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Community Assembly of Biological Soil Crusts of Different Successional Stages in a Temperate Sand Ecosystem, as Assessed by Direct Determination and Enrichment Techniques

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Abstract

In temperate regions, biological soil crusts (BSCs: complex communities of cyanobacteria, eukaryotic algae, bryophytes, and lichens) are not well investigated regarding community structure and diversity. Furthermore, studies on succession are rare. For that reason, the community assembly of crusts representing two successional stages (initial, 5 years old; and stable, >20 years old) were analyzed in an inland sand ecosystem in Germany in a plot-based approach (2 × 18 plots, each 20 × 20 cm). Two different methods were used to record the cyanobacteria and eukaryotic algae in these communities comprehensively: determination directly out of the soil and enrichment culture techniques. Additionally, lichens, bryophytes, and phanerogams were determined. We examine four hypotheses: (1) A combination of direct determination and enrichment culture technique is necessary to detect cyanobacteria and eukaryotic algae comprehensively. In total, 45 species of cyanobacteria and eukaryotic algae were detected in the study area with both techniques, including 26 eukaryotic algae and 19 cyanobacteria species. With both determination techniques, 22 identical taxa were detected (11 eukaryotic algae and 11 cyanobacteria). Thirteen taxa were only found by direct determination, and ten taxa were only found in enrichment cultures. Hence, the hypothesis is supported. Additionally, five lichen species (three genera), five bryophyte species (five genera), and 24 vascular plant species occurred. (2) There is a clear difference between the floristic structure of initial and stable crusts. The different successional stages are clearly separated by detrended correspondence analysis, showing a distinct structure of the community assembly in each stage. In the initial crusts, Klebsormidium flaccidum, Klebsormidium cf. klebsii, and Stichococcus bacillaris were important indicator species, whereas the stable crusts are especially characterized by Tortella inclinata. (3) The biodiversity of BSC taxa and vascular plant species increases from initial to stable BSCs. There are significantly higher genera and species numbers of cyanobacteria and eukaryotic algae in initial BSCs. Stable BSCs are characterized by significantly higher species numbers of bryophytes and vascular plant species. The results show that, in the investigated temperate region, the often-assumed increase of biodiversity in the course of succession is clearly taxa-dependent. Both successional stages of BSCs are diversity “hot spots” with about 29 species of all taxa per 20 × 20 cm plot. (4) Nitrogen and chlorophyll a concentrations increase in the course of succession. The chlorophyll a content of the crusts (cyanobacteria, eukaryotic algae, bryophyte protonemata) is highly variable across the studied samples, with no significant differences between initial and stable BSCs; nor were ecologically significant differences in soil nutrient contents observed. According to our results, we cannot confirm this hypothesis; the age difference between our two stages is probably not big enough to show such an increase.

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References

  1. Ambos R, Kandler O (1987) Einführung in die Naturlandschaft. Mainzer Naturwissenschaftliches Archiv 25:1–28

    Google Scholar 

  2. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24(1):1–14

    Article  PubMed  CAS  Google Scholar 

  3. Bailey D, Mazurak PA, Rosowski JR (1973) Aggregation of soil particles by algae. J Phycol 9:99–101

    Google Scholar 

  4. Bazzaz FA (1975) Plant species diversity in old-field successional ecosystems in southern Illinois. Ecology 56:485–488

    Article  Google Scholar 

  5. Belnap J, Eldridge DJ (2001) Disturbance and recovery of biological soil crusts. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Springer, Berlin

    Google Scholar 

  6. Belnap J, Gardner JS (1993) Soil microstructure in soils of the Colorado Plateau: the role of the cyanobacterium Microcoleus vaginatus. Gt Basin Nat 53:40–47

    Google Scholar 

  7. Belnap J, Harper KT, Warren SD (1993) Surface disturbance of cryptobiotic soil crusts: nitrogenase activity, chlorophyll content, and chlorophyll degradation. Arid Soil Res Rehab 8:1–8

    Google Scholar 

  8. Belnap J, Lange OL (2001) Biological soil crusts: structure, function, and management. Ecological studies 150. Springer, Berlin, p 503

    Google Scholar 

  9. Bergmann, S (2004) Zum Nährstoffhaushalt in Sandökosystemen der nördlichen Oberrheinebene: Sukzession, Ruderalisierungsprozesse und Effekte von Schafbeweidung. PhD Thesis, Darmstadt University of Technology, Germany

  10. Bhatnagar A, Makandar MB, Garg MK, Bhatnagar M (2008) Community structure and diversity of cyanobacteria and green algae in the soils of Thar Desert (India). J Arid Environ 72:73–83

    Article  Google Scholar 

  11. Bischoff HW, Bold HC (1963) Phycological studies. IV. Some soil algae from enchanted rock and related algal species. Univ Texas Publ 6318:1–95

