Plant Soil (2010) 330:447–464 DOI 10.1007/s11104-009-0218-4

REGULAR ARTICLE

Phenotypic plasticity of the coarse root system of flexuosa, a phreatophyte , in the Monte Desert (Argentina)

Aranzazú Guevara & Carla Valeria Giordano & Julieta Aranibar & Marcelo Quiroga & Pablo E. Villagra

Received: 22 June 2009 /Accepted: 20 October 2009 /Published online: 24 December 2009 # Springer Science+Business Media B.V. 2009

Abstract Prosopis flexuosa in the Monte Desert the valley. Coarse surface roots of dune trees were grow in dune and inter-dune valleys, where the water highly branched and grew tortuously at 0.56±0.16 m table is located at 6–14 m depth. We asked whether depth before sinking downward near the tree crown, trees in the dunes, which are less likely to access the suggesting an intensive exploitation of the ephemeral, water table, present a coarse surface root architecture deep, and canopy-linked resources. In contrast, trees that might favor the exploration / exploitation of dune from the valley spread their profuse and less branched resources, compensating for water table inaccessibility. surface roots mainly horizontally at 0.26±0.08 m We characterized the architecture of surface roots of depth, several meters outside the crown probably valley and dune trees, together with the soil environ- exploring this resource-rich site. A model for the ment. The dune held 50 % less and deeper gravimetric environmental control of root architecture together soil water (along a 4 m profile), 3-times less organic with potential ecological effects is discussed. matter, 2-times less available phosphorous, and a sharper contrast of ammonium and nitrate concentra- Keywords Water table . Root architecture . tion between canopies and uncovered soil than Root topology . Dunes . Nutrient patches

Responsible Editor: Rafael S. Oliveira.

A. Guevara : C. V. Giordano (*) J. Aranibar Instituto Argentino de Investigaciones en Zonas Áridas Instituto de Ciencias Básicas, Universidad Nacional de (IADIZA), Consejo Nacional de Investigaciones Científicas Cuyo, Ciudad Universitaria, y Técnicas (CCT-Mendoza CONICET), Parque General San Martín, Av. Ruiz Leal s/n, Parque General San Martín, CP (5500) Mendoza, Argentina CP (5500) Mendoza, Argentina e-mail: [email protected]

J. Aranibar : M. Quiroga : P. E. Villagra Instituto Argentino de Investigaciones en Nivología, Glaciología y Ciencias Ambientales (IANIGLA), P. E. Villagra Consejo Nacional de Investigaciones Científicas y Técnicas Facultad de Ciencias Agrarias, (CCT-Mendoza CONICET), Universidad Nacional de Cuyo, Av. Ruiz Leal s/n, Parque General San Martín, Almirante Brown 500, Chacras de Coria, CP (5500) Mendoza, Argentina 5505 Mendoza, Argentina 448 Plant Soil (2010) 330:447–464

Introduction of environmental stimuli that affect primary root growth, lateral root emergence and growth, and root orientation in the soil. Water and nutrient availability “¿Por qué esconden los árboles el esplendor de are strong modulators of root architecture. Water sus raíces?” shortage induces root elongation and suppresses root branching, which could be interpreted as an adapta- Pablo Neruda, El libro de las preguntas (p.1971) tive response to a drying water front. This is accompanied by a reduction in leaf expansion and Woody perennials are characteristic components of an enhancement in the root:shoot ratio (Lambers et al. the vegetation of arid ecosystems (Schenk and 1998; Malamy 2005; De Smet et al. 2006). Nitrate Jackson 2002; Whitford 2002). Their presence in shortage induces lateral root emergence and elonga- deserts might have been evolutionary favored due to tion, and phosphate deficit reduces growth of primary their ability to develop and maintain a perennial root root and induces lateral root emergence and elonga- system that exploits deep water reservoirs that are tion; though in both cases, lateral root proliferation more stable in time than surface water reservoirs could be further increased in nutrient-rich patches (Noy-Meir 1973; Seyfried et al. 2005). Additional (Hermans et al. 2006; Zhang et al. 2007; Pérez-Torres advantages for deep-rooted species in arid ecosystems et al. 2008). include the access to deep pools of nutrients A nutrient-rich patch can induce the local prolifer- (Walvoord et al. 2003; McCulley et al. 2004), and ation of roots by the activation of lateral meristems, a the ability to redistribute water vertically in the soil typical response elicited by nitrate, ammonium and profile through their roots, facilitating water use and phosphate (Drew 1975; Forde and Lorenzo 2001; root longevity during extended periods of drought Casimiro et al. 2003; Hodge 2004). However, the (Richards and Caldwell 1987; Burgess et al. 1998; degree of root proliferation depends on a systemic Ryel et al. 2004). In arid environments, the relative signal produced after nitrogen assimilation that travels ability of the different plant life-forms to effectively from the shoot to the root, informs about the overall acquire the scarcely available and patchily distributed nutritional status of the plant, and interacts with the water and nutrients is a strong determinant of the local signal in the root, probably at the genetic level coexistence and spatial distribution of plant species (Forde and Lorenzo 2001). As a result, root prolifer- (Noy-Meir 1973;Salaetal.1989; Montaña et al. ation into a nutrient hotspot will occur only when a 1995; Schenk and Jackson 2002; Zencich et al. 2002). certain combination of high nutrient concentration in The ability of a root system to forage and acquire relation to the soil matrix and poor plant nutrient status resources relies greatly on its morphology, dimen- occurs. On the other hand, a high nitrate concentration sions, and spatial orientation in the soil, which supplied homogeneously to the root system induces the determine its three-dimensional spatial structure or opposite phenotype, suppression of lateral root prolif- architecture. Root architecture can be described by eration, by the action of the systemic signal that the arrangement of segments within the branching indicates a high nutrient status (Forde and Lorenzo pattern, called topology; and the dimensions (length 2001;Casimiroetal.2003;DeSmetetal.2006). and radius) of segments, and angles between them, or A series of directional stimuli from the environ- its geometry (Fitter 1987). The topology and geom- ment are able to further modify root architecture etry of a root system highly determine its potential through the induction of tropistic responses. Tropistic and efficiency for soil exploration, water and ions responses interact with each other and share common absorption and transport, and costs of construction cellular and molecular pathways, that result in auxin and maintenance (Fitter 1987; Fitter et al. 1991; Fitter redistribution in the root elongation zone, and and Stickland 1991; Berntson 1994; Bouma et al. asymmetrical root growth that enables root curvature 2001), thus enabling the exercise to predict function towards (positive tropism) or against (negative through the study of structure. tropism) a given stimulus (Eapen et al. 2004). Roots Roots are extremely plastic organs, because though display positive gravitropism [growing straight down- their architecture is determined in part by a genetic ward (embryonic roots) or at a certain angle to the component, it is also strongly modulated by a variety gravity vector (lateral roots)] Blancaflor and Masson Plant Soil (2010) 330:447–464 449

