Diagnostic parameters for selecting against novel spruce (Picea abies) decline: IV. Response of photosynthesis and transpiration to SO2+NO2 exposures

The dose- and time-response effects of 3 days of 6 h day-time sequential exposures to NO₂, SO₂ and SO₂+NO₂ of 0.45–1.81 μl l⁻¹ (ppm) SO₂ and 1.50–7.65 μl l⁻¹ NO₂ on photosynthesis, transpiration and dark respiration were examined for nine Carpatho-Ukrainian half-sib families and a population from the GFR ('Westerhof') of Norway spruce [ Piecea abies (L.) Karst.], all in their 5th growing season.
SO₂+NO₂ inhibited photosynthesis and transpiration and stimulated dark respiration more than SO₂ alone. SO₂ and SO₂+NO₂ at the lowest concentrations inhibited night transpiration, but increased it at the highest concentration, the strongest effects being obtained with combined exposures. Photosynthesis of the different half-sib families was affected significantly differently by SO₂+NO₂ exposures. NO₂ alone had no effects.
Sensitivity to transpiration decline correlated negatively with branch density. Height of trees correlated postitively with decline sensitivity in the seed orchard. The distribution of photosynthesis and transpiration sensitivities over all tested half-sib families correlated negatively with the distribution of decline sensitivity of their parents in a rural Danish seed orchard. The relative photosynthesis and transpiration sensitivities may thus serve as diagnostic parameters for selecting against novel spruce decline.     

Growth of coniferous trees exposed to SO2 and O3 using an open-air fumigation system

Scots pine (Pinus sylvestris L.), Norway spruce (Picea abies (L.) Karst.) and Sitka spruce (Picea sitchensis Bong. Carr.) were planted as 2-year-old seedlings in an open-air fumigation facility at Liphook in southern England in March 1985. The soil was a humoferric podzol of pH 4. SO₂ fumigation began in May 1987 and continued until December 1990. Long-term mean SO₂ concentrations were 4,13 and 22 nmol mo^?1. Three plots, one at each SO₂ level, were also exposed to O₃ at an average of 1–3.times the ambient level. O₃ fumigation ran from March to December 1988, May to December 1989 and February to December 1990. Each species reacted differently to treatment. Scots pine showed no growth response to either pollutant, although other work on the site demonstrated a number of deleterious effects of SO₂ on this species, including increased leaf loss and foliar injury. Stem basal diameter growth of Norway spruce was depressed in SO₂-treated plots. In contrast, extension growth of shoots of Sitka spruce increased in SO₂-treated plots, in apparent response to codeposition of NH₃-N. However, diameter growth of Sitka spruce main stems did not increase. No effects of O₃ on growth were recorded for any species.     

Photosynthetic performance, chloroplast pigments and mineral content of Norway spruce (Picea abies (L.) Karst.) exposed to SO2 and O3 in an open-air fumigation experiment

Photosynthetic performance, mineral content and chloroplast pigments were investigated in August-September 1988 and 1989 in Norway spruce trees (Picea abies (L.) Karst.) exposed to SO₂, and O₃ in an open-air fumigation facility at Liphook, England. The data do not suggest a treatment effect on the mineral content of the needles in terms of nutrient leaching from the foliage. In addition, there were no direct SO₂ and/or O₃ effects on the content and/or composition of the chloroplast pigments. However, the long-term application of SO₂ resulted in a depression of net photosynthesis under light saturation and ambient CO₂ (A ₃₄₀) which was probably caused by a treatment-related depression of the carboxylation efficiency (CE). In 1989, the supposed treatment effects were apparently masked by an insufficient N-supply and probably also by low water availability during summer. However, fumigation appeared to accelerate an N-deficiency-related decrease of CE, stomatal closure and the age-dependent development of the chlorophyll content of the needles. In 1989, an observed depression of the photosynthetic capacity (A₂₅₀₀) was in part accompanied by a decrease in light use efficiency (α), suggesting an enhanced photosensitivity resulting from the impact of several possible interacting stresses (drought, N deficiency and fumigation). The results support the general conclusion that long-term low-level SO₂ dosage adversely affects the photosynthetic performance of the needle, whether directly or indirectly, and may also interact with other environmental stresses. The findings of our investigations are discussed with regard to the hypothesis of forest decline in the mountain regions of the Fichtelgebirge (north-eastern Bavaria, Germany).     

