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Coordination of rooting depth and leaf hydraulic traits defines drought-related strategies in the campos rupestres, a tropical montane biodiversity hotspot

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Abstract

Background and aims

The survival and coexistence of plants in water-limited environments are related to their ability to coordinate water acquisition and regulation of water loss. To assess the coordination among below and aboveground hydraulic traits and the diversity of water-use strategies, we evaluated rooting depth and several leaf hydraulic traits of 15 species in campos rupestres, a seasonally-dry biodiversity hotspot in central Brazil.

Methods

We assessed the depth of plant water acquisition by excavating roots and analyzing the stable isotope composition of hydrogen (δD) and oxygen (δ18O) in the xylem and soil water. We also measured mid-morning stomatal conductance, leaf-water potential at turgor loss point (ѰTLP) and pre-dawn leaf water potentials (ѰPD) during wet and dry seasons.

Results

We demonstrated that rooting depth is a good predictor of seasonal variations in stomatal conductance and ѰPD. Shallow-rooted plants had greater variation in stomatal conductance and ѰPD than deep-rooted plants. Woody plants with shallower roots also had lower ѰTLP than deep-rooted plants, revealing higher drought resistance.

Conclusion

We demonstrate that shallow-rooted species, more exposed to variation in water availability, have mechanisms to confer drought resistance through turgor maintenance. Our results support the theory of hydrological niche segregation and its underlying trade-offs related to drought resistance.

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References

  • Abrahão A, Lambers H, Sawaya ACHF, Mazzafera P, Oliveira RS (2014) Convergence of a specialized root trait in plants from nutrient-impoverished soils: phosphorus-acquisition strategy in a nonmycorrhizal cactus. Oecologia 176:345–355. doi:10.1007/s00442-014-3033-4

    Article  PubMed  Google Scholar 

  • Aguinis H, Gottfredson RK, Joo H (2013) Best-practice recommendations for defining, identifying and handling outliers. Organ Res Methods 16:270–301. doi:10.1177/1094428112470848

    Article  Google Scholar 

  • Alcantara S, Mello-Silva R, Teodoro GS, Drequeceler K, Ackerly DD, Oliveira RS (2015) Carbon assimilation and habitat segregation in resurrection plants: a comparison between desiccation-and non-desiccation-tolerant species of Neotropical Velloziaceae (Pandanales). Funct Ecol 29:1499–1512. doi:10.1111/1365-2435.12462

    Article  Google Scholar 

  • Apezzato-da-Glória B (2003) Morfologia de sistemas subterrâneos. ESALQ/USP, Ribeirao Preto

    Google Scholar 

  • Araya YN, Silvertown J, Gowing DJ, McConway KJ, Linder HP, Midgley G (2011) A fundamental, eco-hydrological basis for niche segregation in plant communities. New Phytol 189:253–258. doi:10.1111/j.1469-8137.2010.03475.x

    Article  PubMed  Google Scholar 

  • Bartelheimer M, Gowing D, Silvertown J (2010) Explaining hydrological niches: the decisive role of below-ground competition in two closely related Senecio species. J Ecol 98:126–136. doi:10.1111/j.1365-2745.2009.01598.x

    Article  Google Scholar 

  • Bartlett MK, Scoffoni C, Sack L (2012) The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis. Ecol Lett 15:393–405. doi:10.1111/j.1461-0248.2012.01751.x

    Article  PubMed  Google Scholar 

  • Bates D, Machler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Blondel J (2003) Guilds or functional groups: does it matter? Oikos 100:223–231. doi:10.1034/j.1600-0706.2003.12152.x

    Article  Google Scholar 

  • Bond WJ, Midgley JJ (2003) The evolutionary ecology of sprouting in woody plants. Int J Plant Sci 164:103–114

    Article  Google Scholar 

  • Brodribb TJ, Holbrook NM, Edwards EJ, Gutierrez MV (2003) Relations between stomatal closure, leaf turgor and xylem vulnerability in eight tropical dry forest trees. Plant Cell Environ 26:443–450. doi:10.1046/j.1365-3040.2003.00975.x

