AOBPreview originally published online on August 5, 2002
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Annals of Botany 90: 337-343, 2002
© 2002 Annals of Botany Company
Soil Cations Influence Bryophyte Susceptibility to Bisulfite
,11 Department of Biological Sciences, Imperial College at Silwood Park, Ascot, Berkshire SL5 7PY, UK
* For correspondence. Fax +44 (0)207 584 2339, e-mail j.bates{at}ic.ac.uk Present address: Department of Crop Physiology, Assam Agricultural University, Jorhat-785013, Assam, India.
Received: 29 January 2002; Returned for revision: 25 March 2002; Accepted: 31 May 2002 Published electronically: 5 August 2002
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ABSTRACT |
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The hypothesis that metal ions absorbed by bryophytes from the underlying soil may ameliorate adverse effects of SO2 was investigated in the terricolous moss species Pleurozium schreberi (Brid.) Mitt. and Rhytidiadelphus triquetrus (Hedw.) Warnst. Dilute sodium bisulfite solutions (equivalent to dissolved SO2) were applied to shoots isolated from soil or in contact with artificial substrata. Marked inhibition of net photosynthesis was observed within 2 h of treatment with 0·3 mM bisulfite in both mosses. Progressive recovery of net photosynthesis occurred 2–8 h after bisulfite treatment, although the extent of this depended on the concentration and pH of the solution. When R. triquetrus and P. schreberi were grown on artificial substrata (calcareous, acid-mineral or acid-organic) with weekly bisulfite applications, the only significant effect was poorer growth of P. schreberi receiving bisulfite on the calcareous and acid-organic substrata. In both species, growth on the calcareous substratum led to increased concentrations of exchangeable Ca2+, whereas exchangeable Fe3+ concentrations increased following growth on the acid-mineral soil. In another experiment the two mosses were pre-treated with either Ca2+ or Fe3+ before incubation with bisulfite. In P. schreberi, the depression of net photosynthetic rate caused by bisulfite was ameliorated from 33 to 64 % of the control by pre-treatment with Fe3+, but it was unaffected by Ca2+ pre-treatment. In R. triquetrus, the amelioration caused by Fe3+ pre-treatment was from 16 to 60 % of the control, but pre-treatment with Ca2+ gave a greater amelioration, to 75 % of the control value. The responses are discussed in terms of soil preferences of the mosses and possible underlying bisulfite amelioration mechanisms.
Key words: Bryophytes, SO2 pollution, bisulfite, amelioration, calcicoly, Ca2+, Fe3+, Pleurozium schreberi, Rhytidiadelphus triquetrus
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INTRODUCTION |
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Bryophytes appear to be at least as sensitive to the major atmospheric pollutants as the much more intensively studied lichens (Bates, 2000, 2002). The pollutant responses of bryophytes that grow on soil (i.e. terricolous), however, have received only modest attention (e.g. Winner and Bewley, 1978; Longton, 1985). This is particularly so if one discounts studies of the pollutant susceptibilities of Sphagnum mosses growing on peat in ombrotrophic mires (e.g. Lee and Studholme, 1992).
It has long been known (Gilbert, 1968, 1970) that bryophytes and lichens growing directly on alkaline masonry show enhanced tolerance to SO2. In solution, SO2 exists in three main ionic forms, viz. sulfite (SO32–), bisulfite (HSO3–) and undissociated sulfurous acid (‘H2SO3’). Sulfite increasingly predominates above pH 6, bisulfite predominates at pH 2–4, whereas sulfurous acid appears as a minor component at pH 4 and dominates the mixture only at pH 1 and below (Saunders and Wood, 1973). Alkaline (usually calcium carbonate-rich) substrata presumably neutralize deposited acids and push the ionic equilibrium for SO2 dissolving in the surface water film towards sulfite, the least harmful of the three ionic forms. More direct ameliorative effects upon physiology may also be brought about by metal ions derived from the substratum. In the lichen Umbilicaria muhlenbergii, Ca2+ and some related metals may protect cell membranes and reduce the binding affinity of pollutant ions (Nieboer et al., 1979; Richardson et al., 1979). Baxter et al. (1989a, b, 1991a, b) demonstrated an alternative ameliorating effect of Fe3+ and other transition metals on SO2 inhibition of photosynthesis and growth in Sphagnum. Fe3+ held on the cell wall cation-exchanger of the peat–moss passively oxidized phytotoxic bisulfite solutions to harmless sulfate. Similar passive protection against SO2 by extracellular Fe3+ has been observed in epiphytic lichens (Miszalski and Niewiadomska, 1993), though the relatively SO2-tolerant lichen Xanthoria parietina may also be capable of metabolically based oxidation of the pollutant (Silberstein et al., 1996). Other amelioration mechanisms, so far only reported in higher plants, include oxidation by peroxidases present in the mesophyll apoplast and photoreduction of the pollutant and its loss from the plant as H2S (for a review, see Legge and Krupa, 2002).
