Abstract
The trophic fate of various food sources is of central interest for ecologists, yet not well understood in coastal lagoon food webs. In this field study, fatty acids (FA), stable isotopes (SI), and compound-specific isotopic analysis (CSIA) on FA were used to investigate how diets from oceanic and local sources are retained in a bivalve species (Spondylus crassisquama; Lamarck 1819) along a transect in the Ojo de Liebre lagoon (BCS, Mexico). Results from SI and FA indicated the contribution of oceanic diatoms at the entrance of the lagoon, through 15N enrichment, and higher proportions of 16:1n-7 and 20:5n-3 in digestive glands. In the inner bay, higher abundance of 18-carbon FA (18:1n-9, 18:3n-3, 18:4n-3) suggested a higher contribution of microheterotrophs, including (dino)flagellates and ciliates, to the diet of this bivalve derived from local production. Significant spatial differences for the δ13C of FA highlighted changes in the origin of food sources. Indeed, a 13C depletion was observed in the δ13C of heterotrophic flagellates biomarkers in individuals from the innermost station, revealing that their origin in the diet of bivalves differs within the lagoon, highlighting the importance of local processes (sediment resuspension, remineralization) in the trophic functioning of the lagoon. The δ13C values of FA considered as diatoms biomarkers (16:1n-7 and 20:5n-3) were consistent, which suggests that diatoms assimilated have very similar origins throughout the lagoon. The complementary of the tracers used here allowed for a better understanding of the trophic functioning of this coastal lagoon submitted to oceanic influences.
Similar content being viewed by others
References
Abrajano TA, Murphy DE, Fang J, Comet P, Brooks JM (1994) 13C12c ratios in individual fatty acids of marine mytilids with and without bacterial symbionts. Org Geochem 21:611–617. https://doi.org/10.1016/0146-6380(94)90007-8
Alfaro AC, Thomas F, Sergent L, Duxbury M (2006) Identification of trophic interactions within an estuarine food web (northern New Zealand) using fatty acid biomarkers and stable isotopes. Estuar Coast Shelf Sci 70:271–286. https://doi.org/10.1016/j.ecss.2006.06.017
Allan EL, Ambrose ST, Richoux NB, Froneman PW (2010) Determining spatial changes in the diet of nearshore suspension-feeders along the South African coastline: stable isotope and fatty acid signatures. Estuar Coast Shelf Sci 87:463–471. https://doi.org/10.1016/j.ecss.2010.02.004
Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263
Bachelet G, De Montaudouin X, Auby I, Labourg P-J (2000) Seasonal changes in macrophyte and macrozoobenthos assemblages in three coastal lagoons under varying degrees of eutrophication. ICES J Mar Sci 57:1495–1506
Bachok Z, Mfilinge PL, Tsuchiya M (2003) The diet of the mud clam Geloina coaxans (Mollusca, Bivalvia) as indicated by fatty acid markers in a subtropical mangrove forest of Okinawa, Japan. J Exp Mar Biol Ecol 292:187–197. https://doi.org/10.1016/S0022-0981(03)00160-6
Bec A, Perga M-E, Koussoroplis A, Bardoux G, Desvilettes C, Bourdier G, Mariotti A (2011) Assessing the reliability of fatty acid–specific stable isotope analysis for trophic studies. Methods Ecol Evol 2:651–659. https://doi.org/10.1111/j.2041-210X.2011.00111.x
Budge SM, Iverson SJ, Koopman HN (2006) Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Mar Mammal Sci 22:759–801. https://doi.org/10.1111/j.1748-7692.2006.00079.x
Budge SM, Wooller MJ, Springer AM, Iverson SJ, McRoy CP, Divoky GJ (2008) Tracing carbon flow in an arctic marine food web using fatty acid-stable isotope analysis. Oecologia 157:117–129
