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Journal of Arid Environments 102 (2014) 82e88

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Variations in leaf respiration and photosynthesis ratio in response to air temperature and water availability among Mediterranean evergreen species Rosangela Catoni*, Loretta Gratani Department of Environmental Biology, Sapienza University of Roma, P.le A. Moro 5, 00185 Rome, Italy

a r t i c l e i n f o

a b s t r a c t

Article history: Received 24 April 2013 Received in revised form 23 October 2013 Accepted 28 November 2013 Available online

Net photosynthesis (PN) and leaf respiration (RL) of the evergreen species co-occurring in the Mediterranean maquis in response to water availability and air temperature variations were analyzed. The results underlined that the ratio RL/PN of the considered species ranged from 0.15  0.08 (in winter) to 1.32  0.80 (in summer). Variations of RL and PN during the year were attested by the PCA which was carried out using leaf physiological and morphological traits of the considered species. In particular, Cistus incanus having the highest mean yearly PN and RL rates and low leaf mass area (LMA) and leaf tissue density (LTD), was furthest from the other species emphasizing its drought semi-deciduous habitus, the highest photosynthetic capability in favorable conditions (spring), but low tolerance to drought. Erica multiflora and Rosmarinus officinalis were characterized by the highest LMA and LTD, low PN rates in drought and the lowest PN ones in spring. Erica arborea, Pistacia lentiscus, Phillyrea latifolia and Quercus ilex had the highest drought tolerance. Arbutus unedo and Smilax aspera were close to this group despite lower RL rates during the year. The xeromorphic leaves of the considered evergreen species (i.e. high LMA and LTD) favor carbon gain profits over transpiration losses during drought, nevertheless, the high construction cost of these leaf type justifies the relatively high RL rates. Ó 2013 Elsevier Ltd. All rights reserved.

Keywords: Leaf respiration Mediterranean evergreen species Net photosynthesis Ratio RL/PN

1. Introduction Photosynthesis and respiration are the most fundamental plant physiological processes which affect carbon cycle on a scale ranging from the leaf to the globe (Cavaleri et al., 2008). Approximately 30e 80% of daily carbon (C) assimilated by photosynthesis is respired back into the atmosphere with 50e70% of whole plant respiration taking place in leaves (Atkin et al., 2007) whereas roots respiration releases back into the atmosphere from 8 to 52% of the carbon dioxide (CO2) assimilated (Lambers et al., 1996). Plant respiration plays a critical role in determining global CO2 concentration because it releases approximately 60 Gt C yr1 into the atmosphere (Schimel, 1995) (i.e. up to 65% of the total CO2 released into the atmosphere from terrestrial ecosystems). Respiration and photosynthesis are strongly coupled and interdependent in leaves of higher plants; whereas respiration relies on photosynthetic substrates, photosynthesis is dependent on respiration for carbon skeletons, ATP required for sucrose synthesis and repair of photosynthetic proteins (Atkin et al., 2007). Respiration is essential for

* Corresponding author. Tel./fax: þ39 06 49913449. E-mail address: [email protected] (R. Catoni). 0140-1963/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jaridenv.2013.11.013

growth and maintenance of plant tissues and plays an important role in C balance of the individual cell, whole plant, ecosystem and global carbon cycle (Gonzalez-Meler et al., 2009). Moreover, leaf respiration protects the photosynthetic apparatus from photoinhibitory damage by oxidizing excess photosynthetic and reducing equivalents (Noguchi and Yoshida, 2008). Despite the global importance of plant respiration, fundamental questions regarding the underlying mechanisms governing respiration rates from the cell to whole-plant level remain (Gonzalez-Meler et al., 2009). Photosynthesis and respiration respond independently and often differently to environmental variations (Turnbull et al., 2001). The temperature sensitivity of photosynthesis differs from that of respiration, and hence the ratio between the two processes may be altered following a short-term change in temperature (Loveys et al., 2002). The temperature sensitivity of respiration is referred to Q10 (i.e. the proportional increase in respiration rate for every 10  C rise in temperature). Q10 varies among species, tissue types and physiological conditions (Atkin et al., 2005) ranging from 1.4 to 4 (Turnbull et al., 2001). However, respiration may increase less markedly, remain unchanged or decrease in response to long-term temperature increase (i.e. respiration thermally acclimate). While, the optimum temperature for photosynthesis in C3 plants rarely exceeds 30  C (Atkinson et al., 2010) at temperatures above the

