Stable isotopes dissect aquatic food webs from the top to the bottom

Biogeosciences

Volumn 11, Issue 8, 2014, Pages 2357-2371

  Middelburg, J J ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AQUATIC ENVIRONMENT; ENERGY FLOW; FOOD WEB; ISOTOPIC RATIO; MEASUREMENT METHOD; RECONSTRUCTION; STABLE ISOTOPE;

EID: 84899660581     PISSN: 17264170     EISSN: 17264189     Source Type: Journal    
DOI: 10.5194/bg-11-2357-2014     Document Type: Article

References (143)

1. Amelung, W., Brodowski, S., Sandhage-Hofmann, A., and Bol, R.: Combining biomarker with stable isotope analyses for assessing the transformation and turnover of soil organic matter, Adv. Agron. 100, 155-250, 2008.
2. Auerswald, K., Wittmer, M. H. O. M., Zazzo, A., Schaeufele, R., and Schnyder, H.: Biases in the analysis of stable isotope discrimination in food webs, J. Appl. Ecol., 47, 936-941, doi:10.1111/j.1365-2664.2009.01764.x, 2010.
3. Azam, F., Fenchel, T., Field, J. G., Gray, J. S., Meyerreil, L. A., and Thingstad, F.: The Ecological Role of Water-Column Microbes in the Sea, Mar. Ecol.-Prog. Ser., 10, 257-263, doi:10.3354/meps010257, 1983.
4. Blair, N. E., Levin, L. A., DeMaster, D. J., and Plaia, G.: The shortterm fate of fresh algal carbon in continental slope sediments, Limnol. Oceanogr., 41, 1208-1219, 1996. (Pubitemid 27027807)
5. Boecklen, W. J., Yarnes, C. T., Cook, B. A., and James, A. C.: On the Use of Stable Isotopes in Trophic Ecology, Annu. Rev. Ecol. Evol. S., 42, 411-440, doi:10.1146/annurev-ecolsys- 102209-144726, 2011.
6. Bontes, B. M., Pel, R., Ibelings, B. W., Boschker, H. T. S., Middelburg, J. J., and Van Donk, E.: The effects of biomanipulation on the biogeochemistry, carbon isotopic composition and pelagic food web relations of a shallow lake, Biogeosciences, 3, 69-83, doi:10.5194/bg-3-69-2006, 2006.
7. Boschker, H. T. S. and Middelburg, J. J.: Stable isotopes and biomarkers in microbial ecology, FEMS Microbiol. Ecol., 40, 85-95, doi:10.1111/j.1574-6941. 2002.tb00940.x, 2002. (Pubitemid 34607172)
8. Boschker, H. T. S., Nold, S. C., Wellsbury, P., Bos, D., de Graaf, W., Pel, R., Parkes, R. J., and Cappenberg, T. E.: Direct linking of microbial populations to specific biogeochemical processes by C-13-labelling of biomarkers, Nature, 392, 801-805, doi:10.1038/33900, 1998. (Pubitemid 28225317)
9. Boschker, H. T. S., Moerdijk-Poortvliet, T. C. W., van Breugel, P., Houtekamer, M., and Middelburg, J. J.: A versatile method for stable carbon isotope analysis of carbohydrates by high-performance liquid chromatography/isotope ratio mass spectrometry, Rapid Commun. Mass Sp., 22, 3902-3908, doi:10.1002/rcm.3804, 2008.
10. Bouillon, S. and Boschker, H. T. S.: Bacterial carbon sources in coastal sediments: a cross-system analysis based on stable isotope data of biomarkers, Biogeosciences, 3, 175-185, doi:10.5194/bg-3-175-2006, 2006.
11. Bouillon, S., Gillikin, D. P., and Connolly, R. M.: Use of stable isotopes to understand food webs and ecosystem functioning in estuaries, in: Treatise on Estuarine and Coastal Science, edited by: Wolanski, E. and McLusky, D. S., 7, 143-173, Waltham: Academic Press, 2012.
