Studies on spatial and temporal distributions of epiphytic

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Linköping Studies in Science and Technology Dissertation thesis No. 1471

Studies on spatial and temporal distributions of epiphytic

lichens

Håkan Lättman

School of Life Science

Södertörn University SE-141 89 Huddinge, Sweden

Department of Physics, Chemistry and Biology Division of Ecology

Linköping University SE-581 83 Linköping, Sweden

Linköping, October 2012

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Linköping Studies in Science and Technology ISBN 978–91–7519–810–1

ISSN 0345–7524 Printed by LiU-Tryck Linköping, Sweden, 2012

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List of papers

The following papers are included in the thesis and are referred in the text by their Roman numerals:

Paper I Lättman H, Brand A, Hedlund J, Krikorev M, Olsson N, Robeck A, Rönnmark F & Mattsson J-E. (2009) Generation time estimated to be 25–30 years in Cliostomum corrugatum (Ach.) Fr. The Lichenologist 41:

557–559.

Paper II Lättman H, Lindblom L, Mattsson J-E, Milberg P, Skage M & Ekman S (2009) Estimating the dispersal capacity of the rare lichen Cliostomum corrugatum. Biological Conservation 142: 1870–1878.

Paper III Lättman H, Milberg P, Palmer MW & Mattsson J-E (2009) Changes in the distribution of epiphytic lichens in southern Sweden using a new statistical method. Nordic Journal of Botany 27: 413–418.

Paper IV Lättman H, Bergman K-O, Rapp M, Tälle M, Westerberg L & Milberg P. Biodiversity in the wake of urban sprawl: loss among epiphytic lichens on large oaks. Submitted manuscript.

Published papers are reproduced with kind permission from the publishers.

My contributions to the papers

I have, together with the co-authors, designed all field work for Paper I–II and IV. I

performed all field work by myself for Paper II, about half in III–IV and in

collaboration with the other authors for Paper I. I also made DNA extractions, PCR

amplification and sequencing for Paper II as well as editing and alignment. I made all

the statistical analyses in Paper I as well as parts of the analyses in Paper II and IV. I

have been writing most of Paper III–IV, and contributed to Paper I–II.

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Abstract

Lättman, H. 2012. Studies on spatial and temporal distributions of epiphytic lichens Doctoral dissertation

Lichens are an important group of organisms in terms of environmental issues, conservation biology and biodiversity, principally due to their sensitivity to changes in their environment. Therefore it is important that we develop our understanding of the factors that affect lichen distribution. In this thesis, both spatial and temporal distributions of epiphytic lichens at different scales have been studied in southern Sweden.

Generation time of the red-listed lichen Cliostomum corrugatum was examined using Bjärka-Säby as the study site. The results showed that the average age of an individual of C. corrugatum is 25–30 years at the onset of spore production.

The rarity of C. corrugatum was also examined. DNA analysis of an intron from 85 samples, collected at five sites in Östergötland, yielded 11 haplotypes. Results from coalescent analysis, mantel test and AMOVA indicated that C. corrugatum have a high ability to disperse. The study concluded that its rarity is most likely connected with the low amount of available habitat, old Quercus robur.

The changes in the distribution of epiphytic lichens in southern Sweden, between 1986 and 2003, were also compared. For each year a centroid was calculated on all combinations of tree and lichen species. The three significant cases showed that the centroid movement pointed toward a north-east or north-north-east direction.

Finally differences in species richness and cover of lichens on large Q. robur were examined between urban and rural environment. The results demonstrated that species number and percent cover was significantly higher on oaks standing rural compared to oaks standing urban. Effects of urban sprawl showed a decline in species richness and cover with increasing age of the surrounding buildings.

Keywords: centroid, Cliostomum corrugatum, direction, dispersal, generation time, global change, habitat availability, lichen, movement, Quercus robur, range shift, urban

Authors address: Håkan Lättman, School of Life Sciences, Södertörn University, SE-141 89 HUDDINGE, Sweden; IFM Division of Biology, Linköping University, SE-581 83 LINKÖPING, Sweden.

E-mail: hakan.lattman@sh.se; hakan.lattman@liu.se

ISSN 1652–7399

ISBN 978–91–7519–810–1

ISSN 0345–7524

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Introduction

Lichens are amazing, fascinating and slightly peculiar organisms. They can be described as small ecosystems in their own right, in which several groups of organisms live together in the same body (Bates et al. 2011). This symbiosis is sensitive to changes in the external environment and therefore is an important model in providing answers to many of our questions concerning the environment. Throughout the history of the Earth the environment has constantly been changing in response to various causes.

Undoubtedly, today humans have had the greatest impact on the environment (Vitousek et al. 1997, Foley et al. 2005) and species diversity (Jenkins 2003). The development of human civilisation has resulted in a widespread exploitation of nature with significant degradation effects, including recent global climatic changes (Vitousek et al. 1997).

Due to mankind’s large and unprecedented impact on our surrounding, it has been suggested that the current geological epoch Holocene has come to an end and that we are now entering Antropocene (Zalasiewicz et al. 2008). Due to our actions, more and more of the Earth’s surface is exploited, resulting in an increasing habitat loss and fragmentation of the remaining habitats. This has led to the decline in abundance and distribution of many species, and also their extinction in several cases (Gonzalez et al.

1998).

In order to understand and predict how species will respond to human activities in natural communities, basic knowledge about species behaviour is vital. It is also important to study their different requirements i.e. sunlight, chemical composition of the atmosphere, temperature, humidity and the choice of substrate in order to conserve biodiversity. How environmental changes will affect individual species are difficult to predict. Many species’ environmental requirements are not fully understood and therefore it is important to be able to draw general conclusions. The environmental impact on a species can in turn affect other species to form a chain reaction where more and more species will be affected either positively or negatively. In Europe especially, the broad-leaved forests have been affected by human disturbance (Hannah et al. 1995).

Many lichens, insects, and fungi are dependent on these forests and are unable to extend

their range to other habitats. Globally, lichens are a group of organisms that have been

less studied than other comparable multi-cellular organisms. Thus, there is a gap in the

scientific knowledge concerning lichen species’ dispersal capacity and establishment on

different substrates, their habitat requirements, and population structure. Our lack of

knowledge of lichens is probably explained by their inconspicuousness and their small

thalli, which may make them difficult to identify. This might also explain why Carl von

Linné (1707–1778) effectively ignored lichens. Fortunately, his protégé, Erik Acharius

(1757–1819), made great progress by identifying many lichen species, estimating them

to comprise of more than 300 taxa (Krempelhuber 1867). In Sweden today there are

more than 2400 known taxa (Feuerer 2009). Hale (1974) reported the worldwide

number of lichen species to be approximately 17000. Ten years later Hawksworth and

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Hill (1984) reported the number to be 13500. At present there are 18803 described lichen species (Feuerer 2009). The reported number of lichens occurring on Earth is probably underestimated. Swedish lichens and flora are well-studied in comparison with other countries, and contains a large proportion of the worlds lichens (Table 1). Shown in Table 1 is the total number of species of some groups of organisms in Sweden (Gärdenfors 2010) and worldwide (Chapman 2009) and the proportion in Sweden. It is almost certainly an exaggeration that 13% of the earth lichen species exist in Sweden, and is an artefact of this extensive local analysis. It is worth noticing the large proportion of moss and mushroom species that are also present in Sweden which are also probably due to a large number of undescribed species worldwide.

