Drought stress mitigation by nitrogen in boreal forests inferred from stable isotopes.

Forest growth in most parts of the boreal zone is originally limited by low temperatures and low nitrogen availability. Due to the rapid climate warming at high latitudes, an increasing forest area is switching to drought limitation, especially in continental and southern parts of the boreal forest. Studies addressing this issue were mostly dendrochronological and remote-sensing analyses focusing on climatic effects, but not answering the question whether drought is effective alone or in combination with nitrogen shortage at limiting the forests' productivity and vitality. Here we show in a case study from larch forests of Mongolia with a combination of stable isotope analyses, tree-ring analysis and bioindication of the local variability of livestock densities using epiphytic lichens that, in the studied highly drought-prone forests at the southern fringe of the boreal forest in Inner Asia, the trees' vulnerability to drought is modified by nitrogen fertilization from livestock kept in the vicinity and the edge of the forests. The most likely mechanism behind this drought-nitrogen interaction is the reduction of stomatal conductance, which is known to be induced by low nitrogen levels in plants. Nitrogen fertilization by the livestock could, thus, shorten the times of stomatal closure and thereby increase tree growth, which we measured as radial stem increment. Even though the underlying mechanisms, which were so far examined in angiosperms, should be experimentally tested for conifers, our results indicate that focusing on water alone is not enough to understand the climate change response of drought-limited boreal forests.

Modelling the productivity of Siberian larch forests from Landsat NDVI time series in fragmented forest stands of the Mongolian forest-steppe.

The monitoring of the spatial and temporal dynamics of vegetation productivity is important in the context of carbon sequestration by terrestrial ecosystems from the atmosphere. The accessibility of the full archive of medium-resolution earth observation data for multiple decades dramatically improved the potential of remote sensing to support global climate change and terrestrial carbon cycle studies. We investigated a dense time series of multi-sensor Landsat Normalized Difference Vegetation Index (NDVI) data at the southern fringe of the boreal forests in the Mongolian forest-steppe with regard to the ability to capture the annual variability in radial stemwood increment and thus forest productivity. Forest productivity was assessed from dendrochronological series of Siberian larch (Larix sibirica) from 15 plots in forest patches of different ages and stand sizes. The results revealed a strong correlation between the maximum growing season NDVI of forest sites and tree ring width over an observation period of 20 years. This relationship was independent of the forest stand size and of the landscape's forest-to-grassland ratio. We conclude from the consistent findings of our case study that the maximum growing season NDVI can be used for retrospective modelling of forest productivity over larger areas. The usefulness of grassland NDVI as a proxy for forest NDVI to monitor forest productivity in semi-arid areas could only partially be confirmed. Spatial and temporal inconsistencies between forest and grassland NDVI are a consequence of different physiological and ecological vegetation properties. Due to coarse spatial resolution of available satellite data, previous studies were not able to account for small-scaled land-cover patches like fragmented forest in the forest-steppe. Landsat satellite-time series were able to separate those effects and thus may contribute to a better understanding of the impact of global climate change on natural ecosystems.

Hydraulic architecture and vulnerability to drought-induced embolism in southern boreal tree species of Inner Asia.

The branch xylem of six important Inner Asian southern boreal forest trees was studied for wood-anatomical and hydraulic traits in order to infer the species' drought tolerance from embolism resistance, potential hydraulic conductivity, mean conduit diameters and conduit density. The only studied angiosperm tree, Betula pendula Roth, was much more sensitive to cavitation than all five conifers (evergreen or summer-green), even when using 88% loss of conductivity (P88) in birch, but 50% (P50) in the conifers as critical thresholds. This suggests that pioneer birch forests, which have widely replaced the conifer climax forests after anthropogenic disturbance (e.g., logging, man-made fire), are more vulnerable to climate warming-induced drought than the original conifer forests. In contrast to expectation, the generally more drought-exposed light taiga species (Larix sibirica Ledeb., Pinus sylvestris L.) did not have consistently lower P50 and P88 values than the dark taiga conifers, suggesting that other drought survival traits are equally important. Among the dark-taiga species, only Pinus sibirica Du Tour, but not Abies sibirica Ledeb. and Picea obovata Ledeb., had relatively high P50 values indicating higher vulnerability. In the light-taiga forest, P. sylvestris revealed lower embolism resistance than L. sibirica. In the face of rapid climate warming and drying in Inner Asia, the drought survival strategies of southern boreal tree species deserve further intensive study, which should include other drought survival traits.

