Photosynthetic responses to water deficit in six - Tree Physiology

Summary We sought to explain the declining distribution inthe Balearic Islands of the endemic shrub Rhamnus ludovici-salvatoris R. Chodat, by comparing its photosynthetic re-sponse to drought with that of several widely distributed, com-peting Mediterranean species (R. alaternus L., Quercus ilex L.,Pistacia lentiscus L., Q. humilis Mill. and P. terebinthus L.).

All of the study species, except for the two Rhamnus spe-cies, avoided desiccation by rapidly adjusting their stomatalconductance at the onset of drought, and maintaining constantleaf relative water content. The two Rhamnus species showeddesiccation-tolerant behavior; i.e., as drought progressed,their predawn leaf relative water content decreased simulta-neously with stomatal closure. All four desiccation-avoidingspecies showed a significant positive correlation between leafthermal dissipation (estimated by the fluorescence parameterNPQ (non-photochemical quenching)) and the de-epoxidationstate of the xanthophyll cycle (DPS). The two Rhamnus spe-cies exhibited maximum DPS regardless of treatment, butonly R. alaternus increased NPQ in response to drought.

Rhamnus ludovici-salvatoris had a high ratio of photorespi-ration to photosynthesis and a low intrinsic water-use effi-ciency; traits that are likely to be unfavorable for plant produc-tivity under arid conditions. It also had the lowest DPS andthermal dissipation among the six species. We conclude thatthe photosynthetic traits of R. ludovici-salvatoris account forits limited ability to compete with other species in the Mediter-ranean region.

Keywords: chlorophyll fluorescence, deciduous, drought, ev-ergreen, gas exchange, leaf mass area, nitrogen, Pistacia,Quercus, Rhamnus, xanthophyll cycle.

Introduction

Drought is the main environmental constraint on plant bio-mass production in the Mediterranean region. Consequently, it

is likely that ecophysiological traits that determine the abilityof a species to cope with drought partially explains its distribu-tion and ecological fitness in the Mediterranean region (Baz-zaz 1979, Schulze 1982, Lambers et al. 1998). The intrinsiclink between photosynthesis and biomass production suggeststhat photosynthesis and its response to drought is likely to playa major role in determining the ability of tree seedlings to es-tablish in drought-prone areas, because unlike adult trees,seedlings do not possess additional compensatory mecha-nisms such as deep roots or dense canopies. The closest asso-ciation between leaf photosynthesis and plant growth is seenin young plants, a fact attributable to their low leaf area index(Gardner et al. 1985). A good correlation between net photo-synthesis and relative growth rate has been observed in sap-lings (Pattison et al. 2001) and a correlation between seasonalphotosynthesis and the percentage of ground covered wasfound in Chaparral species (Oechel et al. 1981).

Differences in photosynthetic properties and responses todrought between evergreen and winter deciduous species mayaccount for differences in the distribution patterns of the twogroups of species in Mediterranean-type ecosystems (Ehler-inger and Mooney 1982, Ne’eman and Goubitz 2000). Decid-uous species generally predominate in cold and humid sub-Mediterranean regions and compensate for their shortergrowth period with a higher photosynthetic capacity (Ehle-ringer and Mooney 1982, Ne’eman and Goubitz 2000, but seeDamesin et al. 1998). In contrast, evergreen species predomi-nate in the hot and dry Mediterranean regions, where they canmaintain high photosynthetic rates during winter when decid-uous species are photosynthetically inactive.

Endemic plants account for 7–8% of the flora of the Medi-terranean islands (Cardona and Contandriopoulos 1979).However, judging from their declining distribution and highextinction rates (Alomar et al. 1997), some endemic speciesare poorly adapted to present conditions. Because climate

Tree Physiology 22, 687–697© 2002 Heron Publishing—Victoria, Canada

Photosynthetic responses to water deficit in six Mediterraneansclerophyll species: possible factors explaining the decliningdistribution of Rhamnus ludovici-salvatoris, an endemic Balearicspecies

J. GULÍAS,1 J. FLEXAS,1,2 A. ABADÍA3 and H. MEDRANO1

1 Laboratori de Fisiologia Vegetal, Departament de Biologia, Universitat de les Illes Balears, Carretera de Valldemossa, Km. 7.5, 07071 Palma deMallorca, Balears, Spain

2 Author to whom correspondence should be addressed ([email protected])3 Departamento de Nutrición Vegetal, Estación Experimental de Aula Dei (Consejo Superior de Investigaciones Científicas), Apartado 202, 50080

Zaragoza, Aragón, Spain

Received September 25, 2001; accepted December 31, 2001; published online June 3, 2002

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change models predict that more arid conditions will prevail inthe Mediterranean Basin (Osborne et al. 2000), many of thesespecies may become extinct. A recent survey of Balearic en-demic species showed that these plants have a lower photosyn-thetic capacity under optimal conditions than their widespreadrelatives (J. Gulías et al., unpublished results). The low photo-synthetic capacity was associated with low specific leaf areaand photosynthetic nitrogen-use efficiency.

