Covid-19 Research

Research Article

Microbial Factors May Contribute to the Persistence of Australian Fairy Circles

Journal of Biomedical Research & Environmental Sciences article abstract with citation details, DOI, publication dates, subject areas, full text links, and references.

View DOI Submit Manuscript

Article Details

Publication record, authors, dates, abstract, and full text access.

Open Access
Article Type Research Article
Subject Environmental Sciences
OCLC JBRES Record
Liron Klipcan, Nina A Kamennaya, Naw Than Than Aye, Ruth Van-Oss-Pinhasi, Ehud Meron, Shmuel Assouline and Hezi Yizhaq*
Issue: Volume5-Issue1
Pages: 033-043
Received: 2023-12-19
Accepted: 2024-01-09
Published: 2024-01-13

Abstract

Fairy Circles (FCs) are roughly circular, spatially periodic barren patches occurring both along the southwestern African coast, spanning the Namib Desert (NFCs), and in the Pilbara region of Western Australia (AFCs). The origin of both NFC and AFC patterns is still debatable and a subject of ongoing research. Recently, it was argued that pathogenic soil microbes may contribute to ring formation of the Triodia basedowii grass which is the same grass species that forms the AFCs. We have analyzed, under controlled laboratory conditions, soil samples taken from different parts of AFCs (center, periphery and m3atrix) for microbiological activities by Lettuce germination experiments under different manipulations. In seven different circles, out of an average of 13, root lengths of germinated seeds were strongly inhibited in the samples taken from the center, and to a lesser extent, in the samples taken from the periphery and the matrix. Quantitative analyses of the soil microbial community from the FC center found no support to the hypothesis that phytotoxic effect was caused by soil crust cyanobacteria due their low abundance. However, in soil of the FCs it identified both heterotrophic bacteria and fungi that may contribute to the phytotoxic effect. Although our study was not done with seeds of Triodia basedowii it supports the idea that microbial activities in the soil may contribute to AFC persistence by inhibiting plant germination and development in the bare soil gaps in addition to the physical soil crusts resulting from weathering. This suggests that negative plant-soil feedback can act in concert with the main driver mechanism of the AFCs, the scale-dependent plant-water feedback.

FullText HTML FullText PDF DOI: 10.37871/jbres1869 Crossmark

Certificate of Publication

Certificate of Publication

Copyright

© 2024 Klipcan L, et al. Distributed under Creative Commons CC-BY 4.0 Creative CommonsAttribution

How to cite this article

Klipcan L, Kamennaya NA, Than Aye NT, Van-Oss-Pinhasi R, Meron E, Assouline S, Yizhaq H. Microbial Factors May Contribute to the Persistence of Australian Fairy Circles. J Biomed Res Environ Sci. 2024 Jan 13; 5(1): 033-043. doi: 10.37871/ jbres1869, Article ID: JBRES1869, Available at: https://www.jelsciences.com/articles/jbres1869.pdf

Subject area(s)

