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. 2003 Aug;92(2):215–222. doi: 10.1093/aob/mcg123

Relationship between Maximum Leaf Photosynthesis, Nitrogen Content and Specific Leaf Area in Balearic Endemic and Non‐endemic Mediterranean Species

JAVIER GULÍAS 1, JAUME FLEXAS 1,*, MAURICI MUS 1, JOSEP CIFRE 1, ELKADRI LEFI 1, HIPÓLITO MEDRANO 1
PMCID: PMC4243646  PMID: 12805082

Abstract

Gas exchange parameters, leaf nitrogen content and specific leaf area (SLA) were measured in situ on 73 C3 and five C4 plant species in Mallorca, west Mediterranean, to test whether species endemic to the Balearic Islands differed from widespread, non‐endemic Mediterranean species and crops in their leaf traits and trait inter‐relationships. Endemic species differed significantly from widespread species and crops in several parameters; in particular, photosynthetic capacity, on an area basis (A), was 20 % less in endemics than in non‐endemics. Similar differences between endemics and non‐endemics were found in parameters such as SLA and leaf nitrogen content per area (Na). Nevertheless, most of the observed differences were found only within the herbaceous deciduous species. These could be due to the fact that most of the non‐endemic species within this group have adapted to ruderal areas, while none of the endemics occupies this kind of habitat. All the species—including the crops—showed a positive, highly significant correlation between photosynthetic capacity on a mass basis (Am), leaf nitrogen content on a mass basis (Nm) and SLA. However, endemic species had a lower Am for any given SLA and Nm. Hypotheses are presented to explain these differences, and their possible role in reducing the distribution of many endemic Balearic species is discussed.

Key words: Balearic endemic species, leaf nitrogen content, Mediterranean climate, photosynthesis, specific leaf area

INTRODUCTION

Relationships between the growth capacity of a species and morphological and physiological leaf traits have been established (Poorter et al., 1990; Poorter and Bergkotte, 1992; Cornelissen et al., 1996, 1997; Grime et al., 1997). These traits include photosynthetic capacity (Am), leaf nitrogen content (Nm), both on a mass basis, leaf life span and specific leaf area (SLA). Species with high SLA and Nm usually show high potential relative growth rates (Hunt and Cornelissen, 1997). Am has been positively correlated with Nm and SLA (Poorter et al., 1990; Reich et al., 1994, 1997).

According to Reich et al. (1999), these patterns are common to all species, because significant nitrogen per unit mass accumulation would be required in leaves to achieve a high Am. Nitrogen accumulation requires thicker leaves, i.e. a lower SLA (Abrams et al., 1994; Niinemets, 1999). However, thick leaves with low SLA show a low Am, probably due to a limited diffusion of light and CO2 to the site of carboxylation (Lloyd et al., 1992; Terashima and Hikosaka, 1995; Hanba et al., 1999). Thus, biophysical constraints place a limit on the maximum photosynthetic rate that can be achieved by a leaf with a given SLA or Nm. Species with a lower Am for a given SLA or Nm are possible from a biophysical point of view. However, they would be potentially less competitive (Reich et al., 1999).

Of all the species, crops are the most likely to have overcome these biophysical constraints since they have been intensely selected to maximize production over hundreds of years. Other species that are likely to have overcome these biophysical constraints are C4 species, which have evolved a more efficient photosynthetic pathway than C3 plants. On the other hand, if species exhibiting a lower Am for a given SLA or Nm were to be found, those having evolved under low competitive pressure would be the primary candidates. Species endemic to the Balearic Islands could meet these conditions, since they have evolved under pre‐human ecological conditions characterized by a high pressure by herbivores (Alcover et al., 2000) and, presumably, relatively low competition between plants. Palynological data clearly show that there was a strong change in the vegetation composition of the islands after the arrival of humans (Burjachs et al., 1994; Yll et al., 1994), which has been dated to approx. 5000 years ago (Alcover et al., 2000). Indeed, in Hawaii, another insular system with a high percentage of endemicity, native species have lower Am, SLA and relative growth rate than invasive species, and this fact has been related to the competitive and invasive ability of the later species (Pattison et al., 1998; Baruch and Goldstein, 1999; Durand and Goldstein, 2001).

Net photosynthesis, leaf nitrogen content and specific leaf area were measured on 78 species, including crops, endemic and non‐endemic species, growing in a Mediterranean climate. The objectives of the present work were (a) to test whether Balearic endemic species have lower Am, Nm and SLA than other Mediterranean species; and (b) to determine if crops and endemic species overcome, respectively, the biophysical and ecological limitations suggested for the relationships between these leaf traits.

MATERIALS AND METHODS

Plant selection and classification into functional groups

Seventy‐three C3 species and five C4 species (Table 1), which represent more than 5·5 % of the Balearic flora (De Bolòs, 1997), were randomly chosen from different habitats to represent different growth forms, leaf habits and evolutionary histories. The species were classified into leaf habits (herbaceous deciduous, woody deciduous, semi‐deciduous and evergreens). Deciduous species comprise all species that shed their leaves outside the growing season. This group was divided into herbaceous and woody deciduous species. Semi‐deciduous species were defined as all woody species that shed some of their leaves outside the growing season, depending on its length and severity, and evergreen species, all woody species that maintain their leaf canopy year round.

Table 1.

List of species considered in this study and several of their traits

Species    Family Evolutionary history Leaf habit Life form Photosyn‐thetic pathway Habitat
Acer opalus Mill. subsp. granatense (Boiss.) F.Q. & Rothm. Aceraceae E WD MP C3 R
Ailanthus altissima (Mill.) Swingle Simaroubaceae NE WD MP C3 RS
Amaranthus blitoides S. Watson Amaranthaceae NE HD Th C4 AF
Amaranthus retroflexus L. Amaranthaceae NE HD Th C4 AF
Anagyris foetida L. Fabaceae NE WD NP(MP) C3 MS
Arbutus unedo L. Ericaceae NE E MP C3 OF
Atriplex halimus L. Chenopodiaceae NE E NP C4 SM
Avena sativa L. Poaceae C HD Th C3 AF
Avenula crassifolia (F.Q.) Holub Poaceae E HD Th C3 R
Beta vulgaris L. Chenopodiaceae NE HD H(Th) C3 AF
Brassica napus L. Brassicaceae C HD Th C3 AF
Brassica oleracea L. Brassicaceae C HD Ch C3 AF
Capparis spinosa L. Capparidaceae C WD NP C3 AF
Capsicum annum L. Solanaceae C HD Th C3 AF
Cephalaria squamiflora (Sieber) Greuter subsp. balearica (Willk.) Greuter Dipsacaceae E E Ch. C3 R
Ceratonia siliqua L. Caesalpiniaceae C E MP C3 AF
Cistus albidus L. Cistaceae NE SD NP C3 MS
Cistus monspeliensis L. Cistaceae NE SD NP C3 MS
Cistus salviifolius L. Cistaceae NE SD NP C3 MS
Cneorum tricoccon L. Cneoraceae NE E NP C3 MS
Convolvulus arvensis L. Convolvulaceae NE HD H(G) C3 AF
Crepis triasii (Camb.) Nyman Asteraceae E E H C3 R
Cichorium intybus L. Asteraceae NE HD H C3 AF
Chenopodium album L. Chenopodiaceae NE HD Th C3 AF
Datura stramonium L. Solanaceae NE HD Th C3 AF
Delphinium pictum Willd. Scrophulariaceae E HD Th C3 MS
Dianthus rupicola Biv. subsp. bocchoriana L. Llorens & Gradaille Caryophyllaceae E E Ch C3 R
Dittrichia viscosa (L.) Greuter Asteraceae NE WD NP C3 AF
Euphorbia margalidiana Kühbier & Lewej. Euphorbiaceae E E NP(Ch) C3 RC
Euphorbia pithyusa L. Euphorbiaceae NE E Ch C3 MS
Ficus carica L. Moraceae C WD MP C3 AF
Fraxinus angustifolia Vahl Oleaceae NE WD MP C3 FWS
Globularia cambessedesii Willk. Globulariaceae E E Ch C3 R
Helianthus annus L. Asteraceae C HD Th C3 AF
Helleborus foetidus L. Ranunculaceae NE E Ch C3 MS
Helleborus lividus Ait. Ranunculaceae E E Ch C3 MS
