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Variation in Hydraulic Architecture and Gas-Exchange in Two Desert Sub-Shrubs, Hymenoclea Salsola (T

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Variation in Hydraulic Architecture and Gas-Exchange in Two Desert Sub-Shrubs, Hymenoclea Salsola (T Oecologia (2000) 125:1–10 © Springer-Verlag 2000 Jonathan P. Comstock Variation in hydraulic architecture and gas-exchange in two desert sub-shrubs, Hymenoclea salsola (T. & G.) and Ambrosia dumosa (Payne) Received: 13 December 1999 / Accepted: 31 March 2000 Abstract Adjustment of hydraulic architecture in re- per unit photosynthetic canopy by increasing allocation sponse to environmental conditions was studied in two to an organ which simultaneously performs photosyn- warm-desert sub-shrubs, Hymenoclea salsola and Am- thetic, support, and transport functions. brosia dumosa, both at the level of genetic adaptation along a climatic gradient and plastic response to immedi- Key words Climatic ecotypes · Hydraulic limitation · ate growth conditions. Individuals of both species origi- Hydraulic signaling · Plant morphology · Allocation nating from southern populations developed higher leaf- specific hydraulic conductance in the common green- house than individuals from northern populations. Hy- Introduction draulic conductance was higher in plants grown at high temperature, but did not vary as a function of growth rel- Relationships between leaf-specific hydraulic ative humidity. Hydraulic conductance was not correlat- conductance (LSC) and transpiration (E) ed within species with individual variation in vessel di- ameter, cavitation vulnerability, or root:shoot ratio, but Hydraulic architecture is increasingly studied with re- was strongly, negatively correlated with the fraction of spect to the limitations placed by within-plant water total plant biomass allocated to leaves. For both species, transport on plant productivity. Stomata play a well- stomatal conductance (gs) at high leaf-to-air vapor pres- understood key role as the control point for integrating ν sure difference ( ) was tightly correlated with variability the often conflicting needs to capture CO2 from the at- in hydraulic conductance, as was the sensitivity of sto- mosphere for photosynthesis and growth, and to limit matal closure to increasing ν. Experimentally increasing water loss from plant tissues to avoid dehydration shoot water potential by soil pressurization, under condi- (Cowan 1977). A substantial body of empirical data and tions where high ν had already caused stomatal closure, theory has been produced over the past few decades on led to substantial stomatal reopening in both species, but the degree of limitation actually imposed on photosyn- recovery was significantly higher in H. salsola. Hydrau- thesis and growth by stomatal closure (Farquhar and lic conductance was higher in H. salsola than A. dumosa. Sharkey 1982), and how stomata should behave in re- H.salsola also differed from A. dumosa by being a repre- sponse to environmental variability to maximize carbon sentative of a highly specialised group of desert shrubs gain over a range of different time-scales (Aphalo and which use the twigs as a major photosynthetic organ. Jarvis 1993; Ball et al. 1987; Cowan and Farquhar 1977; The southern population of H. salsola produced far few- Leuning 1995; Monteith 1995). In recent years, this area er leaves and relied much more heavily on twig photo- has seen considerable development in two related areas: synthesis than the northern population. At the whole- (1) the potential role of hormones, especially those plant level, increased reliance on twig photosynthesis borne in the transpiration stream itself, to make stomata was associated with higher leaf-specific hydraulic con- responsive to root:shoot communications (Dodd et al. ductance, but equivalent whole-plant photosynthesis on 1996; Schurr and Schulze 1996; Tardieu 1996; White- –1 either a dry weight (µmol CO2 g ) or nitrogen basis head 1998), and (2) the role of hydraulic signals which –1 (µmol CO2 g )). This suggests that twig photosynthesis could be transduced either in the root as a function of might be one way of increasing hydraulic conductance root and soil water status, or at the photosynthetic organ where, at the end of the transpiration stream, plant water J. Comstock (✉) Boyce Thompson Institute, Tower Road, Ithaca, NY 14853, USA potentials will be lowest (Comstock and Mencuccini e-mail: [email protected] 1998; Fuchs and Livingston 1996; Saliendra et al. Tel.: +1-607-2541214, +1-607-2541242 1995). 2 Transduction of a water-status signal at the photosyn- Methods thetic organ could be especially important if the hydraulic conductance of the plant, and the consequent water po- Plant material tential gradients between root and shoot, are variable and potentially limiting to plant function. Considerable evi- Seed of H. salsola (T. & G.) and Ambrosia dumosa (Payne), both subshrubs of the Mojave and Sonoran deserts of western North dence exists that hydraulic conductance is indeed partial- America, was collected from natural populations and grown in the ly limiting. Strong correlations have been observed be- greenhouse at the Boyce Thompson Institute for Plant Research in tween stomatal and hydraulic conductances in both crop Ithaca, NY (300 m). In the wild, H. salsola generally occurs in (Meinzer et al. 1990; Mencuccini and Comstock 1999; deep sandy or gravelly soils, especially intermittent stream beds Sober 1997; Sohan et al. 1999; Sperry and Pockman (desert washes), while A. dumosa is broadly distributed on slopes and flats, often with thin soil and minimal water-holding capacity. 