Advertisement

Symbiosis

pp 1–24 | Cite as

The pioneer lichen Placopsis in maritime Antarctica: Genetic diversity of their mycobionts and green algal symbionts, and their correlation with deglaciation time

  • Andreas BeckEmail author
  • Julia Bechteler
  • Angélica Casanova-Katny
  • Iva Dzhilyanova
Article

Abstract

Since ice-free areas in Antarctica are predicted to increase by up to 25% before the end of this century, lichens such as the genus Placopsis will be important colonizers of these newly available grounds and will still be present in later successional stages of the lichen community. The main symbionts of Placopsis species are examined for 56 specimens collected from the South Shetland Islands, Antarctica using molecular (fungal and algal nrITS, fungal RPB1, algal rbcL sequences) and morphological methods. The specimens were collected from soils with different deglaciation times. Eight uni-algal photobiont cultures were obtained and analysed from two specimens. Placopsis antarctica and P. contortuplicata proved to be monophyletic and are sister species, only the former producing vegetative diaspores (soredia). Both share the same photobiont pool and are lichenized with two closely related species, Stichococcus antarcticus and S. allas. Two haplotypes of S. antarcticus are restricted to areas deglaciated for more than 5000 years and the volcanic Deception Island indicating a shift in the photobionts of Placopsis in the course of the soil and lichen community development. These photobiont haplotypes exhibit different ecological preferences, possibly leading to adaptation of the symbiotic entity to changing environmental conditions.

Keywords

Selectivity Phylogeny Stichococcus Climate Change Haplotypes 

Notes

Acknowledgements

We cordially thank Dr. Georg Gärtner (Innsbruck, Austria) for providing the authentic culture of Stichococcus allas (ASIB: IB 37). Mark R. D. Seaward (Bradford, U. K.) is sincerely recognised for improving the English text.

Author Contributions

AB designed the study, collected the samples, isolated and analysed the photobiont cultures, guided the molecular work, prepared the photographs and wrote the manuscript. JB performed part of the molecular work, guided ID, did the phylogenetic analyses and wrote the manuscript. ACK provided logistic support and travel organization to Antarctica, participated in sample collection and revised the MS. ID performed part of the molecular work and revised the MS.

Funding

The molecular part of this work was supported by the Staatliche Naturwissenschaftliche Sammlungen Bayerns [SNSBinnovativ to AB]. Logistic support was provided by the National Fund for Scientific and Technological Development [FONDECYT 1118745 to AC-K] and the Instituto Antártico Chileno [RT-2716 to AC-K].

Supplementary material

13199_2019_624_MOESM1_ESM.docx (48 kb)
ESM 1 (DOCX 48 kb)
13199_2019_624_MOESM2_ESM.docx (28 kb)
ESM 2 (DOCX 27 kb)
13199_2019_624_MOESM3_ESM.xlsx (24 kb)
ESM 3 (XLSX 24 kb)
13199_2019_624_Fig7_ESM.png (700 kb)
Fig. S1

Phylogenetic relationships of Placopsis contortuplicata (PC) and P. antarctica (PA) photobionts and its allies. The phylogeny is based on ITS2 sequences and the topology shown here is the result of the Maximum Likelihood analysis. Bootstrap percentage values ≥70% are indicated at branches, followed by Shimodaira-Hasegawa values ≥0.70. Stars indicate Bayesian Posterior Probability values ≥0.95. AB-numbers refer to cultures. Stichococcus allas and S. antarcticus accessions are coloured according to their collection locality. Black letters indicate additional taxa from Antarctica. Abbreviations: Ar = Ardley, By = Byers Peninsula, Co = Coppermine Peninsula, DI = Deception Island, FI = Fildes Peninsula, KGI = King George Island, LI = Livingston Island, Po = Potter Peninsula, RI = Roberts Island; C = Centre, E = East, NE = Northeast, NW = Northwest, S = South, SE = Southeast, SW = Southwest, W = West. (PNG 699 kb)

13199_2019_624_MOESM4_ESM.eps (7 mb)
High Resolution Image (EPS 7135 kb)
13199_2019_624_Fig8_ESM.png (248 kb)
Fig. S2

Green algal photobiont haplotype network based on rbcL sequences. AU = Austria Ötztal Alps, DI = Deception Island, KGI = King George Island, LI = Livingston Island, RI = Robert Island. (PNG 248 kb)

