Christopher J. Ellis

DNA barcoding of lichenized fungi demonstrates high identification success in a floristic context.

• Efforts are currently underway to establish a standard DNA barcode region for fungi; we tested the utility of the internal transcribed spacer (ITS) of nuclear ribosomal DNA for DNA barcoding in lichen-forming fungi by sampling diverse species across eight orders. • Amplification of the ITS region (ITS1-5.8S-ITS2) was conducted for 351 samples, encompassing 107, 55 and 28 species, genera and families, respectively, of lichenized fungi. We assessed the ability of the entire ITS vs the ITS2 alone to discriminate between species in a taxonomic dataset (members of the genus Usnea) and a floristic dataset. • In the floristic dataset, 96.3% of sequenced samples could be assigned to the correct species using ITS or ITS2; a barcode gap for ITS is present in 92.1% of species. Although fewer species have a barcode gap in the taxonomic dataset (73.3% with ITS and 68.8% with ITS2), up to 94.1% of samples were assigned to the correct species using BLAST. • While discrimination between the most closely related species will remain challenging, our results demonstrate the potential to identify a high percentage of specimens to the correct species, and the remainder to the correct genus, when using DNA barcoding in a floristic context.

Changing climate and historic-woodland structure interact to control species diversity of the ‘Lobarion’ epiphyte community in Scotland

Abstract Question: How will changing climate and habitat structure interact to control the species diversity of lichen epiphytes? Location: Scotland. Method: Species richness (=diversity) of the epiphyte lichen community known as Lobarion (named after Lobaria pulmonaria) was quantified for 94 Populus tremula stands across Scotland, and compared in a predictive model to seven climate variables and eight measures of woodland structure. An optimum model was selected and used to project Lobarion diversity over the geographic range of the study area, based on IPCC climate change scenarios and hypothetical shifts in woodland structure. Results: Species diversity of the Lobarion community was best explained by three climate variables: (1) average annual temperature; (2) autumn and winter precipitation; in combination with (3) historic-woodland extent. Projections indicate a positive effect of predicted climate change on Lobarion diversity, consistent with the physiological traits of cyanobacterial lichens comprising the Lobarion. However, the general response to climate is modified significantly by the effect on diversity of historic-woodland extent. Conclusions: Historic-woodland extent may exert an important control over local climate, as well as impacting upon the metapopulation dynamics of species in the Lobarion. In particular, a temporal delay in the response of Lobarion species to changed woodland structure is critical to our understanding of future climate change effects. Future Lobarion diversity (e.g. in the 2050s) may depend upon the interaction of contemporary climate (e.g. 2050s climate) and historic habitat structure (e.g. 1950s woodland extent). This is supported by previous observations for an extinction debt amongst lichen epiphytes, but suggests an extension of simple climate-response models is necessary, before their wider application to lichen epiphyte diversity.

Reproductive strategy and the compositional dynamics of crustose lichen communities on aspen ( Populus tremula L.) in Scotland

Ecological studies are essential in understanding the response of crustose lichens to habitat dynamics and developing effective conservation strategy. While the combined response of individual crustose species within a community will be tremendously complex, the overall result of individualistic change can be simplified using trait-based analyses. In this paper we examine the response of crustose species with contrasting reproductive traits (predominantly sexual vs asexual reproduction) and which occur within a closely defined habitat (as epiphytes on the lower bole of aspen) to environmental drivers measured at two different scales, i.e. between and within aspen stands. Our results point to the important effect of tree age and subsequent shifts in bark quality (pH) on the composition of the crustose community. However, shifts in community composition putatively controlled by bark quality comprise a change from a community dominated by sexual species to a community with mostly asexual crusts. Our results suggest therefore that variation within this crustose community may be driven by the combined effects of allogenic change (tree age and bark quality) and autogenic processes that are related to a species’ adaptive life-history traits.

Taxon-compared with trait-based analysis of epiphytes, and the role of tree species and tree age in community composition.

