In: Austria. https://www.r-project.org/

  48. Ramírez DA, Querejeta JI, Bellot J (2009) Bulk leaf δ18O and δ13C reflect the intensity of intraspecific competition for water in a semi-arid tussock grassland. Plant Cell Environ 32:1346–1356. https://doi.org/10.1111/j.1365-3040.2009.02002.x

    CAS  Article  PubMed  Google Scholar 

  49. Revell LJ (2010) Phylogenetic signal and linear regression on species data. Methods Ecol Evol 1:319–329. https://doi.org/10.1111/j.2041-210x.2010.00044.x

    Article  Google Scholar 

  50. Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x

    Article  Google Scholar 

  51. Romão RL, Escudero A (2005) Gypsum physical soil crusts and the existence of gypsophytes in semi-arid central Spain. Plant Ecol 181:127–137. https://doi.org/10.1007/s11258-005-5321-x

    Article  Google Scholar 

  52. Ruiz JM, López-Cantarero I, Rivero RM, Romero L (2003) Sulphur phytoaccumulation in plant species characteristic of Gypsiferous soils. Int J Phytoremediation 5:203–210. https://doi.org/10.1080/713779220

    CAS  Article  PubMed  Google Scholar 

  53. Ryel RJ, Ivans CY, Peek MS, Leffler AJ (2008) Functional differences in soil water pools: a new perspective on plant water use in water-limited ecosystems. Prog Bot 69:397–442. https://doi.org/10.1007/978-3-540-72954-9_16

    Article  Google Scholar 

  54. Sarris D, Siegwolf R, Körner C (2013) Inter- and intra-annual stable carbon and oxygen isotope signals in response to drought in Mediterranean pines. Agric For Meteorol 168:59–68. https://doi.org/10.1016/j.agrformet.2012.08.007

    Article  Google Scholar 

  55. Scheidegger Y, Saurer M, Bahn M, Siegwolf R (2000) Linking stable oxygen and carbon isotopes with stomatal conductance and photosynthetic capacity: a conceptual model. Oecologia 125:350–357. https://doi.org/10.1007/s004420000466

    CAS  Article  PubMed  Google Scholar 

  56. Schenk HJ, Jackson RB (2002) Rooting depths, lateral root spreads and below-ground/above-ground allometries of plants in water-limited ecosystems. J Ecol 90:480–494. https://doi.org/10.1046/j.1365-2745.2002.00682.x

    Article  Google Scholar 

  57. 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 106:690–703. https://doi.org/10.1002/ajb2.1285

    Article  PubMed  Google Scholar 

  58. Smith DM, Jarvis PG, Odongo JC (1997) Sources of water used by trees and millet in Sahelian windbreak systems. J Hydrol 198:140–153. https://doi.org/10.1016/S0022-1694(96)03311-2

    CAS  Article  Google Scholar 

  59. Teixeira WG, Sinclair B, Schroth H, Schroth G (2003) Soil water. In: Schroth G, Sinclair F. (eds) Trees, crops and soil fertility. concepts and research methods. CABI Publishing, Wallingford, pp 209–234

  60. Verheye WH, Boyadgiev TG (1997) Evaluating the land use potential of gypsiferous soils from field pedogenic characteristics. Soil Use Manag 13:97–103. https://doi.org/10.1111/j.1475-2743.1997.tb00565.x

    Article  Google Scholar 

  61. Zanne AE, Tank DC, Cornwell WK et al (2014) Three keys to the radiation of angiosperms into freezing environments. Nature 506:89–92. https://doi.org/10.1038/nature12872

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

The author thanks the Yesaires team, especially to Daniel A. Rodríguez Ginart, for making the fieldwork of quantification of species gypsum affinity possible. We thank Dr. Sara Palacio (IPE) and two anonymous reviewers for their helpful revisions and comments on the manuscript. RSM was supported by the Ministry of Science and Innovations (FPU grant FPU17/00629). JPF was supported by Grupo de Referencia H09_20R (Aragón regional government, Spain). Financial support was provided by the Valencian Regional Government (GV/2016/187) and the Spanish Ministry of Science, Innovation and Universities (RTI2018-099672-J-I00; CGL2013-48753-R co-funded by FEDER).

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Sánchez-Martín, R., Querejeta, J.I., Voltas, J. et al. Plant’s gypsum affinity shapes responses to specific edaphic constraints without limiting responses to other general constraints. Plant Soil (2021). https://doi.org/10.1007/s11104-021-04866-4

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Keywords

  • Gypsum affinity
  • Niche segregation
  • Nutrients
  • Stable isotopes
  • Trade‐off
  • Water source