Abstract
A multimetric, fish-based Index of Biotic Integrity (IBI) was developed and tested to assess the ecological status of streams with different riparian conditions in the Piracicaba River Basin. Nine streams with three categories of riparian zone preservation were selected: native forest (NF) with preserved forest, secondary forest (SF) with forest in an advanced state of regeneration and surrounded by sugarcane plantations, and sugarcane (SC) without riparian vegetation and surrounded by SC crops. A continuous scoring system was employed, and candidate metrics were tested for range, responsiveness, and redundancy, resulting in the selection of eight metrics to compose the index. The final IBI score was positively correlated with an Environmental Index both in the dry (Spearman’s rho = 0.76; P = 0.01) and rainy seasons (Spearman’s rho = 0.66; P = 0.04), suggesting that this IBI is a suitable tool for the assessment of the biological conditions of these streams. The highest IBI values were observed in the rainy season at the NF and SF sites, with significant differences between the NF and SC sites (Kruskal–Wallis test: P = 0.03). The results indicated some variability in the biological integrity at SF and SC sites, suggesting a relationship with the intensity of the management of this crop. Patterns were consistent with other studies that have shown the effects of agriculture on the environmental quality of streams, which indicate the importance of the riparian zone to the maintenance of ecosystem integrity and supports the use of the IBI for biological monitoring in similar regions.
Similar content being viewed by others
References
Agostinho AA, Penczak T (1995) Populations and production of fish in two small tributaries of the Paraná River, Paraná, Brazil. Hydrobiologia 312:153–166. doi:10.1007/BF00015508
Allan JD (2004) Landscapes and riverscapes: the influence of land use on stream ecosystems. Annu Rev Ecol Evol S 35:257–284. doi:10.1146/annurev.ecolsys.35.120202.110122
APHA (2005) Standard methods for the examination of water and freshwater. American Public Health Association, Washington
Araújo FG (1998) Adaptation of the index of biotic integrity based on fish assemblages in the Paraíba do Sul River, RJ, Brazil. Braz J Biol 58:547–558
Araújo FG, Fichberg I, Pinto BCT, Peixoto MG (2003) A preliminary index of biotic integrity for monitoring the condition of the Rio Paraíba do Sul, Southeast Brazil. Environ Manage 32:516–526. doi:10.1007/s00267-003-3003-9
Araújo FG, Peixoto MG, Pinto BCT, Teixeira TP (2009) Distribution of guppies Poecilia reticulata (Peters, 1860) and Phalloceros caudimaculatus (Hensel, 1868) along a polluted stretch of the Paraíba do Sul River, Brazil. Braz J Biol. 69:41–48. doi:10.1590/S1519-69842009000100005
Barbour MT, Gerritsen J, Snyder BD, Stribling JB (1999). Rapid bioassessment protocols for use in streams and wadeable rivers: periphyton, benthic macroinvertebrates and fish. EPA 841-B-99-002. U. S. Environmental Protection Agency; Office of Water, Washington, D.C
Beechie TJ, Sibley TH (1997) Relationships between channel characteristics, woody debris, and fish habitat in Northwestern Washington streams. T Am Fish Soc. 126:217–229. doi:10.1577/1548-8659
Birnbaum JS, Winemiller KO, Shen L, Munster CL, Wilcox BP, Wilkins RN (2007) Associations of watershed vegetation and environmental variables with fish and crayfish assemblages in headwater streams of the Pedernales river, Texas. River Res Appl 996:979–996. doi:10.1002/rra.1020
Bozzetti M, Schulz UW (2004) An index of biotic integrity based on fish assemblages for subtropical streams in southern Brazil. Hydrobiologia 529:133–144. doi:10.1007/s10750-004-5738-6
