Some secrets of Argania spinosa water economy in a semiarid climate

Some Secrets of Argania spinosa Water Economy in a Semiarid Climate Mari Cruz Díaz Barradasa, María Zunzuneguia, Mari Paz Esquiviasa, Said Boutalebb, Javier Valera-Burgosa, Tarek Tagmab and Fátima Ain-Lhoutc aDepartamento de Biología Vegetal y Ecología, Universidad de Sevilla, Spain bDépartement de Géologie, Faculté des Sciences, Université Ibn Zohr, Morocco cFaculté Polydisciplinaire de Taroudant, Université Ibn Zohr, Morocco [email protected] Received: July 23rd, 2012; Accepted: September 17th, 2012 Argania spinosa is an example of an avoider tree growing under semi-arid conditions in Morocco. To assess what are the physiological strategies of this species, different variables were measured through an annual cycle in two populations located in the species’ main distribution area. Results show the expected decrease of leaf water potential (Ψ) with an increase of water-use efficiency (A/gs) with the onset of the dry season. In summer, leaf conductance (gs) was sensitive to vapour pressure deficit (VPD), and stomatal closure occurred over 30 mbar of VPD. Surprisingly, carbon isotope discrimination (δ13C) maintained very low values over the year, with almost no relationship with any physiological or morphological variable. Hence Argania spinosa presents a complex set of mechanisms to avoid water deficit, but δ13C cannot be used as an ecological tracer of long term WUE. Keywords: Drought adaptation, Carbon isotope discrimination, Water use efficiency (WUE). Dryland forests and woodlands account for some 6% of the world’s forests. The argan tree [Argania spinosa (L.) Skeels] is an example of a sustainable resource in a semiarid climate [1]. Argan oil, obtained from the seeds, is manufactured by women cooperatives and has become famous in the last two decades for its cosmetic virtues [1-3]. Goats and sheep graze on argan leaves as elevated grasslands, especially during the dry season [4]. Manures produced from animals’ wastes are used as a fertilizer for cereal crops growing under the canopy of the argan trees [5]. In addition, as argan wood is very hard, it can be used as fuel or building of agricultural tools. Furthermore, old trees have spiritual value and are linked to sacred places [6]. On the other hand, biodiversity conservation, the regulation of the hydrological cycle, soil protection and carbon fixation are examples of services generated by these ecosystems and can be defined as cultural landscapes. A. spinosa is endemic to Morocco and grows in areas ranging from lower than 100 to 300 mm of annual rainfall, maintaining an elevated productivity, only shedding leaves for a variable time under extremely dry conditions [4]. The aim of this contribution is to explain some of the water economy peculiarities of this tree in its natural habitat. For this purpose we have used some physiological measurements and carbon isotope discrimination (δ13C) that is widely accepted as an index of long-term WUE [7]. In particular, we try to answer the following questions: (1) what are the seasonal and daily changes in plant and leaf water status and stomatal behaviour in A. spinosa? and (2) whether carbon isotope discrimination could be used as an integrative ecological tracer to evaluate long term WUE in this semiarid species? In two A. spinosa populations in the neighbourhood of Agadir, (main distribution area of the species) detailed seasonalecophysiological measurements were performed during the 2010 annual cycle. One was a coastal population with a rocky soil facing the Atlantic Ocean, and the other was located inland, 5 km to the south of Agadir, in an area traditionally managed for livestock raising, with a well developed soil belonging to the Souss river basin [8]. The climate is temperate, due to marine influence, with maximum temperatures only seldom surpassing 30ºC, and minimum temperatures never below 7ºC. Annual rainfall is scarce, 232 mm, and concentrated from October to April, with a long summer drought. Relative humidity is elevated, with frequent fogs during the summer period. February April September November Leaf water potential (MPa) -3 -2 -1 0 LWPpd Coast LWPpd Inland LWPmd Coast LWPmd Inland Figure 1: Average predawn and midday leaf water potential of A. spinosa trees in the two sampling zones throughout the study period. Each bar represents ±sd. Leaf water potentials (Ψ) of trees were high during the mild winter conditions; figures decline through spring and markedly in summer, reaching the lowest values in September. Water potentials