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Testate amoebae as indicators of water quality and contamination in shallow lakes of the Middle and Lower Yangtze Plain

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Abstract

Testate amoebae are micro-organisms characterized by an agglutinated or autogenous shell enclosing the cytoplasm. Testate amoebae have been widely proposed as valuable bioindicators in a range of ecosystems (such as soils, peatlands and lakes). The use of testate amoebae as bioindicators of water quality in aquatic ecosystems is much less developed than for other microorganisms and previous research is geographically restricted. We investigated a large range of environmental variables and their relations to testate amoeba communities from 37 shallow lakes in the middle and lower Yangtze River Plain of China. Multiple factor analysis, redundancy analysis (RDA) and a forward-selection approach were used to explore the overall community structure and the links between the environmental variables and testate amoeba composition. Results showed that testate amoebae are widely distributed in most of the lakes despite often high levels of pollution. Our data highlight some links between water quality variables and testate amoeba communities. In particular, our results suggest that heavy metals have a role in shaping testate amoeba assemblage structure, although correlations are comparatively weak, perhaps due to lagged responses. Our results support previous suggestions that testate amoebae may be useful bioindicators in aquatic ecosystems but emphasize the need for an improved mechanistic understanding.

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References

  • Asioli A, Medioli FS, Patterson RT (1996) Thecamoebians as a tool for reconstruction of paleoenvironments in some Italian lakes in the foothills of the southern Alps (Orta, Varese and Candia). J Foraminifer Res 26:248–263

    Article  Google Scholar 

  • Avel E, Pensa M (2013) Preparation of testate amoebae sa mples affects water table depth reconstructions in peatland palaeoecological studies. Est J Earth Sci 62:113–119

    Article  Google Scholar 

  • Beyens L, Meisterfeld R (2001) Protozoa: Testate amoebae. In: Smol JP, Birks HJB, Last WM (eds) Tracking Environmental Change Using Lake Sediments. Kluwer Academic Publishers, Dordrecht, pp 121–153

    Google Scholar 

  • Bobrov AA, Charman DJ, Warner BG (1999) Ecology of testate amoebae (Protozoa: Rhizopoda) on peatlands in western Russia with special attention to niche separation in closely related taxa. Protist 150(2):125–136

    Article  Google Scholar 

  • Booth RK (2001) Ecology of testate amoebae (protozoa) in two lake superior coastal wetlands: implications for palaeoecology and environmental monitoring. Wetlands 21:564–576

    Article  Google Scholar 

  • Charman DJ, Roe HM, Gehrels WR (1998) The use of testate amoebae in studies of sea-level change: a case study from the Taf Estuary, south Wales, UK. Holocene 8:209–218

    Article  Google Scholar 

  • Chen X, Qin Y, Stevenson MA, McGowan S (2014) Diatom communities along pH and hydrological gradients in three montane mires, central China. Ecol Indic 45:123–129

    Article  Google Scholar 

  • Cheng X, Li S (2006) An analysis on the evolvement processes of lake eutrophication and their characteristics of the typical lakes in the middle and lower reaches of Yangtze River. Chinese Sci Bull 51:1603–1613

    Article  Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of change in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Dearing JA, Yang X, Dong X, Zhang E, Chen X, Langdon PG, Zhang K, Zhang W, Dawson RP (2012) Extending the timescale and range of ecosystem services through paleoenvironmental analyses, exemplified in the lower Yangtze basin. Proc Natl Acad Sci 109(18):E1111–E1120

    Article  Google Scholar 

  • Dong X, Bennion H, Battarbee R, Yang X, Yang H, Liu E (2008) Tracking eutrophication in Taihu Lake using the diatom record: potential and problems. J Paleolimnol 40:413–429

    Article  Google Scholar 

  • Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366

    Google Scholar 

  • Escobar J, Brenner M, Whitmore TJ, Kenney WF, Curtis JH (2008) Ecology of testate amoebae (thecamoebians) in subtropical Florida lakes. J Paleolimnol 40:715–731