Higher climate warming sensitivity of Siberian larch in small than large forest islands in the fragmented Mongolian forest steppe.

Forest fragmentation has been found to affect biodiversity and ecosystem functioning in multiple ways. We asked whether forest size and isolation in fragmented woodlands influences the climate warming sensitivity of tree growth in the southern boreal forest of the Mongolian Larix sibirica forest steppe, a naturally fragmented woodland embedded in grassland, which is highly affected by warming, drought, and increasing anthropogenic forest destruction in recent time. We examined the influence of stand size and stand isolation on the growth performance of larch in forests of four different size classes located in a woodland-dominated forest-steppe area and small forest patches in a grassland-dominated area. We found increasing climate sensitivity and decreasing first-order autocorrelation of annual stemwood increment with decreasing stand size. Stemwood increment increased with previous year's June and August precipitation in the three smallest forest size classes, but not in the largest forests. In the grassland-dominated area, the tree growth dependence on summer rainfall was highest. Missing ring frequency has strongly increased since the 1970s in small, but not in large forests. In the grassland-dominated area, the increase was much greater than in the forest-dominated landscape. Forest regeneration decreased with decreasing stand size and was scarce or absent in the smallest forests. Our results suggest that the larch trees in small and isolated forest patches are far more susceptible to climate warming than in large continuous forests pointing to a grim future for the forests in this strongly warming region of the boreal forest that is also under high land use pressure.

Carbon pool densities and a first estimate of the total carbon pool in the Mongolian forest-steppe.

The boreal forest biome represents one of the most important terrestrial carbon stores, which gave reason to intensive research on carbon stock densities. However, such an analysis does not yet exist for the southernmost Eurosiberian boreal forests in Inner Asia. Most of these forests are located in the Mongolian forest-steppe, which is largely dominated by Larix sibirica. We quantified the carbon stock density and total carbon pool of Mongolia's boreal forests and adjacent grasslands and draw conclusions on possible future change. Mean aboveground carbon stock density in the interior of L. sibirica forests was 66 Mg C ha(-1) , which is in the upper range of values reported from boreal forests and probably due to the comparably long growing season. The density of soil organic carbon (SOC, 108 Mg C ha(-1) ) and total belowground carbon density (149 Mg C ha(-1) ) are at the lower end of the range known from boreal forests, which might be the result of higher soil temperatures and a thinner permafrost layer than in the central and northern boreal forest belt. Land use effects are especially relevant at forest edges, where mean carbon stock density was 188 Mg C ha(-1) , compared with 215 Mg C ha(-1) in the forest interior. Carbon stock density in grasslands was 144 Mg C ha(-1) . Analysis of satellite imagery of the highly fragmented forest area in the forest-steppe zone showed that Mongolia's total boreal forest area is currently 73 818 km(2) , and 22% of this area refers to forest edges (defined as the first 30 m from the edge). The total forest carbon pool of Mongolia was estimated at ~ 1.5-1.7 Pg C, a value which is likely to decrease in future with increasing deforestation and fire frequency, and global warming.

Rapid recovery of stem increment in Norway spruce at reduced SO2 levels in the Harz Mountains, Germany.

Tree-ring width of Picea abies was studied along an altitudinal gradient in the Harz Mountains, Germany, in an area heavily affected by SO(2)-related forest decline in the second half of the 20th century. Spruce trees of exposed high-elevation forests had earlier been shown to have reduced radial growth at high atmospheric SO(2) levels. After the recent reduction of the SO(2) load due to clean air acts, we tested the hypothesis that stem growth recovered rapidly from the SO(2) impact. Our results from two formerly damaged high-elevation spruce stands support this hypothesis suggesting that the former SO(2)-related spruce decline was primarily due to foliar damage and not to soil acidification, as the deacidification of the (still acidic) soil would cause a slow growth response. Increasing temperatures and deposited N accumulated in the topsoil are likely additional growth-promoting factors of spruce at high elevations after the shortfall of SO(2) pollution.

