Ecology of testate amoebae and their potential use as palaeohydrologic indicators from peatland in Sanjiang Plain, Northeast China

Abstract

Testate amoebae are sensitive indicators of substrate moisture in peatlands. Over the last decades, they have been studied to reconstruct hydrological changes since the Holocene. However, these studies have been geographically restricted to North America and Europe. We conducted the first investigation of testate amoebae on the largest continental fresh water wetland in the Sanjiang Plain, China. The objectives of this study were to provide baseline data on the ecology of testate amoebae in the peatlands of Northeast China and to assess the potential of using them as environmental indicators in this ecosystem. We examined modern testate amoeba assemblages and species-environmental relationships at 46 microsites within 5 waterlogged depressions. The environmental parameters measured included: depth to water table, pH, and loss on ignition. The results showed that the dominant species were Trinema complanatum type, Euglypha rotunda type, Euglypha strigosa type, and Centropyxis cassis type. Redundancy analysis demonstrates that water table depth has the most important effect on testate amoeba assemblages, explaining 16.7% (p=0.002) of the total variance. pH was not a statistically significant factor for testate amoeba assemblages. Weighted averaging and weighted averaging partial least squares models were used to build transfer functions for depth to water table. The best performing transfer function was generated by the weighted averaging partial least squares model with an r²_LOSO of 0.62 and RMSEP_LOSO of 6.96 cm. Results indicate that testate amoebae in waterlogged depression peatland have the potential to be used as indicators for hydrological changes and for palaeohydrologic reconstructions in the Sanjiang Plain.

Key words： palaeoecology; peatland; testate amoebae; transfer function; Sanjiang Wetland; Northeast China

Acknowledgement

We cordially thank Dr. Xuefeng Wang and Mr. Xiumin Yan (Northeast Institute of Geography and Agroecology, CAS, China) for their help with the field sampling, Mr. Dehua Mao (Northeast Institute of Geography and Agroecology, CAS, China) for providing the research site map, and Prof. Jun Yang and Dr. Yangmin Qin for helpful suggestions for improvement and species identifications. We are also deeply grateful to Dr. Louise Loudermilk (Forest Service Station of USDA, USA) and Dr. Mark Judson (Muséum National d’Histoire Naturelle, France) for comments on the manuscript and English language revisions. Lastly, we thank three anonymous reviewers for constructive comments that helped improve the manuscript. Financial assistance was provided by the National Basic Research Program of China (Nos. 2012CB956103 and 2010CB951304), the National Natural Science Foundation of China (Grant No. 41371261), and the CAS/SAFEA International Partnership Program for Creative Research Teams (KZZD-EW-TZ-07).

References

1 Amesbury M J, Mallon G, Charman D J, Hughes P D M, Booth R K, Daley T J, Garneau M (2013). Statistical testing of a new testate amoebae-based transfer function for water-table depth reconstruction on ombrotrophic peatlands in north-eastern Canada and Maine, United States. J Quaternary Sci, 28(1): 27–39

2 Beyens L, Chardez D (1987). Evidence from testate amoebae for changes in some local hydrological conditions between c. 5000 BP and c. 3800 BP on Edgeøya (Svalbard). Polar Res, 5(2): 165–169

3 Birks H J B (1995). Quantitative palaeoenvironmental reconstruction. In Maddy D, Brew J S eds. Statistical Modeling of Quaternary Science Data, Technical Guide (Vol. 5). Cambridge: Quaternary Research Association, 161–254

4 Birks H J B (1998). Numerical tools in palaeolimnology: progress, potentialities, and problems. J Paleolimnol, 20(4): 307–332

5 Bobrov A, Mazei Y, Chernyshov V, Gong Y C, Feng W S (2012). Testate amoebae communities from some freshwater and soil habitats in China (Hubei and Shandong Provinces). Front Earth Sci, 6(1): 1–9

6 Bobrov A, Mazei Y A, Tiunov A V (2010). Testate Amoebae of a Monsoon Tropical Forest of South Vietnam. Acta Protozool, 49(4): 311–325

7 Booth R K (2001). Ecology of testate amoebae (Protozoa) in two lake superior coastal wetlands: implications for paleoecology and environmental monitoring. Wetlands, 21(4): 564–576

8 Booth R K (2008). Testate amoebae as proxies for mean annual water-table depth in Sphagnum-dominated peatlands of North America. J Quaternary Sci, 23(1): 43–57

9 Booth R K (2010). Testing the climate sensitivity of peat-based paleoclimate reconstructions in mid-continental North America. Quat Sci Rev, 29(5–6): 720–731

10 Booth R K, Sullivan M E, Sousa V A (2008). Ecology of testate amoebae in a North Carolina pocosin and their potential use as environmental and paleoenvironmental indicators. Ecoscience, 15(2): 277–289

11 Charman D J (2001). Biostratigraphic and palaeoenvironmental applications of testate amoebae. Quat Sci Rev, 20(16–17): 1753–1764

