Abstract
We investigate the carbon dynamics in Guanabara Bay, an eutrophic tropical coastal embayment surrounded by the megacity of Rio de Janeiro (southeast coast of Brazil). Nine sampling campaigns were conducted for dissolved, particulate and total organic carbon (DOC, POC and TOC), dissolved inorganic carbon (DIC), partial pressure of CO2 (pCO2), chlorophyll a (Chl a), pheo-pigments and ancillary parameters. Highest DOC, POC and Chl a concentrations were found in confined-shallow regions of the bay during the summer period with strong pCO2 undersaturation, and DOC reached 82 mg L−1, POC 152 mg L−1, and Chl a 800 μg L−1. Spatially and temporally, POC and DOC concentrations varied positively with total pigments, and negatively with DIC. Strong linear correlations between these parameters indicate that the production of TOC translates to an equivalent uptake in DIC, with 85% of the POC and about 50% of the DOC being of phytoplanktonic origin. Despite the shallow depths of the bay, surface waters were enriched in POC and DOC relative to bottom waters in periods of high thermohaline stratification. The seasonal accumulation of phytoplankton-derived TOC in the surface waters reached about 105 g C m−2 year−1, representing between 8 and 40% of the net primary production. The calculated turnover time of organic carbon was 117 and 34 days during winter and summer, respectively. Our results indicate that eutrophication of coastal bays in the tropics can generate large stocks of planktonic biomass and detrital organic carbon which are permanently being produced and partially degraded and buried in sediments.
References
Abril G, Nogueira E, Etcheber H, Cabeçadas G, Lemaire E, Brogueira M (2002) Behaviour of organic carbon in nine contrasting European estuaries. Estuar Coast Shelf Sci 54:241–262. https://doi.org/10.1006/ecss.2001.0844
Aminot A, El-Sayed MA, Kerouel R (1990) Fate of natural and anthropogenic dissolved organic carbon in the macrotidal Elorn estuary (France). Mar Chem 29:255–275. https://doi.org/10.1016/0304-4203(90)90017-7
Augusti S, Duarte CM (2013) Phytoplankton lysis predicts dissolved organic carbon release in marine plankton communities. Biogeosciences 10:1259–1264. https://doi.org/10.5194/bg-10-1259-2013
Baines SB, Pace ML (1991) The production of dissolved organic matter by phytoplankton and its importance to bacteria: patterns across marine and freshwater systems. Limnol Oceanogr 36:1078–1090
Crossland J, Baird, D, Ducrotoy J-P (2005) The coastal zone—a domain of global interactions. In: Crossland CJ, Kremer HH, Lindeboom HJ, Marshal Crossland JI, Le Tissier MDALE (eds) Coastal fluxes in the Anthropocene, The IGBP Series. Springer, Berlim, pp 1–34
Banse K (1977) Determining the carbon-to-chlorophyll ratio of natural phytoplankton. Mar Biol 41:199–212
Bauer JE, Bianchi TS (2011) Dissolved organic carbon cycling and transformation. In: McLusky DS, Wolanski E (eds) Treatise on estuarine and coastal science, vol 5, 1st edn. Academic Press, Amsterdam, pp 7–67
Bauer JE, Cai WJ, Raymond P, Bianchi TS, Hopkinson CS (2013) Regnier PG (2013) The changing carbon cycle of the coastal ocean. Nature 504:61–70. https://doi.org/10.1038/nature12857
Berto D, Rampazzo F, Noventa S et al (2013) Stable carbon and nitrogen isotope ratios as tools to evaluate the nature of particulate organic matter in the Venice lagoon. Estuar Coast Shelf Sci 135:66–76. https://doi.org/10.1016/j.ecss.2013.06.021
Bianchi TS, Bauer JE (2011) Particulate organic carbon cycling and transformation. In: McLusky DS, Wolanski E (eds) Treatise on estuarine and coastal science, vol 5, 1st edn. Academic Press, Amsterdam, pp 69–117