12. Bugalho, M. N., Barcia, P., Caldeira, M. C., and Cerdeira, J. O.: Stable isotopes as ecological tracers: an efficient method for assessing the contribution of multiple sources to mixtures, Biogeosciences, 5, 1351-1359, doi:10.5194/bg-5-1351-2008, 2008.
13. Bunn, S. E., Leigh, C., and Jardine, T. D: Diet-tissue fractionation of -15N by consumers from streams and rivers Limnol. Oceanogr., 58, 765-773 doi:10.4319/lo.2013.58.3.0765, 2013.
14. Cabana, G. and Rasmussen, J. B.: Comparison of aquatic food chains using nitrogen isotopes, P. Natl. Acad. Sci. USA, 93, 10844-10847, doi:10.1073/pnas.93.20.10844, 1996. (Pubitemid 26333077)
15. Caraco, N., Bauer, J. E., Cole, J. J., Petsch, S., and Raymond, P.: Millennial-aged organic carbon subsidies to a modern river food web, Ecology, 91, 2385-2393, doi:10.1890/09-0330.1, 2010.
16. Caraco, N. F., Lampman, G. G., Cole, J. J., Limburg, K. E., Pace, M. L., and Fischer, D. T.: Microbial assimilation of DIN in a nitrogen rich estuary: implications for food quality and isotope studies, Mar. Ecol.-Prog. Ser., 167, 59-71, 1998. (Pubitemid 28324766)
17. Carpenter, S. R., Cole, J. J., Hodgson, J. R., Kitchell, J. F., Pace, M. L., Bade, D., Cottingham, K. L., Essington, T. E., Houser, J. N., and Schindler, D. E.: Trophic cascades, nutrients, and lake productivity: whole-lake experiments, Ecol. Monogr., 71, 163-186, doi:10.1890/0012-9615(2001)071[0163: TCNALP]2.0.CO;2, 2001. (Pubitemid 32442446)
18. Carpenter, S. R., Cole, J. J., Pace, M. L., Van de Bogert, M., Bade D. L., Bastviken, D., Gille, C., Hodgson, J. R., Kitchell, J. F., and Kritzberg, E. S.: Ecosystem subsidies: Terrestrial support of aquatic food webs from 13C addition to contrasting lakes, Ecology, 86, 2737-2750, 2005. (Pubitemid 41408069)
19. Caut, S., Angulo, E., and Courchamp, F.: Variation in discrimination factors (115N and 113C): the effect of diet isotopic values and applications for diet reconstruction, J. Appl. Ecol., 46, 443-453, 2009.
20. Caut, S., Angulo, E., Courchamp, F., and Figuerola, J.: Trophic experiments to estimate isotope discrimination factors, J. Appl. Ecol., 47, 948-954, doi:10.1111/j.1365-2664.2010.01832.x, 2010.
21. Cherrier, J., Bauer, J. E., Druffel, E. R. M., Coffin, R. B., and Chanton, J. P.: Radiocarbon in marine bacteria: Evidence for the ages of assimilated carbon, Limnol. Oceanogr., 44, 730-736, 1999. (Pubitemid 29233669)
22. Chikaraishi, Y., Ogawa, N. O., Kashiyama, Y., Takano, Y., Suga, H., Tomitani, A., Miyashita, H., Kitazato, H., and Ohkouchi, N.: Determination of aquatic food-web structure based on compoundspecific nitrogen isotopic composition of amino acids, Limnol. Oceanogr.-Meth., 7, 740-750, 2009.
23. Cole, J. J. and Solomon, C. T.: Terrestrial support of zebra mussels and the Hudson River food web: A multi-isotope, Bayesian analysis, Limnol. Oceanogr., 57, 1802-1815, 2012.
24. Cole, J. J., Carpenter, S. R., Kitchell, J. F., and Pace, M. L.: Pathways of organic C utilization in small lakes: Results from a whole-lake 13C addition and coupled model, Limnol. Oceanogr., 47, 1664-1675, 2002. (Pubitemid 36016825)
25. Cole, J. J., Carpenter, S. R., Pace, M. L., Van de Bogert, M. C., Kitchell, J. L., and Hodgson, J. R.: Differential support of lake food webs by three types of terrestrial organic carbon, Ecol. Lett., 9, 558-568, doi:10.1111/j.1461-0248.2006.00898.x, 2006.
