Effects of changes in precipitation pattern and of seaweed fertilizer addition on plant traits and biological soil crusts

  • Mutian Yuan
  • Huijie XiaoEmail author
  • Ruoshui Wang
  • Yuanjun Duan
  • Qiqi Cao


In arid areas precipitation patterns and soil nutrient determine plant survival. To study the effect of fertilizer addition on plant traits and on biological soil crusts under different rainfall intervals we collected and sowed the seeds of three typical psammophyte species from a natural community in China’s Mu Us Desert, and raised their seedlings in pots. During the growing season we added commercial seaweed fertilizer to the pots and irrigated the plants at different intervals. After one growing season we measured plant traits and the biomass of biological soil crusts, and soil nutrient contents. Seaweed fertilizer increased biomass production. The combined effects of seaweed fertilizer and rainfall interval were related to the life history attributes of the species. For a given fertilizer addition, changing the rainfall interval from 3 to 15 days increased the Agriophyllum squarrosum and Achnatherum splendens biomass, but decreased Glycyrrhiza uralensis biomass. Seaweed fertilizer significantly affected plant traits, but the effects of the rainfall interval on plant traits were not significant. Fertilizer addition increased the soil organic carbon and total nitrogen. Fertilizer addition also promoted biological soil crusts and enriched their total nitrogen content. Structural equation modeling showed that the organic carbon, total nitrogen, and chlorophyll a content of the biological crusts played different roles in biomass production of the three species. Soil carbon and nitrogen affected biological soil crusts more than they affected plant biomass production. Our results show that seaweed fertilizer can promote plant growth and biological crust development, making it useful for ecosystem restoration in arid and semi-arid regions.


Biomass production Plant traits Biological soil crusts Soil organic carbon Soil total nitrogen Structural equation modeling 



We thank the staff at the Yanchi Research Station for their help with field work and Geoff Hart (Pointe-Claire, Canada) for the language editing on the earlier edition of this manuscript. This study was supported by the Fundamental Research Funds for the Central Universities (NO.2015ZCQ-SB-03).


  1. Arioli T, Mattner SW, Winberg PC (2015) Applications of seaweed extracts in Australian agriculture: past, present and future. J Appl Phycol 27:2007–2015CrossRefGoogle Scholar
  2. Bai Y, Wu J, Clark CM, Naeem S, Pan Q, Huang J, Zhang L, Han X (2010) Tradeoffs and thresholds in the effects of nitrogen addition on biodiversity and ecosystem functioning: evidence from inner Mongolia Grasslands. Glob Chang Biol 16:358–372CrossRefGoogle Scholar
  3. Bai Y, She W, Michalet R, Zheng J, Qin S, Zhang Y, Ohlemuller R (2018) Benefactor facilitation and beneficiary feedback effects drive shrub-dominated community succession in a semi-arid dune ecosystem. Appl Veg Sci 21:595–606CrossRefGoogle Scholar
  4. Beier C, Beierkuhnlein C, Wohlgemuth T, Penuelas J, Emmett B, Korner C, de Boeck H, Christensen JH, Leuzinger S, Janssens IA, Hansen K (2012) Precipitation manipulation experiments—challenges and recommendations for the future. Ecol Lett 15:899–911CrossRefGoogle Scholar
  5. Belnap J (1993) Recovery rates of cryptobiotic crusts: inoculant use and assessment methods. Great Basin Naturalist 53:89–95Google Scholar
  6. Belnap J (2006) The potential roles of biological soil crusts in dryland hydrologic cycles. Hydrol Process 20:3159–3178CrossRefGoogle Scholar
