Marine Biology

, Volume 151, Issue 5, pp 1773–1784 | Cite as

Diet induced differences in carbon isotope fractionation between sirenians and terrestrial ungulates

  • Mark T. ClementzEmail author
  • Paul L. Koch
  • Cathy A. Beck
Research Article


Carbon isotope differences (Δ13C) between bioapatite and diet, collagen and diet, and bioapatite and collagen were calculated for four species of sirenians, Dugong dugon (Müller), Trichechus manatus (Linnaeus), Trichechus inunguis (Natterer), and the extinct Hydrodamalis gigas (Zimmerman). Bone and tooth samples were taken from archived materials collected from populations during the mid eighteenth century (H. gigas), between 1978 and 1984 (T. manatus, T. inunguis), and between 1997 and 1999 (D. dugon). Mean Δ13C values were compared with those for terrestrial ungulates, carnivores, and six species of carnivorous marine mammals (cetaceans = 1; pinnipeds = 4; mustelids = 1). Significant differences in mean δ13C values among species for all tissue types were detected that separated species or populations foraging on freshwater plants or attached marine macroalgae (δ13C values < −6‰; Δ13Cbioapatite–diet ∼14‰) from those feeding on marine seagrasses (δ13C values > −4‰; Δ13Cbioapatite–diet ∼11‰). Likewise, Δ13Cbioapatite–collagen values for freshwater and algal-foraging species (∼7‰) were greater than those for seagrass-foraging species (∼5‰). Variation in Δ13C values calculated between tissues and between tissues and diet among species may relate to the nutritional composition of a species’ diet and the extent and type of microbial fermentation that occurs during digestion of different types of plants. These results highlight the complications that can arise when making dietary interpretations without having first determined species-specific Δ13Ctissue–diet values.


Marine Mammal Stomach Content Analysis Harbor Porpoise Terrestrial Carnivore Marine Herbivore 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank the following people for providing tooth and bone material from sirenian and other marine mammal specimens: Donna Kwan and Helene Marsh from James Cook University, Queensland, Australia; Daryl Domning from Howard University, Washington, D.C.; Bruce MacFadden, Pennilynn Higgins, Candace McCaffrey and Laurie Wilkins from the Florida Museum of Natural History, Vertebrate Paleontology and Mammal Collections; Charley Potter and James Mead from the Smithsonian Natural History Museum Washington, D.C.; John Heyning and David Janiger, Los Angeles Co. Museum of Natural History; Doug Long, California Academy of Sciences; Amanda Toperoff and Robert Burton, Moss Landing Marine Laboratory; and the California Department of Fish and Game. We also thank James Estes, Terrie Williams, and Dan Costa for providing information on marine mammal foraging strategies and physiology. Financial support for this research was provided by NSF grant EAR 0087742 to PLK. Funding for MTC was provided by an NSF Predoctoral Fellowship and an Achievement Rewards for College Scientists (ARCS) Fellowship.

Supplementary material

227_2007_616_MOESM1_ESM.doc (54 kb)
Appendix 1. Mean bioapatite, collagen, and diet d13C values; mean D13C values between tissues and diet; and mean D13C values between tissues for all marine mammals analyzed. Within the latter, letters (A-D) following the means identify statistically distinct groupings (post-hoc Bonferroni test, p < 0.05). For diet category, SG = seagrass; MA = marine algae; FW = freshwater plants; TV = terrestrial/marsh vegetation; F = fish; MI = marine invertebrates (DOC 53.5 kb)
227_2007_616_MOESM2_ESM.doc (28 kb)
Appendix 2. Range (%) in total dietary fiber (TDF) content and fiber composition reported for various food plants of sirenians (Jung and Koong 1985a; Dawes 1986b; Nunez-Hernandez et al. 1991c; Applegate and Gray 1995d; Castro-Diez et al. 1997e; Chan et al. 1997f; Wenninger and Shipley 2000g; Nigam 2002h; Burtin 2003i; Fields et al. 2003j). For marine macroalgae, total dietary fiber includes polysaccharides other than cellulose, hemicellulose, and lignin that are not present in vascular plants and are typically indigestible by the stomach and intestinal bacteria of most mammals (DOC 28.5 kb)


