Trophic importance of diatoms in an intertidal Zostera noltii seagrass bed: Evidence from stable isotope and fatty acid analyses

Estuarine, Coastal and Shelf Science

Volumn 92, Issue 1, 2011, Pages 140-153

  Lebreton, Benoit ^a   Richard, Pierre ^a   Galois, Robert ^a   Radenac, Gilles ^a   Pfléger, Camille ^a   Guillou, Gaël ^a   Mornet, Françoise ^b   Blanchard, Gérard F ^a  

^a UNIVERSITÉ DE LA ROCHELLE   (France)

^b IFREMER   (France)

Author keywords

European Atlantic coast; Fatty acid profiles; Food web; Intertidal seagrass bed; Microphytobenthos; Stable isotope ratio; Zostera noltii

Indexed keywords

ALGA; BACTERIUM; BIOMASS; CARBON ISOTOPE; DIATOM; EPIPHYTE; FATTY ACID; FLAGELLATE; FOOD WEB; INTERTIDAL ENVIRONMENT; ISOTOPIC ANALYSIS; PARTICULATE ORGANIC MATTER; PHYTOBENTHOS; SEAGRASS; STABLE ISOTOPE; TROPHIC STATUS;

ATLANTIC COAST [EUROPE];

ALGAE; BACILLARIOPHYTA; BACTERIA (MICROORGANISMS); INVERTEBRATA; MASTIGOPHORA (FLAGELLATES); ZOSTERA NOLTII;

EID: 79952072364     PISSN: 02727714     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ecss.2010.12.027     Document Type: Article

References (87)