  7. Belnap J, Eldridge D (2003) Disturbance and recovery of biological soil crusts. Springer-Verlag, BerlinGoogle Scholar
  8. Biederman JA, Scott RL, Goulden ML, Vargas R, Litvak ME, Kolb TE, Yepez EA, Oechel WC, Blanken PD, Bell TW, Garatuza-Payan J, Maurer GE, Dore S, Burns SP (2016) Terrestrial carbon balance in a drier world: the effects of water availability in southwestern North America. Glob Chang Biol 22:1867–1879CrossRefGoogle Scholar
  9. Bowker MA (2007) Biological soil crust rehabilitation in theory and practice: an underexploited opportunity. Restor Ecol 15:13–23CrossRefGoogle Scholar
  10. Chamizo S, Cantón Y, Miralles I, Domingo F (2012) Biological soil crust development affects physicochemical characteristics of soil surface in semiarid ecosystems. Soil Biol Biochem 49:96–105CrossRefGoogle Scholar
  11. Chen X, Duan Z (2014) Impacts of soil crusts on soil physicochemical characteristics in different rainfall zones of the arid and semi-arid desert regions of northern China. Environ Earth Sci 73:3335–3347CrossRefGoogle Scholar
  12. Chen L, Xie Z, Hu C, Li D, Wang G, Liu Y (2006) Man-made desert algal crusts as affected by environmental factors in Inner Mongolia, China. J Arid Environ 67:521–527CrossRefGoogle Scholar
  13. Craigie JS (2010) Seaweed extract stimuli in plant science and agriculture. J Appl Phycol 23:371–393CrossRefGoogle Scholar
  14. Didiano TJ, Johnson MT, Duval TP (2016) Disentangling the effects of precipitation amount and frequency on the performance of 14 grassland species. PLoS One 11:e0162310CrossRefGoogle Scholar
  15. Dong G, Guo J, Chen J, Sun G, Gao S, Hu L, Wang Y (2011) Effects of spring drought on carbon sequestration, evapotranspiration and water use efficiency in the Songnen meadow steppe in Northeast China. Ecohydrology 4:211–224CrossRefGoogle Scholar
  16. Elmi AA, West CP (1995) Endophyte infection effects on stomatal conductance, osmotic adjustment and drought recovery of tall fescue. New Phytol 131:61–67CrossRefGoogle Scholar
  17. Feng W, Zhang YQ, Wu B, Zha TS, Jia X, Qin SG, Shao CX, Liu JB, Lai ZR, Fa KY (2013) Influence of disturbance on soil respiration in biologically crusted soil during the dry season. Sci World J 2013:408560Google Scholar
  18. Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  19. Groisman PY, Karl TR, Easterling DR, Knight RW, Jamason PF, Hennessy KJ, Suppiah R, Page CM, Wibig J, Fortuniak K, Razuvaev VN, Douglas A, Førland E, Zhai P-M (1999) Changes in the probability of heavy precipitation: important indicators of climatic change. Clkimatic Change 42:243–283Google Scholar
  20. Harper KT, Belnap J (2001) The influence of biological soil crusts on mineral uptake by associated vascular plants. J Arid Environ 47:347–357CrossRefGoogle Scholar
  21. Heisler-White JL, Knapp AK, Kelly EF (2008) Increasing precipitation event size increases aboveground net primary productivity in a semi-arid grassland. Oecologia 158:129–140CrossRefGoogle Scholar
  22. Herrera F, Castillo JE, Chica AF, López BL (2008) Use of municipal solid waste compost (MSWC) as a growing medium in the nursery production of tomato plants. Bioresour Technol 99:287–296CrossRefGoogle Scholar
  23. Hurek T, Handley LL, Reinhold-Hurek B, Piche Y (2002) Azoarcus grass endophytes contribute fixed nitrogen to the plant in an unculturable state. Mol Plant-Microbe Interact 15:233–242CrossRefGoogle Scholar
  24. Illera-Vives M, Seoane Labandeira S, Iglesias Loureiro L, López-Mosquera ME (2017) Agronomic assessment of a compost consisting of seaweed and fish waste as an organic fertilizer for organic potato crops. J Appl Phycol 29:1663–1671CrossRefGoogle Scholar