Small increase in substratum [corrected] pH causes the dieback of one of Europe's most common lichens, Lecanora conizaeoides.

BACKGROUNDS AND AIMS: Lecanora conizaeoides was until recently western and central Europe's most abundant epiphytic lichen species or at least one of the most common epiphytes. The species is adapted to very acidic conditions at pH values around 3 and high concentrations of SO(2) and its derivatives formed in aqueous solution, and thus spread with increasing SO(2) deposition during the 19th and 20th centuries. With the recent decrease of SO(2) emissions to nearly pre-industrial levels within 20 years, L. conizaeoides declined from most of its former range. If still present, the species is no longer the dominant epiphyte, but is occurring in small densities only. The rapid spread of the L. conizaeoides in Europe from an extremely rare species to the probably most frequent epiphytic lichen and the subsequent rapid dieback are unprecedented by any other organism. The present study aimed at identifying the magnitude of deacidification needed to cause the dieback of the lichen. METHODS: The epiphytic lichen diversity and bark chemistry of montane spruce forests in the Harz Mountains, northern Germany, were studied and the results were compared with data recorded with the same methods 13-15 years ago. KEY RESULTS: Lecanora conizaeoides, which was the dominant epiphyte of the study area until 15 years ago, is still found on most trees, but only with small cover values of ≤1 %. The bark pH increased by only 0·4 pH units. CONCLUSIONS: The data suggest that only slight deacidification of the substratum causes the breakdown of the L. conizaeoides populations. Neither competitors nor parasites of L. conizaeoides that may have profited from reduced SO(2) concentrations are likely causes of the rapid dieback of the species.

Diverging climate trends in Mongolian taiga forests influence growth and regeneration of Larix sibirica.

Central and semiarid north-eastern Asia was subject to twentieth century warming far above the global average. Since forests of this region occur at their drought limit, they are particularly vulnerable to climate change. We studied the regional variations of temperature and precipitation trends and their effects on tree growth and forest regeneration in Mongolia. Tree-ring series from more than 2,300 trees of Siberian larch (Larix sibirica) collected in four regions of Mongolia's forest zone were analyzed and related to available weather data. Climate trends underlie a remarkable regional variation leading to contrasting responses of tree growth in taiga forests even within the same mountain system. Within a distance of a few hundred kilometers (140-490 km), areas with recently reduced growth and regeneration of larch alternated with regions where these parameters remained constant or even increased. Reduced productivity could be correlated with increasing summer temperatures and decreasing precipitation; improved growth conditions were found at increasing precipitation, but constant summer temperatures. An effect of increasing winter temperatures on tree-ring width or forest regeneration was not detectable. Since declines of productivity and regeneration are more widespread in the Mongolian taiga than the opposite trend, a net loss of forests is likely to occur in the future, as strong increases in temperature and regionally differing changes in precipitation are predicted for the twenty-first century.

Ammonium and nitrate tolerance in lichens.

Since lichens lack roots and take up water, solutes and gases over the entire thallus surface, these organisms respond more sensitively to changes in atmospheric purity than vascular plants. After centuries where effects of sulphur dioxide and acidity were in the focus of research on atmospheric chemistry and lichens, recently the globally increased levels of ammonia and nitrate increasingly affect lichen vegetation and gave rise to intense research on the tolerance of lichens to nitrogen pollution. The present paper discusses the main findings on the uptake of ammonia and nitrate in the lichen symbiosis and to the tolerance of lichens to eutrophication. Ammonia and nitrate are both efficiently taken up under ambient conditions. The tolerance to high nitrogen levels depends, among others, on the capability of the photobiont to provide sufficient amounts of carbon skeletons for ammonia assimilation. Lowly productive lichens are apparently predisposed to be sensitive to excess nitrogen.