26. Cole, J. J., Prairie, Y. T., Caraco, N. F., McDowell, W. H., Tranvik, L. J., Striegl, R. G., Duarte, C. M., Kortelainen, P., Downing, J. A., Middelburg, J. J., and Melack, J.: Plumbing the global carbon cycle: Integrating inland waters into the terrestrial carbon budget, Ecosystems, 10, 171-184, doi:10.1007/s10021-006-9013-8, 2007. (Pubitemid 46825795)
27. Cole, J. J., Carpenter, S. R., Kitchell, J., Pace, M. L., Solomon, C. T., andWeidel, B.: Strong evidence for terrestrial support of zooplankton in small lakes based on stable isotopes of carbon, nitrogen, and hydrogen, P. Natl. Acad. Sci. USA, 108, 1975-1980, doi:10.1073/pnas.1012807108, 2011.
28. Connolly, R. M., Guest, M. A., Melville, A. J., and Oakes, J. M.: Sulfur stable isotopes separate producers in marine foodweb analysis, Oecologia, 138, 161-167, doi:10.1007/s00442-003-1415-0, 2004. (Pubitemid 38162222)
29. Coplen, T. B.: Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results, Rapid Commun. Mass Sp., 25, 2538-2560, 2011.
30. Craig, H.: The Geochemistry of the Stable Carbon Isotopes, Geochim. Cosmochim. Ac., 3, 53-92, doi:10.1016/0016-7037(53)90001-5, 1953.
31. Dang, C., Sauriau, P. G., Savoye, N., Caill-Milly, N., Martinez, P., Haure, J., Millaret, C., and de Montaudouin, X.: Determination of diet in Manila clams by spatial analysis of stable isotopes, Mar. Ecol.-Prog. Ser., 387, 167-177, 2009.
32. Dawson, T. E., Mambelli, S., Plamboeck, A. H., Templer, P. H., and Tu, K. P.: Stable isotopes in plant ecology, Annu. Rev. Ecol. Syst., 33, 507-559, doi:10.1146/annurev.ecolsys.33.020602.095451, 2002. (Pubitemid 36035150)
33. de Goeij, J. M., van Oevelen, D., Vermeij, M. J. A., Osinga, R., Middelburg, J. J., de Goeij, A. F. P. M., and Admiraal, W.: Surviving in a Marine Desert: The Sponge Loop Retains Resources Within Coral Reefs, Science, 342, 108-110, doi:10.1126/science.1241981, 2013.
34. de Kluijver, A., Soetaert, K., Schulz, K. G., Riebesell, U., Bellerby, R. G. J., and Middelburg, J. J.: Phytoplankton-bacteria coupling under elevated CO2 levels: a stable isotope labelling study, Biogeosciences, 7, 3783-3797, doi:10.5194/bg-7-3783-2010, 2010.
35. de Kluijver, A., Yu, J., Houtekamer, M., Middelburg, J. J., and Liu, Z.: Cyanobacteria as a carbon source for zooplankton in eutrophic Lake Taihu, China, measured by C-13 labeling and fatty acid biomarkers, Limnol. Oceanogr., 57, 1245-1254, doi:10.4319/lo.2012.57.4.1245, 2012.
36. de Kluijver, A., Soetaert, K., Czerny, J., Schulz, K. G., Boxhammer, T., Riebesell, U., and Middelburg, J. J.: A 13C labelling study on carbon fluxes in Arctic plankton communities under elevated CO2 levels, Biogeosciences, 10, 1425-1440, doi:10.5194/bg-10-1425-2013, 2013.
37. De Laender, F., Van Oevelen, D., Soetaert, K., and Middelburg, J. J.: Carbon transfer in herbivore- and microbial loopdominated pelagic food webs in the southern Barents Sea during spring and summer, Mar. Ecol.-Prog. Ser., 398, 93-107, doi:10.3354/meps08335, 2010.
