Comparison of the spatial and temporal variability of macroinvertebrate and periphyton-based metrics in a macrophyte-dominated shallow lake

Abstract

The influence of spatial differences, which are caused by different anthropogenic disturbances, and temporal changes, which are caused by natural conditions, on macroinvertebrates with periphyton communities in Baiyangdian Lake was compared. Periphyton and macrobenthos assemblage samples were simultaneously collected on four occasions during 2009 and 2010. Based on the physical and chemical attributes in the water and sediment, the 8 sampling sites can be divided into 5 habitat types by using cluster analysis. According to coefficients variation analysis (CV), three primary conclusions can be drawn : (1) the metrics of Hilsenhoff Biotic Index (HBI), Percent Tolerant Taxa (PTT), Percent dominant taxon (PDT), and community loss index (CLI), based on macroinvertebrates, and the metrics of algal density (AD), the proportion of chlorophyta (CHL), and the proportion of cyanophyta (CYA), based on periphytons, were mostly constant throughout our study; (2) in terms of spatial variation, the CV values in the macroinvertebrate-based metrics were lower than the CV values in the periphyton-based metrics, and these findings may be caused by the effects of changes in environmental factors; whereas, the CV values in the macroinvertebrate-based metrics were higher than those in the periphyton-based metrics, and these results may be linked to the influences of phenology and life history patterns of the macroinvertebrate individuals; and (3) the CV values for the functional-based metrics were higher than those for the structural-based metrics. Therefore, spatial and temporal variation for metrics should be considered when assessing applying the biometrics.

Keywords

Baiyangdian Lake / biomonitoring / coefficient variation / structural metrics / functional metrics

References

[1] An K G, Park S S, Shin J Y (2002). An evaluation of a river health using the index of biological integrity along with relations to chemical and habitat conditions. Environ Int, 28(5): 411–420

[2] Angermeier P L, Smogor R A, Stauffer J R (2000). Regional frameworks and candidate metrics for assessing biotic integrity in mid-Atlantic highland streams. T Am Fish Soc, 129(4): 962–981

[3] Barbour M T, Gerritsen J, Griffith G E, Frydenborg R, McCarron E, White J S, Bastian M L (1996). A framework for biological criteria for Florida streams using benthic macroinvertebrates. J N Am Benthol Soc, 15: 185–211

[4] Barbour M T, Gerritsen J, Snyder B D, Stribling J B (1999). Rapid Bioassessment Protocols for Use in Streams and Rivers: Periphyton, Benthic Macroinvertebrates, and Fish (2nd ed). EPA 841/B-99/002. US Environmental Protection Agency, Washington, D.C.

[5] Bazzanti M, Seminara M (1995). Eutrophication in a deep, meromictic lake (Lake Albano, Central Italy): spatial-temporal patterns of profundal benthic community as a tool for assessing environmental stress in the hypolimnion. Limnologica Jena, 25(11): 21–31

[6] Beck M W, Hatch L K (2009). A review of research on the development of lake indices of biotic integrity. Environ Rev, 17: 21–44

[7] Beck M W, Hatch L K, Vondracek B, Valley R D (2010). Development of a macrophyte-based index of biotoc integrity for Minnesota Lakes. Ecol Indic, 10(5): 968–979

[8] Berkman H E, Rabeni C F (1987). Effects of siltation on stream fish communities. Environ Biol Fishes, 18: 285–294

[9] Biggs J, Williams P, Whitfield M, Nicolet P, Weatherby A (2005). 15 years of ponds assessment in Britain: results and lessons learned from the work of Pond Conservation. Aquat Conserv: Mar Freshw Ecosyst, 15(6): 693–714

[10] Blocksom K A, Kurtenbach J P, Klemm D J, Fulk F A, Cormier S M (2002). Development and evaluation of the Lake Macroinvertebrate Integrity Index (LMII) for New Jersey lakes and reservoirs. Environ Monit Assess, 77(3): 311–333

[11] Borja Á (2005). The European Water Framework Directive: a challenge for nearshore, coastal and continental shelf research. Cont Shelf Res, 25(14): 1768–1783

[12] Borja A, Franco J, Pérez V (2000). A marine biotic index to eatablish the ecological quality of soft-bottom benthos within European estuarine and coastal environments. Mar Pollut Bull, 40(12): 1100–1114

[13] Brinkhurst R O, Hamilton A L, Herrington H B (1968). Components of the bottom fauna of the St. Lawrence, Great Lakes. No. PR33, Great Lakes Institute, University of Toronto, Toronto, ON, Canada, 50

[14] Brodersen K P, Dall P C, Lindegaard C (2008). The fauna in the upper stony littoral of Danish lakes: macroinvertebrates as trophic indicators. Freshw Biol, 39: 577–592