    Article  Google Scholar 

  • Escofier B, Pages J (1994) Multiple factor analysis (AFMULT package). Comput Stat Data An 18:121–140

    Article  Google Scholar 

  • Gomaa F, Yang J, Mitchell EAD, Zhang WJ, Yu Z, Todorov M, Lara E (2015) Morphological and molecular diversification of Asian endemic Difflugia tuberspinifera (Amoebozoa, Arcellinida): a case of fast morphological evolution in protists? Protist 166(1):122–130

    Article  Google Scholar 

  • Greenberg AE, Clesceri LS, Eaton AD (1992) Standard methods for the examination of water and wastewater. American Public Health Association, Washington, DC, pp 3/34–4/138

    Google Scholar 

  • Hu Y, Qi S, Wu C, Ke Y, Chen J, Chen W, Gong X (2012) Preliminary assessment of heavy metal contamination in surface water and sediments from Honghu Lake, East Central China. Front Earth Sci 6:39–47

    Article  Google Scholar 

  • Institute of Hydrogeography and Engineering Geology, MGMR (1990) Water quality analysis. Geology Press, Beijing (in Chinese)

    Google Scholar 

  • Jin X, Liu H, Tu Q, Zhang Z, Zhu X (1990) Lake eutrophication in China. China Environment Science Press, Beijing (in Chinese)

    Google Scholar 

  • Ju LH, Yang J, Liu LM, Wilkinson DM (2014) Diversity and distribution of freshwater testate amoebae (Protozoa) along latitudinal and trophic gradients in China. Microb Ecol 68:657–670

    Article  Google Scholar 

  • Kauppila T, Kihlman S, Mäkinen J (2006) Distribution of arcellaceans (Testate Amoebae) in the sediments of a mine water impacted Bay of Lake Retunen, Finland. Water Air Soil Poll 172:337–358

    Article  Google Scholar 

  • Kawamura T (1918) Japanese Freshwater Biology. Syoukabou, Tokyo, Japan: 113–115 (in Japanese)

  • Kihlman S, Kauppila T (2009) Mine water-induced gradients in sediment metals and arcellacean assemblages in a boreal freshwater bay (Petkellahti, Finland). J Paleolimnol 42:533–550

    Article  Google Scholar 

  • Kihlman S, Kauppila T (2012) Effects of mining on testate amoebae in a Finnish lake. J Paleolimnol 47:1–15

    Article  Google Scholar 

  • Kumar A, Dalby AP (1998) Identification key for Holocene lacustrine Arcellacean (Thecamoebian) taxa. Paleontol Soc 1:1–36

    Google Scholar 

  • Lamentowicz M, Gałka M, Lamentowicz Ł, Obremska M, Kühl N, Lücke A, Jassey VEJ (2015) Climate change over the last 4000 years in a Baltic bog in northern Poland revealed by a trait-based approach, biotic proxies, and stable isotopes. Palaeogeogr Palaeocl 418:261–277

    Article  Google Scholar 

  • Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280

    Article  Google Scholar 

  • Legendre P, Legendre L (2012) Numerical Ecology. Elsevier, Amsterdam

    Google Scholar 

  • Li H, Wang S, Zhao H, Wang M (2015) A testate amoebae transfer function from Sphagnum -dominated peatlands in the Lesser Khingan Mountains, NE China. J Paleolimnol

  • Liu Y, Hu Z, Gao S, Günther D, Xu J, Gao C, Chen H (2008) In situ analysis of major and trace elements of anhydrous minerals by LA-ICP-MS without applying an internal standard. Chem Geol 257:34–43

    Article  Google Scholar 

  • Macumber AL, Patterson RT, Roe HM, Reinhardt EG, Neville LA, Swindles GT (2014) Autoecological approaches to resolve subjective taxonomic divisions within Arcellacea. Protist 65(3):305–316