2003; Mullen and Hangarter 2003), positive hydrot- soil-resource foraging. We hypothesize that differ- ropism (Eapen et al. 2004;Kiss2007; Kobayashi et ences in the accessibility to groundwater and the al. 2007), negative phototropism to white and blue edaphic environment of valleys and dunes will imprint light (Kiss et al. 2003), and changes in growth architectural characteristics among surface coarse roots direction to the presence of physical barriers or of P. flexuosa trees that would favor the exploitation of mechanical resistance that enables them to circumvent the water and nutrient reservoirs proper of each objects (Kiss 2007). landscape unit. To explore these ideas, we described In the present work we aimed to study the central architectural features in partially root-excavated architecture and phenotypic plasticity of coarse roots adult P. flexuosa trees, accompanied by a stable isotope in phreatophytic trees that access the water table in analysis of xylem sap and characterization of the soil comparison to trees that grow tenths of meters away physical properties, water distribution in the soil profile, from it in an arid ecosystem, and relate root architec- and nutrient concentrations in a valley and a dune. ture to the edaphic environment. We studied Prosopis Previous data about soil water indicated a non- flexuosa D.C. (, Mimosoidae “algarrobo uniform distribution in the soil profile (Jobbágy et al. dulce”) trees from woodlands in the arid extreme of 2008). It is reasonable to suspect a patchy distribution the Central Monte desert (159 mm mean annual of nutrients in the surface, which should be mainly rainfall) in Argentina, an ecosystem with an exogenous located under plant canopies, the “fertility islands”, subsidy of phreatic water from rivers originated in the considering the impact of goat grazing and trampling western Andes (Torres and Zambrano 2000). These in the area (Rossi and Villagra 2003; Noe and Abril woodlands are an important source of wood, fuel and 2008; Abril et al. 2009, Carrera et al. 2009). Keeping food for local inhabitants and for the agricultural this background in mind, we predict that, at the P. irrigated oasis, have been intensively exploited in the flexuosa patch level, the dune and the valley will past, and are at present protected by local law (Alvarez differ in the spatial distribution and magnitude of et al. 2006). P. flexuosa, a tree with a dimorphic root water, and nutrient patches. Overall, water and system (Morello 1958), has the particularity to nutrients in the surface will be lower in the dune than dominate woodlands in valleys where it reaches the in the valley, associated to a lower vegetation cover, water table located at 6–14 m depth, and to sparsely lower tree growth and litter production, and a coarser inhabit the sandy dunes, where the water table is soil texture that favor deep water drainage in the dune distant from the surface and inaccessible to the than in the valley. Under this scenario, three theoret- vegetation (Jobbágy et al. 2008). ical surface root architectures could develop in each The fact that P. flexuosa trees could survive and landscape unit: i) a lower number of surface roots, grow in dunes without tapping the water table is an longer, less branched at higher angles, and located interesting feature to investigate, because it was deeper in the soil profile in trees from the dune than in suggested that in areas with mean annual precipitation trees from the valley, associated to the low availability around 160 mm P. flexuosa trees behave as obligate of rainfall water in the surface and its deep location in phreatophytes, and that they could only grow in dunes the dune; ii) a lower number of surface roots, longer, where the altitude is not an obstacle to reach the water less branched at higher branching angles, but located table (González Loyarte et al. 2000). Morello (1958) shallower in the soil in trees from the dune than in proposed that P. flexuosa communities could not trees from the valley, associated to the lower develop with less than 350 mm of mean annual availability of nutrients in the surface of the dune precipitation without tapping the water table, and that than in the valley; iii) a higher number of surface individual trees could not survive without access to roots, highly branched at lower branching angles, and any deep water reservoir under these conditions. We located shallower in the soil in trees from the dune proposed that this species should display some degree than in trees from the valley, associated to a strong of plasticity in its root system that could explain their response of dune trees to the surface nutrient patch, capacity to grow at long distances from the water driven by a poor tree nutritional status associated to table in the dunes of this extremely arid ecosystem, the low availability of nutrients in the dune. However, and focused on the study of coarse roots, the organs as in natural systems multiple controlling factors act directly involved in large-scale soil exploration and together, the ‘real’ root architecture of P. flexuosa 450 Plant Soil (2010) 330:447–464 trees would probably be a combination of the three season, and that vegetation from the valley access theoretical architectures. This research will provide the phreatic water (Jobbágy et al. 2008; Jobbágy et al, novel information about the coarse root system and under revision). This suggests that P. flexuosa trees in the belowground phenotypic plasticity of P. flexuosa, the dune are less likely to access the water table than and will open leading questions about external and P. flexuosa trees in the valley. internal regulation of root architecture in desert We chose 5 adults P. flexuosa trees in the valley and phreatophytes. five individuals on the SW facing slope (ca. 20°) in the adjacent dune. Individuals were chosen accordingly to the following criteria: they should be single-stemmed, Materials and methods with no woody vegetation under its crown (to facilitate root excavation and minimize root interference), and of Study site similar basal diameter (16.8±3.96 cm), an indicator the tree age in the field (Fig. 1a and b). Tree age was Our study site was located in the Telteca Natural calculated counting the annual growth rings in core Reserve (32° 20′S; 68° 00′W), on the alluvial plain of samples obtained with a gas-powered coring drill Mendoza river at the eastern foothills of the Andes in (TED_262R, Tanaka Kogyo Co. Ltd, Chiba, Japan). Mendoza province, Argentina. The climate is arid, Ages of selected individuals were between 25 years with mean annual precipitation about 155 mm (1972– and 63 years in the dune slope and between 30 years 2007) concentrated in summer. Mean annual temper- and 45 years in the valley. Individuals were also similar ature is 18.5°C with high daily and annual thermal in height (3.75±0.85 m) and crown area (15.79± amplitudes, with absolute maximal and minimal values 6.37 m2). We performed root excavations in late that range from 48°C in summer to −10°C in winter winter, before P. flexuosa sprouting. (Alvarez 2008). An extensive subterranean watershed is recharged in the Andes. Fluvial sediments reworked Water sources used by P. flexuosa trees by winds created an extensive dune system with a NW- SE orientation that alternate with inter-dune valleys. We performed a stable isotope analyses (δ18O and The soils are identified as typical torripsaments δ2H) of P. flexuosa xylem sap, phreatic and surface (Regairaz 2000). The vegetation is part of the Central soil water. In the study area, phreatic and rainfall Monte Desert, and three landscape units that support water had contrasting isotopic values. Groundwater different plant communities are clearly distinguished: has a lower composition of heavy isotopes, (lower dunes, inter-dune valleys, and floodable saline valleys. δ18O and δ2H values) reflecting river water, originat- We limited our research to the dunes and inter-dune ed by winter precipitation fallen in the Andes, 250 km valleys. western of the study site. Local summer rainfall concentrated in summer, showed heavier isotopic Experimental design composition. Local recharge of the water table by rainfall is negligible in the study area (Jobbágy et al. We selected a valley and an adjacent dune of about under revision). The isotopic composition of precip- 20 m height in Puesto La Penca (32° 25′42″S 68°00′ itation and groundwater expressed in the delta 33″ W). We chose this particular site because notation differed by a minimum of 10 and 70 per previous research work by our team demonstrated mil for δ18Oandδ2H respectively, allowing the that i) the water table was located at 7 m depth in the identification of water sources used by the vegetation valley; ii) rainfall water was distributed differently (Jobbágy et al. under revision). within the soil profile in the dune and the valley by We sampled four to six adult P. flexuosa trees from the end of winter: within 1 and at least 5 m depth in each landscape unit in two dates, one at the beginning the dune slope, and from surface to 0.5–1.5 m in the (November) and the other at the end (May) of the interdune valley; iii) isotopic composition analysis of growing season. We collected two to three stems per xylem sap, rainfall and phreatic water revealed that tree, 2–10 mm wide, and immediately sealed them in vegetation from the dune, including adult P. flexuosa 10 ml vials. Phreatic water was sampled at hand-dug trees, use rainfall water throughout the growing wells 6.5 to 7.5 below the surface and in boreholes Plant Soil (2010) 330:447–464 451 Fig. 1 Representative root- excavated P. flexuosa trees ab from the valley (a) and the dune (b). Excavations per- formed at the tree base: tree from the valley (c); tree from the dune (d). Totally excavated roots: in the val- ley (e), roots crossed the soil mainly horizontally and with occasional turns in the horizontal plane; in the dune cd (f) roots took sudden changes in direction in both Surface the horizontal and vertical root Surface planes, even in the up- root growth direction, exactly opposite to the direction of Taproot Taproot gravity, indicated by g. Ob- tuse, recto and acute angles of turns in the excavated Obtuse angle main root axis could also be e f Acute angle observed in the photograph Recto angle

