Relationship between the Al Resistance of Grasses and their Adaptation to an Infertile Habitat
1 UMR 1248 Agir, INRA-ENSAT, BP 52627 Auzeville, 31326 Castanet-Tolosan, France
2 UMR UJF-CNRS 5553, Laboratoire d'Ecologie Alpine, Université J. Fourier, BP 53 X, 38041 Grenoble, France
* For correspondence. E-mail bertoni{at}ensat.fr
Received: 7 December 2006 Returned for revision: 2 January 2007 Accepted: 5 February 2007
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Background and Aims: Original data on Al resistance, relative growth rate and leaf traits of five European grasses as well as literature data on Al resistance, habitat preference and traits of grasses were considered to determine whether (a) Al resistance is correlated to a growth conservative strategy and (b) species occurrence could be useful to assess Al toxicity in meadows on acid soils.
Methods: The Al resistance of 15 species was represented by the Al activity in nutrient solution that resulted in a 50 % decrease in root length, {Al3+}50, or, for published values, in root or plant biomass. The correlations between Al resistance and acidity or nitrogen indices and the correlation between Al resistance and selected traits (relative growth rate, leaf dry matter content, specific leaf area and leaf thickness) were calculated. Principal component analysis was used for the characterization of the relationships between Al resistance and measured traits.
Key Results: The {Al3+}50 values of the resistant species Molinia caerulea and Sieglingia decumbens were 13 and 26 µM {Al3+}50, respectively. The known Al resistance of 15 species that were mainly of the intermediate strategy competitor–stress tolerator–ruderal (C-S-R) type and of the S type was correlated with Ellenberg's nitrogen and acidity indices. For the whole set of species, the correlation between Al resistance and traits was not significant.
Conclusion: The Al resistance of the C-S-R species was variable and independent of their traits. S-type species, adapted to acid soils and with traits of conservative strategy, displayed Al resistance. The large difference in Al resistance between grasses may help assess Al soil toxicity by using the abundance of grasses.
Key words: Grassland, plant functional traits, acid soils, Al resistance, grasses, Arrhenatherum elatius, Festuca rubra, Helictotrichon sulcatum, Molinia caerulea, Sieglingia decumbens
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Soil acidity, as defined by a topsoil pH value below 5·5, is observed in about 37 % of the soils in Europe (von Uexküll and Mutert, 1995). It develops under wet climates in northern Europe as well as in the forests and grasslands of the mountain ranges (Falkengren-Grerup and Tyler, 1993; Baize and Roque, 1998; Austrheim et al., 2005). This natural phenomenon limits plant growth, decreases the diversity of grassland species and selects species which are generally lower yielding (Tyler, 1996; Roem and Berendse, 2000; Austrheim et al., 2005). The acidification is promoted by the geological substratum and enhanced by acid rains and ammonium fertilizers.
In organic acid soils, the acidity due to H+ ions is, by itself, harmful to plants (Kidd and Proctor, 2001). However, in mineral acid soils, the indirect adverse effects of acidity prevail with Al, Mn and Fe toxicity, and P, Ca, Mg, and K deficiency (von Uexküll and Mutert, 1995). Among these adverse effects, Al toxicity, as measured by its chemical activity {Al3+}, is often predominant (Hocking, 2001). Al activity is near zero above pH 5·5 and increases markedly from pH 5·0 to pH 4·1 over the range 1–150 µM (Kinraide, 1991, 2003). It is influenced by Ca and Mg concentrations (Kinraide, 2003) and by Al ligand concentrations, particularly phosphates, sulfates and the anionic forms of soluble organic acids (Ritchie, 1995). Al activity in the soil solution and Al toxicity are thus difficult to assess through the determination of the usual parameters measured in soil analysis. In most cases, the Al toxicity hazard is estimated through the measurements of soil pH value, exchangeable Al concentration and Al/Ca ratio in the soil solution (Houdijk et al., 1993; Roem and Berendse, 2000). Al activity in the soil solution is rarely determined or calculated (Kidd and Proctor, 2001; Schöttelndreier et al., 2001; Kinraide, 2003).
