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Plant function and evolutionary biology
RESEARCH ARTICLE

Hydraulic redistribution by Protea ‘Sylvia’ (Proteaceae) facilitates soil water replenishment and water acquisition by an understorey grass and shrub

Heidi-J. Hawkins A D , Hans Hettasch B , Adam G. West A C and Michael D. Cramer A
+ Author Affiliations
- Author Affiliations

A Department of Botany, University of Cape Town, Private Bag X1, Rondebosch 7701, South Africa.

B Arnelia Farms, PO Box 192, Hopefield 7355, South Africa.

C Department of Integrative Biology, University of California, Berkeley, Berkeley 94720, USA.

D Corresponding author. Email: heidi-jayne.hawkins@uct.ac.za

Functional Plant Biology 36(8) 752-760 https://doi.org/10.1071/FP09046
Submitted: 26 February 2009  Accepted: 16 May 2009   Published: 23 July 2009

Abstract

Proteaceae of the Cape Floristic Region, South Africa, transpire throughout the summer drought, implying access to deep water. Hydraulic redistribution by Protea ‘Sylvia’ [P. susannae E. Phillips × P. exima (Salisb. Ex Knight) Fource; Proteaceae] was investigated in overnight pot and field experiments, where it was hypothesised that (1) Proteaceae replenish water in upper soil layers, (2) hydraulic redistribution facilitates nutrient uptake and (3) shallow-rooted understorey plants ‘parasitise’ water from proteas. Potted Sylvias redistributed ~17% of the tritiated water supplied, equating to 34 ± 1.2 mL plant−1. Shallow-rooted Cyanodon dactylon (L.) Pers. (Poaceae), plants growing in the same pots as Sylvia contained amounts of labelled water similar to those found in Sylvia, indicting water parasitism. In the field, Sylvia plants growing in aeolian sands took up the deuterated water applied at 1.2 m depth as indicated by increased δ2H of plant xylem water from –38 ± 0.8 to 334 ± 157‰. This deuterated water was then redistributed to the upper soil layer (0.2 and 0.4 m), as indicated by increased δ2H of soil water from –24.5 ± 0.7 to –8.0 ± 3.0‰ and soil moisture from 0.48 to 0.89%. Lithium, as a K-analogue, was taken up equally by plants watered with deep water and those not watered, probably since both had access to naturally-occurring deep water. Water in stems of the shallow-rooted understorey shrub, Leysera gnaphalodes (L.) L. (Asteraceae) had similar δ2H values to stems of Sylvia (P = 0.939), again indicating water parasitism was tightly coupled to the protea. We conclude that hydraulic redistribution by Proteaceae plays an important role in soil water replenishment, water supply to shallow-rooted plants, and, thus, ecosystem structure and function during the summer drought of the Cape Floristic Region.

Additional keywords: Cynodon dactylon, deuterium, Lysera gnaphalodes, Proteaceae, stable isotopes, summer drought, tritium.


Acknowledgements

The authors thank Molteno Brothers Pty Ltd, Elgin Glen, South Africa for providing Sylvia cuttings, as well as the National Research Foundation of South Africa and the South African Protea Producers and Exporters Association for financial support during this project. The authors also thank Carin Basson for technical assistance.


References


Barber SA (1995) ‘Soil nutrient bioavailability, a mechanistic approach.’2nd edn. (John Wiley & Sons: New York)

Bond WJ , Cowling RM , Richards MB (1992) Competition and coexistence. In ‘Fynbos nutrients, fire and diversity’. (Ed. RM Cowling) pp. 206–225. (Oxford University Press: Oxford)

Burgess SSO, Adams MA, Turner NC, Ong CK (1998) The redistribution of soil water by tree root systems. Oecologia 115, 306–311.
Crossref | GoogleScholarGoogle Scholar | open url image1

Burgess SSO, Pate JS, Adams MA, Dawson TE (2000) Seasonal water acquisition and redistribution in the Australian woody phreatophyte, Banksia prionotes. Annals of Botany 85, 215–224.
Crossref | GoogleScholarGoogle Scholar | open url image1

Burgess SSO, Adams MA, Turner NC, White DA, Ong CK (2001) Tree roots: conduits for deep recharge of soil water. Oecologia 126, 158–165.
Crossref | GoogleScholarGoogle Scholar | open url image1

Caldwell MM, Richards JH (1989) Hydraulic lift: water efflux from upper roots improves effectiveness of water uptake by deep roots. Oecologia 79, 1–5.
Crossref | GoogleScholarGoogle Scholar | open url image1

Caldwell MM, Dawson TE, Richards JH (1998) Hydraulic lift: consequences of water efflux from the roots of plants. Oecologia 113, 151–161.
Crossref | GoogleScholarGoogle Scholar | open url image1

Coleman ML, Shepherd TJ, Durham JJ, Rouse JE, Moore GR (1982) Reduction of water with zinc for hydrogen isotope analysis. Analytical Chemistry 54, 993–995.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dawson TE (1993) Hydraulic lift and water use by plants: implications for water balance, performance and plant–plant interactions. Oecologia 95, 565–574. open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hawkins H-J, Wolf G, Stock WD (2005) Cluster roots of Leucadendron laureolum (Proteaceae) and Lupinus albus (Fabaceae) take up glycine intact: an adaptive strategy to low mineral N in soils? Annals of Botany 96, 1275–1282.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Heelemann S, Proches S, Rebelo AG, van Wilgen B, Porembski S, Cowling RM (2008) Fire season effects on the recruitment of non-sprouting serotinous Proteaceae in the eastern (bimodal rainfall) fynbos biome, South Africa. Austral Ecology 33, 119–127.
Crossref | GoogleScholarGoogle Scholar | open url image1

van der Heyden F, Lewis OAM (1988) Seasonal variation in the photosynthetic capacity with respect to plant water status of five species of the mediterranean climate region of South Africa. South African Journal of Botany 55, 509–515. open url image1