  1. Ambrose SH, Norr L (1993) Experimental evidence for the carbon isotope ratios of whole diet and dietary protein to those of bone collagen and carbonate. In: Lambert JB, Grupe G (eds) Prehistoric human bone: archaeology at the molecular level. Springer, Heidelberg, pp 1–37Google Scholar
  2. Ames A, Van Vleet ES, Sackett WM (1996) The use of stable carbon isotope analysis for determining dietary habits of the Florida manatee, Trichechus manatus latirostris. Mar Mamm Sci 12:555–563CrossRefGoogle Scholar
  3. Anderson WT, Fourqurean JW (2003) Intra- and interannual variability in seagrass carbon and nitrogen stable isotope values from south Florida, a preliminary study. Org Geochem 34(2):185–194CrossRefGoogle Scholar
  4. André J, Guyuris E, Lawler IR (2005) Comparison of the diets of sympatric dugongs and green turtles on the Orman Reefs, Torres Strait, Australia. Wildl Res 32:53–62CrossRefGoogle Scholar
  5. Applegate RD, Gray PB (1995) Nutritional value of seaweed to ruminants. Rangifer 15:15–18CrossRefGoogle Scholar
  6. Benner R, Fogel ML, Sprague EK, Hodson RE (1987) Deplection of 13C in lignin and its implication for stable carbon isotope studies. Nature 329:708–710CrossRefGoogle Scholar
  7. Best RC (1981) Foods and feeding habits of wild and captive sirenia. Mamm Rev 11:3–29CrossRefGoogle Scholar
  8. Boon PL, Bunn SE (1994) Variations in the stable isotope composition of aquatic plants and their implications for food web analysis. Aquat Bot 48:99–108CrossRefGoogle Scholar
  9. Brandt JF (1846) Contributions to sirenology, being principally an illustrated natural history of Rhytina. Acad Imp Sci St Petersbourg Mem 7:1–160Google Scholar
  10. Bunn SE, Boon PI (1993) What sources of organic carbon drive food webs in billabongs? A study based on stable isotope analysis. Oecologia 96:85–94CrossRefGoogle Scholar
  11. Burn DM (1986) The digestive strategy and efficiency of the West Indian Manatee, Trichechus manatus. Comp Biochem Physiol A: Physiol 85A:139–142CrossRefGoogle Scholar
  12. Burtin P (2003) Nutritional value of seaweeds. Electronic Journal of Environmental, Agricultural and Food Chemistry. ISSN: 1579–4377. Cited 10 Jan 2006
  13. Castro-Diez P, Villar-Salvador P, Perez-Rontome C, Maestro-Martinez M, Montserrat-Marti G (1997) Leaf morphology and leaf chemical composition in three Quercus (Fagaceae) species along a rainfall gradient in NE Spain. Trees 11:127–134Google Scholar
  14. Cerling TE, Harris JM (1999) Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implications for ecological and paleoecological studies. Oecologia 120:347–363CrossRefGoogle Scholar
  15. Chan JC-C, Cheung PC-K, Ang PO Jr (1997) Comparative studies on the effect of three drying methods on the nutritional composition of seaweed Sargassum hemiphyllum (Turn.) C. Ag J Agric Food Chem 45:3056–3059CrossRefGoogle Scholar
  16. Chanton J, Lewis FG (2002) Examination of coupling between primary and secondary production in a river-dominated estuary: Apalachicola Bay, Florida, U.S.A. Limnol Oceanogr 47:683–697CrossRefGoogle Scholar
  17. Clementz MT, Koch PL (2001) Differentiating aquatic mammal habitat and foraging ecology with stable isotopes in tooth enamel. Oecologia 129:461–472CrossRefGoogle Scholar
  18. Dawes C (1986) Seasonal proximate constituents and caloric values in seagrasses and algae on the west coast of Florida. J Coast Res 2:25–32Google Scholar
  19. Domning DP (1978) Sirenian evolution in the North Pacific Ocean. Univ Calif Publ Geol Sci 118:1–176Google Scholar
  20. Domning DP, Hayek LC (1984) Horizontal tooth replacement in the Amazonian manatee. Mammalia 48:105–127CrossRefGoogle Scholar
  21. Fellerhoff C, Voss M, Wantzen KM (2003) Stable carbon and nitrogen isotope signatures of decomposing tropical macrophytes. Aquat Ecol 37:361–375CrossRefGoogle Scholar
  22. Fields JR, Simpson TR, Manning RW, Rose FL (2003) Food habits and selective foraging by the Texas river cooter (Pseudemys texana) in Spring Lake, Hays County, Texas. J Herp 37:726–729CrossRefGoogle Scholar
  23. Fry B (1984) 13C/12C ratios and the trophic importance of algae in Florida Syringodium filiforme seagrass meadows. Mar Biol 79:11–19CrossRefGoogle Scholar
  24. Fry B, Scalan RS, Parker PL (1983) 13C/12C ratios in marine food webs of the Torres Strait, Queensland. Aust J Mar Freshw Res 34:707–715CrossRefGoogle Scholar
