Biocrust science and global change.

Abstract

Global environmental changes such as climate and land-use change affect ecosystems worldwide, and this New Phytologist Virtual Issue brings together fundamental research questions and novel approaches associated with the study of biological soil crusts in the context of such shifts. In a changing world, organisms can display a limited set of responses that will determine their persistence over varied spatial and temporal scales. Specifically, organisms might tolerate the change – for example, via phenotypic plasticity – and remain present in local communities. Alternatively, organisms might shift or retract their range to match their historical niche, they may adapt to the directional selection pressures imposed by change, or they could be driven to local (and possibly global) extinction. Efforts to understand which of these responses particular plant species or assemblages will exhibit are necessary for predicting changes in ecosystem functioning and trophic interactions under global change scenarios, and for managing and supporting sustainable terrestrial ecosystems. Accordingly, the assessment of plant responses to global change has become a significant research focus. Despite this impressive effort, our understanding and combined work to measure the responses to global change for species and communities of nonvascular autotrophs, such as the cyanobacteria, lichens, and bryophytes that form biological soil crusts (Fig. 1), remain rare compared with the large focus on vascular plants (Fig. 2; Reed et al., 2016). Nevertheless, these nonvascular photosynthetic communities and their responses to change could have critical implications for determining ecosystem structure and function at the global-scale (Elbert et al., 2012; Ferrenberg et al., 2017; Rodriguez-Caballero et al., 2018). Biological soil crusts (biocrusts) are a surface community of lichens, mosses, cyanobacteria, and other nonvascular photoautotrophs living on soils worldwide (Fig. 1; Belnap et al., 2003). Wherever soils have direct access to the sun, biocrusts have the potential to exist. Indeed, biocrusts occur on all continents and across contrasting biomes (e.g. polar, temperate, arid), and comprise a majority of cover in many arid and polar systems (Belnap et al., 2016; Torres-Cruz et al., 2018). A recent global estimate suggested that biocrusts cover c. 12% of the Earth's terrestrial surface (Rodriguez-Caballero et al., 2018), and these photosynthetic soil communities play foundational roles in the ecosystems where they occur (Belnap et al., 2016). For example, biocrusts fix significant amounts of carbon and nitrogen through photosynthesis and nitrogen fixation (Elbert et al., 2012; Barger et al., 2016; Sancho et al., 2016), are a deterministic force in stabilizing soils (Belnap & Büdel, 2016), alter the way water moves in these often water-limited environments (Chamizo et al., 2016), affect plant growth and soil fertility (Ferrenberg et al., 2018), and provide habitat for belowground communities (e.g. bacteria, fungi, protists, and invertebrates). As with many scientific fields, research on biological soil crusts continues to evolve and is increasingly focused on understanding how the structure and function of biocrusts, as well as their associated microbial communities, respond to global change (Darrouzet-Nardi et al., 2015; Reed et al., 2016; Ladrón de Guevara et al., 2018). At the same time, the emergence of new methods provides unprecedented opportunities to quantitatively evaluate and predict the changes in biocrust community composition and function under changing environments, and thus, to establish the role of these communities in the functioning of the ecosystems that they occupy. Such tools include coupled automated CO2 and soil microclimate assessments (Tucker et al., 2017), genetic approaches to biocrust taxonomy (Muñoz-Martín et al., 2019), ‘omic’ technologies (e.g. metagenomics, proteomics and metabolomics; Bates et al., 2011; Delgado-Baquerizo et al., 2016; Swenson et al., 2018), trait-based frameworks for prediction and evaluation (Mallen-Cooper & Eldridge, 2016; Deane-Coe & Stanton, 2017; Ferrenberg & Reed, 2017), and new remote sensing platforms that could allow for larger-scale community monitoring (Young & Reed, 2017; Rodriguez-Caballero et al., 2018). In particular, these tools have expansive potential to facilitate the improvement of biocrust conceptual and numerical models to gauge and forecast modifications to ecosystem structure and function in response to global change. While numerous data show that climate plays a strong role in determining the cover, composition, and distribution of biocrust communities (Reed et al., 2012; Bowker et al., 2016), our understanding of how these organisms, and their associated microbial communities, will respond to anthropogenic change such as climate change remains poor. Nevertheless, the information we do have suggests the potential for biocrusts to change quickly, with community changes on the same order as those observed with physical disturbance, such as foot and vehicle trampling (Reed et al., 2012, 2016; Ferrenberg et al., 2015). For example, in this Virtual Issue, Ladrón de Guevara et al. (2018) used an eight-year warming experiment in Spain to show that increased temperatures reduced biocrust cover by 85% and diversity by 25% in plots that originally had high biocrust abundance. A warming experiment in the southwestern United States also showed dramatic