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Polar Biology

, Volume 35, Issue 3, pp 387–399 | Cite as

Assessment of soil bacterial communities on Alexander Island (in the maritime and continental Antarctic transitional zone)

  • C. W. Chong
  • P. Convey
  • D. A. Pearce
  • I. K. P. Tan
Original Paper

Abstract

Despite an increasing number of Antarctic soil diversity assessments, understanding of the bacterial community composition in the arid soil environments of the maritime/continental Antarctic transitional zone remains lacking. Most documented microbiological studies had focused on either the wetter environments of the Antarctic Peninsula/Scotia arc or the exceptionally arid deserts of the Dry Valleys of continental Antarctica. In this study, soil bacterial diversity from three relatively arid sites on Alexander Island and the physicochemical parameters that might influence it were assessed. In general, the study sites exhibited levels of pH, hydration and metal content different from previous reports of maritime or continental Antarctic soil habitats. Although the soil from Alexander Island exhibited similar phylum-level bacterial taxonomic composition to those of other cold and arid environments, each study site was found to harbour significantly different bacterial assemblages. The latter finding was supported by three complementary molecular methods selected to address different elements of diversity. Our analyses of the measured parameters suggest that the differences in bacterial communities were best explained by soil pH and copper content. Using these data, we suggest that soil pH might play an important role in structuring bacterial assemblage patterns across polar soils.

Keywords

DGGE T-RFLP Cloning Bacterial diversity pH 

Notes

Acknowledgments

This project was funded by the Malaysian Antarctic Research Programme (MARP), and the British Antarctic Survey (BAS) provided logistic support and field training. We thank Roger Worland and Paul Dennis for assistance in sample collection. The paper also contributes to the BAS ‘Polar Science for Planet Earth’ and SCAR ‘Evolution and Biodiversity in Antarctica’ programmes.

Supplementary material

300_2011_1084_MOESM1_ESM.doc (275 kb)
Supplementary material 1 (DOC 275 kb)
300_2011_1084_MOESM2_ESM.doc (929 kb)
Supplementary material 2 (DOC 929 kb)

