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Trees (2020) 34:89–99 https://doi.org/10.1007/s00468-019-01899-2 ORIGINAL ARTICLE The adjustment of Prosopis tamarugo hydraulic architecture traits has a homeostatic efect over its performance under descent of phreatic level in the Atacama Desert Marco Garrido1,2 · Horacio Bown3 · José Ayamante2 · Magda Orell3 · Andrea Sánchez2 · Edmundo Acevedo2 Received: 1 April 2019 / Accepted: 10 August 2019 / Published online: 24 August 2019 © Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract Key message Prosopis tamarugo undergoes several modifcations of its hydraulic architecture, which has a homeostatic efect on its performance under descent of phreatic level. Abstract Groundwater extraction for mining has generated a large area of descent of phreatic level in the Llamara Salt Flat, Atacama Desert, where Prosopis tamarugo lives as a strict phreatophyte. We study diferent hydraulic architecture traits of P. tamarugo after 12 years of exposure to a descent of phreatic level of ~ 11 m to assess its acclimation capacity. Under this condition, tree size was reduced making the structure of trees shrubbier. At branch level, leaf shedding increased Huber Value and theoretical leaf-specifc hydraulic conductivity. At vascular tissue level, vessel composition decreased signif- cantly due to an increase in vessel density and a slight decrease in mean vessel area. This meant that there were no difer- ences of theoretical sapwood-specifc hydraulic conductivity and wood density between conditions of descent of phreatic level. Although the theoretical hydraulic efciency is high under descent of phreatic level, a lower midday water potential indicates other possible factors that may afect its performance (e.g., microclimate, daily loss of conductivity and a high root resistances). The above is consistent with a higher leaf mass per area of the remaining leaves, but no diferences were observed in stomatal conductance, leaf 13C isotopic composition and predawn water potential between descent condition. While the adjustment of hydraulic architecture traits has a homeostatic efect on P. tamarugo performance, it is necessary to evaluate the limits of its resistance to contribute to its conservation in a context of intervention of its habit, mainly due to demographic growth and non-metallic mining. Keywords Phreatophyte · Water stress · Wood density · Vascular anatomy · Theoretical sapwood-specifc hydraulic conductivity Introduction Communicated by Nardini. Electronic supplementary material The online version of this The Llamara Salt fat (lat − 21.350921° long − 69.657203°) article (https ://doi.org/10.1007/s0046 8-019-01899 -2) contains is a basin located in the Pampa del Tamarugal National supplementary material, which is available to authorized users. Reserve, Atacama Desert, northern Chile. In this environ- * ment, a thorny forest of very low density is located, where Marco Garrido Prosopis tamarugo P. [email protected] is the most abundant plant species. tamarugo is a legume tree endemic to the Atacama Desert, 1 Centro de Estudios de Zonas Áridas, Facultad de Ciencias adapted to the high thermal oscillation and solar radiation Agronómicas, Universidad de Chile, Las Cardas s/n, of the desert (Lehner et al. 2001, Chávez et al. 2013). The Coquimbo, Chile 2 species is considered a strict phreatophyte that performs Departamento de Producción Agrícola, Facultad de Ciencias hydraulic lifting from the groundwater to the surface soil Agronómicas, Universidad de Chile, Casilla 1004, Santiago, Chile through pivoting roots, also exhibiting a superfcial fascicu- late system that develops in a condition of high soil salin- 3 Facultad de Ciencias Forestales y de la Conservación de la Naturaleza, Universidad de Chile, Casilla 1004, Santiago, ity (Sudzuki 1969; Aravena and Acevedo 1985). Given the Chile absence of rainfall in its environment (Hacke et al. 2006), Vol.:(0123456789)1 3 90 Trees (2020) 34:89–99 the Llamara aquifer is the only signifcant source of water patterns of intra-specifc hydraulic architecture depending for the species. The extraction of water for use in mining has on the availability of water, and even less under the same generated a large area of descent of phreatic level, diminish- meteorological conditions (Zolfaghar et al. 2015). ing the water availability for P. tamarugo, a key factor in the Addington et al. (2006) observed that Pinus palustris performance of the plants and one of the main sources of in a xeric habitat was shorter, had lower HV and a higher variation of traits associated with its function and structure root area: foliar area ratio than in a mesic habitat. These (Maherali et al. 2004; Lambers et al. 2008). adjustments have homeostatic efects that allow P. palustris In the medium and long term, tree functional homeo- to maintain similar stomatal conductance in diferent envi- stasis would be determined by adjustments of its hydraulic ronments. Martínez-Vilalta et al. (2009) observed in Pinus architecture (HA), i.e., the hydraulic design that infuences sylvestris a negative