Dispersal and persistence of an epiphytic lichen in a dynamic pasture-woodland landscape Inauguraldissertation der Philosophisch-naturwissenschaftlichen Fakultät der Universität Bern Vorgelegt von Silke Werth von Deutschland Leiter der Arbeit: PD Dr. C. Scheidegger Eidgenössische Forschungsanstalt WSL, Birmensdorf ZH Dispersal and persistence of an epiphytic lichen in a dynamic pasture-woodland landscape Inauguraldissertation der Philosophisch-naturwissenschaftlichen Fakultät der Universität Bern Vorgelegt von Silke Werth von Deutschland Leiter der Arbeit: PD Dr. C. Scheidegger Eidgenössische Forschungsanstalt WSL, Birmensdorf ZH Von der Philosophisch-naturwissenschaftlichen Fakultät angenommen. Bern, 20. Juni 2005 Der Dekan Prof. Dr. P. Messerli Contents Synthesis 1 Introduction 1 Conclusions 7 Hierarchy theory and a conceptual model of epiphyte dynamics 7 Biology of Lobaria pulmonaria 9 Dispersal versus establishment limitation 11 Implications for conservation of L. pulmonaria 17 Chapter 1 23 Chapter 2 49 Chapter 3 71 Chapter 4 105 Chapter 5 137 Summary 149 Appendix 1 (Population genetic sampling) 153 Appendix 2 (Transplants) 165 Appendix 3 (Snow samples) 167 Acknowledgements 169 Curriculum vitae of Silke Werth 171 Synthesis Introduction Traditional sylvopastoral landscapes exhibit dynamics in the form of shifting mosaics of forested and open areas if disturbances are at intermediate levels (Olff et al. 1999). If grazing pressure is too high, wooded pastures develop into grasslands; in the absence of grazing, successional change leads to climax forests (Gillet et al. 2002). Wooded pastures would not be predicted as a favoured type of habitat for epiphytes requiring long ecological continuity of the forest canopy or for dispersal-limited epiphytes with long generation times, because shifting mosaic dynamics imply limited time for fulfilling life cycles, including dispersal to new patches of habitat. However, the epiphytic lichen Lobaria pulmonaria, which is considered to be dispersal-limited (Walser et al. 2001; Walser 2004), and has a long generation time compared with other foliose lichens (Scheidegger & Goward 2002), has a hotspot of its occurrence in Switzerland in a sylvopastoral landscape in and around the Parc Jurassien Vaudois (Zoller et al. 1999; Rychen 2002). L. pulmonaria is widely distributed in the nemoral and boreal zones of the northern hemisphere, with some additional occurrences in the southern hemisphere (Yoshimura 1971). This tripartite lichenised fungus is associated with the green algae Dictyochloropsis reticulata and cyanobacteria of the genus Nostoc (Geitler 1966; Jordan 1970). The generation time in lichens is defined as the average age at which a population of a lichen produces propagules, be it soredia, isidia, thallus fragments, or ascospores. Generation time in populations of L. pulmonaria in central Europe has been estimated to be 30 years or longer (Scheidegger & Goward 2002). In Europe and North America, L. pulmonaria is mainly associated with old-growth forests (Lesica et al. 1991; Rose 1992; Radies & Coxson 2004). Owing to air-pollution and intensive forest management, the species has faced a severe decline in central and northern Europe (Hallingbäck & Martinsson 1987), where it is red-listed in several countries (Wirth et al. 1996; Aptroot et al. 1999; Scheidegger et al. 2002; Søchting & Alstrup 2002). The population of the L. pulmonaria in the pasture-woodland landscape in the Parc Jurassien Vaudois is not only one of the largest in Switzerland, but also seems to exhibit genetic variation comparable in magnitude to that of populations in the Swiss 1 Synthesis Alps and the Swiss Plateau (Zoller et al. 1999), despite the fact that the forests of the Parc Jurassien Vaudois are and were subjected to disturbances, mainly in the form of grazing pressure on juvenile trees, mainly uneven-aged forestry, some stand-level timber logging, and also stand-replacing disturbances (Vittoz 1998; Kalwij et al. in press). Genetic diversity of populations of L. pulmonaria would be expected to be low in this system for several reasons. Firstly, disturbances affecting carrier trees such as Acer pseudoplatanus resulting in reductions of L. pulmonaria population sizes may lead to instant loss of rare alleles (Nei et al. 1975). Secondly, new populations in disturbed areas which were founded by only few individuals may be subject to genetic drift, i.e., random changes in allele frequencies, leading to fixation or further loss of alleles even if overall mean allele frequencies remain constant among populations (Hartl & Clark 1997). Whether the spatial genetic signature differed among disturbance types in L. pulmonaria interested me greatly. Large population sizes of a putatively dispersal-limited organism