Bidone ED, Lacerda LD (2004) The use of DPSIR framework to evaluate sustainability in coastal areas. Case study: Guanabara Bay basin, Rio de Janeiro, Brazil. Reg Environ Change 4:5–16. https://doi.org/10.1007/s10113-003-0059-2
Borges AV, Abril G (2011) Carbon dioxide and methane dynamics in estuaries. In: McLusky DS, Wolanski E (eds) Treatise on estuarine and coastal science, vol 5, 1st edn. Academic Press, Amsterdam, pp 119–161
Brockmann UH (1994) Organic matter in the Elbe estuary. Netherlands J Aquat Ecol 28:371–381. https://doi.org/10.1007/BF02334207
Cadée GC (1982) Tidal and seasonal variation in particulate and dissolved organic carbon in the western dutch Wadden Sea and Marsdiep tidal inlet. Netherlands J Sea Res 15:228–249. https://doi.org/10.1016/0077-7579(82)90006-0
Cadée GC (1984) Particulate and dissolved organic carbon and chlorophyll A in the Zaire river, estuary and plume. Netherlands J Sea Res 17:426–440. https://doi.org/10.1016/0077-7579(84)90059-0
Cai W-J (2011) Estuarine and coastal ocean carbon paradox: CO2 sinks or sites of terrestrial carbon incineration? Annu Rev Mar Sci 3:123–145. https://doi.org/10.1146/annurev-marine-120709-142723
Carreira RS, Wagener ALR, Readman JW et al (2002) Changes in the sedimentary organic carbon pool of a fertilized tropical estuary, Guanabara Bay, Brazil: an elemental, isotopic and molecular marker approach. Mar Chem 79:207–227. https://doi.org/10.1016/S0304-4203(02)00065-8
Cloern JE, Grenz C, Vidergar-Lucas L (1995) An empirical model of the phytoplankton chlorophyll:carbon ratio—the conversion factor between productivity and growth rate. Limnol Oceanogr 40:1313–1321
Cordeiro RC, Santelli RE, Machado W et al (2017) Biogeochemical factors controlling arsenic distribution in a densely populated tropical estuary (Guanabara Bay, RJ, Brazil). Environ Earth Sci 76:561. https://doi.org/10.1007/s12665-017-6888-y
Costa Santos SJ (2015) Determinação do estado trófico a partir da aplicação dos índices O’Boyle e TRIX nos compartimentos da Baia de Guanabara. Dissertation, Universidade Federal Fluminense
Cotovicz LC Jr, Knoppers BA, Brandini N, Costa Santos SJ, Abril G (2015) A strong CO2 sink enhanced by eutrophication in a tropical coastal embayment (Guanabara Bay, Rio de Janeiro, Brazil). Biogeosciences 12:6125–6146. https://doi.org/10.5194/bg-12-6125-2015
Cotovicz LC Jr, Knoppers BA, Brandini N, Poirier D, Costa Santos SJ, Abril G (2016) Spatio-temporal variability of methane (CH4) concentrations and diffusive fluxes from a tropical coastal embayment surrounded by a large urban area (Guanabara Bay, Rio de Janeiro, Brazil). Limnol Oceanogr 61:238–252. https://doi.org/10.1002/lno.10298
Dittmar T, Hertkorn N, Kattner G, Lara RJ (2006) Mangroves, a major source of dissolved organic carbon to the oceans. Glob Biogeochem Cycles 20:1–7. https://doi.org/10.1029/2005GB002570
Dougherty RC, Strain HH, Svec WA (1970) The structure, properties, and distribution of Chlorophyll c. J Am Chem Soc 92(9):2826–2833. https://doi.org/10.1021/ja00712a037
Dürr HH, Laruelle GG, Van Kempen CM et al (2011) Worldwide typology of nearshore coastal systems: defining the estuarine filter of river inputs to the oceans. Estuaries Coasts 34:441–458. https://doi.org/10.1007/s12237-011-9381-y
Etcheber H, Taillez A, Abril G et al (2007) Particulate organic carbon in the estuarine turbidity maxima of the Gironde, Loire and Seine estuaries: origin and lability. Hydrobiologia 588:245–259. https://doi.org/10.1007/s10750-007-0667-9
Fisher TR, Hagy JD, Rochelle-Newall E (1998) Dissolved and particulate organic carbon in chesapeake bay. Estuaries 21(2):215–229
Fujii M, Murashige S, Ohnishi Y et al (2002) Decomposition phytoplankton in seawater. Part I: kinetic analysis of the effect of organic matter concentration. J Oceanogr 58:433–438