1. Abraham W.-R., Hesse C., Pelz O. Ratios of carbon isotopes in microbial lipids as an indicator of substrate usage. Applied and Environmental Microbiology 1998, 64:4202-4209.
2. Asmus H., Asmus R. The importance of grazing food chain for energy flow and production in three intertidal sand bottom communities of the northern WaddenSea. Helgoländer Meeresuntersuchungen 1985, 39:273-301.
3. Auby I., Labourg P.-J. Seasonal dynamics of Zostera noltii Hornem. In bay of Arcachon (France). Journal of Sea Research 1996, 35:269-277.
4. Baird D., Asmus H., Asmus R. Trophic dynamics of eight intertidal communities of the Sylt-Rømø Bight ecosystem, northern WaddenSea. Marine Ecology Progress Series 2007, 351:25-41.
5. Bannon C.D., Craske J.D., Hilliker A.E. Analysis of fatty acid methyl esters with high accuracy and reliability. V. Validation of theoretical relative response factors of unsaturated esters in the flame ionization detector. Journal of the American Oil Chemists' Society 1986, 63:105-110.
6. 13C in lignin and its implication for stable carbon isotope studies. Nature 1987, 329:708-710.
7. Bergé J.-P., Gouygou J.-P., Dubacq J.-P., Durand P. Reassessment of lipid composition of the diatom, Skeletonema costatum. Phytochemistry 1995, 39:1017-1021.
8. Borowitzka M.A., Lavery P.S., van Keulen M. Epiphytes of seagrasses. Seagrasses: Biology, Ecology and Conservation 2006, 441-461. Springer, Dordrecht. A.W.D. Larkum, R.J. Orth, C.M. Duarte (Eds.).
9. Boschker H.T.S., Wielemaker A., Schaub B.E.M., Holmer M. Limited coupling of macrophyte production and bacterial carbon cycling in the sediments of Zostera spp. meadows. Marine Ecology Progress Series 2000, 203:181-189.
10. Canuel E.A., Martens C.S. Reactivity of recently deposited organic matter: degradation of lipid compounds near the sediment-water interface. Geochimica et Cosmochimica Acta 1996, 60:1793-1806.
11. Carlier A., Riera P., Amouroux J.-M., Bodiou J.-Y., Desmalades M., Grémare A. Spatial heterogeneity in the food web of a heavily modified Mediterranean coastal lagoon: stable isotope evidence. Aquatic Biology 2009, 5:167-170.
12. Cattaneo A., Méthot G., Pinel-Alloul B., Niyonsenga T., Lapierre L. Epiphyte size and taxonomy as biological indicators of ecological and toxicological factors in Lake Saint-François (Québec). Environmental Pollution 1995, 87:357-372.
13. Cebrián J. Patterns in the fate of production in plant communities. The American Naturalist 1999, 154:449-468.
14. Choy E.J., An S., Kang C.-K. Pathways of organic matter through food webs of diverse habitats in the regulated Nakdong River estuary (Korea). Estuarine, Coastal and Shelf Science 2008, 78:215-226.
15. Christie W.W. Extraction and hydrolysis of lipids and some reactions of their fatty acid components. Handbook of Chromatography, Lipids 1984, 33-46. CRC Press, Boca Raton. G. Zweig, J. Sherma (Eds.).
16. Christie W.W. Equivalent chain-lengths of methyl ester derivatives of fatty acids on gas chromatography. A reappraisal. Journal of Chromatography 1988, 447:305-314.
17. Coleman V.L., Burkholder J.M. Response of microalgal epiphyte communities to nitrate enrichment in an eelgrass (Zostera marina) meadow. Journal of Phycology 1995, 31:36-43.
18. Copeman L.A., Parrish C.C., Gregory R.S., Jamieson R.E., Wells J., Whiticar M.J. Fatty acid biomarkers in coldwater eelgrass meadows: elevated terrestrial input to the food web of age-0 Atlantic cod Gadus morhua. Marine Ecology Progress Series 2009, 386:237-251.
19. Daehnick A.E., Sullivan M.J., Moncreiff C.A. Primary production of the sand microflora in seagrass beds of Mississipi sound. Botanica Marina 1992, 35:131-139.
20. 13C study of the feeding habits in four mediterranean Leptomysis species (Crustacea: Mysidacea). Pubblicazioni della Stazione Zoologica di Napoli I. Marine Ecology 1995, 16:93-102.
21. Dechambenoy C.L., Pontier F., Sirou F., Vouvé J. Apport de la thermographie infrarouge aéroportée à la connaissance de la dynamique superficielle des estuaires (système Charente-Seudre-Anse de l'Aiguillon). Comptes Rendus de l'Académie des Sciences Paris 1977, 284:1269-1272.
22. 15N enrichment as an integrator of the effects of C and N on microbial metabolism and ecosystem function. Ecology Letters 2008, 11:389-397.