Farmer et al. (1992) pointed out that the terricolous mosses Rhytidiadelphus triquetrus and Hylocomium splendens had become restricted to calcareous soils in the area affected by atmospheric pollutants around London, UK, whereas they grow on acid soils in unpolluted areas. Although terricolous mosses are believed to be reliant mainly upon wet deposition for inputs of mineral nutrients, there is compelling evidence that elements that are abundant in the soil are also accumulated in the shoots (Bates and Farmer, 1990; Büscher et al., 1990; Bates, 1992). When R. triquetrus was transplanted from calcareous downland to acid soil near London, it continued to thrive, suggesting that its restriction to alkaline soils had come about earlier when atmospheric SO2 concentrations were much higher than they are today (Bates, 1993).
The present paper investigates the hypothesis that accumulation of metal ions from soils by terricolous mosses is important in ameliorating SO2 toxicity. Two species are compared, Rhytidiadelphus triquetrus (Hedw.) Warnst., which appears to be restricted to calcareous soils in polluted areas, and the widespread calcifuge Pleurozium schreberi (Brid.) Mitt. The effects on these mosses of SO2 are considered in interaction with two metal ions, Ca2+ and Fe3+, which, it was hypothesized, would be available to mosses predominantly on calcareous and acid-mineral soils, respectively.
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MATERIALS AND METHODS |
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Plant material
The robust pleurocarpous mosses Pleurozium schreberi (Brid.) Mitt. and Rhytidiadelphus triquetrus (Hedw.) Warnst. were compared in this study. Around London (UK), R. triquetrus is now largely restricted to calcareous soils, whereas P. schreberi, a strict calcifuge, remains frequent on acid soils in this region (Bates, 1993). P. schreberi was collected from acid, sandy loam soil under grassland and scrub at Silwood Park, Berkshire (UK National Grid Reference SU9468). R. triquetrus was collected from a chalk rendzina soil under grassland in the Chiltern Hills, Oxfordshire (UK National Grid Reference SU7093).
Material was brought back to the laboratory in polythene bags and maintained in a metabolically active condition in one of two ways. In summer, the shoot wefts were spread on horticultural capillary matting within plastic propagators closed with clear plastic lids and kept permanently hydrated by daily spraying with double-distilled water (DDW). They were maintained in a growth cabinet at 20 °C with 18 h daylight provided by fluorescent strip lamps giving a mean intensity of 37 µmol PAR (photosynthetically active radiation) m–2 s–1. In winter, the fragments of moss colonies were kept moist and healthy by arranging them densely in open-topped plastic seed trays located on the ground under moderate natural shade from shrubs outside the laboratory at Silwood Park.
Bisulfite application
Bisulfite solutions have been used in several studies with mosses in place of gaseous SO2 (e.g. Inglis and Hill, 1974; Ferguson and Lee, 1979; Okoloko and Bewley, 1982). This approach has the advantage that the concentration received by the mosses is reasonably certain, although there is considerable uncertainty in equating particular solution concentrations of bisulfite to amounts of gaseous SO2 exposure. The bisulfite concentrations used (0·3, 0·6, 1·0 mM) are based on those employed in the studies mentioned above and in more recent work (e.g. Baxter et al., 1989a, b; Miszalski and Niewiadomska, 1993). Bisulfite solutions oxidize rapidly; fresh stocks and working solu tions were therefore prepared daily using standard grade NaHSO3 (S-9000, Lot 90 H 0658, Sigma Aldrich Co. Ltd, Gillingham, UK).
Where effects on photosynthesis were being investigated, the samples of shoots were incubated in 20 cm3 bisulfite solution for 0·5–2 h, but this was not possible without severely disturbing the plants in the cultivation experiment and so the solutions were applied by means of a small hand sprayer. A control treatment involving an equivalent incubation or spray application of DDW was used in the majority of experiments.
