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Plant and Soil

, Volume 437, Issue 1–2, pp 41–54 | Cite as

Seasonal changes in water sources used by woody species in a tropical coastal dune forest

  • C. AntunesEmail author
  • C. Silva
  • C. Máguas
  • C. A. Joly
  • S. Vieira
Regular Article

Abstract

Aims

Our aim was to investigate the water sources used by woody species under contrasting water availability and the extent of water-sources-use differentiation among dominant woody species in a tropical coastal dune forest.

Methods

We sampled 15 woody species in a Brazilian restinga forest and, through Bayesian isotope mixing models, we estimated the proportion of water sources used. We tested whether water-sources-use was (i) different between contrasting water availability conditions; (ii) dependent on growth form, plant size or crown illumination; and (iii) influenced by stand density, evenness or biomass.

Results

We found a seasonal variation in water-sources-use, but no vertical soil-water partitioning among woody species. In wetter periods, plants used mainly water from top-soil, as a shallow water table limited water uptake to top-soil layers recharged with rainwater. Contrastingly, during drier periods, with the absence of rain and a deeper water table, plants generally relied on deeper (50 cm) soil layers. Only under less-wet conditions, a greater evenness and density implied higher water-uptake depth heterogeneity among plants. However, changes in the main water-sources used by plants were neither evoked in more dense or diverse plots, nor induced by plant size.

Conclusions

Our study shows that restinga species have dynamic shifts in water-uptake depth caused by seasonal water availability changes, influenced by the combined effect of insufficient moisture at shallow soil layers and water-table lowering in drier periods. These temporal shifts are common among species, implying that restinga woody community has a homogeneous strategy of water-resources acquisition. This study enhances our understanding of the effects that water variations can have on water-resource use in restinga forests.

Keywords

Water-sources-use Coastal dune ecosystem Restinga forest Stable isotope mixing model Groundwater availability Soil-water partitioning 

Notes

Acknowledgments

We thank to PPG - Ecologia, Instituto de Biologia, Universidade Estadual de Campinas, for the support given to Cristina Antunes in the development of this study. This research was funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) – Cristina Antunes PhD scholarship PROEX 0229083, and Fundação para a Ciência e a Tecnologia (FCT) – projects PTDC/AAC-CLI/118555/2010 and UID/BIA/00329/2013. The scientific project was co-supported by the Brazilian National Research Council/CNPq (PELD Process 403710/2012-0), by the British Natural Environment Research Council/NERC and by The State of São Paulo Research Foundation/FAPESP as part of the projects Functional Gradient, PELD/BIOTA and ECOFOR (Processes 2003/12595-7, 2012/51509-8 e 2012/51872-5, within the BIOTA/FAPESP Program - The Biodiversity Virtual Institute (www.biota.org.br); COTEC/IF 002.766/2013 and 010.631/2013 permits. Namely, we would like to thank: Yvonne Bakker, Luis Quimbayo Guzmán, Thaís Pimenta de Almeida and Marisol Rios for the help given during field surveys; Mauro Lo Cascio and Andreia Anjos for the laboratory work; João Barbosa for data base management; and Rodrigo Maia for isotopic analysis at SIIAF - Faculdade de Ciências, Universidade de Lisboa. The authors have no conflict of interest to declare.

Supplementary material

11104_2019_3947_MOESM1_ESM.pdf (868 kb)
ESM 1 (PDF 868 kb)