13199_2019_624_MOESM5_ESM.eps (47 kb)
High Resolution Image (EPS 46 kb)
13199_2019_624_Fig9_ESM.png (113 kb)
Fig. S3

Green algal photobiont haplotype network based on rbcL and ITS sequences. AU = Austria Ötztal Alps, CH = Switzerland Urner Alps, DI = Deception Island, KGI = King George Island, LI = Livingston Island, RI = Robert Island. (PNG 112 kb)

13199_2019_624_MOESM6_ESM.eps (63 kb)
High Resolution Image (EPS 62 kb)

References

  1. Ahmadjian V (2001) Trebouxia: reflections on a perplexing and controversial lichen photobiont. In: Seckbach J (ed) Symbiosis. Springer, Houten, pp 373–383Google Scholar
  2. Akaike H (1973) Information theory as an extension of the maximum likelihood principle. In: Petrov BN, Csâki F (eds) Second International Symposium on Information Theory. Akadémia Kiado, Budapest, pp 267–281Google Scholar
  3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefGoogle Scholar
  4. Armstrong R (2011) The biology of the crustose lichen Rhizocarpon geographicum. Symbiosis 55:53–67.  https://doi.org/10.1007/s13199-011-0147-x CrossRefGoogle Scholar
  5. Beck A (2002) Selektivität der Symbionten schwermetalltoleranter Flechten. PhD thesis, Ludwig-Maximilians-Universität München, Munich, ISBN: 3-9808102-0-8Google Scholar
  6. Beck A, Koop H-U (2001) Analysis of the photobiont population in lichens using a single-cell manipulator. Symbiosis 31:57–67Google Scholar
  7. Beck A, Mayr C (2012) Nitrogen and carbon isotope variability in the green-algal lichen Xanthoria parietina and their implications on mycobiont-photobiont interactions. Ecol Evol 2:3132–3144CrossRefGoogle Scholar
  8. Belnap J, Büdel B, Lange OL (2001) Biological soil crusts: characteristics and distribution. In: Belnap J, Lange OL (eds) Biological Soil Crusts: Structure, Function, and Management. Ecological Studies (Analysis and Synthesis), vol 150. Springer, BerlinGoogle Scholar
  9. Birkenmajer K (1992) Volcanic succession at Deception Island, West Antarctica: a revised lithostratigraphic standard. Studia Geologica Polonica 101:27–82Google Scholar
  10. Bohuslavová O, Macek P, Redcenko O, Láska K, Nedbalová L, Elster J (2018) Dispersal of lichens along a successional gradient after deglaciation of volcanic mesas on northern James Ross Island, Antarctic Peninsula. Polar Biol 41:2221–2232CrossRefGoogle Scholar
  11. Borchhardt N, Schiefelbein U, Abarca N, Boy J, Mikhai-lyuk T, Sipman HJM, Karsten U (2017) Diversity of algae and lichens in biological soil crusts of Ardley and King George islands, Antarctica. Antarct Sci 29:229–237CrossRefGoogle Scholar
  12. Boy J, Godoy R, Shibistova O, Boy D, McCulloch R, De La Fuente AA, Morales MA, Mikutta R, Guggenberger G (2016) Successional patterns along soil development gradients formed by glacier retreat in the Maritime Antarctic, King George Island. Rev Chil Hist Nat 89.  https://doi.org/10.1186/s40693-016-0056-8
  13. Breen K, Lévesque E (2008) The influence of biological soil crusts on soil characteristics along a High Arctic Glacier Fore-land, Nunavut, Canada. Arct Antarct Alp Res 40:287–297CrossRefGoogle Scholar
  14. Casano LM, Del Campo EM, García-Breijo FJ, Reig-Armiñana J, Gasulla F, Del Hoyo A, Guéra A, Barreno E (2011) Two Trebouxia algae with different physiological performances are ever-present in lichen thalli of Ramalina farinacea. Coexistence versus competition? Environ Microbiol 13:806–818CrossRefGoogle Scholar
  15. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659CrossRefGoogle Scholar
  16. Darriba D, Taboada GL, Doallo R, Posada D (2012) JModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772CrossRefGoogle Scholar