Background: Trait-based assembly rules are a powerful tool in community ecology, used to explore the pattern and process of community structure (richness and composition). Aims: A preliminary test for the utility of trait-based assembly rules in explaining cryptogamic epiphyte communities (lichens and bryophytes). Methods: We sampled epiphytes from three different tree species (aspen, birch and pine), and from trees of contrasting age. The community composition of epiphyte species (taxon analysis) and functional groups (trait analysis) was summarised using multivariate ordination (nonmetric multidimensional scaling, NMDS). Results: Ordination documented a widely observed pattern in which different tree species have taxonomically different epiphyte communities. However, NMDS sample scores were correlated to tree age in the trait-based analysis, but not in the taxon analysis. Conclusions: Our results point to the existence of a common pattern in community traits during succession (on trees of different age) when measured for epiphyte communities with contrasting taxonomic composition. This pattern is evidenced by consistent trends in lichen growth form and reproductive strategy (sexual vs. asexual).

Partitioning the role of climate, pollution and old-growth woodland in the composition and richness of lichen epiphytes in Scotland.

This paper presents a study to partition the role of three regional-scale drivers – woodland extent and continuity, pollution regime, and climatic setting – in explaining the composition and richness of lichen epiphytes in Scotland. To do this we used partial canonical correspondence analysis and multiple least squares regression, to examine lichen communities across 170 study sites. First, our results demonstrate the importance of climate in explaining species composition. This highlights the relatively clean-air environment of Scotland within a European setting, and emphasizes the important consideration of regional context in the development of bioclimatic species-response models. This result contrasts with a previous similar study which collapsed complex environmental data into summary gradients, and which therefore discounted climate as a key factor. Second, we show a functional decoupling between composition and species richness, which was optimally explained by old-growth woodland extent and pollution, and only weakly explained by climate. The difference in explanatory variables between composition and richness is a focal issue in determining the processes by which species compositional change, driven by rapid and deep climate change, may indirectly impact species richness. For example, this impact may occur through an imbalance in rates of species extinction (for sensitive range-edge species) and establishment in a fragmented landscape (for dispersal-limited colonists), though operating against the ‘stabilizing effect’ of microclimatic setting.

Paleoecological Evidence for Transitions between Contrasting Landforms in a Polygon-Patterned High Arctic Wetland

The formation of many arctic wetlands is associated with the occurrence of polygon-patterned permafrost. Existing scenarios to describe and explain surface landforms in arctic wetlands (low-center and high-center polygons and polygon ponds) invoke competing hypotheses: a cyclic succession (the thaw-lake hypothesis) or a linear succession (terrestrialization). Both hypotheses infer the predictable development of polygon-patterned wetlands over millennia. However, very few studies have applied paleoecological techniques to reconstruct long-term succession in tundra wetlands and thereby test the validity of existing hypotheses. This paper uses the paleoecological record of diatoms to investigate long-term development of individual polygons in a High Arctic wetland. Two landform processes were examined: (1) the millennial-scale development of a polygon-pond, and (2) the transition from low-center to erosive high-center polygons. Diatom assemblages were quantified from habitats associated with contrasting landforms in the present-day landscape, and used as an analog to reconstruct past transitions between polygon types. On the basis of this evidence, the paleoecological record does not support either of the existing models describing the predictable succession of polygon landforms in an arctic wetland. Our results indicate a need for greater paleoecological understanding, in combination with in situ observations in present-day geomorphology, in order to identify patterns of polygon wetland development and elucidate the long-term drivers of these landform transitions.

