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Explaining the Composition and Diversity of Lichen Epiphytes on Aspen (Populus Tremula L.)

Christopher J. Ellis Royal Botanic Garden Edinburgh

Published on-line: 2008

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> Historical Background

Aspen was ‘discovered’ by British lichenologists around the turn of the new millennium. Consistent with the belated recognition of aspen as the ‘Cinderella species’ of Scottish conservation, the first detailed survey of aspen lichen epiphytes was undertaken in 2001, by Dr Brian Coppins of the Royal Botanic Garden Edinburgh (RBGE) and Les and Sheila Street (RSPB). Subsequently, Coppins et al. (2001) and Street & Street (2001) provided a species inventory and analysis for six aspen stands in Strathspey. Their reports included the discovery of species new to Britain (e.g. Arthonia patellulata, Bacidia igniarii and Caloplaca ahtii), the rediscovery of a species previously thought extinct (i.e. Lecanora populicola, last recorded from East Norfolk over 150 years ago), and viable populations of species that are rare and/or threatened in the British Isles (e.g. Bacidia vermifera, Biatoridium delitescens, Catinaria neuschildii and Fuscopannaria ignobilis). This exciting work on lichens supported the wider recognition of aspen as a previously neglected habitat-feature which is of special importance to native woodland biodiversity (Cosgrove & Amphlett 2002). The initial lichen survey of aspen stands in Strathspey appeared to confirm for Scotland the results of earlier work carried out in Scandinavia, which had highlighted the difference between the epiphyte flora of aspen and that of co-occurring tree species (Kuusinen 1994, 1996). The individual trees comprising many Scottish aspen stands have bark characteristics that are structurally different and relatively less acidic than those of co-occurring birch, pine and juniper. The lichen flora of aspen is correspondingly different. Thus, the aspen flora frequently includes crustose species more typical of eutrophic conditions, i.e. Bacidia arcuetina, Caloplaca cerinella and C. pyracea, Lecania naegelii, Lecanora carpinea, L. persimilis and L. sambuci and the foliose Xanthoria parietina. In north-east Scotland these crustose assemblages may also include the aspen specialists Arthonia patellulata and Lecanora populicola (including its parasite Candelariella superdistans), and species which apparently show a preference for aspen bark, i.e. Caloplaca ahtii, Diplotomma pharcidium and the rarely recorded Lecania dubitans. However, the character of aspen bark (e.g. its relatively high pH) may also favour the local occurrence of ‘Lobarion’ epiphytes (cf. Gauslaa 1985). In oceanic western Scotland a Lobarion-type community occurs frequently in habitats and on substrata of varying quality. The community becomes increasingly restricted to specific micro-habitats where the climate is sub-optimal (e.g. the drier straths of eastern Scotland) and in such circumstances it is duly considered a characteristic of mature old-growth woodland (cf. Coppins & Coppins 2002). In the woodlands of Strathspey and Deeside, elements of the Lobarion and comparable ‘cyanolichens’ occur on aspen where they are absent from other tree species, suggesting the important role of aspen in providing local micro-habitat to maintain the components of old-growth communities. This paper reports advances in our understanding of the aspen lichen flora which have emerged since the previous aspen conference in 2001. During 2003-2005 a detailed survey of aspen was incorporated into Phase II of RBGE’s Scottish Rare Plants Project. The aspen research programme developed out of a critique of Scottish lichen conservation which called for greater effort towards understanding the response of lichen species and communities to habitat dynamics (Coppins 2003). This critique provided a mandate for the aspen survey, and the research described here aimed to provide an ecological framework explaining variation in lichen species composition and richness in response to the dynamics of the aspen habitat. The survey therefore had two complimentary aims:

(i) to inventory lichen diversity associated with aspen in Scotland, (ii) to develop a framework describing patterns of epiphyte species richness and community

composition at contrasting scales, regional (larger-scale) and local (smaller-scale): i.e. between stands and within stands (between trees). The results are presented here as three key findings, separated according to scale. Each of the highlighted findings is directly relevant to aspen management for biodiversity conservation.

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> Landscape-Scale Processes

Ninety-three aspen stands were surveyed from sites across northern Scotland (Fig. 1a). This wide selection of stands aimed to reflect the status of aspen in the present-day landscape. Sampled aspen stands thus comprised variation in macroclimate (from the oceanic west coast, to the drier north-east), landscape setting (e.g. native mixed wood, broadleaf and pinewood settings, isolated submontane, riparian and wayside stands, and stands in unimproved pasture), topography (e.g. varying aspects and degree of exposure), geology and soil type. However, all stands were sampled from a relatively clean-air region of northern Scotland (cf. NEGTAP 2001), aiming to avoid the confounding effect of air pollution. A comprehensive inventory of lichen epiphytes was determined for each stand. Two-hundred and seventy-nine lichen epiphytes were described growing on aspen across the 93 study sites (see supplementary species list, included below).

> Key-finding One: Species Richness is controlled by Historic Woodland Extent The relationship between the richness of species and spatial area of habitat is one of the most fundamental biogeographic principles. The ‘species-area’ relationship was originally developed to describe a dynamic between the number of species and island area/isolation (MacArthur & Wilson 1967; Thornton 2007) although it is also a powerful tool in conservation. Isolated patches of habitat in a modified landscape can be approximated as islands (e.g. remnant woodland, in a ‘sea’ of farmland or moorland), and changes in habitat area and/or fragmentation fit into a predictive framework with which to assess the threat to biodiversity (Pullin 2002). Consistent with the species-area relationship, a minority of species recorded from aspen are aspen specialists (c. 1.5%), so one would expect the diversity of lichen species in aspen stands (typically < 1 ha) to be functionally related to the amount of woodland in the surrounding landscape. A greater extent of woodland within local proximity may result in a larger species-pool for colonisation into aspen stands nested within this woodland matrix. In an exploration of the species-area relationship, the number of lichen epiphytes in individual aspen stands was compared to the physical extent and fragmentation of woodland in the wider landscape (% woodland cover). In addition, richness was compared to woodland extent/fragmentation at two scales – 1 km2 and 4 km2 – and for two time-frames: (i) extent/fragmentation in the modern landscape (based on analysis of Editions B & C of the Ordnance Survey’s Landranger series) and (ii) in the historic landscape (based on analysis of the Ordnance Survey’s 1st one-inch series: 1869-1886). An observed relationship between lichen epiphyte species richness and woodland extent/fragmentation was statistically significant, though relatively weak (Fig. 2). Nevertheless, the significant relationship confirms a fundamental expectation, and ‘noise’ in the data is attributable to environmental variation when comparing aspen stands which were surveyed from a variety of settings.