[15] Cheruvelil K S, Sorano P A, Madsen J D, Roberson M J (2002). Plant architecture and epiphytic macroinvertebrate communities: the role of an exotic dissected macrophyte. J N Am Benthol Soc, 21: 261–277

[16] China Bureau of Environmental Protection (CBEP) (2002). Methods for monitoring and analysis of water and wastewater (4th ed). Beijing: China Environmental Science Press, 246–248 (in Chinese)

[17] Chinese Academy of Sciences (CAS) (1978). Soil map of China (edited by the Nanjing Institute of Soil Science, Chinese Academy of Sciences). Beijing: Cartographic Publishing House (digital version published 1996 by State Key Laboratory of Resources and Environment Information System, Chinese Academy of Sciences, Beijing)

[18] Costanza R, d’Arge R, De Groot R, Farber S, Grasso M, Hannon B, Limburg K, Naeem S, O'Neill R V, Paruelo J, Raskin R G, Sutton P, van den Belt M (1998). The value of the world’s ecosystem services and natural capital. Ecol Econ, 25(1): 3–15

[19] Cyr H, Downing J A (1988). Empirical relationships of phytomacrofaunal abundance to plant biomass and macrophyte bed characteristics. Can J Fish Aquat Sci, 45: 976–984

[20] De Lange H J, De Haas E M, Maas H, Peeters E T H M (2005). Contaminated sediments and bioassay responses of three macroinvertebrates, the midge larva Chironomus riparius, the water louse Asellus aquaticus and the mayfly nymph Ephoron virgo. Chemosphere, 61(11): 1700–1709

[21] De Szalay F A, Resh V H (2000). Factors influencing macroinvertebrate colonization of seasonal wetlands: responses to emergent plant cover. Freshw Biol, 45(3): 295–308

[22] Diehl S (1992). Fish predation and benthic community structure: the role of omnivory and habitat complexity. Ecology, 73(5): 1646–1661

[23] Fano E A, Mistri M, Rossi R (2003). The ecofunctional quality index (EQI): a new tool for assessing lagoonal ecosystem impairment. Estuar Coast Shelf S, 56(3–4): 709–716

[24] Fellows C, Clapcott J, Udy J, Bunn S, Harch B, Smith M, Davies P (2006). Benthic metabolism as an indicator of stream ecosystem health. Hydrobiologia, 572(1): 71–87

[25] Findlay S, Sinsabaugh R L (2006). Large-scale variation in subsurface stream biofilms: a cross-regional comparison of metabolic function and community similarity. Microb Ecol, 52(3): 491–500

[26] Gabriels W, Lock K, De Pauw N, Goethals P L M (2010). Multimetric Macroinvertebrate Index Flanders (MMIF) for biological assessment of rivers and lakes in Flanders (Belgium). Limnologica-Ecology Management of Inl Waters, 40(3): 199–207

[27] Gérard C (2000). Dynamics and structure of a benthic macroinvertebrate community in a lake after drought. J Freshwat Ecol, 15: 65–69

[28] Gilinsky E (1984). The role of fish predation and spatial heterogeneity in determining benthic community structure. Ecology, 65(2): 455–468

[29] Gold C, Feurtet-Mazel A, Coste M, Boudou A (2002). Field transfer of periphytic diatom communities to assess short-term structural effects of metals (Cd, Zn) in rivers. Water Res, 36(14): 3654–3664

[30] Griffith M B, Hill B H, McCormick F H, Kaufmann P R, Herlihy A T, Selle A R (2005). Comparative application of indices of biotic integrity based on periphyton, macroinvertebrates, and fish to southern Rocky Mountain streams. Ecol Indic, 5(2): 117–136

[31] Hamalainen H, Luotonen H, Koskenniemi E, Liljaniem P (2003). Inter-annual variation in macroinvertebrate communities in a shallow forest lake in eastern Finland during 1990–2001. Hydrobiologia, 506/509: 389–397

[32] Heino J (2000). Lentic macroinvertebrate assemblage structure along gradients in spatial heterogeneity, habitat size and water chemistry. Hydrobiologia, 418: 229–242

[33] Hill B H, Herlihy A T, Kaufmann P R, Stevenson J R, Mccormick F H, Johnson C B (2000). Use of periphyton assemblage data as an index of biotic integrity. J N Am Benthol Soc, 19: 50–67

[34] Hilsenhoff W L (1987). An improved biotic index of organic stream pollution. Great Lakes Entomol, 30: 31–39

[35] Hornung J P, Foote A L (2006). Aquatic invertebrate responses to fish presence and vegetation complexity in western boreal wetlands with implications for waterbird productivity. Wetlands, 26: 1–12