Local experimental growth rates respond to macroclimate for the lichen epiphyte Lobaria pulmonaria

Background: Bioclimatic models are widely applied in biogeography and conservation biology; however, the functional relevance of macroclimate as an explanation for species performance (e.g. establishment, growth and survival, fecundity) has been challenged. Aims: In this study, we aimed to determine whether the ecological performance of an epiphytic lichen is related to coarse-grained macroclimate. Methods: A meta-analysis was carried out to compare local growth rates for a lichen epiphyte, Lobaria pulmonaria, to coarse-grained interpolated climate surfaces. Growth rates were sampled from small-scale experiments conducted within different forest settings and for different regions of the world. Generalised linear mixed models were used to compare thallus growth (response) to a suite of climatic variables derived from the WorldClim dataset. Results: A significant relationship between thallus growth measured for experimental forest microhabitats and macroclimatic variables (total precipitation and annual mean temperature) was found. This relationship was validated through a comparison with L. pulmonarias North American range for which projected growth rates were higher and lower where the species tended to be present and absent, respectively. Conclusions: The ecological relevance of coarse-grained macroclimate applied in bioclimatic modelling has been challenged. We show that the use of macroclimatic data may be functionally defensible where correlated with independent measures of local ecological success.

Epiphyte sensitivity to a cross-scale interaction between habitat quality and macroclimate: an opportunity for range-edge conservation

Bioclimatic envelope models are frequently used to project the species response to climate change scenarios. Development and improvement of bioclimatic models has focussed on data properties and statistical tools, while significant criticism continues to challenge the ecological framework of model assumptions. We hypothesised that a potential for model improvement emerges from linkage across scales, between macroclimate and variation in local habitat quality: i.e. a species’ habitat specificity may shift along macroclimatic gradients. We first sampled two test-case epiphytic lichen species across a steep climatic gradient, and second developed standard bioclimatic models accompanied by a threshold likelihood value for discriminating presences and absences. We used the difference between predicted model values and the threshold as a response variable (Dthr): we show that values for Dthr are explained by an interaction between the climatic setting and habitat quality. A potential error in bioclimatic models is then quantified as the region of false absences or presences, which would be incurred as a consequence of sensitivity to variable habitat. This signature habitat effect occurs at a species’ range-edge, and, as a corollary, provides quantification in support of conservation: i.e. information is provided on how a habitat may be managed in marginal climatic regions (leading or trailing range-edge boundaries) in order to promote species protection.

Archaeobotanical evidence for a massive loss of epiphyte species richness during industrialization in southern England

This paper describes a novel archaeological resource—preserved epiphytes on the timber structure of vernacular buildings—used, to our knowledge, for the first time to quantify a loss of biodiversity between pre-industrial and post-industrial landscapes. By matching the confirmed occurrence of epiphyte species for the pre-industrial period, with a statistical likelihood for their absence in the present-day landscape (post-1960), we robustly identified species that have been extirpated across three contrasting regions in southern England. First, the scale of biodiversity loss observed—up to 80 per cent of epiphytes—severely challenges biodiversity targets and environmental baselines that have been developed using reference points in the post-industrial period. Second, we examined sensitivity in the present-day distribution of extirpated species, explained by three environmental drivers: (i) pollution regime, (ii) extent of ancient woodland, and (iii) climatic setting. Results point to an interacting effect between the pollution regime (sulphur dioxide) and changed woodland structure, leading to distinctive regional signatures in biodiversity loss.

Predicting the biodiversity response to climate change: challenges and advances

This Perspective examines progress, challenges and emerging directions in bioclimatic modelling. The field of bioclimatic modelling provides a toolkit which is widely used to examine the biodiversity response to climate, including future scenarios of climate change. Bioclimatic modelling has been the subject of intense research in statistical ecology; here I trace its development from a highly researched statistical foundation towards a framework that increasingly incorporates the ecological detail of a species’ climatic sensitivity. However, as models become more complex (with greater ecological realism) a choice emerges between two approaches: (i) greater model complexity and biological realism – especially where applied to specific conservation problems; and (ii) acceptance of simple bioclimatic tools as a useful albeit limited component, within a mixed evidence-base to assess climate change threat and conservation action. I conclude that whole-organism biologists working at museums and botanic gardens should claim an increasing stake in the bioclimatic framework, especially as the field develops towards an improved biology, towards the integration of new forms of evidence (evolutionary biology, long-term monitoring, expert knowledge, etc.), and in order to force the expansion from model systems (e.g. birds, butterflies, trees), to biodiversity more generally.