declines in key biocrust populations in the face of elevated temperatures, with a c. 80% decline in moss cover and a c. 50% decline in lichen cover with a 4°C temperature increase (Ferrenberg et al., 2015). Experimental changes to the timing of precipitation have shown even more immediate effects on biocrust communities (Reed et al., 2012; Ferrenberg et al., 2015), which underscores the need for an improved understanding of the effects of increasing temperature and altered precipitation, as well as their interactions. One of the key reasons changes in biocrust communities are of interest is the myriad processes biocrusts help regulate in dryland communities (Belnap et al., 2016). Biocrusts are sometimes described as ‘mantles of fertility’ (Garcia-Pichel et al., 2003; Nejidat et al., 2016), regulating the inputs and outputs of gases, nutrients, and water from desert surfaces (Pointing & Belnap, 2012). The composition of the biocrust community matters to the rates of these biocrust-controlled processes (Housman et al., 2006; Barger et al., 2013), and also to their resilience and response to climatic change (Delgado-Baquerizo et al., 2018; Tucker et al., 2019). Understanding changes in ecosystem-scale community composition in response to environmental change includes the relationship between biocrust organisms and other soil microbes living in drylands. For example, in this Virtual Issue, Delgado-Baquerizo et al. (2018), used a cross-continental (North America, Europe, and Australia) survey to evaluate how biocrust mosses regulate the relationship between aridity and the community composition and diversity of soil bacteria and fungi. These results suggest that increasing aridity is a strong control over microbial composition in the absence of moss; however, when moss is present, the relationship between aridity and the microbial communities was nonexistent. In other words, the data suggest biocrust-forming mosses mitigate the impact of aridity on the community composition of globally distributed microbial taxa. Although biocrust mosses and lichens typically support higher rates of processes such as carbon and nitrogen fixation (Housman et al., 2006; Barger et al., 2013; Tucker et al., 2019), cyanobacteria, while maintaining lower rates, are also a key biotic component of biocrust communities, maintaining fundamental ecosystem processes. Filamentous cyanobacteria, such as those in the genus Microcoleus, are often the major photosynthetic soil colonizers following disturbance or during primary succession. This is due to the cyanobacteria's motility and ability to stabilize soil particles through contact with their extracellular sheaths (Garcia-Pichel & Wojciechowski, 2009). Cyanobacteria play key roles in ecosystem function, yet significant knowledge gaps remain regarding biocrust cyanobacterial diversity and distribution in drylands. This Virtual Issue includes an article by Muñoz-Martín et al. (2019) that addresses this knowledge gap, using next-generation sequencing and bioinformatics analyses to describe cyanobacterial diversity in Mediterranean biocrusts along an aridity gradient. Results suggest the presence of climatic niches for distinct cyanobacteria, and, within the context of climate change, imply that a warmer world could result in a replacement of cool-adapted by warm-adapted cyanobacteria: a switch from the present dominance of Microcoleus vaginatus to more thermotolerant, novel phylotypes of cyanobacteria. Interestingly, differential sensitivities of cyanobacteria to rising temperature and decreasing precipitation point to the potential utility of cyanobacteria as bioindicators of global change (Muñoz-Martín et al., 2019). Cyanobacteria are an interesting focus not only because of their ubiquity, importance in ecosystem function, and potential responsiveness to global change, but also because of their role in one of the most transformative events in the Earth's history: the transition of photosynthetic life from aquatic environments to land. This change both altered the evolutionary history of the newly terrestrial organisms and reshaped the global environment. In this Virtual Issue, Plackett & Coates (2016) describe expert conversation on the colonization of land to reflect on how far the field has come, as well as explore core questions that remain unanswered. The article describes the phases of colonization and the organisms responsible, providing a valuable timeline. This evolutionary perspective also offers an exciting framework for biocrust science in the context of global change, as it helps contextualize the environmental changes already experienced by these organisms and the community and evolutionary responses they made in the past. There is also a rich and diverse heterotrophic community associated with biocrusts, and future work continuing to identify and characterize the functional and taxonomic attributes of the most common microbes (e.g. bacteria, fungi, protists) and soil fauna thriving in biocrust environments would be of great value. Additionally, quantifying the balance of deterministic and stochastic processes in governing the assembly of biocrust communities would greatly advance our ability to predict how specific global change pressures could alter biocrust community structure and to guide restoration efforts through improved knowledge of when and where dispersal vs establishment factors limit biocrust formation. Looking back and looking forward, an improved understanding of the relationship between