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Towards multi-level biomonitoring of nematodes to assess risk of nitrogen and phosphorus pollution in Jinchuan Wetland of Northeast China

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Abstract

Cultivation for agricultural production often poses threats to nearby wetlands ecosystems in fertile landscapes. In this study, nematode ecological indexes were assessed through the main soil properties of the wetlands, farmlands, and edges of wetlands and farmlands in Jinchuan Wetland by the random sampling. Behavior and reproduction in Caenorhabditis elegans (C. elegans) exposed to the sampled waters were also examined. Stress proteins Hsp70 and Hsp90 were measured both in the living field samples of C. elegans and the lab-tested C. elegans. Our results suggested that disturbance to wetland ecosystems by nitrogen and phosphorus reduced nematode richness and proportions of bacterivore nematodes. Bacterivore nematode diversity and plant–parasitic ecological index were proven to be sensitive indicators of the ecological health of wetlands. Nematode Hsp70 were useful biosensors to monitor and assess the levels of nitrogen and phosphorus pollutions in wetlands. Furthermore, multi-level soil faunal assessments by canonical correspondence analysis showed that Jinchuan Wetland is threatened with non-point source pollution from nearby farmlands.

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References

  • Bakonyi G, Nagy P (2000) Temperature- and moisture-induced changes in the structure of the nematode fauna of a semiarid grassland-patterns and mechanisms. Glob Change Biol 6:697–707

    Article  Google Scholar 

  • Bongers T (1990) The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83:14–19

    Article  Google Scholar 

  • Bongers T, Ferris H (1999) Nematode community structure as a bioindicator in environmental monitoring. Trends Ecol Evol 14:224–228

    Article  Google Scholar 

  • Bongers T, Meulen H, Korthals G (1997) Inverse relationship between the nematode maturity index and plant parasite index under enriched nutrient conditions. Appl Soil Ecol 6:195–199

    Article  Google Scholar 

  • Bradford MA, Wood SA, Bardgett RD, Black HIJ, Bonkowski M, Eggers T, Grayston SJ, Kandeler E, Manning P, Setälä H, Jonesk TH (2014) Discontinuity in the responses of ecosystem processes and multifunctionality to altered soil community composition. PNAS 111(40):14478–14483

    Article  CAS  Google Scholar 

  • Brinson MM, Malvárez AI (2002) Temperate freshwater wetlands: types, status, and threats. Environ Conserv 29:115–133

    Google Scholar 

  • Darby BJ, Neher DA, Belnap J (2007) Soil nematode communities are ecologically more mature beneath late- than early-successional stage biological soil crusts. Appl Soil Ecol 35:203–221

    Article  Google Scholar 

  • de Goede RGM, Bongers T (1994) Nematode community structure in relation to soil and vegetation characteristics. Appl Soil Ecol 1:29–44

    Article  Google Scholar 

  • Deegan LA, Johnson DS, Warren RS, Peterson BJ, Fleeger JW, Fagherazzi S, Wollheim WM (2012) Coastal eutrophication as a driver of salt marsh loss. Nature 490:388–392

    Article  CAS  Google Scholar 

  • Eisenhauer N, Dobies T, Cesarz S, Hobbie SE, Meyer RJ, Worm K, Reich PB (2013) Plant diversity effects on soil food webs are stronger than those of elevated CO2 and N deposition in a long-term grassland experiment. PNAS 110(17):6889–6894

    Article  CAS  Google Scholar 

  • Ferris H, Matute MM (2003) Structural and functional succession in the nematode fauna of a soil food web. Appl Soil Ecol 23:93–110

    Article  Google Scholar 

  • Ferris H, Bongers T, de Goedec RGM (2001) A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Appl Soil Ecol 18:13–29

    Article  Google Scholar 

  • Fiscus DA, Neher DA (2002) Distinguishing sensitivity of free-living soil nematode genera to physical and chemical disturbances. Ecol Appl 12:565–575

    Article  Google Scholar 

  • Freckman DW, Ettema CH (1993) Assessing nematode communities in agroecosystems of varying human intervention. Agric Ecosyst Environ 45:239–261

    Article  Google Scholar 

  • Gleason R, Euliss N, Hubbard D, Duffy W (2003) Effects of sediment load on emergence of aquatic invertebrates and plants from wetland soil egg and seed banks. Wetlands 23:26–34

    Article  Google Scholar 

  • Griffiths BS, Neilson R, Bengough AG (2003) Soil factors determined nematode community composition in a 2 year pot experiment. Nematology 5:889–897

    Article  Google Scholar 

  • Jackson WR (2000) Reduction of hazardous levels of the agricultural application of nitrogen and phosphorus relative to toxic ground water and toxic levels in the soil. Med Hypotheses 55(4):294–299

    Article  CAS  Google Scholar 

  • Jairajpuri MS, Dorylaimida AW (1992) Free-living, predaceous and plant–parasitic nematodes. E. J. Brill, New York

    Google Scholar 

  • Jenkins WP (1964) A rapid centrifugal-flotation technique for separating nematodes from soil. Plant Disease Reporte 48:692