Cabello-Pasini A, Muñiz-Salazar R, Ward DH (2003) Annual variations of biomass and photosynthesis in Zostera marina at its southern end of distribution in the North Pacific. Aquat Bot 76:31–47. https://doi.org/10.1016/S0304-3770(03)00012-3
Carlier A, Riera P, Amouroux J-M, Bodiou J-Y, Desmalades M, Grémare A (2008) Food web structure of two Mediterranean lagoons under varying degree of eutrophication. J Sea Res 60:264–275. https://doi.org/10.1016/j.seares.2008.10.006
Clavier J, Chauvaud L, Amice E, Lazure P, Van Der Geest M, Labrosse P, Diagne A, Carlier A, Chauvaud S (2014) Benthic metabolism in shallow coastal ecosystems of the Banc d’Arguin, Mauritania. Mar Ecol Prog Ser 501:11–23
Colombo SM, Parrish CC, Whiticar MJ (2016) Fatty acid stable isotope signatures of molluscs exposed to finfish farming outputs. Aquac Environ Interact 8:611–617
Core Team R (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
Dalsgaard J, St. John M, Kattner G, Müller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340. https://doi.org/10.1016/S0065-2881(03)46005-7
Du X, Peterson W, O’Higgins L (2015) Interannual variations in phytoplankton community structure in the northern California Current during the upwelling seasons of 2001–2010. Mar Ecol Prog Ser 519:75–87
Falkowski PG (1991) Species variability in the fractionation of 13C and 12C by marine phytoplankton. J Plankton Res 13:21–28. https://doi.org/10.1093/oxfordjournals.plankt.a042367
Fenton GE, Ritz DA (1988) Changes in carbon and hydrogen stable isotope ratios of macroalgae and seagrass during decomposition. Estuar Coast Shelf Sci 26:429–436
Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509
France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Mar Ecol Prog Ser 124:307–312
Fry B (1988) Food web structure on Georges Bank from stable C, N, and S isotopic compositions. Limnol Oceanogr 33:1182–1190. https://doi.org/10.4319/lo.1988.33.5.1182
Gaillard B, Meziane T, Tremblay R, Archambault P, Blicher ME, Chauvaud L, Rysgaard S, Olivier F (2017) Food resources of the bivalve Astarte elliptica in a sub-Arctic fjord: a multi-biomarker approach. Mar Ecol Prog Ser 567:139–156
Graham C, Oxtoby L, Wang SW, Budge SM, Wooller MJ (2014) Sourcing fatty acids to juvenile polar cod (Boreogadus saida) in the Beaufort Sea using compound-specific stable carbon isotope analyses. Polar Biol 37:697–705
Hemminga MA, Mateo MA (1996) Stable carbon isotopes in seagrasses: variability in ratios and use in ecological studies. Mar Ecol Prog Ser 140:285–298
Hill JM, McQuaid CD (2008) δ13C and δ15N biogeographic trends in rocky intertidal communities along the coast of South Africa: evidence of strong environmental signatures. Estuar Coast Shelf Sci 80:261–268. https://doi.org/10.1016/j.ecss.2008.08.005
Ibarra-Obando SE, Camacho-Ibar VF, Carriquiry JD, Smith SV (2001) Upwelling and lagoonal ecosystems of the dry Pacific coast of Baja California. In: Seeliger U, Kjerfve B (eds) Coastal marine ecosystems of Latin America. Ecological studies (analysis and synthesis), vol 144. Springer, Berlin, Heidelberg
Jaschinski S, Brepohl DC, Sommer U (2008) Carbon sources and trophic structure in an eelgrass Zostera marina bed, based on stable isotope and fatty acid analyses. Mar Ecol Prog Ser 358:103–114
Jeong HJ, Du Yoo Y, Kim JS, Seong KA, Kang NS, Kim TH (2010) Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Sci J 45:65–91
Kainz M, Lucotte M, Parrish CC (2002) Methyl mercury in zooplankton the role of size, habitat, and food quality. Can J Fish Aquat Sci 59:1606–1615