Hypericum balearicum L. Hypericaceae E E NP C3 MS
Hypericum hircinum L. subsp. cambessedesii (Coss. ex Barceló) Sauvage Hypericaceae E WD NP C3 FWS
Lactuca sativa L. Asteraceae C HD Th C3 AF
Lavandula dentata L. Lamiaceae NE E Ch C3 MS
Lavatera cretica L. Malvaceae NE HD NP(Ch) C3 AF
Ligusticum huteri Porta Apiaceae E E Ch C3 R
Limonium migjornense L. Llorens Plumbaginaceae E E Ch C3 SM
Lycopersicum esculentum Mill. Solanaceae C HD Th C3 AF
Olea europaea L. var. sylvestris (Mill.) Brot. Oleaceae NE E MP C3 MS
Paeonia cambessedesii Willk. Paeoniaceae E HD G C3 MS
Pastinaca lucida L. Apiaceae E HD H C3 MS
Phlomis italica L. Lamiaceae E SD Ch C3 MS
Phillyrea latifolia L. Oleaceae NE E MP C3 MS
Pinus halepensis Mill. Pinaceae NE E MP C3 MS
Pistacia lentiscus L. Anacardiaceae NE E MP C3 MS
Pistacia terebinthus L. Anacardiaceae NE WD MP C3 MS
Pisum sativum L. Fabaceae C HD Th C3 AF
Populus alba L. Salicaceae NE WD MP C3 FWS
Populus nigra L. Salicaceae NE WD MP C3 FWS
Pteridium aquilinum (L.) Kuhn Hypolepidaceae NE HD G C3 OF
Quercus coccifera L. Fagaceae NE E NP(MP) C3 MS
Quercus ilex L. Fagaceae NE E MP C3 OF
Quercus humilis Mill. Fagaceae NE WD MP C3 OF
Rhamnus alaternus L. Rhamnaceae NE E P(Ch) C3 MS
Rhamnus ludovici‐salvatoris R. Chodat Rhamnaceae E E P(Ch) C3 MS
Rosa agrestis Savi Rosaceae NE WD NP C3 MS
Silene mollissima (L.) Pers. Caryophyllaceae E E Ch C3 R
Solanum melongena L. Solanaceae C HD Th(Ch) C3 AF
Solanum tuberosum L. Solanaceae C HD G C3 AF
Sorghum bicolor (L.) Moench Poaceae C HD Th C4 AF
Trifolium subterraneum L. Fabaceae C HD Th C3 AF
Triticale sp. Poaceae C HD C3 AF
Urginea maritima (L.) Baker Liliaceae NE HD G C3 MS
Urtica atrovirens Req. ex Loisel. subsp. bianorii (Knoche) F.Q. & Garcias Urticaceae E HD Th C3 MS
Verbascum sinuatum L. Scrophulariaceae NE HD H C3 AF
Vicia faba L. Fabaceae C HD Th C3 AF
Viola x balearica Rosselló, Mayol & Mus Violaceae E E H C3 R
Viola jaubertiana Marès & Vigin Violaceae E E H C3 R
Viola stolonifera J.J. Rodr. Violaceae E E H C3 MS
Vitex agnus‐castus L. Verbenaceae NE WD MP C3 RC
Vitis vinifera L. cv Manto Negro Vitaceae C WD P C3 AF
Zea mays L. Poaceae C HD Th C4 AF
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Evolutionary history: E, endemic species; NE, non‐endemic species; C, crops. Leaf habit: HD, deciduous herbaceous; WD, woody deciduous; SD, semi‐deciduous; E, evergreen. Life form: P, phanerophyte; NP, nano‐phanerophyte; MP, macro‐phanerophyte; Ch, chamaephyte; G, geophyte; H, hemi‐cryptophyte. Photosynthetic pathway: C3 or C4. Habitat: RC, rocky coast; SD, sandy dunes; SM, saltmarshes; MS, Mediterranean shrub‐land; OF, oak forests; R, rupicolous; AF, agricultural fields; FWS, freshwater streams; RS, roadsides.

Similarly, three evolutionary groups were distinguished: crops, endemic and non‐endemic species. Crop species are those currently being farmed. Endemic species are defined as those with a distribution limited to the Balearic Islands, with the addition of Delphinium pictum and Acer opalus ssp. granatense. Delphinium pictum also occurs on Corsica and Sardinia, and is considered a Balearic–Tyrrhenic species (Contandriopoulos and Cardona, 1984), and A. opalus ssp. granatense also occurs in the south‐east of the Iberian Peninsula and in North Africa, and is considered an Ibero‐Magrebi‐Balearic species (De Bolòs et al., 1993). A classification of the species according to life form, following Raunkiaer (1934), is provided (Table 1).

All plants were field‐grown except Quercus humilis, which was grown outdoors in 90 l pots. The study was carried out in 1999 and 2000 on the island of Mallorca, in the western Mediterranean basin, with dry, hot summers and cool winters. The mean annual precipitation varies from 300 mm on the southern coast, to above 1000 mm in the north‐western mountains, and the rain falls mainly from autumn to spring. The drought period lasts for 2–6 months, with considerable variation between sites and years.

Gas exchange and nitrogen content measurements

Leaf gas exchange rates were measured when water availability was not limiting and maximum photosynthetic rates were expected. That was mostly in spring and, in a few cases, autumn. Measurements were made on well‐ developed sun‐exposed leaves of healthy plants using a Li‐6400 infra‐red gas‐exchange analyser (Li‐Cor Inc., Lincoln, NE, USA). To avoid the midday depression of photosynthesis, measurements were made during mid‐morning on sunny days. Cuvette temperatures were set at levels approximating the air temperature on each sampling occasion. Light intensity was held constant at 1500 µmol photons m–2 s–1 to ensure light‐saturated photosynthesis, and the CO2 partial pressure was set to 360 µmol mol–1. The gas‐exchange parameters were obtained by direct measurements of net CO2 assimilation rate per unit leaf area (A), and computations of stomatal conductance (g), sub‐stomatal CO2 concentration (Ci) and intrinsic water use efficiency (A/g) were based on conventional formulae (von Cammerer and Farquhar, 1981). Single leaves on six to eight different individuals per species were sampled. After measurements, they were collected and the projected one‐sided fresh area was measured using an AM‐100 area meter (Analytical Development Co., Hoddesdon, UK). After drying for 48 h at 70 °C, the SLA was calculated as the ratio of leaf area to dry mass. From A and SLA values, Am was calculated as the CO2 fixed per unit time per unit leaf dry mass. Because the photosynthetic rates were measured at near optimum conditions, they should approach the maximum photosynthetic capacity of the species under field conditions.

Total Nm was determined in the same leaves as those measured for Am, using an elemental analyser (model EA 1108; Carlo Erba Instruments, Milan, Italy). After drying, the leaves of each species were pooled, and the N content was measured as the average of two analyses per sample. The nitrogen data are shown both on a mass (Nm) and area (Na) basis.

Statistical analysis

All the parameters (A, g, Ci, A/g, SLA, Am, Nm and Na) were analysed by a multifactor ANOVA using the multiple range test of statgraphics (Manugistics, 1998). Least square means of the effects and their standard errors were calculated according to Searle (1971) and Snedecor and Cochran (1980), using a linear model that included the effects of evolutionary history (endemic, non‐endemic and crop) and leaf habit (herbaceous deciduous, woody deciduous, semi‐deciduous and evergreen). Regression adjustments and the interaction between factors were analysed by multiple regression techniques (Draper and Smith, 1981), using the multiple regression procedure of statgraphics (Manugistics, 1998).

All these methods solve models with unbalanced data, which cannot be solved by crude means. Least square means yield values of the dependent variable for every level of each factor from an orthogonal decomposition of the information. This means that, for instance, least square means for leaf habit are calculated as if all the individuals had the same evolutionary history.

RESULTS

Effects of leaf habit and evolutionary history on leaf traits

Means and the standard error of all the variables studied for each species are available on the Annals of Botany website [Supplementary Information; http://aob.oupjournals. org]. A first analysis of the variance including the three evolutionary histories revealed that most of the parameters differed significantly (data not shown). However, post hoc tests showed that the differences among evolutionary histories were due only to the differences between crops and the other two groups (not shown). A second analysis excluding crops revealed that all the studied parameters except Ci and Na differed significantly among leaf habits (Table 2). By contrast, no parameter differed significantly among endemic and non‐endemic species. However, for some parameters, in spite of the lack of significance, the differences were not negligible. For instance, A averaged 18·2 µmol CO2 m–2 s–1 in non‐endemic species, but only 15·5 µmol CO2 m–2 s–1 in endemic species, which is proportionally the same difference as that observed between non‐endemic species and crops (20·9 µmol CO2 m–2 s–1). Also, g, SLA and Na differed by 25 % between endemic and non‐endemic species. In addition, the analysis revealed a significant interaction between leaf habit and evolutionary history for A, g, SLA, Am and Nm (Table 2). This implies that some of the differences observed among leaf habits are modulated by evolutionary history.

