Abstract
Estuaries are complex systems where environmental fluctuations occur over distinct timescales due to local meteorological and large-scale climatic factors. Consequently, studies with low temporal resolution and taxonomic coverage may fail to detect isotopic variations in basal sources, providing biased interpretations of isotope mixing models. We investigated the seasonal and El Niño Southern Oscillation (ENSO)-driven interannual variations in δ13C, δ15N and C:N values among distinct basal sources and their implications for mixing models interpretation in a subtropical estuary. δ13C variations among sources differed in their magnitude and timescales, being large enough to confound source-specific values. Macroalgae and POM δ13C varied seasonally, whereas ENSO effects prevailed for C3 and C4 salt marsh plants, highlighting the contrasting influence of local versus remote environmental drivers on short- and long-lived primary producers, respectively. Peaks of δ15N were detected for all sources during short-term anthropogenic nutrient inputs. Isotope mixing model comparisons showed that overlooking isotopic variations in basal sources under distinct ENSO conditions can cause misinterpretation of local trophic interactions and nutrient cycling. The present study contributes to design appropriate sampling delineations in highly variable aquatic environments, emphasizing the importance of comprehensive, long-term monitoring of estuarine primary producers to encompass environmental drivers of stable isotopic variations.
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Data availability
The dataset analyzed during the current study is available at the Global Biodiversity Information Facility (https://www.gbif.org/dataset/35014baf-5683-4267-b19d-8953f1fd3383) through the Brazilian Biodiversity Information Facility Repository (SiBBr).
References
Abreu, P. C., C. Costa, C. Bemvenuti, C. Odebrecht, W. Granéli & A. Anesio, 2006. Eutrophication processes and trophic interactions in a shallow estuary: preliminary results based on stable isotope analysis (δ13C and δ15N). Estuaries and Coasts 29: 277–285.
Abreu, P. C., M. Bergesch, L. A. Proença, C. A. E. Garcia & C. Odebrecht, 2010. Short- and long-term chlorophyll a variability in the shallow microtidal Patos Lagoon Estuary, Southern Brazil. Estuaries and Coasts 33: 554–569.
Anderson, M. J., 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32–46.
Antonio, E. S., A. Kasai, M. Ueno, Y. Ishihi, H. Yokoyama & Y. Yamashita, 2012. Spatial-temporal feeding dynamics of benthic communities in an estuary- marine gradient. Estuarine, Coastal and Shelf Science 112: 86–97.
Baeta, A., R. Pinto, I. Valiela, P. Richard, N. Niquil & J. C. Marques, 2009. δ15N and δ13C in the Mondego estuary food web: seasonal variation in producers and consumers. Marine Environmental Research 67: 109–116.
Bastos, R. F., F. Corrêa, K. O. Winemiller & A. M. Garcia, 2017. Are you what you eat? Effects of trophic discrimination factors on estimates of food assimilation and trophic position with a new estimation method. Ecological indicators 75: 234–241.
Baumgarten, M. G. & L. F. H. Niencheski, 2010. A coluna sedimentar como reservatório e fonte de nutrientes em enseadas estuarinas. Tropical Oceanography 38: 88–105.
Bergamino, L. & N. B. Richoux, 2015. Spatial and temporal changes in estuarine food web structure: differential contributions of marsh grass detritus. Estuaries and Coasts 38: 367–382.
Bergamino, L., T. Dalu & N. B. Richoux, 2014. Evidence of spatial and temporal changes in sources of organic matter in estuarine sediments: stable isotope and fatty acid analyses. Hydrobiologia 732: 133–145.
Bergamino, L., M. Schuerch, A. Tudurí, S. Carretero & F. García-Rodríguez, 2017. Linking patterns of freshwater discharge and sources of organic matter within the Río de la Plata estuary and adjacent marshes. Marine and Freshwater Research 68: 1704–1715.
Bergesch, M., C. Odebrecht & P. Abreu, 1995. Microalgas do estuário da Lagoa Dos Patos: interação entre o sedimento e a coluna d’água. Oecologia Brasiliensis 1: 273–289.
Brazilian National Water Agency. http://hidroweb.ana.gov.br. Accessed 15 Jan 2019.
Childers, D. L., J. W. Day & R. A. Muller, 1990. Relating climatological forcing to coastal water levels in Louisiana estuaries and the potential importance of El Nino-Southern Oscillation events. Climate Research 1: 31–42.
Cifuentes, L. A., J. H. Sharp & M. L. Fogel, 1988. Stable carbon and nitrogen isotope biogeochemistry Delaware estuary. Limnology and Oceanography 33: 1101–1115.