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optimum, photosynthesis often decreases sharply (Ow et al., 2008). At low temperatures (5e10  C) there is a rapid inhibition of photosynthesis due to the inhibit sucrose synthesis (Strand et al., 1999) leading to an accumulation of phosphorylated intermediates and a decrease of ATP/ADP ratio (Hurry et al., 2000). Plants of tropical or sub-tropical origin may incur irreversible damage to photosynthesis by temperatures around 10  C whereas plants from cooler climates may photosynthesize and develop at temperatures around 0  C (Öquist, 1983). Under water stress conditions, photosynthesis may decrease up to 100% becoming totally impaired, and the decrease is mostly mediated by stomatal closure (Gratani and Varone, 2004a). Drought stress is recognized to be one of the most important limiting factors in Mediterranean evergreen species carbon gain (Galmès et al., 2007; Gratani and Varone, 2004a). The overall effects of drought stress on leaf carbon balance depend on the extent to which photosynthesis versus respiration is affected (Atkin and Macherel, 2009). Leaf respiration increasing in drought provides several positive roles since mitochondrial respiration enables survival and rapid recovery of productivity from water-stress conditions (Atkin and Macherel, 2009). Inhibition of leaf respiration under drought was observed in mature leaves of crops and herbaceous species (Haupt-Herting et al., 2001) while high leaf respiration rates were observed in drought stressed shrubs species (Catoni et al., 2013; Gratani et al., 2008). High demand for respiratory ATP under severe water stress seems to be necessary to compensate for the lower ATP production in the chloroplasts to support photosynthesis repair mechanisms (Atkin and Macherel, 2009) whereas no alterations in leaf respiration under drought are mostly reported in some evergreens perennials (Galmés et al., 2007). The ratio respiration/photosynthesis (R/PN) can be considered as a simple approach to leaf carbon balance because it indicates the percentage of photosynthate that is respired (Chu et al., 2011; Loveys et al., 2002). R/PN is indicative of the capacity of plants to produce new biomass for growing and reproductive structures (Cavaleri et al., 2008) giving an indication of the efficiency of plant carbon use (Loveys et al., 2002). On a global scale, Mediterranean-type ecosystems cover 2.5  106 km2 (Allard et al., 2008). This biome is highly represented in southern Europe, particularly in southern France (21,860 km2), Spain (92,000 km2) and Italy (15,700 km2). Mediterranean ecosystems are especially sensitive to climate change because they have large topographic complexity with disparate land uses as well as marked water availability gradients (Lavorel et al., 1998). Among Mediterranean ecosystems, the Mediterranean maquis is largely distributed in areas around the Mediterranean Basin. Its structure is strongly influenced by air temperature and water availability (Gratani et al., 2003, 2012). It is dominated by sclerophyllous species, drought semi-deciduous species, narrow-leaves species and lianas (Gratani et al., 2003, 2012). Mediterranean ecosystems are quite vulnerable to rising temperatures and reduced water availability. In particular, in the Mediterranean Basin, rainfall has declined by 20% during the 20th century, mainly during summer accompanied by more frequent and intense heat-waves (Allard et al., 2008) and a maximum air temperature increase of about 5.1  C by the end of the 21st century (IPCC, 2007). The hypothesized increase of temperature may lead to severe land degradation and finally to desertification causing an overall reduction in plant biomass and the loss of many Mediterranean native species (Rotondi et al., 2003). The main object of this research was to analyze variations in the ratio R/PN of the species co-occurring in the Mediterranean maquis in response to water availability and air temperature during the year. Variations of the ratio R/PN might imply change in Mediterranean species structure and productivity in the long term (Saxe et al., 2001) by causing changes in species presence and, in turn,

