Small-Scale Spatial Heterogeneity of Photosynthetic Fluorescence Associated with Biological Soil Crust Succession in the Tengger Desert, China

  • Shubin Lan
  • Andrew David Thomas
  • Stephen Tooth
  • Li Wu
  • Chunxiang HuEmail author
Soil Microbiology


In dryland regions, biological soil crusts (BSCs) have numerous important ecosystem functions. Crust species and functions are, however, highly spatially heterogeneous and remain poorly understood at a range of scales. In this study, chlorophyll fluorescence imaging was used to quantify millimeter-scale patterns in the distribution and activity of photosynthetic organisms in BSCs of different successional stages (including cyanobacterial, lichen, moss three main successional stages and three intermixed transitional stages) from the Tengger Desert, China. Chlorophyll fluorescence images derived from the Imaging PAM (Pulse Amplitude Modulation) showed that with the succession from cyanobacterial to lichen and to moss crusts, crust photosynthetic efficiency (including the maximum and effective photosynthetic efficiency, respectively) and fluorescence coverage increased significantly (P < 0.05), and that increasing photosynthetically active radiation (PAR) reduced the effective photosynthetic efficiency (Yield). The distribution of photosynthetic organisms in crusts determined Fv/Fm (ratio of variable fluorescence to maximum fluorescence) frequency pattern, although the photosynthetic heterogeneity (SHI index) was not significantly different (P > 0.05) between cyanobacterial and moss crusts, and showed a unimodal pattern of Fv/Fm values. In contrast, photosynthetic heterogeneity was significantly higher in lichen, cyanobacteria-moss and lichen-moss crusts (P < 0.05), with a bimodal pattern of Fv/Fm values. Point pattern analysis showed that the distribution pattern of chlorophyll fluorescence varied at different spatial scales and also among the different crust types. These new results provide a detailed (millimeter-scale) insight into crust photosynthetic mechanisms and spatial distribution patterns associated with their community types. Collectively, this information provides an improved theoretical basis for crust maintenance and management in dryland regions.


Drylands Biological soil crusts Chlorophyll fluorescence Photosynthesis Heterogeneity Succession 


Funding Information

This study was kindly supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (No. XDA17010502), National Natural Science Foundation of china (Nos. 31670456 and 31300322), Youth Innovation Promotion Association CAS (No. 2017385), and European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie Grant (No. 663830). The paper was prepared while S. Lan was a Sêr Cymru Fellow at Aberystwyth University, and L. Wu was a Visiting Scholar at Aberystwyth University.

Supplementary material

248_2019_1356_MOESM1_ESM.docx (132 kb)
ESM 1 (DOCX 131 kb)


