Plant Soil DOI 10.1007/s11104-017-3300-3 REGULAR ARTICLE Maximizing establishment and survivorship of field-collected and greenhouse-cultivated biocrusts in a semi-cold desert Anita Antoninka & Matthew A. Bowker & Peter Chuckran & Nichole N. Barger & Sasha Reed & Jayne Belnap Received: 31 March 2017 /Accepted: 25 May 2017 # Springer International Publishing Switzerland 2017 Abstract methods to reestablish biocrusts in damaged drylands Aims Biological soil crusts (biocrusts) are soil-surface are needed. Here we test the reintroduction of field- communities in drylands, dominated by cyanobacteria, collected vs. greenhouse-cultured biocrusts for mosses, and lichens. They provide key ecosystem func- rehabilitation. tions by increasing soil stability and influencing soil Methods We collected biocrusts for 1) direct reapplica- hydrologic, nutrient, and carbon cycles. Because of this, tion, and 2) artificial cultivation under varying hydration regimes. We added field-collected and cultivated biocrusts (with and without hardening treatments) to Responsible Editor: Jayne Belnap. bare field plots and monitored establishment. Electronic supplementary material The online version of this Results Both field-collected and cultivated article (doi:10.1007/s11104-017-3300-3) contains supplementary cyanobacteria increased cover dramatically during the material, which is available to authorized users. experimental period. Cultivated biocrusts established more rapidly than field-collected biocrusts, attaining A. Antoninka (*) : M. A. Bowker : P. Chuckran School of Forestry, Northern Arizona University, 200 E. Pine ~82% cover in only one year, but addition of field- Knoll Dr., P.O. Box 15018, Flagstaff, AZ 86011, USA collected biocrusts led to higher species richness, bio- e-mail: [email protected] mass (as assessed by chlorophyll a) and level of devel- opment. Mosses and lichens did not establish well in M. A. Bowker e-mail: [email protected] either case, but late successional cover was affected by hardening and culture conditions. P. Chuckran Conclusions This study provides further evidence that it e-mail: [email protected] is possible to culture biocrust components from later M. A. Bowker : S. Reed : J. Belnap successional materials and reestablish cultured organ- United States Geological Survey, Southwest Biological Science isms in the field. However, more research is needed into Center, 2290 S. West Resource Blvd, Moab, UT 84532, USA effective reclamation techniques. S. Reed . e-mail: [email protected] Keywords Biological soil crust Drylands Hardening Field establishment . Ecological restoration . Ecological J. Belnap rehabilitation . Soil erosion resistance e-mail: [email protected] N. N. Barger Abbreviations Department of Ecology and Evolutionary Biology, University of Colorado, Campus Box 334, Boulder, CO 80305-0334, USA LOD Level of biocrust development e-mail: [email protected] UTTR Utah Test and Training Range Plant Soil Introduction A recent key advance has been the cultivation of biocrust components in the lab, which when used in Biological soil crusts (biocrusts) are a critical compo- place of the field grown biocrust significantly re- nent of semiarid and arid ecosystems, providing foun- duces the amount of field disturbance required for dational structure and function in numerous ways; for inoculum. This process involves harvesting small example, influencing plant establishment, controlling amounts of material in the field and then expanded the inputs and cycling of nutrients and carbon into soils, under laboratory or greenhouse conditions, either as stabilizing soil surfaces, and impacting hydrology individual components or as a community (eg. Lan (reviewed in Belnap et al. 2016). Further, the dryland et al. 2013;Buetal.2014; Ayuso Velasco et al. ecosystems where biocrusts are common are among the 2016). This is an important step because cultivation most degraded on Earth due to pressures such as graz- of biocrusts enhances the amount of biocrust that ing, cropland extensification, and climate change can be used for a given problem without causing a (Reynolds et al. 2013). While local consequences of new disturbance by harvesting intact biocrusts as biocrust loss are obvious (e.g., increased soil erosion an inoculum source. Using light pigmented and loss, exotic plant species invasion), the regional and cyanobacteria cultures has been the most common global effects can be equally important. For example, practice for a variety of reasons: because they are loss of biocrust in disturbed drylands in the US early- to mid-successional in most drylands, among Southwest enhances dust emissions which, by acceler- the first biocrust colonizers following disturbance; ating snowmelt, can reduce input to major rivers