  17. De los Ríos A, Raggio J, Pérez-Ortega S, Vivas M, Pintado A, Green TGA, Ascaso C, Sancho LG (2011) Anatomical, morphological and ecophysiological strategies in Placopsis pycnotheca (lichenized fungi, Ascomycota) allowing rapid colonization of recently deglaciated soils. Flora-Morphology, Distribution, Functional Ecology of Plants 206:857–864CrossRefGoogle Scholar
  18. De Wever A, Leliaert F, Verleyen E, Vanormelingen P, Van der Gucht K, Hodgson DA, Sabbe K, Vyverman W (2009) Hidden levels of phylodiversity in Antarctic green algae: further evidence for the existence of glacial refugia. Proc R Soc Lond B Biol Sci 276:3591–3599CrossRefGoogle Scholar
  19. Domaschke S, Fernández-Mendoza F, García MA, Martín M, Printzen C (2012) Low genetic diversity in Antarctic populations of the lichen-forming ascomycete Cetraria aculeata and its photobiont. Polar Res 31:17353–17366CrossRefGoogle Scholar
  20. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973CrossRefGoogle Scholar
  21. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461CrossRefGoogle Scholar
  22. Edgar RC (2016) UCHIME2: Improved chimera detection for amplicon sequences.  https://doi.org/10.1101/074252
  23. Engelen A, Convey P, Popa O, Ott S (2016) Lichen photobiont diversity and selectivity at the southern limit of the maritime Antarctic region (Coal Nunatak, Alexander Island). Polar Biol 39:2403–2410CrossRefGoogle Scholar
  24. Ettl H, Gärtner G (2014) Syllabus der Boden-, Luft- und Flechtenalgen. Springer, BerlinCrossRefGoogle Scholar
  25. Favero-Longo SE, Worland MR, Convey P, Lewis-Smith RI, Piervittori R, Guglielmin M, Cannone N (2012) Primary succession of lichen and bryophyte communities following glacial recession on Signy Island, South Orkney Islands, Maritime Antarctic. Antarct Sci 24:323–336CrossRefGoogle Scholar
  26. Fermani P, Mataloni G, Van de Vijver B (2007) Soil microalgal communities on an Antarctic active volcano (Deception Island, South Shetlands). Polar Biol 30:1381–1393CrossRefGoogle Scholar
  27. Fernández-Mendoza F, Domaschke S, García MA, Jordan P, Martín MP, Printzen C (2011) Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata. Mol Ecol 20:1208–1232CrossRefGoogle Scholar
  28. Frey B, Bühler L, Schmutz S, Zumsteg A, Furrer G (2013) Molecular characterization of phototrophic microorganisms in the forefield of a receding glacier in the Swiss Alps. Environ Res Lett 8:015033CrossRefGoogle Scholar
  29. Fourcade NH (1972) Vulcanismo de la Isla Decepción. Contribución Del Instituto Antartico Argentino 148:1–18Google Scholar
  30. Galloway DJ, Lewis-Smith RI, Quilhot W (2005) A new species of Placopsis (Agyriaceae: Ascomycota) from Antarctica. Lichenologist 37:321–327CrossRefGoogle Scholar
  31. Garrido-Benavent I, de los Ríos A, Fernández-Mendoza F, Pérez-Ortega S (2018) No need for stepping stones: Direct, joint dispersal of the lichen-forming fungus Mastodia tessellata (Ascomycota) and its photobiont explains their bipolar distribution. J Biogeogr 45:213–224CrossRefGoogle Scholar
  32. Haugland JE, Beatty SW (2005) Vegetation establishment, succession and microsite frost disturbance on glacier forelands within patterned ground chronosequences. J Biogeogr 32:145–153CrossRefGoogle Scholar
  33. Hertel H (1988) Problems in monographing Antarctic crustose lichens. Polarforschung 58:65–76Google Scholar
  34. Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing the confidence in phylogenetic analysis. Syst Biol 42:182–192CrossRefGoogle Scholar