  25. Goto M et al (2004) Effects of age, body size and season on the food consumption and digestion of captive dugongs (Dugong dugon). Mar Freshw Behav Physiol 37:89–97CrossRefGoogle Scholar
  26. Hall MO, Eiseman NJ (1981) The seagrass epiphytes of the Indian River, Florida I. Species list with descriptions and seasonal occurrences. Bot Mar 24:139–146Google Scholar
  27. Hedges REM (2003) On bone collagen—apatite–carbonate isotopic relationships. Int J Osteoarchaeol 13:66–79CrossRefGoogle Scholar
  28. Hemminga MA, Mateo MA (1996) Stable carbon isotope values in seagrasses: variability in ratios and use in ecological studes. Mar Ecol Prog Ser 140:285–298CrossRefGoogle Scholar
  29. Hobson KA, Piatt JF, Pitocchelli J (1994) Using stable isotopes to determine seabird trophic relationships. J Anim Ecol 63:786–798CrossRefGoogle Scholar
  30. Husar SL (1978) Dugong dugon. Mammal Species 88:1–7Google Scholar
  31. Irvine AB (1983) Manatee metabolism and its influence on distribution in Florida. Biol Conserv 25:315–334CrossRefGoogle Scholar
  32. Jensen PR, Gibson RA (1986) Primary production in three subtropical seagrass communities: a comparison of four autotrophic components. Fla Sci 49:129–141Google Scholar
  33. Jensen BB, Jorgensen H (1994) Effect of dietary fiber on microbial activity and microbial gas production in various regions of the gastrointestinal tract of pigs. Appl Environ Microbiol 60:1897–1904PubMedPubMedCentralGoogle Scholar
  34. Jim S (2000) The development of bone cholesterol δ13C values as a new source of palaeodietary information: qualitative and quantitative models of its use in conjunction with bone collagen and apatite δ13C values. PhD dissertation, University of BristolGoogle Scholar
  35. Jim S, Ambrose SH, Evershed RP (2004) Stable carbon isotopic evidence for differences in the dietary origin of bone cholesterol, collagen and apatite: implications for their use in paleodietary reconstruction. Geochim Cosmochim Acta 68:61–72CrossRefGoogle Scholar
  36. Jung HG, Koong LJ (1985) Effects of hunger satiation on diet quality by grazing sheep. J Range Manag 38:302–305CrossRefGoogle Scholar
  37. Kleiber M (1975) The fire of life. Krieger, New YorkGoogle Scholar
  38. Koch PL, Tuross N, Fogel ML (1997) The effects of sample treatment and diagenesis on the isotopic integrity of carbonate in biogenic hydroxylapatite. J Archaeol Sci 24:417–429CrossRefGoogle Scholar
  39. Krueger HW, Sullivan CH (1984) Models for carbon isotope fractionation between diet and bone. In: Turnlund JF, Johnson PE (eds) Stable isotopes in nutrition. ACS Symposium Series 258. American Chemical Society, Washington, pp 205–222CrossRefGoogle Scholar
  40. Kwan D (2002) Towards a sustainable indigenous fishery for dugongs in Torres Strait: a contribution of empirical data and process. PhD Thesis, James Cook UniversityGoogle Scholar
  41. Ledder DA (1986) Food habits of the West Indian Manatee, Trichechus manatus latirostris, in South Florida. M.S. thesis, University of Miami, Coral Gables, p 114Google Scholar
  42. Lee-Thorp JA, van der Merwe NJ (1987) Carbon isotope analysis of fossil bone apatite. S Afr J Sci 27:361–372Google Scholar
  43. Lee-Thorp JA, Sealy JC, van der Merwe NJ (1989) Stable carbon isotope ratio differences between bone collagen and bone apatite, and their relationship to diet. J Archaeol Sci 16:585–599CrossRefGoogle Scholar
  44. Loader NJ, Robertson I, McCarroll D (2003) Comparison of stable isotope ratios in the whole wood, cellulose and lignin of oak tree-rings. Palaeogeogr Palaeoclimatol Palaeoecol 196:395–407CrossRefGoogle Scholar
  45. Loneragan NR, Bunn SE, Kellaway DM (1997) Are mangroves and seagrasses sources of organic carbon for penaeid prawns in a tropical Australian estuary? A multiple stable-isotope study. Mar Biol (Berlin) 130:289–300CrossRefGoogle Scholar
  46. MacFadden BJ, Higgins P, Clementz MT, Jones DS (2004) Diets, habitat preferences, and niche differentiation of Cenozoic sirenians from Florida: evidence from stable isotopes. Paleobiology 30:297–324CrossRefGoogle Scholar
  47. Marsh H, Channells PW, Heinsohn GE, Morrissey J (1982) Analysis of the stomach contents of dugongs from Queensland. Aus Wild Res 9:55–67CrossRefGoogle Scholar
