Abstract
We developed MMI models that combine responses of fish and benthic macroinvertebrates for the evaluation of the biotic integrity of streams. The MMI was developed using a dataset covering stream sampling sites in the South of Brazil. Reference streams were identified based on the physical and chemical conditions and riparian vegetation. Thirty-four metrics were calculated and evaluated for their range, redundancy, and responsiveness to the environmental perturbation. We applied a robust approach to select the most sensitive metrics and MMI models based on the complexity and ability of the index in distinguishing impacted and reference sites. The four best MMI models selected are composed of different combinations of the eight metrics: % fish herbivorous, fish evenness, fish abundance, % macroinvertebrate shredder; % macroinvertebrate predator; % macroinvertebrate tolerant, % macroinvertebrate swimmer, and % macroinvertebrate burrower. All of the MMI models selected presented good performance in distinguishing reference streams from those impacted by different forms of land use. This study is one of the few attempts to use more than one biological assemblage in a single-multimetric index. Accordingly, we believe that the unified MMI we developed could be a useful tool to assist in the conservation and management of water resources in Neotropical regions, specially, in the implementation of ecological integrity tools more cost-effectively.
Similar content being viewed by others
References
Allan JD (2004) Landscapes and riverscapes: the influence of land use on stream ecosystem. Annu Rev Ecol Evol Syst 35(1):257–284
Angermeier PL, Karr JR (1984) Fish communities along environmental gradients in a system of tropical streams. Environ Biol Fish 9:117–135
Argillier C, Caussé S, Gevrey M, Pédron S, De Bortoli J, Brucet S, Emmrich M, Jeppesen E, Lauridsen T, Mehner T, Olin M, Rask M, Volta P, Winfield IJ, Kelly F, Krause T, Palm A, Holmgren K (2012) Development of a fish-based index to assess the eutrophication status of European lakes. Hydrobiologia 704:193–211
Avma (2001) Panel on euthanasia. Report of the AVMA panel on euthanasia. J Am Vet Med Assoc 218(5):669–696
Barbour MT, Gerritsen J, Snyder BD, Stribling JB (1999) Rapid bioassessment protocols for use in streams and wadeable rivers: periphyton, benthic macroinvertebrates and fish. 2nd edn Environmental Protection Agency, Office of Water, Washington, D.C, EPA 841-B- 99-002.
Birk S, Bonne W, Borja A, Brucet S, Courrat A, Poikane S, Solimini A, van de Bund W, Zampoukas N (2012) Three hundred ways to assess Europe’s surface waters: An almost complete overview of biological methods to implement the Water Framework Directive. Ecol Indic 18:31–41
Borja A, Dauer D, Díaz R, Llansó RJ, Muxika I, Rodríguez JG, Schaffner L (2008) Assessing estuarine benthic quality conditions in Chesapeake Bay: acomparison of three indices. Ecol Indic 8:395–403
Bozzetti M, Schulz HU (2004) An index of biotic integrity based on fish assemblages for subtropical streams in southern Brazil. Hydrobiologia 529:133–44
Britski HA, Silimon KZS, Lopes BS (1999) Peixes do Pantanal. Manual de Identificação. EMBRAPA, Brasília
Bryce SA, Hughes RM, Kaufman PR (2002) Development of a bird integrity index: using bird assemblages as indicators of riparian condition. Environ Manag 30:294–310
Buendia C, Gibbins CN, Vericat D, Batalla RJ, Douglas A (2013) Detecting the structural and functional impacts of fine sediment on stream invertebrates. Ecol Indic 25:184–196
Buss DF, Vitorino AS (2010) Rapid bioassessment protocols using benthic macroinvertebrates in Brazil: evaluation of taxonomic sufficiency. J N Am Benthol Soc 29(2):562–571
