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Leaf responses to irrigation of the endemic fog-oasis tree Myrcianthes ferreyrae: Can a fog-specialist benefit from regular watering?

David A. Ramírez Coaguila


*, Luis Balaguer 3, Rosa Mancilla 4, Virginia González 1, Daniel

, Carmelo Talavera 4, Luis Villegas 4, Aldo Ortega 4, Percy Jiménez 4, José

M. Moreno1


Departamento de Ciencias Ambientales, Universidad de Castilla – La Mancha, 45071 Toledo, Spain Departamento de Biología, Universidad Nacional Agraria La Molina, Lima, Perú Departamento de Biología Vegetal I, Universidad Complutense de Madrid, E-28040 Madrid, Spain Laboratorio de Ecología, Departamento Académico de Biología, Universidad de San Agustín, Arequipa, Perú



Departamento de Ecología, Universidad de Alicante, 99-E-03080 Alicante, Spain

* Corresponding author: DavidAntonio.Ramirez@uclm.es, Phone: +34 925 268 800 ext.
5470, fax: +34 925 268 840

Running title: Responses to watering of a fog-oasis tree


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Abstract Myrcianthes ferreyrae is an endemic species with a scarce number of individuals located only in fog-oases (named “lomas”) along the Peruvian Desert in the South of Perú, where fogs are the main source of water in this hyperarid region. After centuries of severe deforestation, reforestation this native species was carried out in the “Atiquipa Lomas” (Arequipa, Perú). In 5 slopes, five 2-year-old seedlings were monthly irrigated with water trapped by raschel-mesh fog collectors that supplemented natural rainfall with 0, 20, 40, 60 and 80 mm month-1 from February to August 2008. Plant growth rate was estimated from the variation of shoot basal diameter and maximum height, and both were highly correlated with total biomass. We measured in 4 leaves of each seedling: leaf mass area (LMA), leaf carbon isotope composition (δ13C), nitrogen per leaf area, leaf total carbon and stomatal density. According with the plant growth response, only the LMA and δ13C were higher in irrigated than control plants but with no further response to increasing water supply. This threshold response suggests an on-off strategy fitted to exploit pulses of fog water availability. The absence of a gradual response, however, is in consonance with the low phenotypic plasticity expected in plants from stressful environments

Key Words: Peruvian Desert, δ13C, fog, leaf mass area, Lomas, Myrcianthes ferreyrae


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Introduction “Lomas” ecosystems are fog-oases into of the Peruvian and Atacama deserts which form an hyperarid belt close to the Pacific Ocean coast from North of Perú to North of Chile (7-28ºS latitude) (Dillon et al., 2009). These deserts are considered as the driest of the planet (Rundel et al., 1991), where Cereceda et al. (2008) using 30 years of meteorological records calculated 0.8 mm of the average yearly precipitation in the Atacama Desert. Similar to other hyperarid areas (Henschel and Seely, 2008) the fog from the ocean is the most important water resource for the “lomas” (Cereceda et al., 1999). Thus, trees intercept the fog with their aerial architecture and throughfall and stemflow percolate into the soil and recharges the groundwater (Dawson, 1998; Edner et al., 2011). Fog collectors (Schemenauer et al., 1987) have been set up and tested in these deserts (Cereceda et al., 2008; Larrain et al., 2002; Schemenauer and Cereceda, 1993; Sotomayor and Jiménez, 2008; Westbeld et al., 2009). The amount of water trapped by these collectors in other hyperarid environments reaches maxima of 1.0, 5.7 and 7.0 mm day-1 reported for the Namib Desert (Henschel and Seely, 2008), the West Coast of South Africa (Olivier, 2002) and the Atacama Desert (Cereceda et al., 2008), respectively.

