Temporal change in the bark pH
For reasons of better comparability, only those sampling units were included which had been sampled over the entire study period from 1970 to 2010. Often, even the examined trees were identical.
The results show a marked increase in the pH of all the species of trees that are given (Tilia spp., Populus spp., Malus domestica) and also in both investigated towns (Figure4). However, the initial pH of the various species of trees is different. While the limes - species with naturally acidic bark - started at a low pH, poplars and apple trees had higher pH even during times of high acid immission load. The reason therefore is the better buffering capacity of the poplars and apple trees in comparison with the lime.
In Giessen, where pH measurements on lime already exist from 1970, it is visible that the rise from 1970 to 1985 was insignificant. Since 1985, however, the pH has become markedly higher. This phenomenon can be easily explained by the evolution of the sulfur dioxide concentration (Figure5). Until 1987, the SO2 levels were high and fairly constant but then dropped drastically due to enhanced measures for the reduction of emissions and have stabilized at a low value since 2000.
After the decline in the acid deposition, the pH of the bark has nearly achieved natural values. Since 2005, its further increase might also have another reason: the trend in the lichen abundance suggests that there is an increase of the effects of airborne nitrogen compounds (especially NH3). An increase in ammonia concentration leads to an increase of the pH of the tree bark.
Noteworthy is the differential development of bark pH in Wetzlar and Giessen. In Wetzlar in 1985, the acidification of all tree species was significantly lower than in Giessen, despite the comparable SO2 immissions in both towns. This phenomenon can be explained by a peculiarity pollution situation in Wetzlar. In addition to the acidic immissions, there were lime dust-emitting sources in the north of Wetzlar. In 1970, their basic dusts neutralized the acidic emissions partly leading to a reduced acidification of the local tree bark. Thus, it was not surprising that the first neutrophytic lichens (e.g., Physcia tenella) were found in the north-east of Wetzlar, in the lee of the sources.
In Giessen, the dust deposition has only been measured since 1987. Based on the measurements of other comparable Hessian towns though, (e.g., Kassel[12, 13]) we can assume that the dust deposition in Giessen in 1970 was lower than that in Wetzlar. It was probably less than 200 mg/(m2 × day) and also contained no cement dust.
After the reduction of the acidic pollutant gases and the simultaneous reduction of lime dust emissions through the installation of filters, the relationships between the two towns have converged in 2010 (Figure6[12, 13]). Since many lichens have a close bond to the substrate and its pH, the development of the bark pH will play a role in the development of the lichen vegetation.
Trend in lichen-indicated air quality situation in Wetzlar and Giessen
As the basic data from previous mapping examinations are still available, it was possible to compare the current results with those of earlier studies[2, 3, 5–9, 14, 15]. Over the period from 1970 to 2010, the number of lichen species shows a steady increase (Figure7). The approximate 10-fold increase in the number of species is a first indication of an improving air quality throughout the study period. For methodological reasons, it is not possible to differentiate between the species numbers of Wetzlar and Giessen in the first two studies. Until 1985, a difference between the species numbers of Wetzlar and Giessen is assigned. This imbalance to the disadvantage of Giessen will be retained until 2010 but with a much weaker intensity recently. Giessen gradually catches up with Wetzlar concerning the lichen diversity. Additionally, there has been a conspicuous increase in the number of species in the short period between 2005 and 2010 in both towns.
Figure8 shows the development in Wetzlar. In the period around 1970, the immission load with the components sulfur dioxide and lime dust was extremely high (Figures5 and6) so that in the industrial district in the north of Wetzlar, no lichens were found at all - there existed a ‘lichen desert’. Adjacent to the lichen-free zone, only the crustose lichen L. conizaeoides was recorded in almost the entire town of Wetzlar. The sole occurrence of this species shows an extremely high air pollution. For 1970, a further lichen-based differentiation of the former air quality outside the ‘Lecanora zone’ is not possible due to methodological reasons.
