Abstract
Winter snowfall is an important factor in the growth and development of biological soil crusts (BSCs) in temperate desert regions of China. In this study, intact algae, lichen, and moss crusts from the Gurbantunggut Desert were collected and exposed to five experimental treatments—snow removal (0S), snow decrease to half that of ambient conditions (1/2S), ambient snow (S), snow increase to 1.5 times that of ambient conditions (3/2S), and snow increase to twice that of ambient conditions (2S)—to evaluate the effect of snowfall on the ecophysiological parameters of the BSCs during the melt and at the end of the growing period. The results clearly identified differences in physiological and ecological indexes between snowfall manipulation treatments in March, and further found that the values of most of the ecophysiological indexes were influenced by snow removal/reduction treatments, the type of BSC and their interaction effect. The chlorophyll fluorescence parameters, chlorophyll content, and the rates of photosynthesis and respiration of all three types of crust declined because of decreased soil water content with decreased snow cover, and this effect would likely be even greater under conditions of decreased precipitation. The rates of photosynthesis and respiration of the main types of BSC were changed by variations in the winter snowfall, and confirmed the existence of long-term snowfall impacts on photosynthetic carbon fixation and biomass accumulation. These results provide a foundation for future studies to assess the potential effects of snowfall on the carbon sequestration of BSCs from arid and semi-arid regions.
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References
Angel R, Conrad R (2013) Elucidating the microbial resuscitation cascade in biological soil crusts following a simulated rain event. Environ Microbiol 15:2799–2815
Asner GP, Archer S, Hughes RF, Ansley RJ, Wessman CA (2003) Net changes in regional woody vegetation cover and carbon storage in Texas drylands. Global Change Biol 9:316–335
Belnap J, Gardner JS (1993) Soil microstructure in soils of the Colorado Plateau: the role of the cyanobacterium Microcoleus vaginatus. Great Basin Nat 53:40–47
Belnap J, Troxler T (2006) Soil lichen and moss cover and species richness can be highly dynamic: the effects of invasion by the annual exotic grass Bromus tectorum and the effects of climate on biological soil crusts. Appl Soil Ecol 32:63–76
Belnap J, Phillips SL, Miller ME (2004) Response of desert biological soil crusts to alterations in precipitation frequency. Oecologia 141:306–316
Bokhorst S, Metcalfe DB, Wardle DA (2013) Reduction in snow depth negatively affects decomposers but impact on decomposition rates is substrate dependent. Soil Biol Biochem 62:157–164
Bowker M, Reed SC, Belnap J, Phillips S (2002) Temporal variation in community composition, pigmentation, and Fv/Fm of desert cyanobacterial soil crusts. Microbial Ecol 43:13–25
Bowker MA, Belnap J, Davidson DW, Phillips SL (2005) Evidence for micronutrient limitation of biological soil crusts: importance to arid-lands restoration. Ecol Appl 15:1941–1951
Bowker MA, Belnap J, Chaudhary VB, Johnson NC (2008a) Revisiting classic erosion models: the strong influence of biological soil crusts. Soil Biol Biochem 40:2309–2316
Bowker MA, Johnson NC, Belnap J, Koch GW (2008b) Short-term monitoring of aridland lichen cover and biomass using photography and fatty acids. J Arid Environ 72:869–878
Bowker MA, Maestre FT, Escolar C (2010) Biological crusts as a model system for examining the biodiversity-ecosystem function relationship in soils. Soil Biol Biochem 42:405–417
Buckeridge KM, Grogan P (2008) Deepened snow alters soil microbial nutrient limitations in arctic birch hummock tundra. Appl Soil Ecol 39:210–222
Castillo-Monroy AP, Maestre FT, Rey A, Soliveres S, García-Palacios P (2011) Biological soil crust microsites are the main contributor to soil respiration in a semiarid ecosystem. Ecosystems 14:835–847
