Protea night-life: Ecological and commercial significance for soil hydraulics 1. Heidi-J Hawkins A,C, Hans Hettasch B and Michael D Cramer A

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1 Protea night-life: Ecological and commercial significance for soil hydraulics 1. Heidi-J Hawkins A,C, Hans Hettasch B and Michael D Cramer A A Department of Botany, University of Cape Town, Private Bag X1, Rondebosch, 7701, South Africa; B Arnelia Farms, P.O. Box 192, Hopefield, 7355, South Africa C Corresponding author Tel: Fax: heidi-jayne.hawkins@uct.ac.za 1 Submitted Feb 2009 in detailed format to Functional Plant Biology as Hydraulic redistribution by Protea Sylvia (Proteaceae) facilitates soil water recharge and water acquisition by an understorey grass and shrub. Please use the latter article to cite information. 1

2 Introduction During the day day,, if plant stomata are open, water moves along the water potential (ψ ψw) gradient from soil to leaf to atmosphere via the xylem xylem,, i.e. i.e. transpiration occurs (Fig. 1a) 1a).. A Att night night,, or whenever stomata close close, that gradient is removed removed... However, However, as long as plant roots span wet (usually deeper) deeper) and drier (usually shallow) soil areas, another water gradient exists exists,, i.e. between wet wetter ter and drier soil layers. In this case, w water ater moves along the ψw gradient from wet soil to the root, along the root xylem and out into drier soil soil,, resulting in soil wetting (Fig. 1b). This passive process is called hydraulic redistribution and has been documented for more than 50 taxa including trees, shrubs and grasses grasses,, particularly in summer summer-drought drought Mediterranean areas, but also in deserts deserts,, tropical forests (Jackson et al. 2000) and crop plants ((Sekiya Sekiya and Yano )).. H Hydraulic ydraulic redistribution is thought to be important for soil water recharge and facilitating nutrient uptake in waterwater-limite limite limited d and summer summer--drought drought ecosystems, e.g. Great Basin of the western United States States;; Mediterranean Mediterranean-type type ecosystems such as the Australian kwongan, the Californian chaparral and the Cape Florist Floristic ic Region (CFR) of South Africa Africa.. However, the ecological and commercial importance of hydraulic redistribution has not been well well--demonstrate demonstrate demonstrated d in the field. South African Proteaceae are often the largest shrubs in the CFR (2 (2 up to 10 m, m, Rebelo 2001) and have been shown to continue to transpire throughout the summer drought in the west of the CFR while other shallower shallower--rooted rooted plants cease to tr transpire anspire (van der Heyden and Lewis, 1988). Not only do Proteaceae continue to transpire throughout summer, but Proteaceae grow predominantly during the hot, dry summer months (Rebelo 2001). Roots are dimorphic with deep sinker sinker sinker roots and shallow lateral ro roots ots (Mortimer et al. 2003) similar similar to Australian Proteaceae (Pate et al. 1995). Rooting depths for shrub shrub--forms forms of SA Proteaceae are known to reach at least 3.6 m (Higgins et al. 1987) but may extend deeper depending on the water table table.. This implies that the deeper root rooted ed Proteaceae have access to deep water reserves which sustain photosynthesis, transpiration and growth through the summer. Fig. 1. Soil water moves along water potential gradients. In the day the gradient is usually from soil to plant to atmosphere (a), during the night or when stomata are closed and the gradient to atmosphere is removed, wat water er can move from wet to drier soil in a process called hydraulic redistribution (b). Pictures modified with permission courtesy courtesy of FC Meinzer, USDA Forest Servic Service, e, Forest Science Lab, Corvalis, OR, Our preliminary data using soil moisture probes showed that soil moisture in summer near lateral roots (0.2 ( m ddepth) epth) of Protea Sylvia was indeed higher than slightly deep deeper er in the soil profile (e.g. 0.5 m, m, Fig. 22)) while being similar to deeper soil layers (( m, Fig. 2) suggesting that hydraulic redistribution to dry upper soil layers was occurring. Therefore, we we hypothesize hypothesizedd that Proteaceae are able to hydraulic hydraulically ally redistribute water from deeper 2