23. Duarte C.M. Temporal biomass variability and production/biomass relationships of seagrass communities. Marine Ecology Progress Series 1989, 51:269-276.
24. Duarte C.M., Chiscano C.L. Seagrass biomass and production: a reassessment. Aquatic Botany 1999, 65:159-174.
25. Dunstan G.A., Volkman J.K., Barrett S.M., Leroi J.-M., Jeffrey S.W. Essential polyunsaturated fatty acids from 14 species of diatom (Bacillariophyceae). Phytochemistry 1994, 35:155-161.
26. Fenchel T. Marine plankton food chains. Annual Review of Ecology and Systematics 1988, 19:19-38.
27. Folch J., Lees M., Sloane Stanley G.H. A simple method for the isolation and purification of total lipides from animal tissues. The Journal of Biological Chemistry 1957, 226:497-509.
28. Fry B., Macko S.A., Zieman J.C. Review of Stable Isotopic Investigations of Food Webs in Seagrass Meadows. Proceedings of the Symposium on Subtropical-tropical Seagrasses of the Southeastern United States 1987, Florida Marine Research Publications, Gainesville, 117-138.
29. Fry B. Stable Isotope Ecology 2006, Springer, New-York, 308 pp.
30. Galois R., Richard P., Fricourt B. Seasonal variations in suspended particulate matter in the Marennes-Oléron Bay, France, using lipids as biomarkers. Estuarine, Coastal and Shelf Science 1996, 43:335-357.
31. Green E.P., Short F.T. World Atlas of Seagrasses 2003, University of California Press, Berkeley, 310 pp.
32. Grossmann S., Reichardt W. Impact of Arenicola marina on bacteria in intertidal sediments. Marine Ecology Progress Series 1991, 77:85-93.
33. Guarini J.-M., Blanchard G.F., Bacher C., Gros P., Riera P., Richard P., Gouleau D., Galois R., Prou J., Sauriau P.-G. Dynamics of spatial patterns of microphytobenthic biomass: inferences from a geostatistical analysis of two comprehensive surveys in Marennes-Oléron Bay (France). Marine Ecology Progress Series 1998, 166:131-141.
34. Guarini J.-M., Blanchard G.F., Gros P. Quantification of the microphytobenthic primary production in European intertidal mudflats - a modelling approach. Continental Shelf Research 2000, 20:1771-1788.
35. Guillaumont B. Utilisation de l'imagerie satellitaire pour des comparaisons spatiales et temporelles en zone intertidale. Estuaries and Coasts: Spatial and Temporal Intercomparisons. ECSA19 Symposium 1991, Olsen & Olsen, Fredensborg, 63-68.
36. Harrison P.G. Control of microbial growth and of amphipod grazing by water-soluble compounds from leaves of Zostera marina. Marine Biology 1982, 67:225-230.
37. Héral M., Deslous-Paoli J.-M., Prou J., Razet D. Relations entre la nourriture disponible et la production de mollusques en milieu estuarien: variabilité temporelle de la colonne d'eau. Haliotis 1987, 16:149-158.
38. Herlory O., Richard P., Blanchard G.F. Methodology of light response curves: application of chlorophyll fluorescence to microphytobenthic biofilms. Marine Biology 2007, 153:91-101.
39. Hootsmans M.J.M., Vermaat J.E., Beijer J.A.J. Periphyton density and shading in relation to tidal depth and fiddler crab activity in intertidal seagrass beds of the Banc d'Arguin (Mauritania). Hydrobiologia 1993, 258:73-80.
40. Jacobs R.P.W.M., Huisman W.H.T. Macrobenthos of some Zostera beds in the vicinity of Roscoff (France) with special reference to relations with community structure and environmental factors. Proceedings Koninglijke Nederlandse Akademie Van Wedenschappen Series C-Biological and Medical Sciences 1982, 85:335-356.
41. Jaschinski S., Brepohl D.C., Sommer U. Carbon sources and trophic structure in an eelgrass Zostera marina bed, based on stable isotope and fatty acid analyses. Marine Ecology Progress Series 2008, 358:103-114.
42. Kang C.K., Sauriau P.-G., Richard P., Blanchard G.F. Food sources of the infaunal suspension-feeding bivalve Cerastoderma edule in a muddy sandflat of Marennes-OléronBay, as determined by analyses of carbon and nitrogen stable isotopes. Marine Ecology Progress Series 1999, 187:147-158.
43. Kharlamenko V.I., Kiyashko S.I., Imbs A.B., Vyshkvartzev D.I. Identification of food sources of invertebrates from the seagrass Zostera marina community using carbon and sulfur stable isotope ratio and fatty acid analyses. Marine Ecology Progress Series 2001, 220:103-117.
44. Kharlamenko V.I., Kiyashko S.I., Rodkina S.A., Imbs A.B. Determination of food sources of marine invertebrates from a subtidal sand community using analyses of fatty acids and stable isotopes. Russian Journal of Marine Biology 2008, 34:101-109.
