Ciliates in different types of pools in temperate, tropical, and polar climate zones – implications for climate change

By Hnsjrgnweis - Own work, CC BY-SA 4.0, https://commons.wikimedia.org/w/index.php?curid=49229284
Submitted: 29 November 2020
Accepted: 7 September 2021
Published: 28 September 2021
Abstract Views: 2365
PDF: 337
HTML: 127
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

 Small water bodies are typically characterized by high diversity of various groups of microorganisms. Moreover, these ecosystems react very quickly to even the slightest climate changes (e.g. a temperature increase or water level fluctuations). Thus far, studies of planktonic ciliates in small water bodies having different origins and located in various climate zones have been scarce. Our study aimed to verify the following hypotheses: planktonic ciliate assemblages exhibit higher diversity in pools with higher concentrations of biogenic compounds; pools in warmer climates have higher biodiversity of planktonic ciliates than those in the polar climate zone; individual functional groups of ciliates demonstrate considerable diversity, both between individual pool types and between climate zones. The study was conducted in 21 small pools in temperate, tropical, and polar climate zones. While the type of pool clearly influenced the makeup of microbial communities, the influence of climate was stronger. The factors with the greatest influence on the occurrence of these microorganisms were temperature, total organic carbon, and nutrients. Our results show that in warmer climates the abundance of bacterivorous ciliates is higher, while that of mixotrophs is lower. This has consequences for modelling of climate change and assessment of its influence on the carbon cycle in small water body ecosystems.

Dimensions

Altmetric

PlumX Metrics

Downloads

Download data is not yet available.