Buss DF, Carlise DM, Chon TS, Culp J, Harding JS et al. (2015) Stream biomonitoring using macroinvertebrates around the globe: a comparison of large-scale programs. Environ Monit Assess 187:4132
Cuffney TF, Brightbill RA, May JT, Waite IR (2010) Responses of benthic macroinvertebrates to environmental changes associated with urbanization in nine metropolitan areas. Ecol Appl 20(5):1384–1401
Cuffney TF, Zappia H, Giddings EMP, Coles JF (2005) Effects of urbanization on benthic macroinvertebrate assemblages in contrasting environmental settings: Boston, Massachusetts; Birmingham, Alabama; and Salt Lake City, Utah. Am Fish Soc Symp 47:361–407
Cunico AM, Gubiani ÉA (2017) Effects of land use on sediment composition in low-order tropical streams. Urban Ecosyst 20(2):415–423
Dedieu N, Clavier S, Vigouroux R, Cerdan P, Céréghino R (2016) A multimetric macroinvertebrate index for the implementation of the European Water Framework Directive in French Guiana. East Amazonia. River Res Appl 32:501–515
Dudgeon D, Arthington AH, Gessner MO, Kawabata ZI, Knowler DJ, Leveque C, Naiman RJ, Prieur-Richard AH, Soto D, Stiassny MLJ, Sullivan CA (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Bio Rev 81:163–182
Dufech APS, Azevedo MA, Fialho CB (2003) Comparative dietary analysis of two populations of Mimagoniates rhocharis (Characidae: Glandulocaudinae) from two streams of Southern Brazil. Neotrop Ichthyol 1:67–74
Esselman PC, Infante DM, Wang L, Cooper AR, Wieferich D, Tsang Y-P, Thornbrugh DJ, Taylor WW (2013) Regional fish community indicators of landscape disturbance to catchments of the conterminous United States. Ecol Indic 26:163–173
Fabrizi A, Goretti E, Compin A, Céréghino R (2010) Influence of fish farming on the spatial patterns and biological traits of river invertebrates in an appenine stream system (Italy). Inter Rev Hydrobiol 95:410–427
Fausch KD, Lyons JD, Angermeier PL, Karr JR (1990) Fish communities as indicators of environmental degradation. Am Fish Soc Symp 8:123–144
Fernández HR, Domínguez E (2001) Guía para la determinacíon de los artrópodos bentônicos sudamericanos. Editorial Universitaria de Tucumán, Tucumán
Ferreira MT, Rodríguez-González PM, Aguiar FC, Albuquerque A (2005) Assessing biotic integrity in Iberian rivers: development of a multimetric plant index. Ecol Indic 5:137–149
Ferreira CP, Casatti L (2006) Integridade biótica de um córrego na bacia do Alto Rio Paraná avaliada por meio da comunidade de peixes. Biota Neotrop 6:1–25
Ferreira A, De Paula FR, Ferraz SFB, Gerhard P, Kashiwaqui EAL, Cyrino JEP, Martinelli LA (2011) Riparian coverage affects diets of characids in Neotropical streams. Ecol Freshw Fish 63:1272–1282
Fogaça FNO (2012) Ephemeroptera, Plecoptera e Trichoptera (EPT) como indicadores dos impactos ambientais da urbanização em riachos neotropicais. Tese (doutorado em Ecologia de Ambientes Aquáticos Continentais), Departamento de Biologia, Universidade Estadual de Maringá, Maringá. 62 f.:il
Freund JG, Petty JT (2007) Response of fish and macroinvertebrate bioassessment indices to water chemistry in a mined appalachian watershed. Environ Manag 39:707–720
Google (2014) Google earth. Google, Inc., Mountain View, California
Graça WJ, Pavanelli CS (2007) Peixes da planície de inundação do alto rio Paraná e áreas adjacentes. EDUEM, Maringá
Griffith MB, Brian HH, McCormick FH, Kaufmann PR, Herlihy AT, Selle AR (2005) Comparative application of indices of biotic integrity based on periphyton, macroinvertebrates, and fish to southern Rocky Mountain streams. Ecol Indic 5:117–136
Hauer FR, Lamberti GA (2007) Methods in stream ecology, 2nd edn. Elsevier, Oxford
Helson JE, Williams DD (2013) Development of a macroinvertebrate multimetric index for the assessment of low-land streams in the neotropics. Ecol Indic 29:167–178