In the “lomas” ecosystems reforestation activities have been carried out with the aim to restore endemic and economic tree species which have been reduced by old cutting practices (Suasnabar et al., 2004). Unfortunately, there is little information about reforestations using fog water collected (Estrela et al., 2009), and there are no published studies assessing plant response to the irrigation in “lomas” ecosystems. Our study species was Myrcianthes ferreyrae (McVaugh) McVaugh an evergreen perennial tree. This fog-specialist species is endemic of “lomas” formation in the South coast of Perú


LMA. 2009. foliar isotope carbon composition (δ13C) and nitrogen concentration per leaf area (and other leaf traits) were measured in our study species with the aim to assess the response of planted seedlings to different irrigation treatments using fog water. 2011. 2006). Atkinson et al.. Haase et al. Vitousek et al. and to understand the effect of different practices on plant resource use efficiency (Querejeta et al. Ramírez et al.. Arequipa-Perú (Suasnabar et al. Poorter and Garnier.S.. 2006.. 2005). 2008)... Myrcianthes ferreyrae is listed in the official classification of endangered species of wild flora protected by Peruvian legislation (D.g. In afforestation and previous reforestation studies.g.. Leaf mass area (LMA). Zhang et al. 1990) and other stressing factors. The measured traits have been used to assess plant response to water deficit (e.. we 4 . Mendez-Alonzo et al. 2008). Nº 043-2006-AG) into the “critical endangered” classification based on the red list criteria of the International Union for Conservation of Nature (IUCN. Antunez et al.73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 (Kawasaki and Holst. Poorter et al. Because a proportional water use according with fog availability have been reported in fog-specialist species in high water deficit situations (Dawson.. 2001. and presently it is only located in some patches of the Atiquipa and Taimara “lomas”. leaf nitrogen concentration. 1999. 2008. Ruiz-Robleto and Villar.. 2009). 1999. Our goals were: i) to assess the plasticity degree of the different leaf traits and the growth response to a regular water supplementation by irrigation with fog water. 1984) and carboxylation capacity (Hanba et al. Suzuki. 2005. Gratani and Varone. 2001) respectively.. 2004). 1998.. 2007.. 1998). and ii) to infer from the leaf traits responses the functional process driven by regular watering in plant growth. 1999). These leaf traits are related to plant growth (e.g. water use efficiency (Farquhar and Richards. Wright et al. and δ13C have been analysed to select the adequate species on a functional group basis (Delagrange et al. altitudinal gradients or changes in temperature (e.

5.6 mm year1 (Sotomayor and Jiménez. The fog from the Pacific Ocean. 2008).98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 hypothesize a gradual improvement of the physiological status (indicated by leaf traits and growth) in response to increasing water inputs. 1). 2008). The soil shows sandy clay loam structure (51. The prominent woody perennial species in the Atiquipa “lomas” are: Caesalpinia spinosa.0 mm which is distributed in 21 and 72% in the “wet-cool” (July-November. Arequipa (Fig. The perennial shrub and tree species play an important functional role in the water input of this ecosystem because serve as natural fog collectors.62 mS/cm of electric conductivity (Coaguila.0ºC of average monthly temperature) seasons respectively. with 15. The yearly average rainfall is 54. Our second hypothesis is that the leaf traits could reflect the interaction of other external factors like light intensity with our irrigation treatments allowing us a better understanding of plant growth response to water inputs. 15% of C/N. silt and clay respectively). 5.4ºC of average monthly temperature) and “dry-hot” (January-May. which occurs in the “wet-cool” season. with 21.3 pH and 0. 74°18’W) belonging to the Peruvian Desert in the Caraveli province. 26. can provide an additional water input of 57.8% of organic matter. Duranta armata. Alternanthera ferreyrae and Grindelia tarapacana. Citharexylum flexuosum and Vasconsellea candicans (Coaguila 2008).2. Materials and Methods Study area Our experiment was carried out in the restoration area of the Atiqupa “lomas” located in the Peruvian south coast (15°42’S. Only 34 5 .8 and 22% of sand. Vegetation is mainly dominated by annual species that growth in the “wet-cool” season such as Nicotiana paniculata.