recovered in autumn, except for Ψmd in the inland zone, exhibiting similar low values in November as in September (Figure 1). The coastal population showed lower Ψmd values than the inland population in February and September, but with no significant differences (P>0.05). NPC Natural Product Communications 2013 Vol. 8 No. 1 11 - 14 12 Natural Product Communications Vol. 8 (1) 2013 Barradas et al. In the coastal zone, intrinsic water use efficiency (WUEi=A/gs) was elevated in April and September, while in the inland population the highest values were reached in September. However, significant difference between the two populations was only found in April (P<0.001) (Figure 2). February April September November Water use efficiency (A/g s ) 0 20 40 60 80 100 120 140 Coast Inland Figure 2: Average intrinsic WUE (A/gs) in the two sampling zones throughout the study period. Each bar represents ±sd. A/gs was correlated with ci/ca (r=-0.91, P<0.001), which indicated a strong dependence of stomatal control. Under summer conditions, leaf conductance seemed to respond to the increase in VPD; when it reached values over 20 mbar, there was a fast decrease in stomatal conductance, with a complete stomatal closure over 30 mbar of VPD (Figure 3). VPD (mbar) 10 15 20 25 30 35 40 g s (mol m -2 s -1 ) 0.00 0.05 0.10 0.15 0.20 0.25 0.30 0.35 Y=-0.011 x + 0,408 R2 = 0.497, P<0.001 Figure 3: Relationship between Vapour Pressure Deficit (VPD in mbar) and stomatal conductance (gs in mol m-2s-1) in a summer day, and linear regression between both variables. The points indicate measurements of individual trees in the morning and midday. Figure 4: Average carbon isotope discrimination (δ13C in ‰) in the two sampling zones throughout the study period. Each bar represents ±sd. The large seasonal changes in water availability were not clearly reflected in seasonal changes in δ13C. In both populations, values ranged between -28.5 ‰ in February to -30 ‰ for the rest of the year. Significant differences were found between February and April, and February and September values in the inland population (p<0.05), while in the coastal population significant differences only occurred between the February and April data (P<0.01) (Figure 4). Leaf Mass Area (g m-2) showed a clear increase during the study period, from February (70-100 g m-2) to November, (165-170 g m-2), which might be associated with leaf longevity. The coastal population presented significantly higher values than the inland population throughout the study period (P<0.05), except for November (Figure 5). Figure 5: Average leaf mass area (LMA in g m-2) in the two sampling zones throughout the study period. Each bar represents ±sd. Only a weak correlation was found between Ψpd, Ψmd and δ13C (P<0.05 in inland population). In all other cases, no significant relationships were found between either physiological or morphological variables and δ13C, with only partial relations in a specific month (Table 1). For example, δ13C was correlated with N content (%) in February (P<0.05). Table 1: Pearson correlation coefficients between δ13C and different physiological (Ψpd, Ψmd, N%, A/gs) and morphological (LMA) variables in coastal and inland A. spinosa populations. Coastal Inland Ψ pd 0.231 0.434* Ψmd 0.174 0.442* N% 0.302 0.266 A/gs -0.281 -0.264 LMA -0.027 -0.154 *Significant correlation (P<0.05). The results of this study show that Argania spinosa adjusts its physiological attributes according to environmental conditions, both on a daily and seasonal scale. Over the course of the day, following radiation and temperature maxima, Ψ showed more negative values in all months at midday, as has been reported in Mediterranean species [9-10]. Leaf water potential values exhibited minimum values in summer, as shown in a previous study [4]. Even though the absence of rainfall and the elevated summer temperatures occurring at the beginning of September (due to air masses from the Sahara), Ψmd never decreased below -3 MPa, while in a mountain population summer Ψmd could reach -6 MPa [4]. Our results of Ψpd and Ψmd in this study are similar to those reported for O. europaea without irrigation under Mediterranean climate [11]. The seasonal increase of WUEi in spring and summer might be associated with either an increase in photosynthetic assimilation or February April September November 13C -32 -31 -30 -29 -28 -27 -26 -25 Coast Inland February April September November LMA (g·m -2 ) 0 50 100 150 200 250 Coast Inland Argania spinosa water economy in a semiarid climate Natural Product Communications Vol. 8 (1) 2013 