    Article  Google Scholar 

  • Cade BS, Noon BR (2003) A gentle introduction to quantile regression for ecologists. Front Ecol Environ 1:412–420. doi:10.1890/1540-9295(2003)001[0412:AGITQR]2.0.CO;2

    Article  Google Scholar 

  • Castro SAB, Silveira FAO, Marcato MS, Lemos-Filho JP (2016) So close, yet so different: divergences in resource use may help stabilize coexistence of phylogenetically-related species in a megadiverse grassland. Flora-Morphology, Distribution, Functional Ecology of Plants doi:10.1016/j.flora.2016.11.018

    Article  Google Scholar 

  • Cosme LHM, Schietti J, Costa FRC, Oliveira RS (2017) The importance of hydraulic architecture to the distribution pattern of trees in a central Amazonian forest. New Phytol 215:113–125. doi:10.1111/nph.14508

    Article  PubMed  Google Scholar 

  • Dawson TE, Ehleringer JR (1998) Plants, isotopes and water use: a catchment-scale perspective. In: Kendall C, McDonnell J (eds) Isotope tracers in catchment hydrology. Elsevier, Amsterdam

    Google Scholar 

  • Dawson TE, Pate JS (1996) Seasonal water uptake and movement in root systems of Australian phraeatophytic plants of dimorphic root morphology: a stable isotope investigation. Oecologia 107:13–20. doi:10.1007/bf00582230

    Article  PubMed  Google Scholar 

  • Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable isotopes in plant ecology. Annu Rev Ecol Syst 33:507–559

    Article  Google Scholar 

  • de Souza A, de Moraes MG, Ribeiro RCLF (2005) Gramíneas do cerrado: carboidratos não-estruturais e aspectos ecofisiológicos. Acta Bot Bras 19:81–90

    Article  Google Scholar 

  • Díaz S, Kattge J, Cornelissen JHC, Wright IJ, Lavorel S, Dray S, Reu B, Kleyer M, Wirth C, Prentice IC (2016) The global spectrum of plant form and function. Nature 529:167–171. doi:10.1038/nature16489

    Article  CAS  PubMed  Google Scholar 

  • Dietrich RC, Bengough AG, Jones HG, White PJ (2013) Can root electrical capacitance be used to predict root mass in soil? Ann Bot 112:457–464. doi:10.1093/aob/mct044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding Y, Zhang Y, Zheng Q-S, Tyree MT (2014) Pressure-volume curves: revisiting the impact of negative turgor during cell collapse by literature review and simulations of cell micromechanics. New Phytol 203:378–387. doi:10.1111/nph.12829

    Article  PubMed  Google Scholar 

  • Donovan LA, Linton MJ, Richards JH (2001) Predawn plant water potential does not necessarily equilibrate with soil water potential under well-watered conditions. Oecologia 129:328–335. doi:10.1007/s004420100738

    Article  CAS  PubMed  Google Scholar 

  • Donovan LA, Richards JH, Linton MJ (2003) Magnitude and mechanisms of disequilibrium between predawn plant and soil water potentials. Ecology 84:463–470. doi:10.1890/0012-9658(2003)084[0463:MAMODB]2.0.CO;2

    Article  Google Scholar 

  • Ferri MG (1944) Transpiração de plantas permanentes dos “cerrados”. Bol Fac Filos Ciênc Univ São Paulo 41:161–224

    Google Scholar 

  • Garcia RJF, Longhi-Wagner HM, Pirani JR, Meirelles ST (2009) A contribution to the phytogeography of Brazilian campos: an analysis based on Poaceae. Brazilian J Bot 32:703–713. doi:10.1590/s0100-84042009000400009

    Article  Google Scholar 

  • Giulietti AM, De Menezes NL, Pirani JR, Meguro M, Wanderley MDGL (1987) Flora da Serra do Cipó, Minas Gerais: caracterização e lista das espécies. Boletim de Botânica da Universidade de São Paulo 9:1–151

    Article  Google Scholar 

  • Gonfiantini R (1978) Standards for stable isotope measurements in natural compounds. Nature 271:534–536. doi:10.1038/271534a0

