Stable carbon isotopes in seagrasses: Variability in ratios and use in ecological studies

Marine Ecology Progress Series

Volumn 140, Issue 1-3, 1996, Pages 285-298

  Hemminga, M A ^a   Mateo, M A ^a  

^a NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

Author keywords

Isotope signatures; Seagrasses; Stable carbon isotopes; Variability

Indexed keywords

HALOPHILA;

CARBON ISOTOPE RATIO; CARBON ISOTOPES; ISOTOPE SIGNATURE; ISOTOPE SIGNATURES; SEAGRASS; VARIABILITY;

EID: 0029664139     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps140285     Document Type: Review

References (128)

1. Abal EG, Loneragan N, Bowen P, Perry CJ, Udy JW, Dennison WC (1994) Physiological and morphological responses of the seagrass Zostera capricorni Aschers to light intensity. J Exp Mar Biol Ecol 178:113-129
2. Abel KM (1984) Inorganic carbon source for photosynthesis in the seagrass Thalassia hemprichii (Ehrenb) Aschers. Plant Physiol 76:776-781
3. Abel KM, Drew EA (1989) Carbon metabolism. In: Larkum AWD, McComb AJ, Shepherd SA (eds) Biology of seagrasses. Elsevier, Amsterdam, p 760-796
4. Agami M, Waisel Y (1986) The ecophysiology of roots of submerged vascular plants. Physiol Vég 24:607-624
5. Andrews TJ, Abel KM (1979) Photosynthetic carbon metabolism in seagrasses. Plant Physiol 63:650-656
6. Beer S (1989) Photosynthesis and photorespiration of marine angiosperms. Aquat Bot 34:153-166
7. Beer S, Eshel A, Waisel Y (1977) Carbon metabolism in seagrasses I. The utilization of exogenous inorganic carbon species in photosynthesis. J Exp Bot 28:1180-1189
8. Beer S, Eshel A, Waisel Y (1980b) Carbon metabolism in seagrasses III. Activities of carbon-fixing enzymes in relation to internal salt concentrations. J Exp Bot 31:1027-1033
9. 2 incorporation. J Exp Bot 31:1019-1026
10. Beer S, Waisel Y (1979) Some photosynthetic carbon fixation properties of seagrasses. Aquat Bot 7:129-138
11. Beer S, Wetzel RG (1982) Photosynthetic carbon fixation pathways in Zostera marina and three Florida seagrasses. Aquat Bot 13:141-146
12. Bell JD, Pollard DA (1989) Ecology of fish assemblages and fisheries associated with seagrasses. In: Larkum AWD, McComb AJ, Shepherd SA (eds) Biology of seagrasses. Elsevier, Amsterdam, p 565-597
13. Benedict CR, Scott JR (1976) Photosynthetic carbon metabolism of a marine grass. Plant Physiol 57:876-880
14. Benedict CR, Wong WWL, Wong JHH (1980) Fractionation of the stable isotopes of inorganic carbon by seagrasses. Plant Physiol 65:512-517
15. 13C values in marine organisms from the Great Barrier Reef. Aust J Plant Physiol 3: 25-32
16. Bodner M (1994) Inorganic carbon source for photosynthesis in the aquatic macrophytes Potamogeton natans and Ranunculus fluitans. Aquat Bot 48:109-120
17. Boon PI, Bunn SE (1994) Variations in the stable isotope composition of aquatic plants and their implications for food web analysis. Aquat Bot 48:99-108
18. Boudouresque CF, Crouzet A, Pergent G (1983) Un nouvel outil au service de l'étude des herbiers à Posidonia oceanica: la lépidochronologie. Rapp PV Réun Comm Int Explor Sci Médit, Monaco 28:111-112
19. 14C the undersea beds of dead Posidonia oceanica in the bay of Port-Man (Port-Cros, Var, France). Trav Sci Parc Natl Port-Cros Fr 6: 239-242
20. Boutton TW (1991) Stable carbon isotope ratios of natural materials II: Atmospheric, terrestrial, marine, and freshwater environments. In: Coleman DC, Fry B (eds) Carbon isotope techniques. Academic Press, San Diego, p 137-186
21. Clough BF, Attiwill PM (1980) Primary productivity in Zostera muelleri Irmisch. ex Aschers in Westernport Bay (Victoria, Australia). Aquat Bot 9:1-13
22. Cooper LW (1989) Patterns of carbon isotopic variability in eelgrass, Zostera marina L. from Izembek lagoon, Alaska. Aquat Bot 34:329-339