References

  1. Abdo Z, Schüette UME, Bent SJ, Williams CJ, Forney LJ, Joyce P (2006) Statistical methods for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes. Environ Microbiol 8:929–938. doi: 10.1111/j.1462-2920.2005.00959.x PubMedCrossRefGoogle Scholar
  2. Aislabie JM, Chhour KL, Saul DJ, Miyauchi S, Ayton J, Paetzold RF, Balks MR (2006) Dominant bacteria in soils of Marble Point and Wright Valley, Victoria Land, Antarctica. Soil Biol Biochem 38:3041–3056. doi: 10.1016/j.soilbio.2006.02.018 CrossRefGoogle Scholar
  3. Aislabie JM, Jordan S, Barker GM (2008) Relation between soil classification and bacterial diversity in soils of the Ross Sea region, Antarctica. Geoderma 144:9–20. doi: 10.1016/j.geoderma.2007.10.006 CrossRefGoogle Scholar
  4. An D-S, Lee H-G, Im W-T, Liu Q-M, Lee S-T (2007) Segetibacter koreensis gen. nov., sp. nov., a novel member of the phylum Bacteroidetes, isolated from the soil of a ginseng field in South Korea. Int J Syst Evol Microbiol 57:1828–1833. doi: 10.1099/ijs.0.64803-0 PubMedCrossRefGoogle Scholar
  5. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46. doi: 10.1111/j.1442-9993.2001.01070.pp.x Google Scholar
  6. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA + for PRIMER: guide to software and statistical methods. PRIMER-E, PlymouthGoogle Scholar
  7. André M-F, Hall K (2005) Honeycomb development on Alexander Island, glacial history of George VI sound and palaeoclimatic implications (two step Cliffs/Mars Oasis, W Antarctica). Geomorphology 65:117–138CrossRefGoogle Scholar
  8. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ (2005) At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl Environ Microbiol 71:7724–7736. doi: 10.1128/AEM.71.12.7724-7736.2005 PubMedCrossRefGoogle Scholar
  9. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ (2006) New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Appl Environ Microbiol 72:5734–5741. doi: 10.1128/AEM.00556-06 PubMedCrossRefGoogle Scholar
  10. Bååth E (1996) Adaptation of soil bacterial communities to prevailing pH in different soils. Fems Microbiol Ecol 19:227–237. doi: 10.1111/j.1574-6941.1996.tb00215.x CrossRefGoogle Scholar
  11. Booth IR (1985) Regulation of cytoplasmic pH in bacteria. Microbiol Rev 49:359–378PubMedGoogle Scholar
  12. Bridge PD, Newsham KK (2009) Soil fungal community composition at Mars Oasis, a southern maritime Antarctic site, assessed by PCR amplification and cloning. Fungal Ecol 2:66–74. doi: 10.1016/j.funeco.2008.10.008 CrossRefGoogle Scholar
  13. Cary SC, McDonald IR, Barrett JE, Cowan DA (2010) On the rocks: the microbiology of Antarctic Dry Valley soils. Nat Rev Microbiol 8:129–138. doi: 10.1038/Nrmicro2281 PubMedCrossRefGoogle Scholar
  14. Chong CW, Dunn MJ, Convey P, Tan GYA, Wong RCS, Tan IKP (2009a) Environmental influences on bacterial diversity of soils on Signy Island, maritime Antarctic. Polar Biol 32:1571–1582. doi: 10.1007/s00300-009-0656-8 CrossRefGoogle Scholar
  15. Chong CW, Tan GYA, Wong RCS, Riddle MJ, Tan IKP (2009b) DGGE fingerprinting of bacteria in soils from eight ecologically different sites around Casey Station, Antarctica. Polar Biol 32:853–860. doi: 10.1007/s00300-009-0585-6 CrossRefGoogle Scholar
  16. Chong CW, Pearce DA, Convey P, Tan GYA, Wong RCS, Tan IKP (2010) High levels of spatial heterogeneity in the biodiversity of soil prokaryotes on Signy Island, Antarctica. Soil Biol Biochem 42:601–610. doi: 10.1016/j.soilbio.2009.12.009 CrossRefGoogle Scholar
  17. Chown SL, Convey P (2007) Spatial and temporal variability across life’s hierarchies in the terrestrial Antarctic. Philos Trans R Soc B 362:2307–2331. doi: 10.1098/rstb.2006.1949 CrossRefGoogle Scholar
  18. Chu H, Fierer N, Lauber CL, Caporaso JG, Knight R, Grogan P (2010) Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environ Microbiol 12:2998–3006. doi: 10.1111/j.1462-2920.2010.02277.x PubMedCrossRefGoogle Scholar
  19. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145. doi: 10.1093/nar/gkn879 PubMedCrossRefGoogle Scholar
  20. Connon SA, Lester ED, Shafaat HS, Obenhuber DC, Ponce A (2007) Bacterial diversity in hyperarid Atacama Desert soils. J Geophys Res 112:G04S17. doi: 10.1029/2006jg000311