38. del Rio, C. M.,Wolf, N., Carleton, S. A., and Gannes, L. Z.: Isotopic ecology ten years after a call for more laboratory experiments, Biol. Rev., 84, 91-111, doi:10.1111/j.1469-185X.2008.00064.x, 2009.
39. Deniro, M. J. and Epstein, S.: Influence of diet on the distribution of carbon isotopes in animals, Geochim. Cosmochim. Ac., 42, 495-506, 1978.
40. Deniro, M. J. and Epstein, S.: Influence of Diet on the Distribution of Nitrogen Isotopes in Animals, Geochim. Cosmochim. Ac., 45, 341-351, doi:10.1016/0016-7037(81)90244-1, 1981.
41. Doucett, R. R., Marks, J. C., Blinn, D. W., Caron, M., and Hungate, B. A.: Measuring terrestrial subsidies to aquatic food webs using stable isotopes of hydrogen, Ecology, 88, 1587-1592, doi:10.1890/06-1184, 2007. (Pubitemid 351345232)
42. Dijkman, N. A., Boschker, H. T. S., Middelburg, J. J., and Kromkamp, J. C.: Group-specific primary production based on stable-isotope labeling of phospholipid-derived fatty acids, Limnol. Oceanogr.-Meth., 7, 612-625, 2009.
43. Eldridge, P. M., Cifuentes, L. A., and Kaldy, J. E.:. Development of a stable isotope constraint system for estuarine food web models, Mar. Ecol.-Prog. Ser. 303, 73-90, 2005. (Pubitemid 41820704)
44. Emmery, A., Lefebvre, S., Alunno-Bruscia, M., and Kooijman, S. A. L. M.: Understanding the dynamics of δ13C and δ15N in soft tissues of the bivalve Crassostrea gigas facing environmental fluctuations in the context of Dynamic Energy Budgets (DEB), J. Sea Res., 66, 361-371, 2011.
45. Evans, C., Pond, D. W., and Wilson, W. H.: Changes in Emiliania huxleyi fatty acid profiles during infection with E-huxleyi virus86: physiological and ecological implications, Aquat. Microb. Ecol., 55, 219-228, 2009.
46. Evrard, V., Soetaert, K., Heip, C. H. R., Huettel, M., Xenopoulos, M. A., and Middelburg, J. J.: Carbon and nitrogen flows through the benthic food web of a photic subtidal sandy sediment, Mar. Ecol.-Prog. Ser., 416, 1-16, doi:10.3354/meps08770, 2010.
47. Evrard, V., Huettel, M., Cook, P. L. M., Soetaert, K., Heip, C. H. R., and Middelburg, J. J.: Importance of phytodetritus and microphytobenthos for heterotrophs in a shallow subtidal sandy sediment, Mar. Ecol.-Prog. Ser., 455, 13-31, doi:10.3354/meps09676, 2012.
48. Eybe, T. Bohn, T., Audinot, J. N., Udelhoven, T., Cauchie, H. M., Migeon, H. N., and Hoffmann. L.: Uptake Visualization of Deltamethrin by Nano-SIMS and Acute Toxicity to the Water Flea Daphnia magna, Chemosphere, 76, 134-140, 2009.
49. Fiorini, S., Gattuso J. P., van Rijswijk, P., and Middelburg, J. J.: Coccolithophores lipid and carbon isotope composition and their variability related to changes in seawater carbonate chemistry, J. Exp. Mar. Biol. Ecol., 394, 74-85, 2010.
50. Fry, B.: Stable isotope ecology, Springer, Dordrecht, 2006.
51. Fry, B.: Alternative approaches for solving underdetermined isotope mixing problems, Mar. Ecol.-Prog. Ser., 472, 1-13, doi:10.3354/meps10168, 2013.
