{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,10]],"date-time":"2026-03-10T04:18:35Z","timestamp":1773116315136,"version":"3.50.1"},"reference-count":49,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2018,6,1]],"date-time":"2018-06-01T00:00:00Z","timestamp":1527811200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Remote Sensing"],"abstract":"<jats:p>Here, we demonstrate how a combination of three multivariate statistic techniques can identify key environmental factors affecting the seasonal and spatial variability of chlorophyll-a (Chl-a) in a productive tropical estuarine-lagoon system. Remote estimation of Chl-a was carried out using a NIR-Red model based on MODIS bands, which is highly consistent with the in situ measurement of Chl-a with root mean square error (RMSE) of 15.24 mg m\u22123 and 13.43 mg m\u22123 for two independent datasets used for the model\u2019s calibration and validation, respectively. Our findings suggest that the river discharges and hydraulic residence time of the lagoons promote a stronger effect on the spatial variability of Chl-a in the coastal lagoons, while wind, solar radiation and temperature have a secondary importance. The results also indicate a slight seasonal variability of Chl-a in Munda\u00fa lagoon, which are different the from Manguaba lagoon. The multivariate approach was able to fully understand the relative importance of key environmental factors on the spatiotemporal variability of Chl-a of the aquatic ecosystem, providing a powerful tool for reducing dimensionality and analyzing large amounts of satellite-derived Chl-a data.<\/jats:p>","DOI":"10.3390\/rs10060853","type":"journal-article","created":{"date-parts":[[2018,6,1]],"date-time":"2018-06-01T03:02:50Z","timestamp":1527822170000},"page":"853","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["A Multivariate Analysis Framework to Detect Key Environmental Factors Affecting Spatiotemporal Variability of Chlorophyll-a in a Tropical Productive Estuarine-Lagoon System"],"prefix":"10.3390","volume":"10","author":[{"given":"Regina Camara","family":"Lins","sequence":"first","affiliation":[{"name":"Department of Civil Engineering, Federal University of Pernambuco, 50670-901 Recife, Brazil"}]},{"given":"Jean-Michel","family":"Martinez","sequence":"additional","affiliation":[{"name":"G\u00e9osciences Environnement Toulouse (GET), Unit\u00e9 Mixte de Recherche 5563, IRD\/CNRS\/Universit\u00e9 Toulouse III, 31400 Toulouse, France"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3809-8053","authenticated-orcid":false,"given":"David da","family":"Motta Marques","sequence":"additional","affiliation":[{"name":"Hydraulic Research Institute, Federal University of Rio Grande do Sul, CP 15029 Porto Alegre, Brazil"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8672-0898","authenticated-orcid":false,"given":"Jos\u00e9 Almir","family":"Cirilo","sequence":"additional","affiliation":[{"name":"Department of Civil Engineering, Federal University of Pernambuco, 50670-901 Recife, Brazil"}]},{"given":"Paulo Ricardo Petter","family":"Medeiros","sequence":"additional","affiliation":[{"name":"Institute of Geography, Federal University of Alagoas, 57072-970 Macei\u00f3, Brazil"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5853-6030","authenticated-orcid":false,"given":"Carlos Ruberto","family":"Fragoso J\u00fanior","sequence":"additional","affiliation":[{"name":"Center for Technology, Federal University of Alagoas, 57072-970 Macei\u00f3, Brazil"}]}],"member":"1968","published-online":{"date-parts":[[2018,6,1]]},"reference":[{"key":"ref_1","unstructured":"Tundisi, J.G., and Tundisi, T.M. (2008). Limnologia, Oficina de Textos. [1th ed.]."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ecss.2014.12.027","article-title":"Changes to processes in estuaries and coastal waters due to intense multiple pressures\u2014An introduction and synthesis","volume":"156","author":"Mitchell","year":"2015","journal-title":"Estuar. Coast. Shelf Sci."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Hardisty, J. (2007). Introduction to estuarine systems. Estuaries: Monitoring and Modeling the Physical System, Blackwell Publishing.","DOI":"10.1002\/9780470750889"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"616","DOI":"10.1007\/s10452-004-3428-0","article-title":"Book review: Nutrients and eutrophication in estuaries and coastal waters","volume":"38","author":"Cadee","year":"2004","journal-title":"Aquat. Ecol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"S56","DOI":"10.1016\/j.ecolind.2008.11.013","article-title":"Phytoplankton bloom status: Chlorophyll a biomass as an indicator of water quality condition in the southern estuaries of florida, USA","volume":"9","author":"Boyer","year":"2009","journal-title":"Ecol. Indic."