Upgrowth

Downgrowth g

established for the study in November and May, and Surface and tap root number and diameters surface soil water was sampled from dune and valley boreholes sections <1 m depth (in May), and We excavated the root base along the first 1 m depth immediately sealed. Water from soil and plant stems around the tree base, until the tap root was clearly was extracted using an azeotropic distillation proce- observed in its vertical downward direction (Fig. 1c dure (Ehleringer et al. 1991). All water samples were and d). We measured number and diameter of surface analyzed at the Duke University Environmental roots and taproot. When taproot (TR) was bifurcated Stable Isotope Laboratory using a Finnigan MAT we measured both diameters (d) and calculated an Delta Plus XL continuous flow mass spectrometer. equivalent diameter applying the following formula: The isotopic composition of rainfall for the city of X 2 2 Mendoza, 90 km southwestern of our study site, was Equivalent diameter ¼ ðÞTR d obtained from the GNIP database (IAEA/WMO 2006); monthly weighted means (October–May peri- od) from years 1981–1988 and 1998–1999 are Surface root pathway in the soil reported. We measured the lowest and highest depth of Root architecture emergence of surface roots at the tree base in the excavations shown in Fig. 1c and d.Wealso We approximated the surface root system architecture randomly chose two surface roots from each individ- through the measurement of central architectural ual, one from the northern and other from the features in excavated root portions. southern side of the tree, and excavated them totally 452 Plant Soil (2010) 330:447–464 throughout the horizontal pathway of the main axis Transect direction was NE-SW which is coincident (Fig. 1e and f). Some roots took a sudden change in with the dune slope. Final results were an average of direction from horizontal to vertically downward, the three transects. and further downward excavation was hampered by soil collapse. On each excavated root we measured The soil environment depth of emergence at the stem base, maximum depth throughout its pathway and at its tip or longest We defined the soil environment as a set of soil excavated point, number and angles of changes in properties and abiotic factors that comprised the direction on the horizontal and vertical plane, and environment in which roots developed. the length of the excavated root. We calculated the potential radius of influence of surface roots mea- General physical and chemical soil properties suring the lineal distance from the tree base to the root tip or longest excavated point. We also We took soil samples at 0.15–0.30 m depth nearby calculated the ratio between the potential radius of each individual tree at both landscape units, from influence of surface roots and the radius of the tree beneath the tree crown (mixture of northern and crown. southern subsamples) and from exposed soil areas. In them, we measured soil texture by sedimentation Surface root branching according to Bouyucus method (Okalebo et al. 1993), pH and electric conductivity in saturated soil extracts. On the excavated roots we measured the number of Soil texture was also measured in soil samples taken primary branches, their diameter, and the internal with a manual soil auger at intervals of 0.5 m up to angle between the primary branch and the main root 3 m depth. We took soil samples from the exposed (branching angle). soil area at 0.15–0.30 m with minimal disturbance to measure bulk density. Root topology Soil water content We fully excavated two first order branches from each tree at random, bellow the tree crown. We We obtained soil moisture profiles in the dune and in measured magnitude (m) as the number of external the valley up to 5 m depth, at intervals of 0.25 m (first links, and altitude (a) as the single largest external 0.5 m) and 0.5 m with a manual soil auger. Samples path length, and calculated the topological index were homogenized and a sub-sample of 100 g was (TI) as the regression of log a on log m (Fitter et used to determine soil water content gravimetrically, al. 1991;Berntson1995). We then compared the after drying at 100°C. Samples were taken in slope of the calculated regressions to the maximum December, March and May. value of 1 for herringbone-like topology and an We also registered soil moisture continuously with expected value of 0.53 for random branching (Fitter ECH2O probes (10HS, Decagon Devices Inc., Pull- et al. 1991). man, USA) buried at 0.3 m depth adjacent to the northwestern crown edge of a tree from the dune and Floristic composition and vegetation cover the valley, connected to a data logger (Em50, at the experimental site Decagon Devices Inc., Pullman, USA); measurement interval was 1 h. Probes were soil specific calibrated, We determined the floristic composition and vegeta- in order to improve measurements accuracy. We filled tion cover of the dune and the valley because of the 4 l containers with air dried soil packed at approxi- control that vegetation exerts on water and nutrient mate field bulk density and wetted it with 300 ml dynamics in the soil. We applied the point-quadrat water sequentially until saturation. We constructed method (Passera et al. 1983), by three 50 m transects calibration curves by combining ECH2O probe read- systematically distributed in each landscape unit ings with the average volumetric water content of the trying to cover the entire experimental site; 100 soil they were buried in, according to users’ guide points (50 cm apart) per transect were sampled. instructions. Plant Soil (2010) 330:447–464 453

