Description of spatial and temporal
distributions of epiphytic lichens
by Håkan Lättman
Linköping University and Södertörn University College LiU–Tek–Lic–2008:6
Front cover: Ramalina fastigiata (rosettbrosklav) photo by the author © Håkan Lättman 2008 ISBN 978–91–7393–967–6 ISSN 0280–7971 Printed by LiU-Tryck Linköping, Sweden, 2008
Biology, IFM Rapporttyp Report category X Licentiatavhandling Examensarbete C-uppsats D-uppsats Övrig rapport _ ________________ Språk Language Svenska/Swedish X Engelska/English _ ________________ Titel/Title
Description of spatial and temporal distributions of epiphytic lichens
Författare/Author Håkan Lättman
Sammanfattning/Abstract
Lichens are, in most cases, sensitive to anthropogenic factors such as air pollution, global warming, forestry and fragmentation. Two studies are included in this thesis. The first is an evaluation of the importance of old oak for the rare epiphytic lichen Cliostomum corrugatum (Ach.) Fr. This study analysed whether C. corrugatum was limited by dispersal or restricted to tree stands with an unbroken continuity or the substrate old oaks. The results provide evidence that the investigated five populations in Östergötland, Sweden, of C. corrugatum exhibit substantial gene flow, an effective dispersal and a small genetic variation between the sites. Most of the genetic variation was within the populations. Thus, C. corrugatum is more dependent of the substrate old oaks, rather than limited by dispersal. The second study investigated possible range shift of some common macrolichens, due to global warming, from 64 sites in southern Sweden comparing the two years 1986 and 2003. The centroid of three lichen species had moved a significant distance, all in a north east direction: Hypogymnia physodes (L.) Nyl. and Vulpicida pinastri (Scop.) J.-E. Mattsson and M. J. Lai on the tree species Juniperus communis L. (50 and 151 km, respectively) and H. physodes on
Pinus sylvestris L. (41 km). Considering also the non-significant cases, there is strong evidence for a prevailing NE direction of centroid movement.
ISBN 978–91–7393–967–6
____________________________________________ _________
ISRN
_________________________________________________________________
Serietitel och serienummer ISSN 0280–7971
Linköping studies in science and technology, LIU–TEC–LIC–2008:6
Thesis No. 1348
____________________________________
Nyckelord/Keyword
centroid, continuity, direction, dispersal, ecological continuity, establishment, global change, global warming, habitat availability, lichen, movement, range shift
Datum Date 2008–04–11
URL för elektronisk version Institution
Abstract
Lichens are, in most cases, sensitive to anthropogenic factors such as air pollution, global warming, forestry and fragmentation. Two studies are included in this thesis. The first is an evaluation of the importance of old oak for the rare epiphytic lichen
Cliostomum corrugatum (Ach.) Fr. This study analysed whether C. corrugatum was
limited by dispersal or restricted to tree stands with an unbroken continuity or the substrate old oaks. The results provide evidence that the investigated five populations in Östergötland, Sweden, of C. corrugatum exhibit substantial gene flow, an effective dispersal and a small genetic variation between the sites. Most of the genetic variation was within the populations. Thus, C. corrugatum is more dependent of the substrate old oaks, rather than limited by dispersal. The second study investigated possible range shift of some common macrolichens, due to global warming, from 64 sites in southern Sweden comparing the two years 1986 and 2003. The centroid of three lichen species had moved a significant distance, all in a north east direction: Hypogymnia physodes (L.) Nyl. and Vulpicida pinastri (Scop.) J.-E. Mattsson and M. J. Lai on the tree species
Juniperus communis L. (50 and 151 km, respectively) and H. physodes on Pinus
sylvestris L. (41 km). Considering also the non-significant cases, there is strong
Table of contents
ABSTRACT ... 1 TABLE OF CONTENTS ... 2 LIST OF PAPERS... 3 INTRODUCTION ... 4 LICHENS... 4 DISPERSAL STRATEGIES... 4HUMAN-INDUCED THREATS ON LICHENS... 4
Air pollution... 4 Global warming ... 5 Forestry... 5 Fragmentation ... 5 OBJECTIVES... 6 METHODS ... 7 STUDY SITES... 7 Paper I ... 7 Paper II ... 7 STUDIED SPECIES... 8 Paper I ... 8 Paper II ... 9 LABORATORY METHODS... 10 Paper I ... 10 ANALYSES... 10 Paper I ... 10 Paper II ... 10
RESULTS AND DISCUSSION... 12
Paper I ... 12 Paper II ... 12 ACKNOWLEDGEMENT ... 14 REFERENCES ... 15 PAPER I ... 18 PAPER II ... 40
List of papers
The following papers are included in the thesis and are referred in the text by their Roman numerals.