Table 1. Total number of species in Sweden and worldwide for ten major groups of organisms.

Groups of organisms Sweden Worldwide Proportion of species (%)

Lichens 2419 18803

^¤

12.86 Mosses 1049 16236 6.46

Mushrooms ~5000 98998 5.05

Birds 253 9990 2.53

Insects 23900 ~1000000 2.39

Arachnids 1821 102248 1.78

Mammals 63 5487 1.15

Vascular plants 1556 281621 0.55

Fishes 142 31153 0.45

Amphibians & reptilians 19 15249 0.12

¤ Number taken from Feuerer (2009).

What is a lichen?

Lichen symbiosis always consists of a mycobiont and photobiont. The mycobiont is a fungus, mostly an ascomycete, but in some lichens it is a basidiomycete. A photobiont that is capable of photosynthesis is an algae or a cyanobacterium. In some lichens, both an algae and a cyanobacterium are present together with the fungus. There is one lichen described in which the algae belong to phaeophyceae (Sanders et al. 2004). The different organisms belong to different kingdoms and include two domains. The nature of the symbiotic relationship is not trivial. It appears that the fungus sometime acts like a parasite on the photobiont (Brodo et al. 2001). In other lichens, however, the

relationship should be considered mutualistic. Both the mycobiont and photobiont can be obligately or facultatively associated with the symbiosis. When the association is obligate, the mycobiont and photobiont can only occur in the lichenized stage which is the stage that describes the symbiosis while in the case of facultative association the organisms may either be free living or a part of the symbiosis (Nash III 1996).

Dispersal strategies

The fungal partner in lichens reproduces sexually with spores like other fungi. After

fertilization between two different ascomycete mating types, ascospore production is

established. When talking of sexual reproduction of lichens, it is only the fungal

ascospores that act and function as dispersal units, this is referred to as mycobiont

dispersal. Lichens furthermore have the ability to disperse asexually and in those cases

fungi and photobiont disperse together in a process called vegetative dispersal. Soredia

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and isidia are two examples of asexually produced dispersal units. Soredia are

microscopic globule-shaped units that usually originate from the algae layer and consist of singular algal cells surrounded by some fungal hyphae. Isidia are small outgrowths on the cortex of the lichen that have a similar internal structure as the thallus. Moreover, the thallus in some lichens gets easily fragmented and small pieces of the thallus may disperse from one location to another. Dispersal is when sexually and asexually produced units move from one place to another often away from their place of origin.

Successful dispersal is when vegetative dispersal units or spores from the mycobiont succeed in finding a suitable algae at the new site and establish a relichenization. Thus, dispersal is never successful unless spores or vegetative diaspores (e.g. isidia, fragments of the thallus or soredia) spread and establish functional thalli on uncolonized patches.

The spores and vegetative diaspores of lichens disperse from one site to another by means of both biotic and abiotic vectors. Ants and oribatide mite are examples of biotic vectors (Bailey 1970, Stubbs 1995), while the wind is an abiotic vector (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 than large spores. Usually, most lichen ascospores are small, approximately 1–30 µm. The ascospores of lichens are often assumed to have unlimited dispersal over great distances (Hansson et al.

1992). Large ascospores and most vegetative diaspores are supposed to disperse over a shorter distance. Thus, they mainly contribute to population turnover at a site rather than to dispersal of the species over a longer distance (Hansson et al. 1992). Long distance dispersal (LDD) of ascospores and eventually vegetative diaspores of lichens is necessary in order to expand a species distribution; Nathan (2006) discussed LDD for plants and claimed the importance of extreme weather events to ensure LDD; this may also apply to lichens.

Dispersal of lichens is the activity when the spores or vegetative diaspores of an individual move from one place to another. To establish offspring in new habitats, fast dispersal over long distances may be promoted by easily spread diaspores. This dispersal may be passive or active. The passive dispersal refers to a situation when a vector, e.g., wind, water or animals carries the diaspore. Active dispersal does not occur in lichens but it describes the process when the individual itself actively moves to another site. Conditions such as a high density and high competition are known to influence individuals of certain species to engage in acts of active dispersal (Johst &

Brandl 1997, Bowler & Benton 2005). The success of the dispersal is related to the abundance of acceptable habitats and substrates.

The results of studies examining the distance that different lichen species are able to disperse differ. Tapper (1976), Armstrong (1987, 1990), Heinken (1999) and Lorentsson and Mattsson (1999) have shown that dispersal can range up to a few hundred meters. Dispersal limitation has also been reported for lichens on trees, e.g., within tree stands, between compact tree stands, or between trees up to a few kilometres apart (Dettki et al. 2000, Sillett et al. 2000, Hilmo & Såstad 2001, Johansson & Ehrlén 2003, Walser 2004, Öckinger et al. 2005). However, genetic studies of Xanthoria parietina and Lobaria pulmonaria suggest that they indeed have efficient dispersal within a few kilometres radius and furthermore, there was no sign of any of them being dispersal-restricted (Lindblom & Ekman 2006, 2007, Wagner et al. 2006, Werth et al.

2006a, 2006b). At a large spatial scale, for populations separated by hundreds of

kilometres or more, genetic studies of lichen populations have revealed considerable

gene flow (Printzen et al. 2003, Palice & Printzen 2004, Walser et al. 2005), whereas

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studies relying on biogeographic patterns (Munoz et al. 2004), trapping of lichen fragments in the atmosphere (Harmata & Olech 1991) and observations of lichen fragments on bird feet (Coppins & James 1979) concluded that effective dispersal was frequent. Finally, the small size and weight of the ascospores has been taken as indirect evidence that lichens are able to disperse widely (Nordén & Appelqvist 2001).

Enduring harsh environments, yet also sensitive

Lichens can give us answers to many questions regarding changes in the environment caused by humans since they are sensitive and respond more or less instantly. One explanation for this sensitivity to human activities is the complex structure of the symbiosis. However, somewhat paradoxically, this is also the key to their survival in very harsh environments. The association between the mycobiont and the photobiont in lichens has been a successful relationship lasting at least 4 × 10

⁸

years (Taylor 1995). In partnerships, the two organisms are able to withstand harsh environments that they could not withstand individually. Together they are tough and can survive inhospitable environments where many other organisms have difficulties to survive. For example lichens occur at high altitude and latitude, where other groups of organisms have difficulties to survive. Furthermore, some species live inside stones. With their hyphae they can penetrate even granite, with the only externally visible structure the fruiting body (Brodo et al. 2001).