    Article  Google Scholar 

  • Mazei YA, Marfina OV, Chernyshov VA (2012) Distribution of soil-inhabiting testate amoebae along a mountain slope (Baikal Lake region, Khamar-Daban ridge, Cherskii peak). Biol Bull 39(10):800–804

    Article  Google Scholar 

  • Mitchell EAD, Buttler AJ, Warner BG, Gobat JM (1999) Ecology of testate amoebae (Protozoa: Rhizopoda) in Sphagnum peatlands in the Jura Mountains, Switzerland and France. Ecoscience 6:565–576

    Google Scholar 

  • Mitchell EAD, Charman DJ, Warner BG (2008) Testate amoebae analysis in ecological and paleoecological studies of wetlands: past, present and future. Biodivers Conserv 17(9):2115–2137

    Article  Google Scholar 

  • Mittermeier RA, Mittermeier CG (1997) Megadiversity: Earth’s biological wealthiest nations. Graphic Arts Center Publishing Company, Portland

    Google Scholar 

  • Moor C, Lymberopoulou T, Dietrich V (2001) Determination of heavy metals in soils. Sediments and geological materials by ICP-AES and ICP-MS. Microchim Acta 136(3–40):123–128

    Article  Google Scholar 

  • Neville LA, Christie DG, McCarthy FMG, MacKinnon MD (2010) Biogeographic variation in Thecamoebian (Testate amoeba) assemblages in lakes within various vegetation zones of Alberta, Canada. Int J Biodivers Conserv 2:215–224

    Google Scholar 

  • Ogden CG (1983) Observations on the systematics of the genus Difflugia in Britain (Rhizopoda, Protozoa). Bull Br Mus Nat Hist (Zool.) 44:1–73

    Google Scholar 

  • Olson DM, Dinerstein E (1998) The global 200: a representation approach to conserving the Earth’s most biologically valuable ecoregions. Conserv Biol 12:502–515

    Article  Google Scholar 

  • Organisation for Economic Co-operation and Development, OECD (1982) Eutrophication of waters: monitoring, Assessment and Control. OECD, Paris

    Google Scholar 

  • Patterson RT, Kumar A (2000) Assessment of arcellacea (thecamoebian) assemblages, species and strains as contaminant indicators in variably contaminated James Lake, north eastern Ontario. J Foraminiferal Res 30:310–320

    Article  Google Scholar 

  • Patterson RT, Barker T, Burbridge SM (1996) Arcellaceans (thecamoebians) as proxies of arsenic and mercury contamination in Northeastern Ontario lakes. J Foraminifer Res 26:172–183

    Article  Google Scholar 

  • Patterson RT, Dalby A, Kumar A, Henderson LA, Boudreau REA (2002) Arcellaceans (thecamoebians) as indicators of land-use change: settlement history of the Swan Lake area, Ontario as a case study. J Paleolimnol 28(3):297–316

    Article  Google Scholar 

  • Patterson RT, Roe HM, Swindles GT (2012) Development of an Arcellacean (testate lobose amoebae) based transfer function for sedimentary phosphorous in lakes. Palaeogeogr Palaeocl 348–349:32–44

    Article  Google Scholar 

  • Patterson RT, Chang AS, Prokoph A, Roe HM, Swindles GT (2013a) Influence of the Pacific Decadal Oscillation, El Niño-Southern Oscillation and solar forcing on climate and primary productivity changes in the northeast Pacific. Quat Int 310:124–139

    Article  Google Scholar 

  • Patterson RT, Lamoureux EDR, Neville LA, Macumber AL (2013b) Arcellaceans (testate lobose amoebae) as pH indicators in a pyrite mine acidified lake, northeastern Ontario, Canada. Microbial Ecol 65(3):541–554

    Article  Google Scholar 

  • Payne RJ (2013) Seven reasons why protists make useful bioindicators. Acta Protozool 52:105–113

    Google Scholar 

  • Payne R, Mitchell EA (2009) How many is enough? Determining optimal count totals for ecological and palaeoecological studies of testate amoebae. J Paleolimnol 42(4):483–495