13 a decrease in stomatal conductance. Previous results have shown a linear relationship between A and gs in A. spinosa [4], but in summer the increase in WUEi is mainly associated with stomatal control, which is evidenced by the strong relation between A/gs and ci/ca. Our results suggest that the stomata were responsive to VPD, although we cannot discard a possible role of chemical or hydraulic signals coming from the roots. In olive trees it is widely accepted that VPD is the main driving mechanism for gs control [12]. The results of carbon isotope discrimination suggested differences in the process of leaf maturation; young A. spinosa leaves in February had a less negative δ13C than mature leaves in the rest of the year; similar results have been reported for Quercus pubescens [7]. The existence of a significant correlation between δ13C and N content in February supports the hypothesis that high leaf N concentrations lead to increase photosynthetic capacity during the period of leaf development [13]. In mature leaves, most leaf carbon is formed during periods of good water status, presenting in all cases elevated isotope discrimination. On the other hand, leaves are always very soft, with LMA lower than 170 g m-2 in summer, which indicated high internal leaf conductance and subsequently high discrimination at the site of carboxylation [14]. Hence the leaves of A. spinosa are not very hard, but maintain elevated stomatal control, a high photosynthetic activity during favourable periods [4], and probably a short lifespan. In Mediterranean scrub species [15] found a higher correlation between carbon isotope discrimination and leaf water potential in drought semi-deciduous species that present a shorter leaf lifespan than in evergreen sclerophylls. In A. spinosa we found soft leaves, in which most carbon is assimilated during the favourable season, but not showing a clear relationship with leaf water potential, although this tree is able to assimilate carbon during the early hours of the dry season, maintaining an elevated productivity. Experimental General: In both populations, 10 well developed trees were permanently marked, and measurements of gas-exchange and leaf water potential were taken in the field and leaf samples were collected for leaf mass area and carbon and nitrogen content and stable isotopes measurements. Sampling was carried out during different phases of the seasonal cycle and under contrasted environmental conditions in February, April, September and November. Measurements: Measurement of net photosynthetic rates (A), stomatal conductance (gs) and transpiration rates (E) were made using a portable compact CO2/H2O system (LCi-portable photosynthesis ADC system, UK). Intrinsic water use efficiency (WUEi) was calculated as the ratio of net photosynthesis to stomatal conductance (WUEi=A/gs). Leaf surface was computed in the laboratory (Midebmp, Ordiales, 2000), and gas exchange measurements were recalculated for leaf surfaces. Leaf Mass Area was calculated as the ratio between leaf dry weight and leaf surface (g m-2). Gas-exchange measurements were made between 08.30 and 10.30 hours solar time, and repeated between 12 and 12.30 h to evaluate possible midday depression of leaf conductance. VPD values were calculated using air temperature and moisture content data from our LCi, following the method of Coombs et al. [16]. Predawn (Ψpd) and midday leaf water potential (Ψmd) were determined in the field with a Scholander type pressure chamber (Manofrigido, Lisbon, Portugal) using terminal shoots. Sun exposed leaf samples were collected from the same trees, oven-dried at 60ºC for 48 h, and milled to fine powder for isotopic analysis using a ball mill (Retsch, Haan, Germany). Leaf N and C concentrations and δ15N and δ13C signatures of the ground leaf material were determined in separate runs for N and C using an elemental analyzer, and coupled with a continuous-flow isotope ratio mass spectrometer. For detailed methodology see [15]. Statistical evaluation: Normal distribution of the variables was tested by the Kolmogorov-Smirnov test. One-way ANOVAs were applied to compare significant differences between sites for any of the studied variables. Bivariate correlation tests were made between the different variables. Regression analyses were performed between correlated variables. All statistical tests were made with SPSS 18 for Windows. Acknowledgments - This project was supported by a PCI program of the AECI (Spanish Agency of International Cooperation). 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