Differentiation of benthic marine primary producers using stable isotopes and fatty acids: Implications to food web studies

Aquatic Botany

Volumn 93, Issue 2, 2010, Pages 114-122

  Hanson, Christine E ^a,b   Hyndes, Glenn A ^a   Wang, Shao Fang ^c  

^a EDITH COWAN UNIVERSITY   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c Chemistry Centre Western Australia   (Australia)

Author keywords

Fatty acid; Marine macroalgae; Seagrass; South western Australia; Stable isotope; Two dimensional biomarker

Indexed keywords

ALGA; BIOMARKER; CANONICAL ANALYSIS; CARBON ISOTOPE; FATTY ACID; FOOD WEB; ISOTOPIC ANALYSIS; KELP FOREST; MARINE ECOSYSTEM; MULTIVARIATE ANALYSIS; NEARSHORE ENVIRONMENT; NITROGEN ISOTOPE; PERIPHYTON; PHYTOBENTHOS; PRIMARY PRODUCTION; SEAGRASS; STABLE ISOTOPE; VARIANCE ANALYSIS;

AUSTRALIA;

ALGAE; ECKLONIA RADIATA; PHAEOPHYCEAE; RHODOPHYTA;

EID: 77954862110     PISSN: 03043770     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquabot.2010.04.004     Document Type: Article

References (73)