Climate Change Biology

References

  1. Van Rooyen MW, Theron GK, Van Rooyen N, Jankowitz WJ, Matthews WS. Mysterious circles in the Namib Desert: Review of hypotheses on their origin. Journal of Arid Environments. 2004;57:467-485. doi:10.1016/S0140-1963(03)00111-3.
  2. Getzin S, Yizhaq H, Bell B, Erickson TE, Postle AC, Katra I, Tzuk O, Zelnik YR, Wiegand K, Wiegand T, Meron E. Discovery of fairy circles in Australia supports self-organization theory. Proc Natl Acad Sci. 2016;113:3551-3556. doi: 10.1073/pnas.1522130113.
  3. Getzin S, Yizhaq H, Muñoz-Rojas M, Wiegand K, Erickson TE. A multi-scale study of Australian fairy circles using soil excavations and drone-based image analysis. Ecosphere. 2019;10:e02620. doi: 10.1002/ecs2.2620.
  4. Getzin S, Yizhaq H, Tschinkel WR. Definition of “fairy circles” and how they differ from to other common vegetation gaps and plant rings. Journal of Vegetation Science. 2021;32:13092.
  5. Getzin S, Holch S, Yizhaq H, Wiegand K. Plant water stress, not termite herbivory, causes Namibia’s fairy circles. Perspectives in Plant Ecology, Evolution and Systematics. 2022;57:125698. doi: 10.1016/j.ppees.2022.125698.
  6. Guirado E, Delgado-Baquerizob M, Benitoa BM, Molina-Pardo JL, Martínez-Valderrama J, Maestre FT. The global biogeography and environmental drivers of fairy circles. PNAS. 2023;120:2304032120. doi: 10.1073/pnas.2304032120.
  7. Dong X. Fairy circles tales. PNAS. 2023;120(41):2314908120. doi: 10.1073/pnas.2314908120.
  8. Juergens N. The biological underpinnings of Namib Desert fairy circles. Science. 2013;339:5.
  9. Tarnita CE, Bonachela JA, Sheffer E, Guyton JA, Coverdale TC, Long RA, Pringle RM. A theoretical foundation for multi-scale regular vegetation patterns. Nature. 2017;541:398-401. doi: 10.1038/nature20801.
  10. Juergens N, Groengroeft A, Gunter F. Evolution at the arid extreme: The influence of climate on sand termite colonies and fairy circles of the Namib Desert Phil. Trans. R Soc B. 2023;378:20220149. doi: 10.1098/rstb.2022.0149.
  11. Walsh F, Bidu GK, Bidu N , Evans TA, Judson TM, Kendrick P, Michaels AN, Moore D, Nelson M, Oldham C, Schofield J, Sparrow A, Taylor MK, Taylor DP, Wayne LN, Williams CM, Martu elders. First Peoples’ knowledge leads scientists to reveal ‘fairy circles’ and termite linyji are linked in Australia. Nat Ecol Evol. 2023;7:610-622. doi: 10.1038/s41559-023-01994-1.
  12. Getzin S, Yizhaq H, Cramer MD, Tschinkel WR. Contrasting global patterns of spatially periodic fairy circles and regular insect nests in drylands. Journal of Geophysical Research: Biogeosciences. 2019;124:3327-3342. doi: 10.1029/2019JG005393.
  13. Getzin S, Erickson TE, Yizhaq H, Muñoz‐Rojas M, Huth A, Wiegand K. Bridging ecology and physics: Australian fairy circles regenerate following model assumptions on ecohydrological feedbacks. J Ecol. 2020;1365-(2745):13493. doi: 10.1111/1365-2745.13493.
  14. Getzin S, Yizhaq H, Muñoz-Rojas M, Erickson TE. Australian fairy circles and termite linyji are not caused by the same mechanism. Nature Ecology and Evolution. 2024. doi:10.1038/s41559-023-02225-3.
  15. Meron E. From patterns to function in living systems: Dryland ecosystems as a case study. Annual Review of Condensed Matter Physics. 2018;9:79-103. doi: 10.1146/annurev-conmatphys-033117-053959.