Chemical analysis
Cations within the moss shoots were separated into exchangeable and intracellular fractions using a sequential elution procedure (Bates, 1992; Badacsonyi et al., 2000). Samples of 20 hydrated apices were placed in 100 x 25 mm glass specimen tubes (‘master’ tubes) paired with identical (‘slave’) tubes to which extractants could be added, and linked to them via fine plastic tubes. Solutions were added and withdrawn from the master tubes using a manifold system attached to a reversible pump, and during incubations the samples were agitated by bubble streams and kept at 20 °C. Freely soluble ions on the shoots were removed with three serial incubations (each 10 min, 20 cm3) with DDW. Exchangeable cations held on the fixed negative charges of the cell walls were eluted by two treatments (each 1 h, 20 cm3) with 25 mM SrCl2 (Bates, 1982) or 30 mM NiCl2 (Wells and Brown, 1987). The shoots were oven-dried (80 °C) and weighed. Elements that had been located within the protoplasts (intracellular fraction) were solubilized by digestion with concentrated nitric acid. Cations were determined in the various extracts after addition of lanthanum chloride (7·2 mM La) as a releasing agent using a Thermo Jarrel Ash S12 atomic absorption/emission spectrophotometer (Thermo Elemental, Franklin, MA, USA). Element concentrations are expressed in terms of the oven-dry weights of the shoots. This technique proved effective for K+, Ca2+ and Mg2+, but Fe3+ remained too firmly bound to the cell walls to be fully eluted by Sr2+ or Ni2+ and therefore we report only total Fe3+ concentrations.
Measurement of photosynthesis
Rates of net photosynthesis and dark respiration (results not reported) of the samples of the moss shoots after exposure to the various experimental regimes were routinely determined using an infra-red gas-analyser (IRGA) (ADC Series 225 model; Analytical Development Co. Ltd, Hoddesdon, UK) employing a sample injection method (Larson and Kershaw, 1975). The saturated shoots were lightly blotted to remove excess surface water and placed on moistened filter paper in Perspex assimilation chambers (volumes 98–117 cm3). These were flushed through with air of known CO2 concentration [usually 360 volumes per million (v.p.m.), at 1200 cm3 min–1 for 1 min] by means of inlet and outlet ports that could quickly be stoppered, and sealed at time zero. The chambers were immersed in a water bath at 20 °C during incubation. For net photosynthesis, a light intensity of 222·5 µmol m–2 s–1 was employed, which is about 10 % higher than the saturating intensity for Scleropodium purum (Bharali, 1999) and Brachythecium rutabulum (Kershaw and Webber, 1986), two other mosses from similar habitats with which we have been working (Bharali, 1999). An incubation period of 10 min was used. Immediately afterwards, a 5 cm3 air sample was taken from the chamber using a hypodermic syringe through a stoppered port. This was injected into a CO2-free air-stream via a stoppered port in the external pipework linking the ‘reference’ and ‘sample’ tubes of the IRGA, and sample peak height determined on a chart recorder. After incubation the moss sample was oven-dried at 80 °C and weighed. Net photosynthesis results are expressed as volumes per million CO2 absorbed per gram oven-dry moss per hour (v.p.m. CO2 g–1 h–1).
Incubation experiments
Three short-term experiments were devised to investigate effects of bisulfite on net photosynthetic rates in the two moss species and to study the ameliorating effects of metals on bisulfite depression of photosynthetic rate. The moss samples were incubated directly in the solutions during these experiments and the manifold system described above was used to add and withdraw solutions.
Experiment 1.
Samples of ten 20 mm shoot segments of P. schreberi and R. triquetrus were incubated in 20 cm3 of 0·3, 0·6 or 1·0 mM NaHSO3 for 30 min and then separated from the pollutant solution. The shoots were kept fully hydrated on moist filter paper in Petri dishes at 20 °C and under normal laboratory lighting conditions until measurements of net photosynthesis were made (from 2 to 10 h after the start of incubation).
Experiment 2.
To investigate the effects of varying ratios of the different ionic forms of dissolved SO2 on terricolous mosses, samples of ten 20 mm shoot apices of P. schreberi and R. triquetrus were incubated in 20 cm3 of 0·3 mM NaHSO3 buffered (to pH 3, 4, 5 and 6) with citric acid for 30 min at 20 °C. After removal of the solutions the shoots were kept fully hydrated on moistened filter paper in Petri dishes at 20 °C under normal laboratory lighting. Photosynthetic rate was again determined at periods from 2 to 10 h after the start of incubation.
