Abstract
Assemblages of terrestrial biotas in Antarctica have low species-diversity, taxonomic breadth, and number of trophic links and may provide insights not only into adaptation to extreme environments, but also into an understanding of community structure and dynamics not readily achieved by studying more complex, less tractable, systems. To this end, we collected core-samples of soils and the Bryosystem in the Larsemann Hills, Antarctica, and extracted their contained micrometazoans (tardigrades, rotifers, and nematodes). All these undergo deep, sustained dormancy that enhances their survival under extreme polar conditions. Yields varied greatly (zero to > 1000 per core); 38% of the cores lacked animals entirely and only 13% contained all three taxa together. There were greater abundances in mosses, especially at wet seepages, than in lichens or soils. All taxa occurred in mosses more often than expected from random distribution among habitats, and similar "preferences" were shown by tardigrades and rotifers for soil, nematodes for lichens and tardigrades for algae. Whereas tardigrades and rotifers both occur in soil less often than expected by chance, nevertheless are associated with each other there, suggesting that although soil is a relatively unfavorable habitat for both, they respond in similar ways to variation in edaphic conditions. The above scenario serves as a baseline for assessing increasing structural complexity of Antarctic terrestrial communities as the continent undergoes warming, accompanied by inevitable invasion by external species, including non-cryptobiotic taxa.
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References
Adams BJ, Bardgett RD, Ayres E, Wall DH, Aislabie J, Bamforth S, Bargagli R, Cary C, Cavacini P, Connell L, Convey P, Fell JW, Frati F, Hogg ID, Newsham KK, O'Donnell A, Russell N, Seppelt RD, Stevens MI (2006) Diversity and distribution of Victoria Land biota. Soil Biol Biochem 38:3003–3018
Broady PA (1977) A new genus and two new species of terrestrial chlorohycean algae from Signy Island, South Orkney Islands, Antarctica. Br Phycol J 12:7–15
Broady PA (1979) Quantitative studies on the terrestrial algae of Signy Island, South Orkney Islands. Br Antarct Surv Bull 47:31–41
Cesari M, McInnes SJ, Bertolani R, Rebecchi L, Guid R (2016) Genetic diversity and biogeography of the south polar water bear Acutuncus antarcticus (Eutardigrada: Hypsibiidae)—evidence that it is a truly pan-Antarctic species. Invertebr Syst 30:635–649
Connell L, Redman R, Craig S, Rodriguez R (2006) Distribution and abundance of fungi in the soils of Taylor Valley, Antarctica. Soil Biol Biochem 38:3080–3094
Convey P, McInnes SJ (2005) Exceptional tardigrade-dominated ecosystems in Ellsworth Land, Antarctica. Ecology 86:519–527
Convey P, Chown SL, Clarke A, Barnes DKA, Bokhorst S, Cummings V, Ducklow HW, Frati F, Green TGA, Gordon S, Griffiths HJ, Howard-Williams C, Huiskes AHL, Laybourn-Parry J, Lyons WB, McMinn A, Morley SA, Peck LS, Quesada A, Robinson SA, Schiaparelli S, Wall DH (2014) The spatial structure of Antarctic biodiversity. Ecol Monogr 84:203–244
Degma P, Guidetti R (2007) Notes to the current checklist of Tardigrada. Zootaxa 1579:41–53
Degma P, Bertolani R, Guidetti R (2009–2018) Actual checklist of Tardigrada species. 34th Edition: 15–10–2018, p 46. https://www.tardigrada.modena.unimo.it/miscellanea/Actual%20checklist%20of%20Tardigrada.pdf. Accessed 28 Feb 2019
Gardiner GR, Pidgeon RWJ (1987) Structure and function of terrestrial communities with special reference to Tardigrada. 1986–87 Australian Antarctic Research Program Report. Antarctic Division, Kingston, pp 78–80