Kelly JR, Scheibling RE (2012) Fatty acids as dietary tracers in benthic food webs. Mar Ecol Prog Ser 446:1–22
Kharlamenko VI, Kiyashko SI, Imbs AB, Vyshkvartzev DI (2001) Identification of food sources of invertebrates from the seagrass Zostera marina community using carbon and sulfur stable isotope ratio and fatty acid analyses. Mar Ecol Prog Ser 220:103–117
Layman CA, Araujo MS, Boucek R, Hammerschlag-Peyer CM, Harrison E, Jud ZR, Matich P, Rosenblatt AE, Vaudo JJ, Yeager LA (2012) Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biol Rev 87:545–562
Le Grand F, Soudant P, Siah A, Tremblay R, Marty Y, Kraffe E (2014) Disseminated Neoplasia in the soft-shell Clam Mya arenaria: membrane lipid composition and functional parameters of circulating cells. Lipids 49:807–818. https://doi.org/10.1007/s11745-014-3917-4
Lorrain A, Paulet Y-M, Chauvaud L, Savoye N, Donval A, Saout C (2002) Differential δ13C and δ15N signatures among scallop tissues: implications for ecology and physiology. J Exp Mar Biol Ecol 275:47–61. https://doi.org/10.1016/S0022-0981(02)00220-4
Marchais V, Schaal G, Grall J, Lorrain A, Nerot C, Richard P, Chauvaud L (2013) Spatial variability of stable isotope Ratios in Oysters (Crassostrea gigas) and primary producers along an estuarine gradient (Bay of Brest, France). Estuaries Coasts 36:808–819. https://doi.org/10.1007/s12237-012-9584-x
Nerot C, Meziane T, Schaal G, Grall J, Lorrain A, Paulet Y-M, Kraffe E (2015) Spatial changes in fatty acids signatures of the great scallop Pecten maximus across the Bay of Biscay continental shelf. Cont Shelf Res 109:1–9. https://doi.org/10.1016/j.csr.2015.08.032
Nixon SW (1982) Nutrient dynamics, primary production and fisheries yields of lagoons. In: Proceedings of the international symposium on coastal lagoons SCORI lABO/UNESCO, Bordeaux, 8–14 September 1981, pp 357–371
O’Reilly CM, Hecky RE, Cohen AS, Plisnier P-D (2002) Interpreting stable isotopes in food webs: recognizing the role of time averaging at different trophic levels. Limnol Oceanogr 47:306–309. https://doi.org/10.4319/lo.2002.47.1.0306
Parrish CC, Abrajano TA, Budge SM, Helleur RJ, Hudson ED, Pulchan K, Ramos C (2000) Lipid and phenolic biomarkers in marine ecosystems: analysis and applications. In: Wangersky PJ (eds) Marine chemistry. The handbook of environmental chemistry (Vol. 5 Series: Water pollution), vol 5D. Springer, Berlin, Heidelberg
Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montaña CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189. https://doi.org/10.1007/s00442-006-0630-x
Ramos CS, Parrish CC, Quibuyen TAO, Abrajano TA (2003) Molecular and carbon isotopic variations in lipids in rapidly settling particles during a spring phytoplankton bloom. Org Geochem 34:195–207
Raven JA, Johnston AM, Kübler JE, Korb R, McInroy SG, Handley LL, Scrimgeour CM, Walker DI, Beardall J, Vanderklift M, Fredriksen S, Dunton KH (2002) Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Funct Plant Biol 29:355–378. https://doi.org/10.1071/pp01201
Reddin CJ, Docmac F, O’Connor NE, Bothwell JH, Harrod C (2015) Coastal upwelling drives intertidal assemblage structure and trophic ecology. PLoS One 10:e0130789
Riera P (2007) Trophic subsidies of Crassostrea gigas, Mytilus edulis and Crepidula fornicata in the Bay of Mont Saint Michel (France): a δ13C and δ15N investigation. Estuar Coast Shelf Sci 72:33–41. https://doi.org/10.1016/j.ecss.2006.10.002