45. Khotimchenko S.V. Fatty acids and polar lipids of seagrasses from the sea of Japan. Phytochemistry 1993, 33:369-372.
46. Kitting C.L., Fry B., Morgan M.D. Detection of inconspicuous epiphytic algae supporting food webs in seagrass meadows. Oecologia 1984, 62:145-149.
47. Koch E.W., Ackerman J.D., Verduin J., van Keulen M. Fluid dynamics in seagrass ecology - from molecules to ecosystems. Seagrasses: Biology, Ecology and Conservation 2006, 193-225. Springer, Dordrecht. A.W.D. Larkum, R.J. Orth, C.M. Duarte (Eds.).
48. Lebreton, B., 2009. Analyse de la structure et du fonctionnement du réseau trophique d'un herbier par approche multi-traceurs: traçage isotopique naturel et profils acides gras. Cas de l'herbier intertidal de Zostera noltii du bassin de Marennes-Oléron, France. Ph.D. thesis, La Rochelle Univ., France, unpublished.
49. Lebreton B., Richard P., Radenac G., Bordes M., Bréret M., Arnaud C., Mornet F., Blanchard G.F. Are epiphytes a significant component of intertidal Zostera noltii beds?. Aquatic Botany 2009, 91:82-90.
50. Leduc D., Probert P.K., Frew R.D., Hurd C.L. Macroinvertebrate diet in intertidal seagrass and sandflat communities: a study using C, N, and S stable isotopes. New Zealand Journal of Marine and Freshwater Research 2006, 40:615-629.
51. Lepoint G., Nyssen F., Gobert S., Dauby P., Bouquegneau J.-M. Relative impact of a seagrass bed and its adjacent epilithic algal community in consumer diets. Marine Biology 2000, 136:513-518.
52. MacIntyre H.L., Geider R.J., Miller D.C. Microphytobenthos: the ecological role of the " secret garden" of unvegetated, shallow-water marine habitats. I. Distribution, abundance and primary production. Estuaries 1996, 19:186-201.
53. Malet N., Sauriau P.-G., Ryckaert M., Malestroit P., Guillou G. Dynamics and sources of suspended particulate organic matter in the Marennes-Oléron oyster farming bay: insights from stable isotopes and microalgae ecology. Estuarine, Coastal and Shelf Science 2008, 78:576-586.
54. Mateo M.A., Cebrián J., Dunton K., Mutchler T. Carbon flux in seagrass ecosystems. Seagrasses: Biology, Ecology and Conservation 2006, 159-192. Springer, Dordrecht. A.W.D. Larkum, R.J. Orth, C.M. Duarte (Eds.).
55. Meziane T., Tsuchiya M. Fatty acids as tracers of organic matter in the sediment and food web of a mangrove/intertidal flat ecosystem, Okinawa. Japan. Marine Ecology Progress Series 2000, 200:49-57.
56. Moncreiff C.A., Sullivan M.J. Trophic importance of epiphytic algae in subtropical seagrass beds: evidence from multiple stable isotope analyses. Marine Ecology Progress Series 2001, 215:93-106.
57. Moncreiff C.A., Sullivan M.J., Daehnick A.E. Primary production dynamics in seagrass beds of Mississippi Sound: the contributions of seagrass, epiphytic algae, sand microflora, and phytoplankton. Marine Ecology Progress Series 1992, 87:161-171.
58. Moorthi S., Berninger U.-G. Mixotrophic nanoflagellates in coastal sediments in the western Baltic Sea. Aquatic Microbial Ecology 2006, 45:79-87.
59. Nichols P.D., Klumpp D.W., Johns R.B. Lipid components of the seagrasses Posidonia australis and Heterozostera tasmanica as indicators of carbon source. Phytochemistry 1982, 21:1613-1621.
60. Nichols P.D., Jones G.J., de Leeuw J.W., Johns R.B. The fatty acid and sterol composition of two marine dinoflagellates. Phytochemistry 1984, 23:1043-1047.
61. Nyssen F., Brey T., Dauby P., Graeve M. Trophic position of Antarctic amphipods-enhanced analysis by a 2-dimensional biomarker assay. Marine Ecology Progress Series 2005, 300:135-145.
62. Pascal P.-Y., Dupuy C., Richard P., Mallet C., Armynot du Chatelet E., Niquil N. Seasonal variation in consumption of benthic bacteria by meio- and macrofauna in an intertidal mudflat. Limnology and Oceanography 2009, 54:1048-1059.
63. Philippart C.J.M. Effect of periphyton grazing by Hydrobia ulvae on the growth of Zostera noltii on a tidal flat in the DutchWadden Sea. Marine Biology 1995, 122:431-437.
64. Rajendran N., Suwa Y., Urushigawa Y. Distribution of phospholipid ester-linked fatty acid biomarkers for bacteria in the sediment of Ise Bay, Japan. Marine Chemistry 1993, 42:39-56.