  35. Hjört C, Björck S, Ingólfsson O, Möller P (1998) Holocene deglaciation and climate history of the northern Antarctic Peninsula region: a discussion of correlations between the Southern and Northern Hemispheres. Ann Glaciol 27:110–112CrossRefGoogle Scholar
  36. Hodač L, Hallmann C, Spitzer K, Elster J, Faßhauer F, Brinkmann N, Lepka D, Diwan V, Friedl T (2016) Widespread green algae Chlorella and Stichococcus exhibit polar-temperate and tropical-temperate biogeography. FEMS Microbiol Ecol 92:fiw122CrossRefGoogle Scholar
  37. Jones TC, Hogg ID, Wilkins RJ, Green TGA (2013) Photobiont selectivity for lichens and evidence for a possible glacial refugium in the Ross Sea Region, Antarctica. Polar Biol 36:767–774CrossRefGoogle Scholar
  38. Khan N, Tuffin M, Stafford W, Cary C, Lacap DC, Pointing SB, Cowan D (2011) Hypolithic microbial communities of quartz rocks from Miers Valley, McMurdo Dry Valleys, Antarctica. Polar Biol 34:1657–1668CrossRefGoogle Scholar
  39. Kvíderová J, Lukavský J (2005) The comparison of ecological characteristics of Stichococcus (Chlorophyta) strains isolated from polar and temperate regions. Algol Stud 118:127–140CrossRefGoogle Scholar
  40. Lamb IM (1947) A monograph of the lichen genus Placopsis Nyl. Lilloa 13:151–288Google Scholar
  41. Larget B, Simon DL (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol Biol Evol 16:750–759CrossRefGoogle Scholar
  42. Leavitt SD, Kraichak E, Nelsen MP, Altermann S, Divakar PK, Alors D, Esslinger TL, Crespo A, Lumbsch HT (2015) Fungal specificity and selectivity for algae play a major role in determining lichen partnerships across diverse ecogeographic regions in the lichen-forming family Parmeliaceae (Ascomycota). Mol Ecol 24:3779–3797CrossRefGoogle Scholar
  43. Lee JR, Raymond B, Bracegirdle TJ, Chadès I, Fuller RA, Shaw JD, Terauds A (2017) Climate change drives expansion of Antarctic ice-free habitat. Nature 547:49–54CrossRefGoogle Scholar
  44. Liu K, Warnow TJ, Holder MT, Nelesen SM, Yu J, Stamatakis AP, Linder CR (2012) SATe-II: very fast and accurate simultaneous estimation of multiple sequence alignments and phylogenetic trees. Syst Biol 61:90–106CrossRefGoogle Scholar
  45. López-Martínez J, Serrano E (2002) Geomorphology. In: López-Martínez J, Smellie JL, Thomson JW, Thomson MRA (eds) Geology and geomorphology of Deception Island. British Antarctic Survey. Natural Environment Research Council, Cambridge, pp 31–39Google Scholar
  46. Mäusbacher R (1991) Die jungquartäre Relief- und Klimageschichte im Bereich der Fildeshalbinsel Süd-Shetland-Inseln, Antarktis. Heidelberger Geographische Arbeiten 89Google Scholar
  47. Matheny PB, Liu YJ, Ammirati JF, Hall BD (2002) Using RPB1 and RPB2 nucleotide sequences (Inocybe; Agaricales). Am J Bot 89:688–698CrossRefGoogle Scholar
  48. Medhaug I, Stolpe MB, Fischer EM, Knutti R (2017) Reconciling controversies about the ‘global warming hiatus’. Nature 545:41–47CrossRefGoogle Scholar
  49. Meredith MP, King JC (2005) Rapid climate change in the ocean west of the Antarctic Peninsula during the second half of the 20th century. Geophys Res Lett 32:L19604Google Scholar
  50. Michel RFM, Schaefer CEGR, López-Martínez J, Simas FNB, Haus NW, Serrano E, Bockheim JG (2014) Soils and landforms from Fildes Peninsula and Ardley Island, Maritime Antarctica. Geomorphology 225:76–86CrossRefGoogle Scholar
  51. Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for Inference of Large Phylogenetic Trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010, New Orleans, LA, U.S.A., pp 1–8Google Scholar