Another clear example of their ability to withstand harsh environments has been demonstrated by the lichens Rhizocarpon geographicum and Xanthoria elegans. The two species have survived in outer space (Sancho et al. 2007a). A prerequisite to cope with these harsh environments is that the lichens have had the time to dehydrate. In this dry state, called cryptobiosis, the metabolic rate drops dramatically and the life- sustaining activities in the cells are very low. Once they have entered this state, lichens, as just mentioned, can survive in extreme environments. On the other hand, lichens are sensitive to other changes in abiotic and biotic factors, for instance, polluted air in urban areas. One reason for this is, compared with spermatophytes, the lack of a protective cuticle. A cuticle is a waxy outer layer on, for instance, the leaves that prevents harmful airborne compounds from entering and damaging the internal tissue.

Lichens do not have roots for their uptake of water like spermatophytes; instead they satisfy their need of water from precipitation and moisture in the air. In spermatophytes, the casparian strip in the roots is also a barrier that helps the plants avoid harmful substances. Thus, it is not the difference in absorption capacity that makes lichens sensitive compare to spermatophytes. It is when the precipitation and surrounding air contains harmful and toxic substances that uptake of water becomes a problem as they are unable to control what enters the thallus. The lack of a cuticle allows the substances to enter the tissues and cells and injure or kill the lichen. Thus, lichens can withstand extremely harsh environments, yet they are sensitive to certain types of changes in the environment, especially those related to an increase in harmful substances in the atmosphere and to changes in air humidity. Hence, in addition to the general threats to biodiversity – habitat loss, fragmentation and global warming – lichens are also (locally) threatened by air pollution (Giordani 2007, Affum 2011).

Sunlight

Lichens are dependent on sunlight, since they are photosynthetic organisms. The

amount of light or electromagnetic radiation needed for photosynthesis and how much

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each lichen species can withstand varies among species (Demmig-Adams et al. 1990, Green & Lange 1991, Gauslaa & Solhaug 1996, Kappen et al. 1998). The lichen Verrucaria rubrocincata, which is endolithic and lives in desert environments, has been shown to tolerate a high degree of electromagnetic radiation; even at 2600 μmol/m

²

s

^–1

during a hot summer day the lichen still continues to photosynthesise (Garvie et al.

2008). For the epiphytic forest lichen Lobaria pulmonaria, Gauslaa and Solhaug (2000) showed that the electromagnetic radiation never exceeded 610 μmol/m

²

s

^–1

on the Quercus trunk where the lichen occurred. These authors also transplanted L. pulmonaria to a neighbouring tree trunk where the lichen did not occurred and appeared to have similar light conditions. The results showed that the neighbouring Quercus trunk had 6 hours more radiation above 1000 μmol/m

²

s

^–1

during early spring and peaked with 2000 μmol/m

²

s

^–1

. The transplanted specimen showed extensive bleaching and damage on the chlorophyll. Forestry practices in Sweden have changed during recent centuries including clear-cut. Lichens that have adapted to live in a forest, relatively shaded compared with open habitat, may be permanently damaged due to high electromagnetic radiation (Gauslaa & Solhaug 1999, Gauslaa et al. 2006). Out of all land areas in Sweden (41.3 × 10

⁶

ha), 23 × 10

⁶

ha consists of production forest (NBF 2007). The human impact on the production forest is significant and the forests are managed, primarily to promote economic interests. Prevailing forest management is unfortunately often incompatible with the necessary life conditions for lichens, dependent as they are on old tree trunks and standing and prostate dead wood. Such habitats have become scarce. Thus, the change in the demography of forests towards a greater proportion of younger trees, and the practice of clear-cutting, are negative for many lichen species.

The air

Soon after the industrial revolution in Europe in the late 18

^th

century, air quality started to change. Independent observers in Manchester, England (Grindon 1859), Munich, Germany (cf. Gries 1997) and Paris, France (Nylander 1866) documented in the mid 19

^th

century that lichens were disappearing from the cities. Fifty years later, in the beginning of the 20

^th

century, the same pattern was recognised across the whole of Europe (Erisman & Draaijers 1995, Mylona 1996). The cause for the decline of lichens in cities was first suggested to be the dust from coal, but later it was realised that sulphur dioxide (SO

₂

) was the main toxic agent. This is one of the most lethal substances for lichens and responsible for most of the modern decrease of lichens (Gilbert 1968). Hawksworth and Rose (1970) showed that lichens could be used to monitor the SO

2

content in the air. They used an ordinal scale with teen categories of lichens with increasing sensitivity to SO

2

.

International co-operation with the goal to reduce the effects of air pollutants on the environment has been successful, and a dramatic decrease in SO

2

has been observed in recent decades (UNECE 1999). Schopp et al. (2003) predicted a continued decrease of SO

2

in Europe up until the end of 2030. Recolonization of lichens in London, United Kingdom, has been shown by Hawksworth and McManus (1989) and has been attributed to the decrease in sulphur dioxide. Another example of successful urban recolonisation is the rare Parmelina tiliacea that was found in central Malmö, southern Sweden, ten years ago (Kärnefelt & Lättman 2001). At that time, this species was red- listed in both Denmark and Sweden (critically endangered and vulnerable, respectively).

Most remarkable was that the specimen was healthy-looking and well-developed, and

apparently unaffected by the urban environment. This was in stark contrast to the other

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lichens present on the tree that were not fully healthy-looking, and thereby of typical appearance of lichens in a larger city. Another indication of the improved SO

₂

-

conditions for this lichen is that subsequently, P. tiliacea has been removed from the red list.

Climate change: Temperature and moisture

Anthropogenic greenhouse gases are the main cause of climate change that occurs today (Rosenzweig et al. 2008). Climate is a description of weather for an extended period of time that includes variables such as temperature, precipitation, humidity, atmospheric pressure and wind. During the last decades, many studies of climate change have revealed its enormous impact on numerous different organisms including lichens (Vitousek 1994, Hughes 2000, Saxe et al. 2001, Walther et al. 2002, Parmesan & Yohe 2003, Root et al. 2003, Sanz-Elorza et al. 2003, Perry et al. 2005, Thuiller et al. 2005, Parmesan 2006, Maclean et al. 2008, Allen et al. 2010, Dawson et al. 2011, Gosling et al. 2011). It is difficult to separate and determine which of the various abiotic factors are most important for species’ distribution and abundance. For example, Warren et al.

(2001) expected a positive response to climate warming in their study on butterflies since they benefit from warm conditions. Unexpectedly three-quarters of the surveyed species decreased. The authors concluded that the positive response to climate warming had been overshadowed by the negative response to habitat loss.

Climate warming is probably the major contributor to changing the range boundaries of terrestrial and freshwater habitats (Thomas 2010). Different groups of organisms will have variable successes in meeting the challenges of necessary dispersal.

Malcolm et al. (2002) used several vegetation models to determine whether species are able to move as fast as climate zones change. The results showed that changes of climate zones will, in many cases, exceed species capability to migrate. In all vegetation models, high migration rates ≥ 1000 m per year were relatively common. Species that do not have the ability to move and establish on new sites fast enough will face a rapidly changing environment and extinction of some of these species will be inevitable.

Thomas et al. (2004) modelled extinction risk for some species in 20% of Earths terrestrial environments and estimated that by the year 2050, 15–37% of the species will be committed to extinction.

Discussions about global warming and whether humans affect the process has been and is still under debate. However, according to a survey among climatologists, 96%

believe that global average temperatures the past 100 years have increased and 97% that it is induced by man (Doran & Zimmerman 2009).

Among the weather variables, it is temperature and water in different forms, e.g.,

precipitation, fog and dew that has most impact on lichens. For instance photosynthesis

is only activated when the lichen thallus is moist, and it stops when the lichen thallus is

dehydrated. In the dehydrated state, the lichen is highly resistant to extreme external

environment as discussed earlier, but this does not apply for the moist condition where

the thallus is sensitive. Lichens can withstand a wide range of temperature when

dehydrated, with temperatures ranging from 90°C (or even higher) to –196°C for

several days and –60°C for several years (Nash III 1996). However the exposure of a

moist thallus of Evernia prunastri to 80°C showed to have a strong negative effect

(Pisani et al. 2007). Furthermore some species of the genus Cladonia have proved to be

even more sensitive when moist. Kappen and Smith (1980) examined how close

Cladonia oceanica could grow a hot steam area of Hawaii. The results of maximum

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temperature were 27.2°C in stunted form and 23°C in ramified growth form. Grüninger (1988) sampled ten specimens of Hypogymnia physodes in Reutlingen, West Germany and enveloped the thallus in paper. Two days later he transplanted the lichen thallus on tree trunks on the campus of the University, San José, Costa Rica. Three thalli had died after one week and after ten months they were all dead. The reason for this could be due to the large differences in temperature between Germany and Costa Rica. When a thallus is in a moist state and photosynthesis is activated lichens are most heat sensitive (Rogers 1971, Kappen & Smith 1980). Photosynthesis requires water and the thallus can absorb large amounts. The thallus of green algae lichens can absorb and maintain a water content of 250–400% whilst in cyanolichens this figure can be as high as 600–

2000% and some even higher on a weight basis. When water is available, the thallus reservoir is filled very quickly. In a few seconds 60–70% of the thallus becomes saturated and full saturation is reached within minutes. Photosynthesis has its maximum speed, for green algae lichens, when the thallus has a water content of 70–150% and corresponding value for cyanolichens is 300–600% (Nash III 1996).

Substrate

Corticolous (growing on bark), lignicolous (growing on wood), saxicolous (growing on rock) and terricolous (growing on soil) are convenient terms to describe the substrate preferences of lichens. Some species have the ability to grow on several kinds of surfaces while others are limited to just one or a few. Some epiphytic lichens are able to grow on a variety of tree species, while others only grow on one or just a few.

Furthermore, some are demanding in terms of size or age of the tree and prefer a large, old tree. Wedin et al. (2004) made a remarkable discovery regarding the genera Stictis and Conotrema. They showed that a fungal species can adopt two different lifestyles depending on the circumstances. If the fungal spore ends up on the substrate wood, the fungus adopts a non-lichenized, saprophytic lifestyle and has been called Stictis. On the other hand, if the fungal spore ends up on bark – and the needed photobiont is available – the fungus adopts a lichenized lifestyle and has been called Conotrema. Hence, two different genera proved to be the same fungal species but with different lifestyles:

lichenized or non-lichenized. The fungus’ plasticity in terms of lifestyle and the frequency with which it occurs is unknown but may be common (Hawksworth 2005).

Thus, requirements on the substrate quality for different lichen species vary from generalists to highly specialised lichen species.

As our human population increases, we use more and more land area: we claim more space. As a consequence, the amount of available habitat reduces for most other organisms. This unceasing demand to exploit new areas and their resources for our benefit has created severe situations for many other non-human organisms, particularly those that require large areas for their survival. Furthermore, remaining habitats become fragmented and thus divided from each other into patches often surrounded by areas affected by different kinds of intense human activity (e.g. agriculture, urban areas, roads and railway tracks). Organisms with a limited ability to disperse face a severe situation in fragmented areas. Fragmentation and its edge effects have been shown to have a negative impact on lichen biodiversity (Turner 1996) and abundance (Esseen &

Renhorn 1998).

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Aims of the thesis

The overall goal of this thesis is to increase our knowledge regarding the changes in time and space in the occurrence of epiphytic lichen species and their communities with the use of existing or new methods. The complexity of these factors and their

synergistic effects make it necessary to undertake studies on different spatial and organisational levels. These range from genetic, individual and population levels through to community and biotope levels. Thus, different studies with different objectives and methods were designed in order to target the overall aims of the thesis.

Estimating the generation time of the red-listed crustose epiphytic lichen Cliostomum corrugatum was the objective of Paper I. A method for assessing generation times, from meiospore to meiospore, is often necessary in order to

understand population dynamics as well as to describe evolutionary history both in the short as well as in a long run perspective. The results were used in the following study (Paper II).

Paper II makes an attempt to determine whether the rarity of C. corrugatum is due to difficulties with dispersal or if it is its habitat – old and often large Quercus robur – that is limiting. Using the analysis of a nuclear ribosomal RNA gene, three different methods to analyze the pattern, the lichens ability to disperse were tested.

Paper III examines the problems of describing changes in the lichen flora on a regional scale. From field surveys of common epiphytic lichens in southern Sweden, conducted in 1986 and 2003, the change in position of the centroids of these species over time was assessed. A centroid of a species is the mean position of its sites in an area, calculated from the coordinates of sampling sites.

Finally, in Paper IV the focus is to investigate differences in species richness and cover of some common and rare epiphytic lichens on Q. robur standing in urban and rural environments. The effect of urban sprawl was also examined on species richness and cover on common and rare epiphytic lichens on Q. robur. Two methods were used to measure the degree of urbanization, one of which took into account the average age of five adjacent buildings and the second the area of nearby buildings at six radii centred on a visited tree.

In the rest of this thesis, each of the papers is presented with a general background

introducing the specific study.