because they can be grown rapidly and in large (Painter et al. 2010). A recent study also suggests that quantity in liquid culture; and because they provide a loss of late-successional biocrust could have such an the ecosystem benefit of increased soil stability (Bu extensive influence it could directly affect the Earth’s et al. 2014; Weber et al. 2016). There are two energy balance via changes to dryland surface albedo important disadvantages to these methods. First, (Rutherford et al. 2017). successful establishment generally requires irriga- Although an improved capacity to rehabilitate tion, which is not feasible for many arid and remote biocrusts could provide many benefits to drylands, only regions where water delivery is not possible (Zhao limited progress has been made in rehabilitation tech- et al. 2016). Second, other organisms such as nology. An effective and simple method to reestablish mosses and lichens, which contribute additional biocrusts is to collect biocrusts from areas with high benefits to ecosystem structure and function and cover and redistribute the collected material to areas even attain dominance in many drylands, are not with limited or no biocrusts (Belnap 1993; Chiquoine contained within these inocula. et al. 2016; Condon and Pyke 2016). However, the Mixed cultures of later successional biocrust (in- harvesting of intact biocrust communities can lead to cluding dark-pigmented cyanobacteria, moss and li- significant secondary disturbance. In addition, the dis- chens) and reintroduction have received less research turbed environment itself may present multiple barriers attention. Experimental culturing of biocrust mosses to successfully establishing reintroduced biocrusts. has been successful in a variety of systems, and with Rehabilitation methods have to effectively address the a variety of species (e.g. Chen et al. 2009;Xiaoetal. ecological constraints that may hinder reestablishment 2011; Antoninka et al. 2015). Mosses can make up of a functioning biocrust community (Bowker 2007). 30% or more of the biocrust cover in many drylands, For example, spreading inoculum on unstable soils will providing significant ecosystem services in terms of likely be ineffective because both soils and added dust capture, soil stability, water holding capacity and biocrusts will eventually be transported away from the carbon fixation (reviewed by Seppelt et al. 2016). rehabilitation site by wind or water. Instead, it may be Moss also adds fertility to the soil by supporting the necessary to first address the highest order barrier (e.g. soil food web and housing N2-fixers on their leaves stabilizing soils) before addition of inoculum will be (Wu et al. 2009). Although less studied, some lichens successful. Other challenges, such as climate suitabil- have been successfully cultured (Antoninka et al. 2015; ity, selection of target species, and determination of Bowker and Antoninka 2016), and efforts to understand restoration goals are important to consider in plan- their needs in field transplant experiments have also ning rehabilitation (Zhao et al. 2016). occurred (Davidson et al. 2002). Lichens add ecosystem Plant Soil function by providing armor that reduces weed seed Methods germination, further stabilizes soil, alters soil albedo and, in many cases enhances N2-fixation (reviewed by Experiment 1. Field-collected Biocrust trial Rosentreter et al. 2016). Early successional species, such as cyanobacteria In April of 2013, we collected intact biocrusts from a site in this case, are commonly used for rehabilitation within the Utah Test and Training Range (UTTR, under the assumption that they are the best equipped 41°0625.60″ N 113°30′04.24 W, elevation ~1295 m) to survive and may facilitate colonization by later located in the Great Basin, Great Salt Lake Area. Soils successional species. However, this assumption re- collected from this site were characterized by silt loam mains untested for biocrusts. Another strategy might soils in the Skumpah series. To collect field grown be to introduce several species with differing suc- biocrust material, we scraped biocrusts from the surface cessional preferences and divergent functional traits, of the soil to a depth of 0.5-1 cm using metal dust pans. and to allow the environment to select which are Adhering soil below biocrusts was also removed by most likely to be successful. Thus, applying a mixed scraping. We crumbled biocrusts by hand to fragments inoculum of multiple functional groups may opti- no larger than 0.5 cm, with the majority in the range of mize the chances of biocrust establishment and 0.1–0.2 cm, and homogenized the inoculum. The collect- may enhance ecosystem multi-functionality due to ed inoculum was a mix of light-pigmented cyanobacteria