Claudino, M. C., P. C. Abreu & A. M. Garcia, 2013. Stable isotopes reveal temporal and between-habitat changes in trophic pathways in a southwestern Atlantic estuary. Marine Ecology Progress Series 489: 29–42.
Cloern, J. E., E. A. Canuel & D. Harris, 2002. Stable carbon and nitrogen isotope composition of aquatic and terrestrial plants of the San Francisco Bay estuarine system. Limnology and Oceanography 47: 713–729.
Copertino, M. S. & U. Seeliger, 2010. Habitats de Ruppia maritima e de macroalgas. In Seeliger, U. & C. Odebrecht (eds), Estuário da Lagoa dos Patos: um século de transformações. Editora da FURG, 92–98.
Costa, C. S. B., 1998. Production ecology of Scirpus maritimus in southern Brazil. Journal of the Brazilian Association for the Advancement of Science 50: 273–280.
Costa, C. S. B. & J. C. Marangoni, 2010. As comunidades das marismas. In Seeliger, U. & C. Odebrecht (eds), Estuário da Lagoa dos Patos: um século de transformações. Editora da FURG, 125–133.
Costa, C. S. B., J. C. Marangoni & A. M. G. Azevedo, 2003. Plant zonation in irregularly flooded salt marshes: relative importance of stress tolerance and biological interactions. Journal of Ecology 91: 951–965.
Costanzo, S. D., M. J. O. Õ. Donohue, W. C. Dennison, N. R. Loneragan & M. Thomas, 2001. A new approach for detecting and mapping sewage impacts. Marine Pollution Bulletin 42: 149–156.
Couto, T., B. Duarte, I. Caçador, A. Baeta & J. C. Marques, 2013. Salt marsh plants carbon storage in a temperate Atlantic estuary illustrated by a stable isotopic analysis based approach. Ecological Indicators 32: 305–311.
Dethier, M. N., E. Sosik, A. W. E. Galloway, D. O. Duggins & C. A. Simenstad, 2013. Addressing assumptions: variation in stable isotopes and fatty acids of marine macrophytes can confound conclusions of food web studies. Marine Ecology Progress Series 478: 1–14.
deVries, M. S., C. M. del Rio, T. S. Tunstall & T. E. Dawson, 2015. Isotopic incorporation rates and discrimination factors in mantis shrimp crustaceans. PLoS ONE 10(4): e0122334.
Durako, M. J. & M. O. Hall, 1992. Effects of light on the stable carbon isotope composition of the seagrass Thalassia testudinum. Marine Ecology Progress Series 86: 1991–1993.
Fantle, M. S., A. I. Dittel, S. M. Schwalm, C. E. Epifanio & M. L. Fogel, 1999. A food web analysis of the juvenile blue crab Callinectes sapidus, using stable isotopes in whole animals and individual amino acids. Oecologia 120: 416–426.
Finlay, J. C. & C. Kendall, 2007. Stable isotope tracing of temporal and spatial variability in organic matter sources to freshwater ecosystems. In Michener, R. & K. Lajtha (eds), Stable Isotopes in Ecology and Environmental Science. Blackwell Publishing, Oxford: 283–333.
Fong, P. & R. L. Kennison, 2010. Phase shifts, alternative stable states, and the status of southern California Lagoons. In Kennish, M. J. & H. W. Paerl (eds), Coastal Lagoons: Critical Habitats of Environmental Change. CRC Press, Boca Raton: 227–251.
Fourqurean, J. W., S. P. Escorcia, W. T. Anderson & J. C. Zieman, 2005. Spatial and seasonal variability in elemental content, δ13C, and δ15N of Thalassia testudinum from South Florida and its implications for ecosystem studies. Estuaries 28: 447–461.
Fry, B., 2003. Steady state models of stable isotopic distributions. Isotopes in Environmental and Health Studies 39: 219–232.
Fry, B. & C. Arnold, 1982. Rapid 13C/12C turnover during growth of brown shrimp (Penaeus aztecus). Oecologia 54: 200–204.
Garcia, A. M., M. C. Claudino, R. Mont’Alverne, P. E. R. Pereyra, M. Copertino & J. P. Vieira, 2017. Temporal variability in assimilation of basal food sources by an omnivorous fish at Patos Lagoon Estuary revealed by stable isotopes (2010–2014). Marine Biology Research 13: 98–107.
Garcia, A. F. S., S. Pasquaud, H. Cabral, A. M. Garcia, M. L. dos Santos & J. P. Vieira, 2019. Assimilation of allochthonous matter by estuarine consumers during the 2015 El Niño event. Estuaries and Coasts 42: 1281–1296.