Concentration and spatial distribution of organic roots, two per tree, were averaged to obtain a single matter and nutrients representative value per experimental unit. To evaluate the relationship between certain architectural parameters At the beginning of the growing season, surface soil and tree age and dimensions, we performed linear samples (0–10 cm depth) were collected in different regression analyses between the parameter and tree microsites in the dune and the valley (n=3 under P. basal diameter. Differences in root parameters and flexuosa and n=5 in areas between tree- cano- vegetation cover due to landscape unit location were pies at each landscape unit) for soil organic matter tested by a two-tailed t-test for independent samples. and available phosphorus (P) analyses. Exposed areas When data presented non homogeneous variances we were defined as soils not covered by woody vegeta- used a Welch’s approximate test (Sokal and Rohlf tion (trees or ), but they could be covered by 1995). When necessary, outliers values were removed grasses. Additional soil samples were collected at four after Grubb`s outlier test (Burke 1999). Topological different times during the growing season for mineral Index was calculated with linear regression. Differences nitrogen (N) availability analyses. These samples in organic matter and available phosphorus were tested were collected in the most representative patches of by two way ANOVA, considering two factors, the the ecosystem (under Prosopis flexuosa crowns and landscape unit (site) and below the tree crowns and exposed soil areas in both landscape units, under exposed soil areas (microsite). When data presented Bulnesia retama in the valley and under Tricomaria non-homogeneous variances they were ln transformed. usillo, Ximenia americana, and Larrea cuneifolia in We used Infostat statistical package (InfoStat 2008 the dune) in order to have a preliminary description of version, InfoStat group, FCA, Universidad Nacional de the mineral N variability to plan future soil sampling Córdoba, Argentina). A lowess (locally weighted strategies. Sampling sizes for mineral N determination scatter plot smoothing) curve was fit to the mineral N varied during the sampling period and in different data with R (R Foundation for Statistical Computing, microsites, totaling 88 samples. These samples were Vienna, Austria). sieved (2 mm mesh), extracted with a two normal potassium chloride solution (2 N KCl) immediately after return from the field (20 g of soils in 60 ml of Results 2 M KCl), and frozen until chemical analyses. Soil subsamples were weighted and dried at 100°C to Water sources accessible to P. flexuosa roots determine gravimetric soil moisture. Soil samples for organic matter and available P determinations were Surface soil water (<1 m depth) and phreatic water dried at 60°C and sieved (2 mm mesh) before the showed contrasting isotope values with a difference of analysis. Nitrate and ammonium concentrations were 10‰ to 17‰ for δ18O and 60‰ to 140‰ for δ2H determined by spectrophotometric determinations of (Fig. 2). Phreatic water demonstrated a lighter isotope the soil KCl extracts. Nitrate was determined with composition than surface soil water, associated to its the spongy cadmium method (Jones, 1984), and origin from winter precipitation in the Andes that ammonium with the phenol-hypochlorite method contrasts with surface soil water origin, derived from (Weatherburn 1967). Available soil phosphate was local spring-summer-autumn rains (Fig. 2). Monthly determined in soil extracts (4 g of soils in 10 ml of weighted means of the isotopic composition of

0,5M NaHCO3) and spectrophotometric determination precipitations at Mendoza city from October to May, after reaction with ammonium molybdate (Okalebo et although located 90 Km western to the study site, al. 1993). Organic matter was analyzed by the wet presented isotopic signatures similar to those of the oxidation, Walkley-Black method (Nelson and surface soil water and distant to those of phreatic Sommers 1982). water (Fig. 2). P. flexuosa trees from the valley showed a degree of isotopic values that ranged from Statistical analysis those similar to surface water to those similar to groundwater, suggesting that, although deep rooted We considered each tree as an experimental unit. and capable of using groundwater, they may as well Parameters measured in totally excavated surface use surface soil water mixing the isotope signature of 454 Plant Soil (2010) 330:447–464