Braga FMS, Gomiero LM (2009) Alimentação de peixes na microbacia do Ribeirão Grande, Serra da Mantiqueira oriental, SP. Biota Neotrop 9:207–212. doi:10.1590/S1676-06032009000300021
Britski HA (1972) Peixes de água doce do Estado de São Paulo: Sistemática. In: Branco SM (ed) Poluição e Piscicultura. Faculdade de Saúde Pública da USP e Instituto de Pesca, São Paulo, pp 79–108
Casatti L, Castro RMC (1998) A fish community of the São Francisco River headwaters riffles, Southeastern Brazil. Ichthyol Explor Freshw 9:229–242
Casatti L, Langeani F, Castro RMC (2001) Peixes de riacho do Parque Estadual Morro do Diabo, Bacia do Alto Rio Paraná, SP. Biota Neotrop 1:1–15. doi:10.1590/S1676-06032001000100005
Casatti L, Ferreira CP, Langeani F (2008) A fish-based biotic integrity index for the assessment of lowland streams in southeastern Brazil. Hydrobiologia 623:173–189. doi:10.1007/s10750-008-9656-x
Casatti L, Teresa F, Gonçalves-Souza T, Bessa E, Manzotti AR, Gonçalves CS, Zeni JO (2012) From forests to cattail: how does the riparian zone influence stream fish. Neotrop Ichthyol 10:205–214. doi:10.1590/S1679-62252012000100020
Castro RMC, Casatti L, Santos HF, Melo ALA, Martins LSF, Ferreira KM, Gibran FZ, Benine RC, Carvalho M, Ribeiro AC, Abreu TX, Bockmann FA, Pelição GZ, Stopiglia R, Langeani F (2004) Estrutura e composição da ictiofauna de riachos da bacia do Rio Grande no Estado de São Paulo, Sudeste do Brasil. Biota Neotrop 4:57–95. doi:10.1590/S1676-06032004000100006
CBH-PCJ (2011). Relatório da Situação dos Recursos Hídricos 2011, Ano Base 2010. UGRHI 05—Bacias Hidrográficas dos Rios Piracicaba, Capivari e Jundiaí
CBH-PCJ (2012) Plano das Bacias Hidrográficas dos Rios Piracicaba, Capivari e Jundiaí 2010-2020 (com propostas de atualização do enquadramento dos corpos d’água e de programa para efetivação do enquadramento dos corpos d’água até o ano de 2035). Relatório síntese. http://www.comitepcj.sp.gov.br/Paginas.php?CodPagina=578. Accessed 09 June 2013
CBJ-PCJ (2010) Situação dos Recursos Hídricos das Bacias Hidrográficas dos Rios Piracicaba, Capivari e Jundiaí UGRHI 5 Relatório Técnico Final 1° volume. http://www.comitepcj.sp.gov.br/download/RS/RSituacao-PCJ-Vol-1.pdf. Accessed 03 February 2011
Cerri CEP, Demattê JAM, Ballester MVR, Martinelli LA, Victoria RL, Roose E (2001) GIS Erosion Risk Assessment of the Piracicaba River Basin, Southeastern Brazil. Mapp Sci Remote Sens 38:157–171. doi:10.1080/07493878.2001.10642173
Chapman LL, McKenzie DJ (2009) Behavioural responses and ecological consequences. In: Richards JJ, Brauner CJ, Farrell AP (eds) Hypoxia. Academic Press, San Diego, pp 26–77
Christensen VG, Lee KE, McLees JM, Niemela SL (2012) Relations between retired agricultural land, water quality, and aquatic-community health, Minnesota River Basin. J Environ Qual 41:1459–1472. doi:10.2134/jeq2011.0468
Clarke KR, Gorley RN (2006) Software PRIMER v6 User Manual/Tutorial. Primer-E, Plymouth
Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation. Primer-E Ltd., Plymouth
Corbi JJ, Strixino ST (2006) Environmental diagnostic of metals and organochlorinated compounds in streams near sugar cane plantations activity (São Paulo State, Brazil). Quim Nova 29:61–65. doi:10.1590/S0100-40422006000100013
Costa PF, Schulz UH (2010) The fish community as an indicator of biotic integrity of the streams in the Sinos River basin, Brazil. Braz J Biol 70:195–205. doi:10.1590/S1519-69842010000600009
Dudgeon D (2008) Tropical stream ecology. Academic Press, London
EPA (2002) Developing Metrics and Indexes of Biological Integrity. EPA 822-R-02-016
Esteves RL (2006) História natural da ictiofauna dos riachos da Estação Ecológica de Itirapina (Itirapina, SP). MScDissertation, Universidade Estadual Paulista