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in vegetation. Improving knowledge on processes and factors influencing carbon balance is important in making accurate models of CO2 exchange between vegetation and the atmosphere (Armstrong et al., 2006). Moreover, taking into account that respiration of terrestrial ecosystems is a major flux in the global carbon cycle and a potentially important positive feedback mechanism for climate change (Schimel, 1995), data on the response of the ratio R/PN to environmental changes is an important aspect for predicting future global atmospheric CO2 concentration. 2. Material and methods 2.1. Study area and plant species The study was carried out in the Mediterranean maquis developing along the Latium coast from Fiumicino to Capocotta (Italy 4140ʹN, 12 23ʹE) in the period January 2012eDecember 2012. The maquis under study was characterized by the presence of the following species: Arbutus unedo L., Phillyrea latifolia L., Pistacia lentiscus L., Quercus ilex L. (typical sclerophyllous species), Cistus incanus L. (drought semi-deciduous species), Erica arborea L., Erica multiflora L., Rosmarinus officinalis L. (narrow-leaves species), and Smilax aspera L. (liana) (Gratani et al., 2003). The climate of the area was of the Mediterranean type: the mean minimum air temperature (Tmin) of the coldest months (Januarye February) was 4.2  0.1  C (mean value SD), the mean maximum air temperature (Tmax) of the hottest months (JulyeAugust) was 30.7  0.2  C, and the mean yearly air temperature (Tm) was 16.2  6.2  C. Total annual rainfall was 753 mm, most of it occurring in autumn and winter. Drought was from June to August (total rainfall of 42 mm for the period). During the study period, Tmin of the coldest month (February) was 1.1  2.1  C, Tmax of the hottest month (August) was 33.2  2.4  C, and total rainfall in drought (from the middle of June to the middle of August) was 10 mm. (Data from Lazio Regional Agency for Development and Agricultural Innovation for the years 2004e2012). During the study period, gas exchange measurements were carried out periodically (three days with the same weather conditions in the first week of the month) on three representative shrubs per each of the considered species. 2.2. Gas exchange Gas exchange measurements were carried out using the infrared gas analyzer (ADC LCA4, UK) equipped with a conifer leaf chamber (PLC, Parkinson Leaf Chamber) for E. arborea, E. multiflora and R. officinalis, and with a broad leaf chamber (PLC, Parkinson Leaf Chamber) for Q. ilex, A. unedo, C. incanus, P. latifolia, P. lentiscus and S. aspera. Measurements were taken on fully expanded sun leaves (n ¼ 5 on each sampling occasion for A. unedo, C. incanus, P. latifolia, P. lentiscus, Q. ilex, and S. aspera) and on sun apical shoots (n ¼ 5 on each sampling occasion for E. arborea, E. multiflora and R. officinalis). Net photosynthesis (PN, mmol CO2 m2 s1), stomatal conductance (gs, mol m2 s1), leaf transpiration (E, mmol m2 s1), leaf temperature (Tl,  C) and photosynthetically active radiation (PAR, mmol photons m2 s1) were measured from 9.00 to 11.00 a.m., under natural conditions on cloudefree days (PAR  1000 mmol m2 s1, saturating level) to ensure that nearmaximum daily photosynthetic rates were measured (Reich et al., 1999). Leaf dark respiration (RL) measurements were carried out contemporary to net photosynthesis measurements, by darkening the leaf chamber with a black paper, according to Zarogoza-Castells et al. (2008), for 30 min prior to each measurement to avoid transient post-illumination bursts of CO2 releasing. The ratio RL/PN was

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calculated according to Chu et al. (2011) and Zaragoza-Castells et al. (2008). 3. Statistical analysis All statistical tests were performed using a statistical software package (Statistica, Statsoft, USA). Differences of the means for the considered traits were tested by one-way ANOVA and Tukey test for multiple comparisons. The relationship between PN and Tl (photosynthetic thermal window, sensu Larcher, 1994) was used to calculate leaf temperature (Tl 100%) which favored the highest PN rates, and leaf temperature (Tl 50%) which decreased PN below or above half of its maximum. The considered physiological traits were analyzed by PCA (principal component analysis) on the basis of a matrix of the normalized data. In particular, among the physiological traits, PN and RL during the favorable period (AprileMay), in drought (August), winter (February) and autumn (September) were considered. This analysis was conducted using also data from Bombelli (2001) and Gratani and Varone (2004b) for leaf mass area (LMA) and leaf tissue density thickness (LTD). A multiple regression analysis was calculated to investigate the influence of PN, mean monthly air temperature (Tm) and monthly total rainfall (Rm) on RL, using RL as the dependent variable, and PN, Tm and Rm as independent variables, according to Chu et al. (2011) and Turnbull et al. (2005). 4. Results 4.1. Seasonal variations of leaf carbon balance Gas exchange measurements and the ratio RL/PN during the study period for all the considered species are shown in Figs. 1e3. All the considered species reached the highest PN rates in spring (AprileMay) when Tm was 16.0  2.1  C. Among them, C. incanus showed the highest rates (20.0  0.6 mmol m2 s1) and E. multiflora and R. officinalis the lowest ones (7.4  0.4 mmol m2 s1, mean value). gs showed the same PN trend with the highest rates in AprileMay (0.126  0.054 mol m2 s1, mean value of the considered species), C. incanus having the highest gs rates (0.244  0.049 mol m2 s1) and R. officinalis the lowest one