Such unfavorable conditions, however, could also be identified in Frankfurt/Main, 70 km away from Wetzlar. In the period around 1970, the ‘lichen desert’ in Frankfurt was even larger than that in Wetzlar and affected the town center.
In 1985, the colors red and orange still dominated. At the outer edge of the study area, there were, however, already sampling units with medium and, in the north-west, even an area with high air quality. The significant improvement in the ambient air quality is obvious, and the average air quality index (LGI) value is 2.1 (Table2). At this point, the studied areas have an average hypertrophication index of 1.2, which shows a very small effect of nutrient pollution.
In 1995, there was only one red-colored unit in the far north of Wetzlar. Otherwise, low to moderate air quality conditions dominated; in the south, there are already two areas with high air quality indices. The sampling unit most severely affected is still located in the town's center and in the north industrial area of Wetzlar. The average hypertrophication index value increases from 1.2 to 1.5, which could be an evidence for an increase in the load caused by airborne fertilizer materials.
By 2005, the situation had again improved as 10 sampling units in the control area were given the color green, indicating a high level of air quality in these areas. However, there is also a distinctive increase in indicator species for hypertrophication (Table2), especially in the north of the investigated area.
In the survey year 2010, no area is associated with the color red anymore, but on the other hand, the number of units with the LGI 4 (green) has increased, compared with that in 2005, from 10 to 17. This means that half of the measuring units have a high air quality now. From 2005 to 2010, the hypertrophication index increased only moderately because the effect of eutrophicating air pollutants in Wetzlar is still low.
A basically similar pattern to Wetzlar can also be seen in Giessen, albeit at a lower level (Figure9). Although there were no units without lichens in 1970, large parts of the study area were inhabited only by the toxitolerant and acidophytic L. conizaeoides (color magenta).
In 1985, the situation improved significantly, although there were still two units regarded as highly charged. The average air quality index of 1.1 is a whole level lower than the corresponding initial value in Wetzlar. Hypertrophication indicating lichen species were extremely rare; according to this, the average of the hypertrophic index is 1.0.
The further improvement of the air quality until the year 1995 was not as fast and was not to such a great extent, as observed in Wetzlar. On the other hand, the average hypertrophication index remained at a lower value than in Wetzlar (Table2).
By 2005, Giessen had caught up on Wetzlar: nearly two thirds of all the investigated areas measured only medium to low loads (in Wetzlar, these are at the same time about 80 % of all comparison areas). The mean hypertrophication index had increased slightly but still remained well below that of Wetzlar.
By 2010, Giessen was on the same level as Wetzlar in terms of its air quality: there was neither a red nor an orange sampling unit. The improvement is much more obvious than in Wetzlar. Although the number of areas with green color was still lower than that of Wetzlar, there already was a blue-colored area in Giessen, which shows a very high air quality.
Table2 summarizes the trends of air quality indices and the effects of the hypertrophication of Wetzlar and Giessen from 1985 to 2010. Again, the initial advantage in Wetzlar's lichen-indicated air quality in comparison to Giessen is shown. It is clear, however, that Giessen continuously caught up after the sulfur dioxide played no more essential role in air pollution in both towns (Figure9). Thus, the original advantage of Wetzlar due to its lime dust neutralizing the SO2 immissions ended. Both towns have improved their air quality by 2010. With the increase of the air quality index values, the hypertrophic index values in both towns rose. Considering, however, the maximum values of the year 2010, one might conclude that the conditions in the two Central Hessian towns in terms of hypertrophication risk from airborne nitrogen compounds are still considered to be low to medium.
A comparison of the percentage distribution of the five air quality categories in Giessen over the survey period (Figure10) shows that sampling units with very low air quality (color red) continuously decline and no longer appear in the current study. Conversely, the number of units with high air quality increases. In 2010, for the first time, even a blue-colored measuring unit appears. The results for Wetzlar show a similar pattern.
Evolution trends of different lichen species between 1985 and 2010
Between 1985 and 2010, there were some characteristic differences in the development of the species, which shall be illustrated by typical examples (Figures11 and12).
