A practical guide to measuring functional indicators and traits in biocrusts

Biocrusts are multifunctional communities that are increasingly being used to restore degraded or damaged ecosystems. Concurrently, restoration science is shifting away from the use of purely structural metrics, such as relative abundance, to more functional approaches. Although biocrust restoration technology is advancing, there is a lack of readily available information on how to monitor biocrust functioning and set appropriate restoration goals. We therefore compiled a selection of 22 functional indicators that can be used to monitor biocrust functions, such as CO₂ exchange as an indicator of productivity or soil aggregate stability as a proxy for erosion resistance. We describe the functional importance of each indicator and the available protocols with which it may be measured. The majority of indicators can be measured as a functional trait of species by using patches of biocrust or cultures that contain only one species. Practitioners wishing to track the multifunctionality of an entire biocrust community would be advised to choose one indicator from each broad functional group (erosion resistance, nutrient accumulation, productivity, energy balance, hydrology), whereas a targeted approach would be more appropriate for projects with a key function of interest. Because predisturbance data are rarely available for biocrust functions, restoration goals can be based on a closely analogous site, literature values, or an expert elicitation process. Finally, we advocate for the establishment of a global trait database for biocrusts, which would reduce the damage resulting from repeated sampling, and provide a wealth of future research opportunities.     

Unexpected side effects in biocrust after treating non‐native plants using carbon addition

Carbon addition has been proposed as an alternative to herbicide and manual removal methods to treat non‐native plants and reduce non‐target effects of treatments (e.g. impacts on native plants; surface disturbance). On Mojave Desert pavement and biocrust substrates after experimental soil disturbance and carbon addition (1,263 g C/m² as sucrose), we observed declines in lichens and moss cover in sucrose‐treated plots. To further explore this unforeseen potential side effect of using carbon addition as a non‐native plant treatment, we conducted biocrust surveys 5 and 7 years after treatments, sampled surface soils to observe if treatments additionally affected soil filamentous cyanobacteria, and conducted laboratory trials testing the effects of different levels of sucrose on cyanobacteria and desert mosses. Sucrose addition to biocrust plots reduced lichen and moss cover by 33–78% and species richness by 40–80%. Sucrose reduced biocrust cover in biocrust plots to levels similarly detected in pavement plots (<1%). While cyanobacteria in the field did not appear to be affected by sucrose, laboratory tests showed negative effects of sucrose on both cyanobacteria and mosses. Cyanobacteria declined by 41% 1 month after exposure to 5.4 g C/m² equivalent solutions. We detected injury to photosynthesis in mosses after 96 hour exposure to 79–316 g C/m² equivalent solutions. Caution is warranted when using carbon addition, at least in the form and concentration of sucrose, as a treatment for reducing non‐native plants on sites where conserving biocrust is a goal.     

Biological soil crusts in ecological restoration: emerging research and perspectives

Drylands encompass over 40% of terrestrial ecosystems and face significant anthropogenic degradation causing a loss of ecosystem integrity, services, and deterioration of social‐ecological systems. To combat this degradation, some dryland restoration efforts have focused on the use of biological soil crusts (biocrusts): complex communities of cyanobacteria, algae, lichens, bryophytes, and other organisms living in association with the top millimeters of soil. Biocrusts are common in many ecosystems and especially drylands. They perform a suite of ecosystem functions: stabilizing soil surfaces to prevent erosion, contributing carbon through photosynthesis, fixing nitrogen, and mediating the hydrological cycle in drylands. Biocrusts have emerged as a potential tool in restoration; developing methods to implement effective biocrust restoration has the potential to return many ecosystem functions and services. Although culture‐based approaches have allowed researchers to learn about the biology, physiology, and cultivation of biocrusts, transferring this knowledge to field implementation has been more challenging. A large amount of research has amassed to improve our understanding of biocrust restoration, leaving us at an opportune time to learn from one another and to join approaches for maximum efficacy. The articles in this special issue improve the state of our current knowledge in biocrust restoration, highlighting efforts to effectively restore biocrusts through a variety of different ecosystems, across scales and utilizing a variety of lab and field methods. This collective work provides a useful resource for the scientific community as well as land managers.     

松嫩平原农业区土壤理化性质与真菌代谢产物——球囊霉素相关土壤蛋白的关系

对不同土壤深度的真菌特征代谢产物球囊霉素相关土壤蛋白(glomalin-related soil protein,GRSP)与土壤理化性质相关关系的研究,有助于揭示土壤真菌在不同土壤深度对养分的调节作用。本研究在松嫩平原农田5个土层(0~100 cm)采集360个土样,分析了易提取球囊霉素相关土壤蛋白(EE-GRSP)、总提取球囊霉素相关土壤蛋白(T-GRSP)含量和11个土壤理化性质指标及其相关关系。结果表明:表层EE-GRSP和T-GRSP平均含量为0.74和6.0 mg·g-1,随土层加深均呈显著下降趋势;深层土壤养分储量较大,有机碳、全氮、全磷、全钾、碱解氮、速效磷和速效钾储量在深层(40~100 cm)占总储量的41.2%~62.8%;土壤p H、容重、含水量和电导率也表现了明显的垂直变化规律;各理化性质在不同土层与GRSP的相关关系不同,有机碳在全部深度与GRSP均有显著的相关关系,而p H与GRSP均在20~100 cm深度有极显著的相关性(P0.01),且与EE-GRSP、T-GRSP显著相关的理化性质指标分别在60~80、20~60 cm最多,在表层最少;GRSP在深层土壤与各指标的相关性与表层不同,可能会影响GRSP对不同土壤深度养分的调节功能;鉴于深层土壤中GRSP与养分显著相关,本研究提出,种植与土壤真菌具有共生关系的深根性植物是对富集养分的深层土壤进行生物修复的有效方法。     