Henle K, Davies KF, Kleyer M, Margules C, Settele J (2004) Predictors of species sensitivity to fragmentation. Biodivers Conserv 13:207–251
Hering D, Feld CJ, Moog O, Ofenbock T (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 566:311–324
IPARDES—Instituto Paranaense de Desenvolvimento Econômico e Social (2004) Leituras Regionais, IPARDES, Curitiba. http://www.ipardes.gov.br/webisis.docs/leituras_reg_sumario_executivo.pdf. Accessed 19 May 2015
Ivasauskas TJ, Bettoli PW (2014) Development of a multimetric index for fish assemblages in a cold tailwater in Tennessee. Trans Am Fish Soc 143:495–507
Jackson DA (1993) Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. Ecology 74:2204–2214
Jia Y, Sui X, Chen Y (2013) Development of a fish-based index of biotic integrity for wadeable streams in Southern China. Environ Manag 52:995–1008
Johnson DE (1998) Applied multivariate methods for data analysis. ITP, Pacific Grove
Kane DD, Gordon SI, Munawar M, Charlton MN, Culver DA (2009) The planktonic index of biotic integrity (P-IBI): an approach for assessing lake ecosystem health. Ecol Indic 9:1234–1247
Karr JR (1981) Assessment of biotic integrity using fish communities. Fisheries 6:21–27
Karr JR (1991) Biological integrity: a long-neglected aspect of water resource management. Ecol Appl 1:66–84
Kennard MJ, Harch BD, Pusey BJ, Arthington AH (2006) Accurately defining the reference condition for summary biotic metrics: a comparison of four approaches. Hydrobiologia 572:151–170
Kosnicki E, Sefick SA, Paller MH, Jerrell MS, Prusha BA, Sterrett SC, Tuberville TD, Feminella JW (2016) A stream multimetric macroinvertebrate index (MMI) for the sand hills ecoregion of the southeastern plains, USA. Environ Manag 58:741–751
Kuehne LM, Olden JD, Strecker AL, Lawler JJ, Theobald DM (2017) Past, present, and future of ecological integrity assessment for fresh waters.Front Ecol Environ 15:197–205
Li Y, Li Y, Xu Z, Li L (2016) Assessment of the Huntai River in China using a multimetric index based on fish and macroinvertebrate assemblages. J Freshw Ecol 31(2):169–190
Ligeiro R, Hughes RM, Kaufmann PR, Macedo DR, Firmiano KL, Ferreira WR, Oliveira D, Melo AS, Callisto M (2013) Defining quantitative stream disturbance gradients and the additive role of habitat variation to explain macroinvertebrate taxa richness. Ecol Indic 25:45–57
Lunde KB, Resh VH (2012) Development and validation of a macroinvertebrate index of biotic integrity (IBI) for assessing urban impacts to northern California freshwater wetlands. Environ Monit Assess 184:3653
Masese FO, Kitaka N, Kipkemboi J, Gettel GM, Irvine K, McClain ME (2014) Macroinvertebrate functional feeding groups in Kenyan highland streams: evidence for a diverse shredder guild. Freshw Sci 33:435–450
McDonough TA, Hickman GD (1999) Reservoir fishery assessment index development: a tool for assessing ecological health in Tennessee valley authority impoundments. In: Simon TP (ed) Assessing the sustainability and biological integrity of water resource quality using fish communities. CRC Press, Boca Raton, FL, pp 523–540
McKinney ML (2008) Effects of urbanization on species richness—a review of plants and animals. Urban Ecosyst 11:161–176
Mereta ST, Boets P, Meester LD, Goethals PLM (2013) Development of a multi-metric index based on benthic macroinvertebrates for the assessment of natural wetlands in Southwest Ethiopia. Ecol Indic 29:510–521
Merritt RW, Cummins KW (Eds) (1996) An introduction to the aquatic insects of North America. (3 edn). Kendall/Hunt, Dubuque, Iowa
Metcalfe JL (1989) Biological water quality assessment of running waters based on macroinvertebrate communities: history and present status in Europe. Environ Pollut 60:101–139