Citations

Augustin H, Foissner W, Adam H, 1984. An improved pyridinated silver carbonate method which need few specimens and yields permanent slides of impregnation ciliates (Protozoa, Ciliophora). Mikroskopie 41:134-137.
Amblard C, Carrias JF, Bourdier G, Maurin N, 1995. The microbial loop in a humic lake: seasonal and vertical variations in the structure of different communities. Hydrobiologia 300/3001:71-84. DOI: https://doi.org/10.1007/978-94-011-0293-3_6
Azowski AI, Mazei YA, 2018. Diversity and distribution of free-living ciliates from high-arctic Kara sea sediments. Protist 169:141-157. DOI: https://doi.org/10.1016/j.protis.2018.01.001
Balczon MJ, Pratt RJ, 1996. The functional responses of two benthic algivorous ciliated protozoa with differing feeding strategies. Microb. Ecol. 31:209-224. DOI: https://doi.org/10.1007/BF00167866
Bamforth SS, Wall DH, Virginia RA, 2005. Distribution and diversity of soil protozoa in the McMurdo Dry Valleys of Antarctica. Polar Biol. 28:756-762. DOI: https://doi.org/10.1007/s00300-005-0006-4
Beaver JR, Crisman TL, 1982. The trophic response of ciliated protozoans in freshwater lakes. Limnol. Oceanogr. 27:246-253. DOI: https://doi.org/10.4319/lo.1982.27.2.0246
Bintanja R, 1995. The local surface energy balance of the Ecology Glacier, King George Island, Antarctica: measurements and modeling. Antarct. Sci. 3:315-325. DOI: https://doi.org/10.1017/S0954102095000435
Buosi PRB, Pauleto GM, Lansac-Toha FA, Velho LFM, 2011. Ciliate community associated with aquatic macrophyte roots: effects of nutrient enrichment on the community composition and species richness. Europ. J. Protistol. 47:86-102. DOI: https://doi.org/10.1016/j.ejop.2011.02.001
Carrias JF, Amblard C, Bourdier G, 1994. Vertical and temporal heterogeneity of planktonic ciliated protozoa in a humic lake. J. Plankton Res. 16:471-485. DOI: https://doi.org/10.1093/plankt/16.5.471
Carrick HJ, Fahnenstiel GL, 1990. Planktonic protozoa in lakes Huron and Michigan: seasonal abundance and composition of ciliates and dinoflagellates. J. Great Lakes Res. 16:319-329. DOI: https://doi.org/10.1016/S0380-1330(90)71424-4
Christner BC, Brian HK, Reeve JN, 2003. Molecular identification of bacteria and Eukarya inhabiting an Antarctic cryoconite hole. Extremophiles 7:177-183. DOI: https://doi.org/10.1007/s00792-002-0309-0
Chróst RJ, Siuda W, 2006. Microbial production, utilization, and enzymatic degradation of organic matter in the upper trophogenic layer in the pelagial zone of lakes along an eutrophication gradient. Limnol. Oceanogr. 5:749-762. DOI: https://doi.org/10.4319/lo.2006.51.1_part_2.0749
Connel JH, 1978. Diversity in tropical rain forest and coral reefs. Science 199:1302-1310. DOI: https://doi.org/10.1126/science.199.4335.1302
Crisman TL, Brezonik PL, 1980. Acid rain: threat to sensitive aquatic ecosystems. Proc. 73rd Air Pollution Control Association.
Duran CA, Mayen-Estrada R, 2018. Ciliate species from tank-less bromeliads in a dry tropical forest and their geographical distribution in the Neotropics. Zootaxa 4497:241. DOI: https://doi.org/10.11646/zootaxa.4497.2.5
Fernandez-Galiano D, 1994. The ammoniacal silver carbonate method as a general procedure in the study of protozoa from sewage (and other) waters. Wat. Res. 28:495- 496. DOI: https://doi.org/10.1016/0043-1354(94)90288-7
Finlay BJ, 1980. Temporal and vertical distribution of ciliophoran communities in the benthos of a small eutrophic loch with particular reference to the redox profile. Freshwater Biol. 10:15-34. DOI: https://doi.org/10.1111/j.1365-2427.1980.tb01176.x
Finlay BJ, Curds CR, Bamforth SS, Bafort JM, 1987. Ciliated Protozoa and other Microorganisms from Two African Soda Lakes (Lake Nakuru and Lake Simbi, Kenya). Arch. Protistenk. 133:81-91. DOI: https://doi.org/10.1016/S0003-9365(87)80041-6