18 d O ‰ dune, three of the five excavated trees presented a -20 -15 -10 -5 0 5 50 bifurcated taproot; in both landscape units mean diameter of tap roots did not differed (Table 1). 0

-50 Surface root pathway in the soil H ‰ 2

d -100 The range of emergence depths of surface roots from -150 the root base did not differ between trees of both -200 landscape units, and ranged from 0 m to 0.6 m on P. f. dune (May) Phreatic water (May) average (Table 2). However, during their pathway, Phreatic water (Nov) P. f. dune (Nov) roots from dune trees reached higher depths (around P. f. valley (May) Soil water dune (May) P. f. valley (Nov) Soil water valley (May) 0.56 m) than roots from valley trees (around 0.26 m), Ppt. Mendoza (Oct-May) and 70% of them turned suddenly downward, forming angles near 90° (Table 2). Throughout their way, roots Fig. 2 Natural abundances of hydrogen and oxygen stable from dune trees turned frequently both in the isotopes in phreatic water, surface soil water (<1 m depth) and horizontal and vertical planes in obtuse and acute xylem sap of P. flexuosa trees from the valley and the dune in the study site (Telteca reserve), and in precipitation at Mendoza angles (Fig. 1f), while roots from the valley trees city (monthly weighted means), obtained from GNIP isotope remained less tortuous, with occasional turns in database. Symbol references and sampling months are indicated obtuse angles (Table 2). On average, roots from the in the figure for clarity. Mean isotopic values from precipita- dune trees performed four times and near seven times tions in November and May are circled. The global meteoric water line is indicated more changes in direction in the horizontal and vertical planes respectively than valley trees. In neither of the turning points of excavated roots did both sources. In contrast, dune trees presented heavy we find any physical obstacle, like soil compaction or isotopic values similar to surface soil water in all cases. the presence of a plant. The length of the excavated Although there is some overlap between isotopic roots before the reach of the root tip or their sudden signatures of valley and dune trees, only valley trees change in downward direction tended to be higher in had delta values so similar to groundwater, while dune the valley trees (8.36 m) than in the dune trees trees seemed to use mainly surface soil water derived (5.15 m), though the difference was not statistically from local precipitation. significant (Table 2). The short and tortuous horizon- tal pathway of surface roots from dune trees resulted Coarse root architecture in a shorter potential surface root radius of influence when compared to valley trees (Table 2). When Surface and taproot number and diameter related to the tree crown radius, the horizontal radius of influence of surface roots was around 3.5 fold Number and diameters of surface roots were not correlated with tree basal diameter (r2=0.003, P= 2 0.879; r =0.27, P=0.879 respectively), so we used Table 1 Root number and diameters (d) of surface roots (SR) the absolute values of these parameters for compar- and taproot (TR) in P. flexuosa trees from the valley and the isons. The mean number of surface roots from valley dune slope. Values are means with ± 1 s. e. m. between trees nearly doubled the mean number of surface roots brackets. P-values from two tail t-tests are reported from dune trees, though the high variability in the Valley Dune P-value number of surface roots among trees from the valley (that ranged from 18 to 63) and from the dune (that Number of SR 29.20 (19.02) 15.40 (7.30) 0.17 ranged from 5 to 25) prevented us to find any Mean diameter of SR 2.40 (0.78) 2.37 (0.69) 0.96 statistically significant difference in this variable (cm) Number of TR 1 1.6 (0.55) nd (Table 1). Mean diameter of surface roots did not Diameter of TR (cm) 6.80 (0.72) 10.23 (4.37) 0.15 differed between landscape units. In the valley all the excavated trees had a single taproot, while in the nd not determined Plant Soil (2010) 330:447–464 455 higher than crown radius in valley trees and 1.7 in Root topology dune trees (Table 2). Neither length nor potential radius of influence were correlated with the tree basal Linear regressions of Log altitude on Log magnitude diameter (r2=0.002 P=0.8984; r2=0.0003 P=0.959 for an entirely excavated primary branch rendered respectively). topological indexes (TI) of 0.87 for valley trees (r2= 0.79, P=0.002) and 0.86 for dune trees (r2=0.93, P= Surface root branching 0.017). The average TI=0.86 value was higher than the expected value for random branching, TI=0.53, Primary branches comprised a wide range of diameters, and approximated the value for herringbone-like from <0.5 cm to 3.5 cm in both landscape units branching, TI=1. (Fig. 3a). When divided in diameter classes at intervals of 0.5 cm, primary branches <0.5 cm predominated Floristic composition and vegetation cover (Fig. 3a). The total number of primary branches per at the experimental site unit meter of main root did not differ statistically in trees from both landscape units, though a tendency Cover of woody species and trees was higher in the towards a higher degree of branching in dune trees was valley than in the dune (P=0.017 and P=0.0003 evident (Fig. 3b). This tendency became significant respectively). In the valley the dominant species was when primary branches wider than 0.5 cm were the tree Prosopis flexuosa. An herbaceous cover considered (Figs. 3c and d). First coarse branching predominated in the dune, with the grass Panicum point (>0.5 cm) occurred nearer the tree base in trees urvilleanum as dominant species. Only a few species from the dune (0.36±0.31 m) than in trees from the were shared in common in both landscape units valley (1.04±0.59 m), P=0.05. (Table 3). Branching angles between the main excavated root and first order branches smaller than 45º were more The soil environment represented in dune trees (15 %) than in valley trees (5 %) (Fig. 4). The same pattern was observed when General physical and chemical soil properties branching angles equal to 45° were considered (Fig. 4). An opposite pattern was observed with Soils nearby the root-excavated trees from the dune angles wider than 45°, as they were more represented and the valley presented differences in soil texture in valley trees (71 %) than in dune trees (29 %) within the first 30 cm: soil was sandy in the dune (Fig. 4). (97.4% to 99% sand) and sandy (90.4% and 85.4%

Table 2 Pathway in the soil of surface roots of P. flexuosa trees from the valley and the dune. Values are means with ± 1 s.e.m. between brackets. P-values from two tail t-tests are reported