We studied Rhamnus ludovici-salvatoris R. Chodat, an en-demic evergreen shrub that declined in distribution during thelast century. Until recently, this species was found in Cabrera,Menorca, Serra de Tramuntana and Serra de Llevant (the lasttwo areas located on the island of Mallorca) (Alomar et al.1997). Today, however, the species has disappeared fromMenorca and Serra de Llevant. Furthermore, where it sur-vives, the populations are characterized by a low proportion ofseedlings and young saplings, suggesting low establishmentsuccess. The main objective of this study was to compare thephotosynthetic response to drought of saplings of R. ludovici-salvatoris with that of species that are widely distributed in theMediterranean region. A second goal was to evaluate whetherother species with low distribution in the Balearic Islands (i.e.,winter deciduous species) have the same leaf traits as R. lud-ovici-salvatoris.

Materials and methods

Plant material and environmental conditions

Mallorca, the largest Balearic Island, is situated in the westernMediterranean Basin (39°15′ to 40°00′ N, 2°15′ to 3°30′ E).The climate is Mediterranean, with a mean annual rainfallranging from 300 mm on the south coast to more than1000 mm in some mountain areas in the northwest. Rain fallsmainly from September to April, and drought can last for5–6 months. The dominant vegetation comprises evergreensclerophyll shrublands (dominated by Pistacia lentiscus L.,Rhamnus alaternus L. and Olea europaea L.) and woodlands(dominated by the holm oak, Quercus ilex L.). Winter decidu-ous woodlands are absent.

Six species were studied: Rhamnus alaternus, R. ludovici-salvatoris, Quercus ilex, Q. humilis Mill., Pistacia lentiscusand P. terebinthus L. Rhamnus alaternus, P. lentiscus andQ. ilex are evergreen plants (two shrubs and a tree, respec-tively) widely distributed on the Balearic Islands and along thewestern Mediterranean Basin. Rhamnus ludovici-salvatoris isan evergreen shrub of limited distribution, endemic to theBalearic Islands. Its distribution has diminished during the lastcentury, with the extinction of several populations (authors’unpublished observations). At present, this species is presentin only certain localities of Mallorca and Cabrera, a small is-land south of Mallorca. Pistacia terebinthus and Q. humilis arewinter deciduous trees (the former frequently appearing as ashrub), typical of Mediterranean conditions wetter than thosein Mallorca. The distribution area of P. terebinthus in Mal-lorca is limited to some humid mountain areas, whereasQ. humilis is absent from the Balearics. Among these species,

the shrubs (P. lentiscus and the two Rhamnus species) arenanophylls, and the trees (P. terebinthus and the two Quercusspecies) are nano-microphylls or microphylls (Christodoul-akis and Mitrakos 1987). All these species share some basiccharacteristics: they have a Mediterranean origin and distribu-tion (Suc 1984, Castro-Díez et al. 1998, Ne’eman and Goubitz2000), they are currently growing within the Mediterraneanoak forests and related successional communities (Tomaselli1981, Suc 1984), and they are sclerophyllous (Christodoulakisand Mitrakos 1987).

The study plants, six per species, were grown outdoors atthe University of the Balearic Islands (Mallorca, Spain), inlarge pots (volume 60 l, height 60 cm) containing a 1:1 (v/v)mixture of clay–calcareous soil and horticultural substrate.Although the pots may eventually limit root growth, they oth-erwise simulate natural conditions because about 85% of rootbiomass of sclerophyllous shrubs is located in the upper 50 cmof the soil profile (Jackson et al. 1996). The plants were5 years old at the onset of the experiments, which were con-ducted during the summers (July–September) of 1998, 1999and 2000. The environmental conditions during these sum-mers were similar, with a mean maximum temperature of30 °C and a mean minimum temperature of 19 °C, no rain anda mean monthly evapotranspiration of 160 l m–2.

Treatments and water status determination

Mid-morning (i.e., maximum) light-saturated stomatal con-ductance (g) is very sensitive to water stress. Its complex regu-lation depends on interactions with soil water status, xylemabscisic acid (ABA) content, leaf water status and other fac-tors. We have recently shown that g is indicative of leaf waterstress, regardless of the factor causing the stress (Flexas et al.2002, Medrano et al. 2002). Our main rationale for using g asan indicator of water stress is that many species (includingthose studied here) have similar reductions in photosynthesisat any given g, irrespective of leaf water status and leaf-to-airvapor pressure deficit (Medrano et al. 2002). Based on this cri-terion, mild drought treatments and severe drought treatmentswere defined as soil water deficits causing 50 and 75% reduc-tions in maximum g (i.e., relative to the control treatment), re-spectively. The drought treatments were imposed by with-holding water, and mid-morning g values were measured dailyuntil the values corresponding to each treatment were reached.Typically, under summer conditions, water was withheld forabout 3 days to achieve a mild drought and for 4–6 days toachieve a severe drought.

Although mid-morning g values were used to define thedrought treatments, two other independent measurementswere also performed to characterize the degree of droughtexposure. First, soil water content was determined in four toeight randomly chosen pots per treatment by time domainreflectometry (TDR, Trime System, Imko, Ettlingen, Ger-many), and referred to as percent of field capacity. Soil watercontent was 100% (by definition) under well-watered condi-tions (control), 84 ± 3% for mild drought and 42 ± 2% for se-vere drought. Second, six leaves per species and treatment

688 GULÍAS, FLEXAS, ABADÍA AND MEDRANO

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were sampled before sunrise to determine relative water con-tent (RWC = (fresh weight – dry weight)/(turgid weight – dryweight)). The turgid weight of the leaves was determined after24 h in distilled water at 4 °C in the dark. Dry weights were ob-tained after oven-drying for 48 h at 70 °C.