3 moist soil layers to upper drier soil layers where nutrients occur. Redistributed water may aid in improving the water and nutrient status of the proteas, but it may also positively influence surrounding plants (Dawson 1993) and thus may be an important component maintaining diversity in these systems. In addition, if commercially grown Proteaceae are encouraged to have deep root systems via deep irrigation versus frequent shallow irrigation events, these crops may be made more tolerant to drought stress. Fig. 2 Soil moisture profiles adjacent to Protea Sylvia plants grown on aeolian sands at Arnelia Farms, Hopefield, South Africa, before supply of heavy water label. Values are means ± standard error (n=4). Brief materials and methods Our field experiment was accomplished by sinking PVC plumbing pipes 1.2 m into the soil profile next to farmed five-year old Protea Sylvia plants. Plants were irrigated via these pipes to simulate deep water supply and to encourage root growth near the pipe. After ca. 2 months, plants were either supplied with 25 L labelled water overnight or not. Labelled water, or so-called heavy water was characterized by the ratio of heavy 3

4 hydrogens ( 2 H) to light hydrogens ( 1 H) as δ 2 H (measured in ). Any increase in δ 2 H of the upper soil overnight was interpreted as evidence of hydraulic redistribution or hydraulic lift. Likewise, an increase in δ 2 H of shallow-rooted plants (Leysera gnapholodes, Asteraceae) under the protea was interpreted as evidence of water parasitism by the shrub, since the shrub had no access to water at depth. Lithium, an analogue of potassium that is not metabolised by plants and thus may be traced, was placed around plants receiving labelled water to determine whether a short-term supply of water at depth, and subsequent hydraulic redistribution, could contribute to nutrient uptake. A pot experiment with Sylvia and the shallow-rooted Fynbos grass, Cyanodon dactylon (Poaceae), was used to support field findings. In addition, an irrigation experiment tested the practical implications of hydraulic redistribution on sandy soils. In this experiment, Sylvia received 90 L water week -1, supplied via surface drippers (shallow irrigation), half surface drippers and half via a 1.2 m deep pipe (half shallow/half deep irrigation) or via the 1.2 m pipe only (deep irrigation). Deep irrigation was meant to simulate less frequent, high volume irrigation. Plants receiving deep irrigation were acclimatized to this irrigation over a few months to allow for root growth near the pipe. Results and Discussion It was found that the large Sylvia plants growing in aeolian sands in the so-called Strandveld Fynbos (Arnelia Farms, Hopefield, on the west coast of the CFR, S, E) took up the labelled water at a depth of 1.2 m as was evident from the label found in Sylvia stems (Fig. 3a). This confirmed that Sylvias had root access to the water supplied at depth, as was hoped. More importantly, Sylvia redistributed labelled water from 1.2 m depth to the 0.2 to 0.4 m soil layer, as indicated by increased δ 2 H of soil water from ± 0.7 to ± 3.0 (Fig. 3b) and a 52% increase in soil water from 0.48% to 0.89% moisture content. Linear mixing models attributed 0.68 ± 0.05% of the water in the upper soil layer to the label, or 8.5 ± 0.9% when using Sylvia plants as the label source. This is a rather small redistribution of water and may be linked to the short-term nature (overnight) of the experiment. The small amount of hydraulic redistribution was apparently insufficient to result in there being any difference in Li uptake between plants receiving 25 L heavy water label at depth and those receiving no additional water overnight. This suggests that hydraulic redistribution does not make a measurable contribution to ion uptake in the short-term. However, both treatments accumulated considerable amounts of Li over the three week period subsequent to watering, meaning that both treatments had access to sufficient soil moisture to allow the Li to diffuse to the roots. It is possible that plants in both treatments made use of hydraulically-lifted water from >2m depth (from trenches we know that Sylvia roots extend at least 2 m). Therefore, the amounts of additional water supplied at 1.2 m depth may have made no difference to the amount of Li in soil solution or to that taken up by the plant in this sandy soil. Snyder et al. (2008) found that hydraulically redistributed water did not increase the amount of 15 N acquired by the desert shrub Sarcobatus vermiculatus in dune sand. Both the present and the latter study were performed on sandy soils where hydraulic redistribution may be less important due to relatively less root-soil contact compared to clayey soils. Also matric forces (capillary and electrostatic) between water and sands are small due to the relatively large pore sizes of the sand. Relatively larger gravimetric forces may mean that hydraulically-lifted water quickly drains out of the upper sand layers. Water in stems of the shallow-rooted understorey shrub, L. gnaphalodes had similar δ 2 H values (338 ± 157 ) to stems of Sylvia, indicating water parasitism by L. gnaphalodes. Supporting this field data was pot experiments where Sylvias redistributed ca. 17% of another type of water label (radioactive 3 H 2 O) supplied, equating to 34 ± 1.2 ml plant -1. Also, the shallow-rooted local grass, Cyanodon dactylon (Poaceae), growing in the same pots as Sylvia were labelled, again indicting water parasitism. In the field, the two understory plants are likely dependent on periodic rainfall events during summer and/or reliant on water redistributed by large shrubs. Whatever the competitive interactions between protea and understorey plants during recruitment, once established, the persistence of grass and small shrubs such as the L. gnaphalodes under the canopies of Proteaceae shrubs in Fynbos are likely facilitated by water lifted by proteas during summer drought. This does 4

