Abstract
Adjacent intensive agriculture disturbs the natural condition of wetlands. However, to assess the effect of this agriculture on wetlands, few studies have used indices based on aquatic invertebrates. Multi-metric indices (MMIs) have been successfully used to assess freshwater ecosystems worldwide and are an important management tool, but little is known about their applicability in the Sanjiang Plain, Northeast China. In this study, we developed a MMIs for aquatic invertebrates to assess freshwater wetlands in this region. The aquatic invertebrate assemblages were sampled in 27 wetlands in the Sanjiang Plain that included those in natural reserves and those affected by adjacent, intensive agriculture. Twenty-four candidate metrics were initially reviewed and screened before four core metrics were selected: total number of taxa, number of Hemiptera taxa, proportion of Gastropoda, and proportion of predators. Mann-Whitney U tests, Box and Whisker plots, correlation analyses, and redundant metric tests were used to assess the ability of metrics to distinguish among reference and impaired wetlands. Four ordinal rating categories for wetland were defined: poor, fair, good, and excellent. Of the impaired freshwater wetlands, 76.2% were in poor or fair categories. The MMIs was robust in discriminating reference wetlands from impaired wetlands and therefore have potential as a biomonitoring tool to assess the condition and to guide the restoration efforts of freshwater wetlands in Northeast China.
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References
Baptista D F, Buss D F, Egler M et al., 2007. A multimetric index based on benthic macroinvertebrates for evaluation of Atlantic Forest streams at Rio de Janeiro State, Brazil. Hydrobiologia, 575(1): 83–94. doi: https://doi.org/10.1007/s10750-006-0286-x
Barbour M T, Stribling J B, Karr J R, 1995. The multimetric approach for establishing biocriteria and measuring biological condition. In: Davis W S, Simon T P (eds). Biological Assessment and Criteria: Tools for Water Resource Planning and Decision Making. Boca Raton, London: Lewis Publishers, 63–76.
Barbour M T, Gerritsen J, Griffith G E et al., 1996. A framework for biological criteria for Florida streams using benthic macroinvertebrates. Journal of the North American Benthological Society, 15(2): 185–211. doi: https://doi.org/10.2307/1467948
Batzer D P, Shurtleff A S, Rader R B, 2001. Sampling invertebrates in wetlands. In: Rader R B, Batzer D P, Wissinger S A (eds). Bioassessment and Management of North American Freshwater Wetlands. New York: John Wiley and Sons, 339–354.
Bonada N, Prat N, Resh V H et al., 2006. Developments in aquatic insect biomonitoring: a comparative analysis of recent approaches. Annual Review of Entomology, 51(1): 495–523. doi: https://doi.org/10.1146/annurev.ento.51.110104.151124
Bullock A, Acreman M, 2003. The role of wetlands in the hydrological cycle. Hydrology and Earth System Sciences, 7(3): 358–389. doi: https://doi.org/10.5194/hess-7-358-2003
Clifford H F, 1991. Aquatic Invertebrates of Alberta. Alberta: The University of Alberta Press.
Couceiro S R M, Hamada N, Forsberg B R et al., 2012. A macroinvertebrate multimetric index to evaluate the biological condition of streams in the Central Amazon region of Brazil. Ecological Indicators, 18: 118–125. doi: https://doi.org/10.1016/j.ecolind.2011.11.001
De Bikuña B G, López E, Leonardo J M et al., 2015. Development of a multimetric benthic macroinvertebrate index for assessing the ecological condition of Basque streams (North of Spain). Fundamental and Applied Limnology, 187(1): 21–32. doi: https://doi.org/10.1127/fal/2015/0741
Ferreira W R, Paiva L T, Callisto M, 2011. Development of a benthic multimetric index for biomonitoring of a neotropical watershed. Brazilian Journal of Biology, 71(1): 15–25. doi: https://doi.org/10.1590/S1519-69842011000100005 5ai]Fierro P, Arismendi I, Hughes R M et al., 2018. A benthic macroinvertebrate multimetric index for Chilean Mediterranean streams. Ecological Indicators, 91: 13–23. doi: https://doi.org/10.1016/j.ecolind.2018.03.074
Fu Bojie, Liu Guohua, Chen Liding et al., 2001. Scheme of ecological regionalization in China. Acta Ecologica Sinica, 21(1): 1–6. (in Chinese)
Hawkins C P, Norris R H, Gerritsen J et al., 2000. Evaluation of the use of landscape classifications for the prediction of freshwater biota: synthesis and recommendations. Journal of the North American Benthological Society, 19(3): 541–556. doi: https://doi.org/10.2307/1468113
Hering D, Feld C K, Moog O et al., 2006. Cook book for the development of a multimetric index for biological condition of aquatic ecosystems: experiences from the European AQEM and STAR projects and related initiatives. Hydrobiologia, 566(1): 311–324. doi: https://doi.org/10.1007/s10750-006-0087-2
Huang Q, Gao J F, Cai Y J et al., 2015. Development and application of benthic macroinvertebrate-based multimetric indices for the assessment of streams and rivers in the taihu basin, China. Ecological Indicators, 48: 649–659. doi: https://doi.org/10.1016/j.ecolind.2014.09.014
Hughes R M, 1995. Defining acceptable biological status by comparing with reference conditions. In: Davis W S, Simon T P (eds). Biological Assessment and Criteria: Tools for Water Resource Planning and Decision Making. Boca Raton, FL: Lewis Publishers, 31–47.