Determination of leaf mass area and leaf nitrogen

Samples of the leaves that were used for gas exchange mea-surements were analyzed for leaf nitrogen concentration ([N])with an elemental analyzer (Model EA 1108, Carlo Erba In-struments, Milan, Italy). Leaf mass area (LMA = leaf dryweight/fresh leaf area) was determined with an AM-100 leafarea meter (ADC, Herts, U.K.), after which the leaves weredried and weighed.

Gas exchange measurements

Gas exchange measurements were determined on attachedfully expanded leaves in saturating light (1000 µmol m–2 s–1)with a portable IRGA (LI-6400, Li-Cor, Lincoln, NE). Whenfour to six sun-exposed leaves of a given plant showed a gvalue corresponding to the desired treatment (see above), twowere chosen to construct a light- and a CO2-response curve,respectively. This selection procedure was repeated for fourreplicates per treatment. Temperature was maintained at 30 °Cwith a relative humidity of 40–60% inside the leaf chamberduring measurements (leaf temperatures were between 28 and33 °C, and leaf-to-vapor pressure deficits were between 2 and3 kPa). These measurements were completed during the morn-ing to avoid the midday depression of photosynthesis andstomatal conductance.

The LI-6400 light source enabled automatic changes in pho-tosynthetic photon flux density (PPFD), which were applied at3–5 min intervals to determine the light response curves. ThePPFDs were 1500, 1000, 750, 500, 200, 50, 25 and 0 µmol m–2

s–1. The CO2 flux was adjusted to maintain a concentration in-side the chamber of 360 µmol mol–1.

The CO2 response curves were determined at a PPFD of1000 µmol m–2 s–1. The different CO2 concentrations were ob-tained from portable CO2/air mixture tanks and automaticallycontrolled by the LI-6400 CO2 injector. The CO2 concentra-tion ([CO2]) was first set near zero and then progressively in-creased to 50, 100, 200, 360, 500, 650 and 800 µmol mol–1

(Escalona et al. 1999). Gas exchange measurements were de-termined at each step after maintaining the leaf at the new[CO2] for 5 min. The sub-stomatal [CO2] (Ci) was calculatedaccording to von Caemmerer and Farquhar (1981).

The net CO2 assimilation (AN) versus PPFD and AN versusCi curves were fitted with Sigma Plot 4.0 for Windows (SPSS)by nonlinear regression to hyperbolic and exponential equa-tions, respectively (Martin and Ruiz-Torres 1992, Escalona etal. 1999). Apparent quantum yield (φ) and apparent carboxyl-ation efficiency (ε) were estimated as the initial slopes of theAN–PPFD and AN–Ci curves, respectively. The compensationpoints for light (k) and CO2 (Γ) were calculated from the x-in-tercepts of the AN–PPFD and AN–Ci curves, respectively.Dark respiration (RD) was measured after holding the leaves in

darkness. The stomatal limitation to photosynthesis (l) wascalculated from AN–Ci curves according to Farquhar andSharkey (1982).

Maximum photosynthetic rates at saturating light and [CO2](Amax) were not measured during construction of the AN–Ci

curves, because the [CO2] was not increased above 800 µmolmol–1 to avoid any interference of high [CO2] with stomatalconductance. To ensure that Amax values estimated by the ex-ponential adjustments were close to the real Amax values, weapplied higher CO2 concentrations to different leaves thanthose used for the construction of the AN–Ci curves. Theseleaves were clamped in the LI-6400 chamber at atmospheric[CO2] and allowed to stabilize. The [CO2] was then immedi-ately (within 1 min) increased to 2000 µmol mol–1, andstomatal conductance monitored continuously. After about1 min, photosynthesis was stable, and g was almost un-changed. The value of Amax was then recorded. Figure 1 showsthe relationship between the measured Amax and that estimatedfrom exponential adjustments. All values fall near the 1:1 ra-tio, indicating that the estimated values of Amax are reasonable.

Extrapolation of the curve to Ci = 0 (RL) was used to esti-mate the sum of photorespiration and mitochondrial respira-tion in the light. Although this method could overestimateactual photorespiration, the range of values obtained was con-sistent with estimations made according to the model of Val-entini et al. (1995), which is based on combining gas exchangeand chlorophyll fluorescence measurements (data not shown).

Chlorophyll fluorescence measurements

Chlorophyll fluorescence parameters were measured on at-tached leaves. For each treatment, six measurements weremade on six leaves (i.e., two leaves per plant) with a portablepulse amplitude modulation fluorometer (PAM-2000, Walz,Effeltrich, Germany). At predawn (0600 h), the background

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DROUGHT AND PHOTOSYNTHESIS IN MEDITERRANEAN SPECIES 689

Figure 1. Relationship between light- and CO2-saturated photosyn-thetic rate (Amax) measured at 2000 µmol CO2 mol–1 and that esti-mated from exponential adjustments of AN versus C i curves.Abbreviations: R.l-s. = Rhamnus ludovici-salvatoris; R.a. = Rhamnusalaternus; Q.i. = Quercus ilex; Q.h. = Quercus humilis; P.l. = Pistacialentiscus; and P.t. = Pistacia terebinthus.