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Further background and the included papers

Growth

Lichens have been studied for a long time and knowledge of their biology has

accumulated. However in the light of for example vascular plants we have just begun to understand how lichens function, with this field much less studied. Crustose lichens growth and growth rate has been studied and especially so in the lichen Rhizocarpon geographicum (Armstrong 1983, Proctor 1983, Haworth 1986, Armstrong 2002, 2006, Hansen 2010). In general, lichens are slow-growing and have a reputation for not only this but also for being long-lived (Hale 1973, Matthews & Trenbirth 2011). However, there are both fast- and slow growing lichens. Benedict (2008) reported an annual radial growth rate for R. superficiale to be as little as 0.006 mm per year. An example of a fast growing lichen is Usnea longissima, which showed a maximum growth of 18.4 cm in a single year (Keon & Muir 2002). The variation in growth within a single species may also be large. Hill (1981) reported annual radial growth rates (RGR) of Lecanora muralis to be 0.03–0.55 mm per year while Seaward (1976) showed the RGR to be 2.84–6.05 mm per year. Several methods for study growth rate have been developed (Platt & Amsler 1955, Farrar 1974, Honegger et al. 1996). Lichenometry is a frequently used method where measurement of the lichen thallus RGR is central. The method is used for example to date moraines and the retreat of glaciers (Karlén & Black 2002).

A lichen’s growth curve varies depending on growth form. The growth curve of the crustose lichen R. geographicum can be divided into three parts: 1) where RGR gradually increases to a maximum; 2) maximum speed is kept for a short time period;

and 3) the speed of RGR decreases (Armstrong 2005, Armstrong & Bradwell 2010).

There is no evidence that foliose lichens would have a phase where there is a reduction of RGR as there is in crustose forms. The growth of lichens and their population dynamics is, of course, also influenced by abiotic and biotic factors, but these affects lichens differently depending on the species. The abiotic weather factors that mainly affect lichens are temperature, humidity and sun exposure. Regardless of season there is a growth all year round in R. geographicum but predominantly during the summer months (Armstrong 2006). Other abiotic factors that affect lichens are nutrients.

Gauslaa et al. (2006) performed growth experiments with Lobaria pulmonaria. Some of the thallus was sprayed with clean water and others with nutrients added to the water.

The results showed that water with added nutrients only slightly increased the growth of

L. pulmonaria. Results with stronger support for the importance of nutrients were

presented by McCune and Caldwell (2009), where L. pulmonaria thalli were immersed

in a bath of phosphorus for twenty minutes. After one year the biomass was doubled

compared to the control group. Thus, growth and growth rate is relatively well studied

at least for the lichens R. geographicum and L. pulmonaria.

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Another population dynamic aspect which is also, at least in some areas, relatively well studied is mortality. Most studies on mortality have dealt with pollution such as emission from industries and urban areas to determine the highest concentrations of harmful substances lichens can withstand before they disappear. The knowledge gap in mortality is in knowing the dynamics under normal conditions. For instance, at what age (or size) does a lichen thallus die a natural death or what is the lifespan of a lichen thallus? There is some knowledge about the well studied lichen R. geographicum which can reach an age of about 1000 year (Matthews & Trenbirth 2011) but the maximum age is likely to be very much shorter in epiphytic lichens. In fact, Hypogymnia physodes never reach such an age. Studies have shown that H. physodes has a growth rate of 3–4 mm per year (Gorbach & Kobzar 1981). Since the thallus rarely exceeds 5 cm in diameter this means that the individuals of H. physodes reach approximately 6 to 8 years of age before they die. Furthermore Mattsson et al. (2006) have shown that H.

physodes has a rapid turnover in the sense of appearance/disappearance at sites.

By using the growth rate and lichen thallus diameter, it is possible to estimate the age on an individual thallus. However there are many unanswered questions: what is the population dynamics in terms of mortality, at what age do they die and begin to

reproduce sexually and asexually? Hence, to better understand the population dynamics of lichens, we certainly need much more basic field research.

Generation time of lichens

Generation time can be explained as the time span from a given point in the parent life cycle to the same given point in the offspring. Two different types of generation time can be distinguished i.e. fundamental and realized generation time. The fundamental generation time is based on the shortest possible time (age) of reproduction for an individual of that particular species while realized time is the average parental age at reproduction under natural conditions. Generation length is sometimes used

synonymously with the word generation time. Generation time varies for different eukaryotic organisms, for instance, the oriental latrine fly, Chrysomya megacephala have a short generation time in only 20.7 days (Gabre et al. 2005), in the same way human generation time is approximately 25 years and Japanese timber bamboo, Phyllostachys bambusoides, have a generation time on about 120 years (Janzen 1976).

The consequences of different generation time are that the genetic material will evolve at different rates depending on the species.

The time span between meiosis events is important to estimate as these events have a potential for genetic recombination, while the vegetative phase of organisms is more inert at the genetic level. Thus, knowledge of species’ generation time is essential for calculations of the speed of evolutionary changes.

The relative importance of sexual versus asexual reproduction depends on the species. The spores in mycobiont-dispersed species have undergone genetic

recombinations that may increase genetic variation and the spores are often small and

may be dispersed far away. The downside is that the mycobiont must find a suitable

photobiont before being able to become lichenized. Species that disperse with

vegetative diaspores has the advantage that both partners are spread along together but

there is no recombination as they are clonal (Nash III TH & Gries 2002).

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Paper I

In Paper I, the generation time of Cliostomum corrugatum was studied in Bjärka-Säby, Östergötland, Sweden. The largest thallus area and largest diameter on apothecia were recorded on Quercus robur. Only large trees were included in the study since the occurrence of C. corrugatum is low on trees with a small circumference at breast height (CBH) (e.g. Ranius et al. 2008, Johansson et al. 2009). By plotting thallus area or apothecia diameter against oak diameter and extrapolate the regression line it was possible to identify the age of Q. robur when C. corrugatum colonised it and at what age it becomes fertile. Quercus robur CBH were translated into oak age and the estimated time it takes for C. corrugatum to become fertile (fundamental generation time) for C. corrugatum were found to be 25–30 years (Figure 1). The fertile thallus may then continue to produce spores for many years ahead.

Figure 1. The epiphytic lichen Cliostomum corrugatum becomes fertile at an age of 25–

30 years.

It is surprising that sexual maturity takes such a long time to form in this lichen,

especially considering that by being an epiphyte, its substrate has a limited life span. To

my knowledge, this is the first time that anyone has determined the generation time of

lichens. It would be interesting to estimate this in other suitable lichen species. The

question of whether the generation time is longer among rare and red-listed species than

among common lichens appears to be particularly pertinent. Clearly more research is

required for a comprehensive picture of lichen generation times to emerge.

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Is substrate or dispersal limiting?

Phorophyte and stand

Epiphytes are plants that grow on other plants, principally trees and shrubs but also dwarf shrubs (e.g. Calluna and Vaccinium sp.) and even leaves (in the tropics) can be used as a substrate. The common name for the various substrates is called phorophyte.

The utility of the bark substrate for various lichen species may vary considerably. The common lichen Hypogymnia physodes does not have high demands on the substrate but can grow on a wide range i.e. corticolous, lignicolous or sometimes saxicolous but also man-made substances such as rubber and steel (personal field observations) (Figure 2).

Figure 2. The lichen Hypogymnia physodes is common in Sweden and grows on many different substrates. It inhabits mostly bark, wood or stones but sometimes also man- made substrates such as rubber and steel.