1. Alfaro A.C., Thomas F., Sergent L., Duxbury M. Identification of trophic interactions within an estuarine food web (northern New Zealand) using fatty acid biomarkers and stable isotopes. Estuar. Coast. Shelf Sci. 2006, 70:271-286.
2. Anderson M.J. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 2001, 26:32-46.
3. Anderson M.J., Gorley R.N., Clarke K.R. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods 2008, PRIMER-E, Plymouth, UK.
4. Anderson M.J., Robinson J. Generalized discriminant analysis based on distances. Aust. N. Z. J. Stat. 2003, 45:301-318.
5. Anderson M.J., ter Braak C.J.F. Permutation tests for multi-factorial analysis of variance. J. Stat. Comput. Sim. 2003, 73:85-113.
6. Anderson M.J., Willis T.J. Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 2003, 84:511-525.
7. Auel H., Harjes M., da Rocha R., Stubing D., Hagen W. Lipid biomarkers indicate different ecological niches and trophic relationships of the Arctic hyperiid amphipods Themisto abyssorum and T. libellula. Polar Biol. 2002, 25:374-383.
8. Banaimoon S.A. Fatty acids in marine macroalgae from Southern Yemen (Handramout) including occurrence of eicosatetraenoic (20:4) and eicosapentaenoic (20:5) acids. Bot. Mar. 1992, 35:165-168.
9. Behringer D.C., Butler M.J. Stable isotope analysis of production and trophic relationships in a tropical marine hard-bottom community. Oecologia 2006, 148:334-341.
10. Bell M.V., Batty R.S., Dick J.R., Fretwell K., Navarro J.C., Sargent J.R. Dietary deficiency of docosahexanoid acid impairs vision at low light intensities in juvenile herring (Clupea harengus). Lipids 1995, 30:442-448.
11. Bligh E.G., Dyer W.J. A rapid method for total lipid extraction and purification. Can. J. Biochem. Phys. 1959, 37:911-917.
12. Bode A., Alvarez-Ossorio M.T., Varela M. Phytoplankton and macrophyte contributions to littoral food webs in the Galician upwelling estimated from stable isotopes. Mar. Ecol. Progr. Ser. 2006, 318:89-102.
13. Boutton T.W. Stable carbon isotope ratios of natural materials. I. Sample preparation and mass spectrometric analysis. Carbon Isotope Techniques 1991, 155-171. Academic Press, San Diego. D.C. Coleman, B. Fry (Eds.).
14. Budge S.M., Wooller M.J., Springer A.M., Iverson S.J., McRoy C.P., Divoky G.J. Tracing carbon flow in an arctic marine food web using fatty acid-stable isotope analysis. Oecologia 2008, 157:117-129.
15. Clarke K.R., Gorley R.N. Primer v6: User Manual/Tutorial 2006, PRIMER-E Ltd., Plymouth, UK.
16. Connolly R.M., Hindell J.S., Gorman D. Seagrass and epiphytic algae support nutrition of a fisheries species, Sillago schomburgkii, in adjacent intertidal habitats. Mar. Ecol. Progr. Ser. 2005, 286:69-79.
17. Crawley K.R., Hyndes G.A. The role of different types of detached macrophytes in the food and habitat choice of a surf-zone inhabiting amphipod. Mar. Biol. 2007, 151:1433-1443.
18. Crawley K.R., Hyndes G.A., Ayvazian S.G. Influence of different volumes and types of detached macrophytes on fish community structure in surf zones of sandy beaches. Mar. Ecol. Progr. Ser. 2006, 307:233-246.
19. Crawley K.R., Hyndes G.A., Vanderklift M.A., Revill A.T., Nichols P.D. Allochthonous brown algae are the primary food source for consumers in a temperate, coastal environment. Mar. Ecol. Progr. Ser. 2009, 376:33-44.
20. Dalsgaard J., St John M., Kattner G., Muller-Navarra D., Hagen W. Fatty acid trophic markers in the pelagic marine environment. Adv. Mar. Biol. 2003, 46:225-340.
21. Davenport S.R., Bax N.J. A trophic study of a marine ecosystem off southeastern Australia using stable isotopes of carbon and nitrogen. Can. J. Fish. Aquat. Sci. 2002, 59:514-530.
22. De Angelis L., Rise P., Giavarini F., Galli C., Bolis C.L., Colombo M.L. Marine macroalgae analyzed by mass spectrometry are rich sources of polyunsaturated fatty acids. J. Mass Sp. 2005, 40:1605-1608.
23. DeNiro M.J., Epstein S. Influence of diet on the distribution of carbon isotopes in animals. Geochim. Cosmochim. Acta 1981, 42:495-506.
24. Duffy J.E., Hay M.E. Strong impacts of grazing amphipods on the organization of a benthic community. Ecol. Monogr. 2000, 70:237-263.
25. Firestone D., Horowitz W. IUPAC gas chromatography method for determination of fatty acid composition: collaborative study. J. Assoc. Off. Anal. Chem. 1979, 62:709-721.