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fluorescence signal (Fo), the maximum fluorescence (Fm) andthe maximum quantum yield of photosystem II (PSII) (Fv/Fm

= (Fm – Fo)/Fm) were determined at an irradiance of 0.5 µmolm–2 s–1 and a frequency of 600 Hz. Steady-state fluorescence(Fs) in mid-morning sunlight was determined at an irradianceof 0.5 µmol m–2 s–1 and a frequency of 20 kHz. The PPFD inci-dent on the leaves was always higher than 1000 µmol m–2 s–1,which was above photosynthesis saturation in these plants. Toobtain the steady-state maximum fluorescence yield (Fm′),saturation pulses of about 10,000 µmol m–2 s–1 and 0.8-s dura-tion were applied. The PSII photochemical efficiency(∆F/Fm′) was then calculated according to Genty et al. (1989):

∆F F F F F/ ) /m m s m= ( ,′ ′ − ′ (1)

and used to determine the linear electron transport rate (ETR)(Krall and Edwards 1992):

ETR PPFD0.5 0.84,m= ′( / )∆F F (2)

where PPFD is photosynthetic photon flux density incident onthe leaf, 0.5 is a factor that assumes an equal distribution of en-ergy between the two photosystems, and 0.84 is the leaf ab-sorptance for many sclerophyll species (Ehleringer andComstock 1987). In this study, leaf absorptance was estimatedaccording to Sharp et al. (1984). No significant differenceswere observed among the six species (data not shown). Non-photochemical quenching of chlorophyll fluorescence (NPQ)at mid-morning was calculated as:

NPQ ) / .m m m= − ′ ′( F F F (3)

Pigment analyses

Immediately after chlorophyll fluorescence measurements (atpredawn and midday), discs were punched from leaves of thesame plants showing the same orientation as those used forfluorescence measurements and submersed in liquid nitrogen.Six samples per treatment were taken from different plants(around three to four leaves per sample). The values presentedare means ± SE. Pigments were extracted by grinding leaf tis-sue in a mortar with acetone (1 cm2 of leaf tissue per ml of sol-vent) in the presence of sodium ascorbate. Pigments wereidentified and quantified by high performance liquid chroma-tography according to Abadía and Abadía (1993).

Statistical analyses

Statistical analyses of the data were performed with the SPSS9.0 software package (SPSS, Chicago, IL). Pearson’s correla-tion analysis was performed on all the studied parameters.Two-way ANOVAs, with treatment and species as factors,were performed for the studied parameters. Differences be-tween means were revealed by Tukey’s highest significant dif-ference (HSD) analyses (P < 0.05).

Results

Maximum photosynthesis and stomatal conductance values

Maximum values of photosynthesis and stomatal conductance(Table 1) of the experimental plants were similar to those ob-tained for the same species under field conditions. Net photo-synthetic rates were about 15–16 µmol m–2 s–1 for the Quercusspecies and for P. terebinthus (see Gucci et al. 1997, Damesinet al. 1998, Gulías et al. 2002), and about 11 µmol m–2 s–1 forthe Rhamnus species and for P. lentiscus (see Gucci et al.1997, Flexas et al. 2001, J. Gulías et al., unpublished results).The values under mild and severe drought were similar tothose of field-grown plants at the beginning and at the end ofthe summer, respectively (Damesin and Rambal 1995, García-Plazaola et al. 1997, Faria et al. 1998, Flexas et al. 2001,Gulías et al. 2002).

Variations in RWC, LMA and leaf N concentration withdeclining g

A summary of the ANOVA of the effects of drought treatmentand species, and the combined treatment × species interactionon mid-morning g, predawn leaf relative water content(RWC), leaf mass area (LMA) and leaf [N] is shown in Ta-ble 2. Drought treatment had little effect on RWC; that is, gwas reduced by half before any change in RWC could be de-tected. However, the highly significant effect of the combinedtreatment × species interaction reveals species-dependent dif-ferences in the RWC response. As shown in Figure 2, theQuercus and Pistacia species showed changes in RWC of lessthan 10%, even when stomatal closure was pronounced (wetherefore refer to these species as desiccation avoiders). Incontrast, both Rhamnus species showed large reductions inRWC (> 10%) in response to soil water depletion that wereparalleled by stomatal closure (a response characteristic ofdesiccation-tolerant species). A small reduction in RWC in re-sponse to severe drought has been reported in some species(Henson et al. 1989), and may be a result of tight stomatal reg-ulation in response to rapidly imposed drought.

Drought did not significantly affect LMA. The highly sig-nificant effect of the treatment × species interaction on LMAwas caused by the two Rhamnus species, which showed pro-gressively increasing LMA with increasing soil water deple-tion. Because leaf growth was complete before the start of theexperiments, it is likely that the observed treatment effect onLMA was simply a result of interannual differences.

Although there were significant effects of treatment, spe-cies and treatment × species interaction on leaf [N], the treat-ment effect was evident only under severe drought. Evenunder severe drought, leaf [N] was reduced by less than 30%(Table 2), whereas g was reduced by 75%, suggesting that thereduction in leaf [N] was a consequence of low water uptakeby roots as a result of reduced transpiration. Because no leaf orshoot growth was observed during the experiment, we as-sumed that any influence of developmental and nutritional dif-ferences between treatments was low.