The effects of SO2 and O3 on the foliar nutrition of Scots pine, Norway spruce and Sitka spruce in the Liphook open-air fumigation experiment

Foliar elements were analysed in Scots pine, Sitka spruce and Norway spruce over a 6 year period before and during continuous exposure to SO₂ and O₃ in an open-air fumigation experiment. Sulphur dioxide treatment elevated foliar sulphur concentration in all species, and there were increases in foliar nitrogen in the two spruce species but not in pine. The concentrations of cations were frequently increased by SO₂ treatment, but there was no correlation between the sulphur concentration of needles and their total cation charge. SO₂-related elevations of foliar magnesium were correlated with the concentration of this element in soil solution, but the mechanism by which other cations were enhanced remains unclear. The only consistent effects on nutrient ratios were for SO₂ treatments to increase sulphur/cation ratios.     

THE COMBINED EFFECTS OF LOW TEMPERATURE AND SO2+NO2 POLLUTION ON THE NEW SEASON'S GROWTH AND WATER RELATIONS OF PICEA SITCHENSIS

Picea sitchensis (Bong.) Carr. seedlings were exposed to SO₂, NO₂ and SO₂+ NO₂ during dormancy in controlled environments, and were taken to night temperatures of 4, 0, −5, −10 and −15 °C in a freezer. Conditions in the freezer were carefully monitored during the low–temperature treatments. In two experiments, different photoenvironments and temperature regimes were imposed prior to the cold treatments, and different effects were observed. In the first, only limited frost hardiness was achieved and night temperatures of −15 °C were lethal. Temperatures of −5 and − 10 °C led to poor survival of lateral buds, particularly in plants exposed to 45 ppb SO₂. The poor bud break in plants exposed to SO₂ and to − 5 °C resulted in a loss of the effectiveness of this temperature as a chill requirement. Pressure-volume analysis showed that the shoots of plants exposed to NO₂ had greater elasticity (lower elastic moduli, e), so that loss of turgor occurred at lower relative water contents. In contrast, a hardening period (2 weeks in night/day temperatures of 3/10 °C and 8 h days at 50 μmol m⁻² s⁻¹ PAR) gave decreased elasticity and lower solute potentials of spruce shoots. In the second experiment, exposure to 30 ppb SO₂ and SO₂+ NO₂ led to slight, but consistent, increases in frost injury to the needles of plants frozen to − 5 and − 10 °C. The results suggest that the main interaction of low temperatures and winter pollutants may be on bud survival rather than on needle damage, but that effects are subtle, only occurring with certain combinations of pollutant dose and cold treatment.     

The effect of open-air fumigation with SO2 and O3 on carbohydrate metabolism in Scots pine (Pinus sylvestris) and Norway spruce (Picea abies)

The carbohydrate metabolism of the needles of Scots pine (Pinus sylvestris) and Norway spruce (Picea abies) has been examined in trees that were exposed to SO₂, and O₃, in an open-air fumigation experiment located in the Liphook forest in southern England. Two-year-old seedlings were planted in 1985 in seven experimental plots. Five plots received fumigation treatments of SO₂, O₃ or a combination of these gases to give a 2 × 3 factorial design with one additional ambient plot Fumigation with SO₂, occurred from May 1987 to December 1990 and O₃, fumigation occurred from March to December 1988, May to December 1989 and February to December 1990. Five samples of needles for investigation of carbohydrate metabolism were taken between February and July 1989. The concentrations of soluble carbohydrates (including sucrose and hexoses) were greatly reduced in the needles taken from Scots pine growing in the treated plots, and were also reduced, but to a lesser extent, in the needles taken from Norway spruce. Little variation in the concentration of starch in the needles of either species was detected. The activities of the two final enzymes of sucrose synthesis, sucrose phosphate synthase and sucrose 6-phos-phate phosphatase, were greatly reduced in the needles of Scots pine and were also reduced, but to a lesser extent, in the needles of Norway spruce in the fumigated plots. These reductions could be correlated with decreases in rates of photosynthetic CO₂ assimilation determined by independent groups of researchers working on the Liphook site.     

Early needle senescence and thinning of the crown structure of Picea abies as induced by chronic SO2 pollution. II. Field data basis, model results and tolerance limits