    Google Scholar 

  12. Bliss LC, Gold WG (1999) Vascular plant reproduction, establishment, and growth and the effects of cryptogamic crusts within a polar desert ecosystem, Devon Island, N.W.T., Canada. Can J Bot 77:623–636

    Article  Google Scholar 

  13. Booth WE (1941) Algae as pioneers in plant succession and their importance in erosion control. Am J Bot 22:38–46

    Google Scholar 

  14. Breen K, Lévesque E (2006) Proglacial succession of biological soil crusts and vascular plants: biotic interactions in the High Arctic. Can J Bot 84:1714–1731

    Article  Google Scholar 

  15. Brooker RW, Maestre FT, Callaway RM, Lortie CL, Cavieres LA, Kunstler G, Liancourt P, Tilebörger K, Travis JMJ, Anthelme F, Armas C, Coll L, Corcket E, Delzon S, Forey E, Kikvidze Z, Olofsson J, Pungnaire F, Quiroz CL, Saccone P, Schiffers K, Seifan M, Touzard B, Michalet R (2008) Facilitation in plant communities: the past, the present, and the future. J Ecol 96:18–34

    Article  Google Scholar 

  16. Büdel B (2001) Synopsis: comparative biogeography of soil-crust biota. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Springer, Berlin, pp 141–152

    Google Scholar 

  17. Büdel B, Darienko T, Deutschewith K, Dojani S, Friedl T, Mohr KI, Salisch M, Reisser W, Weber B (2009) Southern African biological soil crusts are ubiquitous and highly diverse in drylands, being restricted by rainfall frequency. Microb Ecol 57(2):229–247

    Article  PubMed  Google Scholar 

  18. Cabała J, Rahmonov O (2004) Cyanophyta and algae as an important component of biological crust from the Pustynia Błędowska Desert (Poland). Polish Bot J 49(1):93–100

    Google Scholar 

  19. Connell JH, Slatyer RO (1977) Mechanisms of succession in natural communities and their roles in community stability and organization. Am Nat 111:1119–1144

    Article  Google Scholar 

  20. Delgadillo C, Zander R (1984) The mosses of the Tehuacán Valley, Mexico, and notes on their distribution. Bryologist 87:319–322

    Article  Google Scholar 

  21. Eckert RE, Peterson FF, Meurisse MS, Stephens JL (1986) Effects of soil-surface morphology on emergence and survival of seedlings in big sagebrush communities. J Range Manag 39:414–420

    Article  Google Scholar 

  22. Eldridge DJ, Freudenberger D, Koen TB (2006) Diversity and abundance of biological soil crust taxa in relation to fine and coarse-scale disturbances in a grassy eucalypt woodland in eastern Australia. Plant Soil 281:255–268

    Article  CAS  Google Scholar 

  23. Eldridge DJ, Greene RS (1994) Microbiotic soil crusts: a review of their roles in soil and ecological processes in the rangelands of Australia. Aust J Soil Res 32:389–415

    Article  Google Scholar 

  24. Eldridge DJ, Koen TB (1998) Cover and floristics of microphytic soil crusts in relation to indices of landscape health. Plant Ecol 137:101–114

    Article  Google Scholar 

  25. Ettl H, Gärtner G (1995) Syllabus der Boden-, Luft- und Flechtenalgen. Fischer, Stuttgart, Jena, New York 721 pp

    Google Scholar 

  26. Flechtner VR, Johansen JR, Clark WH (1998) Algal composition of microbiotic crusts from the central desert of Baja California, Mexico. Gt Bas Nt 58(4):295–311

    Google Scholar 

  27. Frahm J-P, Frey W (2004) Moosflora, 4th edn. Ulmer, Stuttgart, p 538

    Google Scholar 

  28. Foster BL, Tilman D (2000) Dynamic and static views of succession: testing the descriptive power of the chronosequence approach. Plant Ecol 146:1–10

    Article  Google Scholar 

  29. Garcia-Pichel F, López-Cortés A, Nübel U (2001) Phylogenetic and morphological diversity of cyanobacteria in soil desert crusts from the Colorado Plateau. Appl Environ Microbiol 67(4):1902–1910

    Article  PubMed  CAS  Google Scholar 

  30. Geitler L (1932) Cyanophyceae. Dr. L. Rabenhorst's Kryptogamen-Flora von Deutschland. Österreich und der Schweiz. 14. Band: Die Algen. Akademische Verlagsgesellschaft, Leipzig, p 1196

    Google Scholar 

  31. Hach T, Büdel B, Schwabe A (2005) Biologische Krusten in basenreichen Sand-Ökosystemen des Koelerion glaucae-Vegetationskomplexes: taxonomische Struktur und Empfindlichkeit gegenüber mechanischen Störungen. Tuexenia 25:357–372