  48. Marsh H, Spain AV, Heinsohn GE (1978) Physiology of the Dugong. Comp Biochem Physiol A 61A:159–168CrossRefGoogle Scholar
  49. Medina E, Martinelli LA, Barbosa E, Victoria RL (1999) Natural abundance of 13C in tropical grasses from the INPA, Instituto Nacional de Pesquisas da Amazonia, herbarium. Rev Bras Bot 22:1–15CrossRefGoogle Scholar
  50. Metges C, Kempe K, Schmidt HL (1990) Dependence of the carbon-isotope contents of breath carbon dioxide, milk, serum and rumen fermentation products on the d13C value of food in dairy cows. Brit J Nutr 63(2):187–196CrossRefGoogle Scholar
  51. Murray RM, Marsh H, Heinsohn GE, Spain AV (1977) The role of the midgut caecum and large intestine in the digestion of seagrasses by the dugong (Mammalia: Sirenia). Comp Biochem Physiol A 56A:7–10CrossRefGoogle Scholar
  52. Nigam JN (2002) Bioconversion of water-hyacinth (Eichhornia crassipes) hemicellulose acid hydrolysate to motor fuel ethanol by xylose-fermenting yeast. J Biotechnol 97:107–116CrossRefGoogle Scholar
  53. Nunez-Hernandez G, Wallace JD, Holechek JL, Galyean ML, King DW, Kattnig RM (1991) Mountain mahogany and cottonseed meal as supplements for grass hay. J Range Manage 44:497–500CrossRefGoogle Scholar
  54. Osmond CB, Valaane N, Haslam SM, Uotila P, Roksandic Z (1981) Comparisons of δ13C values in leaves of aquatic macrophytes from different habitats in Britain and Finland; some implications for photosynthetic processes in aquatic plants. Oecologia 50:117–124CrossRefGoogle Scholar
  55. Ozawa T (1997) Phylogenetic position of mammoth and Steller’s sea cow within Tethytheria demonstrated by mitochondrial DNA sequences. J Molec Evol 44(4):406–413CrossRefGoogle Scholar
  56. Passey BH, Robinson TF, Ayliffe LK, Cerling TE, Sponheimer M, Dearing MD, Roeder BL, Ehleringer JR (2005) Carbon isotope fractionation between diet, breath CO2, and bioapatite in different mammals. J Archaeol Sci 32:1459–1470CrossRefGoogle Scholar
  57. 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 seagrass. Funct Plant Biol 29:355–378CrossRefGoogle Scholar
  58. Simenstad CA, Duggins DO, Quay PD (1993) High turnover of inorganic carbon in kelp habitats as a cause of δ13C variability in marine food webs. Mar Biol 116:147–160CrossRefGoogle Scholar
  59. Sullivan CH, Krueger HW (1981) Carbon isotope analysis of separate chemical phases in modern and fossil bone. Nature 292:333–335CrossRefGoogle Scholar
  60. Thayer GW, Bjorndal KA, Ogden JC, Williams SL, Zieman JC (1984) Role of large herbivores in seagrass communities. Estuaries 7:351–376CrossRefGoogle Scholar
  61. Tieszen LL, Fagre T (1993) Effect of diet quality and composition on the isotopic composition of respiratory CO2, bone collagen, bioapatite, and soft tissues. In: Lambert JB, Grupe G (eds) Prehistoric human bone: archaeology at the molecular level. Springer, New York, pp 121–155CrossRefGoogle Scholar
  62. Tuross N, Fogel ML, Hare PE (1988) Variability in the preservation of the isotopic composition of collagen from fossil bone. Geochim Cosmochim Acta 52:929–935CrossRefGoogle Scholar
  63. Virnstein RW, Carbonara PA (1985) Seasonal abundance and distribution of drift algae and seagrasses in the mid-Indian River Lagoon, Florida. Aquat Bot 23:67–82CrossRefGoogle Scholar
  64. Wainright SC, Haney JC, Kerr C, Golovkin AN, Flint MV (1998) Utilization of nitrogen derived from seabird guano by terrestrial and marine plants at St. Paul, Pribilof Islands, Bering Sea, Alaska. Mar Biol 131:63–71CrossRefGoogle Scholar
  65. Wedin DA, Tieszen LL, Dewey B, Pastor J (1995) Carbon isotope dynamics during grass decomposition and soil organic matter formation. Ecology 76:1383–1392CrossRefGoogle Scholar
  66. Wenninger PS, Shipley LA (2000) Harvesting, rumination, digestion, and passage of fruit and leaf diets by a small ruminant, the blue duiker. Oecologia 123:466–474CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Mark T. Clementz
    • 1
    Email author
  • Paul L. Koch
    • 2
  • Cathy A. Beck
    • 3
  1. 1.Department of Geology and Geophysics, Dept. 3006University of WyomingLaramieUSA
  2. 2.Department of Earth SciencesUniversity of CaliforniaSanta CruzUSA
  3. 3.U.S. Geological SurveyFlorida Integrated Science Center, Sirenia ProjectGainesvilleUSA

Personalised recommendations