Abstract
Microbial life flourishes in the ponds of the McMurdo Sound Region, which includes the McMurdo Dry Valleys (MDV) and the exposed coastal areas of Ross Island, Antarctica. Diatoms live within resident microbial mats, and because of the simplified trophic structure and limited dispersal vectors, the McMurdo Sound Region is an ideal locality to investigate diatom community assembly processes. Wind is hypothesized to transport microbiota between habitats, and following the species-sorting perspective, local conditions should act as an environmental filter. However, the role of spatial scale versus habitat characteristics on diatom community structure has not been investigated. To gain insight into these processes, we sampled microbial mats from 25 ponds and used variation partitioning to assess the spatial scales at which diatoms were influenced by chemistry and physical variables. We found substantial spatial structure in diatom communities, and spatial scale explained more variability than environmental variables. No diatoms were exclusive to Ross Island, but some species were only found in the MDVs. Furthermore, diatom communities were more likely to resemble those from other nearby ponds rather than distant ones, regardless of environmental conditions. Of the environmental variables, bromide and chloride (both indicators of marine influence) were among the most important. These results suggest that geography, dispersal, and historical environmental conditions play a major role in structuring diatom communities at large spatial scales, and chemistry may be more important within regions. These results help explain the biogeography of diatoms here and elsewhere and expand our knowledge of mechanisms influencing microbial metacommunity structure.
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References
Baas-Becking LGM (1934) Geobiologie of inleiding tot de Milieukunde. Van Stockum and Zoon, The Hague
Blanchet FG, Legendre P, Borcard D (2008a) Forward selection of explanatory variables. Ecology 89:2623–2632. doi:10.1890/07-0986.1
Blanchet FG, Legendre P, Borcard D (2008b) Modelling directional spatial processes in ecological data. Ecol Model 215:325–336. doi:10.1016/j.ecolmodel.2008.04.001
Borcard D, Legendre P (2002) All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecol Model 153:51–68. doi:10.1016/S0304-3800(01)00501-4
Borcard D, Legendre P, Drapeau P (1992) Partialling out the spatial component of ecological variation. Ecology 73:1045–1055. doi:10.2307/1940179
Broady PA (1989) Broadscale patterns in the distribution of aquatic and terrestrial vegetation at three icefree regions on Ross Island, Antarctica. In: Vincent W, Ellis-Evans C (eds) High latitude limnology. Kluwer, Dordrecht. Developments in Hydrobiology 49: 77–95. doi: 10.1007/978-94-009-2603-5_7
Broady PA (1996) Diversity, distribution and dispersal of Antarctic terrestrial algae. Biodivers Conserv 5:1307–1335. doi:10.1007/BF00051981
Brown A, McKnight DM, Chin YP, Roberts EC, Uhle M (2004) Chemical characterization of dissolved organic material in Pony Lake, a saline coastal pond in Antarctica. Mar Chem 89:327–337. doi:10.1016/j.marchem.2004.02.016
Davis SN, Whittemore DO, Fabryka-Martin J (1998) Uses of chloride/bromide ratios in studies of potable water. Groundwater 36:338–350. doi:10.1111/j.1745-6584.1998.tb01099.x