with high genetic variation in a dynamic landscape represent an apparent contradiction, which is why I was particularly interested in studying patterns of genetic diversity in sites differing in disturbance history, as well as dispersal and establishment in L. pulmonaria. Dispersal and establishment are key processes in the life history of organisms (Clobert et al. 2001). The there has been a debate about the role of dispersal in structuring in the composition of local communities, namely if local species assemblages are a function of dispersal ability or of site conditions (Leibold et al. 2004; Ozinga et al. 2005a; Ozinga et al. 2005b). The relative importance of different environmental factors, such as regional- scale versus local factors in structuring communities can be determined by an investigation of communities along regional gradients, while simultaneously measuring site conditions (Ohmann & Spies 1998; Peterson & McCune 2001), and subjecting the resulting dataset to gradient analysis techniques such as constrained ordination (Økland 1990; Borcard et al. 1992). This study aimed (1) to determine if and how genetic structure and diversity of L. pulmonaria are influenced by disturbance type, (2) to partition spatial genetic structure to a clonal and a recombinant component, (3) to reveal to which degree the distribution of L. pulmonaria in the sylvopastoral landscape is limited by propagule availability versus establishment, (4) to assess the significance of a putative barrier to gene flow in the 2 Synthesis sylvopastoral landscape and to determine the spatial extent of populations in the studied landscape, (5) to determine the relative importance of local site conditions vs. regional gradients in shaping epiphytic lichen communities. These issues can be summarised in five main questions: (i) What is the effect of two types of stand-level disturbances on the genetic diversity and spatial genetic structure in L. pulmonaria? (ii) Are there spatially separate populations of L. pulmonaria in the study area, and do large open pastures represent effective barriers to gene flow in this species? (iii) Is the distribution of L. pulmonaria in a sylvopastoral landscape limited by dispersal or establishment, or by both? (iv) What is the spatial extent of clonal versus recombinant genetic structure? (v) How important are local environmental conditions versus large-scale, regional gradients in structuring epiphytic macrolichen communities? The relationship between disturbance type and spatial genetic structure and genetic diversity is analysed in the first chapter. The second chapter determines how many populations are present in the study area, and assesses the effectiveness of a putative barrier, a large pasture, to restrict past gene flow in L. pulmonaria. In the third chapter, the role of dispersal versus establishment in limiting the distribution of L. pulmonaria in the study area is investigated. The spatial extent of overall genetic structure, as well as of its clonal and recombinant component are assessed in the fourth chapter. The importance of local environmental conditions versus large-scale environmental gradients for the species composition of epiphytic macrolichen communities is investigated in the fifth chapter. We furthermore investigated the implications of stand-replacing and stand-level disturbance under different levels of local versus global dispersal for persistence of L. pulmonaria using modelling approaches. The resulting manuscript is not included in this thesis. We discuss the results gained in the light of hierarchy theory. Novel and exciting aspects of the biology of L. pulmonaria are presented. The role of dispersal limitation vs. establishment limitation in structuring the 3 Synthesis local distribution of L. pulmonaria is reviewed, and implications for conservation of L. pulmonaria are discussed. Influence of disturbance type on genetic structure and diversity Old-forest associated lichens are commonly assumed to be negatively affected by tree logging or natural forest disturbances. However, we found that genetic diversity of Lobaria pulmonaria depends on the type of disturbance. Using 895 thalli collected from 41 plots of 1 ha (demes) corresponding to the disturbance categories stand-replacing disturbance, intensive logging and uneven-aged forestry, we determined fragment length at six mycobiont-specific microsatellite loci. There was evidence for multiple independent colonisations of demes located in areas affected by disturbance at forest stand level. Using spatial autocorrelation methods, we determined the spatial scale of similar genetic structure discriminating among the clonal and recombinant component of genetic variation and among disturbance type. Spatial autocorrelation of gene