    Google Scholar 

  32. Hahn A, Kusserow H (1998) Spatial and temporal distribution of algae in soil crusts in the Sahel of W Africa: preliminary results. Willdenowia 28:227–238

    Google Scholar 

  33. Harper KT, Marble JR (1998) A role for nonvascular plants in management of arid and semiarid rangelands. In: Tueller BT (ed) Vegetation science applications for rangeland analysis and management. Kluwer Academic Publishers, Dortdrecht, Boston, London, p 656

    Google Scholar 

  34. Harper KT, Pendleton RL (1993) Cyanobacteria and cyanolichens can they enhance availability of essential minerals for higher plants? Gt Basin Nat 53:59–72

    Google Scholar 

  35. Hawkes CV, Flechtner VR (2002) Biological soil crusts in a xeric Florida Shrubland: composition, abundance, and spatial heterogeneity of crusts with different disturbance histories. Microbial Ecol 43:1–12

    Article  CAS  Google Scholar 

  36. Jafari M, Tavili A, Zargham N, GhA H, Zare Chahouki MA, Shirzadian S, Azarnivand H, GhR Z, Sohrabi M (2004) Comparing some properties of crusted and uncrusted soils in Alagol Region of Iran. Pakistan J Nutrition 3:273–277

    Article  Google Scholar 

  37. Johansen JR (1993) Cryptogamic crusts of semiarid and arid lands of North America. J Phycol 29:140–147

    Article  Google Scholar 

  38. Johansen JR, Ashley J, Rayburn WR (1993) Effects of rangefire on soil algal crusts in semiarid shrub-steppe of the lower Columbia basin and their subsequent recovery. Gt Basin Nat 53:73–88

    Google Scholar 

  39. Johansen JR, St Clair LL, Webb BL, Nebekter GT (1984) Recovery patterns of cryptogamic soil crusts in desert rangelands following fire disturbance. Bryologist 87:238–243

    Article  Google Scholar 

  40. Kaštovská K, Elster J, Stibal M, Šantrůčková H (2005) Microbial assemblages in soil microbial succession after glacial retreat in Svalbard (High Arctic). Microb Ecol 50:396–407

    Article  PubMed  Google Scholar 

  41. Kidron GJ (2007) Millimeter-scale microrelief affecting runoff yield over microbiotic crust in the Negev Desert. Catena 70:266–273

    Article  Google Scholar 

  42. Komárek J, Anagnostidis K (1999) Süßwasserflora von Mitteleuropa 19/1. Cyanoprokaryota, 1. Teil: Chroococcales. Spektrum, Heidelberg, p 548

    Google Scholar 

  43. Komárek J, Anagnostidis K (2005) Süßwasserflora von Mitteleuropa 19/2. Cyanoprokaryota, 2. Teil: Oscillatriales. Spektrum, Heidelberg, p 759

    Google Scholar 

  44. Lange OL (2001) Photosynthesis of soil-crust biota as dependent on environmental factors. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Springer, Berlin, pp 217–240

    Google Scholar 

  45. Lange OL, Kidron GJ, Büdel B, Meyer A, Kilian E, Abeliovich A (1992) Taxonomic composition and photosynthetic characteristics of the “biological soil crusts” covering sand dunes in the western Negev Desert. Func Ecol 6:519–527

    Article  Google Scholar 

  46. Lange OL, Meyer A, Zellner H, Heber U (1994) Photosynthesis and water relations of lichen soil crusts: field measurements in the coastal fog zone of the Namib Desert. Func Ecol 8:253–264

    Article  Google Scholar 

  47. Langhans TM, Storm C, Schwabe A (2009) Biological soil crusts and their microenvironment: impact on emergence, survival and establishment of seedlings. Flora 204(2):157–168

    Google Scholar 

  48. Langhans TM, Storm C, Schwabe A (2010) Regeneration processes of biological soil crusts, macro-cryptogams and vascular plant species after fine-scale disturbance in a temperate region: recolonization or successional replacement? Flora 205(1)

  49. Lesica P, Shelly JS (1992) Effects of cryptogamic soil crust on the population dynamics of Arabis fecunda (Brassicaceae). Am Midl Nat 128:53–60

    Article  Google Scholar 

  50. Loucks OL (1970) Evolution of diversity, efficiency, and community stability. Am Zool 10:17–25

    PubMed  CAS  Google Scholar 

  51. Lukešová A (2001) Soil algae in brown coal and lignite post-mining areas in Central Europe (Czech Republic and Germany). Restor Ecol 9(4):341–350

    Article  Google Scholar 

  52. Lukešová A, Hoffmann L (1996) Soil algae from acid rain impacted forest areas of the Krušné hory Mts. 1. Algal communities. Vegetatio 125:123–136