  52. Mink S, López-Martínez J, Maestro A, Garrote J, Ortega JA, Serrano E, Durán JJ, Schmid T (2014) Insights into deglaciation of the largest ice-free area in the South Shetland Islands (Antarctica) from quantitative analysis of the drainage system. Geomorphology 225:4–24CrossRefGoogle Scholar
  53. Müller K, Müller J, Neinhuis C, Quandt D (2010) PhyDE: Phylogenetic Data Editor, version 0.9971, computer program [online], http://www.phyde.de
  54. Muggia L, Leavitt S, Barreno E (2018) The hidden diversity of lichenized Trebouxiophyceae (Chlorophyta). Phycologia 57:503–524CrossRefGoogle Scholar
  55. Nascimbene J, Mayrhofer H, Dainese M, Bilovitz PO (2017) Assembly patterns of soil-dwelling lichens after glacier retreat in the European Alps. J Biogeogr 44:1393–1404CrossRefGoogle Scholar
  56. Nelsen MP, Rivas Plata E, Andrew CJ, Lücking R, Lumbsch HT (2011) Phylogenetic diversity of trentepohlialean algae associated with lichen-forming fungi. J Phycol 47:282–290CrossRefGoogle Scholar
  57. Neustupa J, Eliáš M, Šejnohová L (2007) A taxonomic study of two Stichococcus species (Trebouxiophyceae, Chlorophyta) with a starch-enveloped pyrenoid. Nova Hedwigia 84:51–63CrossRefGoogle Scholar
  58. Nolan C, Overpeck JO, Allen JRM, Anderson PM, Betancourt JL, Binney HA, Brewer S, Bush MB, Chase BM, Cheddadi R, Djamali M, Dodson J, Edwards ME, Gosling WD, Haberle S, Hotchkiss SC, Huntley B, Ivory SJ, Kershaw AP, Kin S-H, Latorre C, Leydet M, Lézine A-M, Liu K-B, Liu Y, Lozhkin AV, McGlone MS, Marchant RA, Momohara A, Moreno A, Müller S, Otto-Bliesner BL, Shen C, Stevenson J, Takahara H, Tarasov PE, Tipton J, Vincens A, Weng C, Xu Q, Zheng Z, Jackson ST (2018) Past and future global transformation of terrestrial ecosystems under climate change. Science 361:920–923CrossRefGoogle Scholar
  59. Ó Cofaigh C, Davies BJ, Livingstone SJ, Johnson JS, Smith JA, Anderson JB, Bentley MJ, Canals M, Domack E, Dowsdeswell JA, Evans J, Glasser NF, Hillenbrand C-D, Larter RD, Roberts SJ, Simms AR (2014) Reconstruction of ice-sheet changes in the Antarctic Peninsula since the Last Glacial Maximum. Quat Sci Rev 100:87–110CrossRefGoogle Scholar
  60. Olech M (2004) Lichens of King George Island, Antarctica. Drukarnia Uniwersytetu Jagiellńskiego, KrakówGoogle Scholar
  61. Oliva M, Antoniades D, Giralt S, Granados I, Pla S, Toro M, Sanjurjo J, Liu EJ, Vieira G (2016) The Holocene deglaciation of the Byers Peninsula (Livingston Island, Antarctica) based on the dating of lake sedimentary records. Geomorphology 261:89–102CrossRefGoogle Scholar
  62. Olsacher J (1956) Contribución a la geología de la Antártida Occidental: I. Contribución al conocimiento geológico de la Isla Decepción. Contribución Del Instituto Antartico Argentino 2:1–76Google Scholar
  63. Øvstedal D, Lewis-Smith R (2001) Lichens of Antarctica and South Georgia, A Guide to their identification and ecology. Cambridge University Press, CambridgeGoogle Scholar
  64. Pattengale ND, Alipour M, Bininda-Emonds OR, Moret BM, Stamatakis A (2010) How many bootstrap replicates are necessary? J Comput Biol 17:337–354CrossRefGoogle Scholar
  65. Peksa O, Škaloud P (2011) Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Mol Ecol 20:3936–3948CrossRefGoogle Scholar
  66. Pérez-Ortega S, de los Ríos A, Crespo A, Sancho LG (2010) Symbiotic lifestyle and phylogenetic relationships of the bionts of Mastodia tessellata (Ascomycota, incertae sedis). Am J Bot 97:738–752CrossRefGoogle Scholar
  67. Pérez-Ortega S, Ortiz-Álvarez R, Green TGA, de los Ríos A (2012) Lichen myco- and photobiont diversity and their relationships at the edge of life (McMurdo Dry Valleys, Antarctica). FEMS Microbiol Ecol 82:429–448CrossRefGoogle Scholar