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"306","DOI":"10.1016\/j.ecss.2007.04.021","article-title":"Evaluation of the utility of water quality based indicators of estuarine lagoon condition in nsw, australia","volume":"74","author":"Scanes","year":"2007","journal-title":"Estuar. Coast. Shelf Sci."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Paerl, H.W., Valdes-Weaver, L.M., Joyner, A.R., and Winkelmann, V. (2007). Phytoplankton indicators of ecological change in the eutrophying pamlico sound system, north carolina. Ecol. Appl., 17.","DOI":"10.1890\/05-0840.1"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1126\/science.281.5374.200","article-title":"Biogeochemical controls and feedbacks on ocean primary production","volume":"281","author":"Falkowski","year":"1998","journal-title":"Science"},{"key":"ref_9","first-page":"1747","article-title":"Remote sensing applications: An overview","volume":"93","author":"Navalgund","year":"2007","journal-title":"Curr. Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.jglr.2013.04.001","article-title":"Retrospection and introspection on remote sensing of inland water quality: Like d\u00e9j\u00e0 vu all over again","volume":"39","author":"Bukata","year":"2013","journal-title":"J. Great Lakes Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1016\/j.rse.2011.11.013","article-title":"Review of constituent retrieval in optically deep and complex waters from satellite imagery","volume":"118","author":"Odermatt","year":"2012","journal-title":"Remote Sens. Environ."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1307","DOI":"10.1016\/j.scitotenv.2016.01.020","article-title":"Developments in earth observation for the assessment and monitoring of inland, transitional, coastal and shelf-sea waters","volume":"572","author":"Tyler","year":"2016","journal-title":"Sci. Total Environ."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.rse.2005.12.002","article-title":"Estimating chlorophyll a concentrations from remote-sensing reflectance in optically shallow waters","volume":"101","author":"Cannizzaro","year":"2006","journal-title":"Remote Sens. Environ."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1016\/j.pocean.2012.10.002","article-title":"Towards a long-term chlorophyll-a data record in a turbid estuary using modis observations","volume":"109","author":"Le","year":"2013","journal-title":"Prog. Oceanogr."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1016\/j.rse.2005.02.007","article-title":"Assessing the potential of seawifs and modis for estimating chlorophyll concentration in turbid productive waters using red and near-infrared bands","volume":"96","author":"Gitelson","year":"2005","journal-title":"Remote Sens. Environ."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"755","DOI":"10.1016\/j.pce.2009.07.015","article-title":"Estimating chlorophyll concentration in lake malawi from modis satellite imagery","volume":"34","author":"Chavula","year":"2009","journal-title":"Phys. Chem. Earth Parts A\/B\/C"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1016\/j.scitotenv.2015.05.115","article-title":"Evaluation of chlorophyll-a retrieval algorithms based on meris bands for optically varying eutrophic inland lakes","volume":"530\u2013531","author":"Lyu","year":"2015","journal-title":"Sci. Total Environ."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1016\/j.rse.2014.07.024","article-title":"Validation of envisat meris algorithms for chlorophyll retrieval in a large, turbid and optically-complex shallow lake","volume":"157","author":"Palmer","year":"2015","journal-title":"Remote Sens. Environ."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.rse.2012.11.001","article-title":"Evaluation of chlorophyll-a remote sensing algorithms for an optically complex estuary","volume":"129","author":"Le","year":"2013","journal-title":"Remote Sens. Environ."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"464","DOI":"10.1016\/j.rse.2007.01.016","article-title":"Remote chlorophyll-a retrieval in turbid, productive estuaries: Chesapeake bay case study","volume":"109","author":"Gitelson","year":"2007","journal-title":"Remote Sens. Environ."