Biological soil crust
Cryptobiotic soil, cryptogamic soil,
microbiotic soil, microphytic soil,
biocrust
Biological soil crust in Hovenweep National Monument.
Climatearid, semi-arid
Primaryfungi, lichens, cyanobacteria, bryophytes, and algae

Biological soil crusts are communities of living organisms on the soil surface in arid and semi-arid ecosystems. They are found throughout the world with varying species composition and cover depending on topography, soil characteristics, climate, plant community, microhabitats, and disturbance regimes. Biological soil crusts perform important ecological roles including carbon fixation, nitrogen fixation and soil stabilization; they alter soil albedo and water relations and affect germination and nutrient levels in vascular plants. They can be damaged by fire, recreational activity, grazing and other disturbances and can require long time periods to recover composition and function. Biological soil crusts are also known as biocrusts or as cryptogamic, microbiotic, microphytic, or cryptobiotic soils.

Natural history

Biology and composition

Biological soil crusts are most often[1] composed of fungi, lichens, cyanobacteria, bryophytes, and algae in varying proportions. These organisms live in intimate association in the uppermost few millimeters of the soil surface, and are the biological basis for the formation of soil crusts.

Cyanobacteria

Cyanobacteria are the main photosynthetic component of biological soil crusts,[2] in addition to other photosynthetic taxa such as mosses, lichens, and green algae. The most common cyanobacteria found in soil crusts belong to large filamentous species such as those in the genus Microcoleus.[1] These species form bundled filaments that are surrounded by a gelatinous sheath of polysaccharides. These filaments bind soil particles throughout the uppermost soil layers, forming a 3-D net-like structure that holds the soil together in a crust. Other common cyanobacteria species are as those in the genus Nostoc, which can also form sheaths and sheets of filaments that stabilize the soil. Some Nostoc species are also able to fix atmospheric nitrogen gas into bio-available forms such as ammonia.

Bryophytes

Bryophytes in soil crusts include mosses and liverworts. Mosses are usually classified as short annual mosses or tall perennial mosses. Liverworts can be flat and ribbon-like or leafy. They can reproduce by spore formation or by asexual fragmentation, and photosynthesize to fix carbon from the atmosphere.

Lichens

Lichens are often distinguished by growth form and by their photosymbiont. Crust lichens include crustose and areolate lichens that are appressed to the soil substrate, squamulose lichens with scale- or plate-like bodies that are raised above the soils, and foliose lichens with more "leafy" structures that can be attached to the soil at only one portion. Lichens with algal symbionts can fix atmospheric carbon, while lichens with cyanobacterial symbionts can fix nitrogen as well. Lichens produce many pigments that help protect them from radiation.[3]

Fungi

Microfungi in biological soil crusts can occur as free-living species, or in symbiosis with algae in lichens. Free-living microfungi often function as decomposers, and contribute to soil microbial biomass. Many microfungi in biological soil crusts have adapted to the intense light conditions by evolving the ability to produce melanin, and are called black fungi or black yeasts. Fungal hyphae can bind soil particles together.

Free-living green algae

Green algae in soil crusts are present just below the soil surface where they are partially protected from UV radiation. They become inactive when dry and reactivate when moistened. They can photosynthesize to fix carbon from the atmosphere.

Formation and succession

Biological soil crusts are formed in open spaces between vascular plants. Frequently, single-celled organisms such as cyanobacteria or spores of free-living fungi colonize bare ground first. Once filaments have stabilized the soil, lichens and mosses can colonize. Appressed lichens are generally earlier colonizers or persist in more stressful conditions, while more three-dimensional lichens require long disturbance-free growth periods and more moderate conditions.

Recovery following disturbance varies. Cyanobacteria cover can recover by propagules blowing in from adjacent undisturbed areas rapidly after disturbance. Total recovery of cover and composition occurs more rapidly in fine soil textured, moister environments (~2 years) and more slowly (>3800 years)[4] in coarse soil textured, dry environments. Recovery times also depend on disturbance regime, site, and availability of propagules.

Distribution

Geographical range

Biological soil crust in Natural Bridges National Monument near Sipapu Bridge.

Biological soil crusts cover about 12% of the earth's landmass.[5] They are found on almost all soil types, but are more commonly found in arid regions of the world where plant cover is low and plants are more widely spaced. This is because crust organisms have a limited ability to grow upwards and cannot compete for light with vascular plants. Across the globe, biological soil crusts can be found on all continents including Antarctica.[6]

Variation throughout range

The species composition and physical appearance of biological soil crusts vary depending on the climate, soil, and disturbance conditions. For example, biological soil crusts are more dominated by green algae on more acidic and less salty soils, whereas cyanobacteria are more favored on alkaline and haline soils. Within a climate zone, the abundance of lichens and mosses in biological soil crusts generally increases with increasing clay and silt content and decreasing sand. Also, habitats that are more moist generally support more lichens and mosses.

The morphology of biological soil crust surfaces can range from smooth and a few millimeters in thickness to pinnacles up to 15 cm high. Smooth biological soil crusts occur in hot deserts where the soil does not freeze, and consist mostly of cyanobacteria, algae, and fungi. Thicker and rougher crusts occur in areas where higher precipitation results in increased cover of lichen and mosses, and frost heaving of these surfaces cause microtopography such as rolling hills and steep pinnacles. Due to the intense UV radiation present in areas where biological soil crusts occur, biological soil crusts appear darker than the crustless soil in the same area due to the UV-protective pigmentation of cyanobacteria and other crust organisms.[6]

Ecology

Ecosystem function and services

Biogeochemical cycling

Carbon cycling

Biological soil crusts contribute to the carbon cycle through respiration and photosynthesis of crust microorganisms which are active only when wet. Respiration can begin in as little as 3 minutes after wetting whereas photosynthesis reaches full activity after 30 minutes. Some groups have different responses to high water content, with some lichens showing decreased photosynthesis when water content was greater than 60% whereas green algae showed little response to high water content.[4] Photosynthesis rates are also dependent on temperature, with rates increasing up to approximately 28 °C (82 °F).

Estimates for annual carbon inputs range from 0.4 to 37 g/cm*year depending on successional state.[7] Estimates of total net carbon uptake by crusts globally are ~3.9 Pg/year (2.1–7.4 Pg/year).[8]

Nitrogen cycling

Biological soil crust contributions to the nitrogen cycle varies by crust composition because only cyanobacteria and cyanolichens fix nitrogen. Nitrogen fixation requires energy from photosynthesis products, and thus increase with temperature given sufficient moisture. Nitrogen fixed by crusts has been shown to leak into surrounding substrate and can be taken up by plants, bacteria, and fungi. Nitrogen fixation has been recorded at rates of 0.7–100 kg/ha*year, from hot deserts in Australia to cold deserts.[9] Estimates of total biological nitrogen fixation are ~ 49 Tg/year (27–99 Tg/year).[8]

Geophysical and geomorphological properties

Soil stability

Soils in arid regions are slow-forming and easily eroded.[10] Crust organisms contribute to increased soil stability where they occur. Cyanobacteria have filamentous growth forms that bind soil particles together, and hyphae of fungi and rhizines/rhizoids of lichens and mosses also have similar effects. The increased surface roughness of crusted areas compared to bare soil further improves resistance to wind and water erosion. Aggregates of soil formed by crust organisms also increase soil aeration and provide surfaces where nutrient transformation can occur.[11]

Soil water relations

The effect of biological soil crusts on water infiltration and soil moisture depends on the dominant crust organisms, soil characteristics, and climate. In areas where biological soil crusts produce rough surface microtopography, water is detained longer on the soil surface and this increases water infiltration. However, in warm deserts where biological soil crusts are smooth and flat, infiltration rates can be decreased by bioclogging.[4]

Albedo

The darkened surfaces of biological soil crusts decreases soil albedo (a measure of the amount of light reflected off of the surface) compared to nearby soils, which increases the energy absorbed by the soil surface. Soils with well-developed biological soil crusts can be over 12 °C (22 °F) warmer than adjacent surfaces. Increased soil temperatures are associated with increased metabolic processes such as photosynthesis and nitrogen fixation, as well as higher soil water evaporation rates and delayed seedling germination and establishment.[4] The activity levels of many arthropods and small mammals are also controlled by soil surface temperature.[11]

Dust-trapping

The increased surface roughness associated with biological soil crusts increase the capture of dust. These Aeolian deposits of dust are often enriched in plant-essential nutrients, and thus increase both the fertility and the water holding capacity of soils.[11]

Hydration and dehydration cycles

The biological soil crust is an integral part of many arid and semi-arid ecosystems as an essential contributor to conditions such as dust control, water acquisition, and contributors of soil nutrients. Biocrust is poikilohydric and does not have the ability to maintain or regulate its own water retention.[12] This causes the biocrust's water content to change depending on the water in the surrounding environment. Due to biological soil crust existing in mostly arid and semi-arid environments with the inability to hold water, the crust is mainly dormant except for short periods of activity when the crust receives precipitation.[13] Microorganisms like those that make up biological soil crust are good at responding quickly to changes in the environment even after a period of dormancy such as precipitation.

Desiccation can lead to oxidation and the destruction of nutrients, amino acids, and cell membranes in the microorganisms that make up biological soil crust.[14] However, the biological soil crust has adapted to survive in very harsh environments with the aid of cyanobacteria. Cyanobacteria have evolved the ability to navigate the extreme conditions of their surrounding environment by existing in a biocrust. A trait of the biological soil crust community is that it will activate from a dormant state when it is exposed to precipitation transforming from a dry, dead-looking crust to an actively photosynthetic community.[13][14] It will change its appearance to be vibrant and alive to the naked eye. Many crusts will even turn different shades of dark green.[13][14][15] The cyanobacterium Microcoleus vaginatus is one of the most dominant organisms found in biocrust and is fundamental to the crust's ability to reawaken from dormancy when rehydrated due to precipitation or runoff. Cyanobacteria have been found to outcompete the other components of biocrust when exposed to light and precipitation.[15] Cyanobacteria are primarily responsible for the pigment and rejuvenation of the crust during environmental changes that result in short spurts of rehydration for the biocrust.

A filamentous cyanobacterium called Microcoleus vaginatus was found to exist in a dormant, metabolically inactive state beneath the surface of the crust in periods of drought or water deficiency. When the biocrust eventually receives precipitation, it is able to perform hydrotaxis and appears to resurrect.[13] In this stage, the M. vaginatus migrates upward to the surface of the crust when hydrated, to perform oxygenic photosynthesis. In this photosynthetic process, the cyanobacteria carries with it a green-blue photosynthetic pigment to the surface of the crust. When inevitably there is a period of insufficient water again, the M. vaginatus is able to return to a dormant state, migrating back down into the crust and bringing the pigment with it. This process goes along with the rapid turning on of metabolic pathways allowing metabolic functions to occur within the cells in the short periods of time when the crust is hydrated and awakened from dormancy. Cyanobacteria are able to repeat this process over and over again in the event of rehydration in the future.[13][14][15]

The amount of time it takes for the greening process in biocrust to occur varies on the environmental conditions in which the biocrust lives. Biocrust can take anywhere from five minutes to 24 hours to awaken from dormancy.[12][14] The crusts will only awaken if the conditions are conducive to the biocrust.

Biological soil crust role in soil hydrology

Biocrust influences a soil's microtopography, carbohydrate content, porosity, and hydrophobicity which are the major contributing factors to soil hydrology. The relationship between biocrust and soil hydrology is not fully understood by scientists. It is known that the biocrust does play a role in the absorption and retention of moisture in the soil. In arid and semi-arid environments biocrust can cover over 70% of the soil not being covered by plants, indicating that the relationship between soil, water, and biocrust is extremely pertinent to these environments.[16] Biocrusts has been shown to increase infiltration of water and pore space (or porosity) in soil but the opposite may occur depending on thetype of biocrust. The effect biocrust has on water infiltration and the amount of water retained in the soil is greatly dependent on which microorganisms are most dominant in the specific forms of biocrust. Most research studies like that done by Canton et al. support that biological soil crust composed of large amounts of moss and lichens are better able to absorb water resulting in good soil infiltration. In comparison, biocrusts that aredominated by cyanobacteria is more likely to cause biological clogging where the pores of the soil are obstructed by the cyanobacteria responding to the presence of moisture by awakening from their dormancy and swelling. The darkening of the soil surface by biocrust can also raise the soil temperature leading to faster water evaporation. There is limited research however, that indicates that the rough surface of cyanobacteria traps water runoff and lichen in cyanobacteria-dominant biocrust increase the porosity of the soil allowing for better infiltration than soil that does not have any biocrust.[16][17]

The type of soil and its texture is also a major determining factor in the biological soil crust's relationship with water retention and filtration. Soils with a large presence of sand (less soil and clay) have high levels of water retention in their surface levels but have limited downward movement of the water. Soils that were less than 80% sand had greater infiltration due to biocrust creating soil aggregates. Other factors like plant roots may play a role in water retention and soil moisture at depths below the soil crust.[16]

Role in the biological community

Effects on vascular plants

Germination and establishment

The presence of biological soil crust cover can differentially inhibit or facilitate plant seed catchment and germination.[18] The increased micro-topography generally increases the probability that plant seeds will be caught on the soil surface and not blown away. Differences in water infiltration and soil moisture also contribute to differential germination depending on the plant species. It has been shown that while some native desert plant species have seeds with self-burial mechanisms that can establish readily in crusted areas, many exotic invasive plants do not. Therefore, the presence of biological soil crusts may slow the establishment of invasive plant species such as cheatgrass (Bromus tectorum).[19]

Nutrient levels

Biological soil crusts do not compete with vascular plants for nutrients, but rather have been shown to increase nutrient levels in plant tissues, which results in higher biomass for plants that grow near biological soil crusts. This can occur through N fixation by cyanobacteria in the crusts, increased trapment of nutrient-rich dust, as well as increased concentrations of micronutrients that are able to chelate to the negatively charged clay particles bound by cyanobacterial filaments.[11]

Effects on animals

The increased nutrient status of plant tissue in areas where biological soil crusts occur can directly benefit herbivore species in the community. Microarthropod populations also increase with more developed crusts due to increased microhabitats produced by the crust microtopography.[4]

Human impacts and management

Human benefits

Rammed-earth section of the Great Wall of China. Research shows that biocrust is a natural factor in preserving the structure.

A recent study in China shows that biocrusts have been an import factor in the preservation of sections of the Great Wall built using rammed earth methods.[20]

Human disturbance

Biological soil crusts are extremely susceptible to disturbance from human activities. Compressional and shear forces can disrupt biological soil crusts especially when they are dry, leaving them to be blown or washed away. Thus, animal hoof impact, human footsteps, off-road vehicles, and tank treads can remove crusts and these disturbances have occurred over large areas globally. Once biological soil crusts are disrupted, wind and water can move sediments onto adjacent intact crusts, burying them and preventing photosynthesis of non-motile organisms such as mosses, lichens, green algae, and small cyanobacteria, and of motile cyanobacteria when the soil remains dry. This kills remaining intact crust and causes large areas of loss.

Invasive species introduced by humans can also affect biological soil crusts. Invasive annual grasses can occupy areas once occupied by crusts and allow fire to travel between large plants, whereas previously it would have just jumped from plant to plant and not directly affected the crusts.[11]

Climate change affects biological soil crusts by altering the timing and magnitude of precipitation events and temperature. Because crusts are only active when wet, some of these new conditions may reduce the amount of time when conditions are favorable for activity.[21] Biological soil crusts require stored carbon when reactivating after being dry. If they do not have enough moisture to photosynthesize to make up for the carbon used, they can gradually deplete carbon stocks and die.[22] Reduced carbon fixation also leads to decreased nitrogen fixation rates because crust organisms do not have sufficient energy for this energy-intensive process. Without carbon and nitrogen available, they are not able to grow nor repair damaged cells from excess radiation.

Conservation and management

Removal of stressors such as grazing or protection from disturbance are the easiest ways to maintain and improve biological soil crusts. Protection of relic sites that have not been disturbed can serve as reference conditions for restoration. There are several successful methods for stabilizing soil to allow recolonization of crusts including coarse litter application (such as straw) and planting vascular plants, but these are costly and labor-intensive techniques. Spraying polyacrylamide gel has been tried but this has adversely affected photosynthesis and nitrogen fixation of Collema species and thus is less useful. Other methods such as fertilization and inoculation with material from adjacent sites may enhance crust recovery, but more research is needed to determine the local costs of disturbance.[23] Today, direct inoculation of soil native microorganisms, bacteria and cyanobacteria, supposed as a new step, biologic, sustainable, eco-friendly and economically-effective technique to rehabilitate biological soil crust.[24][25]

References

  1. 1 2 Belnap, Jayne (August 5, 2013). "Cryptobiotic Soils: Holding the Place in Place". U.S. Geological Survey. Archived from the original on June 3, 2016. Retrieved May 10, 2016.
  2. ↑ Moore, Lorena B. (March 23, 2010). "Cryptobiotic Crust in the Sonoran Desert". Southern Arizona Desert Botany. Archived from the original on June 4, 2016. Retrieved May 10, 2016.
  3. ↑ Solhaug, Knut Asbjørn; Gauslaa, Yngvar; Nybakken, Line; Bilger, Wolfgang (April 2003). "UV-induction of sun-screening pigments in lichens". New Phytologist. 158: 91–100. doi:10.1046/j.1469-8137.2003.00708.x.
  4. 1 2 3 4 5 Belnap, Jayne; et al. (2001). "Biological Soil Crusts: Ecology and Management" (PDF). U.S. Department of the Interior: Bureau of Land Management and U.S. Geological Survey. Technical Reference 1730-2. Archived from the original (PDF) on 2018-11-05. Retrieved 2014-03-24.
  5. ↑ Naylor, Dan; Sadler, Natalie; Bhattacharjee, Arunima; Graham, Emily B.; Anderton, Christopher R.; McClure, Ryan; Lipton, Mary; Hofmockel, Kirsten S.; Jansson, Janet K. (17 October 2020). "Soil Microbiomes Under Climate Change and Implications for Carbon Cycling". Annual Review of Environment and Resources. 45 (1): 29–59. doi:10.1146/annurev-environ-012320-082720.
  6. 1 2 Rosentreter, R., M. Bowker, and J. Belnap. 2007. A Field Guide to Biological Soil Crusts of Western U.S. Drylands. U.S. Government Printing Office, Denver, Colorado.
  7. ↑ Housman, D.C.; Powers, H.H.; Collins, A.D.; Belnap, J. (2006). "Carbon and nitrogen fixation differ between successional stages of biological soil crusts in the Colorado Plateau and Chihuahuan Desert". Journal of Arid Environments (Submitted manuscript). 66 (4): 620–634. Bibcode:2006JArEn..66..620H. doi:10.1016/j.jaridenv.2005.11.014.
  8. 1 2 Elbert, W.; Weber, B.; Burrows, S.; Steinkamp, J.; Budel, B.; Andreae, M. O.; Poschl, U. (2012). "Contribution of cryptogamic covers to the global cycles of carbon and nitrogen". Nature Geoscience. 5 (7): 459–462. Bibcode:2012NatGe...5..459E. doi:10.1038/ngeo1486.
  9. ↑ Evans R. D. and Johansen J. R. 1999. Microbiotic Crusts and Ecosystem Processes. Critical Reviews in Plant Sciences 18(2): 183-225.
  10. ↑ "The arid environments: Arid zone soils and importance of soil properties". Arid zone forestry: A guide for field technicians. Food and Agriculture Organization of the United Nations. 1989. ISBN 978-92-5-102809-4.
  11. 1 2 3 4 5 Belnap, Jayne (May 2003). "The world at your feet: desert biological soil crusts". Frontiers in Ecology and the Environment. 1 (4): 181–189. doi:10.1890/1540-9295(2003)001[0181:TWAYFD]2.0.CO;2.
  12. 1 2 Green, T. G. Allan; Proctor, Michael C. F. (2016). "Physiology of Photosynthetic Organisms within Biological Soil Crusts: Their Adaptation, Flexibility, and Plasticity". Biological Soil Crusts: An Organizing Principle in Drylands. Ecological Studies. Vol. 226. pp. 347–381. doi:10.1007/978-3-319-30214-0_18. ISBN 978-3-319-30212-6.
  13. 1 2 3 4 5 Rajeev, Lara; da Rocha, Ulisses Nunes; Klitgord, Niels; Luning, Eric G.; Fortney, Julian; Axen, Seth D.; Shih, Patrick M.; Bouskill, Nicholas J.; Bowen, Benjamin P.; Kerfeld, Cheryl A.; Garcia-Pichel, Ferran; Brodie, Eoin L.; Northen, Trent R.; Mukhopadhyay, Aindrila (November 2013). "Dynamic cyanobacterial response to hydration and dehydration in a desert biological soil crust". The ISME Journal. 7 (11): 2178–2191. doi:10.1038/ismej.2013.83. PMC 3806265. PMID 23739051.