  68. Pessi IS, Pushkareva E, Lara Y, Borderie F, Wilmotte A, Elster J (2018) Marked succession of cyanobacterial communities following glacier retreat in the High Arctic. Microb Ecol.  https://doi.org/10.1007/s00248-018-1203-3
  69. Poelking EL, Schaefer CER, Fernandes Filho EI, de Andrade AM, Spielmann AA (2014) Soil-landform-plant communities relationships of a periglacial landscape at Potter Peninsula, Maritime Antarctica. Solid Earth Discussions 6:2261–2292CrossRefGoogle Scholar
  70. Posada D (2005) TCS 1.21 manual. Retrieved from: http://w3.ualg.pt/~rcastil/SOFTWARE_WINDOWS/TCS1.21/docs/TCS1.21.pdf
  71. Pushkareva E, Pessi IS, Wilmotte A, Elster J (2015) Cyanobacterial community composition and impact of nutrient availability in Arctic soil crusts at different stages of development. FEMS Microbiol Ecol 91:fiv143.  https://doi.org/10.1093/femsec/fiv143 CrossRefGoogle Scholar
  72. Pushkareva E, Kvíderová J, Šimek M, Elster J (2017) Nitrogen fixation and diurnal changes of photosynthetic activity in Arctic soil crusts at different development state. Eur J Soil Biol 79:21–31CrossRefGoogle Scholar
  73. Raggio J, Green TGA, Crittenden PD, Pintado A, Vivas M, Pérez-Ortega S, de los Ríos A, Sancho LG (2012) Comparative ecophysiology of three Placopsis species, pioneer lichens in recently exposed Chilean glacial forelands. Symbiosis 56:55–66CrossRefGoogle Scholar
  74. Rindi F, Allali HA, Lam DW, López-Bautista JM (2010) An overview of the biodiversity and biogeography of terrestrial green algae. In: Rescigno V, Maletta S (eds) Biodiversity hotspots. Nova Science Publishers, Hauppauge, pp 105–122Google Scholar
  75. Rippin M, Lange S, Sausen N, Becker B (2018) Biodiversity of biological soil crusts from the Polar Regions revealed by metabarcoding. FEMS Microbiol Ecol 94:fiy036CrossRefGoogle Scholar
  76. Rodriguez JM, Passo A, Chiapella JO (2018) Lichen species assemblage gradient in South Shetlands Islands, Antarctica: relationship to deglaciation and microsite conditions. Polar Biol 41:523–531CrossRefGoogle Scholar
  77. Romeike J, Friedl T, Helms G, Ott S (2002) Genetic diversity of algal and fungal partners in four species of Umbilicaria (lichenized ascomycetes) along a transect of the Antarctic Peninsula. Mol Biol Evol 19:1209–1207CrossRefGoogle Scholar
  78. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefGoogle Scholar
  79. Roy-Ocotla G, Carrera J (1993) Aeroalgae: response to some aerobiological questions. Grana 32:48–56CrossRefGoogle Scholar
  80. Ruprecht U, Brunauer G, Printzen C (2012) Genetic diversity of photobionts in Antarctic lecideoid lichens from an ecological view point. Lichenologist 44:661–678CrossRefGoogle Scholar
  81. Sancho LG, Schulz F, Schroeter B, Kappen L (1999) Bryophyte and lichen flora of South Bay (Livingston Island: South Shetland Islands, Antarctica). Nova Hedwigia 68:301–337Google Scholar
  82. Schmidt SK, Reed SC, Nemergut DR, Grandy AS, Cleveland CC, Weintraub MN, Hill AW, Costello EK, Meyer AF, Neff JC et al (2008) The earliest stages of ecosystem succession in high-elevation (5000 metres above sea level), recently deglaciated soils. Proc R Soc B Biol Sci 275:2793–2802CrossRefGoogle Scholar
  83. Schmitt I, Lumbsch HT, Søchting U (2003) Phylogeny of the lichen genus Placopsis and its allies based on Bayesian analyses of nuclear and mitochondrial sequences. Mycologia 95:827–835CrossRefGoogle Scholar
  84. Seong YB, Owen LA, Lim HS, Yoon HI, Kim Y, Lee YI, Caffee MW (2009) Rate of late Quaternary ice-cap thinning on King George Island, South Shetland Islands, West Antarctica defined by cosmogenic 36Cl surface exposure dating. Boreas 38:207–213CrossRefGoogle Scholar