Hughes R M, Howlin S, Kaufmann P R, 2004. A biointegrity index (IBI) for coldwater streams of Western Oregon and Washington. Transactions of the American Fisheries Society, 133(6): 1497–1515. doi: https://doi.org/10.1577/T03-146.1
Kerans B L, Karr J R, 1994. A benthic index of biotic integrity (B-IBI) for rivers of the tennessee valley. Ecological Applications, 4(4): 768–785. doi: https://doi.org/10.2307/1942007
Leung A S L, Dudgeon D, 2011. Scales of spatiotemporal variability in macroinvertebrate abundance and diversity in monsoonal streams: detecting environmental change. Freshwater Biological, 56(6): 1193–1208. doi: https://doi.org/10.1111/j.1365-2427.2010.02556.x
Ligeiro R, Hughes R M, Kaufmann P R et al., 2013. Defining quantitative stream disturbance gradients and the additive role of habitat variation to explain macroinvertebrate taxa richness. Ecological Indicators, 25: 45–57. doi: https://doi.org/10.1016/j.ecolind2012.09.004
Liu Xingtu, Ma Xuehui, 2002. Natural Environmental Changes and Ecological Protection in the Sanjiang Plain. Beijing: Science Press. (in Chinese)
Lu K L, Wu H T, Xue Z S et al., 2019. Development of a multi-metric index based on aquatic invertebrates to assess floodplain wetland condition. Hydrobiologia, 827(1): 141–153. doi: https://doi.org/10.1007/s10750-018-3761-2
Mereta S T, Boets P, De Meester L et al., 2013. Development of a multimetric index based on benthic macroinvertebrates for the assessment of natural wetlands in Southwest Ethiopia. Ecological Indicators, 29: 510–521. doi: https://doi.org/10.1016/j.ecolind.2013.01.026
Milošević D, Čerba D, Szekeres J et al., 2016. Artificial neural networks as an indicator search engine: the visualization of natural and man-caused taxa variability. Ecological Indicators, 61: 777–789. doi: https://doi.org/10.1016/j.ecolind.2015.10.029
Mitsch W J, Gosselink J G, 2007. Wetlands. 4th ed. New York: John Wiley and Sons, Inc.
Morse J C, Yang L F, Tian L X, 1994. Aquatic Insects of China Useful for Monitoring Water Quality. Nanjing: HoHai University Press.
Ntislidou C, Lazaridou M, Tsiaoussi V et al., 2018. A new multimetric macroinvertebrate index for the ecological assessment of Mediterranean lakes. Ecological Indicators, 93: 1020–1033. doi: https://doi.org/10.1016/j.ecolind.2018.05.071
O’Brien A, Townsend K, Hale R et al., 2016. How is ecosystem health defined and measured? A critical review of freshwater and estuarine studies. Ecological Indicators, 69: 722–729. doi: https://doi.org/10.1016/j.ecolind.2016.05.004
Odountan O H, De Bisthoven L J, Abou Y et al., 2019. Biomonitoring of lakes using macroinvertebrates: recommended indices and metrics for use in West Africa and developing countries. Hydrobiologia, 826(1): 1–23. doi: https://doi.org/10.1007/s10750-018-3745-2
Omernik J M, 1995. Ecoregions: a spatial framework for environmental management. In: Davis W S, Simon T P (eds). Biological Assessment and Criteria: Tools for Water Resource Planning and Decision Making. Boca Raton, FL: Lewis Publishers, 49–62.
Riato L, Leira M, Della Bella V et al., 2018. Development of a diatom-based multimetric index for acid mine drainage impacted depressional wetlands. Science of the Total Environment, 612: 214–222. doi: https://doi.org/10.1016/j.scitotenv.2017.08.181
Rydin H, Jeglum J K, 2013. The Biology of Peatlands. 2nd ed. Oxford: Oxford University Press.