Foissner W, 1996. Terrestial ciliates (Protozoa, Ciliophora) from two islands (Gough, Marion) in the southern oceans, with description of two new species, Arcuospathidium cooperi and Oxytricha ottowi. Arch. Protistenkd. 23:282-291. DOI: https://doi.org/10.1007/s003740050172
Foissner W, 2008. Dispersal of protists: the role of cysts and human introductions. In: Fontaneto D, ed. Biogeography of microscopic organisms. Is everything small everywhere? Cambridge University Press: 363 pp.
Foissner W, Berger H, 1996. A user-friendly guide to the ciliates (Protozoa, Ciliophora) commonly used by hydrobiologists as bioindicators in rivers, lakes and waste waters, with notes on their ecology. Freshwater Biol. 35:375-470. DOI: https://doi.org/10.1111/j.1365-2427.1996.tb01775.x
Foissner W, Berger H, Schaumburg J, 1999. Identification and ecology of limnetic plankton ciliates. Informationsberichte des Bayer: Landesamtes für Wasserwirtschaft, München.
Fujishima M, 2009. Endosymbionts in Paramecium. Springer-Verlag: 252 pp. DOI: https://doi.org/10.1007/978-3-540-92677-1
Golterman HL, 1969. Methods for chemical analysis of freshwaters. Oxford: Blackwell Scientific Publications, Edinburgh.
Järvinen M, 1993. Pelagic ciliates in acidified mesohumic forest lake before and after lime addition. Ver. Internat. Verein. Limnol. 25:534-538. DOI: https://doi.org/10.1080/03680770.1992.11900184
Jassey VEJ, Signarbieux C, Hättenschwiler S, Bragazza L, Buttler A, Delarue F, Fournier B, Gilbert D, Laggoun-Dèfarge F, Lara ETE, Mills R, Mitchell EAD, Payne RJ, Robroek BJM, 2015. An unexpected role for mixotrops in the response of peatland carbon cycling to climate warming. Sci. Rep. 5:16931. DOI: https://doi.org/10.1038/srep16931
Jürgens K, Skibbe O, Jeppesen E, 1999. Impact of metazooplankton on the composition and population dynamics of planktonic ciliates in a shallow, hypertrophic lake. Aquat. Microb. Ecol. 17:61-75. DOI: https://doi.org/10.3354/ame017061
Kalinowska K, 2000. Ciliates in small humic lakes (Masurian Lakeland, Poland): relationship to acidity and trophic parameters. Pol. J. Ecol. 48:169-183.
Kammerlander B, Breiner HW, Filker S, Sommaruga R, Sonntag B, Stoeck T, 2015. High diversity of protistan plankton communities in remote high mountain lakes in the European Alps and the Himalayan mountains. FEMS Microbiol. Ecol. 91:fiv010. DOI: https://doi.org/10.1093/femsec/fiv010
Kepner RL Jr, Wharton RA Jr, 1997. McMurdo LTER: Characterization of protozoan communities in lakes Hoare and Fryxell utilizing artificial substrates. Antarct. J. 31:201-202.
Küppers GC, Gonzàlez Garraza GC, Quiroga MV, Lombardo R, Marinone MC, Vinocur A Mataloni G, 2016. Drivers of highly diverse planktonic ciliate assemblages in peat bog pools from Tierra del Fuego (Argentina). Hydrobiologia 773:117-134. DOI: https://doi.org/10.1007/s10750-016-2686-x
Lara E, Seppey CVW, Gonzàlez Garraza GC, Singer D, Quiroga MV, Mataloni G, 2015. Planktonic eukaryote molecular diversity: discrimination of minerotrophic and ombrotrophic peatland pools in Tierra del Fuego (Argentina). J. Plankton Res. 3:645-655. DOI: https://doi.org/10.1093/plankt/fbv016
Laybourn-Parry J, Marchant HJ, Brown P, 1991. The plankton of a large oligotrophic freshwater Antarctic lake. J. Plankton Res. 13:1137-1149. DOI: https://doi.org/10.1093/plankt/13.6.1137
Lee JJ, Small EB, Lynn DH, Bovee EC, 1985. Some techniques for collecting, cultivating and observing Protozoa, p. 1-7. In: Lee JJ, Hutner SH, Bovee EC (eds.), An Illustrated Guide to the Protozoa. Society of Protozoologists. Allen Press, Lawrence.
Maccario L, Sanguino L, Vogel TM, Larose C. 2015. Snow and ice ecosystems: not so extreme. Res Microbiol. 166:782-795. DOI: https://doi.org/10.1016/j.resmic.2015.09.002
Macek M, Callieri C, Šimek K, Vázquez AL, 2006. Seasonal dynamics, composition and feeding patterns of ciliate assemblages in oligotrophic lakes covering a wide pH range. Arch. Hydrobiol. 166:261–287. DOI: https://doi.org/10.1127/0003-9136/2006/0166-0261