Mondy CP, Villeneuve B, Archaimbault V, Usseglio-Polatera P (2012) A new macroinvertebrate-based multimetric index (I2M2) to evaluate ecological quality of French wadeable streams fulfilling the WFD demands: a taxonomical and trait approach. Ecol Indic 18:452–467
Moya N, Hughes RM, Domínguez E, Gibon MF, Goitia E, Oberdorff T (2011) Macroinvertebrate-based multimetric predictive models for evaluating the human impact on biotic condition of Bolivian streams. Ecol Indic 11:840–847
Mugnai R, Nessimian JL, Baptista DF (2010) Manual de Identificação de Macroinvertebrados do Estado do Rio de Janeiro. Technical Books, Rio de Janeiro
Ode PR, Rehn AC, May JT (2005) A quantitative tool for assessing the integrity of southern coastal California streams. Environ Manag 35:493–504
Oliveira RBS, Baptista DF, Mugnai R, Castro CM, Hughes RM (2011) Towards rapid bioassessment of wadeable streams in Brazil: development of the Guapiaçu-Macau Multimetric Index (GMMI) based on benthic macroinvertebrates. Ecol Indic 11:1584–1593
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2015) Vegan: community ecology package. R package vegan, version 2.2-1. http://www.cran.r-project.org/package=vegan
Pallottini M, Goretti E, Selvaggi R, Cappelletti D, Dedieu N, Cereghino R (2017a) An efficient semi-quantitative macroinvertebrate multimetric index for the assessment of water and sediment contamination in streams. Inland Waters 7:314–322
Pallottini M, Cappelletti D, Fabrizi A, Gaino E, Goretti E, Selvaggi R, Cereghino R (2017b) Macroinvertebrate functional trait responses to chemical pollution in agricultural-industrial landscapes. River Res Appl 33:505–513
Pérez G (1988) Guía par el estudio de los macroinvertebrados acuáticos del Departamento de Antioquia. Editorial Presença, Bogotá
Petchey OL, Gaston KJ (2006) Functional diversity: back to basics and looking forward. Ecol Lett 9:741–758
Pont D, Hugueny B, Beier U et al. (2006) Assessing river biotic condition at a continental scale: A European approach using functional metrics and fish assemblages. J Appl Ecol 43:70–80
Prudente BS, Pompeu PS, Montag L (2018) Using multimetric indices to assess the effect of reduced impact logging on ecological integrity of Amazonian streams. Ecol Indic 91:315–323
Qadir A, Malik RN (2009) Assessment of an index of biological integrity (IBI) to quantify the quality of two tributaries of river Chenab, Sialkot, Pakistan. Hydrobiologia 621:127–153
R Development Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org/
Rabeni CF, Doisy KE, Zweig LD (2005) Stream invertebrate assemblage functional responses to deposited sediment. Aquat Sci 67:395–402
Raburu PO, Masese FO (2012) Development of a fish-based index of biotic integrity (FIBI) for monitoring riverine ecosystems in the lake Victoria Drainage Basin, Kenya. River Res Appl 28:23–38
Reis RE, Kullander SO, Ferraris Jr CJ (2003) Check list of the freshwater fishes of south and central America. Edipucrs, Porto Alegre
Ruaro R, Gubiani EA (2013) A scientometric assessment of 30 years of the Index of Biotic Integrity in aquatic ecosystems: Applications and main flaws. Ecol Indic 29:105–110
Ruaro R, Gubiani ÉA, Cunico AM, Moretto Y, Piana PA (2016) Comparison of fish and macroinvertebrates as bioindicators of Neotropical streams. Environ Monit Assess 188:45
Ruaro R, Mormul RP, Gubiani EA, Piana PA, Cunico AM, da Graça WJ (2018) Non-native fish species are related to the loss of ecological integrity in Neotropical streams: a multimetric approach. Hydrobiologia 817:413–430
Scheiner SM, Gurevitch J (1993) Design and analysis of ecological experiments. Chapman & Hall, New York, NY
Schoolmaster Jr DR, Grace JB, Schweiger EW (2012) A general theory of multimetric indices and their properties. Methods Ecol Evol 3(4):773–781