What may be important for the epiphyte is to what species the phorophyte belongs, and its age (or dimension of the trunk). Several phorophytes together form a stand that is scattered in the landscape in different ways making it more or less suitable (such as sun exposure, pH and structure of the bark), influencing accessibility for the establishment and also how beneficial these stands are for long term survival of the lichen. In general, areas designated for forestry have a lower value than protected stands since production areas are more homogeneous and often lack old and large trees and also are low in dead wood.

Spore dispersal

Present lichen distribution is in part a result of their ability to spread from one place to

another. Lichen ascospores are relatively small ranging in size from 2–3 μm for

Chaenotheca furfuracea to 150 μm for Phlyctis argena with a few other species having

even larger spores (Foucard 2001). The production of spores is large and one fruit body

may contain more than 1 × 10

⁶

spores, which can be equated with 12–18 × 10

⁶

spores in

one square centimetre (Tibell 1994). The main vector for their dispersal is wind which

probably is important for long distance dispersal (LDD). The air at ground level

contains a large amount of spores. Gregory (1978) measured the levels of spores, from

various cryptogams, during five summer months in Rothamsted, England, and showed

average concentrations of 12000 spores m

^-3

but for short periods as many as 1 × 10

⁶

may be present. The concentration decreases with increasing altitude with 10000 spores

m

^-3

one kilometre above the ground and hundreds of spores three kilometres up (Hirst et

al. 1967). In contrast to vascular plants, many lichens have very large geographic

distributions and if their distribution is not cosmopolitan, it may be pantemperate,

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pantropical (Lücking 2003) or amphitropical (Søchting & Olech 1995, Myllys et al.

2003). The lichen Porpidia flavicunda has a circumpolar distribution and Buschbom (2007) showed that the gene flow was high among the four surveyed sites. Furthermore, the gene flow occurred in almost all possible directions and the lichen has had several repeated LDD of vegetative diaspores between the sites. Högberg et al. (2002) made an exciting discovery on Letharia vulpina. They found that in North America, this lichen dispersed sexually by spores but in Europe the populations spread clonally by soredia and/or isidioid soredia. Long distance dispersal with spores of species from the genus Umbilicaria has on several independent occasions traveled to Antarctica from

surrounding temperate areas. This does not only apply to the spores but also to the algal cells. Thus despite the hostile environment prevailing in Antarctica, successful

relichenizations have been established, on multiple occasions, between fungi and algal cells (Romeike et al. 2002).

Several papers have argued that some lichen have limited dispersal abilities.

However, knowledge is often lacking about whether dispersal or substrate availability is the limiting factor for a specific lichen population to survive in the long run, both locally and regionally. To fully understand the importance of these different factors in isolation or in combination, it is necessary to study both dispersal efficiency and the impact of substrate abundance and microhabitat characteristics.

Paper II

In Paper II, I investigated whether the limited occurrence of the lichen C. corrugatum is due to limitation by dispersal or limitation by habitat availability. The investigation was conducted in Östergötland, south-eastern Sweden, at five sites. The laboratory methods involved DNA extraction, PCR amplification and sequencing of a group 1 intron at the end of the small subunit (SSU) nuclear ribosomal RNA gene. Attempts were made using other genomic regions (ITS and IGS) but the variability at these regions were too low for our purposes. Out of the 96 collected samples of C. corrugatum, 85 were successfully extracted and shown to represent 11 haplotypes (Figure 3).

Figure 3. An unrooted haplotype network of the epiphytic lichen Cliostomum

corrugatum. The most common haplotypes 1 (N = 30) and 2 (N = 46) are in the centre

of the network and are most likely the oldest. The terminal haplotypes are rare (N = 1)

and have most likely derived from haplotypes 1 or 2.

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Several statistical methods were used to analyse the genetic variation and to make inference about the lichen’s ability to disperse. Firstly, a coalescent simulation showed that the gene flow was considerable between the five investigated sites. Secondly, a mantel test showed that there were no significant correlation between the genetic distance and the geographic distance matrices. Thirdly, an AMOVA test showed that 0.4% of the variation was between the populations and 99.6% of the variation was within the populations. All three tests indicate that C. corrugatum does not seem to have any difficulties dispersing from one place to another. In addition our results indicate that the five sites behave more or less as a single, sexual interbreeding population, i.e. a panmictic population. Consequently, C. corrugatum rarity is likely to be connected with the limited amounts of the suitable habitat, old oaks. The distribution of Q. robur is more or less the whole of Europe, but unfortunately large, old oaks are relatively scarce.

During several hundred years an oak trunk serves as a suitable substrate for this lichen, a time during which it can, with exception of the first 25 years, disperse spores (Paper I). However, genetic methods have unfortunately its limitations. The result of the genetic information reflects, to some extent, the population of C. corrugatum historical status and not the lichens situation today.

Another context in which to view these results regards the peculiar Quaternary

history of the study area that involves land uplift. Since the end of the last glaciation, all

sites have gone from being submerged to terrestrial (Figure 4).

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a)

b)

Figure 4. The two maps show a snapshot over the five studied sites during and after

the glacial retreat. a) Twelve thousand years ago the glacier edge (solid blue line)

stretched in a WSW/ENE direction and all five sites were submerged. b) Ten thousand

years ago the glacier had retreated and the three sites in the west have become

terrestrial.

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At 10000 BP the three western sites had become terrestrial (Figure 4b). The remaining two sites in the east (Stegeborg and Bråborg) had to wait, approximately, another 5000 years until they emerged from the sea. In southern Scandinavia Quercus invaded early after the last glaciations and they have been present in the study area for at least 6000 years (Bradshaw 2000, Rasmussen 2005). It is important to note that a site becoming terrestrial is just one prerequisite for oak colonisation. Another is the edafic conditions and a third is whether oaks were present in the area at the time. Notably, the three sites in the west, i.e. those with the longest history as terrestrial, also had greater haplotype diversity (Figure 5). What this means for our understanding of C. corrugatum ability to disperse and the evolution is difficult to evaluate. Have the rare haplotypes evolved at these sites, or have they accumulated here through migration over time due to their relatively long history? Should the lack of rare haplotypes in Bråborg and Stegeborg be interpreted as an indication that the species is limited by dispersal?

Figure 5. The three sites in the west are higher above the sea level and have more haplotypes than the two sites in the east.