Table 2.

Effect of leaf habit, evolutionary history and their interaction (LH × EH) on net CO2 assimilation rate on an area basis (A), stomatal conductance (g), sub‐stomatal CO2 concentration (Ci), intrinsic water use efficiency (A/g), specific leaf area (SLA), net CO2 assimilation rate on an mass basis (Am), leaf nitrogen content on a mass basis (Nm) and leaf nitrogen content on an area basis (Na)—only P values are shown

A g C i A/g SLA A m N m N a
Leaf habit <0·001 <0·001 0·20 0·02 <0·001 <0·001 <0·001 0·78
Evolutionary history 0·11 0·15 0·80 0·79 0·09 0·93 0·52 0·06
LH × EH 0·06 0·02 0·47 0·14 0·02 0·01 0·01 0·50
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Table 3 shows mean values and their standard errors of all the studied parameters for each interaction among leaf habit and evolutionary history. Clearly, the effect of evolutionary history was most marked in herbaceous deciduous species. Within this group, strong differences were observed between endemics and both non‐endemics and crops in A, g, A/g, Am and Nm. No effect of evolutionary history was observed in semi‐deciduous and woody deciduous species, except that SLA tended to be higher in endemic species. Nevertheless, it should be noted that the small number of species in some of these interactions may affect the significance of the differences observed for some parameters. Within evergreen species, there was no effect of evolutionary history in either A, g, Ci, A/g or Na. However, there was a strong effect of SLA, which was involved in strong effects in both Am and Nm (Table 3).

Table 3.

Mean values and their standard error (when more than one species was available) for all the parameters studied (abbreviations as in Table 2) for each possible combination of leaf habit and evolutionary history

Group No. of species A g C i A/g SLA A m N m N a
Herbaceous deciduous endemic 5 15·6 ± 1·3a 294·2 ± 45·9a 230·4 ± 6·3a 57·0 ± 5·8b 143·6 ± 25·4a 230·9 ± 48·3a 29·2 ± 4·6a 2·0 ± 0·1a
Herbaceous deciduous non‐endemic 10 20·8 ± 2·0b 625·4 ± 106·5b 239·3 ± 7·3a 43·5 ± 6·9ab 178·7 ± 19·7a 393·8 ± 57·2b 38·5 ± 4·0ab 2·6 ± 0·4a
Herbaceous deciduous crops 13 21·7 ± 1·3b 608·3 ± 60·1b 241·8 ± 4·6a 37·7 ± 2·9a 185·3 ± 10·1a 405·1 ± 32·1b 47·6 ± 1·3b 2·6 ± 0·1a
Woody deciduous endemic 2 12·4 ± 5·0a 210·9 ± 98·7a 228·6 ± 2·4ab 62·3 ± 5·2a 210·0 ± 33·2b 280·3 ± 146·4a 34·4 ± 1·7a 1·7 ± 0·2a
Woody deciduous non‐endemic 9 19·0 ± 1·1a 321·3 ± 32·3a 213·7 ± 3·9a 62·1 ± 2·9a 107·7 ± 9·8a 204·6 ± 15·2a 28·2 ± 1·6a 2·7 ± 0·3a
Woody deciduous crops 3 19·8 ± 4·0a 461·1 ± 157·7a 237·0 ± 8·3b 48·2 ± 8·5a 140·3 ± 15·6a 276·9 ± 52·1a 33·5 ± 6·9a 2·3 ± 0·7a
Semi‐deciduous endemic 1 20·0a 419·3a 238·0a 48·6a 90·8a 182·1a 20·9a 2·3a
Semi‐deciduous non‐endemic 3 20·1 ± 2·2a 421·9 ± 74·3a 249·3 ± 26·8a 54·3 ± 17·3a 79·9 ± 5·7a 163·4 ± 12·2a 19·6 ± 0·7a 3·2 ± 0·6a
Evergreen endemic 14 14·0 ± 0·7a 246·7 ± 25·5a 227·5 ± 6·6a 62·0 ± 4·1a 132·0 ± 18·1c 185·2 ± 25·3c 28·4 ± 2·4b 2·4 ± 0·3a
Evergreen non‐endemic 12 12·7 ± 1·3a 201·6 ± 35·1a 212·3 ± 9·3a 77·7 ± 6·6a 75·3 ± 8·1b 101·8 ± 21·3b 18·0 ± 1·6a 2·4 ± 0·2a
Evergreen crops 1 13·2a 277·5a 241·3a 48·2a 39·6a 52·4a 14·3a 3·6a
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Values within the same evolutionary history group with a different superscript letter differ at P < 0·05.

