Evaluation of bio-indication methods using epiphytes by correlating with SO2-pollution parameters

Abstract:In order to evaluate the relative usefulness of the numerous bio-indication methods that use epiphytes as indicators for air pollution, a range of these different methods was applied within the same region (Flanders, Northern Belgium). The study area shows important air pollution gradients and little climatic differentiation. Ninety-one IAP indices were calculated with data collected in the immediate vicinity of SO₂measuring stations on one randomly chosen tree, on ten neighbouring trees and in a sampling grid placed on the tree carrying the largest number of epiphytes. A large majority of indices showed a significant Spearman rank order correlation with mean SO₂winter values over the 5 years 1990–94. Indices based on a selection of 17 lichens gave better results than those based on all lichens. The latter indices showed higher correlation than those using all epiphytes (including bryophytes). Indices using a quantitative estimate of cover or abundance or a combination of these did not result in a higher correlation. Sampling ten trees gave slightly higher correlation than the grid method or sampling of one tree. Taking into account supplementary evaluation criteria (time investment and degree of lichenological knowledge required), sampling of 17 bio-indicator species using a sampling grid is recommended within the study area. Monitoring the presence of all corticolous lichens within a sampling grid is recommended in general.     

The effect of air pollution from nitrogen dioxide (NO2) on epiphytic lichens in Seville, Spain

The effect of air pollution from nitrogen dioxide (NO₂) on the epiphytic lichens of the city of Seville (Spain) has been studied. Indices of air purity (IAP) were calculated, based on the lichen flora ofMelia azedarach L. present at 25 stations distributed through the city. The arrangement and classification of the stations by principal component analysis and cluster analysis, respectively, enabled the study area to be zoned into four zones of air purity. Accordingly, the zonal map of air purity for the city of Seville yields a gradient of air purity that is very steep from the centre to the outskirts. The dependence of 77.6% of IAP variability with NO₂ pollution levels detected with air emission sensors distributed through the city suggests the relationship between NO₂ levels and zones of air purity.     

Vertical distribution of epiphytic bryophytes and lichens emphasizes the importance of old beeches in conservation

During storms in 2005, a number of beech trees fell over at Biskopstorp, SW Sweden, offering the opportunity to study epiphytes along entire stems. In total 16 beech trees in four beech stands representing three different age classes were included. For each tree, 2 m segments from the base to the top were surveyed. In total 115 species were found (76 lichens, 39 bryophytes), of which 30 were considered to be of conservation concern (22 lichens, 8 bryophytes). For lichens significantly more species were recorded above 2 m in height, whereas more bryophytes were recorded below 2 m in height. Certain red-listed lichens were recorded only above 2 m in height on old trees. In a second data set from the same area 140 age-determined beech trees were surveyed for species of conservation concern at the heights 0–2 and 2–5 m, respectively. These species were found almost exclusively on old beech trees, and presence at 2–5 m was recorded, with one exception, only on those trees which also had species of conservation concern at 0–2 m. Records of these species correlated significantly to microhabitat variables, i.e. the presence of rough bark and moss cover higher up the stems on the old trees. This study indicates that surveying only the base in really old beech forests can underestimate both the number of species of conservation concern and their population sizes. However, surveys restricted to the base in rather even-aged beech stands catch a large proportion of the trees with species of conservation concern.     

Influence of tree age, tree size and crown structure on lichen communities in mature Alpine spruce forests

Testing the relations between tree parameters and the richness and composition of lichen communities in near-natural stands could be a first step to gather information for forest managers interested in conservation and in biodiversity assessment and monitoring. This work aims at evaluating the influence of tree age and age-related parameters on tree-level richness and community composition of lichens on spruce in an Alpine forest. The lichen survey was carried out in four sites used for long-term monitoring. In each site, tree age, diameter at breast height, tree height, the first branch height, and crown projection area were measured for each tree. Trees were stratified into three age classes: (1) <100 years old, immature trees usually not suitable for felling, (2) 100–200 years old, mature trees suitable for felling, and (3) >200 years old, over-mature trees normally rare or absent in managed stands. In each site, seven trees in each age class were selected randomly. Tree age and related parameters proved to influence both tree-level species richness and composition of lichen communities. Species richness increased with tree age and related parameters indicative of tree size. This relation could be interpreted as the result of different joint effects of age per se and tree size with its area-effect. Species turnover is also suspected to improve species richness on over-mature trees. Similarly to species richness, tree-level species composition can be partially explained by tree-related parameters. Species composition changed from young to old trees, several lichens being associated with over-mature trees. This pool of species, including nationally rare lichens, represents a community which is probably poorly developed in managed forests. In accordance to the general aims of near-to-nature forestry, the presence of over-mature trees should be enhanced in the future forest landscape of the Alps especially in protected areas and Natura 2,000 sites, where conservation purposes are explicitly included in the management guidelines.     

Vertical distribution of epiphytic lichens on Quercus laurina Humb. & Bonpl. in a remnant of cloud forest in the state of Veracruz,México

In the tropics, corticolous lichen richness and cover tend to increase from the trunk base to the top of the crown of trees. In this study we calculated the total beta diversity of the lichen community along a vertical gradient on Quercus laurina in Mexican cloud forest. By comparing the richness and cover of the lichens by zone, we show that foliose and fruticose lichens are a minor component of the total lichen species richness, but have a higher cover than the crustose lichens. Five zones were identified along each phorophyte (n = 15) with a diameter at breast height >40 cm. A total of 92 species were identified. Of these, 38% were found only in a single zone, 51% were shared between the different zones and 11% occurred across all zones. Species richness and cover increased from the lowest to the highest zones of the phorophytes. Dissimilarity in species composition between the zones could be explained by species replacement. An indicator species analysis revealed that only a few species, e.g. Hypotrachyna vexans, H. cf. sublaevigata and Ramalina cf. sinaloensis prefer a particular zone. The results show that the lichen community associated with Quercus laurina phorophytes is highly diverse and suggest that species richness and cover are related to the zone and the various growth forms.     

Tree and stand-scale factors affecting richness and composition of epiphytic bryophytes and lichens in deciduous woodland key habitats

Conservation and sustainable forestry are essential in a multi-functional landscape. In this respect, ecological studies on epiphytes are needed to determine abiotic and biotic factors associated with high diversity. The aim of the present study was to evaluate relative sensitivity of conservation targets (epiphytic bryophytes and lichens) in relation to contrasting environmental variables (tree species, tree diameter at breast height, bark crevice depth, pH, tree inclination, pH, forest stand age, area and type) in boreo-nemoral forests. The study was conducted in Latvian 34 woodland key habitat (WKH) boreo-nemoral forest stands. Generalized linear mixed models and canonical correspondence analysis showed that tree species and tree bark pH were the most important variables explaining epiphytic bryophyte and lichen composition and richness (total, Red-listed, WKH indicator species). Forest stand level factors, such as stand size and habitat type, had only minor influence on epiphytic species composition and richness. The results of the present study indicate a need to maintain the diversity of tree species and large trees, particularly Acer platanoides, Carpinus betulus, Fraxinus excelsior, Populus tremula, Tilia cordata, Ulmus glabra and Ulmus laevis in conservation of epiphytic bryophyte and lichen communities in the future.     

Up in the Tree – The Overlooked Richness of Bryophytes and Lichens in Tree Crowns

Assessing diversity is among the major tasks in ecology and conservation science. In ecological and conservation studies, epiphytic cryptogams are usually sampled up to accessible heights in forests. Thus, their diversity, especially of canopy specialists, likely is underestimated. If the proportion of those species differs among forest types, plot-based diversity assessments are biased and may result in misleading conservation recommendations. We sampled bryophytes and lichens in 30 forest plots of 20 m × 20 m in three German regions, considering all substrates, and including epiphytic litter fall. First, the sampling of epiphytic species was restricted to the lower 2 m of trees and shrubs. Then, on one representative tree per plot, we additionally recorded epiphytic species in the crown, using tree climbing techniques. Per tree, on average 54% of lichen and 20% of bryophyte species were overlooked if the crown was not been included. After sampling all substrates per plot, including the bark of all shrubs and trees, still 38% of the lichen and 4% of the bryophyte species were overlooked if the tree crown of the sampled tree was not included. The number of overlooked lichen species varied strongly among regions. Furthermore, the number of overlooked bryophyte and lichen species per plot was higher in European beech than in coniferous stands and increased with increasing diameter at breast height of the sampled tree. Thus, our results indicate a bias of comparative studies which might have led to misleading conservation recommendations of plot-based diversity assessments.     

Hidden crown jewels: the role of tree crowns for bryophyte and lichen species richness in sycamore maple wooded pastures

Tree crowns typically cover the vast majority of the surface area of trees, but they are rarely considered in diversity surveys of epiphytic bryophytes and lichens, especially in temperate Europe. Usually only stems are sampled. We assessed the number of bryophyte and lichen species on stems and in crowns of 80 solitary sycamore maple trees (Acer pseudoplatanus) at six sites in wooded pastures in the northern Alps. The total number of species detected per tree ranged from 13 to 60 for bryophytes, from 25 to 67 for lichens, and from 42 to 104 for bryophytes and lichens considered together. At the tree level, 29 % of bryophyte and 61 % of lichen species were recorded only in the crown. Considering all sampled trees together, only 4 % of bryophyte, compared to 34 % of lichen species, were never recorded on the stem. Five out of 10 red-listed bryophyte species and 29 out of 39 red-listed lichen species were more frequent in crowns. The species richness detected per tree was unexpectedly high, whereas the proportion of exclusive crown species was similar to studies from forest trees. For bryophytes, in contrast to lichens, sampling several stems can give a good estimation of the species present at a site. However, frequency estimates may be highly biased for lichens and bryophytes if crowns are not considered. Our study demonstrates that tree crowns need to be considered in research on these taxa, especially in biodiversity surveys and in conservation tasks involving lichens and to a lesser degree also bryophytes.     

Analysis of the distribution of epiphytic lichens within homogeneousFagus sylvatica stands along an altitudinal gradient (Mount Olympos,Greece)

Epiphytic lichen vegetation onFagus sylvatica sas studied in 4 sites along an altitudinal gradient from 930 to 1500 m on SE facing slopes of Mount Olympos (Greece). The crucial factor determining the spatial heterogeneity of epiphytic lichens onF. sylvatica is the altitude and not the height on the trunk at which lichen community is established. 17 out of 26 taxa are confined to a particular elevation range, while another three are clearly ubiquitous in their distribution. The number of lichen species at breast height is higher than at the base of the trunks. The results were compared with those gathered earlier in an analogous study on the vertical distribution of epiphytic lichens onPinus nigra along an altitudinal gradient from 750 to 1510 m of the same mountain. Comparison suggests that spatial heterogeneity of epiphytic lichens onF. sylvatica is different from the one onP. nigra.     

Epiphytic lichen synusiae and functional trait groups in boreo‐nemoral deciduous forests are influenced by host tree and environmental factors

Deciduous forests with temperate broad‐leaved tree species are particularily important in terms of biodiversity and its protection, but are threatened habitats in northern Europe. Using multivariate analyses we studied the effect of forest site type, environmental variables and host tree properties on epiphytic lichen synusiae as well as on the composition of species‐specific functional traits. Epiphytic lichens were examined on Acer platanoides, Fraxinus excelsior, Quercus robur, Tilia cordata, Ulmus glabra and U. laevis in two types of forests: Humulus‐type floodplain forests and Lunaria‐type boreo‐nemoral forests on the talus slopes of limestone escarpment (klint forests). Klint forests located near the seashore were under greater maritime influence compared to floodplain forests located in inland Estonia which experience stronger air temperature contrasts. In addition to stand level and climatic variables, tree level factors (bark pH, trunk circumference and cover of bryophytes) considerably affected the species composition of the lichen synusiae. Overall, 137 lichen species were recorded, including 14 red‐listed species characteristic of deciduous trees. We defined 13 lichen societies and showed their preference to forests of a specific site type and/or host tree properties. In forests of both types, most of the epiphytic lichens were crustose, and had apothecia as the fruit bodies and chlorococcoid algae as the photobiont. However, the proportion of lichens with a foliose or fruticose growth form, as well as the proportion of lichens with vegatative diaspores, were higher in floodplain forests. In klint forests with a stronger influence from the wind, crustose species completely dominated, while species with vegetative diaspores were rare and most species dispersed sexually. Lichens with Trentepohlia as the photobiont were characteristic of these forests, and lichens with lirellate ascomata were prevailing, indicating the great uniqueness of the kint forests for epiphytic lichens in the boreo‐nemoral region.     

Tree and stand level variables influencing diversity of lichens on temperate broad-leaved trees in boreo-nemoral floodplain forests

Tree and stand level variables affecting the species richness, cover and composition of epiphytic lichens on temperate broad-leaved trees (Fraxinus excelsior, Quercus robur, Tilia cordata, Ulmus glabra, and U. laevis) were analysed in floodplain forest stands in Estonia. The effect of tree species, substrate characteristics, and stand and regional variables were tested by partial canonical correspondence analysis (pCCA) and by general linear mixed models (GLMM). The most pronounced factors affecting the species richness, cover and composition of epiphytic lichens are acidity of tree bark, bryophyte cover and circumference of tree stems. Stand level characteristics have less effects on the species richness of epiphytic lichens, however, lichen cover and composition was influenced by stand age and light availability. The boreo-nemoral floodplain forests represent valuable habitats for epiphytic lichens. As substrate-related factors influence the species diversity of lichens on temperate broad-leaved trees differently, it is important to consider the effect of each tree species in biodiversity and conservation studies of lichens. Nomenclature Randlane et al. (2007) for lichens; Leht (2007) for vascular plants.     

Red-listed lichens in Sweden: habitats, threats, protection, and indicator value in boreal coniferous forests

The three major threats to lichens in Sweden; forestry, air pollution, and structural changes in the agricultural landscape, are outlined. Forestry is the most serious. The majority of the red-listed lichens in forests are found in productive forests with a continuity in tree growth, but nearly 70% of the protected area in Sweden consists of alpine landscapes. Examples of important habitats with red-listed lichens are described, e.g. Alnus glutinosa marshes, alvar-vegetation, broad-leaved deciduous forests and different Picea abies forests. The use of selected indicator species of lichens and macrofungi (mainly red-listed species) in boreal coniferous forests provides information on continuity in tree growth of an area, and on earlier influences of forestry. Examples of indicator species for different types of forest are presented and discussed. In spite of the Swedish right of common accesso, collecting of lichens is forbidden without permission from the land-owner. Collecting in protected areas is allowed only with a permit obtained from the authorities.     

Influence of air pollution on the mountain forests along the Tateyama–Kurobe Alpine route

The effects of air pollution on the growth of mountain trees were investigated at Buna-daira (1,180 m a.s.l.), about half the way up Mt. Tateyama, located in Japan. Every year, about 1 million tourists are transported by highland buses through the Tateyama–Kurobe Alpine route. Since the route opened in 1971, some tree species along the road have declined and have been blighted, suggesting that bus exhaust was the cause. However, the level of regional and long-range transboundary air pollution has also increased significantly over the last few decades. The atmospheric NO₂ concentration at the roadside in the forest was highly correlated with the traffic density of buses and penetration of the exhaust into the forest was detected. However, the maximum average NO₂ concentration was lower than 3.5 ppbv during the peak traffic period in the year. At Buna-daira, the total stem cross-sectional area at breast height (BA) of the forest was nearly unchanged from 1999 to 2006, but the BA of Fagus crenata decreased 10% and that of Cryptomeria japonica increased 6%. Neither tree growth nor tree death was significantly correlated with distance from the road. The cause of the decline of F. crenata could not be attributed to the effects of road, i.e., air pollution emitted from the buses or edge effects of the road. This area was more affected by regional, long-range transport of air pollution (O₃, SO₂, etc.). The average atmospheric O₃ concentration in autumn was higher than 40 ppbv and the recent increase in the O₃ concentration may be an important factor of F. crenata decline through the changes in the interspecific relationships between F. crenata and C. japonica, O₃ sensitive and tolerant species, respectively.     

Significant decrease in epiphytic lichen diversity in a remote area in the European Alps,Austria

We present long-term (1993–2010) monitoring results of lichens from a remote site in Austria. Whereas gaseous pollution is negligible in this area, levels of long-range air pollution of S and N via rain and fog are high. Lichen cover on tree trunks have decreased significantly. Accordingly, we found that the population of all species had declined. The analyses demonstrated significant changes in lichen community composition. The lichen flora suffered a significant decrease in diversity. Our hypothesis is that the breakdown of epiphytic lichens is mainly due to eutrophication through long-term N deposition, and more particularly to ammonia in precipitation and in fog. Since many areas in the European Alps receive high wet deposition loads, a decrease in the abundance and diversity of epiphytic lichens is most probably a widespread phenomenon.     

Air pollution as a possible cause for the decline of some phanerogamic species in The Netherlands

In The Netherlands the decline of some phanerogamic species cannot be readily explained from obvious factors such as lowering of the groundwater table, eutrophication or land reclamation. For a number of species the hypothesis was tested that the decline is partly due to air pollution. A two-factor model was made in which decline is accounted for by (a) habitat destruction assessed from topographic maps and (b) air pollution measured as the SO₂ 95-percentile over the winter period 1978/1979. Effects of both factors were assumed to follow a sigmoid dose-effect curve. For a number of species decline proved to be significantly correlated with air pollution. These are notably species from the syntaxon Violion caninae. A comparison was made with results obtained for epiphytic lichens. It appears that for some phanerogamic species sensitivity is about the same as for moderately sensitive lichens.Nomenclature follows Heukels & van der Meijden (1983).Thanks are due to the Rijksherbarium, for providing some of their unpublished data; and to Ada Groeneveld, for technical assistance.     