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Effects of drought treatment and species on photosyntheticparameters

Because Pearson’s correlation analyses indicated that φ, k andRD were not correlated with other parameters, including RWCand g, these parameters were not considered further. Severalparameters that were significantly correlated with g were alsosignificantly correlated with other parameters (P < 0.001).Among these, ETR showed a highly significant negative cor-

relation with NPQ, whereas Amax, ε and Γ were all strongly in-terrelated. Moreover, Amax, ε and Γ were significantlycorrelated with ETR.

A summary of the ANOVA of the effects of treatment, spe-cies and treatment × species interaction on selected photosyn-thetic parameters is shown in Table 3. Drought significantlyaffected each parameter presented in Table 3, whereas theinterspecific variation was only significant for RL and Fv/Fm.



Table 1. Mean values for the study species and treatments of most of the parameters studied. Different letters indicate significantly (P < 0.05) dif-ferent means among treatments and species (that is a total of 18 treatments, these being the 18 species × treatment combinations). Abbreviations: g(mmol H2O m–2 s–1) = stomatal conductance; RWC (%) = relative water content; LMA (g m–2) = leaf mass area; [N] (mg g–1 dry weight) = leafnitrogen concentration; AN (µmol m–2 s–1) = net CO2 assimilation; A/g (µmol mol–1) = intrinsic water-use efficiency; φ (mol quantum–1) = appar-ent quantum yield; k (µmol m–2 s–1) = compensation points for light; RD (µmol m–2 s–1) = dark respiration ; Amax (µmol CO2 m–2 s–1) = light- andCO2-saturated photosynthesis; ε (mol–1) = apparent carboxylation efficiency; Γ (µmol mol–1) = compensation point for CO2; RL (µmol m–2 s–1) =the sum of photorespiration and mitochondrial respiration in the light; l (dimensionless) = stomatal limitation to photosynthesis; Fv/Fm

(dimensionless) = maximum quantum yield of photosystem II; ETR (µmol m–2 s–1) = electron transport rate; NPQ (relative units) = non-photo-chemical quenching of chlorophyll fluorescence; [Chl] (mmol m–2) = concentration of chlorophyll; [VAZ] (mmol m–2) = concentration ofviolaxanthin, antheraxanthin and zeaxanthin. Treatments: C = control; MD = mild drought; and SD = severe drought.

R. alaternus R. ludovici-salvatoris Q. ilex Q. humilis P. lentiscus P. therebinthus

C MD SD C MD SD C MD SD C MD SD C MD SD C MD SD

g 165.0 59.6 38.5 222.0 115.5 37.9 277.8 112.3 42.8 278.8 134.0 47.2 167.0 78.7 37.1 243.3 129 42.5bc def f ab cdef f a cdef f a cd ef bc def f ab cde f

RWC 87.2 77.2 81.4 88.9 82.2 73.2 80.3 82.7 73.2 95.4 92.3 88.4 90.5 83.4 86.8 89.7 89.5 89.6abc bcde de abc bcde de cde bcd e a a abc ab abc de abc abc abc

LMA 136.1 155.4 162.1 111.5 145.1 174.0 198.3 200.3 217.7 115.9 113.0 116.4 221.8 207.3 265.6 130.4 132.2 120.4abcd cde de a bcde ef fg fg g ab a ab g g h abc abcd ab

[N] 1.98 2.12 1.75 1.84 1.76 1.65 1.34 1.27 1.21 2.59 2.31 2.00 1.30 1.55 0.96 2.42 2.39 1.76def cde efg ef efg fg hi i i a bc de hi gh j ab ab efg

AN 11.5 5.2 4.2 10.9 9.3 3.3 15.5 7.4 3.7 16.0 8.8 4.0 11.2 7.2 2.5 15.2 7.9 3.3bc fghi ghi cde cde i a defgh hi a cdef hi cd efgh i ab cdefg i

AN/g 74.9 87.4 113.9 49.2 83.1 85.1 56.9 66.3 87.5 57.9 66.1 83.9 75.3 91.6 65.8 63.9 63.0 76.0abc abc c a abc abc ab ab abc ab ab abc abc bc ab ab ab abc

φ 0.063 0.042 0.048 0.060 0.048 0.033 0.060 0.032 0.027 0.051 0.071 0.031 0.050 0.049 0.038 0.054 0.055 0.046ab bcdef abcdef abcd abcdef cdef abc def f abcdef a ef abcdef abcdef bcdef abcdef abcde abcdef

k 19.3 37.4 38.8 73.2 46.3 43.0 23.1 52.1 41.5 37.7 45.5 28.8 28.4 33.4 46.4 47.1 40.5 46.4a ab ab c abc abc ab bc ab ab abc ab ab ab abc abc ab abc

RD 1.2 1.5 1.8 4.2 2.1 1.4 1.4 1.5 1.1 1.9 3.3 0.9 1.3 1.6 1.8 2.5 2.3 2.2cd cd cd a bcd cd cd cd cd bcd ab d cd cd cd bc bc bcd

Amax 26.1 19.4 17.1 32.1 26.0 16.7 32.3 14.8 6.7 34.6 15.4 8.5 34.6 26.0 12.6 38.2 22.6 16.6bc cde cdef ab bc cdef ab cdef f ab cdef ef ab bc def a bcd cdef