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Figure 1. The distribution of aspen study sites: A. ninety-three sites included in the Scotland-wide qualitative inventory of aspen epiphytes, B. the sub-selection of sixteen sites for the quantitative analysis of species composition.

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Importantly, when comparing lichen epiphyte richness to woodland extent/fragmentation, richness was significantly related to the extent and fragmentation of woodland in the historic 19th Century landscape, though was not related to woodland extent/fragmentation in the present-day landscape (Ellis & Coppins, 2007a). This surprising result suggests a lag period between a change in woodland extent/fragmentation, and subsequent impacts on lichen epiphyte diversity. Thus, if there is a loss of woodland extent, or an increase in fragmentation, lichen epiphytes may continue to survive in remnant habitat seemingly unaffected. However, as a species’ populations within the remaining woodland senesce and die, there may be a greatly reduced chance of their replacement by colonisation from the surrounding landscape. Over time this process of non-replacement may cause a gradual loss in local diversity. This pattern of long-term species loss subsequent to habitat degradation has come to be known as an ‘extinction debt’. The extinction debt is an emerging theme in conservation (Lindborg & Eriksson, 2004; Helm et al., 2006; Vellend et al., 2006), has been previously demonstrated for lichens (Berglund & Jonsson 2005), and it has severe consequences for conservation. The extinction debt indicates that a fundamental assumption of conservation strategy may be flawed: an assumption that the protection of species-rich sites secures their future may be invalid. Rather, it is necessary to look beyond the protected site, to landscape-scale process over ecologically-realistic time-scales. Thus, certain species-rich sites (even if protected) may exist on ‘borrowed time’, and may be suffering an ongoing loss of species over decades or centuries. The implication is that species-rich remnant habitats may need remedial action – e.g. the regeneration of a native forest network – to prevent a hidden though inexorable loss of epiphyte diversity.

> Key-Finding Two: Compositional Variation is related to Climatic Setting and Historic Woodland Extent The aspen epiphyte extinction debt appears to be stronger for certain types of species. It is possible to partition species into groups according to their ecological traits, and, perhaps not surprisingly, the extinction debt is felt strongest by species which are (in general) relatively more specialist in their habitat requirements and dispersal-limited (Ellis & Coppins, 2007a). For these species the landscape surrounding each woodland remnant (or ‘island’) will more closely approximate to a hypothetical ‘sea’, with fewer opportunities for the colonisation of ‘stepping stones’, that is, intermediate sites in the habitat matrix outwith surviving woodland. There are two problems for species which are subject to this double jeopardy (dispersal limitation, habitat specialisation). First, as the distances between suitable habitats increase, the chances of colonisation (to replace senescent populations or individuals) decreases for dispersal-limited species. Second, there is a strong relationship between woodland area and the heterogeneity of micro-habitats (Gignac & Dale 2005). Smaller woodland fragments are less likely to have suitable niche-space for habitat-specialist epiphytes, so that even if propagules disperse into a woodland the chances of establishment may be reduced by the lack of available micro-habitat.

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Figure 2. Positive relationship between historic woodland extent (at a 1 km2 scale) and the species richness of lichen epiphytes in aspen stands.

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Epiphyte richness, controlled at least in part by historic woodland structure, can be explained as the response of species with particular traits. However, because different species by definition have different adaptive traits, historic woodland structure should, at least partly, also explain species composition. To investigate whether or not this is the case, this paper presents a previously unpublished ordination analysis carried out to examine epiphyte species composition across the 93 study sites (cf. Appendix One). Constrained ordination was used to partition the role of climatic setting and woodland structure in explaining species composition. The study sites occupied a region outwith the influence of strong pollution effects, and lichen epiphytes are known to respond strongly to a steep climatic gradient from the oceanic west coast to the more continental north-east. Consistent with this expectation, climatic setting was found to be the single most important explanatory factor for epiphyte species composition (Fig. 3). It is therefore notable that historic woodland extent (as opposed to present-day woodland structure) was effectively as important an explanatory variable of species composition as climate (i.e. combined at the 1 km2 and 4 km2 scales, historic woodland extent accounts for c. 50% of the explained variation in species composition: Figs 3 & 4, cf. Appendix One). It is also possible to explore the relationship between species composition and patterns in species richness. Thus, while ordination axis one (≈ climatic setting) was uncorrelated with species richness, ordination axis two (≈ historic woodland extent) was significantly correlated with richness (Fig. 3). Taken together, these results support the non-random effect of historic woodland

structure on epiphyte composition (susceptibility of species according to their ecological traits), and, subsequently, on richness.

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Figure 3. Constrained ordination biplot (redundancy analysis cf. Appendix One), used to summarise variation in lichen epiphyte composition compared between aspen stands, with respect to selected explanatory variables: climatic setting and historic woodland extent (at the 1 km2 and 4 km2 scale). Symbols (aspen stands) are size-scaled according to species richness. Richness was significantly related to axis two (r = 0.325, P < 0.005), though not to axis one (r = 0.143, P > 0.05).

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0.3% Figure 4. Venn diagram to partition the effects of climatic setting and historic woodland extent in explaining epiphyte community composition. Total variation explained (c. 9.9%) is reasonably good considering the data matrix consists of 279 species across 93 sites. Importantly, historic woodland extent explains an equivalent amount of compositional variation when compared to the widely acknowledged climatic effect.

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> Stand-scale Processes A sub-set of 16 aspen stands was selected for the quantitative analysis of lichen communities (Fig. 1b). Sites were selected to reflect biogeographic variation between regions, though sampling was also focussed in Strathspey, which contains the greatest concentration of aspen woodland in Scotland. The study aimed to sample aspen trees of different age within each selected stand. Because of their clonal growth by suckering, individual aspen trees within a stand tended to fall into discrete size classes, which corresponded broadly to their age determined by dendrochronology. Trees were grouped into two or three size classes at each site, depending on the number of recognisable cohorts. The community of lichen epiphytes was thus quantified for either two or three trees of contrasting age within each stand. To ensure comparability between sites, sampled trees were subjectively selected to ensure that each was growing vertically and that the bark surface was not subject to aberration, e.g. by wounding, branching etc. The linear distance between the sampled tree and its five nearest neighbours was measured to ensure an approximately equal density of stems and equivalent shading. Community composition (species % frequency of occurrence) was measured for multiple quadrats on a single tree, and a range of bark characteristics was quantified: bark rugosity (roughness), pH and conductivity, and water holding capacity (cf. Appendix Two). > Key-finding Three: A Three-way Dynamic Relationship between Climatic Setting, Tree Age and Vertical Height The detailed sampling of lichen community composition demonstrated a series of gradients corresponding to the dynamics of the aspen habitat, and along which patterns in epiphyte composition were broadly similar. These comparable patterns in epiphyte communities along different gradients provide support towards the ‘similar-gradient hypothesis’, which was first developed for epiphytes in the forests in western North America (McCune 1993). This hypothesis grouped epiphytes according to their ecological traits (as ‘cyanolichens’, ‘alectorioid lichens’, ‘other lichens’ and bryophytes) and described similar patterns in community composition along three contrasting gradients: (i) vertical height in the forest canopy, (ii) local moisture regime, and (iii) along temporal gradients in forest continuity. In a comparable analysis for aspen epiphytes, six ecological trait groups were recognised (cf. Hale 1983): fruticose green-algal lichens, foliose green-algal lichens, foliose cyanolichens, crustose (green-algal) asexually reproducing lichens, and crustose (green-algal) sexually reproducing lichens. With respect to these traits, analogous patterns in community composition appear to operate along three ‘similar-gradients’: (i) Tree age: focussing on aspen stands in northern and eastern Scotland, there appears to be a dynamic succession of epiphytes grouped according to their ecological traits (Fig. 5a).

Thus, small-statured and sexually-reproducing crustose lichens are early colonists of aspen bark (e.g. Caloplaca pyracea, Lecania naegelii, Lecanora carpinea, L. chlarotera, L. populicola, Lecidella elaeochroma). These species become less important in terms of their abundance in the epiphyte community as the tree ages, and they are replaced progressively by foliose lichens, bryophytes and asexually-reproducing crustose lichens (Fig. 5a; cf. Ellis & Coppins 2007b). These changes may be under allogenic control, e.g. in response to change in bark micro-habitat, such as bark rugosity and pH (Fig. 6a).

However, the sequence of change also points to autogenic succession driven by species interaction. Early colonising sexual crusts may be physically out-competed by over-topping from foliose lichens and bryophytes (John 1992; cf. Fig. 7), and appear to be more ruderal in their life-histories than asexual crustose lichens (Ellis & Coppins 2007b). However, while traits provide a generalisable framework, it is important to remember that nested within the trait characteristics of a community are the responses of many individual species. It is therefore possible that two trees may experience an equivalent successional sequence in terms of epiphyte community traits while the species which underlie these changes may themselves be different. Thus, the replacement of sexual crusts by foliose lichens may

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comprise Hypogymnia physodes on a relatively more acid barked tree, compared to Phaeophyscia orbicularis and Xanthoria parietina where the bark pH is higher (Fig. 8).

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Figure 5. Comparison of community trait variation with aspen tree age and height on the tree bole. A. Response of contrasting ecological trait groups to tree age (cf. Ellis & Coppins 2007b). Percent frequency of occurrence was standardised for each aspen stand, thereby controlling for compositional variation related to landscape-scale processes (cf. Figs 2 & 3). Tree age was standardised to enable a comparison between stands with contrasting histories of recruitment, and different age structures, B. Response of epiphyte trait groups to height on the tree bole.

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Figure 6. Comparison of estimated bark pH with aspen tree age and height on the tree bole. A. Comparison of estimated tree age and bark pH (tree mean and 1 S.D.), B. Comparison of bark pH with height on the tree bole.

Figure 7. Ecological dynamics writ small! The foliose species Parmelia sulcata and associated bryophytes are over-growing and out-competing an abundantly fertile though small-statured crustose species in the genus Lecanora.

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Figure 8. Modelled response of some common foliose lichens to aspen bark pH. Models were generated using nonparametric multiplicative regression (McCune 2006), P < 0.001 in all cases.

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(ii) Height on the Tree Bole: a single recently wind-blown tree provided the opportunity for detailed analysis of epiphyte community change with height on the tree bole (Fig. 9).

In most epiphyte analyses quadrats are sampled from an accessible region of the lower bole (up to c. 170 cm height). During the aspen study it was possible to compare community patterns described from the lower boles of aspen trees to samples collected from the full vertical height of a single fallen tree. Thus, quadrats were sampled at 20 cm intervals upwards along the length of the fallen tree. Interestingly, change in community composition with respect to epiphyte traits, upwards along the tree bole, was analogous to the shift in trait composition observed for the lower bole of aspen trees during a successional sequence as the tree ages (cf. Figs 5a & 5b). There may therefore be an upwards shift of early colonising species during the life-span of the aspen tree. Such species may continue to exist within an ageing aspen stand, though higher on the aspen bole and into the canopy, while the lower bole undergoes a succession towards a different community structure.