Responses of soil respiration with biocrust cover to water and temperature in the southeastern edge of Tengger Desert,Northwest China

Aims Soil respiration of the lands covered by biocrusts is an important component in the carbon cycle of arid, semi-arid and dry-subhumid ecosystems (drylands hereafter), and one of the key processes in the carbon cycle of drylands. However, the responses of the rate of soil respiration with biocrusts to water and temperature are uncertain in the investigations of the effects of experimental warming and precipitation patterns on CO₂ fluxes in biocrust dominated ecosystems. The objectives of this study were to investigate the relationships of carbon release from the biocrust-soil systems with water and temperature in drylands. Methods Intact soil columns with two types of biocrusts, including moss and algae-lichen crusts, were collected in a natural vegetation area in the southeastern fringe of the Tengger Desert. Open top chambers were used to simulate climate warming, and the soil respiration rate was measured under warming and non-warming treatments using an automated soil respiration system (LI-8150). Important findings Over the whole observational period (from April 2016 to July 2016), soil respiration rates varied from -0.16 to 4.69 μmol·m^-2·s^-1 for the moss crust-covered soils and from -0.21 to 5.72 μmol·m^-2·s^-1 for the algae-lichen crust-covered soils, respectively, under different rainfall events (the precipitations between 0.3-30.0 mm). The mean soil respiration rate of the moss crust-covered soils is 1.09 μmol·m^-2·s^-1, which is higher than that of the algae-lichen crust-covered soils of 0.94 μmol·m^-2·s^-1. The soil respiration rate of the two types of biocrust-covered soils showed different dynamics and spatial heterogeneities with rainfall events, and were positively correlated with precipitation. The mean soil respiration rate of the biocrust-covered soils without warming was 1.24 μmol·m^-2·s^-1, significantly higher than that with warming treatments of 0.79 μmol·m^-2·s^-1 (p < 0.05). By increasing the evaporation of soil moisture, the simulated warming impeded soil respiration. In most cases, soil temperature and soil respiration rate displayed a similar single-peak curve during the diel cycle. Our results show an approximately two hours’ lag between soil temperature at 5 cm depth and the soil respiration rate of the biocrust-covered soils during the diel cycle.     

Cyanobacteria inoculation as a potential tool for stabilization of burned soils

The practice of “cyanobacterization” (soil inoculation with cyanobacteria) has been shown to be effective in increasing soil fertility and physical stability in natural and agricultural soils, but little is known about its utility for the recovery of burned soils. To partly fill this knowledge gap, we inoculated two cyanobacterial species, Phormidium ambiguum and Scytonema javanicum, in two burned sterilized soils having contrasting properties, and incubated them under laboratory conditions for 45 days. The development of a cyanobacterial biocrust induced by the inoculum was evident and confirmed by the significant increase in chlorophyll a content compared to control soils. Hydrophobicity, surface penetration resistance, and exopolysaccharide content of the two soils were also evaluated. Cyanobacteria inoculation significantly decreased soil hydrophobicity, as assessed by the lower repellency index 15 days after the inoculation compared to the control soils. A significant increase in penetration resistance was recorded in the inoculated samples compared to control ones after 45 days of soil incubation. The effect of cyanobacteria inoculation depended on the characteristics of the burned soil, being more marked in the soil finer in texture, richer in organic carbon and nitrogen, and with lower initial soil hydrophobicity. In conclusion, this study points to the potential of cyanobacterization for the stabilization and recovery of soils in burned areas, which is one of the major concerns in postfire management to avoid net soil loss and major hydrogeological issues.     

Hydroseeding tackifiers and dryland moss restoration potential

Tackifiers are long‐chain carbon compounds used for soil stabilization and hydroseeding and could provide a vehicle for biological soil crust restoration. We examined the sensitivity of two dryland mosses, Bryum argenteum and Syntrichia ruralis, to three common tackifiers—guar, psyllium, and polyacrylamide (PAM)—at 0.5×, 1.0×, and 2.0× of recommended (×) concentrations for erosion control and revegetation. We measured moss shoot, gemma, and protonema production as well as moss organic matter and bound sand masses as indicators of growth and soil holding ability. We tested sand and tackifier chemistry to investigate potential nutrient and toxicant potential on moss growth. Groups of 10 fragments from field‐collected mosses were grown on sand in open petri dishes arranged in a growth chamber in replicated blocks containing each tackifier and concentration combination plus a distilled water control. Bryum (n = 10) and Syntrichia (n = 9) growth were measured at the end of 6 and 5 weeks, respectively. Overall model tests yielded statistically significant results (p < 0.001) for every variable in each species. When compared to water, guar tended to decrease growth, psyllium tended to increase growth, and PAM's effects were generally neutral to positive. Within tackifier types, increasing concentrations of guar tended to decrease growth, while increasing concentrations of psyllium tended to increase growth. Changes in PAM concentrations had little effect on growth. Increases in guar and psyllium lowered pH and increased P and K. Psyllium and PAM yielded promising results as potential agents of dispersal and adherence of dryland mosses in field restoration.     