  16. Zelnik YR, Meron E, Bel G. Gradual regime shifts in fairy circles. Proceedings of the National Academy of Sciences of the United States of America. 2015;112,:12327-12331. doi: 10.1073/pnas.1504289112.
  17. Li J, Guo L, Wilson GWT, Cobb AB, Wang K, Liu L, Zhao H, Huang D. Assessing soil microbes that drive fairy ring patterns in temperate semiarid grasslands. BMC Ecol Evol. 2022 Nov 5;22(1):130. doi: 10.1186/s12862-022-02082-x. PMID: 36335298; PMCID: PMC9636817.
  18. Inderjit, Callaway RM, Meron E. Belowground feedbacks as drivers of spatial self-organization and community assembly. Phys Life Rev. 2021;38:1-24. doi: 10.1016/j.plrev.2021.07.002.
  19. Ramond JB, Pienaar A, Armstrong A, Seely M, Cowan DA. Niche-partitioning of edaphic microbial communities in the Namib Desert gravel plain Fairy Circles. PLoS One. 2014 Oct 3;9(10):e109539. doi: 10.1371/journal.pone.0109539. PMID: 25279514; PMCID: PMC4184855.
  20. Van der Putten WH. Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, Van de voorde TFJ, Wardle DA. Plant soil feedbacks: The past, the present and future challenges. Journal of Ecology. 2013;101:265-276. doi: 10.1111/1365-2745.12054.
  21. Inderjit, Wardle DA, Karban R, Callaway RM. The ecosystem and evolutionary contexts of allelopathy. Trends Ecol Evol. 2011 Dec;26(12):655-62. doi: 10.1016/j.tree.2011.08.003. Epub 2011 Sep 14. PMID: 21920626.
  22. Singh HP, Batish DR, Kohli RK. Autotoxicity: Concept, organisms, and ecological significance. Critical Reviews in Plant Sciences. 1999;18:757-772. doi: 10.1080/07352689991309478.
  23. Bonanomi G, Incerti G, Stinca A, Cartenì F, Giannino F, Mazzoleni S. Ring formation in clonal plants. Community Ecology. 2014;15:77-86. doi: 10.1556/ComEc.15.2014.1.8.
  24. Iuorio A, Salvatori N, Toraldo G, Giannino F. Analysis and numerical simulations of travelling waves due to plant-soil negative feedback. European Journal of Applied Mathematics. 2023. doi: 10.1017/S0956792523000323.
  25. Salvatori N, Moreno M, Zotti M, Iuorio A, Cartení F, Bonanomi G, Mazzoleni S, Giannino F. Process based modelling of plants-fungus interactions explains fairy ring types and dynamics. Scientific Reports. 2023;13(1):19918.
  26. Packer A, Clay K. Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature. 2000; 404:278-281. doi: 10.1038/35005072.
  27. Ross ND, Moles AT. The contribution of pathogenic soil microbes to ring formation in an iconic Australian arid grass, Triodia basedowii (Poaceae). Austr J Bot. 2021;69:113-120. doi: 10.1071/BT20122.
  28. Ramond JB, Pienaar A, Armstrong A, Seely M, Cowan DA. Niche-partitioning of edaphic microbial communities in the Namib Desert gravel plain fairy circles. Plos One. 2014;9:109539. doi: 10.1371/journal.pone.0109539.
  29. Van der Walt AJ, Johnson RM, Cowan DA, Seely M, Ramond JB. Unique Microbial Phylotypes in Namib Desert Dune and Gravel Plain Fairy Circle Soils. Appl Environ Microbiol. 2016 Jul 15;82(15):4592-4601. doi: 10.1128/AEM.00844-16. PMID: 27208111; PMCID: PMC4984285.
  30. Rietkerk M, van de Koppel J. Regular pattern formation in real ecosystems. Trends Ecol Evol. 2008 Mar;23(3):169-75. doi: 10.1016/j.tree.2007.10.013. Epub 2008 Feb 5. PMID: 18255188.