Gattuso JP, Frankignoulle M, Wollast R (1998) Carbon and carbonate metabolism in coastal aquatic ecosystems. Annu Rev Ecol Syst 29:405–434
Gazeau F, Borges A, Barrón C et al (2005) Net ecosystem metabolism in a micro-tidal estuary (Randers Fjord, Denmark): evaluation of methods. Mar Ecol Prog Ser 301:23–41. https://doi.org/10.3354/meps301023
Godoy JM, Oliveira AV, Almeida AC et al (2012) Guanabara Bay sedimentation rates based on 210Pb dating: reviewing the existing data and adding new data. J Braz Chem Soc 23:1265–1273
Gypens N, Borges AV, Lancelot C (2009) Effect of eutrophication on air-sea CO2 fluxes in the coastal Southern North Sea: a model study of the past 50 years. Glob Chang Biol 15:1040–1056. https://doi.org/10.1111/j.1365-2486.2008.01773.x
Howarth R, Chan F, Conley DJ et al (2011) Coupled biogeochemical cycles: eutrophication and hypoxia in temperate estuaries and coastal marine ecosystems. Front Ecol Environ 9:18–26. https://doi.org/10.1890/100008
Kalas F, Carreira RS, Macko SA, Wagener AL (2009) Molecular and isotopic characterization of the particulate organic matter from an eutrophic coastal bay in SE Brazil. Cont Shelf Res 29:2293–2302. https://doi.org/10.1016/j.csr.2009.09.007
Kjerfve B, Ribeiro CA, Dias GTM, Filippo A, Quaresma VS (1997) Oceanographic characteristics of an impacted coastal bay: Baia de Guanabara, Rio de Janeiro, Brazil. Cont Shelf Res 17:1609–1643
Knoppers BA, Opitz SS, De Souza MP, Miguez CF (1984) The spatial distribution of particulate organic matter and some physical and chemical water properties in Conceição Lagoon; Santa Catarina, Brazil. Arq Biol Tecnol 27:59–78
Knoppers BA, Ekau W, Figueiredo AG (1999) The coast and shelf of east and northeast Brazil and material transport. Geo-Mar Lett 19(3):171–178
Kubo A, Maeda Y, Kanda J (2017) A significant net sink for CO2 in Tokyo Bay. Sci Rep 7:44355. https://doi.org/10.1038/srep44355
Laane RWPM (1980) Conservative behaviour of dissolved organic carbon in the Ems-Dollart estuary and the western Wadden Sea. Netherlands J Sea Res 14:192–199
Liénart C, Savoye N, Bozec Y et al (2017) Dynamics of particulate organic matter composition in coastal systems: a spatio- temporal study at multi-systems scale. Prog Oceanogr. https://doi.org/10.1016/j.pocean.2017.03.001
Lorenzen CJ (1967) Determination of chlorophyll and pheo-pigments: spectrophotometric equations. Limnol Oceanogr 12(2):343–346
Maher DT, Eyre BD (2012) Carbon budgets for three autotrophic Australian estuaries: implications for global estimates of the coastal air-water CO2 flux. Glob Biogeochem Cycles. https://doi.org/10.1029/2011GB004075
Maksymowska D, Richard P, Piekarek-Jankowska H, Riera P (2000) Chemical and isotopic composition of the organic matter sources in the gulf of Gdansk (Southern Baltic Sea). Estuar Coast Shelf Sci 51:585–598. https://doi.org/10.1006/ecss.2000.0701
Mantoura RFC, Woodward EMS (1983) Conservative behaviour of riverine dissolved organic carbon in the Severn Estuary: chemical and geochemical implications. Geochim Cosmochim Acta 47:1293–1309
Martins JMA, Silva TSM, Fernandes AM, Massone C, Carreira RS (2016) Characterization of particulate organic matter in a Guanabara Bay-coastal ocean transect using elemental, isotopic and molecular markers. Panamjas 11:276–291
Medeiros PM, Seidel M, Niggemann J et al (2016) A novel molecular approach for tracing terrigenous dissolved organic matter into the deep ocean. Glob Biogeochem Cycles 30:689–699. https://doi.org/10.1002/2015GB005320
Meybeck M (1993) Riverine transport of atmospheric carbon: sources, global typology and budget. Water Air Soil Pollut 70:443–463. https://doi.org/10.1007/BF01105015