In both cases – on the lower bole as the tree ages, and upwards along the bole – the observed change in the frequency of different trait groups correlates with the richness of species included within those groups (Fig. 10). This clearly indicates that a transition between trait groups is not owing to few dominant species replacing one another, but comprises an important change in the richness of species included within those groups. However, as explained with regard to succession on the lower bole, the details of species composition (nested within trait groups) may be determined by specific micro-habitat factors. With regard to the tree bole, there was a clear transition in bark rugosity from the lower bole (rougher) to a smoother portion which comprised most of the upper bole (over c. 2.5 metres in height). In addition, bark pH increased upwards, from c. pH 3.75 at the lower bole, to c. pH 5.5 at heights > 10 m (Fig. 6b). Accordingly, this change in bark pH was accompanied by a shift in species, from those which occur on more acid barked trees (e.g. Hypogymnia physodes, Ochrolechia androgyna) to those more typical of eutrophic bark conditions (e.g. Caloplaca pyracea, Physcia aipolia). This transition included species of specific conservation interest which occurred higher on the tree bole than would normally be searched during a lichen field survey: Arthonia patellulata, at 6.7m; Bacidia subincompta, at 3.2m; Caloplaca ahtii, > 5m; Lecania dubitans, at 5.6 & 6.9m.

Figure 9. Windblown aspen tree near Tombhain (NH 869070), which was subject to detailed vertical sampling upwards along the tree bole and into the canopy.

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Figure 10. Comparison of % frequency of occurrence for contrasting trait groups (crustose and foliose lichens) and the number of component species.

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The upward trend in bark pH with height appears to be a common feature of aspen, and is revealed by the occurrence of the yellow foliose lichen, Xanthoria parietina. This species may occur quite low down on certain trees, though is easily spotted high on the bole on trees that may be colonised by acid bark epiphyte communities where the pH is more acidic on the lower bole. Xanthoria parietina is a ‘lead in’ species, easily spotted and a useful guide when trying to find the smaller aspen specialist species such as Arthonia patellulata, Caloplaca ahtii, Diplotomma pharcidium and Lecanora populicola (and its parasite Candelariella superdistans). These smaller species may occur on patches of bark between the foliose Xanthoria, though would not normally be found on acidic bark colonised by species such as Hypogymnia physodes, or Platismatia glauca. (iii) Climatic Setting: the pattern of change with respect to species’ ecological traits observed for trees within a single stand (e.g. Fig. 5) appears to be offset along a climatic gradient from the relatively drier and more continental climate of north-east Scotland, towards the wetter climate of oceanic western Scotland. Thus, with a shift towards a wetter climatic regime, sexually-reproducing crusts appear to be out-competed relatively earlier during the development of the epiphyte community by foliose lichens and especially bryophytes: i.e. younger trees under a more oceanic regime appear to be similar to relatively older trees in a more continental climatic setting (Ellis & Coppins 2006; cf. Fig. 11). With increasing oceanicity there is also a shift from colonisation by green-algal foliose lichens, towards an increasing abundance of foliose cyanolichens (Fig. 11). In the hyper-oceanic climate of western Scotland foliose cyanolichens are frequently abundant on relatively young aspen trees (> 50 yr), though are found only rarely and typically on old and mossy aspen trees in more continental eastern Scotland, particularly in old-growth woodlands (cf. Ellis & Coppins 2006; Ellis & Coppins 2007c). Ellis & Coppins (2006) hypothesised a facilitation effect for cyanolichens along the climatic gradient from relative wetness to dryness, by which the presence of mosses on older trees might create a humid micro-climate suitable to the establishment of cyanolichens under a sub-optimal climatic regime.

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Figure 11. The abundance of lichen epiphytes classified into different ecological trait groups, quantified for trees of different age (old: 95 ± 8 yr, medium-aged: 63 ± 12 yr, and young: 39 ± 3 yr) in three contrasting climatic settings: an oceanic climate at Loch Sunart, an intermediate climate at Loch Laggan, and a relatively continental climate in Speyside. These patterns are typical of other stands in similar climatic settings.

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> Recommendations for Conservation The description of epiphyte community change with respect to aspen habitat dynamics provides a model sequence along important ecological gradients: e.g. climatic setting, tree age, and height on the tree bole. This template of community change is relevant to aspen dynamics and is limited by sampling targeted towards a series of idealised scenarios (upright trees, without wounding, and with uniform shading). The analysis of traits and subsequent generalisations provide a useful template with which to develop an ecological framework towards the protection of epiphyte species diversity. The idealised dynamic portrayed here will be subject to the distortions of unpredictable and localised effects, and caution should be used to ensure the framework is not applied too literally. However, based on our preliminary analysis of aspen epiphytes, three recommendations are highlighted:

1. Aspen stands from sites across a range of climatic settings should be integrated into woodland management. This will protect different epiphyte species and communities which occur across steep climatic gradients within Scotland.

2. Importantly, aspen may provide suitable habitat for old-growth indicator species (e.g. species in the ‘Lobarion’-community) in localities with a sub-optimal climatic setting. However, where these old-growth species occur in remnant aspen stands they may be subject to an extinction debt. Species-rich aspen stands should be protected by regenerating a network of native woodland. This network would buffer stands from long-term species loss through the reestablishment of effective meta-population dynamics following past periods of habitat loss/fragmentation. As an additional benefit, it is likely that woodland regeneration will also provide a buffer against the impacts/uncertainties of climate change (Ellis & Coppins 2007c, Ellis et al. 2009).