Esteves KE, Alexandre CV (2011) development of an Index of Biotic Integrity based on fish communities to assess the effects of rural and urban land use on a stream in Southeastern Brazil. Int Rev Hydrobiol 96:296–317. doi:10.1002/iroh.201111297
Esteves KE, Lobo AVP, Faria MDR (2008) Trophic structure of a fish community along environmental gradients of a subtropical river (Paraitinga River, Upper Tietê River Basin, Brazil). Hydrobiologia 598:373–387. doi:10.1007/s10750-007-9172-4
Fausch KD, Lyons J, Karr JR, Angermeier PL (1990) Fish communities as indicators of environmental degradation. Am Fisheries Soc Symp 8:123–144
Feld CK (2005) Assessing hydromorphological degradation of sand-bottom lowland rivers in Central Europe using benthic macroinvertebrates. Dissertation, University of Duisburg-Essen
Ferreira KM (2007) Biology and ecomorphology of stream fishes from the Mogi-Guaçu. Neotrop Ichthyol 5:311–326. doi:10.1590/S1679-62252007000300012
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. doi:10.1590/S1676-06032006000300002
Ferreira A, de Paula FR, Ferraz SFB, Gerhard P, Kashiwaqui EAL, Cyrino JEP, Martinelli LA (2012) Riparian coverage affects diets of characids in neotropical streams. Ecol Freshw Fish 21:12–22. doi:10.1111/j.1600-0633.2011.00518.x
Filoso S, Martinelli LA, Williams MR, Lara LB, Krusche A, Ballester MV, Victoria R, Camargo PB (2003) Land use and nitrogen export in the Piracicaba River basin, Southeast Brazil. Biogeochemistry 65:275–294. doi:10.1023/A:1026259929269
Ganasan V, Hughes RM (1998) Application of an index of biological integrity (IBI) to fish assemblages of the rivers Khan and Kshipra (Madhya Pradesh), India. Freshw Biol 40:367–383. doi:10.1046/j.1365-2427.1998.00347.x
Gerhard P (2005) Comunidades de peixes de riachos em função da paisagem da bacia do Rio Corumbataí, Estado de São Paulo. Dissertation, University of São Paulo
Gibran FZ, Ferreira KM, Castro RMC (2001) Diet of Crenicichla britskii (Perciformes: Cichlidae) in a stream of Rio Aguapeí basin, upper Rio Paraná system, Southeastern Brazil. Biota Neotrop 1:1–5. doi:10.1590/S1676-06032001000100007
Gomiero LM, Braga FMS (2007) Reproduction of a fish assemblage in the state of São Paulo, Southeastern Brazil. Braz J Biol 67:283–292. doi:10.1590/S1519-69842007000200013
Graham JB (1997) Air-breathing fishes: evolution, diversity, and adaptation. Academic Press, San Diego
Greig-Smith P (1983) Quantitative plant ecology. Blackwell Scientific Publications, Oxford
Harding JS, Benfield EF, Bolstad PV, Helfman GS, Jones EBD (1998) Stream biodiversity: the ghost of land use past. Proc Natl Acad Sci USA 95:14843–14847
Hering D, Feld CK, 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. doi:10.1007/978-1-4020-5493-8_22
Hermoso V, Clavero M, Blanco-Garrido F, Prenda J (2010) Assessing the ecological status in species-poor systems: a fish-based index for Mediterranean Rivers (Guadiana River, SW Spain). Ecol Indic 10:1152–1161. doi:10.1016/j.ecolind.2010.03.018
Hued AC, Bistoni MA (2005) Development and validation of a Biotic Index for evaluation of environmental quality in the central region of Argentina. Hydrobiologia 543:279–298. doi:10.1007/s10750-004-7893-1
Hughes RM (1994) Defining acceptable biological status by comparing with reference conditions. In: Davis WS, Simon TP (eds) Biological assessment and criteria: tools for water resource planning and decision making. CRC Press, Boca Raton, pp 31–47
Hughes RM, Oberdorff T (1999) Applications of IBI concepts and metrics to waters outside the Unites State and Canada. In: Simon TP (ed) Assessing the sustainability and biological integrity of water resources using fish communities. CRC Press, Boca Raton, pp 79–93