The development of the frequency of L. conizaeoides is shown in Figure11. This toxitolerant and strongly acidophytic species shows the decrease of acid emissions at best. In Wetzlar as well as in Giessen, it was the most common - and sometimes only - lichen at times of high SO2 pollution. Until 1995, its frequency declined due to the reduction of sulfur dioxide. However, this happened in Wetzlar much more strongly than in Giessen. In 2005, L. conizaeoides could hardly be found in Wetzlar, and the further decline is also visible in Giessen; in 2010, it had virtually disappeared. The behavior of this lichen correlates very well with the reduction of SO2 concentration in the period shown here (Figure5). The stronger decline of the species in Wetzlar can be interpreted as follows: in 1985, the concentration of SO2 was still so high that the basic lime dust could hardly reduce the effect of bark acidification. With the following decline of acidic pollutants, the pH of the tree bark increased more quickly due to the more effective neutralizing of the limestone dust. In the period from 1985 to 2010, the acidophytic lichen Hypogymnia physodes showed a similar distribution pattern.
X. parietina shows a different behavior (Figure11). In 1985, this neutrophytic and nutrient-loving lichen species was very poorly developed in both towns due to the acidic pollutant gases. The following increase was hesitant in 1995. Measuring units that were occupied in 1985 remained without evidence of the species in 1995, even though it was found in other units. In 2005, it had established itself in many areas, and the frequency at the examined trees was increased significantly. The well-known preference of X. parietina for higher pH manifests itself clearly in Wetzlar. From the beginning of the study, it preferred the lime dust-affected north of the town, and its distribution pattern was complementary to that of the previously described acidophytes H. physodes and L. conizaeoides. In 2010, both in Wetzlar and Giessen, the number of populated areas increased in comparison to 2005 again, and their frequency on the trees rose. Other indicators of hypertrophication like X. candelaria, X. polycarpa, Phaeophyscia orbicularis, Physcia adscendens and P. tenella increased considerably in this period. Typical of these species is that they emerged first in the north of Wetzlar near the lime dust emitters due to their high bark pH claims.
Although the pattern of the development of Parmelia sulcata (Figure12, moderately acido- to subneutrophytic, moderately sensitive) at first glance seems to be the same as the one of the hypertrophication indicators, upon closer examination, differences can be detected. P. sulcata avoids explicitly - and including in 2010 - the towns' centers. In Wetzlar, the living conditions for the species are obviously better in the south, from which one could derive acidophytic features. However, while the acidophytes declined during the study period (see L. conizaeoides, Figure11), P. sulcata became more common in both towns. This species belongs to a large lichen group that prefers average bark pH conditions. It tolerates only moderate hypertrophication and has a modest sensitivity to air pollution. Thus, P. sulcata is a typical representative of the ‘reference species’ whose occurrence indicates a favorable air quality. Other representatives of this group (with a similar distribution pattern) are Melanohalea exasperatula, Melanelixia glabratula, and Melanelixia subaurifera. These species are slightly more sensitive than P. sulcata; they were first found with some single individuals in a few areas measured in Wetzlar in 1995. In Giessen, they were not found before 2005, but by now, they populate many sampling units there.
Species such as Ramalina farinacea (Figure12) indicate an even higher degree of air quality. Until 1995, they had no possibilities of existence because of the unfavorable immission situation in Wetzlar and Giessen. Throughout the following years, they started settling in both towns, though hitherto only with a few individuals. R. farinacea is a typical representative of a rather demanding species in terms of air quality. It is one of the few fruticose lichens which have returned so far. Occasionally, one now finds representatives of the genus Usnea in both towns. They are so sensitive to air pollution that they were initially only found in a few and very small individuals (and therefore hard to determine). Based on the fact that these species appear every once in a while in a measuring area but disappear in the following mapping and emerge in another one, it can be concluded that the air quality in the study areas of Wetzlar and Giessen is still slightly below the possibilities of existence for R. farinacea and species of the genus Usnea. A few years ago, similar observations were made, for example, for the fruticose lichen Evernia prunastri; today, this species has firmly anchored in Central Hesse even within the towns. The further observation of ‘pioneer species’ is of particular interest as they will clearly show an improvement of the air quality.