Chen R, Zhang Y, Li Y, Wei W, Zhang J, Wu N (2009) The variation of morphological features and mineralogical components of biological soil crusts in the Gurbantunggut Desert of Northwestern China. Environ Geol 57:1135–1143
Colesie C, Green TA, Haferkamp I, Büdel B (2014) Habitat stress initiates changes in composition, CO2 gas exchange and C-allocation as life traits in biological soil crusts. ISME J 8:2104–2115
Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable isotopes in plant ecology. Annu Rev Ecol Syst 33:507–559
Drahorad S, Felix-Henningsen P, Eckhardt KU, Leinweber P (2013) Spatial carbon and nitrogen distribution and organic matter characteristics of biological soil crusts in the Negev desert (Israel) along a rainfall gradient. J Arid Environ 94:18–26
Elbert W, Weber B, Burrows S, Steinkamp J, Budel B, Andreae MO, Poschl U (2012) Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat Geosci 5:459–462
Elise SG, Zachary TA, Roger LS, Mathew JR, Tony S, Suzanne DE, Jeremy JJ (2015) Altered snowfall and soil disturbance influence the early life stage transitions and recruitment of a native and invasive grass in a cold desert. Oecologia 177:595–606
Evans R, Belnap J (1999) Long-term consequences of disturbance on nitrogen dynamics in an arid ecosystem. Ecology 80:150–160
Evans RD, Lange OL (2003) Biological soil crusts and ecosystem nitrogen and carbon dynamics. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Springer, Berlin, pp 263–269
Fassnacht SR, Yang ZL, Snelgrove KR, Soulis ED, Kouwen N (2006) Effects of averaging and separating soil moisture and temperature in the presence of snow cover in a SVAT and hydrological model for a southern Ontario, Canada, watershed. J Hydrometeorol 7:298–304
Fearnehough W, Fullen M, Mitchell D, Trueman I, Zhang J (1998) Aeolian deposition and its effect on soil and vegetation changes on stabilised desert dunes in northern China. Geomorphology 23:171–182
Finch D (2012) Climate change in grasslands, shrublands, and deserts of the interior American West: a review and needs assessment Gen. Tech. Rep. RMRS-GTR-285. U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Fort Collins, CO, pp 4–35
Gombos Z, Wada H, Murata N (1994) The recovery of photosynthesis from low-temperature photoinhibition is accelerated by the unsaturation of membrane lipids: a mechanism of chilling tolerance. PNAS 91:8787–8791
Grote EE, Belnap J, Housman DC, Sparks JP (2010) Carbon exchange in biological soil crust communities under differential temperatures and soil water contents: implications for global change. Global Change Biol 16:2763–2774
Harper KT, Belnap J (2001) The influence of biological soil crusts on mineral uptake by associated vascular plants. J Arid Environ 47:347–357
Havaux M, Ksas B, Szewczyk A, Rumeau D, Franck F, Caffarri S, Triantaphylidès C (2009) Vitamin B6 deficient plants display increased sensitivity to high light and photo-oxidative stress. BMC Plant Biol 9:130
Housman DC, Powers HH, Collins AD, Belnap J (2006) Carbon and nitrogen fixation differ between successional stages of biological soil crusts in the Colorado Plateau and Chihuahuan Desert. J Arid Environ 66:620–634
Huxman TE, Smith MD, Fay PA, Knapp AK, Shaw MR, Loik ME, Pockman WT (2004) Convergence across biomes to a common rain-use efficiency. Nature 429:651–654
Janzen HH (2004) Carbon cycling in earth systems a soil science perspective. Agr Ecosyst Environ 104:399–417
Jarvis P, Rey A, Petsikos C, Wingate L (2007) Drying and wetting of Mediterranean soils stimulates decomposition and carbon dioxide emission: The ‘‘Birch effect’’. Tree Physiol 27:929–940
Jobbagy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10:423–436
Johansson M, Callaghan TV, Bosiö J, Åkerman HJ, Jackowicz-Korczynski M, Christensen TR (2013) Rapid responses of permafrost and vegetation to experimentally increased snow cover in sub-arctic Sweden. Environ Res Lett 8:035025