26. Graeve M., Hagen W., Kattner G. Herbivorous or omnivorous? On the significance of lipid compositions as trophic markers in Antarctic copepods. Deep-Sea Res. I 1994, 41:915-924.
27. Graeve M., Kattner G., Wiencke C., Karsten U. Fatty acid composition of Arctic and Antarctic macroalgae: indicator of phylogentic and trophic relationship. Mar. Ecol. Progr. Ser. 2002, 231:67-74.
28. Graham M.H., Edwards M.S. Statistical significance versus fit: estimating the importance of individual factors in ecological analysis of variance. Oikos 2001, 93:505-513.
29. Guest M.A., Frusher S.D., Nichols P.D., Johnson C.R., Wheatley K.E. Trophic effects of fishing southern rock lobster Jasus edwardsii shown by combined fatty acid and stable isotope analyses. Mar. Ecol. Progr. Ser. 2009, 388:169-184.
30. Gurr M.I., Harwood J.L., Frayn K.N. Lipid Biochemistry 2002, Blackwell Science, Malden, MA.
31. Hemminga M.A., Mateo M.A. Stable carbon isotopes in seagrasses: variability in ratios and use in ecological studies. Mar. Ecol. Progr. Ser. 1996, 140:285-298.
32. Hudson I.R., Pond D.W., Billett D.S.M., Tyler P.A., Lampitt R.S., Wolff G.A. Temporal variations in fatty acid composition of deep-sea holothurians: evidence of bentho-pelagic coupling. Mar. Ecol. Progr. Ser. 2004, 281:109-120.
33. Hyndes G.A., Lavery P.S. Does transported seagrass provide an important trophic link in unvegetated, nearshore areas?. Estuar. Coast. Shelf Sci. 2005, 63:633-643.
34. 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. Mar. Ecol. Progr. Ser. 2008, 358:103-114.
35. Jennings S., Renones O., MoralesNin B., Polunin N.V.C., Moranta J., Coll J. Spatial variation in the N-15 and C-13 stable isotope composition of plants, invertebrates and fishes on Mediterranean reefs: implications for the study of trophic pathways. Mar. Ecol. Progr. Ser. 1997, 146:109-116.
36. Jennings S., Barnes C., Sweeting C.J., Polunin N.V.C. Application of nitrogen stable isotope analysis in size-based marine food web and macroecological research. Rapid Commun. Mass Sp. 2008, 22:1673-1680.
37. Kanazawa A., Teshima S., Ono K. Relationship between essential fatty acid requirements of aquatic animals and the capacity for bioconversion of linolenic acid to highly unsaturated fatty acids. Comp. Biochem. Phys. B. 1979, 63:295-298.
38. Kelly J.R., Scheibling R.E., Iverson S.J., Gagnon P. Fatty acid profiles in the gonads of the sea urchin Strongylocentrotus droebachiensis on natural algal diets. Mar. Ecol. Progr. Ser. 2008, 373:1-9.
39. Kelly J.R., Scheibling R.E., Iverson S.J. Fatty acids tracers for native and invasive macroalgae in an experimental food web. Mar. Ecol. Progr. Ser. 2009, 391:53-63.
40. 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. Mar. Ecol. Progr. Ser. 2001, 220:103-117.
41. Klumpp D.W., Salita Espinosa J.S., Fortes M.D. The role of epiphytic periphyton and macroinvertebrate grazers in the trophic flux of a tropical seagrass community. Aquat. Bot. 1992, 43:327-349.
42. Kuo J., McComb A. Seagrass taxonomy, structure and development. Biology of Seagrasses: A Treatise on the Biology of Seagrasses with Special Reference to the Australian Region 1989, 6-73. Elsevier, Amsterdam. A.W.D. Larkum, A.J. McComb, S.A. Shepherd (Eds.).
43. Lepoint G., Dauby P., Gobert S. Applications of C and N stable isotopes to ecological and environmental studies in seagrass ecosystems. Mar. Poll. Bull. 2004, 49:887-891.
44. 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. Mar. Biol. 2000, 136:513-518.
45. Lin H.J., Nixon S.W., Taylor D.I., Granger S.L., Buckley B.A. Responses of epiphytes on eelgrass, Zostera marina, to separate and combined nitrogen and phosphorus enrichment. Aquat. Bot. 1996, 52:243-258.
46. Loneragan N.R., Bunn S.E., Kellaway D.M. Are mangroves and seagrasses sources of organic carbon for penaeid prawns in a tropical Australian estuary? A multiple stable-isotope study. Mar. Biol. 1997, 130:289-300.
47. McArdle B.H., Anderson M.J. Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 2001, 82:290-297.
48. 15N along food chains: further evidence and the relation between d15N and animal age. Geochim. Cosmochim. Acta 1984, 48:1135-1140.
49. Nyssen F., Brey T., Dauby P., Graeve M. Trophic position of Antarctic amphipods-enhanced analysis by a 2-dimensional biomarker assay. Mar. Ecol. Progr. Ser. 2005, 300:135-145.
