Climatic disequilibrium modulates canopy service across abiotic stress gradients

Abstract

1 INTRODUCTION

Climate change is shifting plant distributions, with some species expanding in newly favourable areas and others declining in increasingly hostile habitats (Kelly & Goulden, 2008). This rapid change has a great scientific and societal relevance and has prompted researchers to devote a great effort to predict the consequences of climate change through species distribution models (Elith & Leathwick, 2009). Early influential studies of species distributions made predictions mainly based on abiotic factors—typically temperature—but it soon became evident that there was a need to include concurrent biotic interactions to increase predictions' accuracy (Austin & Van Niel, 2011; Wisz et al., 2013).

A relevant ecological process that needs to be addressed to correctly predict plant community assembly and dynamics under a changing environment is that occurring between the already established plants (referred as canopy species in this context) and the plants recruiting in their neighbourhood defined as recruit species, which will eventually replace that canopy species (Alcántara et al., 2018; Valiente-Banuet & Verdú, 2013). The extent to which canopy species positively or negatively enhance the recruit species abundance can be named as canopy service (Alcántara et al., 2024; Perea et al., 2021). In some cases, canopy service is positive (i.e. there is a positive interaction); in such cases, we refer to facilitation, where the canopy plants act as nurse species to other recruit species in the communities enhancing their survival beneath them. One mechanism explaining this positive interaction is that canopy species typically buffer the stressful macroclimatic conditions beneath them, enabling the recruit species to remain in the community even beyond their optimal climatic conditions (O'Brien et al., 2019; Perea et al., 2021). This climatic buffering provided to recruiting plants has been shown to be ambivalent, cooling the understory during hot ambient temperatures and warming it when ambient temperatures are cold (De Frenne et al., 2021). However, in other cases, canopy service can be negative in relative terms, as the conditions beneath the canopy may depress recruitment compared to open ground areas (i.e. negative interaction). Factors such as species traits, competition, herbivory and other biotic and abiotic agents play a role in how canopy service varies across communities and species.

In general, canopy plants tend to shift from depressing to enhancing the recruitment of other species as environmental stress levels increase (He et al., 2013; Stress Gradient Hypothesis, SGH; Bertness & Callaway, 1994) That is, canopy service would tend to become more positive as environmental stress intensifies. Indeed, several studies have shown that facilitation is more prevalent in stressed environments, like arid and alpine habitat systems (Armas et al., 2011; Callaway et al., 2002; Cavieres et al., 2006). However, in extreme situations, facilitation can collapse because canopy species are unable to sufficiently improve microclimatic conditions, resulting in a non-linear (i.e. humped-back shape) relationship between stress and facilitation (Michalet et al., 2006). This pattern may also reflect the competition—facilitation trade-off across stress gradients as well (Michalet et al., 2014); however, the overall pattern of facilitation across contrasting environmental stresses has not yet been clearly elucidated.

The improvement of microhabitat conditions offered by canopy plants has been a crucial factor in mitigating the impacts of climatic aridification in the past, helping to prevent the extinction of stress-sensitive species (Valiente-Banuet & Verdú, 2013). This mechanism is likely in operation in plant communities, so it must be considered when predicting the future occurrence of species in the face of current climate change (Bulleri et al., 2016). In fact, current species distribution models predict that threatened species may persist in future stressful climates thanks to the microclimatic buffering effect of dominant plant canopies (Stark & Fridley, 2022). However, the extent to which canopy plants can mitigate the impacts of climate change may depend on their own tolerance to new conditions, which is quantified as the difference between their niche's climatic optimum and the actual local conditions (the so-called climatic disequilibrium [CD]; Blonder et al., 2015; Svenning & Sandel, 2013). In recent years, there has been an accumulation of evidence that plants experiencing greater CD require more facilitation from canopy plants (Díaz-Borrego et al., 2024; Perez-Navarro et al., 2024). However, the other side of this relationship, that is, how the CD of canopy species determines their interactions with recruiting plants, remains largely unexplored.

At present, we have evidence that populations and communities under high climatic disequilibrium are physiologically limited, show poorer plant performance and higher canopy defoliation rates, especially under extreme climatic events (Perez-Navarro et al., 2022; Sapes et al., 2017). In Mediterranean ecosystems, populations in warmer and drier environments tend to have higher disequilibrium (Perez-Navarro et al., 2024). Under these conditions, climatic disequilibrium, combined with susceptibility to aridity, likely contributes to poor plant performance. In contrast, canopy plants in populations close to the species' optimal conditions may achieve greater biomass production or growth (Margalef-Marrase et al., 2023), as well as more aerial biomass and leaf area (Treurnicht et al., 2020). Therefore, it is expected that plants in climatic equilibrium will be more vigorous and more prone to develop complex canopies that would enhance climatic buffering (De Frenne et al., 2021), ultimately increasing the canopy service to the recruitment communities. However, some studies have found that populations with CD located in less arid environments (closer to the wetter edge of the niche) may also develop greater aerial biomass than populations with less CD (Stanik et al., 2020). This suggests that the direction of disequilibrium across the climatic gradient (i.e. wetter vs. drier edge) may also influence the extent of canopy services provided by canopy plants. Overall, this rationale indicates that the relationship between canopy service and CD may be non-linear. This is partly due to the effect of the population's relative position within its species' niche (i.e. along cold-warm and arid-humid gradients) on plant competition, multitrophic interactions and fitness (O'Brien et al., 2017). As previously mentioned, canopy plants with less CD can promote the development of more complex canopies and enhance canopy service, but it may also amplify competition among species (Christiansen et al., 2024). This dual effect suggests a trade-off, where the expected improvement in canopy service due to low CD is counterbalanced by increased competition.

In light of these observations, we hypothesize that canopy species experiencing greater CD will exhibit diminished canopy services, leading to lower recruitment beneath their canopies. We also hypothesize that this relationship is non-linear. Furthermore, we propose that canopy species experiencing drier and hotter conditions than their optimum will provide reduced canopy services compared to both species close to their climatic equilibrium and those near the wetter, low thermal stress edge of their niche.

We anticipate that the reduction in the canopy service will be more pronounced under increasing stress conditions, where facilitation is expected to be more crucial for the recruits persistence. We test these hypotheses along a broad biogeographical and climatic gradient characterized by varying levels of aridity and continentality (latitudinally from North Africa to Central Europe and longitudinally from the Iberian Peninsula to Anatolia) after assessing the CD of more than 300 canopy species and the service they provide to recruiting species.