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 © Håkan Lättman 2012 Linköping Studies in Science and Technology ISBN 978–91–7519–810–1 ISSN 0345–7524 Printed by LiU-Tryck Linköping, Sweden, 2012 II Table of contents LIST OF PAPERS IV MY CONTRIBUTIONS TO THE PAPERS IV ABSTRACT V INTRODUCTION 1 WHAT IS A LICHEN? 2 DISPERSAL STRATEGIES 2 ENDURING HARSH ENVIRONMENTS, YET ALSO SENSITIVE 4 SUNLIGHT 4 THE AIR 5 CLIMATE CHANGE: TEMPERATURE AND MOISTURE 6 SUBSTRATE 7 AIMS OF THE THESIS 8 FURTHER BACKGROUND AND THE INCLUDED PAPERS 9 GROWTH 9 GENERATION TIME OF LICHENS 10 Paper I 11 IS SUBSTRATE OR DISPERSAL LIMITING? 12 Phorophyte and stand 12 Spore dispersal 12 Paper II 13 LARGE-SCALE DYNAMIC OF LICHENS 16 Dynamics of lichen thalli 16 Lichens on the move 17 Paper III 17 LICHENS IN THE URBAN ENVIRONMENT 19 Trees: an important urban element 20 Urban effects on lichens 21 Paper IV 21 CONCLUDING REMARKS 25 POPULÄRVETENSKAPLIG SAMMANFATTNING 26 VAD ÄR EN LAV? 26 RESULTAT FRÅN MIN FORSKNING 26 ACKNOWLEDGEMENT 28 REFERENCES 29 III 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. IV 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: [email protected]; [email protected] ISSN 1652–7399 ISBN 978–91–7519–810–1 ISSN 0345–7524 V 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 1 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.