García-Rodríguez, F., E. Brugnoli, P. Muniz, N. Venturini, L. Burone, M. Hutton, M. Rodríguez, A. Pita, N. Kandratavicius, L. Pérez & J. Verocai, 2014. Warm-phase ENSO events modulate the continental freshwater input and the trophic state of sediments in a large South American estuary. Marine and Freshwater Research 65: 1–11.
Gilbert, P. M., J. J. Middelburg, J. W. McClelland & M. J. V. Zanden, 2019. Stable isotope tracers: enriching our perspectives and questions on sources, fates, rates, and pathways of major elements in aquatic systems. Limnology and Oceanography 64: 950–981.
Grimm, A. M., S. E. T. Ferraz & J. Gomes, 1998. Precipitation anomalies in Southern Brazil associated with El Niño and La Niña events. Journal of Climate 11: 2863–2880.
Haraguchi, L., J. Carstensen, P. C. Abreu & C. Odebrecht, 2015. Long-term changes of the phytoplankton community and biomass in the subtropical shallow Patos Lagoon Estuary, Brazil. Estuarine and Coastal Shelf Science 162: 76–87.
Hardison, A. K., E. A. Canuel, I. C. Anderson, C. R. Tobias, B. Veuger & M. N. Waters, 2013. Microphytobenthos and benthic macroalgae determine sediment organic matter composition in shallow photic sediments. Biogeosciences 10: 5571–5588.
Hemminga, M. A. & M. A. Mateo, 1996. Stable carbon isotopes in seagrasses: variability in ratios and use in ecological studies. Marine Ecology Progress Series 140: 285–298.
Hyndes, G. A., C. E. Hanson & M. A. Vanderklift, 2013. The magnitude of spatial and temporal variation in δ15N and δ13C differs between taxonomic groups: implications for food web studies. Estuarine, Coastal and Shelf Science 119: 176–187.
James, N. C., L. Van Niekerk, A. K. Whitfield, W. M. Potts, A. Götz & A. W. Paterson, 2013. Effects of climate change on South African estuaries and associated fish species. Climate Research 57: 233–248.
Kjerfve, B., 1986. Comparative oceanography of coastal lagoons. In Wolfe, D. A. (ed.), Estuarine Variability. Academic Press, New York: 63–81.
Lanari, M., H. Kennedy, M. S. Copertino, M. Wallner-Kersanach & M. C. Claudino, 2017. Dynamics of estuarine drift macroalgae: growth cycles and contributions to sediments in shallow areas. Marine Ecology Progress Series 570: 41–55.
Lanari, M., M. C. Claudino, A. M. Garcia & M. S. Copertino, 2018. Changes in the elemental (C, N) and isotopic (δ13C, δ15N) composition of estuarine plants during diagenesis and implications for ecological studies. Journal of Experimental Marine Biology and Ecology 500: 46–54.
Lehman, P. W., 2000. The influence of climate on phytoplankton community biomass in San Francisco Bay Estuary. Limnology and Oceanography 45: 580–590.
Lund-Hansen, L. C., K. T. Jensen, T. J. Andersen, M. H. Nielsen, H. Doan-Nhu & L. Nguyen-Ngoc, 2018. Impacts and effects of a historical high and ENSO linked freshwater inflow in the tropical estuary Nha Phu, southeast Vietnam. Regional Studies in Marine Science 17: 28–37.
Lyons, D. A., C. Arvanitidis, A. J. Blight, E. Chatzinikolaou, T. Guy-Haim, J. Kotta, H. Orav-Kotta, A. M. Queirós, G. Rilov, P. J. Somerfield & T. P. Crowe, 2014. Macroalgal blooms alter community structure and primary productivity in marine ecosystems. Global Change Biology 20: 2712–2724.
Macreadie, P. I., T. C. Rolph, R. Boyd, C. J. Schröder-Adams & C. G. Skilbeck, 2015. Do ENSO and coastal development enhance coastal burial of terrestrial carbon? PLoS ONE 10: 1–11.
Marshall, J. D., J. R. Brooks & K. Lajtha, 2007. Sources of variation in the stable isotopic composition of plants. In Michener, R. & K. Lajtha (eds), Stable Isotopes in Ecology and Environmental Science. Blackwell Publishing, Oxford: 22–60.
McArdle, B. H. & M. J. Anderson, 2001. Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82: 290–297.