3. Stand-scale management should aim to ensure the periodic regeneration of aspen stands, and a range of cohorts comprising trees of different age. Where possible, survey and monitoring should consider not just the lower bole of trees, but also shifts in community composition upwards along the tree bole and into the canopy.

4. In addition, the following observations might be made, based on extensive fieldwork: (i) epiphyte diversity is likely to be highest in a gladed pasture woodland setting (as opposed to closely-grown aspen thickets), (ii) epiphyte diversity is highest where trees of different age grow in a variety of local micro-climatic settings, e.g. with respect to topography, aspect, exposure etc, and (iii) this framework of micro-habitat variability also includes differences in aspen bark structure and chemistry, which may be under genetic control (e.g. Bailey et al. 2005) as well as in response to variations in soil types/geologies (Gustafsson & Eriksson 1995).

> Future Directions Studies during the period 2003-2005 aimed to provide a broadly deterministic (i.e. predictive) framework for understanding lichen epiphyte composition and diversity with respect to habitat dynamics. One potential area of great interest which could not be tackled was the effect of aspen clonality on epiphyte composition. Field observations at a number of sites suggested that putatively different aspen clones growing within the same approximate locality (e.g. in terms of climate and geology) can have quite different epiphyte communities. With aspen chemistry (e.g. phenolics) under genetic control it is feasible that the clonal composition of aspen may play a role in generating patterns in epiphyte composition. At a time when aspen is being planted into the British landscape in an effort to regenerate native woodland, the genetic control of epiphyte communities is a question of significant concern.

A further question relates to the limits of deterministic ecology in conservation. In an effort to provide a predictive understanding of epiphyte composition relevant to conservation practitioners, epiphyte communities were simplified by trait classifications, and are explored as the deterministic response to

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easily measured habitat gradients. This builds upon previous work in North America (McCune 1993). Recent work in ecology points to the simultaneous operation of both deterministic and stochastic forces in controlling community structure (Gravel et al. 2006; Adler et al. 2007), and quantifying the relative importance of each of these forces has profound implications for conservation. If communities are strongly structured deterministically, predictive models should provide a powerful evidence base for habitat management. If communities are structured stochastically, and/or there is large ‘redundancy’ between species (i.e. multiple species may occupy the same niche), the predictive management of habitats will be weakened, and the extent of the protected network would need to allow for the fundamental uncertainty in species composition. Ongoing work on epiphytes at RBGE aims to examine the limits to deterministic trait-based models of community structure, exploring the relative importance of stochasticity and species redundancy.

> Acknowledgements

I thank Ern and Val Emmett for their endless enthusiasm and support of the aspen epiphyte project; also, John Parrott for his generosity in sharing insights and data on the spatial extent of aspen stands. The staff at Insh Marshes NNR, and especially Pete Moore, have been extremely supportive in enabling this research, and their keen interest in the potential implications of the results is warmly appreciated. This network of support and interest extends to many organisations, including Trees for Life, FC and Forest Research, RSPB Abernethy, and many private landowners. Finally, I thank the Esmée Fairbairn Foundation and the Scottish Government (RERAD) for funding this research. > References

Adler, P.B., Hille. R, Lambers, J. & Levine, J.M. (2007) A niche for neutrality. Ecology Letters, 10: 95-104. Bailey, J.K., Deckert, R., Schweitzer, J.A., Rehill, B.J., Lindroth, R.L., Gehring, C. & Whitham, T.G.

(2005) Host plant genetics affect hidden ecological players: links among Populus, condensed tannins and fungal endophyte infection. Canadian Journal of Botany, 83: 356-361.

Berglund, H. & Jonsson, B.G. (2005) Verifying an extinction debt among lichens and fungi in northern Swedish boreal forests. Conservation Biology, 19: 338-348.

Coppins, A.M. & Coppins, B.J. (2002) Indices of ecological continuity for woodland epiphytic lichen habitats in the British Isles. British Lichen Society, London.

Coppins, B.J. (2002) Checklist of lichens of Great Britain and Ireland. British Lichen Society, London. Coppins, B.J. (2003) Lichen conservation in Scotland. Botanical Journal of Scotland, 55: 27-38. Coppins, B.J., Street, S. & Street, L. (2001) Lichens of aspen woods in Strathspey. Unpublished Report. Cosgrove, P. & Amphlett, A., eds (2002) The biodiversity and management of aspen woodlands. The

Cairngorms Local Biodiversity Action Plan, Grantown-on-Spey. Ellis, C.J. & Coppins, B.J. (2006) Contrasting functional traits maintain lichen epiphyte diversity in

response to climate and autogenic succession. Journal of Biogeography, 33: 1643-1656. Ellis, C.J. & Coppins, B.J (2007a) 19th Century woodland structure controls stand-scale epiphyte

diversity in present-day Scotland. Diversity and Distributions, 13: 84-91. Ellis, C.J. & Coppins, B.J. (2007b) Reproductive strategy and the compositional dynamics of crustose

lichen communities on aspen (Populus tremula L.) in Scotland. The Lichenologist, 39: 377-391. Ellis, C.J. & Coppins, B.J. (2007c) Changing climate and historic woodland structure interact to control

species diversity of the ‘Lobarion’ epiphyte community in Scotland. Journal of Vegetation Science, 18: 725-734.

Ellis, C.J., Yahr, R. & Coppins, B.J. (2009) Local extent of old-growth woodland modifies epiphyte response to climate change. Journal of Biogeography, in press.

Gauslaa, Y. (1985) The ecology of Lobarion pulmonariae and Parmelion caperatae in Quercus dominated forests in south-west Norway. The Lichenologist, 17: 117-140.

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Gignac, L.D. & Dale, M.R.T. (2005) Effects of fragment size and habitat heterogeneity on cryptogam diversity in the low-boreal forest of western Canada. The Bryologist, 108: 50-66.