[36] Institute of Soil Science, Chinese Academy of Sciences (1978). Physical and Chemical Analysis of Soil. Shanghai: Shanghai Science and Technology Press, 132–136 (In Chinese)

[37] Iwaniec D M, Childers D L, Rondeau D, Madden C J, Saunders C (2006). Effects of hydrologic and water quality drivers on periphyton dynamics in the southern Everglades. Hydrobiologia, 569: 223–235

[38] Johnson R K (1998). Spatiotemporal variability of temperate lake macroinvertebrate communities: detection of impact. Ecol Appl, 8(1): 61–70

[39] Jongman R H, Ter Braak C J F, Van Tongeren O F R (1987). Data analysis in community and landscape ecology, Pudoc, Wageningen, 91–173

[40] Karr J R (1981). Assessment of biotic integrity using fish communities. Fisheries (Bethesda, Md), 6: 21–27

[41] Kashian D R, Burton T M (2000). A comparison of macroinvertebrates of two Great Lakes coastal wetlands: testing potential metrics for and index of ecological integrity. J Great Lakes Res, 26(4): 460–481

[42] Kelly M, Bennion H, Burgess A, Ellis J, Juggins S, Guthrie R, Jamieson J, Adriaenssens V, Yallop M (2009). Uncertainty in ecological status assessments of lakes and rivers using diatoms. Hydrobiologia, 633: 5–15

[43] Kireta A R, Reavie E D, Sgro G V, Angradi T R, Bolgrien D W, Hill B H, Jicha T M (2012). Planktonic and periphytic diatoms as indicators of stress on great rivers of the United States: testing water quality and disturbance models. Ecol Indic, 13(1): 222–231

[44] Kornijów R (1989). Seasonal changes in the macrofauna living on submerged plants in two lakes of different trophy. Arch Hydrobiol, 117: 49–61

[45] Kröncke I, Reiss H (2010). Influence of macrofauna long-term natural variability on benthic indices used in ecological quality assessment. Mar Pollut Bull, 60(1): 58–68

[46] Ledger M E, Hildrew A G (1998). Temporal and spatial variation in the epilithic biofilm of an acid stream. Freshwater Biol, 40(4): 655–670

[47] Lewis P A, Klemm D J, Thoeny W T (2001). Perspectives on use of a multimetric lake bioassessment integrity index using benthic macroinvertebrates. Northeastern Naturalist, 8(2): 233–246

[48] Lu R K (2000). Methods for Soil Agricultural Chemistry Analysis. Beijing: Chinese Agricultural Science and Technology Press

[49] Lunde K B, Resh V H (2012). Development and validation of a macroinvertebrate index of biotic integrity (IBI) for assessing urban impacts to Northern California freshwater wetlands. Environ Monit Assess, 184(6): 3653–3674

[50] Ma M Y, Liu J L, Wang X M (2011). Biofilms as potential indicators of macrophyte-dominated lake health. Ecotoxicology, 20(5): 982–992

[51] Mason W T, Lewis P A Jr, Anderson J B (1971). Maconinvertebrate collections and water quality in the Ohio River Basin, 1963–1967. Office of Technical Programs, AQC Laboratory, Water Quality Office, US Environmental Protection Agency, Cincinnati, OH. 52 pp., Appendix A–1 to A–65

[52] Melaas C L, Zimmer K D, Butler M G, Hanson M A (2001). Effects of rotenone on aquatic invertebrate communities in prairie wetlands. Hydrobiologia, 459(1–3): 177–186

[53] Moore M J C, Langrehr H A, Angradi T R (2012). A submersed macrophyte index of condition for the Upper Mississippi River. Ecol Indic, 13(1): 196–205

[54] O’Connor R J, Walls T E, Hughes R M (1998). Using multiple taxonomic groups to index the ecological condition of lakes. Environ Monit Assess, 61: 207–228

[55] Plafkin J L, Barbour M T, Porter K D, Gross S K, Hughes R M (1989). Rapid bioassessment protocols for use in streams and rivers: benthic macroinvertebrates and fish. EPS/440/4–89/001. US Environmental Protection Agency, Washington, DC. 1–1 to 8–19 pp., Appendices A–1 to 1–42

[56] Rennie M D, Jackson L J (2005). The influence of habitat complexity on littoral invertebrate distributions: pattern differs in shallow prairie lakes with and without fish. Can J Fish Aquat Sci, 62: 2088–2099

[57] Rothrock P E, Simon T P, Stewart P M (2008). Development, calibration, and validation of a littoral zone plant index of biotic integrity (PIBI) for lacustrine wetlands. Ecol Indic, 8(1): 79–88