  14. 1 2 3 4 5 Abed, Raeid M. M.; Polerecky, Lubos; Al-Habsi, Amal; Oetjen, Janina; Strous, Marc; de Beer, Dirk (6 November 2014). "Rapid Recovery of Cyanobacterial Pigments in Desiccated Biological Soil Crusts following Addition of Water". PLOS ONE. 9 (11): e112372. Bibcode:2014PLoSO...9k2372A. doi:10.1371/journal.pone.0112372. PMC 4223047. PMID 25375172.
  15. 1 2 3 Angel, Roey; Conrad, Ralf (June 2013). "Elucidating the microbial resuscitation cascade in biological soil crusts following a simulated rain event: Microbial resuscitation in biological soil crusts". Environmental Microbiology. 15 (10): 2799–3515. doi:10.1111/1462-2920.12140. PMID 23648088.
  16. 1 2 3 Belnap, Jayne (15 October 2006). "The potential roles of biological soil crusts in dryland hydrologic cycles". Hydrological Processes. 20 (15): 3159–3178. Bibcode:2006HyPr...20.3159B. doi:10.1002/hyp.6325. S2CID 129013389.
  17. ↑ Cantón, Yolanda; Chamizo, Sonia; Rodriguez-Caballero, Emilio; Lázaro, Roberto; Roncero-Ramos, Beatriz; Román, José Raúl; Solé-Benet, Albert (6 March 2020). "Water Regulation in Cyanobacterial Biocrusts from Drylands: Negative Impacts of Anthropogenic Disturbance". Water. 12 (3): 720. doi:10.3390/w12030720. hdl:10261/205628.
  18. ↑ Havrilla, Caroline A.; Chaudhary, V. Bala; Ferrenberg, Scott; Antoninka, Anita J.; Belnap, Jayne; Bowker, Matthew A.; Eldridge, David J.; Faist, Akasha M.; Huber‐Sannwald, Elisabeth; Leslie, Alexander D.; Rodriguez‐Caballero, Emilio; Zhang, Yuanming; Barger, Nichole N. (November 2019). Vries, Franciska (ed.). "Towards a predictive framework for biocrust mediation of plant performance: A meta‐analysis". Journal of Ecology. 107 (6): 2789–2807. doi:10.1111/1365-2745.13269. hdl:10261/202886. S2CID 202017609.
  19. ↑ Deines, Lynell; Rosentreter, Roger; Eldridge, David J.; Serpe, Marcelo D. (June 2007). "Germination and seedling establishment of two annual grasses on lichen-dominated biological soil crusts". Plant and Soil. 295 (1): 23–35. doi:10.1007/s11104-007-9256-y. S2CID 43263457.
  20. ↑ Bowker, Matthew A., Manuel Delgado-Baquerizo (8 December 2023). "Biocrusts protect the Great Wall of China from erosion". Science Advances. 9 (49). Retrieved 9 December 2023.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  21. ↑ Ferrenberg, Scott; Reed, Sasha C.; Belnap, Jayne (September 2015). "Climate change and physical disturbance cause similar community shifts in biological soil crusts". Proceedings of the National Academy of Sciences. 112 (39): 12116–12121. Bibcode:2015PNAS..11212116F. doi:10.1073/pnas.1509150112. PMC 4593113. PMID 26371310.
  22. ↑ Belnap, J; Phillips, SL; Miller, ME (2004). "Response of desert biological soil crusts to alteration in precipitation frequency". Oecologia. 141 (2): 306–316. Bibcode:2004Oecol.141..306B. doi:10.1007/s00442-003-1438-6. PMID 14689292. S2CID 27306844.
  23. ↑ Bowker, Matthew A. (March 2007). "Biological Soil Crust Rehabilitation in Theory and Practice: An Underexploited Opportunity". Restoration Ecology. 15 (1): 13–23. doi:10.1111/j.1526-100X.2006.00185.x. S2CID 51779646.
  24. ↑ Kheirfam, Hossein; Sadeghi, Seyed Hamidreza; Homaee, Mehdi; Zarei Darki, Behrouz (2017). "Quality improvement of an erosion-prone soil through microbial enrichment". Soil and Tillage Research. 165: 230–238. Bibcode:2017STilR.165..230K. doi:10.1016/j.still.2016.08.021.
  25. ↑ Kheirfam, Hossein; Sadeghi, Seyed Hamidreza; Zarei Darki, Behrouz; Homaee, Mehdi (May 2017). "Controlling rainfall-induced soil loss from small experimental plots through inoculation of bacteria and cyanobacteria". CATENA. 152: 40–46. Bibcode:2017Caten.152...40K. doi:10.1016/j.catena.2017.01.006.
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