12 Charman D J, Blundell A (2007). A new European testate amoebae transfer function for palaeohydrological reconstruction on ombrotrophic peatlands. J Quaternary Sci, 22(3): 209–221

13 Charman D J, Hendon D, Woodland W A (2000). The identification of testate amoebae (Protozoa: Rhizopoda) in peats. QRA Technical Guide No. 9, London: Quaternary Research Association

14 Charman D J, Hohl V, Blundell A, Mitchell F, Newberry J, Oksanen P (2012). A 1000-year reconstruction of summer precipitation from Ireland: calibration of a peat-based palaeoclimate record. Quat Int, 268: 87–97

15 Charman D J, Warner B G (1992). Relationship between testate amoebae (Protozoa: Rhizopoda) and microenvironmental parameters on a forested peatland in northeastern Ontario. Can J Zool, 70(12): 2474–2482

16 Hendon D, Charman D J (1997). The preparation of testate amoebae (Protozoa: Rhizopoda) samples from peat. Holocene, 7(2): 199–205

17 Juggins S (2012). Riojia Packages: Analysis of Quaternary Science Data. R package version 0.7-3

18 Lamarre A, Magnan G, Garneau M, Boucher É (2013). A testate amoebae-based transfer function for paleohydrological reconstructuion from boreal and subarctic peatlands in northeastern Canada. Quat Int, 306: 88–96

19 Lamentowicz Ł, Lamentowicz M, Gabka M (2008). Testate amoebae ecology and local transfer function from a peatland in western Poland. Wetlands, 28(1): 164–175

20 Lamentowicz M, Mitchell E A D (2005). The ecology of testate amoebae (Protists) in Sphagnum in North-western Poland in relation to peatland ecology. Microb Ecol, 50(1): 48–63

PMID

21 Li H K (2009). Developing testate amoeba-based transfer functions of environmental variable in peatlands in the Changbai Mountains, of Northeast China. Dissertation for Ph.D Degree. Beijing: University of Chinese Academy of Sciences (in Chinese)

22 Li H K, Bu Z J, Wang S Z, An Z S, Zhao H Y, Ma Y Y, Chen X (2009). Environmental implications of the modern testate amoebae in the peatlands in Changbai Mountains. Quaternary Science, 29(4): 817–824 (in Chinese)

23 Li H K, Chen X, Wang S Z, Bu Z J (2008). Discovery of Trigonopyxis arcula in Hani Mire and its implication in paleoenvironmental reconstruction. Wetland Sciences, 6(1): 75–79 (in Chinese)

24 Mazei Y A, Chernyshov V A (2011). Testate amoebae communities in the southern tundra and forest-tundra of Western Siberia. Biol Bull, 38(8): 789–796

25 Meisterfeld R (2002a). Order Arcellinida Kent, 1880. The illustrated guide to the Protozoa, 2: 827–860

26 Meisterfeld R (2002b). Testate amoebae with filopodia. The illustrated guide to the protozoa, 2: 1054–1084

27 Mitchell E A D, Charman D J, Warner B G (2008). Testate amoebae analysis in ecological and paleoecological studies of wetlands: past, present and future. Biodivers Conserv, 17(9): 2115–2137

28 Mitchell E A D, Payne R J, van der Knaap W O, Lamentowicz Ł, Gąbka M, Lamentowicz M (2013). The performance of single- and multi-proxy transfer functions (testate amoebae, bryophytes, vascular plants) for reconstructing mire surface wetness and pH. Quat Res, 79(1): 6–13

29 Ning Y Z, Shen Y F (1999). Community structure and its characteristics of soil protozoa in typical zones of China. Journal of Northwest Normal University (Natural Science), 35(2): 50–54 (in Chinese)

30 Ogden C G, Hedley R H (1980). An atlas of freshwater testate amoebae. Oxford: Oxford University Press, 3–213

31 Patterson R T, Lamoureux E D R, Neville L A, Macumber A L (2013). Arcellacea (testate lobose amoebae) as pH indicators in a pyrite mine-acidified lake, Northeastern Ontario, Canada. Microb Ecol, 65(3): 541–554

PMID

32 Patterson R T, Roe H M, Swindles G T (2012). Development of an Arcellacea (testate lobose amoebae) based transfer function for sedimentary Phosphorus in lakes. Palaeogeogr Palaeoclimatol Palaeoecol, 348–349: 32–44

33 Payne R J (2011). Can testate amoebae-based palaeohydrology be extend to fen? J Quaternary Sci, 26(1): 15–27

34 Payne R J, Kishaba K, Blackford J J, Mitchell E A D (2006). Ecology of testate amoebae (Protista) in south-central Alaska peatlands: building transfer-function models for palaeoenvironmental studies. Holocene, 16(3): 403–414

35 Payne R J, Mitchell E A D (2007). Ecology of testate amoebae from mires in the Central Rhodope Mountains, Greece and development of a transfer function for palaeohydrological reconstruction. Protist, 158(2): 159–171