Stable isotopes of Lithosiini and lichens in Hong Kong show the biodindicator potential of lichenivorous moths

Urban landscapes provide unique environments for a wide variety of plants and animals, but their suitability may be limited by anthropogenic impacts such as pollution. We examined the potential utility of lichen and lichen-feeding moths as biodindicators of air pollution in Hong Kong by comparing carbon (C) and nitrogen (N) stable isotope values in lichens, lichenivorous and non-lichenivorous moths (Lepidoptera: Erebidae) and a moth outgroup (Lepidoptera: Geometridae). Our results show that stable isotope values for C and N were similar for lichens and lichen feeding moths, while non-lichen feeding moths formed a distinct group. In addition, we found consistent δ¹³C and δ¹⁵N values across moth body parts, indicating that any portion of the specimen is suitable for isotopic fingerprinting. Our results highlight that lichen feeding moths may be useful for integrating signals of atmospheric nitrogen pollution and could therefore have utility in monitoring and quantifying air quality over time and space.     

Lichens as air pollution indicators in the metropolitan area of San José, Costa Rica

Lichens were used as air pollution indicators in the metropolitan area of San José, Costa Rica. Transplants showed a positive correlation between the percentage of dead cells in the thallus and the ketone soluble substances deposited on it. Those parts of the city where pollution is greatest (industrial areas and heavy traffic) were also the ones where lichens suffered the most, and in some extreme cases the thallus died after 8 months of exposure. Besides this transplant experiment, the coverage of Parmelia lichens on the bark of several tree species was determined in some areas of the city. The results of these observations suggest that the city of San José has three different kinds of air environment in relation to lichen survival: normal, transitional and desertic, as reported for other cities of the world. The most frequent air pollutants in San José are: CO, CO2, C2H5OH, Cl2, HCl, H2S, H3PO4, H2CrO4, NO, NH3, NH4 Cl, SO2 and Zn.     

Allometric equations to predict the total aboveground biomass of tree species in a planted forest in Egypt

The aim of this study is to estimate the total above‐ground biomass (TAGB), stem height (H), diameter at breast height (dbh) and basal area of five tree species (ages 7‐8 years) irrigated by municipal sewage water in the Egyptian‐Chinese friendship forest, Sadat City, Egypt. From the biomass data that obtained through destructive sampling, models for predicting aboveground biomass were developed. The highest values for stem density and height were estimated for Eucalyptus citriodora, while the lowest value for density was obtained for Dalbergia sissoo and stem height for Khaya senegalensis. The highest values for basal area and dbh were obtained for Casuarina spp., while the lowest values were recorded for Dalbergia sissoo. Eucalyptus camaldulensis had the highest stand stem biomass and TAGB (55.5, 83.9 t DW ha^‐1, respectively). In addition, Casuarina spp. had the highest leafy branches biomass (32.5 t DW ha^‐1) while Dalbergia sissoo had the lowest values for all tree components. All the generated allometric equations had high correlation coefficients at high probability levels. Moreover, the results revealed that not only the dbh data can be used as independent variable for biomass determination, but also stem height and size index are recommended for biomass estimation (© 2012 WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim)     

Corticolous lichens as environmental indicators in urban areas in southern Brazil

Lichens are considered bioindicators and, as such, are widely used for air quality monitoring, especially in urban-industrial areas. The present paper proposes an evaluation of lichen communities in urban areas. The corticolous lichen community was assessed at 29 sampling stations in the city of Porto Alegre, in addition to a reference area located in the State Park in the city of Viamão, southern Brazil. The rubber band method was used for lichen mapping; three hundred host-trees were analyzed, at 11 different height levels. Lichens were evaluated in terms of composition, richness, cover and diversity, and sampling stations were classified based on the Index of Atmospheric Purity (IAP) complemented by the Environmental Classification Factor (ECF). The inclusion of ECF as a complement to the original IAP formula is proposed in the present study and not only richness and cover components are considered, but also data on the lichenized mycota composition (considering its different morphological forms). One hundred and thirty-one (131) taxa have been identified, out of which 13 specimens may be considered as indicators of urban areas, and the predominance of taxa belonging to the crustose and foliose morphological group was verified. The sampling stations were classified into five zones, ranging from lichen-free zones to optimal zones for lichen development. The use of lichen proved to be efficient to both evaluate air quality and identify alterations of urban microclimates. The application of an ECF-based correction factor is expected to complement the use of IAP, making it a more sensitive index, since an analysis of a multivaried information profile was deemed necessary, especially in regions where specimen diversity is higher.