Use of lichen indicator values
Surveys in the field have shown that each lichen species has certain demands to abiotic environmental factors (such as acidity or nutrients of their substrates). Consequently, species prefer environmental conditions that meet these requirements and avoid those that do not fit them. Conversely, the presence and quantity of these factors can be logically deduced from the occurrence of a species with specific environmental requirements. With the use of lichens as indicators of environmental characteristics, one should, however, be aware that their predictive value relates to the average and long-term quality and quantity of environmental parameters in the investigated sites. Additionally, interactions of several environmental factors may affect that result.
The ecological behavior is valuated according to a nine-point scale, with 1 being the lowest and 9 the largest scale means of the respective factor. Average indicator values for a sampling unit can be calculated both unweightedly (only assessing, if the species occur or not) and weightedly (including their frequency).
The temporal development of the reaction value, which allows a statement on the acidity of the substrates colonized by lichens, is shown in Figure13. The increase of the lichen reaction value follows the bark pH (Figure4). Since 1985 the pH has gradually increased almost back to pre-industrial values as a result of the decreasing acid immissions, thereby allowing for the reintroduction of subneutrophytic and neutrophytic lichen species. As demonstrated by the lichen reaction values the largest pH-increase occurred between 1985 and 1995, related to the recently drastically reduced SO2 concentrations (Figure5).
As can be seen in Figure14, changes in the composition of lichens could be caused by a higher load of hypertrophicating air pollutants. This is supported by the increase in nutrient indicator values. In Figures8 and9 (also in Table2), we have already pointed out the increase of hypertrophication indicating lichens in almost all measuring units. However, the value in 1985 has to be queried. It is conceivable that at that time, due to the high SO2 levels, hypertrophication-indicating species could not yet exist despite already existing exposure to nitrogen compounds.
As a main cause for the hypertrophication, airborne nitrogen compounds come into question. Their concentrations, however, do not show any significant changes in the technical measurements in Hesse for the period in question.
One explanation for this apparent contradiction lies in the fact that technically measured nitrogen oxides have no direct relevance for the nutrition of lichens. Plants and lichens are known to metabolize especially NO3 and NH3/NH4[17–20]. These nitrogen compounds are often not detected in environmental monitoring due to technical problems in measuring. The amount of nitrogen emitted in the form of ammonia in Central Europe has approximately the same magnitude as the total emission of nitrogen in form of both, NO and NO2. The ammonia mainly comes from agricultural sources (livestock, manure spreading). It is degraded within a few hours to ammonium or ammonium salts. Therefore, elevated ammonia concentrations can only be measured in the immediate vicinity of sources. The secondary products (ammonium or ammonium salts), however, can be transported as aerosols over long distances. Due to the transport, it appears that these compounds exist over a wide area. While it has been assumed that the NH3 emissions from car exhausts are rather negligible, recent studies published significant concentrations of ammonia from the exhaust gases of occupied, cold, or aged catalysts[22–25]. According to Umweltbundesamt, the petrol-fueled vehicles emit between 20 and 50 mg ammonia/km, depending on the catalyst type and the traffic flow. These findings would also explain why the nitrogen enrichment in lichens is particularly high in the towns, and therein mainly in the vicinity of heavily frequented roads, despite the lack of agricultural emissions[27, 28]. It is further stated that the diversity of nitrophytic lichens, starting from the edges of the roads, gradually decreases. All these facts suggest a significant role of ammonia (or its reaction product ammonium) in the effects of nitrogen compounds on lichens. Only until recently, a metrological reference exists to the increase of ammonia in Hesse (Figure15). As demonstrated, the NH3 levels have increased in different sampling sites in Germany since 2000, amongst those for instance the site in Linden near Giessen. These results provide a plausible explanation for the increase of the nutrient indicator values (Figure14).