  85. Simões JC (2011) O papel do gelo antártico no sistema climático. In: Goldemberg J (ed) Antártica e as mudanḉas globais: um desafio para a humanidade 9. Blucher, São Paulo, pp 69–101Google Scholar
  86. Simoes CL, da Rosa KK, Czapela FF, Vieira R, Simoes JC (2015) Collins Glacier Retreat Process and Regional Climatic Variations, King George Island, Antarctica. Geogr Rev 105:462–471CrossRefGoogle Scholar
  87. Soler-Membrives A, Linse K, Miller KJ, Arango CP (2017) Genetic signature of Last Glacial Maximum regional refugia in a circum-Antarctic sea spider. R Soc Open Sci 4:170615.  https://doi.org/10.1098/rsos.170615 CrossRefGoogle Scholar
  88. Spielmann AA, Pereira AB (2012) Lichens on the Maritime Antarctica. Glalia 4:1–28Google Scholar
  89. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313CrossRefGoogle Scholar
  90. Stamatakis A (2016) The RAxML v8.2.X Manual. Heidelberg Institute for Theoretical Studies. http://sco.h-its.org/exelixis/web/software/raxml/#documentation. (5 June 2018, date last accessed)
  91. Stamatakis A, Hoover P, Rougemont P (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771CrossRefGoogle Scholar
  92. Stiller JW, Hall BD (1997) The origin of red algae: implications for plastid evolution. Proc Natl Acad Sci U S A 94:4520–4525CrossRefGoogle Scholar
  93. Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods), Version 4 edn. Sinauer Associates, SunderlandGoogle Scholar
  94. Thüs H, Muggia L, Pérez-Ortega S, Favero-Longo SE, Joneson S, O'Brien H, Nelsen MP, Duque-Thüs R, Grube M, Friedl T et al (2011) Revisiting photobiont diversity in the lichen family Verrucariaceae (Ascomycota). Eur J Phycol 46:399–415CrossRefGoogle Scholar
  95. Tibell L (2001) Photobiont association and molecular phylogeny of the lichen genus Chaenotheca. Bryologist 104:191–198CrossRefGoogle Scholar
  96. Tishkov RJ (1986) Primary succession in Arctic tundra on the west coast of Spitsbergen (Svalbard). Polar Geogr Geol 10:148–156CrossRefGoogle Scholar
  97. Turner J, Colwell SR, Marshall GJ, Lachlan-Cope TA, Carleton AM, Jones PD, Lagun V, Reid PA, Iagovkina S (2005) Antarctic climate change during the last 50 years. Int J Climatol 25:279–294CrossRefGoogle Scholar
  98. Turner J, Lu H, White I et al (2016) Absence of 21st century warming on Antarctic Peninsula consistent with natural variability. Nature 535:411–415CrossRefGoogle Scholar
  99. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Shinsky J, White T (eds) PCR Protocols: A Guide to Methods and Applications. Academic Press, London, pp 315–322Google Scholar
  100. Wirtz N, Lumbsch HT, Green TGA, Türk R, Pintado A, Sancho L, Schroeter B (2003) Lichen fungi have low cyanobiont selectivity in maritime Antarctica. New Phytol 160:177–183CrossRefGoogle Scholar
  101. Zahradníková M, Andersen HL, Tønsberg T, Beck A (2018) Molecular evidence of Apatococcus, including A. fuscideae sp. nov., as photobiont in the genus Fuscidea. Protist 168:425–438CrossRefGoogle Scholar
  102. Zidarova R (2008) Algae from Livingston Island (S Shetland Islands): a checklist. Phytologia Balcanica 14:19–35Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Botanische Staatssammlung MünchenSNSBMunichGermany
  2. 2.GeoBio-CenterLudwig-Maximilians-Universität MünchenMunichGermany
  3. 3.Nees Institute for Biodiversity of PlantsUniversity of BonnBonnGermany
  4. 4.Núcleo de Estudios Ambientales, Facultad de Recursos NaturalesUniversidad Católica de TemucoTemucoChile

Personalised recommendations