Riera P, Richard P (1996) Isotopic determination of food sources of Crassostrea gigas along a trophic gradient in the estuarine bay of Marennes-Oléron. Estuar Coast Shelf Sci 42:347–360
Ruess L, Chamberlain PM (2010) The fat that matters: soil food web analysis using fatty acids and their carbon stable isotope signature. Soil Biol Biochem 42:1898–1910
Schaal G, Nerot C, Grall J, Chouvelon T, Lorrain A, Mortillaro J-M, Savoye N, Brind’Amour A, Paulet Y-M, Le Bris H (2016) Stable isotope ratios in bentho-demersal biota along a depth gradient in the Bay of Biscay: a multitrophic study. Estuar Coast Shelf Sci 179:201–206. https://doi.org/10.1016/j.ecss.2015.10.023
Taylor AG, Landry MR (2018) Phytoplankton biomass and size structure across trophic gradients in the southern California Current and adjacent ocean ecosystems. Mar Ecol Prog Ser 592:1–17
Van den Meersche K, Middelburg JJ, Soetaert K, Van Rijswijk P, Boschker HT, Heip CH (2004) Carbon-nitrogen coupling and algal-bacterial interactions during an experimental bloom: modeling a 13C tracer experiment. Limnol Oceanogr 49:862–878
Vuorio K, Meili M, Sarvala J (2006) Taxon-specific variation in the stable isotopic signatures (δ13C and δ15N) of lake phytoplankton. Freshw Biol 51:807–822
Zaytsev O (2003) Coastal upwelling activity on the Pacific shelf of the Baja California peninsula. J Oceanogr 59:489–502
Zhukova NV (1991) The pathway of the biosynthesis of non-methylene-interrupted dienoic fatty acids in molluscs. Comp Biochem Physiol Part B Comp Biochem 100:801–804
Acknowledgements
Authors would like to thank the contribution of the Guerrero Negro unit of CIBNOR for hosting the first steps of sample preparation after fieldwork, the LIPIDOCEAN analytical facilities for hosting all fatty acid analyses, and the Pôle Spectrométrie Océan (Clément Tanvet) for running bulk SI and CSIA analyses. Authors thank the fishermen crew for the fieldwork, but also Laura Guzman for their precious help during sampling and dissections, and Dr. Elena Palacios and Dr. Kitty Arredondo Vega, for the laboratory facilities provided for the preparation of samples at the CIBNOR La Paz. Authors address their thanks to the Reserva de la biosfera desierto de “el Vizcaino” for their help and support in carrying out sampling for this study. Authors would like to thank Aurelien Boye for his precious help and advices about statistical analyses. Authors also thank Pr. Sandra Shumway and an anonymous reviewer, for their help in improving this paper.
Funding
This study was supported by the ECOS-ANUIES program (PROPHYMUS project), the “Laboratoire d’Excellence” LabexMER (ANR-10-LABX-19) and co-funded by a grant from the French government under the program “Investissements d’Avenir”. MMR’s PhD fellowship was provided by the French Research Ministry and Region Bretagne.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national and/or institutional guidelines for the care and use of bivalves Spondylus crassisquama were followed. The individuals of S. crassisquama have been sampled under the permit PRMN/DGOPA-011/2017, delivered by the Mexican government.
Additional information
Responsible Editor: S. Shumway.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Reviewed by Undisclosed experts.
Rights and permissions
About this article
Cite this article
Mathieu-Resuge, M., Schaal, G., Kraffe, E. et al. Different particle sources in a bivalve species of a coastal lagoon: evidence from stable isotopes, fatty acids, and compound-specific stable isotopes. Mar Biol 166, 89 (2019). https://doi.org/10.1007/s00227-019-3535-z
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-019-3535-z