High acidity tolerance in lichens with fumarprotocetraric, perlatolic or thamnolic acids is correlated with low pKa1 values of these lichen substances.

The depsidone fumarprotocetraric acid as well as the depsides perlatolic and thamnolic acids are lichen secondary metabolites. Their first dissociation constants (pK(a1)) in methanol were determined to be 2.7 for perlatolic acid and 2.8 for fumarprotocetraric and thamnolic acids by UV spectroscopy. Lower pK(a1) values are, so far, not known from lichen substances. Several lichens producing at least one of these compounds are known for their outstanding tolerance to acidic air pollution. This is demonstrated by evaluating published pH preferences for central European lichens. The low pK(a1) values suggest that strong dissociation of the studied lichen substances is a prerequisite for the occurrence of lichens with these compounds on very acidic substrata, as protonated lichen substances of different chemical groups, but not their conjugated bases, are known to shuttle protons into the cytoplasm and thereby apparently damage lichens.

Water relations and photosynthetic performance in Larix sibirica growing in the forest-steppe ecotone of northern Mongolia.

Shoot water relations were studied in Siberian larch (Larix sibirica Ledeb.) trees growing at the borderline between taiga and steppe in northern Mongolia. Larix sibirica is the main tree species in these forests covering 80% of Mongolia's forested area. Minimum shoot water potentials (Psi(m)) close to the point of zero turgor (Psi(0)) repeatedly recorded throughout the growing season suggest that the water relations in L. sibirica were often critical. The Psi(m) varied in close relation to the atmospheric vapor pressure deficit, whereas Psi(0) was correlated with monthly precipitation. Young larch trees growing at the forest line to the steppe were more susceptible to drought than mature trees at the same sites. Furthermore, isolated trees growing on the steppe exhibited lower Psi(m) and recovered to a lower degree from drought overnight than the trees at the forest line. Indications of drought stress in L. sibirica were obtained in two study areas in Mongolia's forest-steppe ecotone: one in the mountain taiga of the western Khentey in northernmost Mongolia, the other in the forest-steppe at the southern distribution limit of L. sibirica on Mt. Bogd Uul, southern Khentey. Larix sibirica growing in riverine taiga with contact to the groundwater table was better water-supplied than the larch trees growing at the forest line to the steppe. Larch trees from the interior of light taiga forests on north-facing slopes, however, exhibited more critical water relations than the trees at the forest line. Frequent drought stress in mature trees and even more in young larch trees at the forest-steppe borderline suggests that L. sibirica does not have the potential to encroach on the steppe under the present climate, except in a sequence of exceptionally moist and cool years. A regression of the present borderline between forest and steppe is likely to occur, as average temperatures are increasing everywhere and precipitation is decreasing regionally in Mongolia's taiga forest region. Higher stomatal conductance concomitant to lower Psi(m) in trees of northern-slope forests compared to trees from the forest line to the steppe may be the result of a recent increase in drought intensity that affects better drought-adapted trees at the forest edge less than the trees in the forest interior. We conclude that drought is a key factor explaining the forest-steppe borderline in northern Mongolia. The proportion of forests within the present vegetation pattern of forests on north-facing slopes and the grasslands on south-facing slopes in Mongolia's forest-steppe ecotone is not likely to increase under the present climate, but may decrease with increasing aridity due to global warming.

Lichen substances prevent lichens from nutrient deficiency.

The dibenzofuran usnic acid, a widespread cortical secondary metabolite produced by lichen-forming fungi, was shown to promote the intracellular uptake of Cu(2+) in two epiphytic lichens, Evernia mesomorpha and Ramalina menziesii, from acidic, nutrient-poor bark. Higher Cu(2+) uptake in the former, which produces the depside divaricatic acid in addition to usnic acid, suggests that this depside promotes Cu(2+) uptake. Since Cu(2+) is one of the rarest micronutrients, promotion of Cu(2+) uptake by lichen substances may be crucial for the studied lichens to survive in their nutrient-poor habitats. In contrast, study of the uptake of other metals in E. mesomorpha revealed that the intracellular uptake of Mn(2+), which regularly exceeds potentially toxic concentrations in leachates of acidic tree bark, was partially inhibited by the lichen substances produced by this species. Inhibition of Mn(2+) uptake by lichen substances previously has been demonstrated in lichens. The uptake of Fe(2+), Fe(3+), Mg(2+), and Zn(2+), which fail to reach toxic concentrations in acidic bark at unpolluted sites, although they are more common than Cu(2+), was not affected by lichen substances of E. mesomorpha.

