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Altering biocrusts for an altered climate

2016; Wiley; Volume: 210; Issue: 1 Linguagem: Inglês

10.1111/nph.13910

1469-8137

Kristina E. Young, Henry S. Grover, Matthew A. Bowker,

Mycorrhizal Fungi and Plant Interactions

Covering over 40% of the terrestrial Earth surface, drylands – which include arid, semi-arid, and dry subhumid areas where precipitation is scarce and highly variable (Reynolds et al., 2013) – represent our planet's largest terrestrial biome (Schimel, 2010), inhabited by ~38% of the world's population (Millennium Ecosystem Assessment, 2005), and maintaining large stocks of carbon (Lal, 2004). The extent of drylands is expected to expand by > 10% during the next century (Huang et al., 2016). Emerging research suggests that drylands play a larger role in driving global carbon inter-annual variability than previously perceived (Poulter et al., 2014; Ahlström et al., 2015). Simultaneously, it is becoming clear that warming will significantly affect dryland ecosystem functioning (Maestre et al., 2012). Accordingly, the global coverage and significance of drylands, and their expected response to climate change factors, may alter the biogeochemical cycling of the Earth system. Nevertheless, there remain significant unknowns regarding dryland function in the context of future change, including our incomplete understanding of how biological soil crusts (biocrusts) will respond to global climate change. Biocrusts – communities of mosses, lichens, cyanobacteria, and heterotrophs living at the soil surface – are a foundational ecosystem component in drylands world-wide (Belnap et al., 2003; Fig. 1). Biocrusts are ecosystem engineers (Jones et al., 1997), which aggregate and stabilize the soil surface, and regulate critical ecosystem functions such as carbon and nitrogen fixation and surface hydrological cycles (Belnap et al., 2003). The influence of biocrusts on dryland ecosystem functioning is disproportionate to their small size. For example, they exert a dominant influence on soil respiration (Castillo-Monroy et al., 2011) and nitrogen cycling in some dryland ecosystems (Evans & Ehleringer, 1993; Castillo-Monroy et al., 2010), and may be the most important agent of soil stability against erosion (Bowker et al., 2008; Chaudhary et al., 2009). Further, the presence of intact biocrusts can buffer dryland ecosystem function against negative impacts due to climate change (Delgado-Baquerizo et al., 2016). Biocrusts are increasingly recognized as dynamic communities, able to respond to their environment much faster than was previously realized (Bowker et al., 2002; Belnap et al., 2006). Yet the traits that allow biocrusts to quickly respond to variable conditions also increase the possibility for a rapid negative response to climatic change. Indeed, experimental manipulation of climate has resulted in rapid mortality of dominant biocrust species (Reed et al., 2012; Maestre et al., 2013). However, this dynamic nature may also promote success in the use of artificial culture of biocrusts for rehabilitation of drylands to potentially ease some of the impacts of climate change. The organized special session on biocrusts at the Biennial Conference of Science and Management on the Colorado Plateau and Southwest Region on 7 October 2015 brought together 16 researchers working on community interactions of biocrusts, including exploration of the rehabilitation of biocrusts and the future of biocrusts under threats from physical disturbances and an altered climate. Here, we synthesize the findings and highlight the theme that emerged – the potential power of assisting biocrust migration to enhance dryland resilience to global change. Using molecular, isotopic, exometabolomic, and experimental ecological techniques, several speakers highlighted new work on the ways in which biocrust community members affect one another, and the ways in which biocrusts as a community interact with fungal and vascular plant communities (Trent Northen, Lawrence Berkeley National Laboratory (Berkeley, CA, USA); Estelle Couradeau, Arizona State University (Tempe, AZ, USA); Eva Detweiller-Robinson, University of New Mexico (Albuquerque, NM, USA); Cheryl McIntyre, University of Arizona (Tucson, AZ, USA); Carrie Havrilla, University of Colorado (Boulder, CO, USA)). These presentations highlighted biocrust organisms as major nodes in dryland interaction networks. For example, Estelle Couradeau presented work on the consequences of increasing soil temperatures, induced by the colonization of dark-pigmented biocrust species that alter surface albedo and energy balance, which may cause a shift in the dominant cyanobacterial species (Couradeau et al., 2016). This confirms on a local scale what has been observed on a regional scale, that changing