Field data on the sulphur and cation budget of growing Norway spruce canopies (Picea abies [L.] Karst.) are summarized. They are used to test a spruce decline model capable of quantifying effects of chronic SO₂ pollution on spruce forests. At ambient SO₂ concentrations, acute SO₂ damage is rare, but exposure to polluted air produces reversible thinning of the canopy structure with a half-time of a few years. Canopy thinning in the spruce decline model is highest (i) at elevated SO₂ pollution, (ii) in the mountains, (iii) at unfertilized sites with poor K⁺, Mg²⁺ or Zn²⁺ supply, (iv) at low spruce litter decomposition rates, and (v) acidic, shallow soils at high annual precipitation rates in the field and vice versa. Model application using field data from Würzburg (moderate SO₂ pollution, alkaline soils, no spruce decline) and from the Erzgebirge (extreme SO₂ pollution, acidic soils in the mountains, massive spruce decline) predicts canopy thinning by 2–11% in Würzburg and by 45–70% in the Erzgebirge. The model also predicts different SO₂-tolerance limits for Norway spruce depending on the site elevation and on the nutritional status of the needles. If needle loss of more than 25% (damage class 2) is taken to indicate ‘real damage’ exceeding natural variances, then for optimum soil conditions SO₂ tolerance limits range from (27.3 ± 7.4) μg m^?3 to (62.6 ± 16.5) μg m^?3. For shallow and acidic soils, SO₂ tolerance limits range from (22.0 ± 5.5) μg m^?3 to (37.4 ± 7.5) μ m^?3. These tolerance limits, which are calculated on an ecophysiological data basis for Norway spruce are close to epidemiological SO₂-toIerance limits as recommended by the IUFRO, UN-ECE and WHO. The observed statistical regression slope of the plot (damaged spruce trees vs. SO₂-pollution) in west Germany is confirmed by modelling (6% error). Model application to other forest trees allows deduction of the observed sequence of SO₂-sensitivity: Abies > Picea > Pinus > Fagus > Quercus. Thus, acute phytotoxicity of SO₂ seems not to be involved in ‘forest decline’. Chronic SO₂-pollution induces massive canopy thinning of Abies alba and Picea abies only at unfavourable sites, where natural stress factors and secondary effects of SO₂pollution act together to produce tree decline.     

Early needle senescence and thinning of the crown structure of Picea abies as induced by chronic SO2pollution. I. Model deduction and analysis

Regarding time ranges of years, a rationale has been developed which is capable of explaining observed ‘spruce decline’ symptoms observed when spruce is exposed to air containing ambient levels of SO₂. It integrates and interrelates (i) ecophysiological data (tree morphology, assimilate partitioning, canopy turnover, senescence physiology, stomatal conductance, canopy throughfall, sulphur metabolism, tonoplast symport), (ii) pedological data (soil leaching, cation recycling, litter decomposition, forest nutrition), and (iii) meteorological data (site elevation, length of the annual trunk growth period, SO₂-pollution). Furthermore, it can explain field observations at numerous sites of spruce decline in central Europe where SO₂ is implicated as a factor of forest decline: (i) thinning of the canopy structure; (ii) early needle senescence; (iii) cation deficiency; (iv) low SO₂ tolerance at sites with depleted soils in the mountains; (v) synergism of SO₂pollution and acidic precipitation; (vi) recovery after liming, fertilization and after decreasing SO₂ pollution; and (vii) higher SO₂ tolerances of deciduous angiosperms. Different SO₂tolerance strategies are identified that are employed by more SO₂-tolerant tree species. Ecophysiological SO₂tolerance factors interact in a complex synergistic or antagonistic manner. It is concluded that chronic SO₂ pollution at ambient concentrations predisposes mainly evergreen gymnosperms to suffer under synergistic environmental stresses (frost, drought, pathogens, etc.). Thinning of the crown structure is massive at extreme sites, where several stresses act simultaneously on the trees (depleted soils, high SO₂ pollution, acidic rain, etc.). Mathematical formulations allow precise definitions of terms such as cooperativity, synergism, antagonism, vitality, predisposition, latency, etc. This universal rationale, which is applicable to all tree species, is exemplified here for Norway spruce (Picea abies [L.] Karst.). Integration of parameters yields an ordinary differential equation, which can be solved analytically. It predicts reversible dynamics of crown structures and gives an ecophysiological background to‘damage’.     

Diagnostic parameters for selecting against novel spruce (Picea abies) decline: I. Tree morphology and photosynthesis response to acute SO2 exposures