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1016\/j.csr.2016.02.015","article-title":"Factors governing phytoplankton biomass and production in tropical estuaries of western taiwan","volume":"118","author":"Pan","year":"2016","journal-title":"Cont. Shelf Res."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1006\/ecss.2000.0590","article-title":"Spatial and temporal dynamics of phytoplankton communities in a freshwater tidal estuary (schelde, belgium)","volume":"50","author":"Muylaert","year":"2000","journal-title":"Estuar. Coast. Shelf Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.ecss.2015.01.007","article-title":"Factors affecting the accumulation of phytoplankton biomass in irish estuaries and nearshore coastal waters: A conceptual model","volume":"155","author":"Wilkes","year":"2015","journal-title":"Estuar. Coast. Shelf Sci."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"2317","DOI":"10.1016\/j.marpolbul.2011.08.044","article-title":"Phytoplankton distribution and productivity in a highly turbid, tropical coastal system (bach dang estuary, vietnam)","volume":"62","author":"Chu","year":"2011","journal-title":"Mar. Pollut. Bull."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1016\/j.ecss.2015.03.007","article-title":"Long-term changes of the phytoplankton community and biomass in the subtropical shallow patos lagoon estuary, brazil","volume":"162","author":"Haraguchi","year":"2015","journal-title":"Estuar. Coast. Shelf Sci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/j.ecolind.2009.11.001","article-title":"A review of methods for analysing spatial and temporal patterns in coastal water quality","volume":"11","author":"Bierman","year":"2011","journal-title":"Ecol. Indic."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/j.proeng.2012.04.195","article-title":"Feature of phytoplankton community and canonical correlation analysis with environmental factors in xiaoqing river estuary in autumn","volume":"37","author":"Yan","year":"2012","journal-title":"Procedia Eng."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1006\/ecss.1993.1074","article-title":"Regular article: Environmental responses of a tropical coastal lagoon system to hydrological variability: Munda\u00fa-manguaba, brazil","volume":"37","author":"Oliveira","year":"1993","journal-title":"Estuar. Coast. Shelf Sci."},{"key":"ref_29","unstructured":"Guimar\u00e3es J\u00fanior, S.A.M., Nascimento, M.C., Andrade, E.L., Silva, D.J.R.P., and Diniz, F.A.B. (May, January 30). Impactos do uso da terra no complexo estuarino-lagunar munda\u00fa-manguaba\u2014Celmm, alagoas, brasil. Proceedings of the Simp\u00f3sio Brasileiro de Sensoriamento Remoto, Curitiba, Brazil."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1590\/S1519-69842009000200006","article-title":"Determination of eutrophic areas in munda\u00fa\/manguaba lagoons, alagoas-brazil, through studies of the phytoplanktonic community","volume":"69","author":"Medeiros","year":"2009","journal-title":"Braz. J. Biol."},{"key":"ref_31","unstructured":"American Public Health Association, Eaton, A.D., American Water Works Association, and Water Environment Federation (2005). Standard Methods for the Examination of Water and Wastewater, APHA-AWWA-WEF."},{"key":"ref_32","unstructured":"Vermote, E.F., and Vermeulen, A. (1999). Atmospheric Correction Algorithm: Spectral Reflectances (MOD09), University of Maryland. Algorithm Technical Background Document (ATBD)."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/S0304-3800(02)00033-9","article-title":"Prediction of missing values and detection of \u2018exceptional events\u2019 in a chronological planktonic series: A single algorithm","volume":"154","author":"Ibanez","year":"2002","journal-title":"Ecol. Model."},{"key":"ref_34","unstructured":"Jackson, J.E. (2004). Getting started. A User\u2019s Guide to Principal Components, John Wiley & Sons, Inc."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1002\/joc.3370060305","article-title":"Rotation of principal components","volume":"6","author":"Richman","year":"1986","journal-title":"J. Climatol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"3515","DOI":"10.1029\/98WR02854","article-title":"Seasonal runoff forecast for northern south america: A statistical model","volume":"34","author":"Uvo","year":"1998","journal-title":"Water Resour. Res."