temperatures shift the dominance of biocrust cyanobacteria, with unknown ecosystem consequences (Garcia-Pichel et al., 2013). Complex soil interactions were further highlighted by Trent Northen, who examined the relationship between the large number of metabolites excreted by the dominant cyanobacterial species, Microcoleus vaginatus, and the associated microbial community. He highlighted the large number of M. vaginatus exudates that are consumed by a range of microbial species specializing on particular compounds. These soil microbes exude compounds of their own, which are in turn consumed by M. vaginatus. This specialization implies niche partitioning and may be a mechanism for maintaining soil diversity, further implicating the widespread genus Microcoleus as a keystone species in the structure and functioning of dryland soil communities (Baran et al., 2015). The consequence of these interactions is that any perturbation affecting this foundational member of the biocrust community – such as the previously mentioned warming-induced dominance shifts (Couradeau et al., 2016) – is likely to create feedbacks of indirect effects for the community as a whole. In a step toward linking biocrusts, plants, and belowground communities, Eva Detweiller-Robinson explained her preliminary work assessing how nutrients made available by biocrusts (e.g. via nitrogen fixation) might be shared within the soil matrix between biocrust and plant communities. Cheryl McIntyre and Carrie Havrilla delved into the interactions between the physical structure of vascular plant seeds, invasive plant species, and biocrust communities to better elucidate how biocrusts regulate plant species composition by working both as a barrier to seed germination for certain species, and as a facilitator to others. Taken together, the presentations on the interaction networks within biocrusts, and between biocrusts and the greater ecosystem, illustrated the importance of biocrust in regulating ecosystem processes, and punctuated how change experienced by these community members may result in unforeseen change in ecosystem functioning. Because of biocrusts' foundational role within drylands, it is essential to understand how they will react to a changing climate (Reed et al., 2012; Maestre et al., 2013; Ferrenberg et al., 2015). As explained by Sasha Reed (US Geological Survey, Southwest Biological Science Center (Flagstaff, AZ, USA)), it appears that on the Colorado Plateau in the south-western United States, experimental warming and increased frequency monsoonal watering regimes result in major biocrust mortality. Because of the substantial warming expected in the these regions (Schwinning et al., 2008), biocrust mortality could have significant positive and negative feedbacks on global energy balance, as biocrust community shifts could alter albedo. Taking a step further, Scott Ferrenberg (US Geological Survey, Southwest Biological Science Center) compared the impacts of climate change and physical disturbance on biocrusts, finding both mechanisms resulted in a similar decline in biomass, and in community shifts toward early successional species (Ferrenberg et al., 2015). As physical disturbance has already resulted in significant loss of biocrust cover, further mortality induced by climate change will likely have large impacts on dryland albedo, nutrient cycling, soil stability, and biogeochemical cycles. Combined, these talks represent our contemporary understanding of how climate change will impact biocrusts. In light of these potential changes to biocrust survivorship in the American Southwest, and our knowledge of the likely cascading effects on other dryland community members, it becomes clear that there is a need to mitigate changes to biocrust survivorship. An exciting new frontier in biocrust biology is the ability to rapidly cultivate these species ex situ. Sergio Velasco Ayuso (Arizona State University) and Ana Silva Giraldo (Arizona State University) recounted their recent successes in cultivating biocrust cyanobacteria. Ana Silva Giraldo outlined a technique for isolating dominant cyanobacterial species and rapidly amassing them in liquid culture. This success highlighted the potential for large scale, cost effective cyanobacterial production to be used in dryland restoration efforts. Sergio Velasco Ayuso successfully cultivated complete, site-specific cyanobacterial communities for hot and cold deserts using a variety of soil amendments, light intensities, and watering regimes. Both Ana Silva Giraldo and Sergio Velasco Ayuso used genetic sampling (bacterial 16S rRNA approaches) to test the community composition changes during their effort and found no loss of species diversity and only minimal changes in relative abundances. Because cyanobacterial species are the first step in secondary