  21. Convey P (2006) Antarctic climate change and its influences on terrestrial ecosystems. In: Bergstrom DM, Convey P, Huiskes AHL (eds) Trends in Antarctic terrestrial and limnetic ecosystems. Springer, Netherlands, pp 253–272. doi: 10.1007/1-4020-5277-4_12
  22. Convey P, Smith RIL (1997) The terrestrial arthropod fauna and its habitats in northern Marguerite Bay and Alexander Island, maritime Antarctic. Antarct Sci 9:12–26CrossRefGoogle Scholar
  23. Cooksey DA (1993) Copper uptake and resistance in bacteria. Mol Microbiol 7:1–5. doi: 10.1111/j.1365-2958.1993.tb01091.x PubMedCrossRefGoogle Scholar
  24. Costello EK, Halloy SRP, Reed SC, Sowell P, Schmidt SK (2009) Fumarole-supported islands of biodiversity within a Hyperarid, high-elevation landscape on Socompa Volcano, Puna de Atacama, Andes. Appl Environ Microb 75:735–747. doi: 10.1128/Aem.01469-08 CrossRefGoogle Scholar
  25. Culman SW, Bukowski R, Gauch HG, Cadillo-Quiroz H, Buckley DH (2009) T-REX: software for the processing and analysis of T-RFLP data. BMC Bioinformatics 10:171. doi: 10.1186/1471-2105-10-171 PubMedCrossRefGoogle Scholar
  26. DeSantis TZ Jr, Hugenholtz P, Keller K, Brodie EL, Larsen N, Piceno YM, Phan R, Andersen GL (2006) NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res 34:W394–W399. doi: 10.1093/nar/gkl244 PubMedCrossRefGoogle Scholar
  27. Engelen A, Convey P, Hodgson DA, Worland MR, Ott S (2008) Soil properties of an Antarctic inland site: implications for ecosystem development. Polar Biol 31:1453–1460. doi: 10.1007/s00300-008-0486-0 CrossRefGoogle Scholar
  28. Enwall K, Hallin S (2009) Comparison of T-RFLP and DGGE techniques to assess denitrifier community composition in soil. Lett Appl Microbiol 48:145–148. doi: 10.1111/j.1472-765X.2008.02498.x PubMedCrossRefGoogle Scholar
  29. Fell JW, Scorzetti G, Connell L, Craig S (2006) Biodiversity of micro-eukaryotes in Antarctic Dry Valley soils with <5% soil moisture. Soil Biol Biochem 38:3107–3119CrossRefGoogle Scholar
  30. Ferreira AC, Nobre MF, Moore E, Rainey FA, Battista JR, da Costa MS (1999) Characterization and radiation resistance of new isolates of Rubrobacter radiotolerans and Rubrobacter xylanophilus. Extremophiles 3:235–238PubMedCrossRefGoogle Scholar
  31. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364PubMedCrossRefGoogle Scholar
  32. Ganzert L, Lipski A, Hubberten HW, Wagner D (2011) The impact of different soil parameters on the community structure of dominant bacteria from nine different soils located on Livingston Island, South Shetland Archipelago, Antarctica. FEMS Microbiol Ecol. doi: 10.1111/j.1574-6941.2011.01068.x
  33. González Garraza G, Mataloni G, Fermani P, Vinocur A (2011) Ecology of algal communities of different soil types from Cierva Point, Antarctic Peninsula. Polar Biol 34:339–351. doi: 10.1007/s00300-010-0887-8 CrossRefGoogle Scholar
  34. Good IJ (1953) The population frequencies of species and the estimation of population parameters. Biometrika 40:237–264. doi: 10.1093/biomet/40.3-4.237 Google Scholar
  35. Hamady M, Lozupone C, Knight R (2010) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4:17–27. doi: 10.1038/ismej.2009.97 PubMedCrossRefGoogle Scholar
  36. Hinojosa MB, Carreira JA, García-Ruíz R, Dick RP (2005) Microbial response to heavy metal-polluted soils. J Environ Qual 34:1789–1800. doi: 10.2134/jeq2004.0470 PubMedCrossRefGoogle Scholar
  37. Hogg ID, Cary SC, Convey P, Newsham KK, O’Donnell AG, Adams BJ, Aislabie J, Frati F, Stevens MI, Wall DH (2006) Biotic interactions in Antarctic terrestrial ecosystems: are they a factor? Soil Biol Biochem 38:3035–3040. doi: 10.1016/j.soilbio.2006.04.026 CrossRefGoogle Scholar
  38. Holdgate MW (1977) Terrestrial ecosystems in the Antarctic. Philos Trans R Soc Lond B Biol Sci 279:5–25. doi: 10.1098/rstb.1977.0068 CrossRefGoogle Scholar
  39. Hughes KA, Lawley B (2003) A novel Antarctic microbial endolithic community within gypsum crusts. Environ Microbiol 5:555–565. doi: 10.1046/j.1462-2920.2003.00439.x PubMedCrossRefGoogle Scholar
  40. Johnson M, Zaretskaya I, Raytselis Y, Merezhuk Y, McGinnis S, Madden TL (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36:W5–W9. doi: 10.1093/nar/gkn201 PubMedCrossRefGoogle Scholar