Experiment 3.
To investigate the importance of two metal cations (Ca2+, Fe3+) in reducing the damaging effects of bisulfite on terricolous bryophytes, shoot samples of P. schreberi and R. triquetrus were pre-incubated in 20 cm3 CaCl2 (0·6 mM), FeCl3 (0·6 mM) or Na2-EDTA (5·0 mM) for 2 h at 20 °C under normal laboratory lighting. The aim of the metal treatments was to increase the saturation of the cell wall cation-exchanger (see Bates, 2000) with either Ca2+ or Fe3+, whereas treatment with the chelating agent Na2-EDTA aimed to remove as much of the natural exchangeable content of these cations as possible (see also Bates, 1982). The samples were then post-treated with NaHSO3 (0·6 mM, 20 cm3) for 2 h at 20 °C, equal to the time between the start of incubation and the first photosynthesis measurements in incubation experiments 1 and 2, and equal to the duration of the pre-treatments. These treatments were all applied under normal room lighting. Net photosynthesis was determined immediately after incubation.
Cultivation experiment
In the cultivation experiment elongation growth of the main axis was used as an indicator of gametophore performance (Russell, 1988). Samples of 20 mm shoot apices were cut and randomly assigned to the various treatments. At the end of the experiment the total length of the main axis was determined and the growth increment calculated.
To investigate the modifying effects of substratum type on bisulfite sensitivity, samples of 20 mm shoot apices (n = 20) of P. schreberi and R. triquetrus were inserted vertically into the surface layer of three types of substratum (calcareous, acid-mineral, acid-organic; see below) contained within plastic plant pots. A factorial experiment was designed: species x soil type x pollutant treatment, although species results were analysed separately at the conclusion of the experiment as there were large interspecific differences. The shoots were maintained for 50 d in plastic propagators at full hydration in a controlled environment (20 °C, 18 h daylight, mean PAR of 37 µmol m–2 s–1). Once a week, shoots were treated by spraying with either DDW or unbuffered sodium bisulfite solution (0·3 mM). Shoots were sprayed once with DDW on other days. At the end of the experiment the elongation growth of the shoots was measured and their Ca2+, Mg2+, K+ and Fe3+ concentrations were determined.
Three substrata were used: calcareous, acid-mineral and acid-organic. Horticultural limestone chippings (pH 7·5) were used for the calcareous substrate. For the acid-mineral substrate, natural sandy-loam soil beneath grassland at Silwood Park was mixed 1 : 1 (v/v) with horticultural peat (pH 4·0), and the acid-organic substrate consisted entirely of horticultural ‘moss’ peat (pH 3·9). Plastic pots (70 mm high, tops 80 x 80 mm) were filled with the above substrata and 20 shoot apices (20 mm long) of either P. schreberi or R. triquetrus were inserted vertically (growing points upwards) a few millimetres into the surface layer of the substratum to provide moss–soil contact and anchorage. The pots were carefully sprayed with pollutant solutions for 2 min and maintained in propagators in the growth cabinet as described above. There were three replicate blocks (= propagators) in this experiment.
Statistical analyses
Data were analysed by randomized blocks or factorial ANOVA using the GLIM computer program (version 3·77, update 1; Royal Statistical Society, London).
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RESULTS |
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Incubation experiments
Experiment 1.
The photosynthetic rates of the untreated mosses are shown at 0 h. In both moss species the depression of photosynthesis was proportional to the concentration of bisulfite used, with a greater initial depression at the lowest concentration (0·3 mM) in R. triquetrus than in P. schreberi (Fig. 1). The highest bisulfite concentration (1 mM) caused a complete cessation of net photosynthesis 2 h after treatment started in both mosses. However, in both species, and at all bisulfite concentrations, there was evidence of progressive photosynthetic recovery after the initial depression. The extent of recovery 10 h after treatment was inversely proportional to the initial bisulfite concentration.
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Experiment 2.
In general, the photosynthetic depression observed at 2 h was greater the lower the pH of the bisulfite solution (Fig. 2). The differences were smaller in P. schreberi than in R. triquetrus where the effect at pH 6 was less than half that caused at pH 3. Recovery from initial inhibition of photosynthesis was slightly stronger in R. triquetrus than in P. schreberi.
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Experiment 3.