  25. Jia X, Zha TS, Wu B, Zhang YQ, Gong JN, Qin SG, Chen GP, Qian D, Kellomäki S, Peltola H (2014) Biophysical controls on net ecosystem CO2 exchange over a semiarid shrubland in Northwest China. Biogeosciences 11:4679–4693CrossRefGoogle Scholar
  26. Jia X, Zha T, Gong J, Wang B, Zhang Y, Wu B, Qin S, Peltola H (2016) Carbon and water exchange over a temperate semi-arid shrubland during three years of contrasting precipitation and soil moisture patterns. Agric For Meteorol 228-229:120–129CrossRefGoogle Scholar
  27. Jongen M, Pereira JS, Aires LMI, Pio CA (2011) The effects of drought and timing of precipitation on the inter-annual variation in ecosystem-atmosphere exchange in a Mediterranean grassland. Agric For Meteorol 151:595–606CrossRefGoogle Scholar
  28. Khan W, Zhai R, Souleimanov A, Critchley AT, Smith DL, Prithiviraj B (2012) Commercial extract of Ascophyllum nodosum improves root colonization of alfalfa by its bacterial symbiont Sinorhizobium meliloti. Commun Soil Sci Plant Anal 43:2425–2436Google Scholar
  29. Khan W, Palanisamy R, Critchley AT, Smith DL, Papadopoulos Y, Prithiviraj B (2013) Ascophyllum nodosum extract and its organic fractions stimulate Rhizobium root nodulation and growth of Medicago sativa (Alfalfa). Commun Soil Sci Plant Anal 44:900–908Google Scholar
  30. Kidron GJ, Vonshak A, Abeliovich A (2009) Microbiotic crusts as biomarkers for surface stability and wetness duration in the Negev Desert. Earth Surf Process Landf 34:1594–1604CrossRefGoogle Scholar
  31. Knapp AK, Smith MD (2001) Variation among biomes in temporal dynamics of aboveground primary production. Science 291:481–484CrossRefGoogle Scholar
  32. Knops J, Bradley K, Wedin D (2002) Mechanisms of plant species impacts on ecosystem nitrogen cycling. Ecol Lett 5:454–466CrossRefGoogle Scholar
  33. Kumari R, Kaur I, Bhatnagar AK (2011) Effect of aqueous extract of Sargassum johnstonii Setchell & Gardner on growth, yield and quality of Lycopersicon esculentum Mill. J Appl Phycol 23:623–633Google Scholar
  34. Kumari R, Kaur I, Bhatnagar AK (2012) Enhancing soil health and productivity of Lycopersicon esculentum Mill. using Sargassum johnstonii Setchell & Gardner as a soil conditioner and fertilizer. J Appl Phycol 25:1225–1235CrossRefGoogle Scholar
  35. Lan S, Wu L, Zhang D, Hu C (2011) Successional stages of biological soil crusts and their microstructure variability in Shapotou region (China). Environ Earth Sci 65:77–88CrossRefGoogle Scholar
  36. 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
  37. Lauenroth WK, Sala OE (1992) Long-term forage production of North American shortgrass steppe. Ecol Appl 2:397–403CrossRefGoogle Scholar
  38. Layek J, Das A, Idapuganti RG, Sarkar D, Ghosh A, Zodape ST, Lal R, Yadav GS, Panwar AS, Ngachan S, Meena RS (2017) Seaweed extract as organic bio-stimulant improves productivity and quality of rice in eastern Himalayas. J Appl Phycol 30:547–558CrossRefGoogle Scholar
  39. Liu Y, Pan Q, Zheng S, Bai Y, Han X (2012) Intra-seasonal precipitation amount and pattern differentially affect primary production of two dominant species of Inner Mongolia grassland. Acta Oecol 44:2–10CrossRefGoogle Scholar
  40. Liu J, Zhang Y, Feng W, Qin S, Wang L, She W (2016a) Influences of exogenous additives on culture of biological soil crusts (in Chinese, with English summary). J Beijing For Univ 38:100–107Google Scholar
  41. Liu J, Zhang Y, Qin S, Feng W, Sun Y, Wang L, Bai Y (2016b) Sand fixation experiment of Artemisia sphaerocephala Krasch. gum with different concentrations (in Chinese with English summary). Trans Chin Soc Agric Eng 32:149–155Google Scholar
  42. Liu P, Zha T, Jia X, Wang B, Guo X, Zhang Y, Wu B, Yang Q, Peltola H (2016c) Diurnal freeze-thaw cycles modify winter soil respiration in a desert shrub-land ecosystem. Forests 7:161CrossRefGoogle Scholar