References

  1. Antunes C, Díaz Barradas M, Zunzunegui M et al (2018a) Contrasting plant water-use responses to groundwater depth in coastal dune ecosystems. Funct Ecol 32:1931–1943.  https://doi.org/10.1111/1365-2435.13110 CrossRefGoogle Scholar
  2. Antunes C, Díaz Barradas MC, Zunzunegui M et al (2018b) Water source partitioning among plant functional types in a semi arid dune ecosystem. J Veg Sci 29:671–683.  https://doi.org/10.1111/jvs.12647 CrossRefGoogle Scholar
  3. Assis MA, Prata EM, Pedroni F et al (2011) Florestas de Restinga e de Terras Baixas na Planície Costeira do sudeste do Brasil: vegetação e heterogeneidade ambiental. Biota Neotrop 11Google Scholar
  4. Barbeta A, Peñuelas J (2017) Relative contribution of groundwater to plant transpiration estimated with stable isotopes. Sci Rep 7:10580.  https://doi.org/10.1038/s41598-017-09643-x CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bennett A, G Mcdowell N, Allen C, Anderson-Teixeira K (2015) Larger trees suffer most during drought in forests worldwideGoogle Scholar
  6. Brassard BW, Chen HYH, Cavard X et al (2012) Tree species diversity increases fine root productivity through increased soil volume filling. J Ecol 101:210–219.  https://doi.org/10.1111/1365-2745.12023 CrossRefGoogle Scholar
  7. Brienen RJW, Gloor E, Clerici S et al (2017) Tree height strongly affects estimates of water-use efficiency responses to climate and CO2 using isotopes. Nat Commun 8:288.  https://doi.org/10.1038/s41467-017-00225-z CrossRefPubMedPubMedCentralGoogle Scholar
  8. Carminati A, Passioura JB, Zarebanadkouki M et al (2017) Root hairs enable high transpiration rates in drying soils. New Phytol 216:771–781.  https://doi.org/10.1111/nph.14715 CrossRefPubMedGoogle Scholar
  9. Cavalin PO, Mattos EA (2007) Spatio-temporal variation of photosynthetic pigments in the CAM tree Clusia hilariana Schlechtendal associated with dry spells during the rainy season in southeastern Brazil. Trees Struct Funct 21:671–675CrossRefGoogle Scholar
  10. Chave J, Coomes D, Jansen S et al (2009) Towards a worldwide wood economics spectrum. Ecol Lett 12:351–366.  https://doi.org/10.1111/j.1461-0248.2009.01285.x CrossRefPubMedGoogle Scholar
  11. Chen X, Hu Q (2004) Groundwater influences on soil moisture and surface evaporation. J Hydrol 297:285–300.  https://doi.org/10.1016/j.jhydrol.2004.04.019 CrossRefGoogle Scholar
  12. Cooper M, Boschi RS, da Silva LFS et al (2017) Hydro-physical characterization of soils under the Restinga Forest. Sci Agric 74:393–400CrossRefGoogle Scholar
  13. Dawson TE (1993) Water Sources of Plants as Determined from Xylem-Water Isotopic Composition: Perspectives on Plant Competition, Distribution, and Water RelationsGoogle Scholar
  14. Dawson TE (1996) Determining water use by trees and forests from isotopic, energy balance and transpiration analyses: the roles of tree size and hydraulic lift. Tree Physiol 16:263–272CrossRefPubMedGoogle Scholar
  15. 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.  https://doi.org/10.1007/BF00582230 CrossRefPubMedGoogle Scholar
  16. de Oliveira VC (2011) Sobrevivência, morfo-anatomia, crescimento e assimilação de carbono de seis espécies arbóreas neotropicais submetidas à saturação hídrica do solo. Universidade Estadual de CampinasGoogle Scholar
  17. de Oliveira Carvalheiro K, Nepstad DC (1996) Deep soil heterogeneity and fine root distribution in forests and pastures of eastern Amazonia. Plant Soil 182:279–285CrossRefGoogle Scholar
  18. de Oliveira VC, Joly CA (2010) Flooding tolerance of Calophyllum brasiliense Camb. (Clusiaceae): morphological, physiological and growth responses. Trees 24:185–193.  https://doi.org/10.1007/s00468-009-0392-2 CrossRefGoogle Scholar
  19. 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 CrossRefGoogle Scholar
  20. Engelbrecht BMJ, Dalling JW, Pearson TRH et al (2006) Short dry spells in the wet season increase mortality of tropical pioneer seedlings. Oecologia 148:258–269.  https://doi.org/10.1007/s00442-006-0368-5 CrossRefPubMedGoogle Scholar
  21. Evaristo J, McDonnell JJ (2017) Prevalence and magnitude of groundwater use by vegetation: a global stable isotope meta-analysis. Sci Rep 7:44110.  https://doi.org/10.1038/srep44110 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Fan Y, Li H, Miguez-Macho G (2013) Global Patterns of Groundwater Table Depth. Science (80- ) 339:940 LP-943Google Scholar
  23. Fan Y, Miguez-Macho G, Jobbágy EG, et al (2017) Hydrologic regulation of plant rooting depth. Proc Natl Acad Sci 114:10572 LP-10577Google Scholar
  24. Fyllas NM, Bentley LP, Shenkin A et al (2017) Solar radiation and functional traits explain the decline of forest primary productivity along a tropical elevation gradient. Ecol Lett 20:730–740.  https://doi.org/10.1111/ele.12771 CrossRefGoogle Scholar
  25. Gessler A, Nitschke R, de Mattos EA et al (2007) Comparison of the performance of three different ecophysiological life forms in a sandy coastal restinga ecosystem of SE-Brazil: a nodulated N2-fixing C3-shrub (Andira legalis (Vell.) Toledo), a CAM-shrub (Clusia hilariana Schltdl.) and a tap root C3-hemi. Trees 22:105.  https://doi.org/10.1007/s00468-007-0174-7 CrossRefGoogle Scholar
  26. Goldstein G, Meinzer FC, Bucci SJ et al (2008) Water economy of Neotropical savanna trees: six paradigms revisited. Tree Physiol 28:395–404CrossRefPubMedGoogle Scholar
  27. Guderle M, Bachmann D, Milcu A et al (2018) Dynamic niche partitioning in root water uptake facilitates efficient water use in more diverse grassland plant communities. Funct Ecol 32:214–227.  https://doi.org/10.1111/1365-2435.12948 CrossRefGoogle Scholar
  28. Jackson PC, Cavelier J, Goldstein G et al (1995) Partitioning of water resources among plants of a lowland tropical forest. Oecologia 101:197–203.  https://doi.org/10.1007/BF00317284 CrossRefPubMedGoogle Scholar
  29. Jackson PC, Meinzer F, Bustamante M et al (1999) Partitioning of soil water among tree species in a Brazilian Cerrado ecosystem. Tree Physiol 19:717–724.  https://doi.org/10.1093/treephys/19.11.717 CrossRefPubMedGoogle Scholar
  30. Jackson RB, Sperry JS, Dawson TE (2000) Root water uptake and transport: using physiological processes in global predictions. Trends Plant Sci 5:482–488.  https://doi.org/10.1016/S1360-1385(00)01766-0 CrossRefPubMedGoogle Scholar
  31. Joly CA, Assis MA, Bernacci LC et al (2012) Florística e fitossociologia em parcelas permanentes da Mata Atlântica do sudeste do Brasil ao longo de um gradiente altitudinal. Biota Neotrop. 12:125–145CrossRefGoogle Scholar
  32. Keeling H, Phillips O (2007) A calibration method for the crown illumination index for assessing forest light environmentsGoogle Scholar
  33. Kulmatiski A, Beard KH (2013) Root niche partitioning among grasses, saplings, and trees measured using a tracer technique. Oecologia 171:25–37.  https://doi.org/10.1007/s00442-012-2390-0 CrossRefPubMedGoogle Scholar
  34. Kulmatiski A, Adler PB, Stark JM, Tredennick AT (2017) Water and nitrogen uptake are better associated with resource availability than root biomass. Ecosphere 8:e01738.  https://doi.org/10.1002/ecs2.1738 CrossRefGoogle Scholar
  35. Ledo A, Paul KI, Burslem DFRP et al (2018) Tree size and climatic water deficit control root to shoot ratio in individual trees globally. New Phytol 217:8–11.  https://doi.org/10.1111/nph.14863 CrossRefPubMedGoogle Scholar
  36. Magnago LFS, Martins SV, Schaefer CEGR, Neri AV (2012) Restinga forests of the Brazilian coast: richness and abundance of tree species on different soils. An Acad Bras Ciênc 84:807–822CrossRefPubMedGoogle Scholar
  37. Markesteijn L, Poorter L (2009) Seedling root morphology and biomass allocation of 62 tropical tree species in relation to drought- and shade-tolerance. J Ecol 97:311–325.  https://doi.org/10.1111/j.1365-2745.2008.01466.x CrossRefGoogle Scholar
  38. Markesteijn L, Poorter L, Bongers F (2007) Light-dependent leaf trait variation in 43 tropical dry forest tree species. Am J Bot 94:515–525.  https://doi.org/10.3732/ajb.94.4.515 CrossRefPubMedGoogle Scholar
  39. Markesteijn L, Poorter L, Bongers F et al (2011) Hydraulics and life history of tropical dry forest tree species: coordination of species’ drought and shade tolerance. New Phytol 191:480–495.  https://doi.org/10.1111/j.1469-8137.2011.03708.x CrossRefPubMedGoogle Scholar
  40. Markewitz D, Devine L, Davidson EA et al (2010) Soil moisture depletion under simulated drought in the Amazon: impacts on deep root uptake. New Phytol 187:592–607.  https://doi.org/10.1111/j.1469-8137.2010.03391.x CrossRefPubMedGoogle Scholar
  41. Marques MCM, Silva SM, Liebsch D (2015) Coastal plain forests in southern and southeastern Brazil: ecological drivers, floristic patterns and conservation status. Brazilian J Bot 38:1–18.  https://doi.org/10.1007/s40415-015-0132-3 CrossRefGoogle Scholar
  42. McDowell N, Allen CD, Anderson-Teixeira K, et al (2018) Drivers and mechanisms of tree mortality in moist tropical forests. New Phytol n/a-n/a.  https://doi.org/10.1111/nph.15027
  43. Meinzer FC (2003) Functional convergence in plant responses to the environment. Oecologia 134:1–11.  https://doi.org/10.1007/s00442-002-1088-0 CrossRefPubMedGoogle Scholar
  44. Meinzer FC, Andrade JL, Goldstein G et al (1999) Partitioning of soil water among canopy trees in a seasonally dry tropical forest. Oecologia 121:293–301.  https://doi.org/10.1007/s004420050931 CrossRefPubMedGoogle Scholar
  45. Meinzer FC, Woodruff DR, Eissenstat DM et al (2013) Above- and belowground controls on water use by trees of different wood types in an eastern US deciduous forest. Tree Physiol 33:345–356CrossRefPubMedGoogle Scholar
  46. Mueller K, Tilman D, Fornara DA, Hobbie SE (2013) Root depth distribution and the diversity–productivity relationship in a long-term grassland experiment. Ecology 94:787–793.  https://doi.org/10.1890/12-1399.1 CrossRefGoogle Scholar
  47. Nepstad DC, de Carvalho CR, Davidson EA et al (1994) The role of deep roots in the hydrological and carbon cycles of Amazonian forests and pastures. Nature 372:666CrossRefGoogle Scholar
  48. Nepstad DC, Tohver IM, Ray D et al (2007) Mortality of large trees and lianas following experimental drought in an Amazon forest. Ecology 88:2259–2269.  https://doi.org/10.1890/06-1046.1 CrossRefPubMedGoogle Scholar
  49. Oliveira RS, Bezerra L, Davisdson EA et al (2005) Deep root function in soil water dynamics in cerrado savannas of central Brazil. Funct Ecol 19:574–581.  https://doi.org/10.1111/j.1365-2435.2005.01003.x CrossRefGoogle Scholar
  50. Oliveira RS, Eller CB, Bittencourt PRL, Mulligan M (2014) The hydroclimatic and ecophysiological basis of cloud forest distributions under current and projected climates. Ann Bot 113:909–920.  https://doi.org/10.1093/aob/mcu060 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Parnell AC, Phillips DL, Bearhop S et al (2013) Bayesian stable isotope mixing models. Environmetrics 24:387–399.  https://doi.org/10.1002/env.2221 CrossRefGoogle Scholar
  52. Pavlis J, Jeník J (2000) Roots of pioneer trees in the Amazonian rain forest. Trees 14:442–455.  https://doi.org/10.1007/s004680000049 CrossRefGoogle Scholar
  53. Peñuelas J, Terradas J, Lloret F (2011) Solving the conundrum of plant species coexistence: water in space and time matters most. New Phytol 189:5–8.  https://doi.org/10.1111/j.1469-8137.2010.03570.x CrossRefPubMedGoogle Scholar
  54. Phillips OL, van der Heijden G, Lewis SL et al (2010) Drought–mortality relationships for tropical forests. New Phytol 187:631–646.  https://doi.org/10.1111/j.1469-8137.2010.03359.x CrossRefPubMedGoogle Scholar
  55. Pinheiro J, Bates D, DebRoy S, et al (2013) nlme: Linear and Nonlinear Mixed Effects ModelsGoogle Scholar
  56. Poorter L (2001) Light-dependent changes in biomass allocation and their importance for growth of rain forest tree species. Funct Ecol 15:113–123.  https://doi.org/10.1046/j.1365-2435.2001.00503.x CrossRefGoogle Scholar
  57. Poorter L, Bongers F (2006) Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology 87:1733–1743. https://doi.org/10.1890/0012-9658(2006)87[1733:LTAGPO]2.0.CO;2Google Scholar
  58. Raich JW, Clark DA, Schwendenmann L, Wood TE (2014) Aboveground Tree Growth Varies with Belowground Carbon Allocation in a Tropical Rainforest Environment. PLoS One 9:e100275.  https://doi.org/10.1371/journal.pone.0100275 CrossRefPubMedPubMedCentralGoogle Scholar
  59. R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
  60. Rodriguez-Iturbe I, D’Odorico P, Laio F et al (2007) Challenges in humid land ecohydrology: Interactions of water table and unsaturated zone with climate, soil, and vegetation. Water Resour Res 43.  https://doi.org/10.1029/2007WR006073
  61. Rosado BHP, De Mattos EA (2010) Interspecific variation of functional traits in a CAM-tree dominated sandy coastal plain. J Veg Sci 21:43–54.  https://doi.org/10.1111/j.1654-1103.2009.01119.x CrossRefGoogle Scholar
  62. Rosado BHR, Martins AC, Colomeu TC et al (2011) Fine root biomass and root length density in a lowland and a montane tropical rain forest, SP, Brazil. Biota Neotrop. 11:203–209CrossRefGoogle Scholar
  63. Rosado BHP, Mattos EADE, Stermberg LDASL (2013) Are leaf physiological traits related to leaf water isotopic enrichment in restinga woody species? An. Acad. Bras. Cienc. 85:1035–1046CrossRefPubMedGoogle Scholar
  64. Rosado BHP, Joly CA, Burgess SSO et al (2016) Changes in plant functional traits and water use in Atlantic rainforest: evidence of conservative water use in spatio-temporal scales. Trees 30:47–61.  https://doi.org/10.1007/s00468-015-1165-8 CrossRefGoogle Scholar
  65. Rossatto DR, da Silveira Lobo Sternberg L, Franco AC (2012a) 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.  https://doi.org/10.1111/j.1438-8677.2012.00618.x CrossRefPubMedGoogle Scholar
  66. Rossatto DR, de Carvalho Ramos Silva L, Villalobos-Vega R et al (2012b) Depth of water uptake in woody plants relates to groundwater level and vegetation structure along a topographic gradient in a neotropical savanna. Environ Exp Bot 77:259–266.  https://doi.org/10.1016/j.envexpbot.2011.11.025 CrossRefGoogle Scholar
  67. Rossatto DR, Silva LCR, Sternberg LSL, Franco AC (2014) Do woody and herbaceous species compete for soil water across topographic gradients? Evidence for niche partitioning in a Neotropical savanna. South African J Bot 91:14–18.  https://doi.org/10.1016/j.sajb.2013.11.011 CrossRefGoogle Scholar
  68. Sack L (2004) Responses of temperate woody seedlings to shade and drought: do trade-offs limit potential niche differentiation? Oikos 107:110–127.  https://doi.org/10.1111/j.0030-1299.2004.13184.x CrossRefGoogle Scholar
  69. Santiago LS, De Guzman ME, Baraloto C, et al (2004) Coordination and trade-offs among hydraulic safety, efficiency and drought avoidance traits in Amazonian rainforest canopy tree species. New Phytol n/a-n/a.  https://doi.org/10.1111/nph.15058
  70. Scarano FR (2002) Structure, Function and Floristic Relationships of Plant Communities in Stressful Habitats Marginal to the Brazilian Atlantic Rainforest. Ann Bot 90:517–524.  https://doi.org/10.1093/aob/mcf189 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Schenk HJ (2006) Root competition: beyond resource depletion. J Ecol 94:725–739.  https://doi.org/10.1111/j.1365-2745.2006.01124.x CrossRefGoogle Scholar
  72. 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 CrossRefGoogle Scholar
  73. Schwendenmann L, Pendall E, Sanchez-Bragado R et al (2015) Tree water uptake in a tropical plantation varying in tree diversity: interspecific differences, seasonal shifts and complementarity. Ecohydrology 8:1–12.  https://doi.org/10.1002/eco.1479 CrossRefGoogle Scholar
  74. Scott RL, Watts C, Payan JG et al (2003) The understory and overstory partitioning of energy and water fluxes in an open canopy, semiarid woodland. Agric For Meteorol 114:127–139.  https://doi.org/10.1016/S0168-1923(02)00197-1 CrossRefGoogle Scholar
  75. Silva C (2015) Estoque e produção de raiz fina ao longo de um gradiente altitudinal de floresta atlântica na serra do mar. UNICAMP, São PauloGoogle Scholar
  76. Silvertown J (2004) Plant coexistence and the niche. Trends Ecol Evol 19:605–611.  https://doi.org/10.1016/j.tree.2004.09.003 CrossRefGoogle Scholar
  77. Silvertown J, Dodd ME, Gowing DJG, Mountford JO (1999) Hydrologically defined niches reveal a basis for species richness in plant communities. Nature 400(61)Google Scholar
  78. Stock B, Jackson A, Ward E, Venkiteswaran J (2016) MixSIAR: v3.1.7Google Scholar
  79. Stone EL, Kalisz PJ (1991) On the maximum extent of tree roots. For Ecol Manage 46:59–102.  https://doi.org/10.1016/0378-1127(91)90245-Q CrossRefGoogle Scholar
  80. Tyree MT, Velez V, Dalling JW (1998) Growth dynamics of root and shoot hydraulic conductance in seedlings of five neotropical tree species: scaling to show possible adaptation to differing light regimes. Oecologia 114:293–298.  https://doi.org/10.1007/s004420050450 CrossRefPubMedGoogle Scholar
  81. Vieira SA, Alves LF, Aidar M et al (2008) Estimation of biomass and carbon stocks: the case of the Atlantic Forest. Biota Neotrop. 8(0)Google Scholar
  82. Volkmann THM, Haberer K, Gessler A, Weiler M (2016) High-resolution isotope measurements resolve rapid ecohydrological dynamics at the soil–plant interface. New Phytol 210:839–849.  https://doi.org/10.1111/nph.13868 CrossRefPubMedGoogle Scholar
  83. West AG, Hultine KR, Burtch KG, Ehleringer JR (2007) Seasonal variations in moisture use in a piñon–juniper woodland. Oecologia 153:787–798.  https://doi.org/10.1007/s00442-007-0777-0 CrossRefPubMedGoogle Scholar
  84. Wright SJ, Kitajima K, Kraft N, et al (2010) Functional traits and the growth-mortality trade-off in tropical treesGoogle Scholar
  85. Zea-Cabrera E, Iwasa Y, Levin S, Rodríguez-Iturbe I (2006) Tragedy of the commons in plant water use. Water Resour Res 42:n/a-n/a.  https://doi.org/10.1029/2005WR004514
  86. Zencich SJ, Froend RH, Turner JV, Gailitis V (2002) Influence of groundwater depth on the seasonal sources of water accessed by Banksia tree species on a shallow, sandy coastal aquifer. Oecologia 131:8–19.  https://doi.org/10.1007/s00442-001-0855-7 CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.CE3C, Centre for Ecology, Evolution and Environmental ChangesFaculdade de Ciências da Universidade de LisboaLisbonPortugal
  2. 2.Laboratório de Ecologia e Manejo de Ecossistemas, Núcleo de Estudos e Pesquisas AmbientaisUniversidade Estadual de CampinasSão PauloBrazil
  3. 3.PPG – Biologia Vegetal, Instituto de BiologiaUniversidade Estadual de CampinasSão PauloBrazil
  4. 4.Instituto de BiologiaUniversidade Estadual de CampinasSão PauloBrazil

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