    Article  CAS  Google Scholar 

  • Ivanov VY, Hutyra LR, Wofsy SC, Munger JW, Saleska SR, de Oliveira RC Jr, de Camargo PB (2012) Root niche separation can explain avoidance of seasonal drought stress and vulnerability of overstory trees to extended drought in a mature Amazonian forest. Water Resour Res 48. doi:10.1029/2012wr011972

  • Jackson RB, Canadell J, Ehleringer JR, Mooney HA, Sala OE, Schulze ED (1996) A global analysis of root distributions for terrestrial biomes. Oecologia 108:389–411. doi:10.1007/bf00333714

    Article  CAS  PubMed  Google Scholar 

  • Jacobi CM, do Carmo FF, Vincent RC, Stehmann JR (2007) Plant communities on ironstone outcrops: a diverse and endangered Brazilian ecosystem. Biodivers Conserv 16:2185–2200. doi:10.1007/s10531-007-9156-8

    Article  Google Scholar 

  • Klein T (2014) The variability of stomatal sensitivity to leaf water potential across tree species indicates a continuum between isohydric and anisohydric behaviours. Funct Ecol 28:1313–1320. doi:10.1111/1365-2435.12289

    Article  Google Scholar 

  • Koenker R (2017) Quantreg: quantile regression. R package version 5.33. R Foundation for Statistical Computing, Vienna. Available at: http://CRAN.R-project.org/package=quantreg

  • Küppers M, Neales TF, Küppers BIL, Swan AG, Myers BA (1987) Hydraulic flow characteristics in the lignotuberous mallee Eucalyptus behriana F. Muell in the field. Plant Cell Environ 10:27–37. doi:10.1111/j.1365-3040.1987.tb02076.x

    Article  PubMed  Google Scholar 

  • Le Stradic S, Buisson E, Fernandes GW (2015) Vegetation composition and structure of some Neotropical mountain grasslands in Brazil. J Mt Sci 12:864–877. doi:10.1007/s11629-013-2866-3

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Lenz TI, Wright IJ, Westoby M (2006) Interrelations among pressure-volume curve traits across species and water availability gradients. Physiol Plant 127:423–433. doi:10.1111/j.1399-3054.2006.00680.x

    Article  CAS  Google Scholar 

  • Letten AD, Keith DA, Tozer MG, Hui FKC (2015) Fine-scale hydrological niche differentiation through the lens of multi-species co-occurrence models. J Ecol 103:1264–1275. doi:10.1111/1365-2745.12428

    Article  Google Scholar 

  • Meinzer FC, Woodruff DR, Eissenstat DM, Lin HS, Adams TS, McCulloh KA (2013) Above- and belowground controls on water use by trees of different wood types in an eastern US deciduous forest. Tree Physiol 33:345–356. doi:10.1093/treephys/tpt012

    Article  PubMed  Google Scholar 

  • Meinzer FC, Woodruff DR, Marias DE, Smith DD, McCulloh KA, Howard AR, Magedman AL (2016) Mapping ‘hydroscapes’ along the iso-to anisohydric continuum of stomatal regulation of plant water status. Ecol Lett 19:1343–1352. doi:10.1111/ele.12670

    Article  PubMed  Google Scholar 

  • Mitchell PJ, O'Grady AP, Pinkard EA, Brodribb TJ, Arndt SK, Blackman CJ, Duursma RA, Fensham RJ, Hilbert DW, Nitschke CR (2016) An ecoclimatic framework for evaluating the resilience of vegetation to water deficit. Glob Chang Biol. doi:10.1111/gcb.13177

    Article  Google Scholar 

  • Myers BA (1995) The influence of the lignotuber on hydraulic conductance and leaf conductance in Eucalyptus behriana seedlings. Aust J Plant Physiol 22:857–863

    Google Scholar 

  • Nepstad DC, de Carvalho CR, Davidson EA, Jipp PH, Lefebvre PA, Negreiros GH, da Silva ED, Stone TA, Trumbore SE, Vieira S (1994) The role of deep roots in the hydrological and carbon cycles of Amazonian forests and pastures. Nature 372:666–669. doi:10.1038/372666a0