Large-scale dynamic of lichens

Dynamics of lichen thalli

Lichens can be divided into crustose (resembling a crust), foliose (resembling a leaf) and fruticose (resembling a shrub). In the group crustose lichens, many are slow- growing (see above) and some have been used in lichenometry, which is a method for dating exposed rock. I believe this is the major reason why the general picture of lichens is that they grow slowly and have a slow population turnover. In this context, slow population turnover means that the rate of mortality and nativity are low, i.e. individual thallus remain attached to the same site year after year. In comparison with other spore- producing organisms such as bryophytes, most crustose lichens have a slow turnover

Bråborg

Stegeborg

Orräng Bjärka-Säby

Solberga

0 1 2 3 4 5 6

0 20 40 60 80 100

Numb e r of ha ploty pes

Height above see level (m)

y = 0.0271x + 2.2536

R²= 0.8259

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(Pharo & Beattie 1997, Pharo et al. 1999), but this slow turnover does not apply to foliose and fruticose lichens, at least not all of them. Gustafsson and Milberg (2008) demonstrated that the foliose lichen Lobaria pulmonaria had a high turnover in south- eastern Sweden (permanently marked thalii). Mattsson et al. (2006) showed that several common species, e.g. the fruticose lichen Hypogymnia physodes in southern Sweden, has a high turnover (presence/absence at sites). In California, USA, Boucher and Nash III (1990) estimated the annual turnover of biomass of the common fruticose epiphytic lichen Ramalina menziesii to be 29% where the annual turnover of biomass is the sum of all fallen thallus. This implies that R. menziesii contribute substantially to the nutrient turnover in the ecosystem. It also means that lichen thalli are constantly replaced by new ones. Therefore, even though it might look like it is the same lichen thallus that sits on the tree trunk every year, it may be a new one.

Lichens on the move

Being able to move from one place to another is generally fundamental for most organisms, and this also holds true also for lichens. This has become especially important in recent decades with rapid climate change. Since lichens have been shown to be sensitive to changes in their environment, they are a useful group of organisms to help detect the biological response to global warming (Pisani et al. 2007, Sancho et al.

2007b). The change in the amount of lichen biomass will ultimately affect the distribution pattern of individual species.

In a climate that is changing it is expected that lichen species will alter their distribution pattern. Long-term empirical studies in alpine and arctic environment have shown conflicting results in terms of an increase or decrease in the amount of lichen biomass. A decrease has been shown by Kari (2008) and Hudson and Henry (2010) that contradicts findings by Hollister et al. (2005) who found an increase of lichen cover across time. Unchanged amount of lichen biomass have also been reported (Hudson &

Henry 2009). Hauck (2009) proposes an alternative cause for the decline in lichens in alpine and arctic environment. He argues that changes in the use of land and to high atmospheric SO

2

levels in the mid-20

^th

century better correlated with the decline of lichens than an annual increase in average temperature. Models incorporating different types of scenarios have been used to predict future distribution and abundance of different lichen species (Ellis et al. 2007a, Ellis et al. 2007b). To date, research has not yet demonstrated that lichens have been seriously threatened because of climate change but rather that a decrease or increase of species distribution will occur. Aptroot and van Herk (2007) have shown that lichens with green algae Trentepohlia sp. as a photobiont are increasing their distribution. There are areas though which could ultimately be threatened by climate change. Aptroot (2009) highlights areas and habitats likely to experience problems e.g. low-level islands with endemic lichens, arctic and tundra regions and high ground in the tropics. It is important that we have methods to quantify changes in the distribution of different lichens so we are able to take appropriate actions and develop new and improve existing types of lands use, e.g. in forestry.

Paper III

This brings us to Paper III, where studies on lichens movements were investigated. In this paper, movement of the, centre of distribution (centroid) within southern Sweden, of some common epiphytic lichens were studied, based on a small repeated sampling.

The study was conducted at 64 sites and the inventory in the field was carried out in

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1986 and 2003. Fifty-six epiphytic lichens and 22 tree species (phorophytes) were included in the study. Thirty cases were possible to analyze, out of which three showed a significant shift in the centroid. The centroid movements of the lichens Hypogymnia physodes and Vulpicida pinastri on the tree species Juniperus communis were 50 km and 151 km (p-value 0.0258, 0.0002) with the direction 27° and 48°, respectively. The movement of the centroids of H. physodes on Pinus sylvestris was 41 km (p-value 0.0066) with the direction 30° (Figure 6). All three significant cases had moved in a north-east or a north north-east direction.

Figure 6. The three arrows indicate direction and distance that the centroid had moved between the years 1986 and 2003 of Hypogymnia physodes and Vulpicida pinastri on the tree species Juniperus communis but also H. physodes on the tree species Pinus

sylvestris. Squares represent the study sites.

The data set was fairly small with only presence information of epiphytic macrolichens

on different substrates recorded. The sites were only roughly described, without

information on tree size and tree species abundance and trees without lichens were not

recorded. Hence, the statistical power of the analyses was low. Of the two species that

turned out significant at least H. physodes has a large ecological amplitude, which

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should provide a strong resistance against small changes in environmental conditions.

Nevertheless, some significant changes were recorded on the movement of the centroid.

This indicates a greater impact of global warming on the epiphytic lichen flora than previously presumed.

The temperature of the planet is increasing and has done so at least during the past 40 years (Rosenzweig et al. 2008). In our study area, the current trend appears to be the same. On 29 meteorological stations in the study area the average temperature has increased by 0.056°C year

^–1

during the period 1986 to 2003 (Figure 7) (SMHI 1986–

2003). Another explanation why some lichens have moved their centroid may be due to large scale forest structure changes in recent years. Hedwall et al. (2012) used data from the Swedish National Forest Inventory to compare the field- and tree layer in boreal and temperate Sweden between 1994 and 2010. They found that the canopy has become denser and the distribution of species abundance on the forest floor has changed as it has become darker. The lichens could respond in a similar way to a darker environment.

Figure 7. The average temperature over 29 meteorological stations in southern Sweden during the period 1986 to 2003.

Lichens in the urban environment

Urbanization transforms a natural, semi-natural or agricultural landscape into an environment with buildings. In an ecological perspective, the organisms and the environment they live in are, to a varying degree, interconnected and dependent on each other. As an example, trees are of paramount importance for epiphytic lichens and many tree species are, more or less, dependent on mycorrhizal fungi. There are many reasons to maintain a high biodiversity in urban areas especially in highly urbanized areas. In a study in Flanders in Belgium, an area where the proportion of forest is only 10%, Cornelis and Hermy (2004) showed that their 15 surveyed city parks contained about 30%, 50%, 40% and 60% of all wild plant species, nesting birds, butterflies and

y = 0.056x + 6.804 R² = 0.112

0.0 1.0 2.0 3.0 4.0 5.0 6.0 7.0 8.0 9.0

86 87 88 89 90 91 92 93 94 95 96 97 98 99 00 01 02 03

The a v e ra ge tempe ra tu re

Year

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amphibians, respectively, of the total national number. This highlights the magnitude of biodiversity even in cities. Urbanization is a major cause of a homogenization of biotic factors (McKinney 2006), but the goal of biodiversity conservation should be towards diversity.

In Sheffield, United Kingdom, Gaston et al. (2005) tested various methods to increase biodiversity. They added nests for various insects, ponds for birds, dead wood for fungi and patches of Urtica dioica for butterflies. Since urban areas are largely composed of private and residential gardens, the investigation was focused on these spaces. Some of the tested methods were found to boost biodiversity, indicating the potential for retaining biodiversity within city borders.