Figure16 indeed shows an increase in the lichen diversity of reference species for the two towns, indicating an overall improvement in the air quality conditions. This increase becomes even more evident when one omits the calculation of Lecanora conizaeoides, a crustose lichen tolerant to SO2 and therefore the dominant species on tree bark until 1985. However, the simultaneous - and even higher - increase in hypertrophication indicators also points to a significant exposure to substances with nutrient effects.
Lichens as indicators of climate change
If we follow the change in the epiphytic lichen vegetation over long periods of time, it can be seen that apart from the decrease of acidophytes (prefer acidic substrates) and the simultaneous increase in nitrophytes (prefer nutrient-rich substrates), further changes in species composition take place. While lichens that are adapted to cool environmental conditions decrease (or at least do not increase) recently, such species preferring warm-temperate and more humid conditions have spread. In the present study, we have regarded species as indicators of climate change that were entitled in the corresponding VDI guideline (guideline VDI 3957 Part 20, personal communication). Moreover, we added lichens that have a temperature indicator value of 7 to 9. Their presence shows a generally more balanced climate with mild winters, increased annual average temperatures and increased humidity.
In a previous investigation in Hesse, there appeared to be an immigration trend in the lichens on rocks and walls that demonstrated a significant relationship between the measured temperatures and the occurrence of heat-loving lichens[32, 33]. In the Netherlands and in north-western and western Germany, such a change had also been identified for epiphytic lichens a few years ago[28, 34, 35]; now, it is occurring in Central Hesse as well, whereas in 1970 and 1980, not a single heat indicator grew on the examined trees. In 1985, the first of such lichen species could be detected.
In 1995, two species appeared, while there were already five species in 2005 which are assigned to the group of heat indicators. By the year 2010, within 5 years, the number had increased to 14. Our calculations of the average indicator values for temperature show that lichens respond to the changing climatic conditions. In 25 years, the average indicator value for temperature has risen by half a unit (Figure17).
This observation is consistent with the increase in temperature (Figure18; Prof. Schönwiese, personal communication). Between 1820 and 2010, a significant increase in the mean annual values of almost 2°C could be recorded; during the study period from 1970 to 2010, it amounted to almost half a degree.
As can be seen in Figures19 and20, the climate change is particularly noticeable through milder winters. This fact supports the Atlantic lichen species: according to the ‘Law of the Minimum’, formulated by Justus Liebig, the minimum factor limits the growth. As is happening recently, the frost periods are getting shorter and less severe, wherefore also species from the southwest of Europe or the sub-Mediterranean climate area have a chance to survive in Hesse.
Furthermore, it should be noted that the rainfall in Hesse has increased in recent decades and predominates in the winter. This trend is reflected in the average indicator values of lichens. In Figure21, an (albeit slight) increase in the indicator values for humidity can be seen.
In the publication by Kirschbaum and Wirth, an index of climate change, the climate index ‘KI’, was introduced. It is a combination of both the indicator values for temperature and oceanity (the latter is complementary to the indicator value for continentality) and thus integrates the statements of both values. The climatic values are averaged and a climate index (KI) for every measuring unit is calculated. Since the heat indicators are still relatively rare and occur with less frequency on the trees, a weighting of the results in the calculation of the KI - according to the frequency of their occurrence - was omitted. (Because of their low frequency, their values would not influence the results in comparison to the other mostly common species.) Moreover, in this way it was possible to calculate an unweighted index for 1970; a calculation of a weighted index was not possible due to methodological reasons.
As can be seen in Figure22 the climate index for the forty-year study period increased, as well. From this, a tendency to a more Atlantic climate with more balanced seasonal temperatures and precipitation can be concluded. It is remarkable that the increase is not substantially caused by those species that are both heat and hypertrophication indicators; hereby, it is obviously not a synergetic effect between increased airborne nitrogen compounds and the climate change, as is being considered by some authors[37, 38].