Paper I Habitat availability is likely to limit the occurrence of the rare lichen
Cliostomum corrugatum. Manuscript.
Paper II Spatio-temporal range shift of epiphytic lichens within a distribution area. Manuscript.
Introduction
Lichens
Lichen symbiosis always consists of a fungus and an algae or cyanobacteria. In some cases, both algae and cyanobacteria are present together with the fungus. The nature of the symbiotic relationship has been under consideration. Questions have been raised whether it is a mutualistic symbiosis or parasitic. It appears that the fungus sometime acts like a parasite on algae and cyanobacteria; in other cases it is not. Algae and cyanobacteria live in either facultative or obligate association together with the fungus. In the obligate relationship, algae and cyanobacteria do not act as free living organisms; consequently, they are dependent on the fungus. Both sexual fungal spores and many different types of asexual propagules are produced by lichens and serve as dispersal units. (Nash et al. 2002)
Dispersal strategies
The fungal partner in lichens reproduces sexually with spores like other fungi. After fertilization between two different mating types, ascospore production is established. During sexual reproduction, it is usually only the fungal ascospores that act and function as dispersal units. (Mattsson 1997)
Lichens furthermore have the ability to disperse asexually and in those cases fungi and algae and/or cyanobacteria disperse together. Soredia and isidia are two examples of asexually produced dispersal units. Soredia are microscopic globule shaped and usually originate from the algae layer. Isidia are small outgrowths which have a similar internal structure as the thallus. (Nash et al. 2002)
Animals are one type of vector for some lichens to disperse (Bailey 1970; Stubbs 1995), another is the wind (Hansson et al. 1992). The total numbers of dispersed ascospores increase with decreased ascospore size, i.e., small spores often disperse over a greater distance.
Usually, most lichen ascospores are small, approximately 1–30 µm. The ascospores of lichens have often been assumed to have almost unlimited possibilities to disperse over great distances (Hansson et al. 1992). Larger spores and most asexual propagules, that are often larger than ascospores, are supposed to disperse over a short distance. Thus, they should contribute mainly to population growth and stability on the site rather than to dispersing species over a long distance (Hansson et al. 1992).
Human-induced threats on lichens
Air pollution
Soon after the industrial revolution of Europe in the late 18th century, air quality started to change. Sulphur dioxide (SO2) emission and deposition firmly increased from the early 20th century (Erisman and Draaijers 1995; Mylona 1996). Emission of substances with anthropogenic origin has been shown to have a negative impact on the lichens. Sulphur dioxide is one of the most lethal substances for lichens and is largely supposed to be responsible for most of the decrease and death of lichens (Gilbert 1968).
Due to international co-operation to reduce the effects of air pollutants on the environment, a dramatic decrease of, e.g., sulphur dioxide has been possible in the last
decades (UNECO 1999). Schopp et al. (2003) have predicted a continued decrease of sulphur dioxide in Europe to the end of 2030. Recolonization of lichens in London has been shown by (Hawksworth and Mcmanus 1989) and was attributed to the decrease of sulphur dioxide. Taking those aspects in mind, sulphur dioxide is probably a minor problem for lichens in the near future.
Global warming
During the last decades, many studies on global warming have revealed its great impact on organisms (Vitousek 1994; Hughes 2000; Saxe et al. 2001; Parmesan and Yohe 2003; Root et al. 2003; Sanz-Elorza et al. 2003; Thuiller et al. 2005; Parmesan 2006). In a study from the Netherlands, van Herk et al. (2002) revealed that lichens respond to global warming. The results suggest that epiphytic lichens on trees, and other transient substrates, are likely to respond relatively quickly to large-scale change of climate. van Herk et al. (2002) used checklists, data from field meetings, herbarium material and long-term monitoring data to study large-scale changes of lichens. The study was based on the documentation of 329 lichen species collected in 1979, 1984, 1989, 1995 and 2001. The proposed conclusion is that lichens with a northern distribution and a southern distribution limit in the Netherlands have declined. On the other hand, species with a southern distribution are at present invading the country. Epiphytic lichens have been shown to respond quickly to a changing climate and are therefore an important tool for detecting such changes. One of the problems why the progress of research on global warming has been slow is the shortage of available datasets and that methods have focused on species distribution limits.
Forestry
Forestry practices in Sweden have changed during the last centuries. Different kinds of forestry operations have different impact on the forest as a habitat for non-target organisms. Out of all land area (41.3 million ha) in Sweden, 23 million ha consists of production forest (NBF 2007). The human impact on production forest is significant and managed, mainly, in a way to preserve economic values. Prevailing forest management is not always in line with the necessary life conditions for lichens dependent on old tree trunks, as the latter have become scarce. Thus, the change in the demography of the forest towards a greater proportion of younger tree is a negative factor for many lichen species.
Different habitats are required for different lichen species. Some common lichens do not demand a specific substrate, e.g. Hypogymnia physodes (L.) Nyl. that inhabit both rocks and tree trunks of different tree species and sizes, and even steel and rubber (own field observations). Other lichens demand a specific habitat or a specific substrate (Paper I). Production forestry management can be a problem for those lichens that demand old tree trunks as their habitat and have dispersal limitations. Knowledge is often lacking about whether it is dispersal or the substrate that is the limiting factor for a specific lichen to survive. This is of most importance and requires more research. Fragmentation
Humans use more land area as population increases. As a consequence, the amount of available habitat for other organisms decreases. Furthermore, remaining habitats become fragmented and thus divided into patches often bordered by different kinds of intense human activity, like agriculture, urban areas, roads and railway tracks.
increased areas of edge habitats. This may have a negative impact on lichen biodiversity (Turner 1996). Thus, fragmentation of forests is a problem for some lichens.
Objectives
The objectives and questions raised in this thesis are:
• Is the crustose lichen Cliostomum corrugatum (Ach.) Fr. restricted to sites with long temporal continuity or to sites where the substrate and microhabitat meet the certain ecological requirements needed for the species? Molecular methods, an intron situated at the end of the SSU on the RNA gene, were used to answer this question.
• Are there any temporal dispersal trends, distance and direction, of common epiphytic lichens on trees during the last decades in southern Sweden?
Methods
Study sites
Paper I
The studied sites in both Papers I and II are situated in the southern part of Sweden. In Paper I, five sites in the county of Östergötland were selected for sampling (Fig. 1).
Paper II
64 sites in Götaland (except Öland and Gotland) and southern parts of Svealand were selected for sampling in Paper II (Fig. 2). The methods in Papers I and II are briefly presented below; for further details see the papers.
Figure 2. The 64 sites in Paper II, surveyed in 1986 and 2003.
Figure 1. The five sites where Cliostomum corrugatum was sampled for Paper I.
Paper I
The epiphytic lichen Cliostomum corrugatum Ascomycota, Lecanoromycetes, Lecanorales, Ramalinaceae (Fig. 3) was studied on five sites. The thallus has
conspicuous, light yellow to light brown apothecia, as well as black pycnidia (Thor et al. 1999). In Sweden, its geographical distribution largely follows that of Quercus robur L. Cliostomum corrugatum is rare in northern Europe and red-listed in, e.g., Sweden (near threatened), Denmark (vulnerable), and Finland (near threatened). The lichen has a distinctive morphology and habitat preferences that makes it relatively easy to detect in the field.
Lättman et al. (2006a) showed in a study made in the county of Östergötland, Sweden, that the smallest oak tree inhabited by C. corrugatum had a circumference at breast height (CBH) of 204 cm. A tree trunk of this size is at least 100 years old (Lättman et al. 2006a). Most abundant were C. corrugatum on oak trees with a size class CBH 330–377 cm (Lättman et al. 2006a). A similar study made by Lättman et al. (2006b) showed that the smallest oak tree with fertile (observed apothecia) individuals of C. corrugatum had a CBH of 239 cm. The study also showed that the time from which spores were possible to produce their own spores that would be a lichen generation was approximately 20–40 years.
Figure 3. The site Solberga (left) is an example of a typical environment
inhabited by Cliostomum corrugatum; a close-up of the lichen (right). Photo:
A resent study made by Johansson et al. (2008) in the county of Östergötland, Sweden showed that, by all investigated factors, CBH was the most important factor for C.
corrugatum (p-value <0.001) (Fig. 4). Johansson et al. (2008) chose to investigate the
lichens Calicium adspersum, Chaenotheca phaeocephala, Chrysothrix candelaris, C.
corrugatum, Evernia prunastri and Parmelia sulcata. Cliostomum corrugatum was the
one colonizing the oaks last in the succession stages. An oak has to reach the size CBH >300 cm before the probability of occurrence of C. corrugatum, which was the most demanding species, reached 50 % (P50 value).
Samples of C. corrugatum were collected on tree trunks of Quercus robur in 2005. Pair-wise distances between the five sites were evenly distributed and ranged from 6.5 to 83 km. The smallest tree trunk’s CBH, of 618 surveyed that were inhabited by C.
corrugatum, was 204 cm. To avoid the risk of sampling the same individual twice only
one sample was taken per tree. Paper II
In 1986 and 2003, 64 sites were sampled for all present lichens on all present tree species and wood. The sites were originally selected by Jan-Eric Mattsson for a study of the lichen genus Vulpicida. He selected the sites based on herbarium specimens of
Vulpicida collected during a period of about one hundred years. A total of 56 lichen
species, 22 tree species and dead wood where used in the analyses. Most of the lichen species were widespread and abundant with some exceptions, e.g.; Melanelia
laciniatula (Flagey ex H. Olivier) Essl. and Usnea barbata (L.) Weber ex. F. H. Wigg
(Thor et al. 1999), which both are red-listed. The species are, with a few exceptions, Figure 4. An oak trunk must have a circumference at breast height
(CBH) > 300 cm to reach 50% probability of carrying Cliostomum
corrugatum. The study, conducted in Östergötland, was based on 858 oaks in two areas. Cover 1 (solid line) represents lichen
occurrence, cover 2 (broken line) lichen cover of >10 cm2 and
foliose or fruticose but some are crustose. Some of the species are habitat generalists and may occur on several of the tree species surveyed, as well as on rock.
The sites span a wide range of ecological habitats with no apparent bias towards a particular tree diameter (successional stage). The sites were of different sizes ranging from a single tree to one hectare and often delimited by natural boundaries such as creeks or ridges, or by man-made ones such as fences, or differences in land use. The habitats of the sites are among the most common in southern Sweden i.e. coniferous, deciduous and mixed forests, wooded pastures grazing land, parks, and also, in a few cases also trees in towns, villages and farms.
Tree trunks, branches and twigs, were examined to a height of 2 meters above ground in search of all epiphytic macrolichens. On each site, all epiphytic lichen species were collected on all occurring tree species. The number of tree species per site varied from one to eleven and the aim was to investigate ca 50 trees with lichens at each site.
Laboratory methods
Paper I
Laboratory methods on Cliostomum corrugatum where carried out at the Department of Biology, University of Bergen, Norway, during the spring of 2005. DNA extraction, PCR amplification, and sequencing on C. corrugatum followed (Lindblom and Ekman 2006), with a few exceptions. Initial trials where taken to sequence the IGS gene. Unfortunately, the haplotype variation was too small and a decision was taken to choose another gene. The second candidate was ITS but the test on the gel of PCR product showed two bands instead of one. The SSU intron was shown to have a suitable variation and was used in subsequent analyses.
A group 1 intron situated between positions 1516 and 1517 at the end of the small subunit (SSU) of the nuclear ribosomal RNA gene was used in the study (Gargas et al. 1995). This region was amplified using the forward primer ITS1F (White et al. 1990), situated at the end of the SSU but upstream of the intron site, and the newly designed reverse primer ITS1-Cc1-R, situated in the first part of ITS1.
Analyses
Paper I
Different methods where used to analyse the genetic variation of the haplotypes on the gene flow between the five populations. To estimate the genetic exchange between the populations, a coalescent simulation implemented in LAMARK was used. A Mantel test was used to evaluate if any correlation between a matrix on pair-wise genetic distance and a matrix of pair-wise geographic distance. This is a test of the hypothesis; is genetic distance independent of geographic distance? With AMOVA, the genetic differences between the populations where tested. A haplotype network was constructed to illustrate the relationship present in the sample.
Paper II
The spatio-temporal data were analysed with a permutation procedure in Excel, using a newly written Visual Basic Macro written by Michael W. Palmer. The macro involved a
permutation procedure to assess whether changes of distance, of the centroid between the two years was greater than expected due to chance. Each combination of lichen and tree species was analyzed separately.