biocrust communities and climate builds the foundation for improved forecasting of changes in ecosystem structure and function in drylands, and elsewhere (Ferrenberg et al., 2017; Rodriguez-Caballero et al., 2018) and provides tools for biocrust restoration aimed at long-term success (Young et al., 2016, in this Virtual Issue). Such scientific interest in improving our understanding of biocrusts in the context of global change to advance prediction, scaling, and restoration and management options are at the forefront of contemporary biological soil crust science. The science of biocrusts is sustaining increased focus on scaling, modeling, improved quantification of in situ processes, and restoration (Bowker, 2007; Elbert et al., 2012; Doherty et al., 2015; Young et al., 2016; Ferrenberg et al., 2017; Darrouzet-Nardi et al., 2018; Rodriguez-Caballero et al., 2018; Tucker et al., 2019). In general, biocrust science and its communication has increased, for example, the number of articles focused on biocrusts continues to climb (Fig. 2). So too has interest in using a range of emerging methods, including remote sensing, process monitoring with high temporal resolution, and novel restoration techniques. Biocrusts have been suggested as a model system in community, landscape, and ecosystem ecology (Bowker et al., 2014), and could be used as such to find and evaluate changes in ecosystem structure and function under global change scenarios. For some, the new foci stem from a desire to more robustly contextualize biocrusts within the larger framework of ecosystem function and to more quantitatively compare their role to that of other organisms. For example, emerging global carbon cycling data suggest drylands may dominate the size and interannual variability in the terrestrial carbon sink (Poulter et al., 2014; Ahlström et al., 2015). But what role do biocrusts play in these patterns? How do ecosystem-scale rates of biocrust soil CO2 uptake and release compare with those from the same system's vascular plant community? An improved, scalable understanding of biocrusts’ contribution to fundamental ecosystem function would be of immense value. In this Virtual Issue and elsewhere, multiple research groups have suggested the utility of trait-based approaches to understanding biocrusts and their function (Bowker et al., 2011; Mallen-Cooper & Eldridge, 2016, 2019; Deane-Coe & Stanton, 2017; Ferrenberg & Reed, 2017). Grouping and evaluating biocrust individuals, populations, and communities using morphological, ecophysiological, phylogenetic, and functional traits provides new avenues for considering how biocrusts work and how they respond to change. For example, functional trait diversity and composition have been used to predict changes in ecosystem structure and function in response to aridity and grazing by livestock (Mallen-Cooper et al., 2018) – two key components related to desertification globally – and as potential indicators of global change (Concostrina-Zubiri et al., 2016). As with vascular plants, trait-based approaches offer a compelling way forward for biocrust science to advance our knowledge of the role of functional traits in regulating the rates and the responses of biocrust communities and ecosystem functions to global change. We stand on the threshold of a new era of biocrust studies aiming to better quantify, contextualize, and forecast the structure and function of biocrust communities globally. This includes biocrusts’ associated microbial and faunal communities, responses to change, and the use of a more holistic understanding in restoration efforts. This Virtual Issue captures a wide range of perspectives on the state of biocrust science in the context of global change, and we hope readers will enjoy the depth and complementarity of the articles. We note that the articles included in this Virtual Issue are, of course, an incomplete representation of the numerous topics being explored by the research community studying biological soil crusts. For example, there are many additional articles stemming from the Biocrust3 Conference (Ferrenberg & Reed, 2017), including articles in other journal collections (Bowker et al., 2018). A desire to synthesize our contemporary understanding of biocrusts comes through in each of these efforts, and the articles collected here offer a sample of the exciting science occurring within an emerging climate change research theme. This work is part of the growing scientific foundation upon which the next generation of biocrust researchers will continue to build, including the Biocrust4 Conference (Australia, August, 2019) where new ideas will be shared, evaluated, and synthesized. Many of the articles in this Virtual Issue stem from the Third International Workshop on Biological Soil Crusts (Biocrust3) and, in particular, from a global change session at Biocrust3 that was supported by the New Phytologist Trust. The authors are grateful to Kristina Young and an anonymous reviewer for suggestions that improved a previous version of this manuscript. This article was also supported by the US Department of Energy Office of Science (DE-SC-0008168), the Strategic Environmental Research and Develoment Program (RC18-1322), and by the US Geological Survey Ecosystems Mission Area. MD-B acknowledges support from the Marie Sklodowska-Curie Actions of the Horizon 2020 Framework Program H2020-MSCA-IF-2016 under REA grant agreement no. 702057. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the US Government.