ferreyrae.122 123 124 125 126 127 128 129 130 131 132 133 134 135 136 137 138 139 140 141 142 143 144 145 146 adults individuals of Myrcianthes ferreyrae have been reported into the Atiquipa “lomas” (Vizcarra. Four irrigation treatments (20. 2006).irecaunsa.100 (1) where X is the seedling maximum height or basal stem diameter. 1994) supported by two woody 5-m height beans. Each fog collector is a low-cost 48 m2 flat panel (12 m long x 4 m height) compounds by a polypropylene raschel mesh (Schemenauer and Cereceda. The growth was assessed from the percentage of variation from the first measurement (Δ) as: ΔX = [(XAugust.com/unsapadova. Twelve seedlings of contrasted size were removed. canalizes the collected water to a pipe that transport it to a four water reservoirs with 60. A gutter. 40.XFebruary)/XFebruary ] . located the low part of the flat panel. 300.html). The watering was carried out manually at the beginning of the assessed months from February-August 2008. 60. 80 mm month-1) and one control (no watering) were established randomly in 5 seedlings per treatment in the 5 referred slopes. 600 y 1000 m3 of capacity. Other pipes system transported the water from the reservoirs to 5 slopes with a plantation of 2-years old M. Growth assessment The maximum height and basal stem diameter of each seedling was measured at the beginning and the end of the study period. Irrigation treatments with fog water and experimental design Twelve fog collectors were set-upped in different projects research activities carried out in the restoration zone of our study area (http://www. dried and weighted separating the above and below biomass with the aim to fit calibration functions among the seedling maximum height 6 .

Leica Microsystems GmbH.01 mg of resolution) of a beaker with water of known mass after completely immerse the re-hydrated leaf. Germany) assessing the stomatal number in 4 images (located in the central part of the leaf) in 100x field (0. The epidermis of the leaf abaxial side was impressed in a dental resin (3M ESPE Dental Products.58 mm2) per leaf. In the lab the leaves were scanned and the leaf area (A) was measured using ImageJ software (1. USA). Germany) connected to a digital camera system (Leica DC 300F model. Thus.41o version. Following the proposal of Poorter et al. a layer of nail polish was spilt in the impressed leaf size and carefully removed when it was dried. Wetzlar. Maryland. National Institutes of Health. Wetzlar. Leaf traits In August 2008 we collected 4 leaves of similar size and belonging to the same cohort located in the middle of the each seedling.147 148 149 150 151 152 153 154 155 156 157 158 159 160 161 162 163 164 165 166 167 168 169 170 171 and stem basal diameter versus dry total biomass (aboveground + belowground biomass). (2009) we calculated the leaf volume per area (LVA=V/A) as a surrogate of the leaf thickness. after that it was located in a slide cover and analyzed in a inverted microscope (Leica DM IRB model. Leica Microsystems GmbH.’s (2000) protocol. which involves measuring the weight gain (in a balance with 0. USA) with the aim to measure the stomatal density (SD) following the Geisler et al. The leaf mass area (LMA) and the leaf density (LD) were calculated as: LMA = DM/A (2) 7 . (2008) based on the Archimedes principle. The leaves were re-hydrated for 2 days in deionized water at 10ºC and after that we estimated the leaf volume (V) using the same procedure of Mitchell et al. To estimate foliar dry mass (DM) the leaves were dried per 2-days at 70ºC and weighted.

1000 where R is 13 (4) C/12C proportion of the leaf sample and the Pee Dee Belemnite (as standard) and was determined by a continuous flow isotope ratio mass spectrometry (Europe Scientific Hydra 20/20. UK). LMA and DM vs. δ13C. leaf carbon concentration. Cheshire. LMA. Statistical analyses The measured variables were assessed using one-way randomized block ANOVAs testing irrigation treatments and slopes as blocks. foliar C and Narea were measured from 4 leaves collected per individual in a total of 75 seedlings (3 individuals x 5 treatments x 5 slopes). The association among LMA. Narea was analysed using a principal component analysis (PCA). IL. Results Growth response 8 . USA) to run the aforementioned analysis. Chicago. SD. Foliar N and C were determined with an automated 1500 Carbo Erba elemental analyzer.0 version software for Windows (SPSS.172 173 174 175 176 177 178 179 180 181 182 183 184 185 186 187 188 189 190 191 192 193 194 195 196 LD = DM/V (3) The dry leaves were ground using a mill ball and sent at Stable Isotope Facility of the Autonoma de Madrid University where the leaf carbon isotope composition (δ13C) was analyzed as: δ13C (‰) = [(RSample/RStandard) -1] . The nitrogen content per unit area (Narea) was calculated as total foliar N divided per A. We used SPSS 17. δ13C. Linear regressions analyses were carried out between LVA vs. A correlation analyses (Spearman correlation index) was carried out to assess the relationship of the variables with the extracted principal components.