Gravel, D., Canham, C.D., Beaudet, M., & Messier, C. (2006) Reconciling niche and neutrality: the continuum hypothesis. Ecology Letters, 9: 399-409.

Gustafsson, L. & Eriksson, I. (1995) Factors of importance for the epiphytic vegetation of aspen Populus tremula with special emphasis on bark chemistry and soil chemistry. Journal of Applied Ecology, 32: 412-424.

Hale, M.E. (1983) The biology of lichens. Edward Arnold, London. Helm, A., Hanski, I. & Pärtel, M. (2006) Slow response of plant species richness to habitat loss and

fragmentation. Ecology Letters, 9: 72-77. John, E. (1992) Distribution and interthalline interactions of epiphytic foliose lichens. Canadian Journal of

Botany, 70: 818-823. Kuusinen, M. (1994) Epiphytic lichen flora and diversity on Populus tremula in old-growth and managed

forests of southern and middle boreal Finland. Annales Botanici Fennici, 31: 245-260. Kuusinen, M. (1996) Cyanobacterial macrolichens on Populus tremula as indicators of forest continuity in

Finland. Biological Conservation, 75: 43-49. Legrand, I., Asta, J. & Goudard, Y. (1996) Variations in bark acidity and conductivity over the trunk

length of silver fir and Norway spruce. Trees, 11: 54-58. Lepš, J. & Šmilauer, P. (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University

Press, Cambridge. Lindborg, R. & Eriksson, O. (2004) Historical landscape connectivity affects present plant species

diversity. Ecology, 85: 1840-1845. MacArthur, R.H. & Wilson, E.O. (1967) The theory of island biogeography. Princeton University Press,

Princeton. McCune, B. (1993) Gradients in epiphyte biomass in three Pseudotsuga-Tsuga forests of different ages in

western Oregon and Washington. The Bryologist, 96: 405-411. McCune, B. (2006) Non-parametric habitat models with automatic interactions. Journal of Vegetation

Science, 17: 819-830. NEGTAP (2001) Transboundary air pollution: acidification, eutrophication and ground-level ozone in the UK.

National Expert Group on Transboundary Air Pollution, CEH, Edinburgh. Perry, M.C. & Hollis, D.M. (2005) The generation of monthly gridded datasets for a range of climatic

variables over the UK. International Journal of Climatology, 25: 1041-1054. Pullin, A.S. (2002) Conservation biology. Cambridge University Press, Cambridge. Street, L. & Street, S. (2002) The importance of aspen for lichens. In: The biodiversity and management of

aspen woodlands (Cosgrove, P. & Amphlett, A., eds), pp. 16-22. The Cairngorms Local Biodiversity Action Plan, Grantown-on-Spey.

Ter Braak, C.J.F. & Šmilauer, P. (2002) CANOCO v. 4.5, software for canonical community ordination. Ithaca, New York.

Thornton, I. (2007) Island colonization. Cambridge University Press, Cambridge. Vellend, M., Verheyen, K., Jacquemyn, H., Kolb, A., Calster, H.V., Peterken, G. & Hermy, M. (2006)

Extinction debt of forest plants persists for more than a century following habitat fragmentation. Ecology, 87: 542-548.

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> Appendix One, constrained ordination of epiphyte composition Ordination analysis was used to examine the relative importance of climatic setting and woodland structure in controlling epiphyte composition across the 93 aspen stands (cf. Fig. 1a). In an exploratory analysis, epiphyte communities were summarised using detrended correspondence analysis (DCA). The gradient length for the first DCA axis was < 3 (= 2.721), and constrained ordination was therefore performed using redundancy analysis, RDA (Lepš & Šmilauer 2003). Climatic setting: Climate data for each of the aspen study sites was derived from UK Met Office modelled data at a 5-km grid-square scale (Perry & Hollis 2005): estimated monthly and annual climatic averages for average, maximum and minimum monthly temperatures (oC) and precipitation (mm). A suite of 14 climatic variables was calculated for individual 5 km grid-squares corresponding to juniper study sites: mean annual temperature (oC), mean seasonal temperatures, temperatures of the warmest and coldest months of the year, annual temperature range, total annual precipitation (mm), and seasonal precipitation, and days per year with > 1 mm precipitation. Climatic variation compared between sampled juniper sites was summarised using principal components analysis, PCA. Climate data were standardised and centred to equalise variables measured on different scales (Lepš & Šmilauer 2003). The first axis described the majority of site-by-site variation in the climate data (98.7 %) and site scores along this axis were used to summarise the climatic regime. Woodland structure: Woodland surrounding each aspen stand was quantified for two time-periods: modern and historic. The extent and fragmentation of modern woodland was estimated for the period 1994-2004, based on Editions B & C of the Ordnance Survey’s 1:50,000 ‘Landranger’ map series and for historic woodland over a period during the 19th Century (1869-1886) based on the Ordnance Survey’s First (1-inch) Series. Positioning each aspen stand as a central node, woodland extent and fragmentation were estimated at two scales (1 km2 or 4 km2), for the modern and historic landscape, according to methods previously described by Ellis and Coppins (2007a). A trial analysis (RDA) with forward selection and a Monte Carlo test (9999 randomisations) was used to pre-select the most the explanatory variables describing species composition. Three explanatory variables were selected, in the following order: (i) climatic setting (var = 0.05, F = 4.83, P < 0.0001), (ii) historic woodland extent, 1 km2 (var = 0.03, F = 3.3, P < 0.0001), (iii) historic woodland extent, 4 km2 (var = 0.02, F = 1.44, P = 0.0158). A final RDA analysis was used to summarise variation in species composition according to the selected variables: climatic setting and historic woodland extent (Fig. 3). All analyses were performed using CANOCO v. 4.5 (ter Braak & Šmilauer 2002).