Johnson SL, Kuske CR, Carney TD, Housman DC, Gallegos-Graves LV, Belnap J (2012) Increased temperature and altered summer precipitation have differential effects on biological soil crusts in a dryland ecosystem. Global Change Biol 18:2583–2593
Kidron GJ, Yair A, Vonshak A, Abeliovich A (2003) Microbiotic crust control of runoff generation on sand dunes in the Negev desert. Water Resour Res 39:1108–1112
Knapp AK, Smith MD (2001) Variation among biomes in temporal dynamics of aboveground primary production. Science 291:481–484
Kolaksazov M, Laporte F, Goltsev V, Herzog M, Ananiev ED (2014) Effect of frost stress on chlorophyll a fluorescence and modulated 820 nm reflection in Arabis alpina population from Rila mountain. Genet Plant Physiol 4:44–56
Lan S, Wu L, Zhang D, Hu C, Liu Y (2011) Ethanol outperforms multiple solvents in the extraction of chlorophyll-a from biological soil crusts. Soil Biol Biochem 43:857–861
Leffler AJ, Welker JM (2013) Long-term increases in snow pack elevate leaf N and photosynthesis in Salix arctica: responses to a snow fence experiment in the High Arctic of NW Greenland. Environ Res Lett 8:25023–25032
Li XR, Wang XP, Li T, Zhang JG (2002) Microbiotic soil crust and its effect on vegetation and habitat on artificially stabilized desert dunes in Tengger Desert, North China. Biol Fert Soils 35:147–154
Li XR, Tian F, Jia RL, Zhang ZS, Liu LC (2010) Do biological soil crusts determine vegetation changes in sandy deserts? Implications for managing artificial vegetation. Hydrol Process 24:3621–3630
Li XR, Jia RL, Chen YW, Huang L, Zhang P (2011) Association of ant nests with successional stages of biological soil crusts in the Tengger Desert, Northern China. Appl Soil Ecol 47:59–66
Li XR, Zhang P, Su YG, Jia RL (2012) Carbon fixation by biological soil crusts following revegetation of sand dunes in arid desert regions of China: a four-year field study. Catena 97:119–126
Lindo Z, Nilsson MC, Gundale MJ (2013) Bryophyte-cyanobacteria associations as regulators of the northern latitude carbon balance in response to global change. Global Change Biol 19:2022–2035
Liu LC, LiS Z, Duan ZH, Wang T, Zhang ZS (2006) Effects of microbiotic crusts on dew deposition in the restored vegetation area at Shapotou, northwest China. J Hydrol 328:331–337
Liu Y, Li X, Xing Z, Zhao X, Pan Y (2013) Responses of soil microbial biomass and community composition to biological soil crusts in the revegetated areas of the Tengger Desert. Appl Soil Ecol 65:52–59
Lundell R, Saarinen T, Hänninen H (2010) Effects of snowmelt on the springtime photosynthesis of the evergreen dwarf shrub Vaccinium vitis-idaea. Plant Ecol Divers 3:121–130
Maestre FT, Huesca M, Zaady E, Bautista S, Cortina J (2002) Infiltration, penetration resistance and microphytic crust composition in contrasted microsites within a Mediterranean semi-arid steppe. Soil Biol Biochem 34:895–898
Mager DM (2010) Carbohydrates in cyanobacterial soil crusts as a source of carbon in the southwest Kalahari, Botswana. Soil Bio Biochem 42:313–318
Mayland HF, Mcintosh TH (1966) Availability of biologically fixed atmospheric nitrogen-15 to higher plants. Nature 209:421–422
Miralles I, Trasar-Cepeda C, Leirós MC, Gil-Sotres F (2013) Labile carbon in biological soil crusts in the Tabernas desert, SE Spain. Soil Biol Biochem 58:1–8
Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421
Palmqvist K (2000) Carbon economy in lichens. New Phytol 148:11–36
Pattison RR, Welker JM (2014) Differential ecophysiological response of deciduous shrubs and a graminoid to long-term experimental snow reductions and additions in moist acidic tundra, Northern Alaska. Oecologia 174:339–350
Perata P, Armstrong W, Voesenek LACJ (2011) Plants and flooding stress. New Phytol 190:269–273
Pointing SB, Belnap J (2012) Microbial colonization and controls in dryland systems. Nat Rev Microbiol 10:551–562
Rajeev L, da Rocha UN, Klitgord N, Luning EG, Fortney J, Axen SD, Mukhopadhyay A (2013) Dynamic cyanobacterial response to hydration and dehydration in a desert biological soil crust. ISME J 7:2178–2191