52. Gattuso, J.-P., Gentili, B., Duarte, C. M., Kleypas, J. A., Middelburg, J. J., and Antoine, D.: Light availability in the coastal ocean: impact on the distribution of benthic photosynthetic organisms and their contribution to primary production, Biogeosciences, 3, 489-513, doi:10.5194/bg-3-489-2006, 2006. (Pubitemid 44705644)
53. Germain, L. R., Koch, P. L., Harvey, J., and McCarthy, M. D.: Nitrogen isotope fractionation in amino acids from harbor seals: implications for compound-specific trophic position calculations, Mar. Ecol.-Prog. Ser., 482, 265-277, doi:10.3354/meps10257, 2013.
54. Gribsholt, B., Boschker, H. T. S., Struyf, E., Andersson, M., Tramper, A., De Brabandere, L., van Damme, S., Brion, N., Meire, P., Dehairs, F., Middelburg, J. J., and Heip, C. H. R.: Nitrogen processing in a tidal freshwater marsh: A whole-ecosystem (15)N labeling study, Limnol. Oceanogr., 50, 1945-1959, 2005. (Pubitemid 41692199)
55. Gribsholt, B., Veuger, B., Tramper, A., Middelburg, J. J., and Boschker, H. T. S.: Long-term N-15-nitrogen retention in tidal freshwater marsh sediment: Elucidating the microbial contribution, Limnol. Oceanogr., 54, 13-22, doi:10.4319/lo.2009.54.1.0013, 2009.
56. Guilini, K., Van Oevelen, D., Soetaert, K., Middelburg, J. J., and Vanreusel, A.: Nutritional importance of benthic bacteria for deep-sea nematodes from the Arctic ice margin: Results of an isotope tracer experiment, Limnol. Oceanogr., 55, 1977-1989, doi:10.4319/lo.2010.55.5.1977, 2010.
57. Hall, R. O. and Meyer, J. L.: The trophic significance of bacteria in a detritus-based stream food web, Ecology, 79, 1995-2012, doi:10.1890/0012- 9658(1998)079[1995:TTSOBI]2.0.CO;2, 1998. (Pubitemid 28453416)
58. Hamilton, S. K., Tankm J. L., Raikow, D. E., Siler, E. R., Dorn N. J., and Leonard, N. E.: The role of instream vs allochthonous N in stream food webs: Modeling the results of an isotope addition experiment, J. North Am. Benthol. Soc., 23, 429-448, 2004. (Pubitemid 39320804)
59. Hannides, C. C. S., Popp, B. N., Landry, M. R., and Graham, B. S.: Quantification of zooplankton trophic position in the North Pacific Subtropical Gyre using stable nitrogen isotopes, Limnol. Oceanogr., 54, 50-61, doi:10.4319/lo.2009.54.1.0050, 2009.
60. Hansen, T., Burmeister, A., and Sommer, U.: Simultaneous delta N-15, delta C-13 and delta S-34 measurements of low-biomass samples using a technically advanced high sensitivity elemental analyzer connected to an isotope ratio mass spectrometer, Rapid Commun. Mass Sp., 23, 3387-3393, doi:10.1002/rcm.4267, 2009.
61. Hayes, J. M.: Fractionation of carbon and hydrogen isotopes in biosynthetic processes, in: Organic geochemistry of contemporaneous and ancient sediments, edited by: Valley, J. S. and Cole, D. R., Mineralogical Society of America, 225-277, 2001.
62. Herman, P. M. J., Middelburg, J. J., Widdows, J., Lucas, C. H., and Heip, C. H. R.: Stable isotopes' as trophic tracers: combining field sampling and manipulative labelling of food resources for macrobenthos, Mar. Ecol.-Prog. Ser., 204, 79-92, doi:10.3354/meps204079, 2000.