    Google Scholar 

  • Johnston CA, Zedler JB, Tulbure MG, Frieswyk CB, Bedford BL, Vaccaro L (2009) A unifying approach for evaluating the condition of wetland plant communities and identifying related stressors. Ecol Appl 19:739–757

    Google Scholar 

  • Jordan D, Ponder F Jr, Hubbard VC (2003) Effects of soil compaction, forest leaf litter and nitrogen fertilizer on two oak species and microbial activity. Appl Soil Ecol 23:33–41

    Article  Google Scholar 

  • Kardol P, Bezemer TM, van der Wal A, van der Putten WH (2005) Successional trajectories of soil nematode and plant communities in a chronosequence of ex-arable lands. Biol Conserv 126:317–327

    Article  Google Scholar 

  • Khanna N, Cressman CP, Tatara CP, Williams PL (1997) Tolerance of the nematode Caenorhabditis elegans to pH, salinity, and hardness in aquatic media. Arch Environ Contam Toxicol 32(1):110–114

    Article  CAS  Google Scholar 

  • Lenz R, Eisenbeis G (1998) The vertical distribution of decomposition activity and of litter-colonizing nematodes in soils under different tillage. Pedobiologia 42:193–204

    Google Scholar 

  • Liang W, Zhang X, Li Q, Jiang Y, Ou W, Neher D (2005) Vertical distribution of bacterivorous nematodes under different land uses. J Nematol 37:254–258

    Google Scholar 

  • Manlay RJ, Cadet P, Thioulouse J, Chotte JL (2000) Relationships between abiotic and biotic soil properties during fallow periods in the Sudanian zone of Senegal. Appl Soil Ecol 14:89–101

    Article  Google Scholar 

  • Minh LQ, Tuong TP, van Mensvoort MEF, Bouma J (1998) Soil and water table management effects on aluminum dynamics in an acid sulphate soil in Vietnam. Agric Ecosyst Environ 68:255–262

    Article  CAS  Google Scholar 

  • Mishra CC, Dash MC (1987) Effects of soil amendments on soil moisture, pH, microbial population, soil respiration and nematodes. Ann Biol 3:17–27

    Google Scholar 

  • Morris JP, Thatje S, Hauton C (2013) The use of stress-70 proteins in physiology: a re-appraisal. Mol Ecol 22:1494–1502

    Article  CAS  Google Scholar 

  • Murialdo SE, Fuertes MG, Gonzalez JF, Chavez E (2002) Nematodes as indicators of wetland pollution. J Environ Biol 23:423–428

    CAS  Google Scholar 

  • Nadeau D, Corneuau S, Plante I, Morrow G, Tanguay RM (2001) Evaluation for Hsp70 as a biomarker of effect of pollutants on the earthworm Lumbricus terrestris. Cell Stress Chaperon 6(2):153–163

    Article  CAS  Google Scholar 

  • Neher DA (1999) Nematode communities in organically and conventionally managed agricultural soils. J Nematol 31:142–154

    CAS  Google Scholar 

  • Neher DA, Wub J, Barbercheck ME, Anas O (2005) Ecosystem type affects interpretation of soil nematode community measures. Appl Soil Ecol 30:47–64

    Article  Google Scholar 

  • O’Connell JL, Smith Johnson LA, McMurry LM, Haukos DA (2012) Influence of land-use and conservation programs on wetland plant communities of the semiarid United States Great Plains. Biol Conserv 146:108–115

    Article  Google Scholar 

  • O’Connell JL, Johnson LA, Daniel DW, McMurry ST, Smith LM, Haukos DA (2013) Effects of agricultural tillage and sediment accumulation on emergent plant communities in playa wetlands of the U.S. high plains. J Environ Manage 120:10–17

    Article  Google Scholar 

  • Pielou EC (1966) Shannon’s formula as a measure of species diversity: its use and misuse. Am Nat 100:463–465

    Article  Google Scholar 

  • Popovici I (1992) Nematodes as indicators of ecosystem disturbance due to pollution. Stud Univ Babes-Bolyai Ser Biol 37:5–27

    Google Scholar 

  • Pyza E, Mak P, Kramarz P, Laskowski R (1997) Heat shock proteins (HSP70) as biomarkers in ecotoxicological Studies. Ecotox Environ Safety 38(3):44–251

    Google Scholar 

  • Sánchez-Moreno S, Minoshima H, Ferris H, Jackson EL (2006) Linking soil properties and nematode community composition: effects of soil management on soil food webs. Nematology 8:703–715

    Article  Google Scholar 

  • Sánchez-Moreno S, Nicola NL, Ferris H, Zalom FG (2009) Effects of agricultural management on nematode-mite assemblages: soil food web indices as predictors of mite community composition. Appl Soil Ecol 41:107–117

    Article  Google Scholar 

  • Sarathchandra SUGA, Yeates GW, Barch G, Cox NR (2001) Effect of nitrogen and phosphate fertilisers on microbial and nematode diversity in pasture soils. Soil Biol Biochem 33:953–964