  41. Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3:442–453. http://www.nature.com/ismej/journal/v3/n4/suppinfo/ismej2008127s1.html Google Scholar
  42. Kunito T, Saeki K, Oyaizu H, Matsumoto S (1999) Influences of copper forms on the toxicity to microorganisms in soils. Ecotoxicol Environ Saf 44:174–181. doi: 10.1006/eesa.1999.1820 PubMedCrossRefGoogle Scholar
  43. Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415CrossRefGoogle Scholar
  44. Lawley B, Ripley S, Bridge P, Convey P (2004) Molecular analysis of geographic patterns of eukaryotic diversity in Antarctic soils. Appl Environ Microbiol 70:5963–5972. doi: 10.1128/Aem.70.10.5963-5972.2004 PubMedCrossRefGoogle Scholar
  45. Malosso E, Waite IS, English L, Hopkins DW, O’Donnell AG (2006) Fungal diversity in maritime Antarctic soils determined using a combination of culture isolation, molecular fingerprinting and cloning techniques. Polar Biol 29:552–561. doi: 10.1007/s00300-005-0088-z CrossRefGoogle Scholar
  46. Männistö MK, Tiirola M, Häggblom MM (2007) Bacterial communities in Arctic fjelds of Finnish Lapland are stable but highly pH-dependent. Fems Microbiol Ecol 59:452–465. doi: 10.1111/j.1574-6941.2006.00232.x PubMedCrossRefGoogle Scholar
  47. Margesin R, Sproer C, Schumann P, Schinner F (2003) Pedobacter cryoconitis sp. nov., a facultative psychrophile from alpine glacier cryoconite. Int J Syst Evol Microbiol 53:1291–1296. doi: 10.1099/ijs.0.02436-0 PubMedCrossRefGoogle Scholar
  48. Maslen NR, Convey P (2006) Nematode diversity and distribution in the southern maritime Antarctic—clues to history? Soil Biol Biochem 38:3141–3151. doi: 10.1016/j.soilbio.2005.12.007 CrossRefGoogle Scholar
  49. Mulder E, Deinema M (2006) The genus Haliscomenobacter. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 602–604. doi: 10.1007/0-387-30747-8_22
  50. Newsham KK, Pearce DA, Bridge PD (2010) Minimal influence of water and nutrient content on the bacterial community composition of a maritime Antarctic soil. Microbiol Res 165:523–530. doi: 10.1016/j.micres.2009.11.005 PubMedCrossRefGoogle Scholar
  51. Niederberger TD, McDonald IR, Hacker AL, Soo RM, Barrett JE, Wall DH, Cary SC (2008) Microbial community composition in soils of Northern Victoria Land, Antarctica. Environ Microbiol 10:1713–1724. doi: 10.1111/j.1462-2920.2008.01593.x PubMedCrossRefGoogle Scholar
  52. Oren A (2006) The genera Rhodothermus, Thermonema, Hymenobacter and Salinibacter. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 712–738. doi: 10.1007/0-387-30747-8_29
  53. Pearce DA, Hughes KA, Lachlan-Cope T, Harangozo SA, Jones AE (2010) Biodiversity of air-borne microorganisms at Halley station, Antarctica. Extremophiles 14:145–159. doi: 10.1007/s00792-009-0293-8 PubMedCrossRefGoogle Scholar
  54. Pointing SB, Chan Y, Lacap DC, Lau MCY, Jurgens JA, Farrell RL (2010) Highly specialized microbial diversity in hyper-arid polar desert. Proc Natl Acad Sci USA 107:1254. doi: 10.1073/pnas.0913882107 Google Scholar
  55. Potts M (1994) Desiccation tolerance of prokaryotes. Microbiol Rev 58:755–805PubMedGoogle Scholar
  56. Powell SM, Bowman JP, Snape I, Stark JS (2003) Microbial community variation in pristine and polluted nearshore Antarctic sediments. FEMS Microbiol Ecol 45:135–145. doi: 10.1016/s0168-6496(03)00135-1 PubMedCrossRefGoogle Scholar
  57. Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351. doi: 10.1038/ismej.2010.58 PubMedCrossRefGoogle Scholar
  58. Salam AK, Helmke PA (1998) The pH dependence of free ionic activities and total dissolved concentrations of copper and cadmium in soil solution. Geoderma 83:281–291CrossRefGoogle Scholar
  59. Sattin S, Cleveland C, Hood E, Reed S, King A, Schmidt S, Robeson M, Ascarrunz N, Nemergut D (2009) Functional shifts in unvegetated, perhumid, recently-deglaciated soils do not correlate with shifts in soil bacterial community composition. J Microbiol 47:673–681. doi: 10.1007/s12275-009-0194-7 PubMedCrossRefGoogle Scholar
  60. Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506. doi: 10.1128/AEM.71.3.1501-1506.2005 PubMedCrossRefGoogle Scholar
  61. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. doi: 10.1128/AEM.01541-09 PubMedCrossRefGoogle Scholar