Dissociation and metal-binding characteristics of yellow lichen substances suggest a relationship with site preferences of lichens.

BACKGROUND AND AIMS: Many species of lichen-forming fungi contain yellow or orange extracellular pigments belonging to the dibenzofurans (usnic acid), anthraquinones (e.g. parietin) or pulvinic acid group. These pigments are all equally efficient light screens, leading us to question the potential ecological and evolutionary significance of diversity in yellow and orange lichen substances. Here the hypothesis is tested that the different pigments differ in metal-binding characteristics, which suggest that they may contribute to adaptation to sites differing in pH and metal availability. METHODS: UV spectroscopy was used to study the dissociation and the pH dependence of the metal-binding behaviour of seven isolated lichen substances in methanol. Metals applied were selected macro- and micro-nutrients (Cu(2+), Fe(2+), Fe(3+), Mg(2+), Mn(2+) and Zn(2+)). KEY RESULTS: All the pigments studied are strong to moderate acids with pK(a1) values between 2.8 and 4.5. Metal complexation is common in the lichen substances studied. Complexation takes place under acidic conditions with usnic acid, but under alkaline conditions with parietin and most compounds of the pulvinic acid group. The pulvinic acid derivative rhizocarpic acid forms metal complexes both in the acidic and the alkaline range. CONCLUSIONS: Metal complexation by lichen substances could be a prerequisite for lichen substance-mediated control of metal uptake. Assuming such an effect at pH values where the affinity of the metal for the lichen substance is intermediate would explain the strong preference of lichens with usnic or rhizocarpic acids to acidic substrata. Moreover, it would explain the preference of lichens with parietin and some lichens with compounds of the pulvinic acid group either for nutrient-rich substrata at low pH or for calcareous substrata.

Usnic acid controls the acidity tolerance of lichens.

The hypotheses were tested that, firstly, lichens producing the dibenzofuran usnic acid colonize substrates characterized by specific pH ranges, secondly, this preferred pH is in a range where soluble usnic acid and its corresponding anion occur in similar concentrations, and thirdly, usnic acid makes lichens vulnerable to acidity. Lichens with usnic acid prefer an ambient pH range between 3.5 and 5.5 with an optimum between 4.0 and 4.5. This optimum is close to the pK(a1) value of usnic acid of 4.4. Below this optimum pH, dissolved SO(2) reduces the chlorophyll fluorescence yield more in lichens with than without their natural content of usnic acid. This suggests that usnic acid influences the acidity tolerance of lichens. The putative mechanism of the limited acidity tolerance of usnic acid-containing lichens is the acidification of the cytosol by molecules of protonated usnic acid shuttling protons through the plasma membrane at an apoplastic pH

Surface hydrophobicity causes SO2 tolerance in lichens.

BACKGROUND AND AIMS: The superhydrophobicity of the thallus surface in one of the most SO(2)-tolerant lichen species, Lecanora conizaeoides, suggests that surface hydrophobicity could be a general feature of lichen symbioses controlling their tolerance to SO(2). The study described here tests this hypothesis. METHODS: Water droplets of the size of a raindrop were placed on the surface of air-dry thalli in 50 lichen species of known SO(2) tolerance and contact angles were measured to quantify hydrophobicity. KEY RESULTS: The wettability of lichen thalli ranges from strongly hydrophobic to strongly hydrophilic. SO(2) tolerance of the studied lichen species increased with increasing hydrophobicity of the thallus surface. Extraction of extracellular lichen secondary metabolites with acetone reduced, but did not abolish the hydrophobicity of lichen thalli. CONCLUSIONS: Surface hydrophobicity is the main factor controlling SO(2) tolerance in lichens. It presumably originally evolved as an adaptation to wet habitats preventing the depression of net photosynthesis due to supersaturation of the thallus with water. Hydrophilicity of lichen thalli is an adaptation to dry or humid, but not directly rain-exposed habitats. The crucial role of surface hydrophobicity in SO(2) also explains why many markedly SO(2)-tolerant species are additionally tolerant to other (chemically unrelated) toxic substances including heavy metals.