Results and discussion
Paper I
The lichen Cliostomum corrugatum was represented by eleven haplotypes of the studied SSU intron. Out of the 96 samples, 85 were used in the statistical analyses. Hence a loss of 11 samples occurred because of difficulties to amplify and sequence the gene in the laboratory. The length of the alignment on the SSU intron was 614 nucleotides including gaps. Ten positions were variable.
The coalescent simulation showed that the gene flow is considerable between the five investigated sites in spite of uncertainty in the data due to the small dataset. The coalescent simulation suggests that a scenario of low genetic exchange is unlikely. The Mantel test showed no significant correlation between the two matrices: genetic and geographic distances. Thus, the dispersal between the populations on the investigated sites is effective. The AMOVA showed that 0.4 % of the variance is between populations and 99.6 % within populations. An indication of the result is that the five populations behave more or less as a single panmictic population because of the small genetic variation between the five populations. Thus, C. corrugatum exhibits substantial gene flow, an effective dispersal and a small genetic variation between the sites. All in all, results point in the same direction: C. corrugatum does not seem to have any difficulties to disperse between the five investigated sites. The results proposed are that the rare lichen C. corrugatum appears to be limited in the amount of suitable habitat and not by the ability of the species to disperse.
Paper II
The surveys from 64 sites in southern Sweden in 1986 and 2003 showed that the centroid of two lichen species had moved in a north easterly direction. Thus, the centroid movements of the lichens Hypogymnia physodes (L.) Nyl. and Vulpicida
pinastri (Scop.) J.-E. Mattsson and M. J. Lai on the tree species Juniperus communis L.
were 50 km and 151 km (p-value 0.0258, 0.0002) with the direction 26.9° and 47.7°, respectively. The movement of lichen centroids by Hypogymnia physodes on the tree species Pinus sylvestris L. was 41 km (p-value 0.0066) with the direction 30.5°.
The centroid movements of the three cases that turned out to be significant, was in a NE direction. The cumulative distribution of all possible pair-wise directions between the 64 sites was calculated. Furthermore, a corresponding cumulative distribution was compiled from all the permuted directions. Instead of a straight line, which would be the case if all investigated sites were symmetrically arranged (i.e. if they where arrange in straight rows and columns with the same distance between sites), there are two soft bumps that are due to the shape of the 64 investigated sites which together have an area that is elongated (Fig. 2).
It is clear that most of the centroid movements are going in a north east/south west direction with 16 and nine respectively (Fig. 5).
In the opposite diagonal direction, north west/south east, there are only two versus three cases. One possible explanation to the great majority north east/south west direction is the prevailing wind direction in Sweden. Thus, the great majority wind direction in Sweden makes the lichens and their centroid movements more favourable. Another possible explanation could be the shape of the investigated area.
Figure 5. Two inventories conducted on epiphytic lichens with present/absent data from 64 sights in southern Sweden 1986 and 2003. Thirty possible cases were possible to conduct out of witch three turned out significant.
Acknowledgement
I am most grateful to my supervisors Jan-Eric Mattsson and Per Milberg, this because of the tremendous support, encouragement and help to make the right decisions. Thanks to you both. Thanks to Yann Bertrand and Ivailo Simoff for nice discussions and Yann for your hospitality. Lars Westerberg and Karl-Olof Bergman thanks for taking your time and answers to all my questions. Agneta Rundgren helped me with some administrative PhD-stuff and made me feel welcome at Linköping University. Thanks to room mates Nicklas Jansson at Linköping University and Fredrik Hårdeman, Anna Edlund and Emma Eklöf at Södertörns University Collage. Anders Göthberg and Hasan Dzuho thanks for your help. Thanks Johan Bergstedt for interesting conversations and snus-support. Kristina Articus and Anders Nordin many thanks for your help with the identification of lichens in the genera Bryoria, Melanelia and Usnea. Great thanks to Dan Wahlström for taking your time to answer my questions on fungi and for lending me literature on ditto. The group members of Quercus-gruppen and Växt Ekologiskt Forum, thanks for your input on my work. From Randolph Kricke, University Duisburg-Essen, Germany, I borrowed a pH meter, thanks. Thanks everyone, not mentioned above, at IFM Biology, Linköping University and School of Life Science, Södertörns University Collage. Last but not least, I want to thank Åsa and my children for just being around.
Håkan Lätman January 2008
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