Plant resistance to Al toxicity (Kochian et al., 2005) has been measured by the Al activity {Al3+}50 for which above ground or root biomass (Wheeler et al., 1992; Wheeler, 1995) or root length (Wright et al., 1987; Kinraide, 2003) is decreased by 50 %. The variability in Al resistance between grasses ranges from 1 to 50 µM {Al3+}50 (Wenzl et al., 2001). However, the {Al3+}50 value is known only for a small number of meadow grasses of the temperate zone: for the resistant species Agrostis capillaris ({Al3+}50 >30 µM), Festuca rubra and Holcus lanatus ({Al3+}50 10–20 µM), for the moderately sensitive species Dactylis glomerata, Festuca arundinacea, Lolium spp. ({Al3+}50 approx. 5 µM) and for the sensitive species ({Al3+}50 <2 µM) such as Bromus spp., Cynosurus cristatus, cultivars of Lolium perenne, Poa pratensis and Phleum pratense (Wheeler et al., 1992; Wheeler, 1995). Besides, an intraspecific variability in the resistance to Al was observed in rye grass and orchard grass (1–5 and 2–10 µM {Al3+}50, respectively; Wheeler 1992, 1995). Intraspecific variabilities, without any mention of the corresponding {Al3+}50 values, were reported in Yorkshire fog (Kidd and Proctor, 2001) and in fescues (Liu et al., 1996).
The numerous observations on the adaptation of some grass species to soil acidity were synthesized in Ellenberg's acidity indices (Ellenberg et al., 1992). Low values (1–3) of the acidity index correspond, with few exceptions, to species whose pH optimum can be assumed to be below 5·5, i.e. lying in the potential range of Al toxicity (Schaffers and Sykora, 2000). However, a precise correspondence between tolerance to soil acidity (using Ellenberg's indices) and resistance to Al does not appear to have been ascertained.
To our knowledge, since the investigations of Wheeler (1995), neither the Al resistance potential of other grasses of the temperate zone nor the possible links between tolerance to acid soils and resistance to Al have been further investigated. Likewise, the possible link between resistance to Al and adaptation to infertile soils (conservation strategy vs. capture strategy) has not been investigated. The assumption is that Al-resistant grasses are, in the first place, adapted to limited nutrition conditions. The adaptation to infertile soils can be represented by Ellenberg's nitrogen index which is issued from the classification of observed niches and is well correlated to species productivity (Schaffers and Sykora, 2000). Functional traits that are characteristic of the species strategy (Reader, 1998; Wilson et al., 1999; Ansquer et al., 2004), relative growth rate (RGR), specific leaf area (SLA), leaf dry matter content (LDMC) and leaf thickness (LT) were also considered. The aim of the investigations reported here was to analyse the relationships between resistance to Al and these indices and traits so as to ascertain a diagnosis of the extent of Al toxicity from the occurrence of various grass species in acid grasslands.
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MATERIALS AND METHODS |
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Growth conditions and quantification of Al resistance
The grasses to be studied were chosen in relation to their occurrence in moderately acidic soils of grasslands in the Central Pyrenees (1°17'E, 42°51'N, 600–900 m a.s.l.). The abundance of the grass species was determined in three acidic stands with infertile soil and potential Al toxicity (stands 1, 2 and 3) and in a less acidic and slightly more fertile stand with no Al toxicity (stand 4). The disturbance induced by the defoliation pressure increased from stand 1 (only mowed once or twice a year) to stands 2 and 3 (two foliage removals by mowing and grazing) and to stand 4 (three foliage removals: mowed, grazed and re-grazed). To give an index of the fertility differences between the stands, the nitrogen nutrition was measured on the first cut: the hay was dried (80 °C, 48 h), weighed, ground, and analysed for total N content (CHN 2000 analyser, Leco, St Joseph, MI, USA). The nitrogen nutrition index (NNI), expressed as a percentage of the optimum nutrition, was then calculated according to Lemaire and Gastal (1997). The pH (soil water ratio 1 : 2·5, v/v) and the Al exchangeable content (cobaltihexamine method; Orsini and Remy, 1976) were measured at 0–5 cm soil depth. The abundance was measured according to Daget and Poissonet (1971) and expressed as the percentage of the abundance of the grasses (n = 2–4 replications by stand).