Glime JM (2017) Tardigrade survival. Chapter 5–1 in Bryophyte Ecology (ebook). In: Glime Jm (ed) Vol. 2 Bryological Interaction. Michigan Technological University and the International Association of Bryologists. Updated 21 April 2017. https://digitalcommons.mtu.edu/bryophyte-ecology2/
Greene SW, Gressitt JL, Koob D, Llano GA, Rudolph ED, Singer R, Steere WC, Ugolini FC (not dated) Terrestrial life in Antarctica. Antarctic Map Folio Series, Folio 5, plate 10, sheet 2. American Geographical Society, New York
Gressitt JL (ed) (1967) Entomology of Antarctica. Antarctic Research Series, vol. 10. American Geophysical Union, Washington DC
Gressitt JI, Weber NA (1959) Biographic introduction to Antarctic-Subantarctic entomology. Pac Insects 4:441–480
Gressitt JL, Fearon CE, Rennell K (1964) Antarctic mite populations and negative arthropod surveys. Pac Insects 6:531–540
Guidetti R, Bertolani R (2005) Tardigrade taxonomy: an updated check list of the taxa and a list of characters for their identification. Zootaxa 845:1–46
Heatwole H (1995) Energetics of desert invertebrates. Section 6.4 (pp 184–191) Anhydrobiosis. In: Chapter 6. Quiescence and dormancy: waiting out energy shortages. Springer Verlag, Berlin, pp 184–191
Heatwole H, Saenger P, Spain A, Kerry E, Donelan J (1989) Biotic and chemical characteristics of some soils from Wilkes Land, Antarctica. Antarct Sci 1:225–234
Heatwole H, Alter J, Charley J, Stephenson J, Bedford P, O'Donoghue P, Miller WR, Rey R (1999) From bedrock to biota: weathering, physicochemical properties, protozoans and micrometazoans of some soils of East Antarctica. ANARE Rep 140:1–91
Heatwole H, Trémont S, Broese E (2013) Point-diversity, a critical tool for assessing dynamics of guilds of scavenging ants (Hymenoptera: Formicidae): an example from a eucalypt woodland. Syst Biodivers. https://doi.org/10.1080/14772000.2013.788578
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
Holgate MW (1977) Terrestrial ecosystems in the Antarctic. Philos Trans R Soc Lond B 279:5–25
Janetschek H (1963) On the terrestrial fauna of the Ross Sea area, Antarctica. Pac Insects 5:305–311
Janetschek H (1967) Arthropod ecology of South Victoria Land. Entomol Antarct Antarct Res Ser 10:205–293
Janiec K (1996) Short distance wind transport of microfauna in maritime Antarctica (King George Islands). Pol Polar Res 18:203–211
Keilin D (1959) The problem of anabiosis or latent life: history and current concept. Proc R Soc B 150:149–191
Maslen NR, Convey P (2006) Nematode diversity and distribution in the southern maritime Antarctic—clues to history? Soil Biol Biochem 38:3141–3151
Miller WR, Miller JD, Heatwole H (1994a) Tardigrades of the Australian Antarctic Territory: assessing diversity within a sample. Mem Qld Mus 36:137–145
Miller WR, Heatwole H, Pidgeon RWJ, Gardiner GR (1994b) Tardigrades of the Australian Antarctic Territories the Larsemann Hills, East Antarctica. Trans Am Microsc Soc 113:142–460
Miller WR, Horning DS, Heatwole HF (2001) Tardigrades of the Australian Antarctic: Macquarie Island, sub-Antarctica. Zool Anz 240:473–489. https://doi.org/10.1078/0044-5231-00057
Mogle MJ, Kimball SA, Miller WR, McKown RD (2018) Evidence of avian-mediated long distance dispersal in American tardigrades. Peer J 6:e5035. https://doi.org/10.7717/peerj.5035
Muñoz J, Felicimo AM, Cabezas F, Burrgaz AR, Martine I (2004) Wind as a long-distance dispersal vehicle in the Southern Hemisphere. Science 304:1144–1147
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
Powers LE, Freckman DW, Virginia RA (1995) Spatial distribution of nematodes in polar desert soils of Antarctica. Polar Biol 15:325–333
Ptatscheck C, Gansfort B, Traunspurger W (2017) The extent of wind-mediated wind dispersal of small metazoans, focusing nematodes. Sci Rep 8:1–10. https://doi.org/10.1038/s41598-018-24747-8