Doran PT, Priscu JC, Lyons WB, Walsh JE, Fountain AG, McKnight DM, Moorhead DL, Virginia RA, Wall DH, Clow GD, Fritsen CH, McKay CP, Parsons AN (2002) Antarctic climate cooling and terrestrial ecosystem response. Nature 415:517–520. doi:10.1038/nature710
Esposito RMM, Horn SL, McKnight DM, Cox MJ, Grant MC, Spaulding SA, Doran PT, Cozzetto KD (2006) Antarctic climate cooling and response of diatoms in glacial meltwater streams. Geophys Res Lett 33:L07406.1-L07406.4. doi: 10.1029/2006GL025903
Esposito RMM, Spaulding SA, McKnight DM, Van de Vijver B, Kopalová K, Lubinski D, Hall B, Whittaker T (2008) Inland diatoms from the McMurdo Dry Valleys and James Ross Island, Antarctica. Can J Botany 86:1378–1392. doi:10.1139/B08-100
Fenchel T, Finlay BJ (2004) The ubiquity of small species: patterns of local and global diversity. Bioscience 54:777–784. doi:10.1641/0006-3568(2004)054[0777:TUOSSP]2.0.CO;2
Fountain AG, Lyons WB, Burkins MB, Dana GL, Doran PT, Lewis KJ, McKnight DM, Moorhead DL, Parsons AN, Priscu JC, Wall DH, Wharton RA, Virginia RA (1999) Physical controls on the Taylor Valley ecosystem, Antarctica. Bioscience 49:961–971. doi:10.1525/bisi.1999.49.12.961
Gooseff MN, McKnight DM, Runkel RL, Duff JH (2004) Denitrification and hydrologic transient storage in a glacial meltwater stream, McMurdo Dry Valleys, Antarctica. Limnol Oceanogr 49:1884–1895. doi:10.4319/lo.2004.49.5.1884
Haegeman B, Hamelin J, Moriarty J, Neal P, Dushoff J, Weitz JS (2013) Robust estimation of microbial diversity in theory and in practice. ISME J 7:1092–1101. doi:10.1038/ismej.2013.10
Healy M, Webster-Brown JG, Brown KL, Lane V (2006) Chemistry and stratification of Antarctic meltwater ponds II: inland ponds in the McMurdo Dry Valleys, Victoria Land. Antarct Sci 18:525–533. doi:10.1017/S0954102006000575
Heino J, Tolkkinen M, Pirttilä AM, Aisala H, Mykrä H (2014) Microbial diversity and community–environment relationships in boreal streams. J Biogeogr 41:2234–2244. doi:10.1111/jbi.12369
Hijmans RJ (2014) geosphere: Spherical Trigonometry. R package version 1.3-11. http://CRAN.R-project.org/package=geosphere. Accessed 20 Nov 2015
Howard-Williams C, Hawes I (2007) Ecological processes in Antarctic inland waters: interactions between physical processes and the nitrogen cycle. Antarct Sci 19:205–217. doi:10.1017/S0954102007000284
Jost L, Chao A, Chazdon RL (2011) Compositional similarity and beta diversity. In: Magurran AE, McGill BJ (eds) Biological diversity: Frontiers in measurement and assessment. Oxford University Press, Oxford, pp 68–84
Kawecka B, Olech M, Nowogrodzka-Zagórska M, Wojtuń B (1998) Diatom communities in small water bodies at H. Arctowski Polish Antarctic Station (King George Island, South Shetland Islands, Antarctica). Polar Biol 19:183–192. doi:10.1007/s003000050233
Kociolek JP, Spaulding SA (2000) Freshwater diatom biogeography. Nova Hedwigia 71:223–242
Kohler TJ, Kopalová K, Van de Vijver B, Kociolek JP (2015a) The genus Luticola D.G.Mann (Bacillariophyta) from the McMurdo Sound Region, Antarctica, with the description of four new species. Phytotaxa 208:103–134. doi:10.11646/phytotaxa.208.2.1
Kohler TJ, Stanish LF, Crisp SW, Koch JC, Liptzin D, Baeseman JL, McKnight DM (2015b) Life in the main channel: long-term hydrologic control of microbial mat abundance in McMurdo Dry Valley streams, Antarctica. Ecosystems 18:310–327. doi:10.1007/s10021-014-9829-6
Konfirst MA, Sjunneskog C, Scherer RP, Doran PT (2011) A diatom record of environmental change in Fryxell Basin, Taylor Valley, Antarctica, late Pleistocene to present. J Paleolimnol 46:257–272. doi:10.1007/s10933-011-9537-6
Kopalová K, Van de Vijver B (2013) Structure and ecology of freshwater benthic diatom communities from Byers Peninsula, Livingston Island, South Shetland Islands. Antarct Sci 25:239–253
Kopalová K, Nedbalová L, Nývlt D, Elster J, Van de Vijver B (2013) Diversity, ecology and biogeography of the freshwater diatom communities from Ulu Peninsula (James Ross Island, NE Antarctic Peninsula). Polar Biol 36:933–948
Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69:1–24. doi:10.1890/0012-9615(1999)069[0001:DBRATM]2.0.CO;2
Leibold MA, Holyoak M, Mouquet N et al (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7:601–613. doi:10.1111/j.1461-0248.2004.00608.x
Lyons WB, Welch KA, Gardner CB, Jaros C, Moorhead DL, Knoepfle JL, Doran PT (2012) The geochemistry of upland ponds, Taylor Valley, Antarctica. Antarct Sci 24:3–14. doi:10.1017/S0954102011000617
Martiny JBH, Bohannan BJ, Brown JH et al (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112. doi:10.1038/nrmicro1341
McCune B, Grace JB (2002) Analysis of ecological communities. MjM Software Design, Gleneden Beach
McKnight DM, Andrews ED, Spaulding SA, Aiken GR (1994) Aquatic fulvic acids in algal-rich Antarctic ponds. Limnol Oceanogr 39:1972–1979. doi:10.4319/lo.1994.39.8.1972
McKnight DM, Niyogi DK, Alger AS, Bomblies A, Conovitz PA, Tate CM (1999) Dry valley streams in Antarctica: ecosystems waiting for water. Bioscience 49:985–995. doi:10.1525/bisi.1999.49.12.985
Monaghan AJ, Bromwich DH, Powers JG, Manning KW (2005) The climate of the McMurdo, Antarctica, region as represented by one year of forecasts from the Antarctic Mesoscale Prediction System. J Clim 18:1174–1189
Nkem JN, Wall DH, Virginia RA, Barrett JE, Broos EJ, Porazinska DL, Adams BJ (2006) Wind dispersal of soil invertebrates in the McMurdo Dry Valleys, Antarctica. Polar Biol 29:346–352. doi:10.1007/s00300-005-0061-x
Nylen TH, Fountain AG, Doran PT (2004) Climatology of katabatic winds in the McMurdo Dry Valleys, southern Victoria Land. Antarctica. J Geophys Res-Atmos 109:D03114. doi:10.1029/2003JD003937
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) Vegan: community ecology package. R package version 2.0-10. http://CRAN.R-project.org/package=vegan. Accessed 20 Nov 2015
Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices - estimation and comparison of fractions. Ecology 87:2614–2625. doi:10.1890/0012-9658(2006)87[2614:VPOSDM]2.0.CO;2
Pla-Rabes S, Toro M, Van De Vijver B, Rochera C, Villaescusa JA, Camacho A, Quesada A (2013) Stability and endemicity of benthic diatom assemblages from different substrates in a maritime stream on Byers Peninsula, Livingston Island, Antarctica: the role of climate variability. Antarct Sci 25:254–269. doi:10.1017/S0954102012000922
R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed 20 Nov 2015
Roberts D, McMinn A (1999) Diatoms of the saline lakes of the Vestfold Hills, Antarctica. Bibliotheca Diatomologica 44:1–82
Roberts D, McMinn A, Johnston N, Gore DB, Melles M, Cremer H (2001) An analysis of the limnology and sedimentary diatom flora of fourteen lakes and ponds from the Windmill Islands, East Antarctica. Antarct Sci 13:410–419. doi:10.1017/S0954102001000578
Rochera C, Fernandez-Valiente E, Van de Vijver B, Rico E, Toro M, Vincent WF, Quesada A, Camacho A (2013) Community structure and photosynthetic activity of benthic biofilms from a waterfall in the maritime Antarctica. Polar Biol 36:1709–1722. doi:10.1007/s00300-013-1388-3
Šabacká M, Priscu JC, Basagic HJ, Fountain AG, Wall DH, Virginia RA, Greenwood MC (2012) Aeolian flux of biotic and abiotic material in Taylor Valley, Antarctica. Geomorphology 155–156:102–111. doi:10.1016/j.geomorph.2011.12.009
Sabbe K, Verleyen E, Hodgson DA, Vanhoutte K, Vyverman W (2003) Benthic diatom flora of freshwater and saline lakes in the Larsemann Hills and Rauer Islands, East Antarctica. Antarct Sci 15:227–248. doi:10.1017/S095410200300124X
Saunders KM, Hodgson DA, McMinn A (2009) Quantitative relationships between benthic diatom assemblages and water chemistry in Macquarie Island lakes and their potential for reconstructing past environmental changes. Antarct Sci 21:35–49. doi:10.1017/S0954102008001442
Saunders KM, Hodgson DA, McMurtrie S, Grosjean M (2015) A diatom–conductivity transfer function for reconstructing past changes in the Southern Hemisphere westerly winds over the Southern Ocean. J Quat Sci 30:464–477. doi:10.1002/jqs.2788
Sokol ER, Herbold CW, Lee CK, Cary SC, Barrett JE (2013) Local and regional influences over soil microbial metacommunities in the Transantarctic Mountains. Ecosphere 4:art136. doi: 10.1890/ES13-00136.1
Spaulding SA, McKnight DM, Stoermer EF, Doran PT (1997) Diatoms in sediments of perennially ice-covered Lake Hoare, and implications for interpreting lake history in the McMurdo Dry Valleys of Antarctica. J Paleolimnol 17:403–420. doi:10.1023/A:1007931329881
Spaulding S, Van de Vijver B, Hodgson D, McKnight D, Verleyen E, Stanish L (2010) Diatoms as indicators of environmental change in Antarctic and subantarctic freshwaters. In: Smol JP, Stoermer EF (eds) The diatoms: applications for the environmental and earth sciences, 2nd edn. Cambridge University Press, Cambridge, pp 267–286
Speirs JC, Steinhoff DF, McGowan HA, Bromwich DH, Monaghan AJ (2010) Foehn winds in the McMurdo Dry Valleys, Antarctica: the origin of extreme warming events. J Climate 23:3577–3598. doi:10.1175/2010JCLI3382.1
Stanish LF, Nemergut DR, McKnight DM (2011) Hydrologic processes influence diatom community composition in Dry Valley streams. J N Am Benthol Soc 30:1057–1073. doi:10.1899/11-008.1
Stanish LF, Kohler TJ, Esposito RMM, Simmons BL, Nielsen UN, Wall DH, Nemergut DR, McKnight DM (2012) Extreme streams: flow intermittency as a control on diatom communities in meltwater streams in the McMurdo Dry Valleys, Antarctica. Can J Fish Aquat Sci 69:1405–1419. doi:10.1139/f2012-022
Stanish LF, Bagshaw EA, McKnight DM, Fountain AG, Tranter M (2013a) Environmental factors influencing diatom communities in Antarctic cryoconite holes. Environ Res Lett 8:045006. doi:10.1088/1748-9326/8/4/045006
Stanish LF, O’Neill SP, Gonzalez A, Legg TM, Knelman J, McKnight DM, Spaulding SA, Nemergut DR (2013b) Bacteria and diatom co-occurrence patterns in microbial mats from polar desert streams. Environ Microbiol 15:1115–1131. doi:10.1111/j.1462-2920.2012.02872.x
Steinman A, Lamberti GA, Leavitt PR (1996) Biomass and pigments of benthic algae. In: Hauer FR, Lamberti GA (eds) Methods in stream ecology, 2nd edn. Academic Press, San Diego, pp 357–379
Van de Vijver B, Beyens L (1999) Freshwater diatoms from Ile de la Possession (Crozet Archipelago, sub-Antarctica): an ecological assessment. Polar Biol 22:178–188. doi:10.1007/s003000050408
Vanormelingen P, Verleyen E, Vyverman W (2008) The diversity and distribution of diatoms: from cosmopolitanism to narrow endemism. Biodivers Conserv 17:393–405. doi:10.1007/s10531-007-9257-4
Vanormelingen P, Vyverman W, De Bock D, Van der Gucht K, Meester LD (2009) Local genetic adaptation to grazing pressure of the green alga Desmodesmus armatus in a strongly connected pond system. Limnol Oceanogr 54:503–511. doi:10.4319/lo.2009.54.2.0503
Venables WN, Ripley BD (2002) Modern Applied Statistics with S, 4th edn. Springer, New York, p 498
Verleyen E, Hodgson DA, Vyverman W, Roberts D, McMinn A, Vanhoutte K, Sabbe K (2003) Modelling diatom responses to climate induced fluctuations in the moisture balance in continental Antarctic lakes. J Paleolimnol 30:195–215. doi:10.1023/A:1025570904093
Verleyen E, Vyverman W, Sterken M, Hodgson DA, De Wever A, Juggins S, Van de Vijver B, Jones VJ, Vanormelingen P, Roberts D, Flower R, Kilroy C, Sabbe K (2009) The importance of dispersal related and local factors in shaping the taxonomic structure of diatom metacommunities. Oikos 118:1239–1249. doi:10.1111/j.1600-0706.2009.17575.x
Verleyen E, Hodgson DA, Gibson J et al (2012) Chemical limnology in coastal East Antarctic lakes: monitoring future climate change in centres of endemism and biodiversity. Antarct Sci 24:23–33. doi:10.1017/S0954102011000642
Vincent WF, Downes MT, Castenholtz RW, Howard-Williams C (1993) Community structure and pigment organization of cyanobacterial-dominated microbial mats in Antarctica. Eur J Phycol 28:213–231. doi:10.1080/09670269300650321
Vyverman W, Verleyen E, Sabbe K, Vanhoutte K, Sterken M, Hodgson DA, Mann DG, Juggins S, Van de Vijver B, Jones V, Flower R, Roberts D, Chepurnov VA, Kilroy C, Vanormelingen P, De Wever A (2007) Historical processes constrain patterns in global diatom diversity. Ecology 88:1924–1931. doi:10.1890/06-1564.1
Vyverman W, Verleyen E, Wilmotte A et al (2010) Evidence for widespread endemism among Antarctic microorganisms. Polar Sci 4:103–113. doi:10.1016/j.polar.2010.03.006
Welch KA, Lyons WB, Whisner C, Gardner CB, Gooseff MN, McKnight DM, Priscu JC (2010) Spatial variations in the geochemistry of glacial meltwater streams in the Taylor Valley, Antarctica. Antarct Sci 22:662–672. doi:10.1017/S0954102010000702
Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39:1985–1992. doi:10.4319/lo.1994.39.8.1985
West W, West GS (1911) Freshwater algae. British Antarctic Expedition (1907–1909) Science Report. Biology 1:263–298
Whittaker TE, Hall BL, Hendy CH, Spaulding SA (2008) Holocene depositional environments and surface-level changes at Lake Fryxell, Antarctica. Holocene 18:775–786. doi:10.1177/0959683608091797
Witkowski A, Lange-Bertalot H, Metzeltin D (2000) Diatom flora of marine coasts I. Iconographia Diatomologica 7:1–925
Acknowledgments
We thank Chris Jaros, Rae Spain, Holly Hughes, Kateřina Kopalová, Steven Crisp, Jean Pennycook, and Amy Chiuchiolo for field and laboratory assistance. Dieter Piepenburg, Manuel Toro, and two anonymous reviewers provided useful comments that greatly improved the manuscript. PHI helicopters provided logistic support. Funding was provided by the MCMLTER (OPP-1115245) and National Science Foundation Antarctic Organisms and Ecosystems Program Award #0839020.
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Sakaeva, A., Sokol, E.R., Kohler, T.J. et al. Evidence for dispersal and habitat controls on pond diatom communities from the McMurdo Sound Region of Antarctica. Polar Biol 39, 2441–2456 (2016). https://doi.org/10.1007/s00300-016-1901-6
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DOI: https://doi.org/10.1007/s00300-016-1901-6