23. Cooper LW, DeNiro MJ (1989) Stable carbon isotope variability in the seagrass Posidonia oceanica: evidence for light intensity effects. Mar Ecol Prog Ser 50:225-229
24. Cooper LW, McRoy CP (1988) Stable carbon isotope ratio variations in marine macrophytes along intertidal gradients. Oecologia 77:238-241
25. Cosper E (1982) Influence of light intensity on diel variations in growth, respiration and organic release of a marine diatom: comparison of diurnally constant and fluctuating light. J Plankton Res 4:705-724
26. Craig H (1953) The geochemistry of the stable carbon isotopes. Geochim Cosmochim Acta 3:53-92
27. Craig H (1954) Carbon-13 in plants and the relationship between carbon-13 and carbon-14 variations in nature. J Geol 62:115-149
28. Dainty J (1963) Water relations of plant cells. In: Preston RD (ed) Advances in botanical research. Academic Press, London, p 276-326
29. Den Hartog C (1970) The seagrasses of the world. North-Holland Publ, Amsterdam
30. Descolas-Gros C, Oriol L (1992) Variations in carboxylase activity in marine phytoplankton cultures, β-carboxylation in carbon flux studies. Mar Ecol Prog Ser 85:163-169
31. 13C values of three seagrasses from the great barrier reef. Aust J Plant Physiol 3:9-23
32. Dring MJ (1982) The biology of marine plants. Cambridge University Press, Cambridge
33. Duarte CM, Marbá N, Agawin N, Cebrián J, Enríquez S, Fortes MD, Gallegos ME, Mérino M, Olesen B, Sand-Jensen K, Uri J, Vermaat J (1994) Reconstruction of seagrass dynamics: age determinations and associated tools for the seagrass ecologist. Mar Ecol Prog Ser 107:195-209
34. - in Thalassia testudinum (Hydrocharitaceae). Mar Biol 115:373-380
35. Durako MJ, Hall MO (1992) Effects of light on the stable carbon isotope composition of the seagrass Thalassia testudinum. Mar Ecol Prog Ser 86:99-101
36. Durako MJ, Sackett WM (1991) Influence of the carbon source on the stable carbon isotopic composition of the seagrass Thalassia testudinum. In: Flitton S (ed) Stable isotopes in plant nutrition, soil fertility and environmental studies. International Atomic Energy Agency, Vienna, p 453-462
37. 2(aq) on the carbon isotopic composition of the seagrass Thalassia testudinum Banks ex König (Hydrocharitaceae). J Exp Mar Biol Ecol 169:167-180
38. Ehleringer JR, Osmond CB (1989) Stable isotopes. In: Pearcy RW, Ehleringer JR, Mooney HA, Rundel PW (eds) Plant physiological ecology. Chapman & Hall, London, p 281-300
39. Enoch HZ, Olesen JM (1993) Plant response to irrigation with water enriched with carbon dioxide. New Phytol 125: 249-258
40. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Ann Rev Plant Physiol Plant Mol Biol 40:503-537
41. Farquhar GD, O'Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9:121-137
42. Fischer G, Wiencke C (1989) Stable carbon isotopes in organic matter from benthic marine macroalgae (Antarctica): evidence of light intensity effects. J Mar Biol Ass UK 69:7321
43. Fleming M, Lin G, Sternberg L (1990) Influence of mangrove detritus in an estuarine ecosystem. Bull Mar Sci 47: 663-669
44. France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Mar Ecol Prog Ser 124:307-312
45. Fry B (1977) Stable carbon isotope ratios: a tool for tracing food chains. MA thesis, University of Texas, Austin
46. 12C ratios and the trophic importance of algae in Florida Syringodium filiforme seagrass meadows. Mar Biol 79:11-19
47. 12C comparison of food webs in Caribbean seagrass meadows and coral reefs. Aquat Bot 14:389-398
48. 13C evidence for the importance of benthic plants. Estuar Coast Mar Sci 8:499-509
49. 12C ratios in marine food webs of the Torres Strait, Queensland. Aust J Mar Freshwater Res 34:707-715
50. Grice AM, Loneragan NR, Dennison WC (1996) Light intensity and the interactions between physiology, morphology and stable isotope ratios in five species of seagrass. J Exp Mar Biol Ecol 195:91-110