  62. Smith RIL (1984) Terrestrial plant biology of the subantarctic and Antarctic. In: Laws RM (ed) Antarctic ecology, vol 1. Academic Press, London, pp 61–162Google Scholar
  63. Smith RIL (1988) Bryophyte oases in ablation valleys on Alexander Island, Antarctica. Bryologist 91:45–50CrossRefGoogle Scholar
  64. Smith CJ, Danilowicz BS, Clear AK, Costello FJ, Wilson B, Meijer WG (2005) T-Align, a web-based tool for comparison of multiple terminal restriction fragment length polymorphism profiles. Fems Microbiol Ecol 54:375–380. doi: 10.1016/j.femsec.2005.05.002 PubMedCrossRefGoogle Scholar
  65. Smith JJ, Tow LA, Stafford W, Cary C, Cowan DA (2006) Bacterial diversity in three different Antarctic cold desert mineral soils. Microb Ecol 51:413–421. doi: 10.1007/s00248-006-9022-3 PubMedCrossRefGoogle Scholar
  66. Snape I, Scouller RC, Stark SC, Stark J, Riddle MJ, Gore DB (2004) Characterisation of the dilute HCl extraction method for the identification of metal contamination in Antarctic marine sediments. Chemosphere 57:491–504PubMedCrossRefGoogle Scholar
  67. Solioz M, Odermatt A, Krapf R (1994) Copper pumping ATPases: common concepts in bacteria and man. FEBS Lett 346:44–47PubMedCrossRefGoogle Scholar
  68. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599. doi: 10.1093/molbev/msm092 PubMedCrossRefGoogle Scholar
  69. Usher MB, Booth RG (1986) Arthropod communities in a maritime Antarctic moss-turf habitat: multiple scales of pattern in the mites and Collembola. J Anim Ecol 55:155–170CrossRefGoogle Scholar
  70. Vincent WF (2000) Evolutionary origins of Antarctic microbiota: invasion, selection and endemism. Antarct Sci 12:374–385CrossRefGoogle Scholar
  71. Wakelin SA, Chu G, Lardner R, Liang Y, McLaughlin M (2010) A single application of Cu to field soil has long-term effects on bacterial community structure, diversity, and soil processes. Pedobiologia 53:149–158CrossRefGoogle Scholar
  72. Ward NL, Challacombe JF, Janssen PH, Henrissat B, Coutinho PM, Wu M, Xie G, Haft DH, Sait M, Badger J, Barabote RD, Bradley B, Brettin TS, Brinkac LM, Bruce D, Creasy T, Daugherty SC, Davidsen TM, DeBoy RT, Detter JC, Dodson RJ, Durkin AS, Ganapathy A, Gwinn-Giglio M, Han CS, Khouri H, Kiss H, Kothari SP, Madupu R, Nelson KE, Nelson WC, Paulsen I, Penn K, Ren Q, Rosovitz MJ, Selengut JD, Shrivastava S, Sullivan SA, Tapia R, Thompson LS, Watkins KL, Yang Q, Yu C, Zafar N, Zhou L, Kuske CR (2009) Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol 75:2046–2056. doi: 10.1128/aem.02294-08 Google Scholar
  73. Wood SA, Rueckert A, Cowan DA, Cary SC (2008) Sources of edaphic cyanobacterial diversity in the Dry Valleys of Eastern Antarctica. ISME J 2:308–320. doi: 10.1038/ismej.2007.104 PubMedCrossRefGoogle Scholar
  74. Wynn-Williams DD (1996) Antarctic microbial diversity: the basis of polar ecosystem processes. Biodivers Conserv 5:1271–1293CrossRefGoogle Scholar
  75. Xie C-H, Yokota A (2006) Reclassification of [Flavobacterium] ferrugineum as Terrimonas ferruginea gen. nov., comb. nov., and description of Terrimonas lutea sp. nov., isolated from soil. Int J Syst Evol Microbiol 56:1117–1121. doi: 10.1099/ijs.0.64115-0 PubMedCrossRefGoogle Scholar
  76. Yergeau E, Bokhorst S, Huiskes AHL, Boschker HTS, Aerts R, Kowalchuk GA (2007a) Size and structure of bacterial, fungal and nematode communities along an Antarctic environmental gradient. Fems Microbiol Ecol 59:436–451. doi: 10.1111/j.1574-6941.2006.00200.x PubMedCrossRefGoogle Scholar
  77. Yergeau E, Newsham KK, Pearce DA, Kowalchuk GA (2007b) Patterns of bacterial diversity across a range of Antarctic terrestrial habitats. Environ Microbiol 9:2670–2682. doi: 10.1111/j.1462-2920.2007.01379.x PubMedCrossRefGoogle Scholar
  78. Yoon M-H, Im W-T (2007) Flavisolibacter ginsengiterrae gen. nov., sp. nov. and Flavisolibacter ginsengisoli sp. nov., isolated from ginseng cultivating soil. Int J Syst Evol Microbiol 57:1834–1839. doi: 10.1099/ijs.0.65011-0 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • C. W. Chong
    • 1
  • P. Convey
    • 2
  • D. A. Pearce
    • 2
  • I. K. P. Tan
    • 1
  1. 1.Institute of Biological Sciences, Faculty of ScienceUniversity of MalayaKuala LumpurMalaysia
  2. 2.British Antarctic SurveyNERCCambridgeUK

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