  43. Lötze E, Hoffman EW (2015) Nutrient composition and content of various biological active compounds of three South African-based commercial seaweed biostimulants. J Appl Phycol 28:1379–1386CrossRefGoogle Scholar
  44. Maestre FT, Martin N, Diez B, Lopez-Poma R, Santos F, Luque I, Cortina J (2006) Watering, fertilization, and slurry inoculation promote recovery of biological crust function in degraded soils. Microb Ecol 52:365–377CrossRefGoogle Scholar
  45. Mansori M, Chernane H, Latique S, Benaliat A, Hsissou D, El Kaoua M (2014) Seaweed extract effect on water deficit and antioxidative mechanisms in bean plants (Phaseolus vulgaris L.). J Appl Phycol 27:1689–1698CrossRefGoogle Scholar
  46. Mzibra A, Aasfar A, El Arroussi H, Khouloud M, Dhiba D, Kadmiri IM, Bamouh A (2018) Polysaccharides extracted from Moroccan seaweed: a promising source of tomato plant growth promoters. J Appl Phycol 30:2953–2962CrossRefGoogle Scholar
  47. Nelson DW, Sommers LE, Sparks DL, Page AL, Helmke PA, Loeppert RH, Soltanpour PN, Tabatabai MA, Johnston CT, Sumner ME (1996) Total carbon, organic carbon, and organic matter. Methods Soil Anal 9:961–1010Google Scholar
  48. Pietrasiak N, Regus JU, Johansen JR, Lam D, Sachs JL, Santiago LS (2013) Biological soil crust community types differ in key ecological functions. Soil Biol Biochem 65:168–171CrossRefGoogle Scholar
  49. Pramanick B, Brahmachari K, Mahapatra BS, Ghosh A, Ghosh D, Kar S (2017) Growth, yield and quality improvement of potato tubers through the application of seaweed sap derived from the marine alga Kappaphycus alvarezii. J Appl Phycol 29:3253–3260Google Scholar
  50. Robertson TR, Bell CW, Zak JC, Tissue DT (2009) Precipitation timing and magnitude differentially affect aboveground annual net primary productivity in three perennial species in a Chihuahuan Desert grassland. New Phytol 181:230–242CrossRefGoogle Scholar
  51. Rouphael Y, De Micco V, Arena C, Raimondi G, Colla G, De Pascale S (2016) Effect of Ecklonia maxima seaweed extract on yield, mineral composition, gas exchange, and leaf anatomy of zucchini squash grown under saline conditions. J Appl Phycol 29:459–470CrossRefGoogle Scholar
  52. Sala O, Lauenroth W, Parton W (1992) Long-term soil water dynamics in the shortgrass steppe. Ecology 73:1175–1181CrossRefGoogle Scholar
  53. Salvagiotti F, Cassman KG, Specht JE, Walters DT, Weiss A, Dobermann A (2008) Nitrogen uptake, fixation and response to fertilizer N in soybeans: a review. Field Crop Res 108:1–13CrossRefGoogle Scholar
  54. Sathya B, Indu H, Seenivasan R, Geetha S (2010) Influence of seaweed liquid fertilizer on the growth and biochemical composition of legume crop, Cajanus cajan (L.) Mill sp. J Phytology 2:50–63Google Scholar
  55. Shaw MR, Zavaleta ES, Chiariello NR, Cleland EE, Mooney HA, Field CB (2002) Grassland responses to global environmental changes suppressed by elevated CO2. Science 298:1987–1990CrossRefGoogle Scholar
  56. Shipley B (2000) Cause and correlation in biology: correlation in biology: a user’s guide to path analysis, structural equations, and causal inference. Q Rev Biol 82:646–649Google Scholar
  57. Singh S, Singh MK, Pal SK, Trivedi K, Yesuraj D, Singh CS, Anand KGV, Chandramohan M, Patidar R, Kubavat D, Zodape ST, Ghosh A (2015) Sustainable enhancement in yield and quality of rain-fed maize through Gracilaria edulis and Kappaphycus alvarezii seaweed sap. J Appl Phycol 28:2099–2112CrossRefGoogle Scholar
  58. Sparks DL, Page AL, Helmke PA, Loeppert RH, Soltanpour PN, Tabatabai MA, Johnston CT, Sumner ME (1996) Methods of soil analysis. Part 3 - chemical methods. American Society of Agronomy, MadisonGoogle Scholar