Valley Dune P-value

Range of emergence depth at root base (m) 0.0–0.59 0.0–0.64 0.74 (0.20) (0.27) Maximum depth during the pathway (m) 0.26 (0.08) 0.56 (0.16) 0.01 Number of changes in direction (horizontal plane) 2.9 (0.96) 11.8 (6.32) 0.04 Number of changes in direction (vertical plane) 1.8 (1.35) 12.1 (6.49) 0.03 Angles of turns in the horizontal plane 100% obtuse 80% obtuse nd 20% acute Percentage of roots that sink vertically downward into the soil 40% 70% nd Root length up to the longest excavated point (m) 8.36 (2.75) 5.15 (0.68) 0.06 Potential radius of influence (m) 7.15 (2.72) 3.69 (0.38) 0.05 Surface root radius: Tree crown radius 3.50 (1.45) 1.70 (0.47) 0.03 nd not determined 456 Plant Soil (2010) 330:447–464 Fig. 3 (a) Frequency distri- 1.0 -1 16 bution of diameter classes of a 14 P=0.07 b first order branches in both 0.8 valley (grey bars) and dune 12 (white bars) trees. 0.6 10 (b) Number of total first 8 order branches per meter of main surface root, (c) num- 0.4 6 ber of branches coarser than 4 0.2

0.5 cm and (d) coarser than Relative frecuency 2 1 cm. Bars are means ± 1 s. e. m.; P- values from the 0.0 Total primary branches m 0 ≥ 0.5 0.5-1 1-1.5 1.5-2 2-2.5 2.5-3 3-3.5 two-tailed t-test are Valley Dune indicated in each graphic Branch diameter class (cm) -1 -1 2.0 4 c d P=0.05 P=0.009 3 1.5

2 1.0

1 0.5

0 0.0 Primary branches > 1 cm m Primary branches > 0.5 cm m Valley Dune Valley Dune sand) or loamy sand (78.4% to 84.9% sand) in the Soil water content valley; in both cases sand was the major soil component (Table 4). Differences in soil texture Soil water content profiles in exposed soil areas from disappeared at greater depths, and were sandy in both the surface up to 5 m depth revealed differences in the landscape units (Table 4). Soil in the valley had total amount of water, vertical distribution, and slightly more electric conductivity than in the dune temporal dynamics between the valley and the dune (although neither of them was saline), and a slightly (Fig. 5a and b). In each measured date (December, but significantly lower bulk density than soil from the March and May), the valley presented an overall dune (Table 4). pH was alkaline and similar in both higher amount of water than the dune (Fig. 5a). In the landscape units (Table 4). valley, a deep reservoir of soil water that extended from 1 m to 5 m depth and peaked around 4 m was evident in December and March; this reservoir disappeared towards May (Fig. 5a). In the dune, a 1.0 deep water reservoir that extended from 1.5 m to 4 m 0.8 depth that was absent in December was evident in 0.6 March, and persisted in May (Fig. 5b). Continuous soil water monitoring by soil moisture 0.4 sensors buried at 0.3 m depth (average depth of 0.2 surface coarse roots) next to P. flexuosa trees from the dune and the valley, indicated differences in the Cumulative relative frecuency 0 10 20 30 40 50 60 70 80 90 45 amount and dynamics of surface water between both Branching angle (degrees) landscape units (Fig. 6). Surface soil moisture in the valley (2.6–4.8% w/w) was higher than in the dune Fig. 4 Cumulative frequencies of branching angles of primary – branches in valley (closed circles) and dune (open circles) trees. (0 1.8% w/w) throughout the measured period. The Symbols are means ± 1 s. e. m. dynamics of formation and attenuation of soil Plant Soil (2010) 330:447–464 457

Table 3 Floristic composition and vegetation cover in the (site effect, Table 4). Significant differences in micro- valley and the dune, expressed in percentage frequency site concentration of organic matter and phosphate Valley Dune were evident, as the highest concentrations occurred beneath tree crowns in both landscape units (microsite Uncovered soil 46.33 54.67 effect, Table 4). Among all microsites, the organic Vegetation cover 53.67 45.33 matter and phosphate richest patches occurred be- Woody vegetation cover 46.67 26.33 neath the crowns of valley trees, and exposed soil Tree cover 35.67 4.00 areas in the dune demonstrated the lowest values of Prosopis flexuosa 26.67 3.00 organic matter. Phosphate concentration in exposed Bulnesia retama 9.00 1.33 soil areas of the valley and the dune and beneath the Shrub cover 15.67 22.33 crowns of dune trees were similar and lower than Lycium tenuispinosum 8.00 beneath the crowns of valley trees (Table 4). Capparis atamisquea 7.67 Mineral N presented a high temporal and spatial 4.33 variability (Fig. 7). Ammonium concentration showed Baccharis retamoides 6.33 the highest variability, with extremely high values Trichomaria usillo 12.33 under plant canopies from the valley (Fig. 7a). This Ximenia americana 0.67 microsite also presented the highest values of nitrate Herbaceous vegetation cover 10.67 22.00 concentrations (Fig. 7b). On the contrary, exposed Grasses areas in the dune showed the lowest concentration of Sporobolus rigens 6.67 both, ammonium and nitrate. If the percentage of soil Bouteloua aristidoides 1.67 not covered with woody vegetation (representing the Aristida adcencionis 1.00 exposed area samples) in the dune and the valley are Setaria leucopila 0.67 considered (54 % in the valley and 74 % in the dune, Trichloris crinita 0.67 calculated from Table 3), the overall mineral N Panicum urvilleanum 16.67 availability was clearly lower in the dune than in the valley. Aristida mendocina 4.00 Setaria mendocina 0.67 Bouteloua aristidoides 0.67 Discussion