1993) and wild plant species (Bond and Kavanagh 1999; For both species, seed collection sites were chosen from both the Irvine et al. 1998; Meinzer et al. 1999; Ryan and Yoder southern and northern extremes of the natural range. The northern 1997). Several studies have also reported that short-term collection site was dominated by Larrea scrub and Joshua tree manipulations of shoot water status can be directly linked woodland just south of the Beaverdam mountains at 945 m eleva- tion and 37.00°N latitude. The southern seed-collection site was lo- to changes in stomatal aperture (see previous paragraph). cated in similar topography in the Organ Pipe National Monument on the Arizona-Mexico border at 512 m elevation and 31.90 N lati- tude. These sites had strongly contrasting conditions during the Relationship to climate growing season, driven largely by the seasonality of precipitation (Mencuccini and Comstock 1997). The northern site had a strong unimodal precipitation pattern with maximums in the winter The expected relationship between plant hydraulic con- months, and most plant growth in the spring as temperatures ductance and productivity should be very sensitive to cli- warmed. The southern site had milder winters and a bimodal pre- matic factors that affect photosynthetic water-use effi- cipitation pattern. In the south, both spring and summer growing ciency. In this context, the intermountain west of North periods could regularly support activity by the study species, and the growing season was warmer. America presents some excellent experimental gradients. Due, in part, to the presence of north-south-running mountain chains bounding it on both the east and west, a Cultural conditions continuous belt of aridland ecosystems runs from north- The plants were grown in 30-dm3 pots in a soil mix of 3:1:1 fritted ern Mexico to southern Canada. Although mostly classi- clay (Turface):silica sand:pasteurized topsoil, and were watered fied as arid or semi-arid, these ecosystems vary greatly daily with nutrient solution containing 55:18:55 ppm N:P:K from in mean annual temperature and the seasonality of pre- Peter’s Excel. Photoperiod from combined artificial (an alternating cipitation, both of which strongly affect the leaf-to-air bank of 1000-W high-pressure Na vapor, 1000-W Super Metal Ha- ν lide, and 150-Watt incandescent floodlights) and natural lighting vapor pressure difference ( ) driving water-loss during was 12 h with a total irradiance (400–700 nm) of 44 mol m–2 day–1 the growing season. Comstock and Ehleringer (1992) re- in all treatments. All treatments were set up in well-ventilated ported that some warm-desert species occupying the greenhouses with internal fans for stirring foliage. CO2 concentra- southern half of this gradient experience a more than tions were monitored continuously by a single infra-red gas-ana- ν lyser (IRGA) (Horiba, model PIR-2000, Irvine, Calif., USA) which 2-fold difference in growing-season among different cycled continuously between air sampling lines from each of the populations, and, for Hymenoclea salsola, showed a cor- three greenhouses and an outside reference line. Mean CO2 was relation between an index of growing-season ν and inter- 375/390 µmol mol–1 (day/night). Although variations in mean daily –1 population variation in both tissue-level intrinsic water {CO2} of up to 15 µmol mol were seen as a function of different weather patterns, all the greenhouse bays and outside air had the use efficiency (i.e., intracellular [CO2] as indicated by same daily mean values±1.0 µmol mol–1. carbon isotope discrimination), and also canopy architec- Plants from both populations were grown under three contrast- ture (i.e., relative contribution of twigs to the photosyn- ing conditions of temperature and humidity to test whether tem- thetic canopy). perature itself or ν during growth had a greater effect on the plas- tic development of hydraulic conductance. These growth treat- The geographic variation in these traits suggests that ments included a hot environment (33/20°C day/night) at low hu- population-level adaptation has occurred in H. salsola to midity, 26% daytime relative humidity (RH), a similar hot envi- adjust intrinsic plant factors in a manner that may com- ronment at high humidity (67% RH), and a cool environment pensate for climatic factors influencing plant water use (23/20°C day/night) at low RH (37%), referred to as hot-dry (h), and status. Direct measurements of hydraulic conduc- hot-humid (hh) and cool-dry (c), respectively. The hh and c had the same ν. The species had photosynthetic temperature optima tance, however, were not previously made on plants very near 29°C (Comstock and Ehleringer 1988), and so photo- from this gradient.
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