As expected, comparing leaf habits, evergreen species were more clearly separated from the other three groups, showing 30–40 % lower A and g values and a significantly higher A/g (Table 3).

Relationships between leaf traits

Figure 1 shows that the 73 C3 species fitted a single positive curvilinear relationship between g and A (r = 0·91, P < 0·001). The endemic species lay mainly in the linear part of the regression, as did most of the typical Mediterranean species. Only some crops and weeds (Beta, Chenopodium, Cychorium, Datura, Lavatera and Verbascum) were in the saturated part of the regression (i.e. at g above 0·6 mol H2O m–2 s–1).

graphic file with name mcg123f1.jpg

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Fig. 1. Relationship between net photosynthetic rate on an area basis (A) and stomatal conductance (g). Filled circles correspond to non‐endemic species, empty squares to endemic species and filled triangles to crops. Values correspond to means of six to eight replicates. The curve of best fit is shown as a hyperbolic adjustment (A = 4·80 + 35·75g/(0·62 + g); (r2 = 0·75). C4 species were excluded from the relationship.

Considering all the species, Am and Nm were positively correlated with SLA (not shown). However, endemic species showed a significant (P < 0·05), somewhat reduced, Am for high SLA (Fig. 2). According to a covariance analysis of the regression coefficients, the slopes of Am–Nm relationships differed marginally (P = 0·07) between endemic and non‐endemic species (Fig. 2). By contrast, crop relationships were closer to the general ones observed in non‐endemics. The five C4 species were also close to the general pattern described for the 73 C3 species (Fig. 2), but some of them showed a slightly higher Am than expected for their Nm and SLA. The five species included here may not be enough to determine whether the whole C4 species group shares the same regression pattern as the C3 species. On an area basis, A showed no significant correlation with Na (r = 0·22, n.s.).

graphic file with name mcg123f2.jpg

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Fig. 2. Relationship between log net photosynthetic rate on a mass basis (Am) and log specific leaf area (SLA) (A), and log Am and log leaf nitrogen content on a mass basis (Nm) (B). Filled circles correspond to non‐endemic species, empty squares to endemic species, filled triangles to crops, and empty triangles to C4 species. Regression fits are shown as solid lines (non‐endemic), short dashed lines (crops) and long dashed lines (endemic). For non‐endemic species, log10 Am = 1·41 log10 SLA – 0·60 (r2 = 0·84) and log10 Am = 1·56 log10 Nm + 0·06 (r2 = 0·77). For crops, log10 Am = 1·25 log10 SLA – 0·24 (r2 = 0·84) and log10 Am = 1·46 log10 Nm + 0·15 (r2 = 0·79). For endemic species, log10 Am = 0·99 log10 SLA + 0·17 (r2 = 0·79) and log10 Am = 1·37 log10 Nm + 0·29 (r2 = 0·69). C4 species were not included in regressions. Values corres pond to means of six to eight replicates.

DISCUSSION

Differences in photosynthetic capacity between Balearic endemic and non‐endemic species

On average, endemic species showed a 20 % lower net photosynthetic capacity on an area basis than non‐endemics and crops. Baruch and Goldstein (1999) and McDowell (2002) have reported similar results in Hawaii and Oregon, respectively. In the study by Baruch and Goldstein (1999), native species had a 30 % lower net CO2 assimilation than invasive species. These differences were even larger (50 %) in a comparison of two invasive and two non‐invasive Rubus species (McDowell, 2002). It is noticeable that the differences observed in the present study are of a similar order of magnitude, regardless of the fact that only a few of the species studied exhibit invasive behaviour.

Although Balearic endemics also had a lower stomatal conductance than the other evolutionary groups, the similarity of the average Ci for all the groups suggests that reduced g was not the cause of photosynthetic limitation, but rather a consequence of it (Wong et al., 1979). Therefore, it is likely that a non‐stomatal factor is responsible for the lower photosynthetic capacity of endemics. Possibilities include a higher mesophyll resistance in endemics than in other species (i.e. a larger difference between Ci and the actual CO2 concentration in the chloroplasts), a reduced Rubisco content, activity and/or specificity factor, and/or higher respiration rates.

A higher mesophyll resistance in woody plants than in herbs, and in sclerophylls than in mesophytes, has been reported (Lloyd et al., 1992; Evans and von Caemmerer, 1996). However, the effects of leaf habit were taken into account in our statistical analysis, and thus cannot be responsible for the observed differences between endemics and non‐endemics. Mesophyll resistance of endemic species has not been evaluated, so this possibility should be addressed in future studies.

Variations in the Rubisco specificity factor, i.e. the relative affinity of Rubisco for CO2 and O2, have been reported for C3 plants. A few Balearic endemic species have been analysed in this regard. Their specificity factor is 15–20 % lower than that for other common species (Delgado et al., 1995) which, according to the model of Laing et al. (1974), would result in 10–20 % less CO2 assimilation in endemic species, consistent with the present observations. The Rubisco specificity factor would need to be determined for a larger number of endemic and non‐endemic species to confirm this trend.

Respiration rates were determined in only one endemic species, Rhamnus ludovici‐salvatoris (Gulías et al., 2002). This has twice the respiration rate of its relative R. alaternus. Similar results were observed by McDowell (2002) in Rubus species. Further studies are needed to elucidate the role of each of these possible limitations to photosynthesis in Balearic endemic species.

Interactions between leaf habit and evolutionary history in photosynthetic capacity and related parameters

Besides the overall differences between endemic and non‐endemic species, most of these differences were found within the herbaceous deciduous group. The high proportion of rupicolous species within the endemics could have been responsible for this, since this type of species has evolved in a resource‐limiting environment. Nevertheless, no significant differences were found for any parameter between rupicolous and non‐rupicolous endemic species in a separate ANOVA (data not shown). Another possible explanation for the observed differences between endemic and non‐endemic herbaceous deciduous species is a differential specialization for habitat among the two groups. While a high proportion of the non‐endemic herbaceous deciduous species usually live in ruderal areas, only a few endemic species share this kind of habitat. This fact could account for the higher photosynthetic capacity and nitrogen content of the former, which could be the result of adaptation to a high‐resource habitat.

Endemic species showed lower SLA than non‐endemic species in the herbaceous deciduous group, but this was higher in all the other leaf habit groups. Similarly, SLA for invasive and non‐invasive species yielded opposite results in the studies of Baruch and Goldstein (1999) and McDowell (2002).

Leaf trait relationships: ecological implications

A highly significant hyperbolic correlation was obtained between A and g (Fig. 1), consistent with other reports using a single species (Farquhar et al., 1987) or various species (Field and Mooney, 1986). Most of the typically Mediterranean species lay on the linear part of the A–g relationship (i.e. the region of highest A/g) suggesting that low water availability in a Mediterranean climate has exerted an important evolutionary pressure on both endemic and non‐endemic species.

The present data clearly support the general correlation between Nm, Am and SLA described by Reich et al. (1997) for six biomes and different plant life forms (Fig. 2). Even the slopes of the regressions among these parameters were similar to those described by Reich et al. (1997). Leaf habit does not modify these general relationships, as described by Reich et al. (1997, 1999).

As expected, crops had higher Am and lower A/g than the other groups because they have been selected to maximize plant production but not to improve the efficiency of resource use (Boyer, 1982, 1996). Despite these differences, crops lay close to the general relationships between Am, Nm and SLA, in agreement with the hypothesis of Reich et al. (1999) that no species can improve Am without increasing SLA, due to biophysical limitations. Similar results were observed by Schulze et al. (1994).