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Shayestehfar A, Mayel M, Rezaie B, Dehghani L, Karam A, Saadzadeh E, Rasekhi MH, Sami S, Gashmardi N, Dezhkam L, Motamedi F (1998) Biological observations of soil nematodes around Parishan (Fammur) Lake, Kazeroun, Fars-Iran. J Environ Biol 19:357–361

    Google Scholar 

  • Simpson EH (1949) Measurement of diversity. Nature 163:668

    Google Scholar 

  • Smolik JD, Dodd JL (1983) Effect of water and nitrogen and grazing on nematodes in a shortgrass prairie. J Range Manag 36:744–748

    Article  Google Scholar 

  • Sochová I, Hofman J, Holoubek I (2006) Using nematodes in soil ecotoxicology. Environ Int 32(3):374–383

    Article  Google Scholar 

  • Sohlenius B (1985) Influence of climatic conditions on nematode coexistence: a laboratory experiment with a coniferous forest soil. Oikos 44:430–438

    Article  Google Scholar 

  • Todd TC, Powers TO, Mullin PG (2006) Sentinel nematodes of land-use change and restoration in tallgrass prairie. J Nematol 38:20–27

    CAS  Google Scholar 

  • Tsai JS, Venne LS, McMurry ST, Smith LM (2007) Influences of land use and wetland characteristics on water loss rates and hydroperiods of playas in the Southern High Plains, USA. Wetlands 27:683–692

    Article  Google Scholar 

  • Wagg C, Bender SF, Widmerc F, van der Heijdena MGA (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. PNAS 111(14):5266–5270

    Article  CAS  Google Scholar 

  • Wang Y, Ezemaduka AN (2014) Combined effect of temperature and zinc on Caenorhabditis elegans wild type and daf-21 mutant strains. J Therm Bio. 41:16–20

    Article  Google Scholar 

  • Wang Y, Xu J, Sheng L, Zheng Y (2007) Field and laboratory investigations of the thermal influence on tissue-specific Hsp70 levels in common carp (Cyprinus carpio). Comp Bioch Phys 148A:821–827

    Article  CAS  Google Scholar 

  • Wang Y, Gao J, Wu D (2013) Effects of temperature on copper resistance in daf-21 mutant and Hsp90 expression of Caenorhabditis elegans. Paddy Water Environ, 11:249–254

    Article  Google Scholar 

  • Wardle DA (1995) Impacts of disturbance on detritus food webs in agro-ecosystems of contrasting tillage and weed management practices. In: Begon M, Fitter AH (eds) Advances in ecological research. Academic Press, New York, pp 105–185

    Google Scholar 

  • Wasilewska L (1995) Difference in development of soil nematode communities in single- and multi-species grass experimental treatments. Appl Soil Ecol 21:53–64

    Article  Google Scholar 

  • Whitford WG (1989) Abiotic controls on the functional structure of soil food webs. Biol Fert Soils 8:1–6

    Article  Google Scholar 

  • Wittebolle L, Marzorati M, Clement A, Balloi A, Daffonchio D, Heylen K, DeVos P, Verstraete W, Boon N (2009) Initial community evenness favors functionality under selective stress. Nature 458:623–626

    Article  CAS  Google Scholar 

  • Wu J, Fu C, Lu F, Chen J (2005) Changes in free-living nematode community structure in relation to progressive land reclamation at an intertidal marsh. Appl Soil Ecol 29:47–58

    Article  Google Scholar 

  • Yeates GW (2003) Nematodes as soil indicators: functional and biodiversity aspects. Biol Fertil Soils 37:199–210

    Google Scholar 

  • Yeates GW, Bongers T, de Goede RGM, Freckman DW, Georgieva SS (1993) Feeding habits in soil nematode families and genera—an outline for soil ecologists. J Nematol 25:315–331

    CAS  Google Scholar 

  • Yeates GW, Wardle DA, Watson RN (1999) Responses of soil nematode populations, community structure, diversity and temporal variability to agricultural intensification over a seven-year period. Soil Biol Biochem 32:1721–1733

    Article  Google Scholar 

  • Zhao J, Neherb DA (2013) Soil nematode genera that predict specific types of disturbance. Appl Soil Ecol 64:135–141

    Article  Google Scholar 

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Acknowledgments

This work was supported by Grants from National Natural Science Foundation of China (Nos. 41271485, 41001339), Jilin Province Science and Technology Development Planning Project (Nos. 20130102038JC, 201201004), the Special Funds of the State Environmental Protection Public Welfare Industry (201509040) and the Open Fund of the State Environmental Protection Key Laboratory of Wetland Ecology and Vegetation Restoration, Northeast Normal University (No. 130026520), We would like to thank Dr. Tai L. Guo and Dr. Steven D. Holladay of the University of Georgia and Xuefeng Wang and Xiumin Yan of IGA CAS for their critical review and technical assistance.

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Correspondence to Chunguang He or Lianxi Sheng.

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Wang, Y., Qiao, J., He, C. et al. Towards multi-level biomonitoring of nematodes to assess risk of nitrogen and phosphorus pollution in Jinchuan Wetland of Northeast China. Ecotoxicology 24, 2190–2199 (2015). https://doi.org/10.1007/s10646-015-1550-5

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