50. Parrish C.C., Abrajano T.A., Budge S.M., Helleur R.J., Hudson E.D., Pulchan K., Ramos C. Lipid and phenolic biomarkers in marine ecosystems: analysis and applications. The Handbook of Environmental Chemistry 2000, 193-233. Springer, Berlin, Germany. P. Wangersky (Ed.).
51. Peterson B.J., Fry B. Stable isotopes in ecosystem studies. Ann. Rev. Ecol. Syst. 1987, 18:293-320.
52. Petursdottir H., Gislason A., Falk-Petersen S., Hop H., Svavarsson J. Trophic interactions of the pelagic ecosystem over the Reykjanes Ridge as evaluated by fatty acid and stable isotope analyses. Deep-Sea Res. Pt. II 2008, 55:83-93.
53. Pinnegar J.K., Polunin N.V.C. Contributions of stable-isotope data to elucidating food webs of Mediterranean rocky littoral fishes. Oecologia 2000, 122:399-409.
54. Polat S., Ozogul Y. Biochemical composition of some red and brown macro algae from the Northeastern Mediterranean Sea. Int. J. Food Sci. Nutr. 2008, 59:566-572.
55. Raven J.A. Inorganic carbon acquisition by marine autotrophs. Adv. Bot. Res. 1997, 27:85-209.
56. Raven J.A., Johnston A.M., Kubler J.E., Korb R., McInroy S.G., Handley L.L., Scrimgeour C.M., Walker D.I., Beardall J., Vanderklift M., Fredriksen S., Dunton K.H. Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Funct. Plant Biol. 2002, 29:355-378.
57. Richoux N.B., Froneman P.W. Trophic ecology of dominant zooplankton and macrofauna in a temperate, oligotrophic South African estuary: a fatty acid approach. Mar. Ecol. Progr. Ser. 2008, 357:121-137.
58. Ruess L., Haggblom M.M., Zapata E.J.G., Dighton J. Fatty acids of fungi and nematodes - possible biomarkers in the soil food chain?. Soil Biol. Biochem. 2002, 34:745-756.
59. Sargent J.R., Parkes R.J., Mueller-Harvey I., Henderson R.J. Lipid biomarkers in marine ecology. Microbes in the Sea 1987, 119-138. Halsted Press, New York. M.A. Sleigh (Ed.).
60. Sargent J.R., Tocher D.R., Bell J.G. The lipids. Fish Nutrition 2002, 182-246. Academic Press, New York. J.E. Halver, R.W. Hardy (Eds.).
61. Sargent J.R., Whittle K.J. Lipids and hydrocarbons in the marine food web. Analysis of Marine Ecosystems 1981, 491-533. Academic Press, New York. A.R. Longhurst (Ed.).
62. Schmidt K., Atkinson A., Petzke K.-J., Voss M., Pond D.W. Protozoans as a food source for Antarctic krill, Euphausia superba: complementary insights from stomach content, fatty acids, and stable isotopes. Limnol. Oceanogr. 2006, 51:2409-2427.
63. 14N isotope ratios in the Southern Benguela Ecosystem: indicators of food web relationships among different size-classes of plankton and pelagic fish; differences between fish muscle and bone collagen tissues. Mar. Ecol. Progr. Ser. 1991, 78:23-31.
64. Smit A.J., Brearley A., Hyndes G.A., Lavery P.S., Walker D.I. Delta N-15 and delta C-13 analysis of a Posidonia sinuosa seagrass bed. Aquat. Bot. 2006, 84:277-282.
65. Thurber A.R. Diets of Antarctic sponges: links between the pelagic microbial loop and benthic metazoan food web. Mar. Ecol. Progr. Ser. 2007, 351:77-89.
66. Vander Zanden M.J., Rasmussen J.B. Variation in d15N and d13C trophic fractionation: implications for aquatic food web studies. Limnol. Oceanogr. 2001, 46:2061-2066.
67. Vanderklift M.A., Kendrick G.A. Contrasting influence of sea urchins on attached an drift macroalgae. Mar. Ecol. Progr. Ser. 2005, 299:101-110.
68. Vanderklift M.A., Kendrick G.A., Smit A.J. Differences in trophic position among sympatric sea urchin species. Estuar. Coast. Shelf Sci. 2006, 66:291-297.
69. Vizzini S., Mazzola A. Seasonal variations in the stable carbon and nitrogen isotope ratios (C-13/C-12 and N-15/N-14) of primary producers and consumers in a western Mediterranean coastal lagoon. Mar. Biol. 2003, 142:1009-1018.
70. Vizzini S., Sara G., Michener R.H., Mazzola A. The role and contribution of the seagrass Posidonia oceanica (L.) Delile organic matter for secondary consumers as revealed by carbon and nitrogen stable isotope analysis. Acta Oecol. 2002, 23:277-285.
71. Wakefield R.L., Murray S.N. Factors influencing food choice by the seaweed-eating marine snail Norrisia norrisi (Trochidae). Mar. Biol. 1998, 130:631-642.
72. Wernberg T., Kendrick G.A., Phillips J.C. Regional differences in kelp-associated algal assemblages on temperate limestone reefs in south-western Australia. Divers. Distrib. 2003, 9:427-441.
73. Wernberg T., Vanderklift M.A., How J., Lavery P.S. Export of detached macroalgae from reefs to adjacent seagrass beds. Oecologia 2006, 147:692-701.