05). The ANOVA analysis also detected significant differences among irrigation treatments in stomatal density (SD) and leaf carbon concentration (%C) (see Table 1 and 2). SD (ranged between 198.8.0 and -23.3 g m-2) and leaf carbon isotope composition (δ13C. Plants in the control treatment showed significant lower values of Δ Diam and Δ Height than those submitted to the other watering treatments (Fig.61).5x-37.3x-24. r2=0. p<0.5 and 53. Significant differences among watering treatments were detected in the variation of the stem basal diameter (Δ Diam) and seedling maximum height (Δ Height) from the first assessment (Table 1). r2=0. Differences between blocks were not significant only in δ13C and Narea which reflects the spatial variability at the restoration site (Table 1). ranged between -27. ranged between 105. 9 . while the %C (ranged between 40.4%) was only different between the control and maximum irrigation treatment (Table 2). No significant differences were found in the nitrogen content per unit area (Narea. Thus.4 stomata mm-2) in the 80 mm month-1 treatment was lower than the other irrigation treatments. 2 and Table 2).8 and 360.95.08) (Fig. The block effect was not significant in Δ Diam and Δ Height (Table 1).01) than with the seedling maximum height (y=1.7‰) were lower in the control than the other irrigation treatments (Table 1 and Fig. Leaf traits responses to irrigation treatments The leaf mass area (LMA.197 198 199 200 201 202 203 204 205 206 207 208 209 210 211 212 213 214 215 216 217 218 219 220 221 Stem basal diameter showed a stronger relationship with the aboveground + belowground biomass (y=7. nor in the irrigation factor (Table 1 and 2).50 g N m-2).76.7 and 352. p<0. 2).20 and 0.7. ranged between 0. 3). while no relationship was found between the former and leaf density (r2=0. The LMA was explained by the leaf volume per area (r2=0.

Discussion Seedlings of M. Narea plots were far away of the averages belonging to other the irrigation treatments (Fig. The averages of the control (nowatering) in LMA vs..222 223 224 225 226 227 228 229 230 231 232 233 234 235 236 237 238 239 240 241 242 243 244 245 246 Relationship among leaf traits The three component extracted by PCA explained 76. The component 3 was highly positively correlated with %C (r Spearman = 0. while the SD and Narea were negatively and positively correlated with component 2 (r Spearman = -0. 1996) in turn enhanced by a slow return of biomass investment into de “leaf economics spectrum” (Wright et al. in disagreement with our first hypothesis. A high proximity or/and association between LMA and δ13C was found in the multivariate space established by the three extracted components (Fig. 4). A lower phenotypic plasticity is expected in poor or less favourable environments in specialized plants (Lortie and Aarssen. LMA and δ13C with the water input (Fig. but rather was asymptotic. 2).77 and -0. Our results suggest that the water use in our fogspecialist species could be limited by a low phenotypic plasticity (in according with Lortie and Aarssen. 1996). ferreyrae significantly increased their growth. 5). Growth response to the irrigation The different irrigation treatments tested in this work tried to simulate water gains from fog intercepted by trees and that reach the understory and soil via stemflow and 10 .67 respectively).7% of the total variance (Table 3). However. The component 1 was highly correlated in negative way with LMA and δ13C (r Spearman = -0.70 respectively).80) (Table 3). 2004) typical of sclerophyllous species with high LMA. Narea and δ13C vs. this response was not gradual. depending on amount of water.71 and 0.

our irrigation treatments tried to simulate situations with different tree cover without shading effect. representing the minimum water quantity to improve the regeneration niche in this habitats. thus for example in the redwood forest (Sequoia sempervirens) in California the fog water dripped from the vegetation was ranged from 22 to 46 mm year-1 which correspond to 13-45% of its annual transpiration (Dawson.. 2007). The lack of correspondence of growth according with the water increments tested by each watering treatments (Fig. 2a) could reflects a threshold (20 mm month-1) beyond which water increments does not causes a significant growth rise. Because the seedlings are not able to intercept important quantities of fog water.. 2004). 1998). (Niinemets et al. ii) this threshold could provide some reliability to drive the growth of individuals belonging to the “seedling bank” where the lowgrowth seedlings are waiting for the conditions improvement (Antos et al. Because a high LMA is characteristic of slow-growth species (Poorter and Garnier. 2007. Larger trees with a high number of leaves and branches are able to intercept higher fog volumes and could allow a greater water inputs to the vegetation below them. 2009). However. M. 2005). which is considered as the bottleneck for successful species establishment (Poorter.. in our study area 96 mm day-1 has been collected as maximum bellow to Caesalpinia spinosa tree (Villegas et al. ferreyrae shows a high LMA values (210 g m-2 of global average) which is coherent with the more sclerophyll Australian shrubs (66–313 g m-2.247 248 249 250 251 252 253 254 255 256 257 258 259 260 261 262 263 264 265 266 267 268 269 270 271 throughfall.. We hypothesize two implications of the growth asymptotic response to water input in the restoration of this species: i) this threshold value (or close values) could be crucial in the regeneration phase of this specie. Wright et al. it is possible that we might have required a longer time of assessment to detect growth differences driven by our watering treatments. On 11 . unpublished data). For example. this value is close to the reported by Schemenauer and Cereceda (1994) below a Olea europaea tree (70 mm day-1).

. Fig.. allow a more efficient use of incident light as well as a higher capacity to safely dissipate excess photon energy. 5). 2008). 3) which indicates that the leaves belonging to individuals submitted to the irrigation treatments could have been more exposed to the solar radiation. components and its response to the irrigation treatments LVA and LD are components of LMA whose contributions become more important under different environmental situations (Lambers et al. 12 . 2009).. Our measured leaf traits and their components support the hypothesis that light-processing efficiency is more important than structural components synthesis drove by water inputs. More studies are required to understand the root growth dynamic and its response to water inputs in these fog-oases ecosystems. LVA has more weight in environments with higher irradiance (Poorter et al. In our study. Narea has been related to micro-environments with high irradiance to optimize the canopy photosynthesis (Hirose and Werger. LMA. LD explained 61% of the LMA variability (Fig. due to the fact that in dryland species the root biomass is often higher than shoot biomass (high values of root biomass/shoot biomass index. in our study individuals submitted to the watering treatments trended to have higher values of this variable (without statistical significance) than control plants (Table 2. in turn. 2003). Thus also. we can not exclude that our different irrigation treatments may have had a differential effect in the belowground biomass. 2008) resulting in a thicker mesophyll that may. Under full sun exposure.272 273 274 275 276 277 278 279 280 281 282 283 284 285 286 287 288 289 290 291 292 293 294 295 296 the other hand. Larcher. 1987). (2008) work who suggested that in conditions of high light availability the symplast per area fraction is bigger than structural fraction in leaves of evergreen shade-tolerant species. This last is in agreement with Lusk et al. a larger parenchyma is developed (Onoda et al.

2) highlights the coherence in the leaf structure and photosynthetic (CO 2 diffusion and carboxilation) responses to water levels in fog-oases arid environments. Hanba et al..... Nobuhito and Katsuya. 2c). we hypothesize that in the former a high Rubisco activity could decrease the discrimination against the heavy carbon isotope and the δ13C rise. SD trends to drop when the water conditions rise (Yang et al. Paula and Pausas.. 2008). Zhang et al.. The high association of LMA and δ13C (Fig. because the SD was significantly lower in the greater irrigation treatment.. 2004. Yang et al. Lamont et al. 1997. 1990. 2009). Small gm driven by a ticker mesophyll (Vitousek et al. 2008) and the others assessed leaf traits prevent us to relate this 13 . The lack of correlation of SD with δ13C (a useful variable to explain the stomatal formation. SD had been positively related to WUE (Xu and Zhou. 2009 but see Laureti et al. 4 and Table 3) and their correspondence with plant growth in our study species (Fig. 1999) and carboxilation (Wright et al. Niinemets et al. 5b). 2008.297 298 299 300 301 302 303 304 305 306 307 308 309 310 311 312 313 314 315 316 317 318 319 320 321 Possible functional mechanisms driven by the irrigation with fog water A positive correlation between LMA and δ13C has been found in inter-specific studies (Hoffmann et al. 2002). In our study we found that watered plants trend to show higher Narea and δ13C than control plants (Fig. 2007) we can’t to state that the WUE is increased by our watering treatments (Fig. 2006) where the comparisons were carried out with contrasted leaf types.. 2008. we results confirm the first aforementioned pattern only in conditions of a high water inputs. Furthermore. 2004). Thus also. 2005. Xu et al. Because in tick-leaved species (with high LMA like our study species) there is an important decoupling between δ13C and water-use efficiency (WUE) (Marshall et al. LMA affects gm and consequently chloroplastic carbon and δ13C (Seibt et al.. 2002... 2001). 2006) or under extreme drought (Xu and Zhou.... Narea has been related to higher Rubisco content (Hanba et al.. 1999) could cause a rise of chloroplastic carbon demand and subsequently δ13C increment (Lamont et al.

2007. 2008). improves its growth and morfo-functional traits in response to water pulses from fog water. however this response is not gradual according with regular water inputs possibly caused by a low phenotypic plasticity typical of stressed environments. However. 2008). all these aspects require specific experiments that help us to understand the functional process drove by the water input by fog. all these could allow the processing of more quantity photons and higher Rubisco activity with a subsequent plant growth rise. 14 . vital source for the maintaining of this fog-oasis into the Peruvian and Atacama Deserts. ii) the relationship between SD and gas exchange is yet poorly known in plants (Xu and Zhou. this quantity will allow to save water or use this for the reclamations of more trees species. Due to the consistent response of LMA and δ13C with plant growth to the irrigation with fog water. our work highlights the use of these variables in the assessment of the reclamation of endemic species (in our study Myrcianthes ferreyrae) in the “Lomas” ecosystems. We hypothesize that rise of the water input in the seedlings drive the arrangement of more irradiated leaves (possibly by more horizontal leaf angles) with a thicker mesophyll and higher content of nitrogen per area. an endemic and specialist species of fog-oasis ecosystems. In practical terms we recommend a moderate water quantity (20 mm month-1) collected from fog to irrigate 2-year seedlings of Myrcianthes ferreyrae..322 323 324 325 326 327 328 329 330 331 332 333 334 335 336 337 338 339 340 341 342 343 344 345 346 variable with process involved in the gas exchange and carboxilation and consequently with WUE. Conclusions Myrcianthes ferreyre. We think that the leaf gas exchange assessments in future studies in our study species could be very useful for two main reasons: i) there is an uncoupling between δ13C and WUE especially in sclerophyll species (Marshall et al. Seibt et al..

UCLM.D. The authors are very grateful with the community of Atiquipa who help them to setup the experiment and were closely involved in the restoration activities. Fenol for allowing us to carry out the analysis in the facilities of the Plant Physiology Area . Delgado to teach us the dental impression technique for the stomatal density assessment and to M. 15 .C. We thank to M. y suelo aledaño en ecosistemas de desierto húmedo al sur de Perú” funded by General Foundation of the Castilla-La Mancha University (UCLM). L. S2009/AMB-1783).B.347 348 349 350 351 352 353 354 355 356 357 358 359 360 361 Acknowledgements The financial support of this study was provided by the projects: “Seguimiento adaptativo de la restauración ecológica del bosque de nieblas de las Lomas de Atiquipa” (SEGARNIEBLA) funded by BBVA Foundation. and “Elaboración de una propuesta para el estudio de la demanda y uso de agua de plantones nativos reforestados. was funded by the Madrid Regional Govt. (project REMEDINAL-2.

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s.05 22 . 20. 1.4 n.s. F-values of one-way randomized block ANOVA testing irrigation treatments (control.5 * 6. stomatal density (SD). 40.s. 3. Blocks 1. ** p<0.01. * p<0.4 n. 6. leaf carbon isotope composition (δ13C).540 541 542 543 544 545 546 547 Irrigation Treatments Δ Diam Δ Height LMA δ13C SD %C Narea 548 549 6. leaf mass area (LMA).6 ** 2.s. 80 mm month-1) in five blocks (slopes) in: variation of the stem basal diameter and seedling maximum height from the first assessment (Δ Diam and Δ Height respectively ).6 * 0.5 ** 0.3 ** 2. 60. p>0.2 * 5. leaf carbon concentration (%C) and nitrogen content per unit area (Narea).0 ** 2.s. n.3 n.6 ** 3.05.s.4 ** 8. Table 1.4 n.4 n.