65. Ramos C.S., Parrish C.C., Quibuyen T.A.O., Abrajano T.A. Molecular and carbon isotopic variations in lipids in rapidly settling particles during a spring phytoplankton bloom. Organic Geochemistry 2003, 34:195-207.
66. Raniello R., Iannicelli M.M., Nappo M., Avila C., Zupo V. Production of Cocconeis neothumensis (Bacillariophyceae) biomass in batch cultures and bioreactors for biotechnological applications: light and nutrient requirements. Journal of Applied Phycology 2007, 19:383-391.
67. Renaud S.M., Thinh L.-V., Parry D.L. The gross chemical composition and fatty acid composition of 18 species of tropical Australian microalgae for possible use in mariculture. Aquaculture 1999, 170:147-159.
68. Riera P., Richard P. Isotopic determination of food sources of Crassostrea gigas along a trophic gradient in the estuarine bay of Marennes-Oléron. Estuarine, Coastal and Shelf Science 1996, 42:347-360.
69. 13C in particulate organic matter and oyster Crassostrea gigas in Marennes-Oléron Bay (France): effect of freshwater inflow. Marine Ecology Progress Series 1997, 147:105-115.
70. Round F.E., Crawford R.M., Mann D.G. The Diatoms: Biology and Morphology of the Genera 1990, Cambridge University Press, Cambridge, 747 pp.
71. Sargent J.R., Whittle K.J. Lipids and Hydrocarbons in the Marine Food Web. Analysis of Marine Ecosystems 1981, 491-533. Academic Press, London. A.R. Longhurst (Ed.).
72. Sargent J.R., Parkes R.J., Mueller-Harvey I., Henderson R.J. Lipid Biomarkers in Marine Ecology. Microbes in the Sea 1987, 119-138. Ellis Horwood Limited, Chichester. M.A. Sleigh (Ed.).
73. Schaal G., Riera P., Leroux C. Trophic coupling between two adjacent benthic food webs within a man-made intertidal area: a stable isotopes evidence. Estuarine, Coastal and Shelf Science 2008, 77:523-534.
74. Schanz A., Polte P., Asmus H. Cascading effects of hydrodynamics on an epiphyte-grazer system in intertidal seagrass beds of the WaddenSea. Marine Biology 2002, 141:287-297.
75. Shin P.K.S., Yip K.M., Xu W.Z., Wong W.H., Cheung S.G. Fatty acid as markers to demonstrating trophic relationships among diatoms, rotifers and green-lipped mussels. Journal of Experimental Marine Biology and Ecology 2008, 357:75-84.
76. 13C analysis of diet. Oecologia 1983, 57:32-37.
77. Valentine J.F., Heck K.L., Kirsch K.D., Webb D. Role of sea urchin Lytechinus variegatus grazing in regulating subtropical turtlegrass Thalassia testudinum meadows in the Florida Keys (USA). Marine Ecology Progress Series 2000, 200:213-228.
78. 13C trophic fractionation: implications for aquatic food web. Limnology and Oceanography 2001, 46:2061-2066.
79. Viso A.-C., Marty J.-C. Fatty acids from 28 marine microalgae. Phytochemistry 1993, 34:1521-1533.
80. Viso A.-C., Pesando D., Bernard P., Marty J.-C. Lipid components of the mediterranean seagrass Posidonia oceanica. Phytochemistry 1993, 34:381-387.
81. Volkman J.K., Johns R.B., Gillan F.T., Perry C.J. Microbial lipids of an intertidal sediment. I. Fatty acids and hydrocarbons. Geochimica et Cosmochimica Acta 1980, 44:1133-1143.
82. Volkman J.K., Jeffrey S.W., Nichols P.D., Rogers G.I., Garland C.D. Fatty acid and lipid composition of 10 species of microalgae used in mariculture. Journal of Experimental Marine Biology and Ecology 1989, 128:219-240.
83. Volkman J.K., Barrett S.M., Blackburn S.I., Mansour M.P., Sikes E.L., Gelin F. Microalgal biomarkers: a review of recent research developments. Organic Geochemistry 1998, 29:1163-1179.
84. Volkman J.K., Revill A.T., Holdsworth D.G., Fredericks D. Organic matter sources in an enclosed coastal inlet assessed using lipid biomarkers and stable isotopes. Organic Geochemistry 2008, 39:689-710.
85. Vouvé, F., 2000. Régénération benthique dans les vasières intertidales de Marennes-Oléron: nature de la matière organique, son impact sur la production et l'incorporation de l'ammonium. Ph.D. thesis, Perpignan Univ., France, unpublished.
86. Wannigama G.P., Volkman J.K., Gillan F.T., Nichols P.D., Johns R.B. A comparison of lipid components of the fresh and dead leaves and pneumatophores of the mangrove Avicennia marina. Phytochemistry 1981, 20:659-666.
87. Wear D.J., Sullivan M.J., Moore A.D., Millie D.F. Effects of water-column enrichment on the production dynamics of three seagrass species and their epiphytic algae. Marine Ecology Progress Series 1999, 179:201-213.