IRRIGART (2006) Plano de gerenciamento integrado para remediação e proteção dos recursos hídricos da Sub-Bacia do Atibaia com ênfase no Reservatório de Salto Grande – Americana – SP. http://www.comitepcj.sp.gov.br/download/PGISaltoGrande_Relatorio.pdf. Accessed 30 Jan 2012
Karr JR (1981) Assessment of biotic integrity using fish communities. Fisheries 6:21–27
Karr JR, Toth LA, Dudley DR (1985) Fish communities of midwestern rivers: a history of degradation. Bioscience 35:90–95
Karr JR, Fausch KD, Angermeier PL, Yant PR, Schlosser IJ (1986) Assessing biological integrity in running waters: a method and its rationale. Illinois Natural History Survey Special Publication 5. Urbana, IL
Krebs CJ (1989) Ecological methodology. Harper Collins Publishers, New York
Lammert M, Allan JD (1999) Assessing biotic integrity of streams: effects of scale in measuring the influence of land use/cover and habitat structure on fish and macroinvertebrates. Environ Manag 23:257–270
Lenat DR, Crawford JK (1994) Effect of land use on water quality and aquatic biota of the three North Carolina Piedmont streams. Hydrobiologia 294:185–199. doi:10.1007/BF00021291
Lorion CM, Kennedy BP (2009) Riparian Forest buffers mitigate the effects of deforestation on fish assemblages in tropical headwater streams. Ecol Appl 19:468–479. doi:10.1890/08-0050.1
Lowe-McConnell RH (1987) Ecological studies in tropical fish communities. Cambridge University Press, Cambridge
Luiz EA, Agostinho AA, Gomes LC, Hahn NS (1998) Ecologia trófica de peixes em dois riachos da Bacia do Rio Paraná. Braz J Biol 58:273–285
Lyons J (1992) Using the Index of Biotic Integrity (IBI) to Measure Environmental Quality in Warm Water Streams of Wisconsin. United States Department of Agriculture. General Technical Report, NC-149
Lyons J, Navarro-Pérez S, Cochran PA, Santana E, Guzmán-Arroyo M (1995) Index of biotic integrity based on fish assemblages for the conservation of streams and rivers in west-central Mexico. Conserv Biol 9:569–584. doi:10.1046/j.1523-1739.1995.09030569.x
Martinelli LA, Filoso S (2008) Expansion of sugarcane ethanol production in Brazil: environmental and social challenges. Ecol Appl 18:885–898
Mazzoni R, Fenerich-Verani N, Caramaschi EP (2000) Electrofishing as a sampling technique for a coastal stream fish populations in the Southeast of Brazil. Braz J Biol 60:205–216. doi:10.1590/S0034-71082000000200003
McCormick FH et al (2001) Development of an Index of Biotic Integrity for the mid-atlantic highlands region. T Am Fish Soc 130:857–877. doi:10.1577/1548-8659(2001)
McCune B, Mefford MJ (2011) Multivariate analysis of ecological data. Version 6.0. MjM Software, Gleneden Beach, Oregon
Oberdorff T, Hughes RM (1992) Modification of an index of biotic integrity based on fish assemblages to characterize rivers of the Seine basin, France. Hydrobiologia 228:117–130. doi:10.1007/BF00006200
Oliveira DC, Bennemann ST (2005) Ictiofauna, recursos alimentares e relações com as interferências antrópicas em um riacho urbano no sul do Brasil. Biota Neotrop 5:95–107. doi:10.1590/S1676-06032005000100011
Pellegrino GQ, Moraes JM, Ballester MVR, Victoria RL, Martinelli LA (2001) Análise espaço-temporal de componentes hidroclimáticos na bacia do rio Piracicaba. Rev Bras Meteorol 9:125–135
Petesse ML, Petrere M Jr, Agostinho  (2014) Defining a fish bio-assessment tool to monitoring the biological condition of a cascade reservoirs system in tropical area. Ecol Eng 69:139–150. doi:10.1016/j.ecoleng.2014.03.070
Piacente FJ (2005) Agroindústria canavieira e o sistema de gestão ambiental: o caso das usinas localizadas nas bacias hidrográficas dos rios Piracicaba, Capivari e Jundiaí. Dissertation, University of Campinas