51. Guy RD, Fogel MF, Berry, JA, Hoering TC (1987) Isotope fractionation during oxygen production and consumption by plants. In: Biggins J (ed) Progress in photosynthetic research III. Martinus Nijhoff, Dordrecht, p 597-600
52. Guy RD, Vanderberghe GC, Turpin DH (1989) Significance of phosphoenolpyruvate carboxylase during ammonium assimilation. Plant Physiol 89:1150-1157
53. Haines EB (1976a) Stable carbon isotope ratios in the biota, soils and tidal water of a Georgia salt marsh. Estuar Coast Mar Sci 4:609-616
54. Haines EB (1976b) Relation between stable isotope composition of fiddler crabs, plants and soils in a salt marsh. Limnol Oceanogr 21:880-883
55. Harlin MM, Thorne-Miller B, Boothroyd JC (1982) Seagrass-sediment dynamics of a flood-tidal delta in Rhode Island (U.S.A.). Aquat Bot 14:127-138
56. Harrigan P, Zieman JC, Macko SA (1989) The base of nutritional support for the gray snapper (Lutjanus griseus): an evaluation based on a combined stomach content and stable isotope analysis. Bull Mar Sci 44:65-77
57. Heck Jr KL, Able KW, Roman CT, Fahay MP (1995) Composition, abundance, biomass, and production of macrofauna in a New England estuary: comparisons among eelgrass meadows and other nursery habitats. Estuaries 18: 379-389
58. 13C. Mar Ecol Prog Ser 130:169-178
59. Hemminga MA, Nieuwenhuize J (1990) Seagrass wrack-induced dune formation on a tropical coast (Bane d'Arguin, Mauritania). Estuar Coast Shelf Sci 31:499-502
60. Hemminga MA, Slim FJ, Kazungu J, Ganssen GM, Nieuwenhuize J, Kruyt NM (1994) Carbon outwelling from a mangrove forest with adjacent beds and coral reefs (Gazi Bay, Kenya). Mar Ecol Prog Ser 106:291-301
61. Howard RK, Edgar GJ, Hutchings PA (1989) Faunal assemblages of seagrass beds. In: Larkum AWD, McComb AJ, Shepherd SA (eds) Biology of seagrasses. Elsevier, Amsterdam, p 536-564
62. IUPAC (1994) Atomic weights of the elements 1993. Pure Appl Chem 66:2423-2444
63. 2 via its roots. Nature 310:694-695
64. Keeley JE, Sandquist DR (1992) Carbon: freshwater plants. Plant Cell Environ 15:1021-1035
65. 2 in the world oceans. Deep Sea Res 32(1):57-84
66. Kübier JE, Raven JA (1994) Consequences of light limitation for carbon acquisition in three rhodophytes. Mar Ecol Prog Ser 110:203-209
67. Kübler JE, Raven JA (1995) The interaction between inorganic carbon acquisition and light supply in Palmaria palmata (Rhodophyta). J Phycol 31:369-375
68. Kuo J, McComb AJ (1989) Seagrass taxonomy, structure and development. In: Larkum AWD, McComb AJ, Shepherd SA (eds) Biology of seagrasses. Elsevier, Amsterdam, p 6-73
69. Lajtha K, Marshall JD (1994) Sources of variation in the stable isotopic composition of plants. In: Lajtha K, Michener RH (eds) Stable isotopes in ecology and environmental science. Blackwell, London, p 1-21
70. Larkum AWD, Roberts G, Kuo J, Strother S (1989b) Gaseous movements in seagrasses. In: Larkum AWD, McComb AJ, Shepherd SA (eds) Biology of seagrasses. Elsevier, Amsterdam, p 686-722
71. 2 gas exchange of two intertidal seagrass species, Zostera marina L. and Zostera noltii Hornem., during emersion. Aquat Bot 45:53-62
72. Limnology & Oceanography (1995). New manuscript guidelines for the reporting of stable hydrogen, carbon, and oxygen isotope-ratio data. Limnol Oceanogr 40(6):1182
73. 13C values for the seagrass Thalassia testudinum and its relations to mangrove carbon. Aquat Bot 40:333-341
74. 13C by marine plants. Oecologia 91: 481-492
75. Mateo MA, Romero J, Pérez Littler M, Littler, D (1996) Dynamics of millenary organic deposits resulting from the growth of the Mediterranean seagrass Posidonia oceanica. Estuar Coast Shelf Sci (in press)
76. 13C label identifies eelgrass (Zostera marina) carbon in an Alaskan estuarine food web. Mar Biol 53:263-269