Meybeck M, Vörösmarty C (1999) Global transfer of carbon by rivers. Glob Chang Newsl IGBP Newslett 37:18–19
Moore CM, Mills MM, Arrigo KR et al (2013) Processes and patterns of oceanic nutrient limitation. Nat Geosci 6:701–710. https://doi.org/10.1038/ngeo1765
Myklestad SM (2000) Dissolved organic carbon from phytoplankton. Mar Chem 5:112–144. https://doi.org/10.1016/j.marchem.2009.01.001
Nixon SW (1995) Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia. 41:199–219
O’Boyle S, McDermott G, Noklegaard T, Wilkes R (2013) A simple index of trophic status in estuaries and coastal bays based on measurements of pH and dissolved oxygen. Estuaries Coasts 36:158–173. https://doi.org/10.1007/s12237-012-9553-4
Paranhos R, Pereira AP, Mayr LM (1998) Diel variability of water quality in a tropical polluted bay. Environ Monit Assess 50:131–141
Raymond PA, Hopkinson CS (2003) Ecosystem modulation of dissolved carbon age in a temperate marsh-dominated estuary. Ecosystems 6:694–705. https://doi.org/10.1007/s10021-002-0213-6
Rebello AL, Ponciano CR, Melges LH (1988) Avaliação da produtividade primaria e da disponibilidade de nutrientes na Baia de Guanabara. An Acad Bras Cienc 60:419–430
Ribeiro CHA, Kjerfve B (2002) Anthropogenic influence on the water quality in Guanabara Bay, Rio de Janeiro, Brazil. Reg Environ Change 3:13–19. https://doi.org/10.1007/s10113-001-0037-5
Sarmiento JL, Gruber N (2006) Ocean biogeochemical dynamics. Princeton University Press, Princeton, p 503
Sathyendranath S, Stuart V, Nair A et al (2009) Carbon-to-chlorophyll ratio and growth rate of phytoplankton in the sea. Mar Ecol Prog Ser 383:73–84. https://doi.org/10.3354/meps07998
Valentin JL, Tenenbaum DR, Bonecker ACT et al (1999) O sistema planctônico da Baía de Gaunabara: Síntese do conheciemnto. In: Silva SHG, Lavrado HP (eds) Ecologia dos Ambientes Costeiros do Estado do Rio de Janeiro. Série Oecologia Brasiliensis, Rio de Janeiro, pp 35–59
Vollenweider RA, Giovanardi F, Montanari G, Rinaldi A (1998) Characterization of the trophic conditions of marine coastal waters with special reference to the NW Adriatic Sea: proposal for a trophic scale, turbidity and generalized water quality index. Environmetrics 9:329–357
Wafart M, Le Corre P, Birrien JL (1984) Seasonal changes of dissolved organic matter (C, N, P) in permanently well mixed temperate Waters. Limnol Oceanogr 29(5):1127–1132
Watanabe K, Kuwae T (2015) How organic carbon derived from multiple sources contributes to carbon sequestration processes in a shallow coastal system? Glob Change Biol 21:2612–2623. https://doi.org/10.1111/gcb.12924
Acknowledgments
This study was supported by the sciences without border program of the Brazilian National Council of Research and Development (CNPq-Pve No 401.726/2012-6) and by the Carlos Chagas Foundation for Research Support of the State of Rio de Janeiro (FAPERJ; proc. no. E-26202.785/2016). Luiz C. Cotovicz Jr. is a postdoctoral researcher of the Carlos Chagas Foundation for Research Support of the State of Rio de Janeiro (FAPERJ; proc. no. E-26202.785/2016); B.A. Knoppers is a senior scientist of CNPq (proc. no. 301572/2010-0). We would like to thank also the FAPERJ Project Nr. E-26/111.190/2011 that contributed with the logistical support. The raw data of this study are available as online resource 4.
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Cotovicz, L.C., Knoppers, B.A., Brandini, N. et al. Predominance of phytoplankton-derived dissolved and particulate organic carbon in a highly eutrophic tropical coastal embayment (Guanabara Bay, Rio de Janeiro, Brazil). Biogeochemistry 137, 1–14 (2018). https://doi.org/10.1007/s10533-017-0405-y
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DOI: https://doi.org/10.1007/s10533-017-0405-y