8  0.0 b 238.5  0.9  0.3 3.8  0.2 a a a 80 19.2 3.3 a 45.4 ab ab ab 3. Different letters mean significant differences detected by post-hoc Tukey test of the one-way ANOVA (see Table 1) at p<0.6  8.8 a a a 46.2  0.0  3.8 a 2.550 551 552 553 554 555 556 Table 2.2  2.4 46.7  0.3 a 260.2 a Treatments (mm/month) 20 40 60 12. leaf carbon concentration (%C) and nitrogen content per unit area (Narea) grouped per each irrigation treatment.0  4.0 b b b 260.2 a 23 .5 b 3.7  3. Δ Height SD (stomata mm-2) %C Narea (g N m-2) 557 558 559 560 561 562 563 564 565 566 567 568 569 Control 5.9  0.Mean ( standard error) value of the variation of the seedling height from the first assessment (Δ Height).7 271.9  0.9 265.0 15.5 46.1  7.7  6.3  0.5  0.3  5.4 b 47. stomatal density (SD).05.5  2.0 14.6  3.

Spearman correlation index among the extracted components using multivariate principal components analysis (PCA) and foliar variables.12 0.7 δ13C -0.05 respectively.01 and p<0. LMA= leaf mass area. SD = stomatal density. Narea= nitrogen content per unit area.35** 0. Comp. 2 Comp.51** LMA -0. ** and * mean significant values at p<0. δ13C= leaf carbon isotope composition.30* 0.26 -0.90 76.70** Eigenvalue Cumulative Variance (%) 577 578 579 580 581 582 583 584 585 586 587 588 589 590 591 592 593 594 595 596 597 1.41** Narea -0.570 571 572 573 574 575 576 Table 3. In grey the main correlations with /r Spearman/> 0.23 58. %C= leaf carbon concentration.6. 1 Comp.67** -0.30* 0.77** %C 0.16 0.30 1.80** 0.70 34.71** -0. 3 SD 0.30* 0.7 * 0.1 24 ..

25 . Figure 3. Ordination of the leaf variables in a 3D space from the three principal components extracted in the PCA. (c) leaf carbon isotope composition (δ13C). Relationship among leaf mass area (LMA) and its components: leaf density (LD) and leaf volume per area (LVA ~ thickness).598 599 600 601 602 603 604 605 606 607 608 609 610 611 612 613 614 615 616 617 618 619 620 621 622 623 624 625 626 Figure Captions Figure 1. Relationship among leaf mass area (LMA) and leaf carbon isotope composition (δ13C) versus nitrogen content per unit area (Narea) averaged for control plants and individuals subject to each of the irrigation treatments tested (circled values). (b) leaf mass area (LMA). Figure 5. Figure 4. Leaf traits and plant growth response to the irrigation treatments: (a) variation of the basal diameter from the first assessment (Δ Diam).05) detected by the post-hoc Tukey test of the ANOVA. For specification of PCA and abbreviation of the variables see Table 3. Error bars represent SE. * means significant differences (at p<0. Error bars represent SE. Study area map Figure 2.

627 628 629 630 631 632 633 634 Figure 1 75 73 71 14 Lima Caraveli Lomas de Atiquipa 18 P A C AREQUIPA Arequipa IF IC OC EA N 0 30 km 635 636 637 26 .

638 639 640 Figure 2 641 642 643 644 645 646 647 648 649 650 651 Figure 3 27 .

652 653 654 655 656 657 658 28 .

659 660 661 662 Figure 4 663 664 665 666 667 668 669 670 671 672 673 674 675 676 677 678 679 680 681 682 683 684 685 686 687 688 689 29 .

690 691 692 693 694 Figure 5 695 696 697 698 699 700 701 702 703 704 705 706 707 30 .

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