Marker AFH, Nusch A, Rai H, 1980. The measurement of photosynthetic pigments in freshwater and standardization of methods: conclusions and recommendation. Arch. Hydrobiol. Beih. Ergebn. Limnol. 14:1-106.
Martinov V, Rakusa-Suszczewski S, 1989. Ten years of climate observations at the Arctowski and Bellingshausen Station (King George Islands, South Shetlands, Antarctis, p. 80-90. In: A. Breymeyer (ed.), Global Change Regional Research Centres: Scientific problems and concept developments. Warsaw.
Mieczan T, 2005. Periphytic ciliates in littoral zone of three lakes of different trophic status. Pol. J. Ecol. 53:489-502.
Mieczan T, Bielańska-Grajner I, Tarkowska-Kukuryk M, 2012. Hydrochemical and microbiological distinction and function of ombrotrophic peatland lagg as ecotone between Sphagnum peatland and forest catchment (Poleski National Park, eastern Poland). Ann. Limnol. Int. J. Lim. 48:323-336. DOI: https://doi.org/10.1051/limn/2012022
Mieczan T, Górniak D, Świątecki A, Zdanowski M, Tarkowska-Kukuryk M, 2013. The distribution of ciliates on Ecology Glacier (King George Island, Antarctica): relationships between species assemblages and environmental parameters. Polar Biol. 36: 249-258. DOI: https://doi.org/10.1007/s00300-012-1256-6
Mieczan T, Adamczuk M, Pawlik-Skowrońska B, Toporowska M, 2014. Eutrophication of peatbogs: consequences of P and N enrichment for microbial and metazoan communities in mesocosm experiments. Aquat. Microb. Ecol. 74:1-20. DOI: https://doi.org/10.3354/ame01727
Mieczan T, Niedźwiecki M, Tarkowska-Kukuryk M, 2015. Effect of rotifers, copepods and chironomid larvae on microbial communities in peatlands. Eur. J. Protistol. 51:386-400. DOI: https://doi.org/10.1016/j.ejop.2015.06.010
Mioduszewski W, 2012. Small water reservoirs – their function and construction. J. Water Land Dev. 17:45–52. DOI: https://doi.org/10.2478/v10025-012-0032-x
Nguyen-Viet H, Gilbert D, Mitchell EAD, Badot PM, Bernard N, 2007. Effects of experimental lead pollution on the microbial communities associated with Sphagnum fallax (Bryophyta). Microb. Ecol. 54:232-241. DOI: https://doi.org/10.1007/s00248-006-9192-z
Packroff G, 2000. Protozooplankton in acid mining lakes with special respect to ciliates. Hydrobiologia 433:157-166. DOI: https://doi.org/10.1023/A:1004095426532
Petz W, 1997. Ecology of the active soil microfauna (Protozoa, Metazoa) of Wilkes Land, East Antarctica. Polar Biol. 18:33-44. DOI: https://doi.org/10.1007/s003000050156
Pfister G, Auer B, Arndt H, 2003. Pelagic ciliates (Protozoa, Ciliophora) of different brackish and freshwater lakes - a community analysis at the species level. Limnologica 32:147-168. DOI: https://doi.org/10.1016/S0075-9511(02)80005-6
Quiroga MV, Unrein F, Gonzàlez Garraza GC, Küppers GC, Lombardo R, Marinone MC, Marque SM, Vinocur A, Mataloni G, 2013. The plankton communities from peat bog pools: structure, temporal variation and environmental factors. J. Plankton Res. 6:1234-1253. DOI: https://doi.org/10.1093/plankt/fbt082
R Core Team, 2019. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available from: https://www.R-project.org/
Roberts EC, Priscu JC, Wolf C, Lyons B, Laybourn-Parry J, 2004. The distribution of microplankton in the McMurdo Dry Valley Lakes, Antarctica: response to ecosystem legacy or present-day climatic control? Polar Biol. 27:238-249. DOI: https://doi.org/10.1007/s00300-003-0582-0
Saad JE, Schiaffino MR, Vinocur A, O᾿Farrell I, Tell G, Izaguirre I, 2013. Microbial planktonic communities of freshwater environments from Tierra del Fuego: dominant trophic strategies in lakes with contrasting features. J. Plankton Res. 6:1220-1233. DOI: https://doi.org/10.1093/plankt/fbt075
Safi K, Hawens I, Sorrell B, 2012. Microbial population responses in three stratified Antarctic meltwater ponds during the autumn freeze. Antarct. Sci. 1:1-18.