The determination of architectural parameters in moisture peaks associated to rain events (indicated by portions of the root system of adult P. flexuosa trees arrows in Fig. 6) let us compare the time of soil let us compose a picture of some central features of its hydration and drying at both landscape units, that architecture. We found that adult P. flexuosa trees should be the net result of water infiltration, evapo- demonstrated a high degree of phenotypic plasticity in ration, drainage and plant absorption. Considering the its root system when growing in different landscape highest peak associated to the major rain event of units, with different access to the water table and January 11th (the wider arrow in Fig. 6), soil wetted at under different soil environments. Distinctive root − − a velocity of 0.27% d 1 in the valley and 0.31% d 1 in architecture patterns could be summarized as follows: − the dune, and dried at a velocity of 0.057% d 1 in the valley trees maintained a relatively high amount of − valley and 0.071% d 1 in the dune, suggesting a surface roots, that spread extensively and horizontally longer duration of soil water at a given point in the several meters away from the tree base with a low valley than in the dune. frequency of primary branching and high branching angles (>45°) (Fig. 8). Oppositely, dune trees pre- Concentration and spatial distribution of organic sented a low number of surface roots, that grew matter and nutrients tortuously and penetrated deeply in the soil, sinking vertically few meters from the tree base mostly Organic matter and phosphate presented an overall beneath the tree crown zone of influence, with a high higher concentration in the valley than in the dune frequency of primary branching and low branching 458 Plant Soil (2010) 330:447–464

Table 4 The soil environment at the valley and the dune. Values are means with ± 1 s. e. m. between brackets. P-values from two tail t-tests and the two way-ANOVA (for organic matter and phosphorous) are reported

Valley Dune P-values

EC (μS/cm)1 432 303 nd pH 9.7 9.2 nd Texture (0.15–0.3 m) Loamy sand (3/5) Sandy nd sandy (2/5) nd Texture (0.3–3 m) Sandy Sandy nd Bulk density (g/cm3) 1.47 (0.04) 1.56 (0.01) 0.01 Tree crown Exposed soil Tree crown Exposed soil S2 Ms3 S*Ms Organic matter (%) 1.15 (0.12) 0.67 (0.29) 0.42 (0.06) 0.16 (0.03) <0.0001 0.003 0.38 Phosphorus (μg /g) 14.7 (3.71) 8.86 (1.26) 6.74 (3.09) 4.78 (0.74) 0.0001 0.004 0.10

1 μS/cm = microsiemens per centimeter 2 S= site (valley and dune) 3 Ms= microsite (tree crown and exposed soil) nd= not determined

angles (<45°) (Fig. 8). In trees from the dune the soil depths, in concordance with previous data of taproot presented an early branching point with a Jobbágy et al. (2008). A different pattern of water lateral branch growing downward as well as the dynamics was observed in the valley, where a deep taproot (Table 1). water reservoir present at the beginning of the These root architectures developed in trees grow- growing season (December) disappeared towards the ing at different distances to the water table, with end of the season (May, Fig. 5a), probably due to different possibilities to access it (Fig. 2), and in plant absorption. It’s interesting to note that by the contrasting soil environments proper of each land- end of the growing season (May, following the rains scape unit. The valley could be characterized as a and the maximal vegetation activity) soil water rich-resource and temporary more stable site where profiles of the valley and the dune were quite water content and nutrient concentrations in the opposite: in the valley, water was located within the surface were higher than in the dune (Table 4, Figs. 5, 6, and 7). Water content could be enhanced in the soil surface of the valley by run-off from higher topo- 0 1 2 3 4 5 0 1 2 3 4 5 graphical positions, hydraulic lift by trees connected to the water table, lower direct solar radiation and 100 evaporation in the shadow of the woody vegetation 200 cover (Table 3), and by a higher temporal retention associated with a finer soil texture when compared to 300 the dune (Table 4). In the dune, soil water should be more ephemeral than in the valley, due to a higher Depth (cm) 400 direct solar radiation and evaporation associated with 500 a low woody vegetation cover (Table 3), and a rapid deep drainage in coarse soil textures (Table 4). The water reservoir located from 2 m to 4 m depth that December March May formed in March and persisted in May in the dune (Fig. 5b) suggested a seasonal dynamics dominated Fig. 5 Vertical distribution and temporal dynamics of soil by an amount of rainfall water not absorbed by moisture in exposed soil areas in the valley (a) and the dune during the growing season that percolates to deeper (b). Each symbol represents a single measurement Plant Soil (2010) 330:447–464 459

6 58.4 11.4 15.8 2.4 valley 5 dune

4

3

2

Soil moisture (% w/w) 1

0 0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150 160 170 180 190 Day

Fig. 6 Continuous soil moisture monitoring at 0.3 m depth at the tree crown northwestern edge in the valley (continuous line) and in the dune (dashed line). Days in the abscissa are counted from January 1st to June 15th. Arrows and numbers indicate rain events in mm first 0.5–1.5 m, and in the dune within 1.5– 4m probably overestimates the real N availability to the (Fig. 5a and b). The idea of the valley as a site were plants, given by the shorter water pulses in the dune. water might be retained in the soil for a longer period Some features of the coarse surface root architec- of time than in the dune is also supported by ture of valley trees appeared in concordance with this continuous soil water monitoring (Fig. 6). relatively high-resource site, where surface soil con- The higher concentration of organic matter and ditions (high nutrient concentrations, water availabil- nutrients in the valley than in the dune occurred ity) might promote surface lateral root emergence and beneath the crowns of P. flexuosa trees (organic growth (Drew 1975; Caldwell 1994; Hodge 2004). matter and phosphorous) and representative plant Promotion of fine root density by high nitrate was species from both communities (nitrate and ammoni- reported Prosopis glandulosa seedlings, suggesting um), and in exposed soil areas (Table 4, Fig. 7). This that root production in Prosopis species should should be related to the relatively high woody respond to variations in nutrient concentrations vegetation cover of the valley, the dominance of P. (Jarrell and Virginia 1990). Interestingly, surface roots flexuosa trees (Alvarez et al. 2009), and the accessi- from valley and dune trees followed extremely bility to the water table that should promote P. different pathways into the soil, resulting in a deeper flexuosa and other species growth, leaf and litter penetration in the soil profile in the dune than in the production, and overall valley productivity. Although valley (Table 2,Fig.8). The trade-off between there are not previous reports on the growth rate of P. nutrient foraging in the surface and water foraging flexuosa trees from valleys and dunes in the Monte deep in the soil of the dune seemed to have been Desert, some preliminary data suggest a greater leaf solved in favor to water foraging, probably through expansion in trees from the valley than trees from the the induction of positive hydrotropic responses to dune even during an exceptional rainy year (unpub- increasing soil water potential gradients (Kiss 2007; lished data). In exposed soil areas, low nutrient Kobayashi et al. 2007). There was evidence of production and rapid water drainage should leak adaptation to chronic drought by a related species, mobile nutrients as nitrate, and should be the cause Prosopis glandulosa, through the proliferation of of the extremely low nitrate concentration in exposed large roots (2–10 mm diameter) into deep soil soil in the dune (Fig. 7b). Nitrogen availability to horizons, as observed in a long term experiment with plants follows water dynamics, because microbial adult trees (Ansley et al. 2007). In summary, surface mineralization and nitrification are enhanced by soil root number and location in the soil could be wetting events (D’Odorico et al. 2003; Austin et al. associated to a local control of water and nutrient 2004) and nutrient absorption is facilitated by soil availability and distribution in the soil in both moisture. Then, the generally lower mineral N concen- landscape units, as proposed in predictions i) and ii) tration in the dune found in soil extracts (Fig. 7), in the “Introduction”. 460 Plant Soil (2010) 330:447–464