McClelland, J. W. & I. Valiela, 1998. Linking nitrogen in estuarine producers to land-derived sources. Limnology and Oceanography 43: 577–585.
McClelland, J. W., I. Valiela & R. H. Michener, 1997. Nitrogen-stable isotope signatures in estuarine food webs: a record of increasing urbanization in coastal watersheds. Limnology and Oceanography 42: 930–937.
McCutchan, J. H. J. & W. M. J. Lewis, 2001. Seasonal variation in stable isotope ratios of stream algae. Verhandlungen des Internationalen Verein Limnologie 27: 3304–3307.
Möller, O. O., P. Castaing, J. C. Salomon & P. Lazure, 2001. The influence of local and non-local forcing effects on the subtidal circulation of Patos Lagoon. Estuaries 24: 297–311.
National Oceanic and Atmospheric Administration (NOAA). http://www.cpc.noaa.gov. Accessed 1 Sept 2019.
Nordström, M., K. Aarnio & E. Bonsdorff, 2009. Temporal variability of a benthic food web: patterns and processes in a low-diversity system. Marine Ecology Progress Series 378: 13–26.
Odebrecht C. & P. C. Abreu, 2019. Phytoplankton and water quality parameters in the Patos Lagoon estuary and adjacent marine coast. Sistema de Informação sobre a Biodiversidade Brasileira—SiBBr. Sampling event dataset. https://doi.org/10.15468/xmlvxm accessed via GBIF.org on 2019-05-03.
Odebrecht, C., P. C. Abreu, C. E. Bemvenuti, M. Copertino, J. H. Muelbert, J. P. Vieira & U. Seeliger, 2010. The Patos Lagoon Estuary, Southern Brazil: biotic responses to natural and anthropogenic impacts in the last decades (1979–2008). In Kennish, M. J. & H. W. Paerl (eds), Coastal Lagoons: Critical Habitats of Environmental Change. CRC Press, Boca Raton: 433–455.
Odebrecht, C., P. C. Abreu & J. Carstensen, 2015. Retention time generates short-term phytoplankton blooms in a shallow microtidal subtropical estuary. Estuarine, Coastal and Shelf Science 162: 35–44.
Olin, J. A., N. E. Hussey, S. A. Rush, G. R. Poulakis, C. A. Simpfendorfer, M. R. Heupel & A. T. Fisk, 2013. Seasonal variability in stable isotopes of estuarine consumers under different freshwater flow regimes. Marine Ecology Progress Series 487: 55–69.
Oliveira, M. C. L. M., R. Mont’Alverne, L. A. Sampaio, M. B. Tesser, L. R. V. Ramos & A. M. Garcia, 2017. Elemental turnover rates and trophic discrimination in juvenile Lebranche mullet Mugil liza under experimental conditions. Journal of Fish Biology 91: 1241–1249.
Olsen, Y. S., S. E. Fox, E. L. Kinney, M. Teichberg & I. Valiela, 2010. Differences in urbanization and degree of marine influence are reflected in δ13C and δ15N of producers and consumers in seagrass habitats of Puerto Rico. Marine Environmental Research 69: 198–206.
Peixoto, A. R. & C. S. B. Costa, 2004. Produção primária líquida aérea de Spartina densiflora Brong. (Poaceae) no estuário da laguna dos Patos, Rio Grande do Sul. Brasil Iheringia Série Botânica 59: 27–34.
Possamai, B., J. P. Vieira, A. M. Grimm & A. M. Garcia, 2018. Temporal variability (1997–2015) of trophic fish guilds and its relationships with El Niño events in a subtropical estuary. Estuarine, Coastal and Shelf Science 202: 145–154.
Possamai, B., D. J. Hoeinghaus, C. Odebrecht, P. C. Abreu, L. E. Moraes, A. C. A. Santos & A. M. Garcia, 2020. Freshwater inflow variability affects the relative importance of allochthonous sources contribution to estuarine fishes. Estuaries and Coasts 48: 880–893.
Pruell, R. J., B. K. Taplin, J. L. Lake & S. Jayaraman, 2006. Nitrogen isotope ratios in estuarine biota collected along a nutrient gradient in Narragansett Bay, Rhode Island, USA. Marine Pollution Bulletin 52: 612–620.
Ramos, R. & J. González-Solís, 2012. Trace me if you can: the use of intrinsic biogeochemical markers in marine top predators. Frontiers in Ecology and the Environment 10: 258–266.
Rodríguez-Graña, L., D. Calliari, D. Conde, J. Sellanes & R. Urrutia, 2008. Food web of a SW Atlantic shallow coastal lagoon: spatial environmental variability does not impose substantial changes in the trophic structure. Marine Ecology Progress Series 362: 69–83.