Pinto BCT, Araújo FG (2007) Assessing of biotic integrity of the fish community in a heavily impacted segment of a Tropical River in Brazil. Braz Arch Biol Techn 50:489–502. doi:10.1590/S1516-89132007000300015
Pinto BCT, Araujo FG, Hughes RM (2006) Effects of landscape and riparian condition on a fish index of biotic integrity in a large southeastern Brazil river. Hydrobiologia 556:69–83. doi:10.1007/s10750-005-9009-y
Pusey BJ, Arthington AH (2003) Importance of the riparian zone to the conservation and management of freshwater fish: a review. Mar Freshw Res 54:1–16. doi:10.1071/MF02041
Rabeni CF, Smale MA (1995) Effects of siltation on stream fishes and the potential mitigating role of the buffering riparian zone. Hydrobiologia 303:211–219. doi:10.1007/BF00004881
Richards C, Johnson LB, Host GE (1996) Landscape-scale influences on stream habitats and biota. Can J Fish Aquat Sci 53:295–311. doi:10.1139/f96-006
Rolla APPR, Esteves KE, Silva AOA (2009) Feeding ecology of a stream fish assemblage in an Atlantic Forest remnant (Serra do Japi, SP, Brazil). Neotrop Ichthyol 7:65–76. doi:10.1590/S1679-62252009000100009
Rondineli G, Gomiero LM, Carmassi AL, Braga FMS (2011) Diet of fishes in Passa Cinco Stream, Corumbataí River sub-basin, São Paulo state, Brazil. Braz J Biol 71:157–167. doi:10.1590/S1519-69842011000100023
Rosgen DL (1994) A classification of natural rivers. Catena 22:169–199. doi:10.1016/0341-8162(94)90001-9
Ross ST (1991) Mechanisms structuring stream fish assemblages: are there lessons from introduced species? Environ Biol Fish 30:359–368. doi:10.1007/BF02027979
Roth NE, Allan JD, Erickson DL (1996) Landscape influences on stream biotic integrity assessed at multiple spatial scales. Landsc Ecol 11:141–156. doi:10.1007/BF02447513
Santos FB, Ferreira FC, Esteves KE (2015) Assessing the importance of the riparian zone for stream fish communities in a sugarcane dominated landscape (Piracicaba River Basin, Southeast Brazil). Environ Biol Fish. doi: 10.1007/s10641-015-0406-4
São Paulo (2011) Biodiversidade no Estado de São Paulo. São Paulo: Secretaria do Meio Ambiente http://www.ambiente.sp.gov.br/wp-content/uploads/2013/09/25411-Miolo-Cartilha-Biodiversidade-Portugues-para-Aprova.pdf. Accessed 20 March 2013
Scarsbrook MR, Boothroyd IKG, Quinn JM (2000) New Zealand’s national river water quality network: long-term trends in macroinvertebrate communities. New Zeal J Mar Fresh 34:289–302
Schleiger SL (2000) Use of an index of biotic integrity to detect effects of land uses on stream fish communities in west-central Georgia. Trans Am Fish Soc 129:1118–1133. doi:10.1577/1548-8659(2000)
Schlosser IJ (1991) Stream fish ecology: a landscape perspective. Bioscience 41:704–712
Shearer JS, Berry CR (2002) Index of biotic integrity utility for the fishery of the James River of the Dakotas. J Freshw Ecol 17:575–588
Silva AM, Nalon MA, Kronka FJN, Alvares CA, Camargo PB, Martinelli LA (2007) Historical land-cover/use in different slope and riparian buffer zones in watersheds of the state of São Paulo, Brazil. Sci Agric 64:325–335. doi:10.1590/S0103-90162007000400003
SMA (2011) Biodiversidade no Estado de São Paulo. Secretaria de Estado do Meio Ambiente. SMA, São Paulo
Stanfield LW, Kilgour BW (2012) How proximity of land use affects stream fish and habitat. River Res Appl 29:891–905. doi:10.1002/rra.2585
Stauffer JC, Goldstein RM, Newman RM (2000) Relationship of wooded riparian zones and runoff potential to fish community composition in agricultural streams. Can J Fish Aquat Sci 57:307–316
Teresa FB, Casatti L (2010) Importância da vegetação ripária em região intensamente desmatada no sudeste do Brasil: um estudo com peixes de riachos. Pan-American J Aquat Sci 5:444–453
Thomaz SM, Agostinho AA, Gomes LC, Silveira MJ, Rejmánek M, Aslan CE, Chow E (2012) Using space-for-time substitution and time sequence approaches in invasion ecology. Freshw Biol. 57:2401–2410. doi:10.1111/fwb.12005
Vazzoler AE (1996) Biologia da reprodução de peixes teleósteos: teoria e prática. EDUEM, Maringá
Wang L, Lyons J, Kanehl P, Gatti R (1997) Influences of watershed land use on habitat quality and biotic integrity in Wisconsin streams. Fisheries 22:6–12. doi:10.1577/1548-8446(1997)
Wang L, Seelbach PW, Lyons J (2006) Effects of levels of human disturbance on the influence of catchment, riparian, and reach-scale factors on fish assemblages. In: Hughes RM, Wang L, Seelbach PW (eds) Landscape Influences on Stream Habitats and Biological Assemblages, American Fisheries Society Symposium 48, Bethesda, pp 199–219
Whately M, Cunha P (2007) Cantareira 2006: um olhar sobre o maior manancial de água da Região Metropolitana de São Paulo. Instituto Socioambiental, São Paulo
Whittier TR et al (2007) A structured approach for developing indices of biotic integrity: three examples from streams and rivers in the Western USA. T Am Fish Soc 136:718–735
Wichert GA, Rapport DJ (1998) Fish community structure as a measure of degradation and rehabilitation of riparian systems in an agricultural drainage basin. Environ Manag 22:425–443. doi:10.1007/s002679900117
Winemiller KO (1989) Patterns of variation in life history among South American fishes in seasonal environments. Oecologia 81:225–241. doi:10.1007/BF00379810
Wing MG, Skaugset A (2002) Relationships of channel characteristics land ownership, and land use patterns to large woody debris in western Oregon streams. Can J Fish Aquat Sci 59:796–807. doi:10.1139/f02-052
Zaret TM, Rand AS (1971) Competition in tropical stream fishes: support for the competitive exclusion principle. Ecology 52:336–342
Zuurbier P, Vooren JV (2008) Sugarcane ethanol: Contributions to climate change mitigation and the environment. Academic Publishers, Wageningen
Acknowledgments
The authors thank the Instituto de Pesca (APTA/SAA) for providing the infrastructure, its staff and students for their help in field work (Sérgio Luiz da Silva, Paulo Henrique Gusmão, Ludmila Cristina Baldi, Katerine Pereira Carvalho and Juliana Macedo Santana), Fundação de Amparo à Pesquisa do Estado de São Paulo for financial support (Proc. 2010/52069-6), Conselho Nacional de Desenvolvimento Científico e Tecnológico for the MSc scholarship (Proc. 154078/2010-7), Maria Letizia Petesse for suggestions and comments on the manuscript, Osvaldo T. Oyakawa for fish identification, Cíntia Kameyama for macrophyte identification, Mirna Ferracini for map drawing, André Vaz and Eduardo Paes for help with the statistical analyses and José Carlos Perdigão and Walter Lima for help in locating the sampling sites. This study was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Grant Number 2010/52069-6. Fernanda Bastos dos Santos has received a MSc grant from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Grant Number 154078/2010-7) .
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical Standards
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Human and Animal Rights
All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. This study was approved by the Ethics Committee of the Fisheries Institute of São Paulo (CEEAIP) (Protocol 07/2010).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
dos Santos, F.B., Esteves, K.E. A Fish-Based Index of Biotic Integrity for the Assessment of Streams Located in a Sugarcane-Dominated Landscape in Southeastern Brazil. Environmental Management 56, 532–548 (2015). https://doi.org/10.1007/s00267-015-0516-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00267-015-0516-y