77. 12C ratios in seagrasses. Aquat Bot 9:237-249
78. Millhouse J, Strother S (1986) The effect of pH on the inorganic carbon source for photosynthesis in the seagrass Zostera muelleri Irmisch ex Aschers. Aquat Bot 24: 199-209
79. Mook WG, Bommerson JC, Staverman WH (1974) Carbon isotope fractionation between dissolved bicarbonate and gaseous carbon dioxide. Earth Planet Sci Lett 22:169-176
80. 13C method of estimation of carbon allocation to roots in a young chestnut coppice. Plant Cell Environ 9:735-739
81. 14C) isotope methods. J Plankton Res 17:1449-1460
82. O'Leary MH, Reife JE, Slater JD (1981) Kinetic and isotope effect studies of maize phosphoenolpyruvate carboxylase. Biochemistry 20:7308-7314
83. Parker PL (1964) The biogeochemistry of the stable isotopes of carbon in a marine bay. Geochim Cosmochim Acta 28: 1155-1164
84. Parker PL (1976) Stable carbon isotope ratios of food webs and biogeochemical cycles in seagrass systems. Progress Report to the International Decade of Ocean Exploration: Seagrass Two Progress Report, Seagrass Ecosystem Study, Washington, DC, p 43-49
85. Pedersen O, Sand-Jensen K (1993) Water transport in submerged macrophytes. Aquat Bot 44:385-406
86. Pergent-Martini C, Pergent G (1994) Lepidochronological analysis in the Mediterranean seagrass Posidonia oceanica: state-of-the-art and future developments. Oceanol Acta 17:673-681
87. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Ann Rev Ecol Syst 18:293-320
88. Peterson BJ, Howarth RW (1987) Sulfur, carbon, and nitrogen isotopes used to trace organic matter flow in the salt-marsh estuaries of Sapelo Island, Georgia. Limnol Oceanogr 35:1195-1213
89. Prins HBA, Elzenga JTM (1989) Bicarbonate utilization: function and mechanism. Aquat Bot 34:59-83
90. Rao RG, Woitchik AF, Goeyens L, Van Riet A, Kazungu J, Dehairs F (1994) Carbon, nitrogen contents and stable carbon isotope abundance in mangrove leaves from an East African coastal lagoon (Kenya). Aquat Bot 47:175-183
91. 2 and productivity in past oceans. Nature 341:516-518
92. Raven JA (1992) Present and potential uses of the natural abundance of stable isotopes in plant science, with illustrations from the marine environment. Plant Cell Environ 15:1083-1091
93. Raven JA, Johnston AM (1991) Mechanisms of inorganic-carbon acquisition in marine phytoplankton and their implications for the use of other resources. Limnol Oceanogr 36: 1701-1714
94. Raven JA, Johnston AM, MacFarlane JJ (1990) Carbon metabolism. In: Cole KM, Sheath RG (eds) The biology of the red algae. Cambridge University Press, New York, p 171-202
95. Raven JA, Lucas WJ (1985) Energy costs of carbon acquisition In: Lucas WJ, Berry JA (eds) Inorganic carbon uptake by aquatic photosynthetic organisms. Am Soc Plant Physiol, Rockville, MD, p 305-325
96. 13C natural abundance measurements for photosynthetic performance by marine macrophytes in their natural environment. Mar Ecol Prog Ser 123:193-205
97. Rezende CE, Lacerda LD, Ovalle ARC, Silva CAR, Martinelli LA (1990) Nature of POC transport in a mangrove ecosystem: a carbon stable isotopic study. Estuar Coast Shelf Sci 30:641-645
98. Richardson K, Griffiths H, Reed ML, Raven JA, Griffiths NM (1984) Inorganic carbon assimilation in the isoetids, Isoetes lacustris L. and Lobelia dortmanna L. Oecologia 61:115-121
99. Rodelli MR, Gearing JN, Gearing PJ, Marshall N, Sasekumar A (1984) Stable isotope ratio as a tracer of mangrove carbon in Malaysian ecosystems. Oecologia 61:326-333
100. Roeske CA, O'Leary MH (1984) Carbon isotope effects on the enzyme-catalyzed carboxylation of ribulose biphosphate. Biochemisty 23:6275-6284
101. Romero J, Pérez M, Mateo MA, Sala E (1994) The below-ground organs of the Mediterranean seagrass Posidonia oceanica as a biogeochemical sink. Aquat Bot 47:13-19
102. 2. Mar Biol 80:247-253