(0.076  0.003 mol m2 s1). RL increased from February to Aprile May (2.45  0.67 mmol m2 s1, mean value), C. incanus having the highest rates (3.80  0.14 mmol m2 s1) and A. unedo the lowest one (1.58  0.11 mmol m2 s1). The ratio RL/PN ratio was 0.24  0.08 (mean value of the considered species) R. officinalis and E. multiflora having the highest ratio (0.36  0.05, mean value) and A. unedo the lowest ones (0.13  0.03). In summer (June, July, August), PN of the considered species decreased, on an average, by 56% compared to the spring maximum, decreasing by 73% in August when Tmax was 33.2  0.4  C, and total rainfall was 3.3 mm. In particular, C. incanus, E. multiflora, R. officinalis and S. aspera showed the highest decrease (85%, mean value) and P. latifolia the lowest one (57%). gs decreased by 76% (mean value of the considered species) S. aspera having the highest decrease (89%) and E. arborea the lowest one (51%). In this season RL of the considered species was 2.98  0.72 mmol m2 s1, mean value, with C. incanus having the highest rates (4.20  0.40 mmol m2 s1) and S. aspera the lowest ones (1.80  0.18 mmol m2 s1). The ratio RL/PN was 1.32  0.80 (mean value of the considered species) E. multiflora and R. officinalis having the highest ratio (2.47  0.63, mean value) and A. unedo the lowest one (0.49  0.05). In autumn (September, October, November), particularly in September, after the first rainfall (177 mm) following drought, on an average, PN of the considered species recovered by 69% of the spring maximum. In particular, Q. ilex and P. latifolia show the highest PN rates (84% of the spring maximum) and S. aspera the lowest one (48% of the spring maximum). In the same period, A. unedo had the highest gs rates (0.154  0.010 mol m2 s1) and S. aspera the lowest ones (0.020  0.003 mol m2 s1). In September, RL decreased, on an average, by 32% than the measured value in August, C. incanus having the highest rates (2.92  0.27 mmol m2 s1) and A. unedo the lowest ones (1.19  0.07 mmol m2 s1). The ratio RL/PN was 0.28  0.09 (mean value of the considered species) and it ranged from 0.13  0.01 in A. unedo to 0.43  0.11 in R. officinalis. In winter (December, January and February) PN, gs and RL of the considered species, on an average, decreased respect to the spring maximum, reaching the lowest rates in February (Tmin ¼ 1.1  2.1  C). In particular, PN was 8.2  1.1 mmol m2 s1 in Q. ilex and 3.5  0.1 mmol m2 s1 (mean value) in E. multiflora and

Fig. 1. Trend of the net photosynthetic rates (PN) during the study period for the considered species. Each point is the mean value of three sampling days per months (n ¼ 27). Mean values (SD) are shown.

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Fig. 2. Trend of leaf dark respiration (RL) during the study period for the considered species. Each point is the mean value of three sampling days per months (n ¼ 27). Mean values (SD) are shown.

R. officinalis. gs decreased by 53% in February, Q. ilex showing the highest rates (0.085  0.003 mol m2 s1) and R. officinalis the lowest ones (0.035  0.002 mol m2 s1). In this period RL showed the lowest yearly rates (0.76  0.42 mmol m2 s1, mean value of the considered species) C. incanus having the highest rates (1.70  0.18 mmol m2 s1) and A. unedo the lowest one (0.30  0.18 mmol m2 s1). The RL/PN ratio was 0.15  0.08 (mean value of the considered species) E. arborea and E. multiflora having the highest ratio (0.25  0.01) and A. unedo the lowest one (0.04  0.01).

when Tl was in the range 21.4e25.1  C. PN dropped below half of the maximum rates when Tl was over 33.3  C and under 13.0  C for C. incanus, E. multiflora, R. officinalis and S. aspera, and over 36.2  C and under 10.8  C for A. unedo, E. arborea, P. latifolia, P. lentiscus and Q. ilex. Multiple regression analysis showed that mean air temperature (Tm) was the most significant (p < 0.01) variable explaining RL variations in the considered species. The resulting regression equation was: RL ¼ 0.0847 þ 0.0838 PN þ 0.0883 Tm (r2 ¼ 0.50; n ¼ 108; p < 0.05).

5. Statistical analysis

5.1. Principal component analysis

The results of the regression analysis showed a significant (p < 0.01) correlation between PN and Tl for all the considered species; in particular, the highest PN rates (100%) were monitored

The PCA highlighted that the first two principal components accounted for 73% of the total variance (Fig. 4). In particular, the first component explained 45% of the total variance and it was

Fig. 3. The ratio leaf respiration and net photosynthesis (RL/PN) during spring, summer, autumn and winter. Means (S.D.) of four sampling days in each month (n ¼ 27). Mean values with the same letters, in the same season, are not significantly different (ANOVA, p > 0.05).

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Fig. 4. Principal Component Analysis (PCA) carried out using physiological traits (PN and RL) measured in spring, summer, autumn and winter and leaf morphological (LMA and LTD) traits. Component 1, accounting for 45% of the total variance, was significant related to PN and RL during spring and autumn and RL in summer and in winter. Component 2, accounting for 28% of the total variance, was significantly related to LMA and LTD.

correlated to PN and RL in spring (r ¼ 0.85 and 0.86, respectively), PN and RL in autumn (r ¼ 0.77 and r ¼ 0.77, respectively), RL in winter (r ¼ 0.72) and RL in summer (r ¼ 0.81). The second component explained 28% of the total variance and it was correlated to LMA (r ¼ 0.70) and LTD (r ¼ 0.82). Along the first component, C. incanus showed the highest values and S. aspera the lowest ones, while E. multiflora, E. arborea, R. officinalis, Q. ilex, P. latifolia and P. lentiscus were in the middle. A. unedo was closer to S. aspera. Along the second component, E. multiflora and R. officinalis had the highest values and A. unedo the lowest ones, C. incanus, P. latifolia, P. lentiscus, E. arborea and Q. ilex were in the middle, while S. aspera was closer to A. unedo. 6. Discussion Shrub communities are distributed in semi-arid ecosystems, including the Mediterranean Basin (Caravaca et al., 2003). In the Mediterranean Basin, plants are characterized by a high diversity of growth forms, habits and phenology that enable them to survive under high temperatures and prolonged summer drought conditions (Galmés et al., 2007). High leaf consistency, leaf tissue density, leaf thickness, and reduced leaf area improve drought resistance by decreasing photochemical damages to the photosynthetic apparatus (Gratani and Ghia, 2002). Fonseca et al. (2000) underline a general tendency for species inhabiting arid and semi-arid regions to have high-LMA leaves associated to low photosynthetic rates (Reich et al., 1999) and high LMA values occurring at the expense of low photosynthetic potential (Peña-Rojas et al., 2005). On the whole, the results show that the ratio RL/PN of the considered species varies from 0.15  0.08 (in winter), 0.26  0.03 (in autumn and spring, mean value) to 1.32  0.80 (in summer) and it is indicative of the different sensitivity of both RL and PN to water availability and air temperature variation during the year. The results of the multiple regression analysis show that air temperature has the largest impact on the ratio RL/PN. In particular, in spring, when air temperature is favorable (in the range14.5e17.5  C) and water is available (125 mm, total rainfall in AprileMay), the RL/PN

ratio is indicative of a lower proportion of carbon respired compared to that assimilated and it reflects plant potential productivity (Poorter and Bongers, 2006). In this period, the relatively high RL rates provide energy for producing new leaves and maintenance of the oldest ones (Gratani et al., 2008). Nevertheless, some differences are evident among the considered species. E. multiflora and R. officinalis show the highest RL/PN ratio (0.36  0.05, mean value) which is the result of the relatively high RL rates and the lowest PN rates. This latter may be justified by the high LMA (25.9  3.2 and 20.2  3.4 mg cm2, respectively) and LTD values (756  69 and 582  73 mg cm3, respectively). C. incanus (the drought semi-deciduous species), P. latifolia, P. lentiscus and Q. ilex (the typical sclerophyllous species) and E. arborea (the narrowleaves species) have a lower RL/PN ratio (0.22  0.02, mean value) that is determined by high RL and PN rates confirming the high photosynthetic efficiency in favorable conditions. In particular, the highest PN and RL rates of C. incanus are typical for pioneer species (Chazdon et al., 1996) emphasizing its role in the first reconstruction stages of the Mediterranean maquis after fire (Gratani and Amadori, 1991). Moreover, the highest RL rates of C. incanus are related to the loss of most of its leaves (winter leaves) in springbeginning of summer, thus demanding more respiratory activity necessary to produce new leaves (summer leaves), which are characterized by a reduced LA and a higher LMA than winter leaves (Catoni et al., 2012; Gratani et al., 2008). S. aspera shows a similar C. incanus RL/PN ratio (0.17  0.03) which is determined by high PN rates associated to low RL rates. This latter can be related to S. aspera shade-tolerance (Sack et al., 2003). In fact, plants adapted to low light environments have lower carbon losses via RL than those not adapted, as underlined by Lusk and Reich (2000). A. unedo has the lowest RL/PN ratio (0.13  0.03) among the considered species that is due to high PN rates resulting from a larger light-capture area deployed per mass (Gratani and Ghia, 2002) which underline the photosynthetic efficiency in favorable conditions. The highest RL/PN ratio of the considered species in summer is determined by the highest RL rates (18% higher than the spring rates) and a 73% decrease of PN rates from the maximum, being

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indicative of a higher proportion of the carbon respired for the mobilization of the stored material in response to plant requirements for maintenance in drought (Butler and Lansberg, 1981). Variations in drought resistance among the co-occurring species are also related to differences in root depth. In particular, the short E. multiflora and R. officinalis root system accesses water from the superficial soil profile that is subjected to large changes in water content (Gratani and Varone, 2004b). Thus, the high RL/PN ratio (2.47  0.63, mean value) is the result of the 82% PN decrease from the maximum, as attested by the thermal window analysis. S. aspera shows a relatively high RL/PN ratio (1.78  0.05) due to the 90% PN decrease from the maximum and a lower RL rate (1.80  0.18 mmol m2 s1). The relatively high RL/PN ratio (1.49  0.13) in C. incanus is also due to the 86% PN decrease from the maximum by its shallow and markedly planar root system (Amato and Sarnataro, 2001) that accesses water only from the superficial soil profile and the low LMA (14.3  1.5 mg cm2) which does not contribute enough to limit photo-damage to the photosynthetic apparatus. A lower RL/PN ratio (0.80  0.14, mean value) in the sclerophyllous species (P. latifolia, P. lentiscus and Q. ilex), and in E. arborea is due to a lower PN decrease in drought (62%), associated to high LMA and LTD values (18.3  4.0 mg cm2 and 559  76 mg cm3, mean value, respectively) and the high relative leaf water content (Catoni et al., 2013) which favors drought tolerance. Among the considered species, A. unedo has the lowest RL/PN ratio in August (0.49  0.05). A. unedo is functionally adapted to cope with the summer drought by its capability to reduce gas exchange via stomatal regulation (Gratani and Ghia, 2002) and by having a steeper leaf inclination (Gratani and Ghia, 2002) which is a prevention mechanism against a potential photo-inhibition of water-stressed leaves during drought. In autumn, specifically in September, the 17% average increase of the ratio RL/PN from the spring value is mainly due to a 32% lower PN rates. The high RL/PN ratio (0.38  0.04) in S. aspera underlines its lower PN recovery capacity after drought (43% of the spring value) while Q. ilex has the highest recovery capacity (87% of the spring value) resulting in a lower RL/PN (0.27  0.02). In winter, the considered species have the lowest RL/PN ratio in response to the lowest air temperatures, which represent an additional limitation to the Mediterranean plant production. PN decreases by 48% (in February) compared to the maximum by the limitation of the maximum catalytic activity of the respiratory enzymes (Atkin and Tjoelker, 2003). Among the considered species, Q. ilex is the most cold-tolerant species as confirmed by the photosynthetic thermal window that shows PN dropping below half of its maximum when Tl is lower than 8.0  C. The low RL/PN ratio (0.09  0.04) is justified by low RL rates (0.70  0.49 mmol m2 s1) associated to a 28% PN decrease. On the contrary, C. incanus seems to be the most cold-susceptible species, with a higher RL/PN ratio (0.21  0.03) due to a 59% PN decrease and the highest RL rates (1.70  0.19 mmol m2 s1). E. arborea, E. multiflora and R. officinalis have the same trend with a high RL/PN ratio (0.24  0.02) due to a 54% PN decrease and a high RL rate (0.87  0.08 mmol m2 s1). The low RL/PN ratio (0.08  0.04, mean value) in A. unedo, P. latifolia, P. lentiscus and S. aspera is due to a low PN decrease (46%) associated to low RL rates (0.45  0.15 mmol m2 s1, mean value). The PCA confirms the differences in physiological and morphological traits among the considered species. In particular, C. incanus has the highest mean yearly PN and RL rates, relatively low LMA and LTD and it is furthest from the other species emphasizing its drought semi-deciduous habitus. E. multiflora and R. officinalis are characterized by the highest LMA and LTD, higher RL rates in favorable, drought, autumn and winter periods, and the lowest PN rates in the favorable period. The group formed by E. arborea, P. lentiscus, P. latifolia and Q. ilex is in the middle. A. unedo