Ranta and Viljanen (2011) list the causes of the relatively high biodiversity of vascular plants in Finnish cities as spacious urban structure, small human populations, late urbanisation, and abundant remnant natural vegetation (forest). The investigations demonstrated that much can be done to increase biodiversity in urban environments and there is certainly room for improvement. Hahs et al. (2009) examined the factors affecting the rate of plant extinction from urban environment. They concluded that it largely has to do with the city’s history in combination with current proportion of native vegetation. They also claim that the transformation of the landscape to an urban area is likely to involve an extinction debt, i.e. that there is a time delay in the loss of

biodiversity from our cities when they grow.

Trees: an important urban element

Trees in cities are in a stressful environment because usually they stand in a soil with poor quality and their roots often have a limited ability to spread. In addition, roots are frequently damaged during ground works i.e. when various types of pipes and cables should be buried (Jim 1998). Increased runoff from buildings, hard surfaces and drainage (Leopold 1968) which reduces the impact of a positive long-term effect of moister from the precipitation in cities and the smog in some cities can cause tissue damage on the trees (Middleton et al. 1958, Tripathi & Gautam 2007, Honour et al.

2009). Nevertheless, trees are often an important feature of cities. Hence, trees have been planted, or retained from native or rural setting during urban sprawl, for a number of reasons: wellbeing of people, economic value, aesthetics, the production of shade and, in some situation, even for fire prevention purposes. Lohr et al. (2004) surveyed residents in the United States concerning advantages and disadvantages associated with trees in a city. Results from their study showed that the public evaluated trees ability to shade and cool the surroundings highest and secondly it helped people feel calmer.

Highest ranked disadvantages were that they can cause allergies and block store signs.

Lohr et al. (2004) concluded that most people clearly appreciated the value of urban trees in their lives.

Several studies have shown that trees in cities are highly economically valued. For instance Donovan and Butry (2011) showed that an increased number of trees in a residential garden increased the monthly rent by USD5.62 and trees in the public right of way increasing the rent even more. Not surprisingly, the sale prices of buildings are affected by trees. An increase in the number of trees also added an extra USD8870 to a house in Portland, Oregon and reduced the time on the market by 1.7 days (Donovan &

Butry 2010). Nowak et al. (2002) calculated the value of urban forests using tree

valuation methods and field data. The evaluated total compensatory value was 101 ×

10

⁶

and 5.2 × 10

⁹

USD in Jersey City and New York, respectively. Donovan et al.

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(2011) showed a reduced risk of poor birth outcomes by 1.42 per 1000 births if canopy cover were increased by 10% within 50 m of residential buildings. Clearly is that those who can afford, like to have trees around.

The studies above give us an indication that even in the future; trees will continue to be highly valued in cities, although increasing land prices adds a threat towards retained trees. On balance, the prospect for continued survival of epiphytic organisms in cities seems brighter than for many other types of organisms.

Urban effects on lichens

Lichens have different tolerance or preferences concerning substrates. This means that some lichens grow on different substrates, even some man-made. Hence, there are lichens that grow on either coniferous or deciduous trees or others confined to a particular tree species (Washburn & Culley 2006, Spier et al. 2010). Other lichens can be restricted to a particular size of a tree e.g. large tree (Washburn & Culley 2006) that usually has a coarse bark structure. Such specialized lichens have declined since the supply of substrate is less in urban environments (Shukla & Upreti 2011).

Large trees of Quercus have proved to be very rich in species that also include lichens (Rose 1974, Hultengren 1995), but few studies of lichens have been conducted in an urban setting, an exception being Larsen et al. (2007) who investigated lichen distribution on Quercus robur and Q. petraea in London, England in relation to air pollution. The authors were able to distinguish three zones where lichen species increase in number from the inner to the outer zones.

Lichens have been used to estimate air quality in urban areas. Wielgolaski (1975) inventoried several groups of organisms such as vascular plants, bryophytes, lichens, microorganisms, invertebrates, fish and plankton on their biological value to use as a tool for evaluating air, freshwater and marine quality. The author argued that most foliose and fruticose lichen in a wider sense can be used for evaluating the air quality.

Hawksworth and Rose (1970) well-known work was more fine-tuned and they also used crustose lichens and algae. They were positioning a selection of lichens (and algae), on a ten-point scale reflecting various sensitivities, and then used it to estimate the air quality with particular attention to SO

₂

. During the 1970s a number of studies showed that lichens are adversely affected by road traffic emissions of SO

2

(e.g. Brawn &

Ogden III 1977). Even the air quality and quantity of heavy metals has been investigated by means of lichens (Pandey et al. 2002, Montero Alvarez et al. 2006).

Even though there are positive signs that the air quality is beginning to improve in urban environments (Lisowska 2011), SO

2

is still, 30 years later, considered the main limiting factor for lichens in urban settings (Giordani 2007). Trees surrounding an expanding city will be enclosed with buildings. Lichens on these trees will be isolated and activities such as dispersal and establishment may be negatively affected. Mobile organisms like animals can escape while trees will inevitably be incorporated and trapped into the city or cut down during urban sprawl. The fate of epiphytic lichens will parallel that of the trees.

Paper IV

In Paper IV, I examined species number and cover of epiphytic lichens on remnant oaks

in urban and rural environment. In Linköping, County of Östergötland, Sweden, 105

urban and 109 rural oak trees were surveyed for 17 selected lichen species. Trees with a

CBH > 250 cm were selected from a database developed by the County Administrative

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Board in Östergötland. The majority of the available urban trees were selected since there were only a limited number. I then selected a population of rural trees, aiming for (i) a population of similar circumferences and (ii) similar densities of oaks in the surrounding. I calculated densities with a radius of 302 m, as a previous study had identified this as the appropriate scale for lichen richness in the study area (Muhammadi 2011). Nine of the lichens were common and eight were rare. During the field-work, CBH, depth of bark crevices and sun exposure were documented per tree. The density of oaks in the vicinity of target trees was calculated within radii of 150, 250, 350, 500, 700 and 1000 m. Two variables were also constructed as a measure of degree and age of urbanisation. Firstly, the density of buildings around each Q. robur within a radius of 150, 250, 350, 500, 700 and 1000 m was calculated. Secondly, the average age of the five closest buildings were also used as a measure of the age since urbanization.

Lichens richness and cover was higher in the rural environment than in the urban

environment there were, however, one exception: Lepraria incana (Figure 8).

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Figure 8. a) to c) Fourteen investigated lichen species and their occurrence and cover between urban and rural environment on tree trunks of Quercus robur are compared.

a) Shows the proportion of trees with lichen occurrence. b) Shows the average

percentage cover on trees with occurrence. c) Shows the average percentage cover of

all trees (also those lacking the species in question).

Studies on spatial and temporal distributions of epiphytic

Linköping Studies in Science and Technology Dissertation thesis No. 1471