PMID

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

37 Payne R J, Ryan P A, Nishri A, Gophen M (2010). Testate amoeba communities of the drained Hula wetland (Israel): implications for ecosystem development and conservation management. Wetlands Ecol Manage, 18(2): 177–189

38 Payne R J, Telford R J, Blackford J J, Blundell A, Booth R K, Charman D J, Lamentowicz Ł, Lamentowicz M, Mitchell E A D, Potts G, Swindles G T, Warner B G, Woodland W (2012b). Testing peatland testate amoebae transfer functions: appropriate methods for clustered training-sets. Holocene, 22(7): 819–825

39 Payne R J, Thompson A M, Standen V, Field C D, Caporn S J M (2012a). Impact of simulated nitrogen pollution on heathland microfauna, mesofauna and plants. Eur J Soil Biol, 49: 73–79

40 Qin Y M, Fournier B, Lara E, Gu Y S, Wang H M, Cui Y D, Zhang X K, Mitchell E A D (2013a). Relationships between testate amoeba communities and water quality in Lake Donghu, a large alkaline lake in Wuhan, China. Front Earth Sci, 7(2): 182–190

41 Qin Y M, Mitchell E A D, Lamentowicz M, Payne R J, Lara E, Gu Y S, Huang X Y, Wang H M (2013b). Ecology of testate amoebae in peatlands of central China and development of a transfer function for paleohydrogical reconstruction. J Paleolimnol, 50(3): 319–330

42 Qin Y M, Payne R J, Gu Y S, Huang X Y, Wang H M (2012). Ecology of testate amoebae in Dajiuhu peatland of Shennongjia Mountains, China, in relation to hydrology. Front Earth Sci, 6(1): 57–65

43 Qin Y M, Xie S C, Gu Y S, Zhou X (2008). Pontigulasia pangulostoma nov. spec., a new testate amoeba from the peat land of Shennongjia Mountains, China. Acta Protozool, 47: 155–160

44 Qin Y M, Xie S C, Smith H G, Swindles G T, Gu Y S (2011). Diversity, distribution and biogeography of testate amoebae in China: implications for ecological studies in Asia. Eur J Protistol, 47(1): 1–9

PMID

45 Roe H M, Patterson R T, Swindles G T (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(4): 955–975

46 Shen Y F (1983). Aquatic Invertebrates of the Teibetan Plateau. Beijing: Science Press, 48–100 (in Chinese)

47 Swindles G T, Charman D J, Roe H M, Sansum P A (2009). Environmental controls on peatland testate amoebae (Protozoa: Rhizopoda) in the North of Ireland: implications for Holocene palaeoclimate studies. J Paleolimnol, 42(1): 123–140

48 Telford R J, Birks H J B (2011). Effect of uneven sampling along an environmental gradient on transfer-function performance. J Paleolimnol, 46(1): 99–106

49 Ter Braak C J F, Šmilauer P (2002). CANOCO Reference Manual and CanoDraw for Windows User’s Guide: Software for Canonical Community Ordination (Version 4.5). Microcomputer Power, Ithaca, NY

50 Turner T E, Swindles G T, Charman D J, Blundell A (2013). Comparing regional and supra-regional transfer functions for palaeohydrological reconstruction from Holocene peatlands. Palaeogeogr Palaeoclimatol Palaeoecol, 369: 395–408

51 Warner B G (1988). Methods in quaternary ecology# 5. Testate amoebae (Protozoa). Geoscience Canada, 15(4): 251–260

52 Wilkinson D M (2008). Testate amoebae and nutrient cycling: peering into the black box of soil ecology. Trends Ecol Evol, 23(11): 596–599

PMID

53 Wilkinson D M, Mitchell E A D (2010). Testate Amoebae and Nutrient Cycling with Particular Reference to Soils. Geomicrobiol J, 27(6–7): 520–533

54 Yang J, Feng W S, Miao W (2004). A taxonomic catalogue of freshwater and soil testate amoebae in China with a discussion of their faunal similarity. Acta Hydrobiologica Sinica, 28(4): 426–433 (in Chinese)

55 Yang J, Meisterfeld R, Zhang W J, Shen Y F (2005). Difflugia mulanensis nov. spec., a freshwater testate amoeba from Lake Mulan, China. Eur J Protistol, 41(4): 269–276

56 Yang J, Shen Y F (2005). Morphology, biometry and distribution of Difflugia biwae Kawamura, 1918 (Protozoa: Rhizopoda). Acta Protozool, 44: 103–111

57 Yang J, Zhang W J, Shen Y F (2009). Relationships between testate amoebae assemblages (Protozoa) and geographic factors in Yunnan Plateau lakes, China. J Freshwat Ecol, 24(3): 437–443

58 Yang Q, Lv X G (1996). Kinds of soil and their characteristics in the ecological experimental area of mire-wetlands. In: Chen G Q ed. The Study of Marsh in the Sanjiang Plain. Beijing: Science Press, 1–26 (in Chinese)