    Article  CAS  Google Scholar 

  • Nie Y-p, Chen H-s, Wang K-l, Tan W, Deng P-y, Yang J (2011) Seasonal water use patterns of woody species growing on the continuous dolostone outcrops and nearby thin soils in subtropical China. Plant Soil 341:399–412. doi:10.1007/s11104-010-0653-2

    Article  CAS  Google Scholar 

  • Oliveira RS, Bezerra L, Davidson EA, Pinto F, Klink CA, Nepstad DC, Moreira A (2005a) Deep root function in soil water dynamics in cerrado savannas of central Brazil. Funct Ecol 19:574–581. doi:10.1111/j.1365-2435.2005.01003.x

    Article  Google Scholar 

  • Oliveira RS, Dawson TE, Burgess SSO, Nepstad DC (2005b) Hydraulic redistribution in three Amazonian trees. Oecologia 145:354–363. doi:10.1007/s00442-005-0108-2

    Article  PubMed  Google Scholar 

  • Oliveira RS, Christoffersen BO, Barros FV, Teodoro GS, Bittencourt P, Brum MMJ, Viani RAG (2014) Changing precipitation regimes and the water and carbon economies of trees. Theor Exp Plant Physiol 26:65–82. doi:10.1007/s40626-014-0007-1

    Article  Google Scholar 

  • Oliveira RS, Galvao HC, de Campos MCR, Eller CB, Pearse SJ, Lambers H (2015) Mineral nutrition of campos rupestres plant species on contrasting nutrient-impoverished soil types. New Phytol 205:1183–1194. doi:10.1111/nph.13175

    Article  CAS  PubMed  Google Scholar 

  • Oliveira RS, Abrahão A, Pereira C, Teodoro GS, Brum M, Alcantara S, Lambers H (2016) Ecophysiology of Campos Rupestres plants. In: Fernandes GW (ed) Ecology and conservation of mountaintop grasslands in Brazil. Springer International Publishing

  • Parnell A, Jackson A (2013) Siar: stable isotope analysis in R. R package version 4.2. Available from: http://CRAN.R-project.org/package=siar. Accessed 23 March 2014

  • Parnell AC, Phillips DL, Bearhop S, Semmens BX, Ward EJ, Moore JW, Jackson AL, Grey J, Kelly DJ, Inger R (2013) Bayesian stable isotope mixing models. Environmetrics 24:387–399. doi:10.1002/env.2221

    Article  Google Scholar 

  • Pivovaroff AL, Pasquini SC, De Guzman ME, Alstad KP, Stemke JS, Santiago LS (2015) Multiple strategies for drought survival among woody plant species. Funct Ecol. doi:10.1111/1365-2435.12518

    Article  Google Scholar 

  • Poot P, Lambers H (2003) Are trade-offs in allocation pattern and root morphology related to species abundance? A congeneric comparison between rare and common species in the south-western Australian flora. J Ecol 91:58–67. doi:10.1046/j.1365-2745.2003.00738.x

    Article  Google Scholar 

  • Porembski S, Barthlott W (2000) Granitic and gneissic outcrops (inselbergs) as centers of diversity for desiccation-tolerant vascular plants. Plant Ecol 151:19–28. doi:10.1023/a:1026565817218

    Article  Google Scholar 

  • Quesada CA, Hodnett MG, Breyer LM, Santos AJB, Andrade S, Miranda HS, Miranda AC, Lloyd J (2008) Seasonal variations in soil water in two woodland savannas of central Brazil with different fire history. Tree Physiol 28:405–415. doi:10.1093/treephys/28.3.405

    Article  PubMed  Google Scholar 

  • Romero R, Nakajima JN (1999) Espécies endêmicas do Parque Nacional da Serra da Canastra, Minas Gerais. Rev Bras Bot 22:259–265