Rogers MC, Sullivan PF, Welker JM (2011) Evidence of nonlinearity in the response of net ecosystem CO2 exchange to increasing levels of winter snow depth in the high Arctic of northwest Greenland. Arct Antarct Alp Res 43:95–106
Schimel JP, Bilbrough C, Welker JM (2004) Increased snow depth affects microbial activity and nitrogen mineralization in two Arctic tundra communities. Soil Biol Biochem 36:217–227
Segawa T, Miyamoto K, Ushida K, Agata K, Okada N, Kohshima S (2005) Seasonal change in bacterial flora and biomass in mountain snow from the Tateyama Mountains, Japan, analyzed by 16S rRNA gene sequencing and real-time PCR. Appl Environ Microbiol 71:123–130
Serpe MD, Roberts E, Eldridge DJ, Rosentreter R (2013) Bromus tectorum litter alters photosynthetic characteristics of biological soil crusts from a semiarid shrubland. Soil Biol Biochem 60:220–230
Sponseller RA (2007) Precipitation pulses and soil CO2 flux in a Sonoran Desert ecosystem. Global Change Biol 13:426–436
Starr G, Oberbauer SF, Ahlquist LE (2008) The photosynthetic response of Alaskan tundra plants to increased season length and soil warming. Arct Antarct Alp Res 40:181–191
Stevens CJ, Dupre C, Dorland E, Gaudnik C, Gowing DJ, Bleeker A, Dise NB (2010) Nitrogen deposition threatens species richness of grasslands across Europe. Env Pollut 158:2940–2945
Su YG, Wu L, Zhou ZB, Liu YB, Zhang YM (2013) Carbon flux in deserts depends on soil cover type: a case study in the Gurbantunggute desert, North China. Soil Biol Biochem 58:332–340
Theocharis A, Clément C, Barka EA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235:1091–1105
Torp M, Witzell J, Baxter R, Olofsson J (2010) The effect of snow on plant chemistry and invertebrate herbivory: experimental manipulations along a natural snow gradient. Ecosystems 13:741–751
Viles HA (2008) Understanding dryland landscape dynamics: do biological crusts hold the key? Geogr Compass 2:899–919
Wang XQ, Jiang J, Wang YC, Luo W, Song C, Chen J (2006) Responses of ephemeral plant germination and growth to water and heat conditions in the southern part of Gurbantunggut Desert. Chin Sci Bull 51:110–116
Wang WB, Liu YD, Li DH, Hu CX, Rao BQ (2009) Feasibility of cyanobacterial inoculation for biological soil crusts formation in desert area. Soil Biol Biochem 41:926–929
West NE (1990) Structure and function of soil microphytic crusts in wildland ecosystems of arid and semi-arid regions. Adv Ecol Res 20:179–223
Zelikova TJ, Housman DC, Grote EE, Neher DA, Belnap J (2012) Warming and increased precipitation frequency on the Colorado Plateau: implications for biological soil crusts and soil processes. Plant Soil 355:265–282
Zhang J, Zhang YM (2014) Diurnal variations of chlorophyll fluorescence and CO2 exchange of biological soil crusts in different successional stages in the Gurbantunggut Desert of northwestern China. Ecol Res 29:289–298
Zhang YM, Chen J, Wang L, Wang XQ, Gu ZH (2007) The spatial distribution patterns of biological soil crusts in the Gurbantunggut Desert, Northern Xinjiang, China. J Arid Env 68:599–610
Zhang BC, Zhang YM, Zhao JC, Wu N, Chen R, Zhang J (2009) Microalgal species variation at different successional stages in biological soil crusts of the Gurbantunggut Desert, Northwestern China. Biol Fert Soils 45:539–547
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This study was supported by the National Basic Research Program of China (2013CB429901) and the National Natural Science Foundation of China (Grant Nos. 31230014, 41371100, 41271061).
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Zhao, R., Hui, R., Wang, Z. et al. Winter snowfall can have a positive effect on photosynthetic carbon fixation and biomass accumulation of biological soil crusts from the Gurbantunggut Desert, China. Ecol Res 31, 251–262 (2016). https://doi.org/10.1007/s11284-016-1335-1
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DOI: https://doi.org/10.1007/s11284-016-1335-1