  1. 1.
    Hu C, Gao K, Whitton BA (2012) Semi-arid regions and deserts. In: Whitton BA (ed) Ecology of cyanobacteria II: their diversity in space and time. Springer Science+Business Media, Dordrecht, pp 345–369CrossRefGoogle Scholar
  2. 2.
    Lan S, Wu L, Zhang D, Hu C (2015) Analysis of environmental factors determining development and succession in biological soil crusts. Sci Total Environ 538:492–499CrossRefGoogle Scholar
  3. 3.
    Hu C, Liu Y, Song L, Zhang D (2002) Effect of desert soil algae on the stabilization of fine sands. J Appl Phycol 14:281–292CrossRefGoogle Scholar
  4. 4.
    Lan S, Wu L, Zhang D, Hu C (2012) Successional stages of biological soil crusts and their microstructure variability in Shapotou region (China). Environ Earth Sci 65(1):77–88CrossRefGoogle Scholar
  5. 5.
    Hu C, Zhang D, Huang Z, Liu Y (2003) The vertical microdistribution of cyanobacteria and green algae within desert crusts and the development of the algal crusts. Plant Soil 257:97–111CrossRefGoogle Scholar
  6. 6.
    Lan S, Zhang Q, Wu L, Liu Y, Zhang D, Hu C (2014) Artificially accelerating the reversal of desertification: cyanobacterial inoculation facilitates the succession of vegetation communities. Environ Sci Technol 48:307–315CrossRefGoogle Scholar
  7. 7.
    Belnap J, Gillette DA (1998) Vulnerability of desert biological soil crusts to wind erosion: the influences of crust development, soil texture, and disturbance. J Arid Environ 39(2):133–142CrossRefGoogle Scholar
  8. 8.
    Elliott DR, Thomas AD, Hoon SR, Sen R (2014) Niche partitioning of bacterial communities in biological crusts and soils under grasses, shrubs and trees in the Kalahari. Biodivers Conserv 23:1709–1733CrossRefGoogle Scholar
  9. 9.
    Eldridge DJ, Zaady E, Shachak M (2000) Infiltration through three contrasting biological soil crusts in patterned landscapes in the Negev, Israel. Catena 40:323–336CrossRefGoogle Scholar
  10. 10.
    Lan S, Hu C, Rao B, Wu L, Zhang D, Liu Y (2010) Non-rainfall water sources in the topsoil and their changes during formation of man-made algal crusts at the eastern edge of Qubqi Desert, Inner Mongolia. Sci China Life Sci 53:1135–1141CrossRefGoogle Scholar
  11. 11.
    Li X, Jia X, Long L, Zerbe S (2005) Effects of biological soil crusts on seed bank, germination and establishment of two annual plant species in the Tengger Desert (N China). Plant Soil 277:375–385CrossRefGoogle Scholar
  12. 12.
    Li X, Jia R, Chen Y, 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 47:59–66CrossRefGoogle Scholar
  13. 13.
    Pickett STA, Cadenasso ML (1995) Landscape ecology: spatial heterogeneity in ecological systems. Science 269:331–334CrossRefGoogle Scholar
  14. 14.
    Wiegand T, Moloney KA (2004) Rings, circles and null-models for point pattern analysis in ecology. Oikos 104:209–229CrossRefGoogle Scholar
  15. 15.
    Shen G, He F, Waagepetersen R, Sun I, Hao Z, Chen Z, Yu M (2013) Quantifying effects of habitat heterogeneity and other clustering processes on spatial distributions of tree species. Ecology 94(11):2436–2443CrossRefGoogle Scholar
  16. 16.
    Bowker MA, Belnap J, Davidson DW, Goldstein H (2006) Correlates of biological soil crust abundance across a continuum of spatial scales: support for a hierarchical concep tualmodel. J Appl Ecol 43:152–163CrossRefGoogle Scholar
  17. 17.
    Baillod AB, Tscharntke T, Clough Y, Batáry P (2017) Landscape-scale interactions of spatial and temporal cropland heterogeneity drive biological control of cereal aphids. J Appl Ecol 54:1804–1813CrossRefGoogle Scholar
  18. 18.
    Liu Y, Cockell CS, Wang G, Hu C, Chen L, De Philippis R (2008) Control of lunar and Martian dust-experimental insights from artificial and natural cyanobacterial and algal crusts in the desert of Inner Mongolia, China. Astrobiology 8:75–86CrossRefGoogle Scholar
  19. 19.
    Zaady E, Kuhn U, Wilske B, Sandoval-Soto L, Kesselmeier J (2000) Patterns of CO2 exchange in biological soil crusts of successional age. Soil Biol Biochem 32:959–966CrossRefGoogle Scholar
  20. 20.
    Zaady E, Karnieli A, Shachak M (2007) Applying a field spectroscopy technique for assessing successional trends of biological soil crusts in a semi-arid environment. J Arid Environ 70:463–477CrossRefGoogle Scholar
  21. 21.
    Kidron GJ, Vonshak A, Abeliovich A (2008) Recovery rates of microbiotic crusts within a dune ecosystem in the Negev Desert. Geomorphology 100:444–452CrossRefGoogle Scholar
  22. 22.
    Viles HA (2008) Understanding dryland landscape dynamics: do biological crusts hold the key? Geogr Compass 2(3):899–919CrossRefGoogle Scholar
  23. 23.
    Garcia-Pichel F, Belnap J (1996) Microenvironments and microscale productivity of cyanobacterial desert crusts. J Phycol 32:774–782CrossRefGoogle Scholar
  24. 24.
    Bowker MA, Belnap J, Davidson DW, Phillips SL (2005) Evidence for micronutrient limitation of biological soil crusts: importance to arid-lands restoration. Ecol Appl 15:1941–1951CrossRefGoogle Scholar
  25. 25.
    Abed RMM, Lam P, De Beer D, Stief P (2013) High rates of denitrification and nitrous oxide emission in arid biological soil crusts from the Sultanate of Oman. ISME J 7:1862–1875CrossRefGoogle Scholar
  26. 26.