Endemic species, and some of them in particular, did not follow the general relationships between SLA, Nm and Am (Fig. 2). The differences between endemic and non‐endemic species were maximal at high SLA and Nm, whereas the reduced number of existing endemic species with low SLA and Nm precludes the establishment of clear differences in that region of the relationship. These differences may imply that a higher proportion of the leaf biomass is made up of non‐photosynthetic compounds and structures in the endemics than in non‐endemics, which could be a consequence of the prevailing conditions during the evolution of these species. If endemic species were evolving under low niche competition, as commonly observed on islands (Cox and Moore, 1993), a low photosynthetic capacity would not be as unfavourable as it is under high competitive pressure. On the other hand, the reduced competitive ability of endemics could be a consequence of devoting high amounts of resources to the synthesis of defensive compounds, a likely consequence of evolution under (a well‐described) high pressure by herbivores on these islands (Bover and Alcover, 2000). Indeed, high photosynthetic nitrogen‐use efficiency has been related to a high nitrogen investment in photosynthetic compounds and to a high Rubisco specific activity (Poorter and Evans, 1998).

Competition among plants may have increased due to the introduction of continental plant species by humans (Burjachs et al., 1994; Yll et al., 1994). Owing to their lower competitive ability (among other possible factors), the distribution of endemic species should have been reduced since humans arrived on the islands. Indeed, there is palynological evidence to show that some of the genera that are now extinct or that have a very narrow distribution were widespread before humans arrived on the islands (Burjachs et al., 1994; Yll et al., 1994). Remarkably, some of the endemic species with a more restricted distribution (namely Acer, Ligusticum, Paeonia or Rhamnus ludovici‐salvatoris) actually fall in the lower part of the A–SLA relationship. A similar situation can be found at present in Hawaii, where invasion of plant species is much more recent. In these islands, native species have been shown to have some disadvantageous traits compared with invasive species, which means that they are less able to capture resources efficiently and have a lower growth capacity (Pattison et al., 1998; Baruch and Goldstein, 1999; Durand and Goldstein, 2001).

Concluding remarks

Prior to the present study, different plant traits that were related to a low competitive ability, and resulted in a shrinking distribution range of these species, were suggested to be present in species endemic to islands. Among these traits, pollination and seed dispersal limitations have been suggested (Givnish, 1998). Also, it has been suggested that species endemic to islands synthesize fewer chemical defences (Carlquist, 1970), although the opposite has been proposed as well (Bohm, 1998). Recently, Hawaiian native species have been shown to have lower Am and SLA than invasive ones, and this has been related to their lower competitive and invasive ability (Baruch and Goldstein, 1999). The present results support the hypothesis that photosynthetic capacity is another important factor contributing to the limited distribution of some endemic species. Moreover, the similarity of the present results and those reported in Hawaii, a group of islands recently invaded by alien species and with a tropical climate, suggests a convergence pattern of photosynthetic traits in native species on islands.

The observed differences between endemic and non‐endemic species support the hypothesis presented here that evolution in a low competitive environment may allow the occurrence of species with a low Am for a given SLA. According to the ecological interpretation of Reich et al. (1999), these leaf traits may be disadvantageous for competition with other plant species, suggesting a possible cause for the decline in the distribution of many Balearic endemic species after the introduction of allochthonous species (Alomar et al., 1997). Interestingly, characters negatively affecting competition have also been described in animals endemic to islands (Sondaar, 1977; McNab, 1994), including the extinct Balearic bovid Myotragus (Alcover et al., 1999; Bover and Alcover, 1999).

SUPPLEMENTARY INFORMATION

Mean values of gas exchange parameters (net CO2 assimilation rate on an area basis, stomatal conductance, sub‐stomatal CO2 concentration, intrinsic water use efficiency and net CO2 assimilation rate on an mass basis), specific leaf area and leaf nitrogen content (on a mass and on an area basis) for each species are available on the Annals of Botany website (http://aob.oupjournals.org).

ACKNOWLEDGEMENTS

We thank Dr E. Descals (IMEDEA, CSIC‐UIB) and Dr S. Jonasson for grammatical corrections, and Dr. A. Traveset and Dr. P. B. Reich for helpful discussions.This work is part of Project CICYT PB97‐1174, supported by the Spanish Ministry of Education and Science. J.F. was granted a ‘Beca d’Investigació’ by the UIB. J.G. was supported by grants awarded to Project FEDER IFD97‐0551.

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Received: 23 September 2002; ; Returned for revision: 17 December 2002. Accepted: 13 April 2003    Published electronically: 12 June 2003

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