  59. Stirk WA, Tarkowská D, Turečová V, Strnad M, van Staden J (2013) Abscisic acid, gibberellins and brassinosteroids in Kelpak®, a commercial seaweed extract made from Ecklonia maxima. J Appl Phycol 26:561–567Google Scholar
  60. Sun YM, Zhang NN, Wang ET, Yuan HL, Yang JS, Chen WX (2009) Influence of intercropping and intercropping plus rhizobial inoculation on microbial activity and community composition in rhizosphere of alfalfa (Medicago sativa L.) and Siberian wild rye (Elymus sibiricus L.). FEMS Microbiol Ecol 70:62–70CrossRefGoogle Scholar
  61. Sun Y, Zhang Y, Feng W, Qin S, Liu Z, Bai Y, Yan R, Fa K (2016) Effects of xeric shrubs on soil microbial communities in a desert in northern China. Plant Soil 414:281CrossRefGoogle Scholar
  62. van der Molen MK, Dolman AJ, Ciais P, Eglin T, Gobron N, Law BE, Meir P, Peters W, Phillips OL, Reichstein M, Chen T, Dekker SC, Doubková M, Friedl MA, Jung M, van den Hurk BJJM, de Jeu RAM, Kruijt B, Ohta T, Rebel KT, Plummer S, Seneviratne SI, Sitch S, Teuling AJ, van der Werf GR, Wang G (2011) Drought and ecosystem carbon cycling. Agric For Meteorol 151:765–773CrossRefGoogle Scholar
  63. Voronin PY, Black CC (2005) The importance and place of the photosynthetic carbon sequestration in the organic branch of its global cycle. Russ J Plant Physiol 52:69–76CrossRefGoogle Scholar
  64. Wang W, Liu Y, Li D, Hu C, Rao B (2009) Feasibility of cyanobacterial inoculation for biological soil crusts formation in desert area. Soil Biol Biochem 41:926–929CrossRefGoogle Scholar
  65. Watt MS, Palmer DJ (2012) Use of regression kriging to develop a carbon:nitrogen ratio surface for New Zealand. Geoderma 183–184:49–57CrossRefGoogle Scholar
  66. Wei YK, Gao YB, Xu H, Su D, Zhang X, Wang YH, Lin F, Chen L, Nie LY, Ren AZ (2006) Occurrence of endophytes in grasses native to northern China. Grass Forage Sci 61:422–429CrossRefGoogle Scholar
  67. Wei Y, Guo K, Chen J (2008) Effect of precipitation pattern on recruitment of soil water in Kubuqi desert, northwestern China (in Chinese with English summary). J Plant Ecol 32:1346–1355Google Scholar
  68. Weltzin JF, Loik ME, Schwinning S, Williams DG, Fay PA, Haddad BM, Harte J, Huxman TE, Knapp AK, Lin G (2003) Assessing the response of terrestrial ecosystems to potential changes in precipitation. AIBS Bull 53:941–952Google Scholar
  69. 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
  70. Wythers K, Lauenroth W, Paruelo J (1999) Bare-soil evaporation under semiarid field conditions. Soil Sci Soc Am J 63:1341–1349CrossRefGoogle Scholar
  71. Zhang B, Zhu J, Pan Q, Liu Y, Chen S, Chen D, Yan Y, Dou S, Han X (2017) Grassland species respond differently to altered precipitation amount and pattern. Environ Exp Bot 137:166–176CrossRefGoogle Scholar
  72. Zhao Y, Xu M, Wang Q, Shao M (2006) Impact of biological soil crust on soil physical and chemical properties of rehabilitated grassland in Hilly Loess Plateau, China (in Chinese with English summary). J Nat Resour 21:441–448Google Scholar
  73. Zhu RQ, Zhang ZS, Liu LC, Hui R, Zhang H, Bao JT (2015) Adaptive mechanisms of seven psammophytes in an arid desert margin in Shapotou area, China (in Chinese with English summary). Chin J Ecol 34:2749–2756Google Scholar
  74. Zhuang W, Downing A, Zhang Y (2015) The influence of biological soil crusts on15N translocation in soil and vascular plant in a temperate desert of northwestern China. J Plant Ecol 8:420–428CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Mutian Yuan
    • 1
  • Huijie Xiao
    • 1
    Email author
  • Ruoshui Wang
    • 1
  • Yuanjun Duan
    • 1
  • Qiqi Cao
    • 1
  1. 1.Yanchi Research Station, School of Soil and Water ConservationBeijing Forestry UniversityBeijingChina

Personalised recommendations