Rounsevell DE (1977) The ecology of the pan-Antarctic mite Nanorchestes antarcticus (Strandtmann). In: Proceedings of 3rd SCAR symp antarctic biol, adaptations within antarctic ecosystems. Gulf Publishing, Houston, pp 123–133
Rounsevell DE (1981) A population of Nanorchestes antarcticus (Acari: Prostigmata) at the Vestfold Hills, Antarctica. ANARE Sci Rep Ser B 131:1–100
Rounsevell DE, Horne PA (1986) Terrestrial, parasitic and introduced invertebrates of the Vestfold Hills. In: Pickard H (ed) Antarctic oasis, terrestrial environments and history of the Vestfold Hills. Academic Press, Sydney, pp 309–331
Seppelt RD (1988) Plants and landscape in the Vestfold Hills, Antarctica. Hydrobiologia 165:185–196
Sømme L, Meier T (1995) Cold tolerance in Tardigrada from Dronning Maud Land, Antarctica. Polar Biol 15:221–224
Stewart J (1990) Antarctica, an encyclopedia, vols. 1–2. McFarland & Co., London
Stuwe K, Braun HM, Peer H (1989) Geology and structure of the Larsemann Hills area, Prydz Bay, East Antarctica. Aust J Earth Sci 36:219–241
Tilbrook PJ (1967) The terrestrial invertebrate fauna of the Maritime Antarctica. Philos Trans R Soc Lond B 252:261–278
Tsujimoto M, McInnes SJ, Convey P, Imura S (2014) Preliminary description of tardigrade species diversity and distribution pattern around coastal Syowa Station and inland Sør Rondane Mountains, Dronning Maud Land, East Antarctica. Polar Biol 37:1361–1367
Tsujimoto M, Satoshi I, Hiroshi K (2015) Recovery and reproduction of an Antarctic tardigrade retrieved from a moss sample frozen for over 30 years. Cryobiology 72:78–81
Usher MB, Edwards M (1984) A dipteran from south of the Antarctic circle: Belgica antarctica (Chironomidae) with a description of its larvae. Biol J Linn Soc 23:19–31
Velasco-Castrillón A, Gibson JAE, Stevens MI (2014a) A review of current Antarctic limno-terrestrial microfauna. Polar Biol. https://doi.org/10.1007/s00300-014-1544-4
Velasco-Castrillón A, Schultz MB, Columbo F, Gibson JAE, Davie KA, Austin AD, Stevens MI (2014b) Distribution and diversity of soil microfauna from East Antarctica: assessing the link between biotic and abiotic factors. PLoS ONE 98(1–17):e87529. https://doi.org/10.1371/journal.pone.0087529
Velasco-Castrillón A, McInnes SJ, Schultz MB, Arröni-Crespo M, D'Haese CA, Gibson JAE, Adams BJ, Page TJ, Austin AD, Cooper SJB, Stevens MI (2015) Mitochondrial DNA analyses reveal widespread tardigrade diversity in Antarctica. Invertebr Syst 29:578–590
Wall DH, Adams BJ, Barrett JE, Hopkins DW, Virginia RA (2006) A synthesis of soil biodiversity and ecosystem functioning in Victoria Land, Antarctica. Soil Biol Biochem 38:3001–3002
Young SR (1979) Respiratory metabolism of Alaskozetes antarcticus. J Insect Physiol 25:361–369
Young SR (1979) Effect of temperature range on the metabolic rate of an Antarctic mite. J Comp Physiol 131:341–346
Walton DWH (1990) Colonization of terrestrial habitats–-organisms, opportunities and occurrence. In: Kerry KR, Hempel G (eds) Antarctic ecosystems. Ecological change and conservation. Springer, Berlin, pp 51–60
West CC (1984) Micro-arthropod and plant species associations in two Subantarctic terrestrial communities. Oikos 42:66–73
Acknowledgements
The field work was supported by the Australian National Antarctic Research Expeditions field program 1987. We are indebted to Robert Pidgeon and G. R. Gardiner for collection of samples in the field and to Frances Reay and Kerrie Davies for identification of nematodes.
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Heatwole, H., Miller, W.R. Structure of micrometazoan assemblages in the Larsemann Hills, Antarctica. Polar Biol 42, 1837–1848 (2019). https://doi.org/10.1007/s00300-019-02557-6
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DOI: https://doi.org/10.1007/s00300-019-02557-6