Fig. 7 Soil ammonium (a) and nitrate (b) concentration measured during the sum- a mer in the dune and the valley, under the canopies of trees and shrubs and in exposed areas. VC = valley under canopies; VE = valley exposed areas; DC = dune under canopies; DE = dune exposed areas. A lowess -1 (locally weighted scatterplot smoothing) curve is shown for each set of data. Each symbol represents a single measurement Ammonium, µg g

b -1 Nitrate, µg g Plant Soil (2010) 330:447–464 461

Fig. 8 Schematic drawing of P. flexuosa coarse root system architecture in the valley and in the dune

Surprisingly, the relative soil resource richness in As a result of differences in the pathway of surface the valley was not accompanied by a higher surface roots into the soil, the potential horizontal radius of root primary branching, as expected in lieu of a local influence of surface roots in valley trees nearly effect of nutrients and water availability. On the doubled that of dune trees (Table 2), while surface contrary, roots from dune trees were more branched roots of dune trees might have a greater impact deep and at lower angles than valley trees (Figs. 3 and 4). in the soil profile. The depletion of soil moisture This could be interpreted as a strategy of local and during the active growing season in the dune about intense exploitation of scarce and ephemeral resour- 1.50 m, suggests root absorption until this depth ces in dune trees mainly located beneath the tree (Fig. 5b). The maximum water absorption in the crown, in contrast to a large scale exploration of valley, based on the soil moisture profiles, seems to higher, more stable and spatially continuous resources occur at 0.5 m (Fig. 5a). This might have various in valley trees. There is a trade-off between the scale ecological effects, both related to the area within of soil exploration and the intensity of exploitation of which negative (competition) and/or positive (facili- a resource patch by roots, as both strategies are tation) plant-plant interactions mediated by roots associated to opposite root architectures and alloca- might occur in each landscape unit (Casper et al. tion patterns of a given pool of biomass that could not 2003; Hartle et al. 2006), and the horizontal and be maximized at the same time: exploration is favored vertical distance within which water and nutrients are by a long main axis with a high diameter, long links absorbed and re-cycled through trees, rendering a and high branching angles, and exploitation is favored differential impact of P. flexuosa in each community by a high specific root density at low cost, associated mediated by differential root architectures. to a highly branched root system, fine diameters and Differences observed in coarse root architecture narrow angles (Fitter 1987, 1994; Spek and Van contrast with the lack of differences in primary branch Noordwijk 1994). It seems possible that an internal topology, which in both landscape units approximated a regulation related to a probable poor nutrient status of herringbone-like topology. Herringbone-like topologies dune P. flexuosa trees (which could be generated by are considered to be favored in species proper of poor- the poor-nutrient availability in the dune) might resourced habitats or under transient conditions of promote a stronger branching response to the local resource scarcity (Fitter et al. 1991; Fitter and Stickland resource patch, as proposed in prediction iii) in the 1991), which coincides with the general characteristics “Introduction” (Forde and Lorenzo 2001). of the Monte desert. The lack of differences in this trait 462 Plant Soil (2010) 330:447–464 despite the differences in microenvironment character- sion to work in Telteca Natural Reserve, and park ranger istics where they grew (below tree crown, Table 4) Silvana Piccone for her logistic assistance and hospitality. We are grateful to Hugo Debandi, Carmen Sartor, Diego Odales, might suggest that topology is a less plastic architectural and Gualberto Zalazar for their collaboration with field work; to character than spatial orientation and branching in this Víctor Hugo Videla and Rafael Bottero for their technical and species. creative support; to Ana Srur, María Alejandra Giantomassi and In summary: Alberto Rippalta for their help with dendrochronological analysis; to Esteban Jobbágy for his unconditional support. 1- P. flexuosa roots demonstrated a great phenotypic We are particularly thankful to Mariano, Chicho, Valeria and doña Cecilia for their candid hospitality. plasticity when growing with different access to This research was supported by Agencia Nacional de the water table and in different soil environments. Promoción Científica y Tecnológica PICT 2007-01222. The coarse surface root architecture of dune trees suggests forage for deep water reservoirs and an intense exploitation of them. 2- Based on the characteristics of the soil environment References in both landscape units and on previous knowledge on resource regulation on root architecture, we Abril A, Villagra PE, Noe L (2009) Spatiotemporal heteroge- propose that two main sets of environmental cues neity of soil fertility in the Central Monte desert (Argentina). J Arid Environ 73:901–906 might exert a strong control on P. flexuosa root Alvarez JA (2008) Bases ecológicas para el manejo sustentable system architecture in dunes and valleys in the del bosque de algarrobos (Prosopis flexuosa D.C.) en el Monte Desert: a) heterogeneity in the amount, noreste de Mendoza. Argentina. 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