ε 0.066 0.044 0.043 0.080 0.064 0.037 0.089 0.070 0.028 0.099 0.057 0.059 0.080 0.058 0.021 0.128 0.089 0.041bcde defg defg bcd bcdef efg bc bcde fg abc cdefg cdef bcd cdefg g a bc efg

Γ 74.6 98.3 103.3 96.7 93.1 163.9 69.0 79.1 117.5 63.0 89.9 93.1 73.3 77.3 102.7 74.4 80.8 107.8abc abcd bcd abcd abcd e ab abc d a abcd abcd abc abc bcd abc abcd cd

RL 4.9 4.3 4.5 7.8 6.0 5.9 6.2 5.4 3.3 6.2 5.1 5.4 5.9 4.4 2.1 9.0 7.1 4.4bcde cde bcde ab abcd abcd abcd bcde de abcd bcde bcde abcd bcde e a abc cde

l 0.43 0.51 0.62 0.33 0.38 0.59 0.39 0.34 0.53 0.38 0.36 0.35 0.41 0.66 0.62 0.38 0.46 0.64abcdef abcdef def a ab bcdef a abcd abcdef ab abcdef ef abcde cdef f ab abcdef ef

Fv/Fm 0.794 0.741 0.736 0.799 0.791 0.737 0.816 0.807 0.797 0.824 0.825 0.805 0.804 0.775 0.766 0.779 0.785 0.792abcd ef f abcd abcd f ab abc abcd a a abc abc cde ef bcd bcd cd

ETR 96.1 64.9 44.9 106.1 74.4 80.0 164.8 105.3 46.0 184.2 78.4 69.0 134.8 105.0 36.1 163.5 106.8 64.9def fgh gh def efg def ab cde gh a def fg bc cde h ab cd fgh

NPQ 2.7 3.9 3.8 2.7 3.2 3.3 2.3 2.9 3.8 2.0 4.2 3.0 2.7 2.9 5.1 1.2 2.8 3.6bcd def def bcd bcde bcde abc bcd def ab ef bcd bcd bcd f a bcd cde

[Chl] 22.5 30.1 37.0 26.1 33.9 45.5 21.6 31.2 26.9 25.9 27.3 26.6 19.7 31.6 22.5 33.0 23.8 25.3efg bcdef b cdefg bc a fg bcde cdefg cdefg cdefg cdefg g bcde bcdef bcd defg cdefg

[VAZ] 10.5 7.6 9.0 7.4 9.5 4.8 5.9 5.8 7.9 9.2 9.8 10.8 8.2 8.7 11.4 8.5 12.2 9.9abc cdef abcde cdef abc f def ef cdef abcd abc abc bcde bcde ab bcde a abc

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The treatment × species interaction had a significant effect onall parameters presented in Table 3, except RL, suggesting spe-cies-dependent differences in the RL response to drought. Fig-ures 3 and 4 show parameters that were significantly affectedby treatment × species interaction.

The response of AN to drought followed that of g (Fig-ures 3A–C), except in drought-treated plants of R. ludovici-salvatoris, which maintained an almost constant AN in controlplants and in plants subjected to mild drought (Figure 3A).Among species in the well-watered treatment, R. ludovici-salvatoris had the lowest intrinsic water-use efficiency (AN/g)(Figure 3D). In all species, AN/g increased with decreasing gand AN (Figures 3D–F), reaching maximum values in plants inthe severe drought treatment. Among species in the mild andsevere drought treatments, the highest AN/g values were foundin R. alaternus and P. lentiscus, and the lowest values werefound in P. terebinthus. Stomatal limitation (l ), calculatedfrom AN–Ci curves, showed a similar pattern to that of AN/g(Figure 3G–I).

Drought caused decreases in Amax (Figure 4A–C), ε (Fig-ure 4D–F) and ETR (Figure 4G–I). The drought-induced de-clines in these parameters followed a similar pattern in allspecies, although the relative decreases were slightly higher in

the Quercus and Pistacia species (60–80%) than in the Rham-nus species (40–50%).

Pigment composition and its relationship with photochemistry

Some interspecific and treatment-dependent differences wereobserved in leaf pigment composition. Area-based total chlo-rophyll concentration differed markedly among species (Ta-ble 1), but variations between drought treatments were small.For the two Rhamnus species, there was a progressive increasein chlorophyll concentration paralleling the increase in soilwater depletion; however, this could simply be a consequenceof interannual differences. The total VAZ (sum of violaxan-thin, antheraxanthin and zeaxanthin) pool as a proportion ofchlorophyll concentration was species-dependent, but washardly affected by the drought treatments (Table 1).

All of the species had a drought-induced sustained DPS atpredawn (Figure 5A), ranging from 0.12 to 0.23. PredawnDPS was related to low Fv/Fm only in the three shrub species,whereas the tree species maintained an Fv/Fm close to 0.8, irre-spective of DPS (Figure 5A). A correlation between mid-morning NPQ and DPS was observed when the six specieswere considered together (Figure 5B); however, there was nocorrelation between these parameters if only the Rhamnus spe-cies were considered. The two Rhamnus species had maxi-mum DPS values even during irrigation. If only the four desic-cation-avoiding species are considered, the correlationimproves (r 2 = 0.67, P < 0.01). Maximum DPS was similar(0.8–0.9) for five of the study species, but was lower (0.65)for R. ludovici-salvatoris, which was also the only species thatshowed no increase in NPQ in response to drought, and highETR even during severe drought (Figure 4G).