Susceptibility to acidic precipitation contributes to the decline of the terricolous lichens Cetraria aculeata and Cetraria islandica in central Europe.

The effective quantum yield of photochemical energy conversion in photosystem II (Phi2) was shown to be reduced in the terricolous lichens Cetraria aculeata and Cetraria islandica by short-term exposure to aqueous SO2 at pH values occurring in the precipitation of areas with high SO2 pollution. Significant reduction of Phi2 was found at pH

Metal homeostasis in Hypogymnia physodes is controlled by lichen substances.

The hypothesis was tested that the lichen substances produced by the epiphytic lichen Hypogymnia physodes control the intracellular uptake of divalent transition metals. Incubating lichen thalli with and without their natural content of lichen substances with metal solutions showed that the lichen substances of H. physodes selectively inhibit the uptake of Cu(2+) and Mn(2+), but not of Fe(2+) and Zn(2+). Such behavior is ecologically beneficial, as ambient concentrations of Cu(2+) and Mn(2+) in precipitation and bark are known to limit the abundance of H. physodes, whereas limiting effects of Fe(2+) or Zn(2+) have never been found. This suggests that increasing the Cu(2+) and Mn(2+) tolerance stimulated the evolution of lichen substances in H. physodes. The depsidone physodalic acid is apparently most effective at reducing Cu(2+) and Mn(2+) uptake among the seven lichen substances produced by H. physodes. Probably lichen substances play a general role in the metal homeostasis of lichens.

Lichen substances affect metal adsorption in Hypogymnia physodes.

Lichen substances are known to function as chelators of cations. We tested the hypothesis that lichen substances can control the uptake of toxic metals by adsorbing metal ions at cation exchange sites on cell walls. If true, this hypothesis would help to provide a mechanistic explanation for results of a recent study showing increased production of physodalic acid by thalli of the lichen Hypogymnia physodes transplanted to sites with heavy metal pollution. We treated cellulose filters known to mimic the cation exchange abilities of lichen thalli with four lichen substances produced by H. physodes (physodic acid, physodalic acid, protocetraric acid, and atranorin). Treated filters were exposed to solutions containing seven cations (Ca(2+), Cu(2+), Fe(2+), Fe(3+), Mg(2+), Mn(2+), and Na(+)), and changes to the solution concentrations were measured. Physodalic acid was most effective at influencing metal adsorption, as it increased the adsorption of Fe(3+), but reduced the adsorption of Cu(2+), Mn(2+), and Na(+), and to a lesser extent, that of Ca(2+) and Mg(2+). Reduced Na(+) adsorption matches with the known tolerance of this species to NaCl. The results may indicate a possible general role of lichen substances in metal homeostasis and pollution tolerance.

Epiphytic lichen diversity on dead and dying conifers under different levels of atmospheric pollution.

Based on literature data, epiphytic lichen abundance was comparably studied in montane woodlands on healthy versus dead or dying conifers of Europe and North America in areas with different levels of atmospheric pollution. Study sites comprised Picea abies forests in the Harz Mountains and in the northern Alps, Germany, Picea rubens-Abies balsamea forests on Whiteface Mountain, Adirondacks, New York, U.S.A. and Picea engelmannii-Abies lasiocarpa forests in the Salish Mountains, Montana, U.S.A. Detrended correspondence analysis showed that epiphytic lichen vegetation differed more between healthy and dead or dying trees at high- versus low-polluted sites. This is attributed to greater differences in chemical habitat conditions between trees of different vitality in highly polluted areas. Based on these results, a hypothetical model of relative importance of site factors for small-scale variation of epiphytic lichen abundance versus atmospheric pollutant load is discussed.