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and S. aspera are close to this group, despite lower RL rates during the year as compared to the others species, and their relatively low LMA and LTD. Moreover, the results underline that leaf morphology are part of the adaptive strategy of the considered species to Mediterranean climate stress factors. In fact, the xeromorphic leaf type, attested by a small leaf area, high leaf thickness (i.e. high LMA) and leaf density (i.e. high LTD) favors carbon gain profits over transpiration losses during the year with the maintenance of relatively high profits during drought. Nevertheless, the construction cost in these leaf types justifies the relatively high RL rates reflecting the high metabolic expenditure of photosynthate in the leaf structure. Across different species, LMA correlates with leaf life span (LL), photosynthesis and respiration, describing the trade-off between long-lived leaves with greater allocation to structural rather than metabolic components vs. short-lived leaves with high metabolic activity and less physical protection (Reich et al., 1999). Long LL in resource-poor environments is generally thought to enhance nutrient conservation providing a longer time for the amortization of leaf construction cost in species with low rates of carbon gain (Aerts and van der Peijl, 1993). The considered species are characterized by a relatively long LL, and in particular, the typical sclerophyllous species (P. latifolia, P. lentiscus and Q. ilex) have the longest LL (48  1 months, 18  6 months and 36  2 months, respectively), the narrow-leaf species (E. arborea, E. multiflora and R. officinalis) of 11  1 months (mean value), A. unedo and S. aspera of 11  1 months, and C. incanus of 5  1 months (summer leaves) and 8  1 months (winter leaves) (Bombelli, 2001; Gratani and Varone, 2004b). Thus, LL is a good indicator of carbon investment strategies of the considered species, considering that construction and maintenance costs of leaves are related to the benefit accrued in terms of carbon fixation. Moreover, these results confirm the general trend underlined by Wright et al. (2001) whereby species growing in dry-sites have high leaf respiration rates. 7. Conclusions The ratio RL/PN can be used to evaluate plant carbon gain in response to environmental factor variations. Moreover, our findings of a seasonal variation in the ratio RL/PN are consistent with those of Zaragoza-Castells et al. (2008) showing that the ratio increases in response to the increase of temperature and in drought. The hypothesized extension of the dry season in the Mediterranean area, as forecasted in the next decades by climatic models (IPCC, 2007) might favor P. latifolia, P. lentiscus, Q. ilex, A. unedo and E. arborea by their capability to maintain a lower RL/PN ratio (less than 1.0) during drought, which is indicative of a more positive carbon balance, compared to C. incanus, E. multiflora, R. officinalis and S. aspera. Thus, we can assume that the species able to keep a positive carbon balance during drought will be more adapted in dealing with intensified environmental stress. The vegetation of the Mediterranean shrublands contributes to a relevant amount of carbon sequestration at a global level (Gratani et al., 2012), and in the long term the different competitive ability could determine change in the community structure and composition, resulting in variations of the CO2 sequestration capacity. References Aerts, R., van der Peijl, M.J., 1993. A simple model to explain the dominance of lowproductive perennials in nutrient-poor habitats. Oikos 66, 144e147. Allard, V., Ourcival, J.M., Rambal, S., Joffre, R., Rocheteau, A., 2008. Seasonal and annual variation of carbon exchange in an evergreen Mediterranean forest in southern France. Global Change Biol. 14, 714e725. Amato, M., Sarnataro, M., 2001. Root analysis of maquis at Castel Volturno, Italy. In: Mazzoleni, S., Colin, C.J. (Eds.), ModMED: Modelling Mediterranean Ecosystem

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