Discussion

Relationship between g and RWC

The study species fell into two groups on the basis of their re-



Table 2. Two-way ANOVA of the effects of treatment, species andtreatment × species interaction on mid-morning stomatal conductance(g), predawn leaf relative water content (RWC), leaf mass area(LMA) and leaf nitrogen concentration on a dry mass basis ([N]).

Parameter Treatment Species Treatment × speciesP-value P-value P-value

g < 0.001 0.044 0.024RWC 0.104 0.059 < 0.001LMA 0.077 < 0.001 < 0.001[N] < 0.001 < 0.001 < 0.001

Table 3. Two-way ANOVA of the effects of treatment, species andtreatment × species interaction on the photosynthetic parametersfound to correlate with stomatal conductance. Abbreviations: AN

(µmol m–2 s–1) = net CO2 assimilation; A/g (µmol mol–1) = intrinsicwater-use efficiency; Amax (µmol CO2 m–2 s–1) = light- and CO2-satu-rated photosynthesis; RL (µmol m–2 s–1) = the sum of photorespira-tion and mitochondrial respiration in the light; l (dimensionless) =stomatal limitation to photosynthesis; ETR (µmol m–2 s–1) = electrontransport rate; Fv/Fm (dimensionless) = maximum quantum yield ofPhotosystem II.

Parameter Treatment Species Treatment × speciesP-value P-value P-value

AN < 0.001 0.266 < 0.001AN/g 0.025 0.201 0.027Amax < 0.001 0.191 < 0.001RL 0.004 0.024 0.069l 0.010 0.089 0.007ETR (NPQ) < 0.001 0.244 < 0.001Fv/Fm 0.031 0.015 < 0.001

Figure 2. Relationship between predawn leaf relative water content(RWC) and mid-morning stomatal conductance (g) for: �, Rhamnusludovici-salvatoris; �, R. alaternus; �, Quercus ilex; �, Q. humilis;�, Pistacia lentiscus; and �, P. terebinthus.

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sponse to soil water depletion; dessication-tolerant speciesand dessication-avoiding species. Both Rhamnus species ex-hibited simultaneous decreases in g and RWC, which is typi-cal of desiccation-tolerant species (Gucci et al. 1997, Martín-ez-Ferri et al. 2000). The Quercus and Pistacia speciesachieved 50% stomatal closure before showing a reduction inpredawn RWC. This rapid stomatal response to soil dryingmay enable these species to delay dehydration so, at least withrespect to this characteristic, they can be considered desicca-tion-avoiding species. Other studies have identified P. len-tiscus (Tenhunen et al. 1987, Gucci et al. 1997), Q. humilis(Damesin et al. 1998, Schwanz and Polle 1998, Nardini andPitt 1999) and Q. ilex (Sala and Tenhunen 1996, Damesin et al.1998) as drought-avoiding species, although the latter specieshas also been described as desiccation-tolerant (Sala and Ten-hunen 1994). The desiccation-avoiding trait may impose a se-rious constraint on the winter deciduous species P. terebinthusand Q. humilis, because it implies that they close their stomatarapidly at the onset of drought, thus severely limiting carbonassimilation during the summer. For the evergreen species,P. lentiscus and Q. ilex, this trait may not constrain year-roundassimilation as much as it does in the two deciduous speciesbecause the evergreen species maintain photosynthetic activ-ity during winter (Damesin et al. 1998, Joffre et al. 1999).

These photosynthetic differences may explain why P. terebin-thus is rare and limited to humid places (Castro-Díez et al.1998), and why Q. humilis is absent in Mallorca and other aridMediterranean zones (Ne’eman and Goubitz 2000).

Desiccation tolerance in the Rhamnus species facilitatesmaintenance of high assimilation rates during the onset of wa-ter deficit. However, the disadvantage is that the plants desic-cate progressively during the summer. In the present study,R. ludovici-salvatoris saplings lost 15% of leaf RWC in5 days. During especially dry and long summers, survival ofadult trees as well as seedlings may be threatened.

Leaf photosynthetic capacity

The photosynthetic characteristics of Mediterranean ever-green trees and shrubs are reported to be similar (Ehleringerand Mooney 1982). However, although we found that Amax

was similar in well-watered plants of all the study species, thehighest g, AN and ε were found in the tree species, and thehighest intrinsic water-use efficiency (AN/g) was found in theshrub species. Our findings suggest that g and perhaps meso-phyll conductance, but not photosynthetic capacity, were themain determinants of interspecific differences in AN (cf. Epronet al. 1995, Syversten et al. 1995).



Figure 3. Drought effects on mean values of net CO2 assimilation (AN; A–C), intrinsic water-use efficiency (AN/g; D–F) and stomatal limitation(l; G–I) in the two Rhamnus species (A, D, G), the two Quercus species (B, E, H) and the two Pistacia species (C, F, I). Values are means ± SE offour replicates. Within a species and parameter, different letters indicate significant differences between treatments (P < 0.05).

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Rhamnus ludovici-salvatoris was an exception among thestudy species, with both low maximum photosynthetic ratesand intrinsic water-use efficiency under irrigation. Moreover,it had the highest light respiration rates, indicating a disadvan-tageous carbon balance and low electron-use efficiency. Thesephotosynthetic characteristics imply that R. ludovici-salva-toris has relatively low resource-use efficiency, in addition tolow rates of Amax. Together these ecophysiological characteris-tics could account for the low competitiveness of this species,even under favorable conditions, compared with the othersstudied.