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> Appendix Two, methods for the detailed analysis of lichen community structure

The lichen community of each sampled tree was quantified in a series of 6 x 6 cm quadrats (comprising nine 2 x 2 cm sub-units), positioned at 20 cm intervals along a linear transect that spiralled around the bole (Fig. 10). The linear transect incorporated the shortest distance between ascending nodes marked on opposite sides of the bole at 0, 100 and 200 cm (side x) and 50 and 150 cm (side y). The number of quadrats sampled (i.e. sample area) was therefore dependent on the size of the bole (i.e. habitat area). Lichen species were recorded in the field as presence-absence in each of the nine sub-units, and a bark sample (c. 2 x 2 cm) was collected from each of the quadrats, incorporating any unidentified taxa which were returned to the herbarium for identification. Surface area of the tree bole was estimated for the region between the lowest and highest quadrats; i.e. approximating the bole as a series of stacked cylinders, based on the girth measured at the height from which each contiguous quadrat was sampled. Bole area was compared to the sampled quadrat area using product-moment correlation, confirming that the sampling method incorporates habitat area into the analysis of species composition and richness (r = 0.888, P < 0.001 with 38 d.f.). A core was collected from each of the sampled trees using a Presler-type increment borer. The tree was bored at a level height of 1 m, the core extracted and placed into an open-ended plastic tube which was labelled and sealed. The tree cores were sanded (180 grain sandpaper) to expose a plane surface. Cores were then stained by immersion first in a solution of 1% phloroglucinol and 95% ethyl alcohol for 1 minute and second in 50 % aqueous hydrochloric acid for c. 30 seconds, before rinsing under tap-water. Tree rings were counted to estimate tree age. Bark topography (Bt) was estimated for each quadrat using a measure based on Pythagorean theorem. Within each quadrat a transect was aligned perpendicular to the longitudinal structure of ridges and furrows; the width of ridges (r) and furrows (fl) and the depth of furrows (fd) was therefore measured. A measure of ridge versus furrow habitat within each quadrat was devised as the quotient of ridge and furrow ‘length’. Approximating the furrows within the bark as an isosceles triangle in cross-section, the depth of the furrow (fd) forms one side of two right-angled triangles. This depth is known (fd), while the other side is equal to half of the length of the furrow (fl / 2). The ‘length’ of furrow habitat (fL) can thus be calculated as twice the hypotenuse:

6 cm

6 c

m

2 m

A.

B.

Figure 12. The spiral transect quadrat method. A. The position of a line-transect as a spiral that circles up the tree bole, and the quadrat which is sampled at 20 cm intervals along the transect, B. The quadrat in action.

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fL = [√ (fl / 2)2 + (fd)2] * 2 Eq. 1

The log-quotient of ridge versus furrow habitat available in a cross section of each quadrat was therefore approximated:

Bt = LOG [r / fL] Eq. 2

The bark sample collected from each of the quadrats was examined in the laboratory for pH, electrical conductivity (µS/cm) and water-holding capacity. Bark samples were examined for pH and conductivity using a modification of the method described by Legrand et al. (1996), which is similar to that applied to aspen bark by Kuusinen (1994). The surface of each bark sample was cleaned of extraneous debris, lichens, other fungal material and bryophytes were removed, and the bark sample placed in a drying-oven at 35 oC for 24 hr. The dried bark sample was broken into small fragments, weighed and placed into a plastic beaker with an equivalent amount of deionised water at the ratio 1 ml:100 mg. The beaker was sealed and left to stand at room temperature (c. 21 oC) for 24 hr. Water in the beaker was agitated after c. 6 and 18 hr. A temperature-corrected measure of conductivity followed by pH was made for the aqueous solution (Hanna Instruments HI-991300 portable meter with an HI-1288 probe). Soaked bark samples were removed from the beakers, drip-dried in a jet of air and weighed wet. Samples were oven-dried at 80 oC for 76 hr and reweighed. The water-holding capacity was estimated as percentage H2O per mg dry weight.

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> SPECIES LIST < List of 280 lichen species recorded as aspen epiphytes across the ninety-three study sites (cf. Fig. 1a).

Nomenclature is mostly according to Coppins (2002) – with taxonomic updates included. Absconditella pauxilla Acrocordia cavata Acrocordia gemmata Alectoria sarmentosa subsp sarmentosa Amandinea punctata Anaptychia ciliaris subsp. ciliaris Anisomeridium biforme Anisomeridium polypori Arctomia delicatula Arthonia apatetica Arthonia didyma Arthonia mediella Arthonia muscigena Arthonia patellulata Arthonia punctiformis Arthonia radiata Arthonia vinosa Arthopyrenia analepta Arthopyrenia cerasi Arthopyrenia cinereopruinosa Arthopyrenia punctiformis Arthopyrenia salicis Bacidia absistens Bacidia arcuetina Bacidia beckhausii Bacidia caesiovirens Bacidia circumspecta Bacidia igniarii Bacidia neosquamulosa Bacidia rubella Bacidia subcircumspecta Bacidia subincompta Bacidia vermifera Biatora chrysantha Biatora efflorescens Biatora epixanthoides Biatoridium delitescens Bryoria fuscescens var. fuscescens Buellia disciformis Biatora erubescens Buellia griseovirens Buellia schaereri Calicium glaucellum Calicium salicinum Calicium viride Caloplaca ahtii Caloplaca asserigena

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Caloplaca cerina var. cerina Cerina cerinella Cerina cerinelloides Caloplaca ferruginea Caloplaca flavorubescens Caloplaca obscurella Caloplaca phlogina Caloplaca pyracea Caloplaca ulcerosa Candilariella reflexa Candilariella superdistans Candelariella xanthostigma Catillaria nigroclavata Catinaria atropurpurea Catinaria neuschildii Chaenotheca chrysocephala Chaenotheca furfuracea Chrysothrix candelaris Cladonia chlorophaea Cladonia coniocraea Cladonia fimbriata Cladonia furcata subsp. furcata Cladonia glauca Cladonia macilenta Cladonia ochrochlora Cladonia polydactyla var. polydactyla Cladonia pyxidata Cladonia ramulosa Cladonia squamosa var. squamosa Cliostomum griffithii Collema auriforme Collema fasciculare Collema furfuraceum Collema nigrescens Collema occultatum Collema subflaccidum Cyrtidula hippocastani Degelia atlantica Degelia plumbea Dimerella lutea Dimerella pineti Diplotomma pharcidium Evernia prunastri Fuscidea arboricola Fuscidea lightfootii Fuscidea recensa Fuscopannaria ignobilis Fuscopannaria leucophaea Fuscopannaria mediterranea Fuscopannaria sampaiana Gomphillus calcyioides Graphina anguina Graphis scripta

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Gyalecta derivata Halecania viridescens Hypocenomyce scalaris Hypogymnia physodes Hypogymnia tubulosa Hypotrachyna sinuosa Japewia subaurifera Lauderlindsaya acroglypta Lecania cyrtella Lecania cyrtellina Lecania dubitans Lecania naegelii Lecania sambucina Lecanora carpinea Lecanora chlarotera Lecanora confusa Lecanora conizaeoides Lecanora expallens Lecanora farinaria Lecanora horiza Lecanora intumescens Lecanora jamesii Lecanora persimilis Lecanora populicola Lecanora pulicaris Lecanora rugosella Lecanora salina Lecanora sambuci Lecanora symmicta Lecidea erythrophaea Lecidea hypopta Lecidea nylanderi Lecidea sanguineoeatra Lecidea turgidula Lecidella elaeochroma f. elaeochroma Lecidella elaeochroma f. soralifera Lecidella flavosorediata Lepraria eburnea Lepraria elobata Lepraria jackii Lepraria lobificans Lepraria rigidula Lepraria umbricola Leproloma membranaceum Leptogium cyanescens Leptogium lichenoides Leptogium saturninum Leptogium teretiusculum Leptorhaphis atomaria Lobaria amplissima Lobaria pulmonaria Lobaria scrobiculata Lobaria virens

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Lopadium disciforme Loxospora elatina Megalaria grossa Megalaria pulverea Megalospora tuberculosa Melanelia exasperata Melanelia exasperatula Melanelia fuliginosa subsp. glabratula Melanelia laciniatula Melanelia septentrionalis Melanelia subaurifera Menegazzia terebrata Micarea cinerea f. cinerea Micarea leprolusa Micarea lignaria var. lignarea Micarea micrococca Micarea nitschkeana Micarea peliocarpa Mycoblastus affinis Mycoblastus ceasius Mycoblastus fucatus Mycobastus sanguinaris f. sanguinaris Mycomicrothelia confusa Nephroma leavegatum Nephroma parile Normandina pulchella Ochrolechia androgyna Ochrolechia microstictoides Ochrolechia parella Ochrolechia subviridis Ochrolechia szatelaensis Ochrolechia tartarea Opegrapha atra Opegrapha herbarum Opegrapha multipuncta Opegrapha niveoatra Opegrapha ochrocheila Opegrapha rufescens Opegrapha sorediifera Opegrapha varia Opegrapha vulgata Pannaria conoplea Pannaria rubiginosa Parmotrema chinense Parmotrema crinita Parmelia saxatalis Parmelia sulcata Parmeliella parvula Parmeliella triptophylla Peltigera collina Peltigera horizontalis Pelitigera hymenina Peltigera membranacea

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Peltigera praetextata Peltigera rufescens Pertusaria albescens var. albescens Pertusaria albescens var. corallina Pertusaria amara f. amara Pertusaria coccodes Pertusaria corallina Pertusaria coronata Pertusaria flavida Pertusaria hemisphaerica Pertusaria hymenea Pertusaria leioplaca Pertusaria multipuncta Pertusaria ophthalmiza Pertusaria pertusa Pertusaria pupillaris Phaeocalicium populneum Phaeocalicium praecedens Phaeophyscia endophonecia Phaeophyscia orbicularis Phlyctis argena Physcia adscendens Physcia aipolia Physcia ceasia Physcia leptalea Physcia stellaris Physcia tenella Physconia distorta Physconia enteroxantha Physconia perisidiosa Platismatia glauca Porina aenea Protopannaria pezizoides Protoparmelia ochrococca Pseudevernia furfuracea s. lat. Pseudocyphellaria norvegica Pyrenula laevigata Pyrenula macrospora Pyrenula occidentalis Pyrrhospora quernea Ramalina farinacea Ramalina fastigiata Ramalina fraxinea Rinodina efflorescens Rinodina laevigata Rinodina oleae Rinodina sophodes Schaereria corticola Schismatomma graphidioides Sclerophora pallida Sclerophora peronella Scoliciosporum chlorococcum Scoliciosporum sarothamni

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Scoliciosporum umbrinum Sphaerophorus globosus Sticta canariensis (blue-green photosymbiodeme) Sticta fuliginosa Sticta limbata Sticta sylvatica Strangospora moriformis Strigula taylorii Tephromela atra var. atra Thelotrema lapadinum Thelotrema macrosporum Tomasellia gelatinosa Trapeliopsis flexuosa Trapeliopsis pseudogranulosa Tuckermanopsis chlorophylla Usnea cornuta Usnea filipendula Usnea flammea Usnea fragilescens var. mollis Usnea hirta Usnea subfloridana Usnea wasmuthii Xanthoria parietina Xanthoria polycarpa Tentative identifications: Diplotomma triseptata Phaeocalicium interruptum Ropalopsora viridis Specimens 'ad interim': Bacidia coralloidea cf. Biatora sp. Lecanora cf. 'caladonica' Melaspilea 'sp. D' Melaspilea 'sp. nov.'