    Article  Google Scholar 

  • Rossatto DR, Sternberg LSL, Franco AC (2013) The partitioning of water uptake between growth forms in a Neotropical savanna: do herbs exploit a third water source niche? Plant Biol 15:84–92. doi:10.1111/j.1438-8677.2012.00618.x

    Article  CAS  PubMed  Google Scholar 

  • Sarmiento G, Monasterio M (1983) Life forms and phenology. In: Bourliere F (ed) Ecosystems of the world. Elsevier, Amsterdam

  • 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. doi:10.1046/j.1365-2745.2002.00682.x

    Article  Google Scholar 

  • Schwinning S (2010) The ecohydrology of roots in rocks. Ecohydrology 3:238–245. doi:10.1002/eco.134

    Article  Google Scholar 

  • Schwinning S, Ehleringer JR (2001) Water use trade-offs and optimal adaptations to pulse-driven arid ecosystems. J Ecol 89:464–480. doi:10.1046/j.1365-2745.2001.00576.x

    Article  Google Scholar 

  • Schwinning S, Kelly CK (2013) Plant competition, temporal niches and implications for productivity and adaptability to climate change in water-limited environments. Funct Ecol 27:886–897. doi:10.1111/1365-2435.12115

    Article  Google Scholar 

  • Schwinning S, Sala OE, Loik ME, Ehleringer JR (2004) Thresholds, memory, and seasonality: understanding pulse dynamics in arid/semi-arid ecosystems. Oecologia 141:191–193. doi:10.1007/s00442-004-1683-3

    Article  PubMed  Google Scholar 

  • Silveira FAO, Negreiros D, Barbosa NPU, Buisson E, Carmo FF, Carstensen DW, Conceição AA, Cornelissen TG, Echternacht L, Fernandes GW, Garcia QS, Guerra TJ, Jacobi CM, Lemos-Filho JP, Le Stradic S, Morellato LPC, Neves FS, Oliveira RS, Schaefer CE, Viana PL, Lambers H (2016) Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority. Plant Soil 1–24. doi:10.1007/s11104-015-2637-8

    Article  Google Scholar 

  • Silvertown J, Dodd ME, Gowing DJG, Mountford JO (1999) Hydrologically defined niches reveal a basis for species richness in plant communities. Nature 400:61–63. doi:10.1038/21877

    Article  CAS  Google Scholar 

  • Silvertown J, Araya Y, Gowing D (2015) Hydrological niches in terrestrial plant communities: a review. J Ecol 103:93–108. doi:10.1111/1365-2745.12332

    Article  Google Scholar 

  • Team RC (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Turner NC (1988) Measurement of plant water status by the pressure chamber technique. Irrig Sci 9:289–308. doi:10.1007/bf00296704

    Article  Google Scholar 

  • West AG, Dawson TE, February EC, Midgley GF, Bond WJ, Aston TL (2012) Diverse functional responses to drought in a Mediterranean-type shrubland in South Africa. New Phytol 195:396–407. doi:10.1111/j.1469-8137.2012.04170.x

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We gratefully acknowledge CAPES agency for the scholarships granted to MB and AA; financial support by the São Paulo Research Foundation (FAPESP) with a scholarship to GST (2010/50327-8 and 2012/21015-3) and grant to RSO (2010/10204-0; 2011/52072-0). We thank Dr. Lucy Rowland for reviewing the manuscript; Caroline S. Muller and José Carmelo for helping in the field work, Dr. Plinio B. de Camargo, Dr. Marcelo Z. Moreira and Mr. Geraldo de Arruda for allowing the use of laboratory facilities at CENA-USP, ICMBio for allowing this study at PNSC, and Canastra Adventure and Dona Vicentina for the logistic support. The authors confirm do not have conflict of interest.

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Correspondence to Mauro Brum or Rafael Silva Oliveira.

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Brum, M., Teodoro, G.S., Abrahão, A. et al. Coordination of rooting depth and leaf hydraulic traits defines drought-related strategies in the campos rupestres, a tropical montane biodiversity hotspot. Plant Soil 420, 467–480 (2017). https://doi.org/10.1007/s11104-017-3330-x

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