[58] Seele J, Mayr M, Staab F, Raeder U (2000). Combination of two indication systems in pre-alpine lakes-diatom index and macrophyte index. Ecol Model, 130(1–3): 145–149

[59] Sierra M V, Gomez N (2007). Structual characteristics and oxygen consumption of the epipelic biofilm in three lowland streams exposed to different land uses. Water Air Soil Pollut, 186(1): 115–127

[60] Sorace A, Formichetti P, Boano A, Andreani P, Gramegna C, Mancini L (2002). The presence of a river bird, the dipper, in relation to water quality and biotic indices in central Italy. Environ Pollut, 118(1): 89–96

[61] Tangen B A, Bulter M G, Michael J E (2003). Weak correspondence between macroinvertebrate assemblages and land use in Prairie Pothole Region wetlands. USA. Wetlands, 23: 104–115

[62] Tipping B, Bass J A B, Hardie D, Haworth E Y, Hurley M A, Wills G (2002). Biological responses to the reversal of acidification in surface waters of the English Lake District. Environ Pollut, 116(1): 137–146

[63] Tolonen K T, Hämäläinen H, Holopainen I J, Karjalainen J (2001). Influences of habitat type and environmental variables on littoral macroinvertebrate communities in a large lake system. Arch Hydrobiol, 152: 39–67

[64] Tolonen K T, Hämäläinen H, Holopainen I J, Mikkonen K, Karjalainen J (2003). Body size and substrate association of littoral insects in relation to vegetation structure. Hydrobiologia, 499(1–3): 179–190

[65] Townsend C R, Hildrew A G (1994). Species traits in relation to a habitat templet for river systems. Freshw Biol, 31(3): 265–275

[66] Trigal C, García-Criado F, Fernández-Aláez C (2006). Among-habitat and temporal variability of selected macroinvertebrate based metrics in a Mediterranean shallow lake (NW Spain). Hydrobiologia, 563(1): 371–384

[67] Trigal C, García-Criado F, Fernández-Aláez C (2007). Macroinvertebrate communities of mediterranean ponds (North Iberian Plateau): importance of natural and human-induced variability. Freshw Biol, 52(10): 2042–2055

[68] USEPA (1998a). Environmental monitoring and assessment program-surface waters: field operations and methods for measuring the ecological conditions of wadeable streams, EPA/620/R-94/004F, U.S.EPA, Research Triangle Park, North Carolina

[69] USEPA (1998b). Lake and reservoir bioassessment and biocriteria: Technical Guidance Document, EPA 841-B-98–007, USEPA, Washington, D.C.

[70] USEPA (1999). Rapid bioassessment protocols for use in wadeable streams and rivers, EPA 841-B-99–002, U.S.EPA, Washington, D.C.

[71] Wallace J B, Anderson N H (1996). Habitat, life history, and behavioral adaptations of aquatic insects. In: Merritt RW, Cummins KW, eds. An Introduction to the Aquatic Insects of North America(3rd ed). Dubuque: Kendall/Hunt Publishing Co., 41–73

[72] Wefering F M, Danielson L E, White N M (2000). Using the AMOEBA approach to measure progress toward ecosystem sustainability within a shellfish restoration project in North Carolina. Ecol Model, 130(1–3): 157–166

[73] White J, Irvine K (2003). The use of littoral mesohabitats and their macroinvertebrate assemblages in the ecological assessment of lakes. Aquat Conserv, 13(4): 331–351

[74] Xu F L, Tao S, Dawson R W, Li P G, Cao J (2001). Lake ecosystem health assessment: indicators and methods. Water Res, 35(13): 3157–3167

[75] Zhang L L, Liu J L, Yang Z F, Li Y, Yang Y (2013). Integrated ecosystem health assessment of a macrophyte-dominated lake. Ecol Model, 242: 141–152

[76] Zhou Q F, Zhang J B, Fu J J, Shi J B, Jiang G B (2008). Biomonitoring: an appealing tool for assessment of metal pollution in the aquatic ecosystem. Anal Chim Acta, 606(2): 135–150

[77] Zimmer K D, Hanson M A, Butler M G, Duffy W G (2001). Size distribution of aquatic invertebrates in two prairie wetlands, with and without fish, with implications for community production. Freshw Biol, 46(10): 1373–1386

Acknowledgments

This study was supported by the National Water Pollution Control Major Project of China (2012ZX07203-006), and the National Science Foundation for Innovative Research Group (No. 51121003). We also want to thank Q.Y. Chen for providing critical feedback during the preparation of the manuscript. Lastly, we thank M.Y. Ma and X.M. Wang for providing the calculating and collection methods regarding periphytons.

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg