Advertisement

Oecologia

, Volume 162, Issue 1, pp 11–21 | Cite as

Hydraulic lift and tolerance to salinity of semiarid species: consequences for species interactions

  • Cristina Armas
  • Francisco M. Padilla
  • Francisco I. Pugnaire
  • Robert B. Jackson
Physiological Ecology - Original Paper

Abstract

The different abilities of plant species to use ephemeral or permanent water sources strongly affect physiological performance and species coexistence in water-limited ecosystems. In addition to withstanding drought, plants in coastal habitats often have to withstand highly saline soils, an additional ecological stress. Here we tested whether observed competitive abilities and C–water relations of two interacting shrub species from an arid coastal system were more related to differences in root architecture or salinity tolerance. We explored water sources of interacting Juniperus phoenicea Guss. and Pistacia lentiscus L. plants by conducting physiology measurements, including water relations, CO2 exchange, photochemical efficiency, sap osmolality, and water and C isotopes. We also conducted parallel soil analyses that included electrical conductivity, humidity, and water isotopes. During drought, Pistacia shrubs relied primarily on permanent salty groundwater, while isolated Juniperus plants took up the scarce and relatively fresh water stored in upper soil layers. As drought progressed further, the physiological activity of Juniperus plants nearly stopped while Pistacia plants were only slightly affected. Juniperus plants growing with Pistacia had stem-water isotopes that matched Pistacia, unlike values for isolated Juniperus plants. This result suggests that Pistacia shrubs supplied water to nearby Juniperus plants through hydraulic lift. This lifted water, however, did not appear to benefit Juniperus plants, as their physiological performance with co-occurring Pistacia plants was poor, including lower water potentials and rates of photosynthesis than isolated plants. Juniperus was more salt sensitive than Pistacia, which withstood salinity levels similar to that of groundwater. Overall, the different abilities of the two species to use salty water appear to drive the outcome of their interaction, resulting in asymmetric competition where Juniperus is negatively affected by Pistacia. Salt also seems to mediate the interaction between the two species, negating the potential positive effects of an additional water source via hydraulic lift.

Keywords

Juniperus phoenicea Pistacia lentiscus Root system Stable isotopes Water sources 

Notes

Acknowledgments

We thank the Junta de Andalucía Environmental Agency for permission to work in the Natural Reserve; Will Cook, Jonathan Karr and Antonio Delgado Huertas for help with isotope and ion analyses; Tracey Crocker and Maria José Jorquera for help with lab determinations and plant care, and Harriet Whitehead for comments on an earlier version. This work was partly funded by the Spanish Ministry of Education and Science (grants CGL2004-00090 and CGL2007-63718). C. A. was supported by a Spanish MEC-Fulbright fellowship and by an I3P-CSIC contract. F. M. P. acknowledges the isotope training received thanks to an exchange grant of the ESF-SIBAE programme.

Supplementary material

442_2009_1447_MOESM1_ESM.doc (81 kb)
Supplementary material 1 (DOC 81 kb)

References

  1. Ackerly D (2004) Functional strategies of chaparral shrubs in relation to seasonal water deficit and disturbance. Ecol Monogr 74:25–44CrossRefGoogle Scholar
  2. Armas C, Pugnaire FI (2009) Ontogenetic shifts in interactions of two dominant shrub species in a semi-arid coastal sand dune system. J Veg Sci 20:535–546CrossRefGoogle Scholar
  3. Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16CrossRefGoogle Scholar
  4. Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413–428Google Scholar
  5. Burgess SSO, Adams MA, Turner NC, Ong CK (1998) The redistribution of soil water by tree root systems. Oecologia 115:306–311CrossRefGoogle Scholar
  6. Burgess SSO, Adams MA, Turner NC, White DA, Ong CK (2001) Tree roots: conduits for deep recharge of soil water. Oecologia 126:158–165CrossRefGoogle Scholar
  7. Callister AN, Arndt SK, Adams MA (2006) Comparison of four methods for measuring osmotic potential of tree leaves. Physiol Plant 127:383–392CrossRefGoogle Scholar
  8. Canadell J, Zedler PH (1995) Underground structures of woody plants in Mediterranean ecosystems of Australia, California, and Chile. In: Kalin-Arroyo MT, Zedler PH, Fox MD (eds) Ecology and biogeography of Mediterranean ecosystems in Chile, California and Australia. Springer, New York, pp 177–210Google Scholar
  9. Canadell J et al (1999) Structure and dynamics of the root system. In: Rodá F, Retana J, Gracia CA, Bellot J et al (eds) Ecology of Mediterranean evergreen oak forests. Springer, Berlin, pp 47–59Google Scholar
  10. Casper BB, Jackson RB (1997) Plant competition underground. Annu Rev Ecol Syst 28:545–570CrossRefGoogle Scholar
  11. Castillo JM, Casal AEB, Luque CJ, Luque T, Figueroa ME (2002) Comparative field summer stress of three tree species co-occurring in Mediterranean coastal dunes. Photosynthetica 40:49–56CrossRefGoogle Scholar
  12. Cregg BM (1992) Leaf area estimation of mature foliage of Juniperus. For Sci 38:61–67Google Scholar
  13. Dawson TE (1993) Hydraulic lift and the water use by plants: implications for water balance, performance and plant–plant interactions. Oecologia 95:565–574Google Scholar
  14. Dawson TE, Pate JS (1996) Seasonal water uptake and movement in root systems of Australian phreatophytic plants of dimorphic root morphology: a stable isotope investigation. Oecologia 107:13–20CrossRefGoogle Scholar
  15. Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable isotopes in plant ecology. Annu Rev Ecol Syst 33:507–559CrossRefGoogle Scholar
  16. Ehleringer JR (1993) Carbon and water relations in desert plants: an isotopic perspective. In: Ehleringer JR, Hall AE, Farquhar GD (eds) Stable isotopes and plant carbon/water relations. Academic Press, San Diego, pp 155–172Google Scholar
  17. Ehleringer JR, Dawson TE (1992) Water uptake by plants: perspectives from stable isotope composition. Plant Cell Environ 15:1073–1082CrossRefGoogle Scholar
  18. Ehleringer JR, Osmond CB (1989) Stable isotopes. In: Pearcy RW, Ehleringer JR, Mooney HA, Rundel PW (eds) Plant physiological ecology field methods and instrumentation. Chapman & Hall, London, pp 281–300Google Scholar
  19. Ehleringer JR, Schwinning S, Gebauer RE, Press MC, Scholes R, Barker MG (1999) Water use in arid land ecosystems. Advances in plant physiological ecology. British Ecological Society, Blackwell, London, pp 347-365Google Scholar
  20. Ellsworth PZ, Williams DG (2007) Hydrogen isotope fractionation during water uptake by woody xerophytes. Plant Soil 291:93–107CrossRefGoogle Scholar
  21. Filella I, Peñuelas J (2003a) Indications of hydraulic lift by Pinus halepensis and its effects on the water relations of neighbour shrubs. Biol Plant 47:209–214CrossRefGoogle Scholar
  22. Filella I, Peñuelas J (2003b) Partitioning of water and nitrogen in co-occurring Mediterranean woody shrub species of different evolutionary history. Oecologia 137:51–61CrossRefPubMedGoogle Scholar
  23. Franco AC, Nobel PS (1990) Influences of root distribution and growth on predicted water uptake and interspecific competition. Oecologia 82:151–157CrossRefGoogle Scholar
  24. Greenway H, Munns R (1980) Mechanisms of salt tolerance in nonhalophytes. Annu Rev Plant Physiol 31:149–190CrossRefGoogle Scholar
  25. Haase P, Pugnaire FI, Fernandez EM, Puigdef bregas J, Clark SC, Incoll LD (1996) An investigation of rooting depth of the semiarid shrub Retama sphaerocarpa (L.) Boiss. by labelling of ground water with a chemical tracer. J Hydrol 177:23–31CrossRefGoogle Scholar
  26. Haase P, Pugnaire FI, Clark SC, Incoll LD (1999) Diurnal and seasonal changes in cladode photosynthetic rate in relation to canopy age structure in the leguminous shrub Retama sphaerocarpa. Funct Ecol 13:640–649CrossRefGoogle Scholar
  27. Hasegawa PM, Bressan RA, Zhu J-K, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499CrossRefPubMedGoogle Scholar
  28. Huxman TE, Snyder KA, Tissue DT, Leffler AJ, Ogle K, Pockman WT, Sandquist DR, Potts DL, Schwinning S (2004) Precipitation pulses and carbon fluxes in semiarid and arid ecosystems. Oecologia 141:254-268Google Scholar
  29. Jackson RB, Canadell J, Ehleringer JR, Mooney HA, Sala OE, Schulze ED (1996) A global analysis of root distributions for terrestrial biomes. Oecologia 108:389–411CrossRefGoogle Scholar
  30. Jackson RB, Moore LA, Hoffmann WA, Pockman WT, Linder CR (1999) Ecosystem rooting depth determined with caves and DNA. Proc Natl Acad Sci USA 96:11387–11392CrossRefPubMedGoogle Scholar
  31. Jakab G, Ton J, Flors V, Zimmerli L, Metraux JP, Mauch-Mani B (2005) Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiol 139:267–274CrossRefPubMedGoogle Scholar
  32. Lin G, Sternberg LSL (1993) Hydrogen isotopic fractionation by plant roots during water uptake in coastal wetland plants. In: Ehleringer JR, Hall AE, Farquhar GD (eds) Stable isotopes and plant carbon–water relations. Academic Press, New York, pp 497–510Google Scholar
  33. Ludwig F, Dawson TE, Prins HHT, Berendse F, de Kroon H (2004) Below-ground competition between trees and grasses may overwhelm the facilitative effects of hydraulic lift. Ecol Lett 7:623–631CrossRefGoogle Scholar
  34. Martínez García F, Rodríguez JM (1988) Distribución vertical de las raíces del matorral de Doñana. Lagascalia 15:549–557Google Scholar
  35. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250CrossRefPubMedGoogle Scholar
  36. Nosetto MD, Jobbágy EG, Tóth T, Jackson RB (2008) Regional patterns and controls of ecosystem salinization with grassland afforestation along a rainfall gradient. Global Biogeochem Cycles 22:GB2015CrossRefGoogle Scholar
  37. Noy-Meir I (1973) Desert ecosystems: environment and producers. Annu Rev Ecol Syst 4:25–51CrossRefGoogle Scholar
  38. Padilla FM, Pugnaire FI (2007) Rooting depth and soil moisture control Mediterranean woody seedling survival during drought. Funct Ecol 21:489–495CrossRefGoogle Scholar
  39. Pagter M, Bragato C, Malagoli M, Brix H (2009) Osmotic and ionic effects of NaCl and Na2SO4 salinity on Phragmites australis. Aquat Bot 90:43–51CrossRefGoogle Scholar
  40. Pulido-Bosch A, Navarrete F, Molina L, Martínez-Vidal JL (1991) Quantity and quality of groundwater in the Campo de Dalías (Almería, SE Spain). Water Sci Technol 24:87-96Google Scholar
  41. Richards JH, Caldwell MM (1987) Hydraulic lift: substantial nocturnal water transport between soil layers by Artemisia tridentata roots. Oecologia 73:486–489CrossRefGoogle Scholar
  42. Salim M (1988) Loss of sodium from mung bean shoots to saline root media. J Agron Crop Sci 160:314–318CrossRefGoogle Scholar
  43. Schenk HJ, Jackson RB (2002) The global biogeography of roots. Ecol Monogr 72:311CrossRefGoogle Scholar
  44. Schlesinger WH et al (1990) Biological feedbacks in global desertification. Science 247:1043–1048CrossRefPubMedGoogle Scholar
  45. Schulze ED et al (1996) Rooting depth, water availability and vegetation cover along an aridity gradient in Patagonia. Oecologia 108:503–511CrossRefGoogle Scholar
  46. Schulze ED et al (1998) Downward flux of water through roots (i.e. inverse hydraulic lift) in dry Kalahari sands. Oecologia 115:460–462CrossRefGoogle Scholar
  47. Schwinning S, Davis K, Richardson L, Ehleringer JR (2002) Deuterium enriched irrigation indicates different forms of rain use in shrub/grass species of the Colorado Plateau. Oecologia 130:345–355CrossRefGoogle Scholar
  48. Schwinning S, Sala OE, Loik ME, Ehleringer JR (2004) Thresholds, memory, and seasonality: understanding pulse dynamics in arid/semi-arid ecosystems. Oecologia 141:191–193PubMedGoogle Scholar
  49. Schwinning S, Starr BI, Ehleringer JR (2005) Summer and winter drought in a cold desert ecosystem (Colorado Plateau). Part I. Effects on soil water and plant water uptake. J Arid Environ 60:547–566CrossRefGoogle Scholar
  50. Scott RL, Cable WL, Hultine KR (2008) The ecohydrologic significance of hydraulic redistribution in a semiarid savanna. Water Resour Res 44:W02440CrossRefGoogle Scholar
  51. Sobrado MA (2001) Effect of high external NaCl concentration on the osmolality of xylem sap, leaf tissue and leaf glands secretion of the mangrove Avicennia germinans (L.) L. Flora 196:63–70Google Scholar
  52. Specht RL (1988) Mediterranean-type ecosystems. A data source book. Kluwer, DordrechtGoogle Scholar
  53. Tattini M et al (2006) Morpho-anatomical, physiological and biochemical adjustments in response to root zone salinity stress and high solar radiation in two Mediterranean evergreen shrubs, Myrtus communis and Pistacia lentiscus. New Phytol 170:779–794CrossRefPubMedGoogle Scholar
  54. Valentini R, Scarascia Mugnozza E, Ehleringer JR (1992) Hydrogen and carbon isotope ratios of selected species of a Mediterranean macchia ecosystem. Funct Ecol 6:627–631CrossRefGoogle Scholar
  55. Williams DG, Ehleringer JR (2000) Intra- and interspecific variation for summer precipitation use in pinyon-juniper woodlands. Ecol Monogr 70:517–537Google Scholar
  56. Willson CJ, Manos PS, Jackson RB (2008) Hydraulic traits are influenced by phylogenetic history in the drought-resistant, invasive genus Juniperus (Cupressaceae). Am J Bot 95:299–314CrossRefGoogle Scholar
  57. Zou CB, Barnes PW, Archer S, McMurtry CR (2005) Soil moisture redistribution as a mechanism of facilitation in savanna tree–shrub clusters. Oecologia 145:32–40CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Department of BiologyDuke UniversityDurhamUSA
  2. 2.Estación Experimental de Zonas ÁridasConsejo Superior de Investigaciones CientíficasAlmeríaSpain

Personalised recommendations