Shi X, Liu J L, You X G et al., 2017. Evaluation of river habitat integrity based on benthic macroinvertebrate-based multimetric model. Ecological Modelling, 353: 63–76. doi: https://doi.org/10.1016/j.ecolmodel.2016.07.001
Šidagytė E, Višinskienė G, Arbačiauskas K, 2013. Macroinvertebrate metrics and their integration for assessing the ecological status and biocontamination of Lithuanian lakes. Limnologica, 43(4): 308–318. doi: https://doi.org/10.1016/j.limno.2013.01.003
Song K S, Wang Z M, Du J et al., 2014. Wetland degradation: its driving forces and environmental impacts in the Sanjiang Plain, China. Environmental Management, 54(2): 255–271. doi: https://doi.org/10.1007/s00267-014-0278-y
Stoddard J L, Larsen D P, Hawkins C P et al., 2006. Setting expectations for the ecological condition of streams: the concept of reference condition. Ecological Applications, 16(4): 1267–1276. doi: https://doi.org/10.1890/1051-0761(2006)016[1267:SEFTEC]2.0.CO;2
Stoddard J L, Herlihy A T, Peck D V et al., 2008. A process for creating multimetric indices for large-scale aquatic surveys. Journal of the North American Benthological Society, 27(4): 878–891. doi: https://doi.org/10.1899/08-053.1
Vander Laan J J, 2012. Environmental Assessment of Streams: Linking Land Use, Instream Stressors, and Biological Indices to Infer Likely Causes of Ecological Impairment. Logan, Utah: Utah State University.
Verhoeven J T A, Arheimer B, Yin C Q et al., 2006. Regional and global concerns over wetlands and water quality. Trends in Ecology & Evolution, 21(2): 96–103. doi: https://doi.org/10.1016/j.tree.2005.11.015
Wang Li, Song Changchun, Hu Jinming et al., 2010. Response of regeneration diversity of Carex Lasiocarpa community to different water levels in Sanjiang Plain, China. Chinese Geographical Science, 20(1): 37–42. doi: https://doi.org/10.1007/s11769-010-0037-9
Wang Z M, Song K S, Ma W H et al., 2011. Loss and fragmentation of marshes in the Sanjiang plain, Northeast China, 1954–2005. Wetlands, 31(5): 945–954. doi: https://doi.org/10.1007/s13157-011-0209-0
Weilhoefer C L, 2011. A review of indicators of estuarine tidal wetland condition. Ecological Indicators, 11(2): 514–525. doi: https://doi.org/10.1016/j.ecolind.2010.07.007
Whittier T R, Stoddard J L, Larsen D P et al., 2007. Selecting reference sites for stream biological assessments: best professional judgment or objective criteria. Journal of the North American Benthological Society, 26(2): 349–360. doi: https://doi.org/10.1899/0887-3593(2007)26[349:SRSFSB]2.0.CO;2
Williams M R, Filoso S, Longstaff B J et al., 2010. Long-term trends of water quality and biotic metrics in Chesapeake Bay: 1986–2008. Estuaries and Coasts, 33(6): 1279–1299. doi: https://doi.org/10.1007/s12237-010-9333-y
Wu Haitao, Lu Xianguo, Jiang Ming et al., 2009. Impacts of soil fauna on litter decomposition at different succession stages of wetland in Sanjiang Plain, China. Chinese Geographical Science, 19(3): 258–264. doi: https://doi.org/10.1007/s11769-009-0258-y
Wu H T, Lu X G, Wu D H et al., 2010. Biogenic structures of two ant species Formica sanguinea and Lasius flavus altered soil C, N and P distribution in a meadow wetland of the Sanjiang Plain, China. Applied Soil Ecology, 46(3): 321–328. doi: https://doi.org/10.1016/j.apsoil.2010.10.011
Wu H T, Guan Q, Lu X G et al., 2017. Snail (Mollusca: Gastropoda) assemblages as indicators of ecological condition in freshwater wetlands of Northeastern China. Ecological Indicators, 75: 203–209. doi: https://doi.org/10.1016/j.ecolind.2016.12.042
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The staff of the Sanjiang Mire Wetland Experimental Station and Honghe National Natural Reserve provided support. We thank Dr. Darold P Batzer for a helpful review of the earlier version of this paper.
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Foundation item: Under the auspices of National Key Research and Development Project of China (No. 2016YFC0500408), National Natural Science Foundation of China (No. 41871099, 41671260), Science and Technology Development Program of Jilin Province (No. 20180101080JC)
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Wu, H., Lu, K., Lyu, X. et al. A Macroinvertebrate Multimetric Index for the Bioassessment of Wetlands Adjacent to Agriculture Fields in the Sanjiang Plain, China. Chin. Geogr. Sci. 29, 974–984 (2019). https://doi.org/10.1007/s11769-019-1083-6
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DOI: https://doi.org/10.1007/s11769-019-1083-6