Sarvala J, Kankaala P, Zingel P, Arvola L, 1999. Food webs of humic waters, p. 181-184. In: J. Keskitalo and P. Eloranta (eds.), Limnology of humic waters. Backhuys Publishers, Leiden.
Säwström C, Mumford P, Marshall W, Hadson A, Laybourn-Parry J, 2002. The microbial communities and primary productivity of cryoconite holes in Arctic glacier (Svalbard 79oN). Polar Biol. 25:591-596. DOI: https://doi.org/10.1007/s00300-002-0388-5
Searles PS, Kropp BR, Flint SD, Caldwell MM, 2001. Influence of solar UV-B radiation on peatland microbial communities of southern Argentinia. New Phytol. 152:213-221. DOI: https://doi.org/10.1046/j.0028-646X.2001.00254.x
Shannon CE, Weaver W, 1949. The mathematical theory of communication. Urbana: University Illinois Press.
Utermöhl H, 1958. [Zur Vervollkommnung der quantitativen Phytoplankton-Methodik].[Article in German]. Mitt Internat. Ver. Limnol. 9:1-38. DOI: https://doi.org/10.1080/05384680.1958.11904091
Vallesi A, Giuli G, Bradshaw RA, Luporini P, 1995. Autocrine mitogenic activity of pheromones produced by the protozoan ciliate Euplotes raikovi. Nature 376:522–524. DOI: https://doi.org/10.1038/376522a0
Vincent WF, James MR, 1996. Biodiversity in extreme aquatic environments: lakes, ponds and streams in the Ross Sea sector, Antarctica. Biodivers. Conserv. 5:1451-1471. DOI: https://doi.org/10.1007/BF00051987
Vinocur A, Pizarro H, 2000. Microbial mats of twenty-six lakes from Potter Peninsula, King George Island, Antarctica. Hydrobiologia 437:171-185. DOI: https://doi.org/10.1023/A:1026511125146
Wantzen KM, Rothhaupt KO, Mörtl M, Cantonati M, Tóth LG, Fisher P, 2008. Ecological effect of water-level fluctuations in lakes: an urgent issue. Hydrobiologia 613:1-4. DOI: https://doi.org/10.1007/s10750-008-9466-1
Weisse T. 2006. Freshwater ciliates as ecophysiological model organisms - lessons from Daphnia, major achievements, and future perspectives. Arch. Hydrobiol. 167:371-402. DOI: https://doi.org/10.1127/0003-9136/2006/0167-0371
Weisse T, 2016. Functional diversity of aquatic ciliates. Eur. J. Protistol. 61:331-358. DOI: https://doi.org/10.1016/j.ejop.2017.04.001
Weisse T, Moser M, Scheffel U, Stadler P, Berendonk T, Weithoff G, Berger B, 2013. Systematics and species-specific response to pH of Oxytricha acidotolerans sp. nov. and Urosomoida sp. (Ciliophora, Hypotricha) from acid mining lakes. Europ. J. Protistol. 49:255-271. DOI: https://doi.org/10.1016/j.ejop.2012.08.001
Weisse T, Stadler P, Lindstrőm ES, 2002. Interactive effect of temperature and food concentration on growth rate: a test case using the small freshwater ciliate Urotricha farcta. Limnol. Oceanogr. 47:1447-1455. DOI: https://doi.org/10.4319/lo.2002.47.5.1447
Wilbert N, 1975. Eine verbesserte Technik der Protargolimpra¨gnation fur Ciliaten. Mikrokosmos 64:171-179.
Wilkinson DM, 2001. What is the upper size limit for cosmopolitan distribution in free-living microorganisms? J. Biogeogr. 28:258-291. DOI: https://doi.org/10.1046/j.1365-2699.2001.00518.x
Wille A, Sonntag B, Sattler B, Psenner, R, 1999. Abundance, biomass and size structure of the microbial assemblage in the high mountain lake Gossenköllesee (Tyrol, Austria) during the ice-free period. J. Limnol. 58:117. DOI: https://doi.org/10.4081/jlimnol.1999.117
Xu H, Min GS, Choi JK, Kim SJ, Jung JH, Lim BJ, 2009. An approach to analyses of periphytic ciliate communities from monitoring water quality using a modified artificial substrate in Korean coastal waters. Mar. Biol. 89:669-679. DOI: https://doi.org/10.1017/S0025315409000204

Edited by

Diego Copetti, CNR-IRSA Brugherio, Italy

How to Cite

Mieczan, Tomasz, and Urszula Bronowicka-Mielniczuk. 2021. “Ciliates in Different Types of Pools in Temperate, Tropical, and Polar Climate Zones – Implications for Climate Change”. Journal of Limnology 81 (1). https://doi.org/10.4081/jlimnol.2021.1997.

Similar Articles

1 2 3 4 5 6 7 8 9 10 > >> 

You may also start an advanced similarity search for this article.