Following pre-incubation with DDW and post-incubation with bisulfite, the rate of photosynthesis in P. schreberi was reduced to only one-third that in the controls (Table 1). The rate was similarly reduced following pre-treatment with Na2-EDTA or CaCl2 solution. However, following pre-incubation with FeCl3, a much smaller depression of photosynthesis was observed.
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An even greater reduction in photosynthesis (to 16 % of control) was observed in R. triquetrus pre-incubated with DDW and post-incubated with NaHSO3 (Table 1). This did not differ significantly from the photosynthetic rate of plants pre-treated with Na2-EDTA. However, in sharp contrast to the situation in P. schreberi, pre-incubation with CaCl2 markedly reduced photosynthetic depression by bisulfite. Pre-incubation with FeCl3 also strongly ameliorated the bisulfite depression of photosynthesis, but not as effectively as CaCl2 pre-treatment.
Cultivation experiment
Although appreciable shoot elongation occurred (Table 2) during the experiment, the repeated applications of sodium bisulfite did not significantly inhibit growth. Only in the case of P. schreberi was a significant (interaction) effect of substratum type observed: growth of shoots receiving NaHSO3 applications was significantly poorer on the calcareous and acid-organic substrata than on the acid-mineral soil. Nevertheless, the substratum treatments caused significant changes in the levels of major cations in the tissues (Table 3). Greatly elevated concentrations of exchangeable Ca2+ were detected in both species on the calcareous substratum, while Mg2+ concentrations were often lower on the calcareous substratum than on the acid substratum in both the exchangeable and intracellular fractions, and a similar picture was obtained for exchangeable K+. Concentrations of total Fe3+ in the shoots were significantly higher on the acid-mineral soil than on the other two substrata. No effects of the bisulfite treatments upon cation levels were detected, nor were there any significant interactions.
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DISCUSSION |
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There is a marked disparity between the results showing substantial inhibition of photosynthesis as a result of short-term bisulfite exposure of the mosses, and those indicating little effect of the pollutant on longer-term growth. In a cultivation experiment (not reported here; see Bharali, 1999), single applications of sodium bisulfite solution had little effect on the growth of a range of different terricolous mosses even though their shoots had no contact with the substratum and its available cation pool. Cations previously derived from the native soil and carried over on the cell wall exchanger (e.g. Bates and Farmer, 1990; Bates, 1993), however, may have been sufficient to ameliorate the effects of single bisulfite applications. In the cultivation experiment presented here (Table 2), even repeated weekly pollutant treatments had little deleterious effect, possibly because here the moss shoots were also in contact with various substrata containing potentially available ameliorating solutes. From these results we conclude that the short-term photosynthetic depression caused by bisulfite is normally quickly reversed, and probably without lasting cellular injury or growth reduction.
The recovery of net photosynthesis observed at all bisulfite concentrations in Fig. 1 and at some bisulfite acidities in Fig. 2 points to the presence of detoxification or repair mechanisms in these mosses. The possibility of metabolic detoxification of SO2 by oxidation to SO42– was suggested at an early stage in the tolerant epiphytic moss Dicranoweisia cirrata (Syratt and Wanstall, 1969) but has not been verified. Puckett et al. (1974) showed that an SO2-sensitive lichen, Umbilicaria muhlenbergii, has the ability to recover from several repeated short exposures to aqueous forms of the pollutant before suffering total photosynthetic collapse. In this case the recoveries were less complete when the experiment was repeated at low temperature. Thus, metabolic detoxification mechanisms may be present in some cryptogams.
Cultivation of moss shoots in contact with three artificial substrata under laboratory conditions led to some marked shifts in their cation contents (Table 3). On the calcareous substratum, the exchangeable Ca2+ concentration was boosted by a factor of six in both Pleurozium schreberi and Rhytidiadelphus triquetrus, whereas exchangeable and intracellular Mg2+ were reduced in P. schreberi. A reciprocal relationship between these two cations has been demonstrated in several earlier studies, apparently the result of competitive displacement on the cell wall cation-exchanger (e.g. Bates, 1989). On the acidic substrata, the most notable changes were an increased total Fe3+ concentration in both mosses on the acid-mineral soil and a slightly lowered intracellular K+ content of R. triquetrus on both acid substrata. Only one significant bisulfite x substratum interaction effect was noted in this experiment (Table 2): growth of P. schreberi was significantly higher on the acid-mineral soil than on the other two substrata. This result is consistent with the hypothesis that an enhanced Fe3+ uptake from the acid-mineral soil (Table 3) ameliorates bisulfite toxicity in P. schreberi.