The dose- and time-response effects of single 4-h day-exposures to 0.50, 0.79, 1.28, 1.58, 2.38 or 3.35 μl l^?1 (ppm) SO₂ followed by single 3-h night-exposures of 0.60, 0.87, 1.54, 1.91, 2.91 or 3.98 μl l^?1 SO₂ on photosynthesis, transpiration and dark respiration were examined for nine East European (Carpatho-Ukrainian, ‘Rachovo’) half-sib families and for two populations, one from the FRG (‘Westerhof’) and one from the GDR (‘Schmiedefeld’) of Norway spruce [Picea abies (L.) Karst.], all in their 4th growing season. Even the lowest SO₂ concentration reduced photosynthesis and transpiration within 1 h. Photosynthesis of the different spruce types was affected significantly differently, the most sensitive spruce being suppressed 2.5 times more than the most tolerant spruce. ‘Westerhof’ was more resistant to SO₂ than the average ‘Rachovo’ half-sibs. Neither transpiration (stomatal reaction), which was affected alike by all SO₂ concentrations, nor SO₂ uptake, explained adequately the effects on photosynthesis. Night transpiration, but not dark respiratin, was stimulated by night SO₂ preceded by day SO₂ exposure. The gradient of different SO₂ sensitivities among young trees from the half-sib families demonstrated a significant negative correlation with the gradient of different sensitivities to novel decline symptoms of their parents growing in a rural seed orchard in Denmark, and with the gradients of four morphology parameters, (height, branching, branch density and the number of Lammas shoots) of the young trees, which in turn demonstrated a positive correlation with decline sensitivity in the seed orchard. The relative photosynthesis sensitivity and the morphology of half-sibs may serve as diagnostic parameters for laboratory selection of the most resistent trees to novel spruce decline in the field. There was a positive correlation between SO₂ induced scorching of Lammas shoots and the inhibition of photosynthesis, but not between the severity of SO₂ scorching and symptoms of novel spruce decline. The two visible types of symptoms looked very different.     

SO2-dependent cation competition and compartmentalization in Norway spruce needles

Ion contents in needles from Norway spruce trees [Picea abies (L.) Karst.] growing in Würzburg and in the SO₂-polluted Erzgebirge mountains were analysed to quantify cations which accumulate together with sulphate. In Würzburg there was a positive correlation of potassium (0.680 ± 0.300 Eq Eq^?1 SO₄^?2), magnesium (0.415 ± 0.111 Eq Eq^?1 SO₄^?2) and zinc (0.059 ± 0.006 Eq Eq^?1 SO₄^2?). In the Erzgebirge, potassium was also the stoichiometrically most important cation (0–887 ± 0–180 Eq K⁺ Eq^?1 SO₄^2?). All other correlations examined were weak or statistically non-significant. At both sites the calcium content of spruce needles did not depend on the sulphate content. The lack of a role for Ca²⁺ in neutralizing sulphate is a consequence of the presence of free oxalic acid in needles. Soluble oxalic acid precipitates Ca²⁺, which thereby becomes unavailable as a counterion for SO₄^2?. The activity coefficients of Ca²⁺ and oxalate^2?, and the solubility product of Ca-oxalate, were determined from in vivo data. It is concluded that the chronic accumulation of atmospheric sulphate in spruce needle vacuoles depletes available potassium and thereby strongly interferes with spruce growth and canopy turnover. This leads to impaired spruce vitality, even at sites where acute SO₂ disease symptoms are absent.     

Competition increasingly dominates the responsiveness of juvenile beech and spruce to elevated CO2 and/or O3 concentrations throughout two subsequent growing seasons

Saplings of Fagus sylvatica and Picea abies were grown in mono‐ and mixed cultures in a 2‐year phytotron study under all four combinations of ambient and elevated ozone (O₃) and carbon dioxide (CO₂) concentrations. The hypotheses tested were (1) that the competitiveness of beech rather than spruce is negatively affected by the exposure to enhanced O₃ concentrations, (2) spruce benefits from the increase of resource availability (elevated CO₂) in the mixed culture and (3) that the responsiveness of plants to CO₂ and O₃ depends on the type of competition (i.e. intra vs. interspecific). Beech displayed a competitive disadvantage when growing in mixture with spruce: after two growing seasons under interspecific competition, beech showed significant reductions in leaf gas exchange, biomass development and crown volume as compared with beech plants growing in monoculture. In competition with spruce, beech appeared to be nitrogen (N)‐limited, whereas spruce tended to benefit in terms of its plant N status. The responsiveness of the juvenile trees to the atmospheric treatments differed between species and was dominated by the type of competition: spruce growth benefited from elevated CO₂ concentrations, while beech growth suffered from the enhanced O₃ regime. In general, interspecific competition enhanced these atmospheric treatment effects, supporting our hypotheses. Significant differences in root : shoot biomass ratio between the type of competition under both elevated O₃ and CO₂ were not caused by readjustments of biomass partitioning, but were dependent on tree size. Our study stresses that competition is an important factor driving plant development, and suggests that the knowledge about responses of plants to elevated CO₂ and/or O₃, acquired from plants growing in monoculture, may not be transferred to plants grown under interspecific competition as typically found in the field.