The adjustments in Amax and ε to drought were similar in allthe species, suggesting that these non-stomatal limitations tophotosynthesis do not determine interspecies differences inacclimation to arid conditions. This is consistent with the pro-gressive increases in AN/g and l as drought progressed. OnlyP. lentiscus had a decrease in AN/g in response to severedrought, but this species had the lowest g (37 mmol H2O m–2

s–1), which may have been below the inflexion point of the re-sponse of AN/g to g (Martin and Ruiz-Torres 1992, Flexas et al.2002). High values of AN/g (up to 120) have been measured infield-grown P. lentiscus at g values of 50 mmol H2O m–2 s–1 inmidsummer (Flexas et al. 2001).

Leaf photochemistry and xanthophyll cycle

The relationship between midday DPS and NPQ differed be-tween the desiccation-avoiding and desiccation-tolerant spe-cies. In the four desiccation-avoiding species, there was a highcorrelation between DPS and NPQ at mid-morning, as previ-ously described for many species (Demmig et al. 1988, John-son et al. 1993, García-Plazaola et al. 1997). However, thiscorrelation was not observed in the two desiccation-tolerantRhamnus species, which showed maximum DPS regardless oftheir water status. Similar findings have been reported byMunné-Bosch and Alegre (2000) for the Mediterranean spe-cies Lavandula stoechas L. However, the two Rhamnus spe-cies showed distinct de-epoxidation patterns. Among thestudy species, R. alaternus had the highest DPS values, and in-creased NPQ in response to drought. We hypothesize that, inthis species, as in L. stoechas (Munné-Bosch and Alegre2000), a high DPS, even in well-watered plants, represents astrategy for coping with rapidly induced (days to weeks)drought events typical of Mediterranean climates. In contrast,R. ludovici-salvatoris had the lowest de-epoxidation capacityamong the study species, which was accompanied by lowNPQ and, consequently, a high electron transport rate even



Figure 4. Drought effects on mean values of light- and CO2-saturated CO2 assimilation (Amax; A–C), apparent carboxylation efficiency (ε; D–F)and electron transport rate (ETR; G–I) in the two Rhamnus species (A, D, G), the two Quercus species (B, E, H) and the two Pistacia species (C, F,I). Values are means ± SE of four replicates. Within a species and parameter, different letters indicate significant differences between treatments(P < 0.05).

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during severe drought with almost no CO2 assimilation. Thismight explain the sustained high photorespiration rates ofR. ludovici-salvatoris under drought conditions.

The three shrub species showed some degree of permanentphotoinhibition under drought conditions, as assessed by de-creased predawn Fv/Fm, which was correlated with drought-induced sustained DPS during the night, as previously ob-served in other Mediterranean sclerophyll species (Demmig etal. 1988, Martínez-Ferri et al. 2000). This suggests that ahighly efficient, long-lasting photoprotective mechanism,rather than photodamage, was responsible for decreased Fv/Fm

in the shrub species. In contrast, the tree species had a constantFv/Fm irrespective of drought. Constant Fv/Fm values werealso found in the two Quercus species even when droughtcompletely stopped photosynthesis (Damesin and Rambal1995, Méthy et al. 1996). Constant Fv/Fm values may be acharacteristic of Quercus species (Epron et al. 1992).

Conclusions

We analyzed several photosynthetic characteristics and theirresponse to drought in Rhamnus ludovici-salvatoris, an en-demic shrub of the Balearic Islands that is declining in distri-bution, and compared the values with those of several widelydistributed species. We found that R. ludovici-salvatoris dis-played several traits that limit plant biomass production undersemi-arid conditions, including high ratios of respiration andphotorespiration to photosynthesis and a low intrinsic wa-ter-use efficiency that was not linked to a high photosyntheticrate. Stomatal closure at the onset of water deficit was also de-layed in this species. Moreover, among the six study species,R. ludovici-salvatoris had the lowest de-epoxidation state ofthe xanthophyll cycle and the lowest thermal dissipation.These unfavorable photosynthetic traits may result in lowercarbon gains under favorable conditions, a lower capacity toadjust photosynthesis under drought conditions, and lowerphotoprotection ability even during drought, compared withthe other study species. It is well known that anthropogenicfactors account for most landscape degradation in the BalearicIslands (Morey and Martínez 2000). Thus, the photosynthetictraits displayed by R. ludovici-salvatoris may contribute to itslow rates of establishment and recovery after degradation. Thedeciduous species studied did not display the same photosyn-thetic traits as R. ludovici-salvatoris, therefore, their low dis-tribution in the Balearic Islands is probably related to the ab-sence of carbon gain during winter. In addition, their drought-avoiding characteristics will strongly limit their ability to ac-cumulate carbon during summer in arid locations.

Acknowledgments

This work is part of Projects CICYT PB97-1174 and PB97-1176, sup-ported by the Spanish Ministry of Education and Science. J.F. wassupported by the UIB with a Beca d’Investigació. J.G. was supportedby the Project FEDER IFD97-0551. We are indebted to Dr. E. Des-cals and to Dr. M. Ribas-Carbó for grammar corrections.

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Photosynthetic responses to water deficit in six - Tree Physiology

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