    Lan S, Wu L, Zhang D, Hu C (2017) Biological soil crust community types differ in photosynthetic pigment composition, fluorescence and carbon fixation in Shapotou region of China. Appl Soil Ecol 111:9–16CrossRefGoogle Scholar
  27. 27.
    Wu L, Lan S, Zhang D, Hu C (2011) Small-scale vertical distribution of algae and structure of lichen soil crusts. Microb Ecol 62:715–724CrossRefGoogle Scholar
  28. 28.
    Wu L, Lan S, Zhang D, Hu C (2013) Functional reactivation of photosystem II in lichen soil crusts after long-term desiccation. Plant Soil 369:177–186CrossRefGoogle Scholar
  29. 29.
    Swap RJ, Annegarn HJ, Suttles JT et al (2002) The Southern African Regional Science Initiative (SAFARI 2000): overview of the dry season field campaign. S Afr J Sci 98(3):125–130Google Scholar
  30. 30.
    Dean WRJ, Milton SJ, Jeltsch F (1999) Large trees, fertile islands, and birds in arid savanna. J Arid Environ 41:61–78CrossRefGoogle Scholar
  31. 31.
    Hu H, Li R, Wei Y, Zhu H, Chen J, Shi Z (1980) Freshwater algae in China. Shanghai Science and Technology Press, Shanghai (in Chinese)Google Scholar
  32. 32.
    Rosentreter R, Bowker M, Belnap J (2007) A Field Guide to Biological Soil Crusts of Western U.S. Drylands. U.S. Government Printing Office, DenverGoogle Scholar
  33. 33.
    Ohad I, Raanan H, Keren N, Tchernov D, Kaplan A (2010) Light-induced changes within photosystem II protects Microcoleus sp. in biological desert sand crusts against excess light. PLoS One 5(6):e11000CrossRefGoogle Scholar
  34. 34.
    Wu L, Lei Y, Lan S, Hu C (2017) Photosynthetic recovery and acclimation to excess light intensity in the rehydrated lichen soil crusts. PLoS One 12(3):e0172537CrossRefGoogle Scholar
  35. 35.
    Heber U, Bilger W, Shuvalov VA (2006) Thermal energy dissipation in reaction centres and in the antenna of photosystem II protects desiccated poikilohydric mosses against photo-oxidation. J Exp Bot 57:2993–3006CrossRefGoogle Scholar
  36. 36.
    Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113CrossRefGoogle Scholar
  37. 37.
    Green TGA, Schlensog M, Sancho LG, Winkler JB, Broom FD, Schroeter B (2002) The photobiont determines the pattern of photosynthetic activity within a single lichen thallus containing cyanobacterial and green algal sectors (photosymbiodeme). Oecologia 130:191–198CrossRefGoogle Scholar
  38. 38.
    Hu H, Wang X (2008) Unified index to quantifying heterogeneity of complex networks. Physica A 387(14):3769–3780CrossRefGoogle Scholar
  39. 39.
    Ripley BD (1976) The second-order analysis of stationary point processes. J Appl Probab 13:255–266CrossRefGoogle Scholar
  40. 40.
    Shi P, Ge F, Yang Q, Wang J (2009) A new algorithm of the edge correction in the point pattern analysis and its application. Acta Ecol Sin 29(2):804–809Google Scholar
  41. 41.
    Wiegand T, Moloney KA (2014) A handbook of spatial point pattern analysis in ecology. Chapman and Hall/CRC press, Boca Raton, FLGoogle Scholar
  42. 42.
    Law R, Illian J, Burslem DFRP, Gratzer G, Gunatilleke CVS, Gunatilleke IAUN (2009) Ecological information from spatial patterns of plants: insights from point process theory. J Ecol 97:616–628CrossRefGoogle Scholar
  43. 43.
    Lan S, Wu L, Zhang D, Hu C (2013) Assessing level of development and successional stages in biological soil crusts with biological indicators. Microb Ecol 66:394–403CrossRefGoogle Scholar
  44. 44.
    Müller P, Li X, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566CrossRefGoogle Scholar
  45. 45.
    Mugnai G, Rossi F, Felde VJ, Colesie C, Büdel B, Peth S, Kaplan A, De Philippis R (2018) Development of the polysaccharidic matrix in biocrusts induced by a cyanobacterium inoculated in sand microcosms. Biol Fertil Soils 54:27–40CrossRefGoogle Scholar
  46. 46.
    Wu L, Zhang G, Lan S, Zhang D, Hu C (2013) Microstructures and photosynthetic diurnal changes in the different types of lichen soil crusts. Eur J Soil Biol 59:48–53CrossRefGoogle Scholar
  47. 47.
    Lan S, Wu L, Zhang D, Hu C (2012) Composition of photosynthetic organisms and diurnal changes of photosynthetic efficiency in algae and moss crusts. Plant Soil 351:325–336CrossRefGoogle Scholar
  48. 48.
    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 66:620–634CrossRefGoogle Scholar
  49. 49.
    Bowker MA, Reed SC, Belnap J, Phillips SL (2002) Temporal variation in community composition, pigmentation, and Fv/Fm of desert cyanobacterial soil crusts. Microb Ecol 43:13–25CrossRefGoogle Scholar
  50. 50.
    Belnap J (1993) Recovery rates of cryptobiotic crusts: inoculant use and assessment methods. Great Basin Nat 53:89–95Google Scholar
  51. 51.
    Li X, Xiao H, He M, Zhang J (2006) Sand barriers of straw checkerboards for habitat restoration in extremely arid desert regions. Ecol Eng 28:149–157CrossRefGoogle Scholar
  52. 52.
    Thomas AD (2012) Impact of grazing intensity on seasonal variations in SOC and soil CO2 efflux in two semiarid grasslands in southern Botswana. Philos T Roy Soc B 367:3076–3086CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Algal Biology, Institute of HydrobiologyChinese Academy of SciencesWuhanChina
  2. 2.Department of Geography and Earth SciencesAberystwyth UniversityAberystwythUK
  3. 3.School of Resources and Environmental EngineeringWuhan University of TechnologyWuhanChina

Personalised recommendations