    Article  Google Scholar 

  53. Lukešová A, Komárek J (1987) Sucession of soil algae on dumps from strip coal-mining in the Most Region (Czechoslovakia). Folia Geobot Phytotaxon 22:355–362

    Google Scholar 

  54. Malam Issa O, Trichet J, Défarge C, Couté A, Valentin C (1999) Morphology and microstrucutre of microbiotic soil crusts on a tiger bush sequence (Niger, Sahel). Catena 37:175–196

    Article  Google Scholar 

  55. Mazor G, Kidron GJ, Vonshak A, Abeliovich A (1996) The role of cyanobacterial exopolysaccharides in structuring desert microbial crusts. FEMS Microb Ecol 21:121–130

    Article  CAS  Google Scholar 

  56. Pluis JLA (1994) Algal crust formation in the inland dune area, laarder Wasmeer, the Netherlands. Vegetatio 113:41–51

    Article  Google Scholar 

  57. Rayburn WR, Mack RN, Metting B (1982) Conspicuous algal colonization of the ash from Mount St. Helens. J Phycol 18:537–543

    Article  Google Scholar 

  58. Rippka R, Desrulles J, Waterbury JB, Herdman M, Stanier RY (1979) Genetic assignment, strain histories and properties of pure cultures of cyanobacteria. J Gen Microb 11:1–61

    Google Scholar 

  59. Rivera-Aguilar V, Montejano G, Rodríguez-Zaragoza S, Durán-Díaz A (2006) Distribution and compaosition of cyanobacteria, mosses and lichens of the biological soil crusts of the Tehuacán Valley, Puebla, México. J Arid Environ 67:208–225

    Article  Google Scholar 

  60. Ronen R, Galun M (1984) Pigment extraction from lichens with dimethyl sulfoxide (DMSO) and estimation of chlorophyll degradation. Environ Exp Bot 24:239–245

    Article  CAS  Google Scholar 

  61. Schoonmaker P, McKee A (1988) Species composition and diversity during secondary succession of coniferous forests in the western Cascade Mountains of Oregon. For Sci 34:960–979

    Google Scholar 

  62. Shields LM, Drouet F (1962) Distribution of terrestrial algae within the Nevada Test Site. Am J Bot 49:547–554

    Article  Google Scholar 

  63. Shubert E, Starks TL (1980) Soil–algal relationships from surface mined soils. Br Phycol J 15:417–428

    Article  Google Scholar 

  64. Süss K, Storm C, Zehm A, Schwabe A (2004) Succession in inland sand ecosystems: which factors determine the occurrence of the tall grass species Calamagrostis epigejos (L.) Roth and Stipa capillata L.? Plant Biol 6:465–476

    Article  PubMed  Google Scholar 

  65. Tilman D (1987) Secondary succession and the pattern of plant dominance along experimental nitrogen gradients. Ecolog Monogr 57:189–214

    Article  Google Scholar 

  66. Tirkey J, Adhikary SP (2005) Cyanobacteria in biological soil crusts of India. Curr Sci 89(3):515–521

    Google Scholar 

  67. VDLUFA (Verband der landwirtschaftlichen Untersuchungs- und Forschunganstalten) (1991) Methodenbuch. Band 1. Die Untersuchung von Böden, 4th edn. VDLUFA-Verlag, Darmstadt

    Google Scholar 

  68. Whittaker RH (1972) Evolution and measurement of species diversity. Taxon 21:213–251

    Article  Google Scholar 

  69. Wirth V (1995) Flechtenflora, 2nd edn. Ulmer, Stuttgart, p 661

    Google Scholar 

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Acknowledgments

The study was carried out with the support of a PhD grant by the Darmstadt University of Technology. We thank Prof. Dr. B. Büdel (Kaiserslautern) for most valuable help concerning the study and determination of BSCs and Ursula Lebong for technical assistance. The improvement of the English text by Dr. A. Thorson (Oxford) is much appreciated. Especially, thanks to the “Regierungspräsidium Darmstadt” for permission to work in the area.

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  1. Department Biology, Vegetation Ecology, Darmstadt University of Technology, Schnittspahnstraße 4, 64287, Darmstadt, Germany

    Tanja Margrit Langhans, Christian Storm & Angelika Schwabe

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  1. Tanja Margrit Langhans
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  2. Christian Storm
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  3. Angelika Schwabe
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Correspondence to Angelika Schwabe.

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Langhans, T.M., Storm, C. & Schwabe, A. Community Assembly of Biological Soil Crusts of Different Successional Stages in a Temperate Sand Ecosystem, as Assessed by Direct Determination and Enrichment Techniques. Microb Ecol 58, 394–407 (2009). https://doi.org/10.1007/s00248-009-9532-x

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