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"3546","DOI":"10.1002\/joc.3926","article-title":"Cluster analysis applied to the spatial and temporal variability of monthly rainfall in alagoas state, northeast of brazil","volume":"34","author":"Lyra","year":"2014","journal-title":"Int. J. Climatol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1167","DOI":"10.2307\/1938672","article-title":"Canonical Correspondence Analysis: A New Eigenvector Technique for Multivariate Direct Gradient Analysis","volume":"67","year":"1986","journal-title":"Ecology"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"664","DOI":"10.1590\/1519-6984.23814","article-title":"Water residence time affecting phytoplankton blooms: Study case in ibitinga reservoir (s\u00e3o paulo, brazil) using landsat\/tm images","volume":"76","author":"Londe","year":"2016","journal-title":"Braz. J. Biol."},{"key":"ref_40","unstructured":"Souza, A.P. (2017). Avalia\u00e7\u00e3o do Efeito do Assoreamento na Hidrodin\u00e2mica e no Tempo de Resid\u00eancia de um Complexo Estuarino Lagunar Tropical. [Ph.D. Thesis, Federal University of Alagoas]."},{"key":"ref_41","first-page":"133","article-title":"Tidal exchange in a choked coastal lagoon: A study of munda\u00fa lagoon in northeastern brazil","volume":"17","author":"Fragoso","year":"2018","journal-title":"Reg. Stud. Mar. Sci."},{"key":"ref_42","unstructured":"Lins, R.C., Fragoso, C.R., and Cirilo, J.A. (2013). Simula\u00e7\u00f5es da hidrodin\u00e2mica no complexo estuarino lagunar munda\u00fa-manguaba\u2014Celmm\/al. XX Simp\u00f3sio Brasileiro de Recursos H\u00eddricos, ABRH."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s10498-010-9104-1","article-title":"Sources and distribution of parcitulate organic matter of a tropical estuarine-lagoon system from ne brazil as indicated by lipid biomarkers","volume":"17","author":"Costa","year":"2011","journal-title":"Aquat. Geochem."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1016\/j.ecss.2016.05.024","article-title":"The relative influence of local and regional environmental drivers of algal biomass (chlorophyll-a) varies by estuarine location","volume":"178","author":"Wainger","year":"2016","journal-title":"Estuar. Coast. Shelf Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1016\/j.microc.2010.03.001","article-title":"Polycyclic aromatic and aliphatic hydrocarbons in mytella charruana, a bivalve mollusk from munda\u00fa lagoon, brazil","volume":"96","author":"Maioli","year":"2010","journal-title":"Microchem. J."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Descy, J.-P., Reynolds, C.S., and Padis\u00e1k, J. (1994). The long, the short and the stalled: On the attributes of phytoplankton selected by physical mixing in lakes and rivers. Phytoplankton in Turbid Environments: Rivers and Shallow Lakes, Proceedings of the 9th Workshop of the International Association of Phytoplankton Taxonomy and Ecology (IAP), Mont Rigi, Belgium, 10\u201318 July 1993, Springer.","DOI":"10.1007\/978-94-017-2670-2_2"},{"key":"ref_47","unstructured":"Pereira-Barros, J.B. (1972). Fisiecologia do Sururu do Nordeste do Brasil\u2014Mytella Falcata (D\u2019orbigny, 1846)\u2014da Lagoa Munda\u00fa, Macei\u00f3, Alagoas: Resist\u00eancia e Crescimento sob Varia\u00e7\u00f5es da Salinidade no Ambiente Natural. [Ph.D. Thesis, Universidade Federal de S\u00e3o Paulo]."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"3297","DOI":"10.1007\/s10661-012-2791-x","article-title":"Assessment of the trophic status of four coastal lagoons and one estuarine delta, eastern brazil","volume":"185","author":"Brandini","year":"2013","journal-title":"Environ. Monit. Assess."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1574","DOI":"10.1128\/AEM.06908-11","article-title":"Characteristics of the freshwater cyanobacterium microcystis aeruginosa grown in iron-limited continuous culture","volume":"78","author":"Dang","year":"2012","journal-title":"Appl. Environ. Microbiol."}],"container-title":["Remote Sensing"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-4292\/10\/6\/853\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T15:06:44Z","timestamp":1760195204000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-4292\/10\/6\/853"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,6,1]]},"references-count":49,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2018,6]]}},"alternative-id":["rs10060853"],"URL":"https:\/\/doi.org\/10.3390\/rs10060853","relation":{},"ISSN":["2072-4292"],"issn-type":[{"value":"2072-4292","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,6,1]]}}}