Higgins KB, Lamb AJ, Van Wilgen BW (1987) Root systems of selected plant species in mesic mountain fynbos in the Jonkershoek Valley, south-western Cape Province, South Africa. South African Journal of Botany 53, 249–258. open url image1

Horton JL, Hart SC (1998) Hydraulic lift: a potentially important ecosystem process. Trends in Ecology & Evolution 13, 232–235.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jackson RB, Sperry JS, Dawson TE (2000) Root water uptake and transport: using physiological processes in global predictions. Trends in Plant Science 5, 482–488.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Leffler AJ, Ivans CY, Ryel RJ, Caldwell MM (2004) Gas exchange and growth responses of the desert shrub Artemisia tridentata and Chrysothamnus nauseosus to shallow- vs. deep-soil water in a glasshouse experiment. Environmental and Experimental Botany 51, 9–19.
Crossref | GoogleScholarGoogle Scholar | open url image1

Leffler AJ, Peek MS, Ryel RJ, Ivans CY, Caldwell MM (2005) Hydraulic redistribution through the root systems of senesced plants. Ecology 86, 633–642.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lu N, Likos WJ (2004) Rate of capillary rise in soil. Journal of Geotechnical and Geoenvironmental Engineering 130, 646–650.
Crossref | GoogleScholarGoogle Scholar | open url image1

Marschner H (1995) ‘Mineral nutrition of higher plants.’ (Academic Press: London)

McElrone AJ, Bichler J, Pockman WT, Addington RN, Linder CR, Jackson RB (2007) Aquaporin-mediated changes in hydraulic conductivity of deep tree roots accessed via caves. Plant, Cell & Environment 30, 1411–1421.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mortimer P, Swart JC, Valentine AG, Jacobs G, Cramer MD (2003) Does irrigation influence the growth, yield and water use efficiency of the Sylvia hybrid ‘Sylvia’ (Protea susannae × Protea eximia)? South African Journal of Botany 69, 135–143. open url image1

Pate JS, Jeschke WD, Aylward MJ (1995) Hydraulic architecture and xylem structure of the dimorphic root systems of south-West Australian species of Proteaceae. Journal of Experimental Botany 46, 907–915.
Crossref | GoogleScholarGoogle Scholar | open url image1

Peñuelas J, Filella I (2003) Deuterium labelling of roots provide evidence of deep water access and hydraulic lift by Pinus nigra in a Mediterranean forest of NE Spain. Environmental and Experimental Botany 49, 201–208.
Crossref | GoogleScholarGoogle Scholar | open url image1

Proches S, Cowling RM, Du Preez DR (2005) Patterns of geophyte diversity and storage organ size in the winter-rainfall region of southern Africa. Diversity & Distributions 11, 101–109.
Crossref | GoogleScholarGoogle Scholar | open url image1

Querejeta JI, Egerton-Warburton LM, Allen MF (2007) Hydraulic lift may buffer rhizosphere hyphae against the negative effects of severe soil drying in a California oak savanna. Soil Biology & Biochemistry 39, 409–417.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rebelo AG (2001) ‘Proteas. A field guide to the Proteas of Southern Africa.’ (Fernwood Press: Cape Town, South Africa)

Richards JH, Caldwell MM (1987) Hydraulic lift: substantial nocturnal water transport between soil layers by Artemisia tridentata roots. Oecologia 73, 486–489.
Crossref | GoogleScholarGoogle Scholar | open url image1

Richards MB, Cowling RM, Stock WD (1997) Soil factors and competition as determinants of the distribution of six fynbos Proteaceae species. Oikos 79, 394–406.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ryel RJ (2004) Hydraulic redistribution. Progress in Botany 65, 413–435. open url image1

Ryel RJ, Caldwell MM, Leffler AJ, Yoder CK (2003) Rapid soil moisture recharge to depth by roots in a stand of Artemisia tridentata. Ecology 84, 757–764.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sekiya N, Yano K (2004) Do pigeon pea and sesbania supply groundwater to intercropped maize through hydraulic lift? – Hydrogen stable isotope investigation of xylem waters. Field Crops Research 86, 167–173.
Crossref | GoogleScholarGoogle Scholar | open url image1

Snyder KA, James JJ, Richards JH, Donovan LA (2008) Does hydraulic lift or nighttime transpiration facilitate nitrogen acquisition? Plant and Soil 306, 159–166.
Crossref | GoogleScholarGoogle Scholar | open url image1

Thuiller W, Lavorel S, Midgley G, Lavergne S, Rebelo T (2004) Relating plant traits and species distributions along bioclimatic gradients for 88 Leucadendron taxa. Ecology 85, 1688–1699.
Crossref | GoogleScholarGoogle Scholar | open url image1

Vlok JHJ, Yeaton RI (2000) Competitive interactions between overstorey proteas and sprouting understorey species in South African mountain fynbos. Diversity & Distributions 6, 273–281.
Crossref | GoogleScholarGoogle Scholar | open url image1

West AG, Patrickson SJ, Ehleringer JR (2006) Water extraction times for plant and soil materials used in stable isotope analysis. Rapid Communications in Mass Spectrometry 20, 1317–1321.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Witkowski ETF, Mitchell DT (1987) Variations in soil phosphorus in the fynbos biome, South Africa. Journal of Ecology 75, 1159–1171.
Crossref |
open url image1