Schoolmaster DR, Grace JB, Schweiger EW, Guntenspergen GR, Mitchell BR, Miller KM, Little AM (2013) An algorithmic and information-theoretic approach to multimetric index construction. Ecol Indic 26:14–23
Souza RF, Machado SA, Galvão F, Figueiredo Filho A, Picoli AC (2019) Forests of the Iguaçu National Park: structure, composition, and richness. Floresta Ambient 26(1):e20150267
Stevenson RJ, Tang T, Infante DM (2018) Advancing evaluation of bioassessment methods: a reply to Liu and Cao. Sci Total Environ 645:895–900
Stoddard JL, Larsen DP, Hawkins CP, Norris RK, Johnson RH (2006) Setting expectations for the ecological condition of running waters: the concept of reference condition. Ecol Appl 16:1267–1276
Stoddard JL, Herlihy AT, Peck DV, Hughes RM, Whittier TR, Tarquino E (2008) A process for creating multimetric indices for large-scale aquatic surveys. J N Am Benthol Soc 27(4):878–891
Strahler AN (1957) Quantitative analysis of watershed geomorphology. Trans Am Geophys Union 38:913–920
Tanaka MO, De Souza ALT, Moschini LE, De Oliveira AK (2016) Influence of watershed land use and riparian characteristics on biological indicators of stream water quality in southeastern Brazil. Agr Ecosyst Environ 216:333–339
Tomanova S, Goitia E, Helešic J (2006) Trophic levels and functional feeding groups of macroinvertebrates in Neotropical streams. Hydrobiologia 556:251–264
Van Sickle J (2010) Correlated metrics yield multimetric indices with inferior per-formance. Trans Am Fish Soc 139:1802–1817
Waite IR, Herlihy AT, Larsen DP, Urquhart S, Klemm D (2004) The effects of macroinvertebrate taxonomic resolution in large landscape bioassessments: an example from the Mid-Atlantic Highlands, U.S.A. Freshw Biol 49:474–489
Walters DM, Roy AH, Leigh DS (2009) Environmental indicators of macroinvertebrate and fish assemblage integrity in urbanizing watersheds. Ecol Indic 9:1222–1233
Walton BM, Sailing M, Wyles J, Wolin J (2007) Biological integrity in urban streams: toward resolving multiple dimensions of urbanization. Landsc Urban Plan 79:110–123
Wellemeyer JC, Perkin JS, Fore JD, Boyd C (2018) Comparing assembly processes for multimetric indices of biotic integrity. Ecol Indic 89:590–609
Whittier TR, Hughes RM, Stoddard JL, Lomnicky GA, Peck DV, Herlihy AT (2007) A structured approach to developing indices of biotic integrity: three examples from western USA streams and rivers. Trans Am Fish Soc 136:718–735
Wood PJ, Armitage PD (1997) Biological effects of fine sediment in the lotic environment. Environ Manag 21(2):203–217
Zhu D, Chang J (2008) Annual variations of biotic integrity in the upper Yangtze River using an adapted index of biotic integrity (IBI). Ecol Indic 8:564–572
Acknowledgements
We would like to thank Fundação Parque Tecnológico Itaipu (FPTI) for granting the first author a scholarship. The researchers and technicians of Grupo de Pesquisas em Recursos Pesqueiros e Limnologia—Gerpel and of Laboratório de Ecologia, Pesca e Ictiologia—LEPI supported us during the present study. We would also like to thank Jhony Ferry Mendonça da Silva for his help in developing the location map. Finally, we would like to thank MCT/CNPq/CT-Hidro (Proc. 555185/2006-0) for funding the Pirapó watershed project. ÉAG is grateful to CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for the continuous research productivity grants (PQ Process Number: 308578/2017-1). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Rights and permissions
About this article
Cite this article
Ruaro, R., Gubiani, É.A., Cunico, A.M. et al. Unified Multimetric Index for the Evaluation of the Biological Condition of Streams in Southern Brazil Based on Fish and Macroinvertebrate Assemblages. Environmental Management 64, 661–673 (2019). https://doi.org/10.1007/s00267-019-01210-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00267-019-01210-6