When Al resistance was unknown, the Al resistance of the abundant species was quantified in nutrient solution culture in a growth chamber. One cultivated species, L. perenne (Lp) ‘Clerpin’, and one wild ecotype of F. rubra were taken as sensitive and resistant controls, respectively. Seeds of the seven wild grasses were collected in their native habitat: Arrhenatherum elatius, F. rubra, Helictotrichon sulcatum (Gay) Pilger, C. cristatus, D. glomerata, Molinia caerulea and Sieglingia decumbens.
Growth conditions
Surface-sterilized and vernalized seeds were germinated for 1 or 2 weeks, depending on the species, on wet filter paper in Petri dishes. After germination, 12–20 uniform seedlings of each species were sorted in four lots. Each lot of 3–5 plants was taken as one experimental unit. When the principal root length was 1 ± 0·5 cm, the seedlings were transferred into the different nutrient solutions, with or without Al, in a growth chamber with the following conditions: day, 14 h, photosynthic photon flux density at mean plant height 260 µmol m–2 s–1 of PAR (photosynthetically active radiation), temperature 25 °C, relative humidity approx. 70 %; night, 10 h, temperature 18 °C. The species were cultivated in trays floating on four 48 L tanks corresponding to the four Al treatments. The same experimental protocol was time-replicated three times.
Low ionic strength nutrient solutions simulated an infertile acid soil solution according to Wenzl et al. (2003). The composition of the nutrient solution (pH 4·2) was as follows (in µM): 100 NO3, 10 NH4, 60 Ca, 30 Mg, 60 K, 1 P, 100 S, 6 B, 5 Fe, 1 Zn, 1 Mn, 0·2 Cu, 5 Si, 5 H2EDTA, 0·001 Mo, 160 Na. Al was added at concentrations of 0 (control), 40, 80 and 160 µM of acidified AlCl3, corresponding to 0, 22, 43 and 83 µM {Al3+}. These values correspond to the range of {Al3+} expected in temperate acid soils (Wright et al., 1987). The solutions were continuously aerated and renewed every 3 d in order to minimize variations in the concentration of the nutrients. The HCl concentration (55·4 µM) was adjusted in order to obtain a pH value of the solution in the range 4·2 ± 0·1. The activity of Al3+ was calculated with GEOCHEM 2·0 (Parker et al., 1987) by using the constants of stability of Nordstrom and May (1989) and the solubility constants of Al (OH)3 mentioned by Kinraide and Parker (1989).
Quantification of Al resistance
Seedlings were harvested after 14 (species with a high RGR) or 21 d (species with a low RGR) of growth at the different Al concentrations. They were separated into roots and shoots. Roots were stained with a 1 % (v/v) dilution of a methyl violet stock solution (1 g 100 mL–1 ethanol) and scanned with a flatbed scanner. The WinRhizo software (Regent Instruments Inc., Quebec, Canada) was used to obtain the overall length of roots. The data of the three successive replications for each species and treatment were pooled for calculations. Relative root elongation (RRE) of the plants treated with Al and the activity {Al3+}50 at which RRE was reduced to 50 % of the control were adapted from Wenzl et al. (2001). Briefly, RRE and {Al3+}50 were calculated as follows:
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is the mean root length at the highest level of Al, and RL0 is the mean root length in the control solution (0 µM Al). RRE values for C. cristatus (sensitive to Al), L. perenne and D. glomerata (moderately sensitive) were taken as control values. The response of RRE to {Al} was fitted to a Weibull equation as suggested by Kinraide and Parker (1989):
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The activity {Al3+}50 at which RRE was reduced to 50 % of the control was calculated from a and b empirical values according to the formula:
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As the {Al3+} values tested (22–83 µM) were high, the calculations were not suitable for sensitive species with low {Al3+}50 values (1–6 µM {Al3+}50) such as C. cristatus, D. glomerata and L. perenne.
Leaf traits and RGR measurement
Leaf dry matter content and specific leaf area were measured on the same species. For each species, samples of 5–15 tillers (n = 5–12 samples) developed under sunlight conditions were harvested in the field during May–June, in acidic meadows (pH 4·7–6·6) of Ariège (Central Pyrenees, France). Each tiller was cut at its base and immediately plunged into a test tube filled with water in order to avoid wilting. LDMC and SLA measurements were made following the protocol described by Garnier et al. (2001) and Cornelissen et al. (2003) evaluating water-saturated blades (excluding sheaths) on the youngest fully expanded leaf of the tiller. Leaf thickness (LT) was calculated from measured SLA and LDMC according to Vile et al. (2005).
RGR was measured on the species presenting some Al resistance: A. elatius, F. rubra (taken as a control), H. sulcatum, M. caerulea and S. decumbens. The young plants were cultivated in nutrient solution in a growth chamber with climatic conditions as previously described. The composition of the nutrient solution was as follows (in µM): 450 NO3, 150 NH4, 800 Ca, 200 Mg, 350 K, 50 P, 1000 S, 6 B, 5 Fe, 1 Zn, 1 Mn, 0·1 Cu, 0·1 Mo. The solution was renewed every 10 d. Holes in the Styrofoam cover of the 48 L tanks received bungs with three homogeneous seedlings of each species. RGR was measured using a fresh weight method adapted from Causton (1991). Each bung was removed from the tank, blotted dry, weighed, and then replaced in the solution. By this means, the fresh weight of the same unit of three plants could be monitored throughout the experiments. Let the fresh weight of the sample at date ti be Wi; RGR was calculated as follows:
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As species differed in growth rate, RGR was calculated over a period when the different species had a similar total dry weight (between 100 and 450 mg dry weight per plant) and yielded high RGRs. Values are the mean of three independent replications of RGR measurement except for H. sulcatum (two replications).
Al–traits relationships
In order to gain an insight on a greater number of species (15 species), the Al–traits relationships were studied using a collection of values published by other authors in addition to measured values on five species from this study. Published values of {Al3+}50 are scarce. Data issued from long-term measurement of {Al3+}50 on shoot biomass, which had been suggested to be in accordance with those on root biomass (Wheeler et al., 1992), were found in Wheeler et al. (1992) and Wheeler (1995). When a range of resistance was known for a species, the value used was the median value of the resistance range. For the other species, the estimated {Al3+}50 value was used. The {Al3+}50 value of D. flexuosa was estimated from growth data and nutrient concentrations of Rorison (1985), using GEOCHEM 2·0.
Published values of traits were collected in Poorter and Remkes (1990), Hunt and Cornelissen (1997), Meziane and Shipley (1999), Poorter and de Jong (1999), Ryser and Urbas (2000), Ryser and Wahl (2001), Taub (2002), Al Haj Khaled et al. (2005) and Sugiyama (2005). Ellenberg indices were obtained from Ellenberg et al. (1992). Details are given in Table 3.
Statistics
One-way (species) analysis of variance of RRE was performed with the StatBox 2·0 statistical package (Grimmersoft, Paris, France) on log-transformed data at each level of Al. Significant differences between means refer to the probability level of 0·05 by Newman and Keuls's bilateral test. For {Al3+}50 estimation, the Weibull function was fitted using the non-linear square procedure in R software 1·9·0 (Ihaka and Gentleman, 1996). The standard error s.e. {Al3+}50 was calculated according to Wenzl et al. (2001). Significance of the {Al3+}50 values refers to the unilateral comparison to the 0 value (t-test; n = 12; A. elatius, n = 11).
Relationships between {Al3+}50 and traits were tested with the linear correlation coefficient r. For the overview of {Al3+}50 and traits relationships, principal component analysis (PCA) was performed on the correlation matrix of the selected variables using R 1·9·0. Groups of species in the first plane of the PCA were distinguished using a distance analysis based on Ward's criteria.
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RESULTS |
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Ranking of Al resistance
In the acidic stands 1, 2 and 3, with Al toxicity hazard, A. capillaris, F. rubra and H. sulcatum were always more abundant than in the control stand 4 (Table 1). Molinia caerulea, S. decumbens and B. pinnatum were observed only in the acidic stand 1. Conversely, the species that were abundant in the control plot with no Al toxicity hazard (D. glomerata, H. lanatus and L. perenne) were scarce or absent in the acidic stands. The number of grass species in the acidic stands was rather restricted in comparison with the control plot. Thus, the abundances of the grasses may be related to the Al toxicity hazard of the stands.
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In nutrient solution culture, the {Al3+} 22 µM level (Fig. 1A) was highly toxic to the controls C. cristatus and D. glomerata (RRE 2 and 5 %, respectively). In contrast, S. decumbens and M. caerulea displayed a markedly higher relative growth (59 and 38 %, respectively). The growth of L. perenne ‘Clerpin’ (11 %), A. elatius (20 %), F. rubra (25 %) and H. sulcatum (35 %) was intermediate. The {Al3+} 43 µM level (Fig. 1B) allowed two groups of species to be distinguished: sensitive (RRE below 3 %: C. cristatus, D. glomerata and L. perenne cv. Clerpin) and resistant species (RRE ranging from 11 to 38 %: F. rubra, S. decumbens, M. caerulea and H. sulcatum). Arrhenatherum elatius (11 %) was intermediate.
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When the response of RRE to {Al3+} was fitted to a Weibull function, the resistance of M. caerulea and S. decumbens was corroborated with calculated activities {Al3+}50 of 13 and 26 µM (Table 2). Higher data variability and/or a lower {Al3+}50 value resulted in non-significant {Al3+}50 values for A. elatius, F. rubra and H. sulcatum. Most of the resistant species (H. sulcatum, S. decumbens and M. caerulea and the red fescue ecotype selected as a control) displayed traits that are characteristic of a conservation strategy (low SLA, high LDMC, low RGR; Table 2). Arrhenatherum elatius, with a high SLA, a median LDMC value and a relatively low RGR, presented traits of an intermediate strategy between capture and conservation.
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Relationships with plant functional traits
For all the species whose acidity index was expressed numerically, the resistance to Al was correlated negatively to the acidity index (H index; Table 3). The grasses that are most resistant to Al were referenced as resistant to acidity (H index 2–6) or indifferent to acidity (H index x). Conversely, the species with an H index of 7–8 are weakly resistant to Al. However, large discrepancies are observed for the species listed as indifferent to acidity (H index x) which include species that are sensitive to Al (C. cristatus and P. pratensis), as well as species that are moderately sensitive (D. glomerata and P. pratense) or resistant (H. lanatus and M. caerulea). The negative correlation between N index and Al resistance reflects the low N index (2–3) of the resistant species (D. flexuosa, M. caerulea and S. decumbens) and the high N index (6–7) of some sensitive grasses (D. glomerata, L. perenne, P. pratense and P. pratensis). However, the relationship is rather loose: for example, the Al-susceptible species C. cristatus and B. inermis had the same moderate N index (4–5) as the resistant species H. lanatus and A. capillaris.
As the traits are correlated between themselves (SLA – LDMC, r = –0·77, P = 0·01; SLA – LT, r = –0·83, P = 0·001; LDMC – LT = 0·33, non-significant) and the nitrogen index is correlated to SLA (0·63, P = 0·05) and LDMC (–0·74, P = 0·01), a PCA was carried out on a selection of less redundant variables: {Al3+}50, LDMC, LT and RGR (Fig. 2). Axis 1 separates capture strategy species (right) and conservation strategy species (left). Axis 2 opposes Al-susceptible (bottom) to Al-resistant (top) species. This distribution pattern underlines the independence between Al resistance (represented on axis 2) and functional traits (represented on axis 1).
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The datum points corresponding to the grass species constitute five main groups. Species with low RGR and high LDMC (group 1) are on the whole more resistant than species with high RGR and low LDMC (group 4). However, A. capillaris with capture strategy traits is resistant to Al (group 2), whereas B. inermis, C. cristatus, P. pratensis and F. arundinacea with traits of intermediate strategy between capture and conservation (group 5) are sensitive to Al. Helictotrichon sulcatum and A. elatius (group 3) are intermediate between group 1 and group 4.
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DISCUSSION |
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Ranking of Al resistance
The slow growth of C. cristatus, L. perenne and D. glomerata in the presence of 22 µM Al is in agreement with their high sensitivity ({Al3+}50 0–6 µM; Wheeler et al., 1992). The resistance of M. caerulea is consistent with its occurrence on acid soils with high Al/Ca ratios (Houdijk et al., 1993). The Al resistance of S. decumbens appears to be in agreement with observations of Antuna et al. (1980) in acid soils and with the resistance of the related species Danthonia linkii (Crawford and Wilkens, 1997). To our knowledge, there are no data on the Al resistance of A. elatius, H. sulcatum and the {Al3+}50 value of these species in the literature. The value obtained for the F. rubra ecotype (9 µM) used as a control is lower though compatible with the range (10–20 µM {Al3+}50) previously defined by Wheeler et al. (1992).
Stand 1 displayed an exchangeable Al rate (4·5 cmol (+) kg–1; Table 1) which was intermediate between the values associated with low (2·8) and high (7·2) Al toxicity by Curtin and Smillie (1986). In spite of the acidity (pH 5·2), the much lower exchangeable Al values (0·7 and 0·2, respectively) of stands 2 and 3 suggest a very low level or the absence of Al toxicity in these stands. The absence of the species B. pinnatum, M. caerulea and S. decumbens in stands 2, 3 and 4 may be related to their low ability to withstand increased defoliation (disturbance indices of M. caerulea and B. pinnatum 0·10, S. decumbens 0·24; Grime et al., 1988). The increase in fertility from stand 1 (NNI 39 %, Table 1) to stands 2 and 3 (NNI 58 %) and to stand 4 (NNI 64 %) may also give a competitive advantage to the species with the higher relative growth rate, as shown for H. lanatus and L. perenne by Mountford et al. (1993). Thus, increasing disturbance and competition may contribute to the exclusion of the relatively slower growing species B. pinnatum, M. caerulea and S. decumbens in stands 2, 3 and 4, and to the reduced abundances of A. capillaris, F. rubra and H. sulcatum in stand 4.
Taking into account the Al resistance values of H. sulcatum, M. caerulea and S. decumbens (Table 2) and those of A. capillaris, F. rubra and H. lanatus (Wheeler et al., 1992), the resistant grass species in the stands with Al toxicity hazard and in the control, represented up to 90 and 30 % of the observed grasses, respectively (Table 1). Al resistance variability at the ecotype level limits the possibility of diagnosis of Al toxicity which would be based upon the presence of a particular species (e.g. H. lanatus; Kidd and Proctor, 2001). However, an analysis based upon the presence or absence of several species might be more reliable. The assesment of the Al toxicity hazard through the abundance of the Al-resistant grasses had the advantage of taking into account simultaneously 5–6 grass species that represented the majority of the grass species in acidic stands (Table 1). The knowledge of the Al resistance of the two other grasses investigated (Anthoxanthum odoratum, estimated optimum pH 4·0–6·0; Brachypodium pinnatum, estimated optimum pH 5·5–6·5; Antuna et al., 1980; Grime et al., 1988) might improve this approach.
Relationships with plant functional traits
For the species with known RGRs, the trait values obtained here are in good agreement with those reported previously (A. elatius 214, F. rubra 196; Hunt and Cornelissen, 1997). Likewise, the proposed SLA values are close to those expected for observations on infertile soils (A. elatius 35–37, F. rubra 13–15, M. caerulea 21–24; Poorter and de Jong, 1999). The LDMC value of A. elatius is in general agreement with that reported previously (218; Al Haj Khaled et al., 2005).