Rolff, C., 2000. Seasonal variation in δ13C and δ15N of size-fractionated plankton at a coastal station in the northern Baltic proper. Marine Ecology Progress Series 203: 47–65.
Román, M., S. Rendal, E. Fernández & G. Méndez, 2018. Seasonal variability of the carbon and nitrogen isotopic signature in a Zostera noltei Meadow at the NW Iberian Peninsula. Wetlands 38: 739–753.
Simenstad, C. A. & R. C. Wissmar, 1985. δ13C evidence of the origins and fates of organic carbon in estuarine and nearshore food webs. Marine Ecology Progress Series 22: 141–152.
Stephenson, R. L., F. C. Tan & K. H. Mann, 1984. Stable carbon isotope variability in marine macrophytes and its implications for food web studies. Marine Biology 230: 223–230.
Stock, B. C. & B. X. Semmens, 2016. MixSIAR GUI User Manual. Version 3.1. https://doi.org/10.5281/zenodo.47719
Trilla, G. G., S. de Marco, J. Marcovecchio, R. Vicari & P. Kandus, 2010. Net primary productivity of Spartina densiflora brong in an SW Atlantic Coastal salt marsh. Estuaries and Coasts 33: 953–962.
Trudeau, V. & J. B. Rasmussen, 2003. The effect of water velocity on stable carbon and nitrogen isotope signatures of periphyton. Limnology and Oceanography 48: 2194–2199.
Viana, I. G. & A. Bode, 2015. Variability in δ15N of intertidal brown algae along a salinity gradient: differential impact of nitrogen sources. Science of the Total Environment 512–513: 167–176.
Vizzini, S. & A. Mazzola, 2003. Seasonal variations in the stable carbon and nitrogen isotope ratios (13C/12C and 15N/14N) of primary producers and consumers in a western Mediterranean coastal lagoon. Marine Biology 142: 1009–1018.
Wang, C., C. Deser, J.-Y. Yu, P. DiNezio & A. Clement, 2016. El Niño-southern oscillation (ENSO): a review. In Glymn, P., D. Manzello & I. Enochs (eds), Coral Reefs of the Eastern Pacific. Springer Science Publisher, New York: 85–106.
Ward, K. M., J. C. Callaway & J. B. Zedler, 2003. Episodic colonization of an intertidal mudflat by native cordgrass (Spartina foliosa) at Tijuana Estuary. Estuaries 26: 116–130.
Woodland, R. J., M. A. Rodríguez, P. Magnan, H. Clément & G. Cabana, 2012. Incorporating temporally dynamic baselines in isotopic mixing models. Ecology 93: 131–144.
Ye, F., W. Guo, Z. Shi, G. Jia & G. Wei, 2017. Seasonal dynamics of particulate organic matter and its response to flooding in the Pearl River Estuary, China, revealed by stable isotope (δ13C and δ15N) analyses. Journal of Geophysical Research: Oceans 122: 6835–6856.
Acknowledgments
This study is a contribution of the research group ‘‘Grupo de Análises de Isótopos Estáveis em Ambientes Aquáticos’’ (GAIA-FURG/CNPq) and was conducted within the program Brazilian Long-Term Ecological Research (BR-LTER) in the Patos Lagoon Estuary and Adjacent Marine Coast sponsored by the National Scientific and Technological Development Council (CNPq), the Fundação de Amparo à Pesquisa do Rio Grande do Sul (FAPERGS), and the Newton Fund (British Council). This study was also financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001. AMG thanks CNPq by productivity scholarship [Grant Number: 309208/2018-1]. ML was granted a CAPES postdoc scholarship [Grant Number: 88887.357827/2019-00]. We also thank the anonymous reviewers and editors for comments and suggestions that greatly improved the manuscript.
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AMG, MSC, ML, and BP conceived the study. AMG conceived the long-term isotopic monitoring research. BP conducted fieldwork and processed the material for stable isotope analysis. BP and ML performed statistical analyses. ML wrote the manuscript with valuable inputs and edits by the co-authors. All authors read and approved the final manuscript.
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Lanari, M., Possamai, B., da Silva Copertino, M. et al. Seasonal and El Niño Southern Oscillation-driven variations in isotopic and elemental patterns among estuarine primary producers: implications for ecological studies. Hydrobiologia 848, 593–611 (2021). https://doi.org/10.1007/s10750-020-04462-0
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DOI: https://doi.org/10.1007/s10750-020-04462-0