  31. Bennett JJR, Bidesh KB, Michel F, Yizhaq H, Getzin S, Meron E. Phenotypic plasticity a missing element in the theory of vegetation pattern formation. PNAS. 2023;150(50):2311528120. doi: 10.1073/pnas.231152812.
  32. Cramer MD, Barger NN, Tschinkel WR. Edaphic properties enable facilitative and competitive interactions resulting in fairy circle formation. Ecography. 2017;40:1210-1220. doi: 10.1111/ecog.02461.
  33. Levin N, Levental S, Morag H. The effect of wildfires on vegetation cover and dune activity in Australia’s desert dunes: A multisensor analysis. Int J Wildland Fire. 2012;21:459-475. doi: 10.1071/WF10150.
  34. Bertin C, Harmon R, Akaogi M, Weidenhamer JD, Weston LA. Assessment of the phytotoxic potential of m-tyrosine in laboratory soil bioassays. Journal of Chemical Ecology. 2009;35:1288-1294. doi: 10.1007/s10886-009-9707-4.
  35. Bååth E, Söderström B. The significance of hyphal diameter in calculation of fungal biovolume. Oikos. 1979; 11-14. doi: 10.2307/3544505.
  36. D’Hertefeldt T, Van der Putten WH. Physiological integration of the clonal plant carex arenaria and its response to Soil-Borne pathogens. Oikos. 1998;81:229. doi: 10.2307/3547044
  37. Van der Putten WH. Pathogen-driven forest diversity. Nature. 2000 Mar 16;404(6775):232-3. doi: 10.1038/35005188. PMID: 10749191.
  38. Saqrane S, El Ghazali I, Oudra B, Bouarab L, Vasconcelos V. Effects of cyanobacteria producing microcystins on seed germination and seedling growth of several agricultural plants. J Environ Sci Health B. 2008 Jun;43(5):443-51. doi: 10.1080/10934520701796192. PMID: 18576226.
  39. Barazani O, Friedman J. Allelopathic bacteria and their impact on higher plants. Crit Rev Microbiol. 2001;27(1):41-55. doi: 10.1080/20014091096693. PMID: 11305367.
  40. Du S, Trivedi P, Wei Z, Feng J, Hu HW, Bi L, Huang Q, Liu YR. The Proportion of Soil-Borne Fungal Pathogens Increases with Elevated Organic Carbon in Agricultural Soils. mSystems. 2022 Apr 26;7(2):e0133721. doi: 10.1128/msystems.01337-21. Epub 2022 Mar 21. PMID: 35311561; PMCID: PMC9040864.
  41. Mikryukov V, Dulya O, Zizka A, Bahram M, Hagh-Doust N, Anslan S, Prylutskyi O, Delgado-Baquerizo M, Maestre FT, Nilsson H, Pärn J, Öpik M, Moora M, Zobel M, Espenberg M, Mander Ü, Khalid AN, Corrales A, Agan A, Vasco-Palacios AM, Saitta A, Rinaldi A, Verbeken A, Sulistyo B, Tamgnoue B, Furneaux B, Duarte Ritter C, Nyamukondiwa C, Sharp C, Marín C, Gohar D, Klavina D, Sharmah D, Dai DQ, Nouhra E, Biersma EM, Rähn E, Cameron E, De Crop E, Otsing E, Davydov E, Albornoz F, Brearley F, Buegger F, Zahn G, Bonito G, Hiiesalu I, Barrio I, Heilmann-Clausen J, Ankuda J, Doležal J, Kupagme J, Maciá-Vicente J, Djeugap Fovo J, Geml J, Alatalo J, Alvarez-Manjarrez J, Põldmaa K, Runnel K, Adamson K, Bråthen KA, Pritsch K, Tchan Issifou K, Armolaitis K, Hyde K, Newsham KK, Panksep K, Lateef AA, Hansson L, Lamit L, Saba M, Tuomi M, Gryzenhout M, Bauters M, Piepenbring M, Wijayawardene NN, Yorou N, Kurina O, Mortimer P, Meidl P, Kohout P, Puusepp R, Drenkhan R, Garibay-Orijel R, Godoy R, Alkahtani S, Rahimlou S, Dudov S, Põlme S, Ghosh S, Mundra S, Ahmed T, Netherway T, Henkel T, Roslin T, Nteziryayo V, Fedosov V, Onipchenko V, Yasanthika WAE, Lim Y, Van Nuland M, Soudzilovskaia N, Antonelli A, Kõljalg U, Abarenkov K, Tedersoo L. Connecting the multiple dimensions of global soil fungal diversity. Sci Adv. 2023 Dec;9(48):eadj8016. doi: 10.1126/sciadv.adj8016. Epub 2023 Nov 29. PMID: 38019923; PMCID: PMC10686567.