    Article  Google Scholar 

  • Payne R, Charman DJ, Matthews S, Eastwood W (2008) Testate amoebae as palaeoclimate proxies in Sürmene Ağaçbaşi Yaylasi peatland (Northeast Turkey). Wetlands 28:311–323

    Article  Google Scholar 

  • Penard E (1902) Faune rhizopodique du bassin du Léman. Kündig.v, Genève

    Book  Google Scholar 

  • Podani J, Csányi B (2010) Detecting indicator species: Some extensions of the IndVal measure. Ecol Ind 10:1119–1124

    Article  Google Scholar 

  • Qin B, Hu W, Guang G, Luo L, Zhang J (2004) Dynamics of sediment resuspension and the conceptual schema of nutrient release in the large shallow Lake Taihu, China. Chinese Sci Bull 49:54–64

    Article  Google Scholar 

  • Qin Y, Xie S, Swindles GT, Gu Y (2008) Pentagonia zhangduensis nov. spec. (Lobosea, Arcellinida), a new freshwater species from China. Eur J Protistol 44(4):287–290

    Article  Google Scholar 

  • Qin Y, Booth RK, Gu Y, Wang Y, Xie S (2009) Testate amoebae as indicators of 20th century eutrophication in Lake Zhangdu, China. Fund Appl Limnol 175(1):29–38

    Article  Google Scholar 

  • Qin Y, Xie S, Smith HG, Swindles GT, Gu Y (2011) Diversity, distribution and biogeography of testate amoebae in China: implications for ecological studies in Asia. Eur J Protistol 47:1–9

    Article  Google Scholar 

  • Qin Y, Mitchell EAD, Lamentowicz M, Payne RJ, Lara E, Gu Y, Huang X, Wang H (2013) Ecology of testate amoebae in peatlands of central China and development of a transfer function for palaeohydrological reconstruction. J Paleolimnol 50(3):319–330

    Article  Google Scholar 

  • Reinhardt EG, Dalby AP, Kumar A, Patterson RT (1998) Arcellaceans as pollution indicators in mine tailing contaminated lakes near Cobalt, Ontario, Canada. Micropaleontol 44:131–148

    Article  Google Scholar 

  • Roe HM, Patterson RT (2006) Distribution of thecamoebians (testate amoebae) in small lakes and ponds, Barbados, West Indies. J Foraminifer Res 36:116–134

    Article  Google Scholar 

  • Roe HM, Patterson RT (2014) Arcellacea (Testate Amoebae) as bio-indicators of road salt contamination in lakes. Microbial Ecol 68:299–313

    Article  Google Scholar 

  • Roe HM, Patterson RT, Swindles GT (2010) Controls on the contemporary distribution of lake thecamoebians (testate amoebae) within the Greater Toronto Area and their potential as water quality indicators. J Paleolimnol 43:955–975

    Article  Google Scholar 

  • Ryding SO, Rast W (1989) The control of eutrophication of lakes and reservoirs. The United Nations Educational Scientific and Cultural Organization, Paris, pp 37–43

    Google Scholar 

  • Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, Urbana

    Google Scholar 

  • Shen Y (1983) Protozoa of the Teibetan Plateau. In: Jiang XZ, Shen YF, Gong XJ (eds) Aquatic invertebrates of the Teibetan Plateau. Science press, Beijing, pp 48–100 (in Chinese)

    Google Scholar 

  • Shi K, Zhang Y, Zhu G, Liu X, Zhou Y, Xu H, Qin B, Liu G, Li Y (2015) Long-term remote monitoring of total suspended matter concentration in Lake Taihu using 250 m MODIS-Aqua data. Remote Sens Environ 164:43–56

    Article  Google Scholar 

  • Shu J, Huang W, Wu Y (1996) Studies on the classification of trophic types of China’s lakes. Lake Sci 8:193–200 (in Chinese)