association between environmental the movement of water from roots to leaves, and therefore aridity and leaf area:sapwood area ratio, and a positive cor- defnes the amount of water, which can be provided to the relation with leaf-specifc hydraulic conductivity although canopy (Cruiziat et al. 2002; Cosme et al. 2017). Among the trees exhibited foliage shedding; however, no P50 difer- components of the HA are listed the maximum hydraulic ences were observed in branches. In phreatophytes, Zolfa- conductivity, hydraulic vulnerability (P 50), tissue capaci- ghar et al. (2015) observed that Eucalyptus trees subject to tance, tree height (H) and Huber Value (HV; sapwood to deeper phreatic level have lower P50 in branches and higher leaf area ratio) (Sperry et al. 1988; Tyree and Ewers 1991; HV. However, they did not observe diferences in branch Cruiziat et al. 2002; Meinzer et al. 2009; Jupa et al. 2016). sapwood-specifc hydraulic conductivity or wood density. A In addition, other functional traits have been considered similar trend was observed in Banksia attenuata and B. men- by its integrative character, such as leaf mass per area and ziesii, facultative phreatophytes that, growing in upper dunes wood density (Cosme et al. 2017). A high leaf mass per with greater aridity, developed a vascular tissue more toler- area is associated with low water potential at leaf turgor ant to embolism than trees established in the more humid loss point (Bucci et al. 2004; Johnson et al. 2018) and water lower part (Canham et al. 2009). In P. tamarugo, it has been potential at 50% loss of leaf hydraulic conductance (John- observed that in a condition of descent of phreatic level, son et al. 2018), while wood density is a complex trait that there are shorter trees (Garrido et al. 2018), lower radial could integrate mechanical and hydraulic properties of tis- stem growth (Decuyper et al. 2016), drought induced leaf sue, e.g., vessel implosion tolerance and capacitance (Hacke shedding (Chávez et al. 2013) and increased leaf mass per et al. 2001; Bucci et al. 2004; Zanne et al. 2010). Although area (Garrido et al. 2018), which gives evidence of adapta- denser wood can be associated with narrow vessels and a tion. However, the degree of adaptation of other HA traits low vessels density that result in a low volume of lumen and their infuence on the performance of P. tamarugo under (Preston et al. 2006), fbers fraction must be considered prolonged descent of phreatic level remain unknown. because its thick cell walls contributing to wood density In this study, traits associated with the hydraulic architec- (Fortunel et al. 2013), and ultimately the variation in tis- ture of P. tamarugo at the vascular tissue, organ and whole sue composition as being the primary determinant of wood tree level were evaluated with the aim to know the species’ density (Poorter et al. 2010; Zanne et al. 2010; Zanne and plasticity after 12 years of exposure to severe descent of Falster 2010). water table. Our working hypothesis is that in a condition The inter-specific variability of the HA has been of descent of phreatic level, P. tamarugo adjusts its HA by evaluated in several biomes, observing a hydraulic ef- increasing its hydraulic safety in relation to a control con- ciency–safety trade-of, i.e., a trade-of between water trans- dition, with homeostatic efects on the performance of P. port capacity and tolerance to low water potential (Tyree tamarugo in the Llamara Salt Flat, Atacama Desert. et al. 1994; Sperry et al. 2008; Maherali et al. 2004). At a xylematic tissue level, this trade-of is shown through an inter-specifc positive association between sapwood-specifc Materials and methods hydraulic conductivity and P 50 (Maherali et al. 2004). There- fore, the decrease in water transport efciency imposed by Study site, experimental setup and sampling the environment is compensated by increasing the hydraulic safety of the system (lower P50, Sperry et al. 2008). This is The study was carried out during the summer season achieved by investing in xylem vessels of smaller diameter 2017–2018 in the Llamara Salt Flat located in the Ata- (Sperry and Saliendra 1994; Meinzer et al. 2009) associated cama Desert, northern Chile (Fig. 1; lat − 21.350921° long with higher wood density (Hacke et al. 2001; Bucci et al. − 69.657203°). In this area, there is an arborescent shrub 2004; Fortunel et al. 2013). Although HA plasticity consti- forest consisting of P. tamarugo (< 10% coverage) and tutes a key acclimation mechanism to drought (Tyree and Caesalpinia aphylla (< 25% coverage). Llamara Salt Flat Ewers 1991), there are few studies that evaluate response has a tropical hyper-arid bioclimate (Leubert and Pliscof 1 3 Trees (2020) 34:89–99 91 was closest to the pumping well. The second group called No_DPL was a control group located 4 km in a linear transect (Fig. 1c). In the study area, there are two observation wells used to monitor the current depth of phreatic level from the begin- ning of groundwater pumping to the date (Fig.

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