Climate warming causes photobiont degradation and carbon starvation in a boreal climate sentinel lichen

Abstract

Premise The long‐term potential for acclimation by lichens to changing climates is poorly known, despite their prominent roles in forested ecosystems. Although often considered “extremophiles,” lichens may not readily acclimate to novel climates well beyond historical norms. In a previous study (Smith et al., 2018), Evernia mesomorpha transplants in a whole‐ecosystem climate change experiment showed drastic mass loss after 1 yr of warming and drying; however, the causes of this mass loss were not addressed. Methods We examined the causes of this warming‐induced mass loss by measuring physiological, functional, and reproductive attributes of lichen transplants. Results Severe loss of mass and physiological function occurred above +2°C of experimental warming. Loss of algal symbionts (“bleaching”) and turnover in algal community compositions increased with temperature and were the clearest impacts of experimental warming. Enhanced CO2 had no significant physiological or symbiont composition effects. The functional loss of algal photobionts led to significant loss of mass and specific thallus mass (STM), which in turn reduced water‐holding capacity (WHC). Although algal genotypes remained detectable in thalli exposed to higher stress, within‐thallus photobiont communities shifted in composition toward greater diversity. Conclusions The strong negative impacts of warming and/or lower humidity on Evernia mesomorpha were driven by a loss of photobiont activity. Analogous to the effects of climate change on corals, the balance of symbiont carbon metabolism in lichens is central to their resilience to changing conditions.

Growth-dependent acclimation constrains climatic response for the lichen epiphyte Lobaria pulmonaria

“…On this basis, measures of thallus growth (as dry mass gain or loss) remain a useful functional metric for climate change response (see e.g. Ellis et al 2017;Smith et al 2018;Ellis 2019;Meyer et al 2023) since they incorporate the ability to acclimate to environmental change. If climate change crosses a threshold beyond which growth is no longer possible, then phenotypic acclimation would no longer be effective for L. pulmonaria, and the species would be considered at risk.…”

“…Ellis et al . 2017; Smith et al 2018; Ellis 2019; Meyer et al 2023) since they incorporate the ability to acclimate to environmental change. If climate change crosses a threshold beyond which growth is no longer possible, then phenotypic acclimation would no longer be effective for L .…”

Lichen ecophysiology in a changing climate

“…The effects of increasing ambient CO 2 on lichens has been shown to be variable, with some species increasing photosynthetic rates and growth, whilst in others there is little or no fertilization effect (Lange and Green, 2008; Smith et al, 2018; Meyer et al, 2023). Baldauf et al (2021) suggest that CO 2 fertilization in Diploschistes diacapsis is able to mitigate the negative effects of reduced moisture associated with climate change.…”

“…However, these observational studies cannot distinguish between within‐thallus turnover and changing associations across generations, and little is known about the rates of individual algal cell turnover within thalli. A transplant experiment was unable to induce photobiont turnover in the soil crust lichen Psora decipiens (Williams et al, 2017), although a recent climate change experiment suggests temperature‐induced photobiont genotype changes in the boreal epiphyte Evernia mesomorpha (Meyer et al, 2023). Novel techniques are needed to adequately document photobiont (and possibly mycobiont) cell and genotype turnover.…”

“…In cold environments such as Antarctica, species responses to increased temperature are mixed, with some species sensitive and others seemingly unaffected or enhanced (Bokhorst et al, 2016), although growth rates may be positively associated with temperature (Sancho et al, 2017(Sancho et al, , 2019. In temperate and mediterranean environments warming has more often been found to have negative effects, such as reducing species numbers (Aptroot and van Herk, 2007), cover (Escolar et al, 2012) and growth (Smith et al, 2018), often attributed to degradation of photosynthetic capacity (Pisani et al, 2007) and photobiont loss (Meyer et al, 2023).…”