5 Fig. 3. δ 2 H of plants (a) and soil (b) at 20 to 40 cm soil depth the morning after supplying labelled water at depth to Protea Sylvia roots (labelled) or not (unlabelled). Values are means ± standard error (n=8). Letters indicate difference at the P<0.05 level after a one-way ANOVA and Newman Keuls multiple range test. 5

6 not imply that hydraulic redistribution always facilitates water use by shallow rooted plants, as some plants clearly redistribute water downwards after rains (e.g. Burgess et al., 1998) resulting in the removal of water resources away from shallower rooted understory plants. In the irrigation experiment, it was found that plants grew best on shallow irrigation compared to half shallow/half deep or just deep irrigation (Fig. 4). This confirmed to an extent what was found above, i.e. that hydraulic redistribution occurs and allows plants to acquire sufficient nutrients to grow but that, on a sandy soil, this does not equate to large volumes of water. It is possible that deep irrigation would make a plant more drought tolerant but this was not tested. It should be stressed that deep irrigation may well have more benefits on clay-containing soil. Regardless of soil type, the implication of hydraulic redistribution by proteas for commercial protea growers is that, after plant establishment, irrigation scheduled to encourage deep-rooted growth would enable plants access to moist soil, or even the water table, making these plants less dependent on irrigation events during the summer drought. After roots have reached this moist or wet deep layer, the grower would have the choice of irrigating to maximize production, or if water was limiting, to reduce irrigation shortterm without risking plant death. Fig. 4. Stem length of Protea Sylvia plants grown for 130 d with deep, shallow or half deep and half shallow irrigation. Values are means ± standard errors (n=15). Conclusions Protea Sylvia redistributed water from deep tap roots to surface lateral roots in both a pot and field study and this redistribution both recharged the soil water and was available to understorey plants. This is the first report of hydraulic redistribution and water parasitism in the Cape Floristic Region (CFR). We conclude that hydraulic redistribution by Proteaceae (and likely other deep-rooted plants) plays an important role in soil water recharge, water supply to shallow-rooted plants, and thus soil hydraulics and plants community structure during the summer drought of the Cape Floristic Region. Hydraulic redistribution is also an important adaptive feature that growers can consider when scheduling irrigation. 6

7 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 Burgess SSO, Adams MA, Turner NC, Ong CK (1998) The redistribution of soil water by tree root systems. Oecologia 115, Dawson T.E. (1993). Hydraulic lift and water use by plants: implications for water balance, performance and plant-plant interactions. Oecologia 95, Higgins KB, Lamb AJ and 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, Jackson RB, Sperry JS, Dawson TE (2000) Root water uptake and transport: using physiological processes in global predictions. Trends in Plant Science 5, 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 x Protea eximia)? South African Journal of Botany 69, 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, Rebelo AG (2001) Proteas. A field guide to the Proteas of Southern Africa. Fernwood Press, South Africa. ISBN 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, Snyder KA, James JJ, Richards JH, Donovan LA (2008) Does hydraulic lift or nighttime transpiration facilitate nitrogen acquisition? Plant and Soil 306, 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,