Microbial inoculum production for biocrust restoration: testing the effects of a common substrate versus native soils on yield and community composition

Human activities are causing unprecedented disturbances in terrestrial ecosystems across the globe. To reverse soil deterioration in drylands, a promising tool is the ex situ cultivation of biological soil crusts, topsoil geobiological assemblages that provide key ecosystem services. One approach is to transplant biocrusts cultivated in greenhouse nursery facilities into degraded sites to accelerate recovery. Lichen‐ and moss‐dominated biocrusts have been successfully grown using a common, sandy soil. We compared the use of a common, sandy soil versus native soils as a substrate for the cultivation of cyanobacteria‐dominated biocrusts. In greenhouse experiments, we inoculated natural biocrusts collected from three Southwestern USA dryland sites on to either a common, sandy soil or on their respective native soils. The common substrate resulted in a moderate enhancement of growth yield relative to native soils. While changes in bacterial phyla composition remained low in all cases, the use of a common substrate introduced larger shifts in cyanobacterial community composition than did using native soils. The shift increase attributable to the common, sandy soil was not catastrophic—and typical cyanobacteria of field biocrusts remained dominant—unless textural differences between the common substrate and native soils were marked. Because collecting native soils adds a significant effort to growing cyanobacterial biocrusts in greenhouses for restoration purposes, the use of a common, sandy substrate may be considered by land managers as a standard practice. But we recommend to regularly monitor the composition of the grown biomass.     

Bio‐priming seeds with cyanobacteria: effects on native plant growth and soil properties

Cyanobacteria are photosynthetic bacteria that form a fundamental part of soil biocrusts, enhance soil function and structure, and can promote plant growth. We assessed the potential of cyanobacteria as a seed bio‐primer for mine‐site restoration in an arid region in Western Australia, examining its effects on native plant growth and the characteristics of mine soil substrates used in dryland restoration. Cyanobacteria strains indigenous to the study region (Leptolyngbya sp., Microcoleus sp., Nostoc sp., and Scytonema sp.) were used to create an inoculant. Seeds of seven native plant species were bio‐primed with the inoculant, and their germination and growth assessed in a laboratory experiment. Seedling growth after bio‐priming was assessed in a glasshouse experiment for a subset of three species, in two different substrates (topsoil and mine waste). Soil properties related to soil function, e.g. total organic carbon, total nitrogen, and microbial activity, were also measured. Minor effects on germination were recorded with only significantly higher germination rates reported in E. gamophylla. Soil parameters were generally higher in topsoil than in mine waste, regardless of bio‐priming treatment. However, bio‐priming resulted in seedlings of four species producing longer radicles and/or shoots. For example, seedling root lengths of bio‐primed G. wickhamii were 57% larger than the control treatment (30.1 ± 4.3 and 13.0 ± 1.6 mm, respectively); and shoots of T. wiseana were 54% longer in the bio‐primed treatment (18.6 ± 1.6 mm) compared to the control (8.53 ± 1.4 mm). Overall, our results highlight that bio‐priming with cyanobacteria may improve plant growth for some species commonly used in dryland restoration.     

Inoculation and habitat amelioration efforts in biological soil crust recovery vary by desert and soil texture

As dryland degradation continues, it is increasingly important to understand how to effectively restore biocrust communities. Potential techniques include the addition of biocrust inoculum to accelerate biocrust recovery. Enhanced erosion typical of degraded environments creates a challenge for these approaches, due to loss by wind or water and burial by saltating particles. To retain and protect added inoculum, the inclusion of habitat‐amelioration techniques can improve recovery rates. This study tested three different types of inoculum (field‐collected, greenhouse‐cultivated, and laboratory‐cultivated biocrust) coupled with two treatments to augment soil stability and ameliorate habitat limitations: soil surface polyacrylamide additions and installation of straw barriers. This was done across two deserts (Great Basin and Chihuahuan) and separated into generally coarse‐ or finer‐textured soils in each desert, with results monitored for 3 years (2015, 2016, 2017). While the inoculum type, coupled with habitat ameliorations, occasionally enhanced biocrust growth across years and treatments, in other cases, it made no difference compared to natural recovery rates. Rather, the desert location and soil texture groupings were the most prominent factors in determining recovery trajectories. Recovery proportions were similar in the finer‐textured sites in both the Great Basin and the Chihuahuan deserts, while the coarser‐textured site in the Great Basin did show some recovery over time and the Chihuahuan coarser‐textured site did not. This study demonstrates the importance of understanding site potential and identifying key limitations to biocrust recovery for successful restoration projects.