As the species listed as indifferent to acidity (H index x) by Ellenberg were not included in the calculation of the correlation, the agreement between Al resistance and the acidity index is overestimated. In fact, the species C. cristatus, D. glomerata, P. pratense and P. pratensis, listed as indifferent to acidity, appear actually to be susceptible to Al. The discrepancy may be accounted for in terms of occurrence of these species in slightly acidic grasslands with low Al activity, as a result of soil parent rock and/or organic matter content. From these discrepancies between H index and Al resistance and the loose negative correlation between resistance to Al and Ellenberg's nitrogen index, it can be concluded that Ellenberg's indices are only moderately useful to evaluate Al resistance of grasses.
The range of variation of traits in plants is much wider than that observed on these C3 grasses (SLA 2–50, LDMC 100–600, LT 200–1200, Shipley et al., 2005; RGR 100–380, Poorter and Van der Werf, 1998). As a result, the independence between resistance to Al and traits may be due to the limited range of trait variation taken into account in considering C3 grasses only. The consideration of other plant groups such as C4 grasses, herbs, shrubs and trees might improve the relationships.
The absence of relationships between Al resistance and traits can also be accounted for in terms of data classification into several groups of species with differing Al resistance and traits (Fig. 2). Group 1 species include S-type species (D. flexuosa, M. caerulea and S. decumbens) and the polymorphic species F. rubra (C-S-R, S, C or S-C) which all exhibit a resistance to Al. Although the subject is little documented in the literature, a physiological mechanism allowing these S-type species simultaneously to adapt to infertile soils and to become resistant to Al can be considered. As a matter of fact, in D. flexuosa, the exudation of dicarboxylic anions such as malate is involved in a higher efficiency of P uptake in infertile soils (Tyler and Ström, 1995) and in a higher resistance to Al toxicity in acid soils (Schöttelndreier et al., 2001). The distribution of F. rubra and M. caerulea in acid soils and in calcareous soils (Grime et al., 1988) also suggests the involvement of an exudation capacity for di- or tri-carboxylic anions (Tyler and Ström, 1995). However, as the exudates of group 4 grasses and S-type grasses remain insufficiently documented, the assumption cannot be generalized.
Species groups 2, 4 and 5 correspond to C-S-R type species with regard to their ecological strategies (A. capillaris, C. cristatus, D. glomerata, H. lanatus, L. perenne, P. pratense and P. pratensis; Grime et al., 1988). Their Al resistance is different between groups and in some cases within the same group (H. lanatus vs. L. perenne, group 4). The comparison of the traits of the Al-resistant species of groups 2 and 4 (A. capillaris and H. lanatus) with those of the Al-resistant species (D. flexuosa, F. rubra, M. caerulea and S. decumbens) of group 1 suggests that low RGR, low SLA and high LDMC are not causally related to Al resistance. It may be in accordance with the implication of a limited number of genes in Al resistance, as suggested by Delhaize et al. (2004), with little or no relationship to global traits.
The usually low fertility (N, P) of acid soils may account for conservation strategy traits in Al-resistant species of group 1 which exhibit the highest LDMC and the lowest RGR values. These species occur in reduced abundance in more fertile and more disturbed stands. Conversely, the Al-resistant species H. lanatus exhibits capture strategy traits (with the highest SLA and RGR values) and presents a limited abundance in the infertile soils. The limited abundances of A. capillaris on stands 1 and 4 may deserve further attention. In conclusion, Al resistance alone cannot explain the relative abundance of Al-resistant grasses in infertile or fertile acid soils. As Al-resistant species have to compete with other grasses, their abundance depends, in the first place, on their adaptation to the fertility level and to the disturbance of the habitat and, only in the second place, on their Al resistance.
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ACKNOWLEDGEMENTS |
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We thank Eric Lecloux for field work and laboratory assistance. We thank Yves Rauzy (Chambre d'Agriculture de l'Ariège, Foix, France) for the establishment of stand 1, Pauline Ansquer, Rauda Al Haj and Stephanie Gaucherand for communicating unpublished trait data, Michel Duru (INRA, Toulouse, France) and Daniel Sayag (ENSA, Toulouse, France) for critical review of the typescript. David R. Parker (University of California, Riverside) kindly provided us with GEOCHEM 2·0 software. V.P. received a grant from the Iranian Ministry of Science, Research and Technology.
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LITERATURE CITED |
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