By analogy with other recent studies (Baxter et al., 1989a, b, 1991a, b; Miszalski and Niewiadomska, 1993), it appears likely that the recovery of net photosynthesis in the terricolous mosses, following an initial depression, is related to progressive loss of the bisulfite from the incubation solution and/or water free space of the hydrated tissues. This might involve transformation (oxidation or reduction) of the bisulfite to a harmless form or could involve uptake and metabolism within the moss tissues. The incubation experiment in which pre-treatment with Fe3+ strongly ameliorated the photosynthetic decline caused by bisulfite treatment in P. schreberi and R. triquetrus (Table 6) is indicative of passive, external oxidation of the bisulfite, as proposed by Baxter et al. (1989a, b, 1991a, b) in Sphagnum. In nature, R. triquetrus, unlike P. schreberi, is seldom found on strongly acid soils where the potentially high mobility of Fe3+ would enable significant accumulations of the ion on its cation-exchanger. It is therefore interesting to discover that Ca2+ pre-treatment caused an even greater amelioration of the bisulfite-induced photosynthetic depression in R. triquetrus than Fe3+. In contrast, the ameliorating effect of Ca2+ in the calcifuge P. schreberi was negligible. Importantly, amelioration in R. triquetrus appears to be an effect of the Ca2+ ion (CaCl2 solution was used) rather than of its carbonate. The latter is normally at the heart of the pH-mediated interactions that characterize the chemistry of calcareous soils.
As Ca2+ does not readily undergo changes in oxidation state and could not directly oxidize bisulfite, it is most likely to be exerting an influence on cell membrane function in the mosses. In a study of 42K+ uptake by two terricolous liverworts, Jefferies et al. (1969) observed that increasing the external Ca2+ (as chloride or sulfate) concentration from 0·1 mM to 3·0 mM stimulated the rate of 42K+ influx into the calcicole Leiocolea turbinata but partially inhibited the process in the calcifuge Cephalozia connivens. They proposed that the configuration of the specific protein that carries K+ through the plasmalemma is sensitive to the concentration of other ions in the external solution and, in particular, responds in opposite ways in these two species to the presence of Ca2+. In a similar vein, studies of epilithic calcicole and calcifuge bryophytes revealed a greater tendency of calcicoles to leak intracellular K+ when challenged with acid solutions (Bates, 1982). The latter author postulated that growth on calcareous substrata ensures that the water free space of the calcicoles is rarely deficient in Ca2+. Furthermore, he observed that the accumulation of this divalent ion close to the cell surface is enhanced by the consistently higher cation exchange capacity of the cell walls of calcicole bryophytes compared with that of calcifuges (see Bates, 2000). The present results are consistent with the hypothesis that important membrane components, perhaps the carriers responsible for bisulfite import or molecules concerned with oxidative activity, respond to Ca2+ quite differently in Pleurozium schreberi and Rhytidiadelphus triquetrus.
As in previous studies with epiphytic lichens (Türk and Wirth, 1975) and Sphagnum species (Ferguson and Lee, 1979), increasing the acidity of the bisulfite solution led to a greater depression of net photosynthesis (Fig. 2). Moreover, photosynthetic recovery was poorest when the bisulfite solution was buffered at pH 3·0, the most acid solution used in this experiment. This may indicate, as has previously been suggested, that bisulfite ions (HSO3–) and undissociated sulfurous acid (‘H2SO3’), the prevalent forms under acid conditions, are more phytotoxic than sulfite ions (SO32–). A further hypothesis, that detoxification is less effective under acid conditions, may now also deserve consideration.
Finally, in view of the results of the metal pre-treatment experiment (Table 1), one might conjecture whether Rhytidiadelphus triquetrus, faced with SO2 pollution, could in some circumstances become restricted to acid rather than alkaline soils, deriving protection from their greater Fe3+ availability. Presumably other factors such as the high solubility of Al3+ in many acid soils would prevent this, but, still hindered by a very hazy understanding of the reasons for calcicole and calcifuge behaviour in bryophytes (Bates, 2000), we cannot rule out this possibility.
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ACKNOWLEDGEMENTS |
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We gratefully acknowledge financial support of the Indian High Commission and the generous leave from Assam Agricultural University that enabled B.B. to visit Imperial College for his doctoral studies.
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