Nuanced qualitative trait approaches reveal environmental filtering and phylogenetic constraints on lichen communities

Abstract

We propose that a qualitative trait approach based on more detailed nuanced traits may reveal previously overlooked patterns, especially when combined with phylogenetic perspectives. By sampling epiphytic lichens and using a functional approach based on nuanced qualitative traits, such as a much greater resolution over photobiont identity, type of cortex, and chemical compounds, we evaluated the effects of environmental filtering and phylogenetic constraints on community assembly along a natural succession of Atlantic rainforest. We found changes in taxonomic, functional, and phylogenetic composition, structure, and diversity. Functional traits such as photobiont genera, type of cortex, reproductive structures, propagule size, and protection strategies showed strong responses to succession. Mature forests with a closed canopy impose strong environment filtering that is reflected in lichen species turnover, limiting diversity, but also holding different functional and phylogenetic composition. The use of a nuanced qualitative trait approach may overcome some of the limitations of using this type of traits and shows the importance of often‐overlooked key lichen functional traits, including the presence of carbon‐concentrating mechanisms in photobionts and cortex properties. Furthermore, this is the first study showing how patterns of phylogenetic assembly along forest succession structure lichen communities.

Evolutionary biology of lichen symbioses

“…A CCM is thought to be important in concentrating inorganic carbon in low‐CO 2 environments, and the switch to algae with a CCM could play a role in mitigating prolonged water saturation and inhibited CO 2 diffusion in lichen thalli. However, in aquatic algae the convergent loss of a CCM is associated with low‐light conditions (Raven, 2003) and indeed, the absence of a CCM in lineages such as Trentepohliales may explain their predominance in low‐light environments (Koch et al ., 2022).…”

Carbon‐concentrating mechanisms are a key trait in lichen ecology and distribution

“…This approach likely owes its success to the outsized effect of the pyrenoid‐containing genera Trebouxia and Asterochloris , especially among nontropical macrolichens, that has masked the physiological diversity of eukaryotic lichen photobionts. More recently, renewed attention has been given to the differences between Trentepohlia and chlorococcoid green algal lichen distributions (Käffer et al, 2021; Koch et al, 2022), and it is tempting to continue such an approach rather than using genus‐level photobiont identification. However this simple clade‐based distinction is still not mechanistic, overlooking the absence of CCMs in major chloroccoid genera such as Symbiochloris .…”

“…However, these broad categories mask considerable variation in physiology, in particular within the chlorococcoid green algae. Indeed, recent work has found that finer scale, genus‐level photobiont occurrence is associated with environmental changes during forest succession (Koch et al, 2022). These fine‐scale responses align with the presence or absence of CCMs.…”

Lichen ecophysiology in a changing climate

“…These anatomical adaptations are not, however, universal and have been convergently lost in multiple algal lineages, especially in terrestrial/subaerial environments (e.g., Trentepohlia , Symbiochloris ). Lichenized algae lacking CCMs are therefore more susceptible to carbon limitation by water saturation (Palmqvist et al, 1997) but potentially more tolerant of low light (Koch et al, 2022) and better able to utilize water vapor (Phinney et al, 2019), with consequences for distributions along environmental gradients (Koch et al, in press).…”

“…Water relations are driven not only by WHC, but also by rates of water acquisition and loss. Water‐holding capacity may be impacted by surface properties (Lakatos et al, 2006) and photobiont physiology (Phinney et al, 2019; Koch et al, 2022), while the latter may be quite responsive to thallus temperature and therefore albedo (color/albedo studies). It is also important to recognize that not all potential traits will be universally applicable.…”