    Article  Google Scholar 

  • Song L, Li H, Wang K, Wu D (2014) Ecology of testate amoebae and their potential use as palaeohydrologic indicators from peatland in Sanjiang Plain, Northeast China. Front Earth Sci 8:564–572

    Article  Google Scholar 

  • Sullivan ME, Booth RK (2011) The potential influence of short-term environmental variability on the composition of testate amoeba communities in Sphagnum peatlands. Microbial Ecol 62:80–93

    Article  Google Scholar 

  • Swindles GT, Charman DJ, Roe HM, Sansum PA (2009) Environmental controls on peatland testate amoebae (Protozoa: Rhizopoda) in the North of Ireland: Implications for Holocene palaeoclimate studies. J Paleolimnol 42:123–140

    Article  Google Scholar 

  • Tsugeki N, Oda H, Urabe J (2003) Fluctuation of the zooplankton community in Lake Biwae during the 20th century: a paleolimnological analysis. Limnology 4:101–107

    Article  Google Scholar 

  • Turner TE, Swindles GT, Charman DJ, Blundell A (2013) Comparing regional and supra-regional transfer functions for palaeohydrological reconstruction from Holocene peatlands. Palaeogeogr Palaeocl 369(1):395–408

    Article  Google Scholar 

  • Wang R, Dearing JA, Langdon PG, Zhang E, Yang X, Dakos V, Scheffer M (2012) Flickering gives early warning signals of a critical transition to a eutrophic lake state. Nature 492(7429):419–422

    Article  Google Scholar 

  • Warner BG, Asada T, Quinn NP (2007) Seasonal influences on the ecology of testate amoebae (Protozoa) in a small Sphagnum peatland in southern Ontario, Canada. Microbial Ecol 54(1):91–100

    Article  Google Scholar 

  • Yang J, Beyens L, Shen Y, Feng W (2004) Redescription of Difflugia tuberspinifera Hu, Shen, Gu et Gong, 1997 (Protozoa: Rhizopoda: Arcellinida: Difflugiidae) from China. Acta Protozool 43:281–289

    Google Scholar 

  • Yang X, Dong X, Gao G, Pan H, Wu J (2005) Relationships between surface sediment diatoms and summer water quality in shallow lakes of the middle and lower reaches of Yangtze River. J Integr Plant Biol 47(2):153–164

    Article  Google Scholar 

  • Yang X, Jone A, Dong X, Shen J (2008) Surface sediment diatom assemblages and epilimnetic total phosphorus in large, shallow lakes of the Yangtze floodplain: their relationships and implications for assessing long-term eutrophication. Freshwater Biol 53:1273–1290

    Article  Google Scholar 

  • Yang Z, Wang Z, Zhang Z (2011) Biomonitoring of testate amoebae (protozoa) as toxic metals absorbed in aquatic bryophytes from the Hg-Tl mineralized area (China). Environ Monit Assess 176:321–329

    Article  Google Scholar 

  • Yao M, Li Y, Yang X, Liu Q (2011) Three-year changes in planktonic diatom communities in a eutrophic lake in Nanjing, Jiangsu Province. China. J Freshwater Ecol 26(1):133–141

    Article  Google Scholar 

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Acknowledgments

This work was supported by 973 program (2011CB808800), the National Natural Science Foundation of China (No. 41530753, 41330103, 41502167), and the 111 project (B08030) and. RJP was supported by the Russian Scientific Fund, Grant 14-14-00891.

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Correspondence to Yangmin Qin.

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Supplementary Table 1

Spearman Rank correlation coefficients (Rs) between environmental variables in this study. Rs values only shown where P < 0.05. (XLS 62 kb)

Supplementary Table 2

Environmental data of the 37 lakes in this study (DOCX 33 kb)

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Qin, Y., Payne, R., Yang, X. et al. Testate amoebae as indicators of water quality and contamination in shallow lakes of the Middle and Lower Yangtze Plain. Environ Earth Sci 75, 627 (2016). https://doi.org/10.1007/s12665-016-5442-7

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