  42. Kaminsky R. The Microbial Origin of the Allelopathic Potential of Adenostoma fasciculatum H & A. Ecological Monographs. 1981;51:365-382. doi: 10.2307/2937279.
  43. Tschinkel WR. The life cycle and life span of Namibian fairy circles. PLoS One. 2012;7(6):e38056. doi: 10.1371/journal.pone.0038056. Epub 2012 Jun 27. PMID: 22761663; PMCID: PMC3384657.
  44. Armstrong G, Legge S. The post-fire response of an obligate seeding Triodia species (Poaceae) in the fire-prone Kimberley, north-west Australia. Int J Wildland Fire. 2011;20:974. doi: 10.1071/WF10130.
  45. Carlton L, Duncritts NC, Chung YA, Rudgers JA. Plant-microbe interactions as a cause of ring formation in Bouteloua gracilis. Journal of Arid Environments. 2018;152:1-5. doi: 10.1016/j.jaridenv.2018.02.001.
  46. Herooty Y, Bar (Kutiel) P, Yizhaq H, Katz O. Soil hydraulic properties and water source-sink relations affect plant rings’ formation and sizes under arid conditions. Flora. 2020;270:151664. doi: 10.1016/j.flora.2020.151664.
  47. Sheffer E, Yizhaq H, Gilad E, Shachak M, Meron E. Why do plants in resource-deprived environments form rings? Ecological Complexity. 2007;4:192-200. doi: 10.1016/j.ecocom.2007.06.008.
  48. Sheffer E, Yizhaq H, Shachak M, Meron E. Mechanisms of vegetation-ring formation in water-limited systems. J Theor Biol. 2011 Mar 21;273(1):138-46. doi: 10.1016/j.jtbi.2010.12.028. Epub 2010 Dec 25. PMID: 21187102.
  49. Yizhaq H, Stavi I, Swet N, Zaady E, Katra I. Vegetation ring formation by water overland flow in water-limited environments: Field measurements and mathematical modelling. Ecohydrology. 2019;12:e2135. doi: org/10.1002/eco.2135.
  50. Yizhaq H, Al-Tawaha ARMS, Stavi I. A first study of Urginea maritima rings: A case study from southern Jordan. Land. 2022;11:285. doi: 10.3390/land11020285.
  51. Yizhaq Y, Stavi I. Ring formation in Stipagrostis obtusa in the arid north-eastern Negev, Israel, Flora. 2023;306:152353. doi: 10.1016/j.flora.2023.152353.
  52. Meron E, Gilad E, von Hardenberg J, Shachak M, Zarmi Y. Vegetation patterns along a rainfall gradient. Chaos, Solitons & Fractals, Fractals in Geophysics. 2004;19:367-376. doi: 10.1016/S0960-0779(03)00049-3.
  53. Marasco A, Iuorio A, Cartení F, Bonanomi G, Tartakovsky DM, Mazzoleni S, Giannino F. Vegetation pattern formation due to interactions between water availability and toxicity in plant-soil feedback. Bull Math Biol. 2014 Nov;76(11):2866-83. doi: 10.1007/s11538-014-0036-6. Epub 2014 Oct 23. PMID: 25338554.
  54. Marasco A, Giannino F, Iuorio A. Modelling competitive interactions and plant-soil feedback in vegetation dynamics. Ric Mat. 2020;69(2):553-577. doi: 10.48550/arXiv.1912.04166.
Publish with JBRES — Peer-reviewed, multidisciplinary Open Access with rapid review, DOI, and global visibility.
Double-Blind CrossRef DOI Discoverable
Submit Manuscript Membership