succession of biocrusts, their successful cultivation represents a significant advance for dryland restoration efforts. Marked success was also observed in growing fully intact biocrust communities. Matthew Bowker (Northern Arizona University (Flagstaff, AZ, USA)) explained results from work growing lichen and moss species originating from cold deserts. Within a glasshouse setting, the most rapid growth occurred in the lichen genus Collema, a dominant nitrogen fixer and mid-successional member within biocrust communities. Most intriguingly, Matthew Bowker found that this lichen's growth facilitated the growth of biocrust mosses. This suggests that an improved understanding of species interactions may be a key to quickly and effectively growing full biocrust communities. While still in its infancy, early work suggests the potential for successful biocrust restoration in field settings, carrying with it exciting potential for biocrust rehabilitation in degraded dryland ecosystems. Many researchers outlined attempts to inoculate and grow biocrust in hot and cold drylands of the American Southwest (Anita Antoninka, Northern Arizona University; Akasha Faist, University of Colorado Boulder (CO, USA); Kristina Young, Northern Arizona University; Chris Ives, Northern Arizona University; Nichole Barger, University of Colorado Boulder). Work begun by Anita Antoninka and continued by Akasha Faist indicated that cyanobacteria distributed in a cold desert system were able to grow and survive in the field. However, efforts in hot desert and monsoonal systems have had less success; more work is needed to understand how to re-establish biocrust in these extreme environments. Importantly, the early stage of this work represents an opportunity to incorporate our understanding of likely climate change impacts on biocrust into cultivation and restoration efforts. While examining the vulnerability of biocrusts to climate change and the negative implications for rehabilitation success, a synthetic theme of the meeting emerged: the potential for engineering biocrust communities for resilience to climate fluctuations. One possible approach is assisted migration, or the directed movement and introduction of biocrust organisms that are already more adapted than local organisms to anticipated future climate conditions of a region. However, this possibility raises an important question: Can and should we merge our ecosystem rehabilitation efforts with assisted migration of biocrusts? If we do not, climate change may erase our best efforts at rehabilitation. Some efforts to enhance vascular plant migration and adaptation are already underway (Vitt et al., 2010), however, migration of biocrust species and genotypes may be an equally essential measure to ensure dryland function in the future, given their large ecosystem roles. Indeed, biocrusts may be ideal organisms for assisted migration. Easily transferable, biocrust communities can be manipulated along elevation and latitudinal gradients, as well as in glasshouses. Experimental manipulation over gradients of intact and inoculated biocrust communities could tell us about their resilience to environmental changes, as well as their ability to colonize novel ecosystems (Fig. 2). Importantly, biocrust autotrophs appear to be characterized by low global species diversity, and some taxa are common around the world (Bowker et al., 2016). Within those limited species numbers, however, is an unknown amount of genetic and phenotypic variation (Darby et al., 2006) to the many divergent dryland climates (Safriel et al., 2005). This variation could be experimentally explored to determine the response to environmental stress within geographically separated populations of biocrust communities. Migrating biocrusts will not only maintain the ecosystem services of soil stability and nutrient cycling, but the bacteria, fungi, and other soil organisms that interact directly with plants would also be moved within the biocrust–soil matrix. This could directly enhance natural and assisted plant migration, as soil organisms are increasingly recognized as essential for robust plant growth under historical and altered environmental conditions (Van Der Heijden et al., 1998; Lau & Lennon, 2012). In light of the global importance of drylands, it is of paramount importance to establish resiliency in these systems. Ensuring the continued presence of biocrusts in these changing dryland ecosystems may help maintain a high degree of functionality in drylands that might otherwise be lost (Delgado-Baquerizo et al., 2016). Many thanks go to the wonderful speakers of the biocrust special session and to the session and conference organizers and sponsors. Special thanks to Sasha Reed and Scott Ferrenberg for their constructive reviews, and to Kyle Doherty for his help with figures.