103. 2 concentrations during growth. Oecologia 70:426-432
104. Sand-Jensen K, Pedersen MF, Nielsen SL (1992) Photosynthetic use of inorganic carbon among primary and secondary plants in streams. Freshwater Biol 27:283-293
105. Sand-Jensen K, Revsbech NP, Jorgensen BB (1985) Microprofiles of oxygen in epiphyte communities on submerged macrophytes. Mar Biol 89:55-62
106. Scoffin TP (1970) The trapping and binding of subtidal carbonate sediments by marine vegetation in Bimini Lagoon, Bahamas. J Sediment Petrol 40:249-273
107. 2 concentrating mechanism In: Lucas WJ, Berry JA (eds) Inoorganic carbon uptake by aquatic photosynthetic organisms. Am Soc Plant Physiol, Rockville, MD, p 389-401
108. 13C evidence of the origins and fates of organic carbon in estuarine and nearshore food webs. Mar Ecol Prog Ser 22:141-152
109. 14C uptake by marine phytoplankton. J Plankton Res 6:249-257
110. 12C ratios for higher plants. Plant Physiol 47:380-384
111. 12C ratios in plant tissues. Bot Gaz 137:99-104
112. - and to carbon isotopic discrimination. New Phytol 86:245-259
113. Stephenson LR, Tan FC, Mann KH (1984) Stable carbon isotope variability in marine macrophytes and its implications for food web studies. Mar Biol 81:223-230
114. Stephenson LR, Tan FC, Mann KH (1986) Use of stable carbon isotope ratios to compare plant material and potential consumers in a seagrass bed and a kelp bed in Nova Scotia, Canada. Mar Ecol Prog Ser 30:1-7
115. Sternberg LSL, DeNiro MJ, McJunkin D, Berger R, Keeley JE (1985) Carbon, oxygen and hydrogen isotope abundances in Stylites reflect its unique physiology. Oecologia 67:598-600
116. Surif MB, Raven JA (1990) Photosynthetic gas exchange under emersed conditions in eulittoral and normally submersed members of the Fucales and the Laminariales: interpretation in relation to C isotope and N and water use efficiency. Oecologia 82:68-80
117. Svejcar TJ, Boutton TW, Trent JD (1990) Assessment of carbon allocation with stable carbon isotope labeling. Agron J 82:18-21
118. Thayer GW, Parker PL, Croix MWL, Fry B (1978) The stable carbon isotope ratio of some components of an eelgrass, Zostera marina, bed. Oecologia 35:1-12
119. Thompson PA, Calvert SE (1994) Carbon-isotope fractionation by a marine diatom: the influence of irradiance, daylength, pH and nitrogen source. Limnol Oceanogr 39: 1835-1844
120. Thompson PA, Calvert SE (1995) Carbon isotope fractionation by Emiliania huxleyi. Limnol Oceanogr 40:673-679
121. Tomlinson PB (1974) Vegetative morphology and meristem dependence. The foundation of productivity in seagrasses. Aquaculture 4:107-130
122. Wefer G, Killingley JS (1986) Carbon isotopes in organic matter from a benthic alga Halimeda incrassata (Bermuda): effects of light intensity. Chem Geol (Isotope Geosciences Section) 59:321-326
123. Wetzel RG, Pennale PA (1979) Transport of carbon and excretion of dissolved organic carbon by leaves and roots/rhizomes in seagrasses and their epiphytes. Aquat Bot 6: 149-158
124. Wheeler WN (1980) Effect of boundary layer transport on the fixation of carbon by the giant kelp Macrocystis pyrifera. Mar Biol 56:103-110
125. Wiencke C, Fischer G (1990) Growth and stable carbon isotope composition of cold-water macroalgae in relation to light and temperature. Mar Ecol Prog Ser 65:283-292
126. Yamamuro M, Kayanne H, Minagawa M (1995) Carbon and nitrogen stable isotopes of primary producers in coral reef ecosystems. Limnol Oceanogr 40:617-621
127. Zhang JA, Quay PD, Wilber DO (1995) Carbon isotope fractionation during gas-water exchange and dissolution. Geochim Cosmochim Acta 59:107-114
128. Zieman JC, Macko SA, Mills AL (1984) Role of seagrasses and mangroves in estuarine food webs: temporal and spatial changes in stable isotope composition and amino acid content during decomposition. Bull Mar Sci 35:380-392