63. Hochberg, M. E. and Lawton, J. H.: Competition between Kingdoms, Trends Ecol. Evol., 5, 367-371, doi:10.1016/0169-5347(90)90097-W, 1990. (Pubitemid 120036324)
64. Holmes, R. M., Peterson, B. J., Deegan, L., Hughes, J., and Fry, B.: Nitrogen biogeochemistry in the oligohaline zone of a New England estuary, Ecology, 81, 416-432, 2000. (Pubitemid 30445980)
65. Hughes, J. E., Deegan, L. A., Peterson, B. J., Holmes, R. M., and Fry, B.: Nitrogen flow through the food web in the oligohaline zone of a new England estuary, Ecology, 81, 433-452, doi:10.1890/0012-9658(2000)081[0433:NFTTFW]2.0. CO;2, 2000. (Pubitemid 30445981)
66. Karlsson, J., Berggren, M., Ask, J., Bystrom, P., Jonsson, A., Laudon, H., and Jansson, M.: Terrestrial organic matter support of lake food webs: Evidence from lake metabolism and stable hydrogen isotopes of consumers, Limnol. Oceanogr., 57, 1042-1048, 2012.
67. Kirchman, D. L.: The Uptake of Inorganic Nutrients by Heterotrophic Bacteria, Microb. Ecol., 28, 255-271, doi:10.1007/BF00166816, 1994.
68. Krumins, J. A., van Oevelen, D., Bezemer, T. M., De Deyn, G. B., Hol, W. H. G., van Donk, E., de Boer, W., de Ruiter, P. C., Middelburg, J. J., Monroy, F., Soetaert, K., Thebault, E., van de Koppel, J., van Veen, J. A., Viketoft, M., and van der Putten, W. H.: Soil and Freshwater and Marine Sediment Food Webs: Their Structure and Function, Bioscience, 63, 35-42, doi:10.1525/bio.2013. 63.1.8, 2013.
69. Legendre, L. and Rassoulzadegan, F.: Plankton and Nutrient Dynamics in Marine Waters, Ophelia, 41, 153-172, 1995.
70. Lengger, S. K., Lipsewers, Y. A., de Haas, H., Sinninghe Damsté, J. S., and Schouten, S.: Lack of 13C-label incorporation suggests low turnover rates of thaumarchaeal intact polar tetraether lipids in sediments from the Iceland shelf, Biogeosciences, 11, 201-216, doi:10.5194/bg-11-201-2014, 2014.
71. Lorrain A., Paulet, Y.-M., Chauvaud, L., Savoye, N., Donval, A., and Saout, C.: Differential δ13C and δ15N signatures among scallop tissues: implications for ecology and physiology, J. Exp. Mar. Biol. Ecol., 275, 47-61, 2002. (Pubitemid 34839102)
72. Lubetkin, S. C. and Simenstad, C. A.: Multi-source mixing models to quantify food web sources and pathways, J. Appl. Ecol., 41, 996-1008, doi:10.1111/j.0021-8901.2004.00957.x, 2004. (Pubitemid 39348290)
73. Maher, D. T., Santos, I. R., Leuven, J. R. F. W., Oakes, J. M., Erler, D. V., Carvalho, M. C., and Eyre, B. D.: Novel use of cavity ring-down spectroscopy to investigate aquatic carbon cycling from microbial to ecosystem scales', Environ. Sci. Technol., 47, 12938-12945, 2013.
74. Marty, J. and Planas, D.: Comparison of methods to determine algal delta C-13 in freshwater, Limnol. Oceanogr.-Meth., 6, 51-63, 2008. (Pubitemid 351773949)
75. McCallister, S. L., Bauer, J. E., Cherrier, J. E., and Ducklow, H. W.: Assessing sources and ages of organic matter supporting river and estuarine bacterial production: A multiple-isotope (Delta C-14, delta C-13, and delta N-15) approach, Limnol. Oceanogr., 49, 1687-1702, 2004. (Pubitemid 39320759)
76. McCallister, S. L. and del Giorgio, P. A.: Evidence for the respiration of ancient terrestrial organic C in northern temperate lakes and streams, P. Natl. Acad. Sci. USA, 109, 16963-16968, doi:10.1073/pnas.1207305109, 2012.
77. McCarthy, M. D., Lehman, J., and Kudela, R.: Compoundspecific amino acid delta N-15 patterns in marine algae: Tracer potential for cyanobacterial vs. eukaryotic organic nitrogen sources in the ocean, Geochim. Cosmochim. Ac., 103, 104-120, doi:10.1016/j.gca.2012.10.037, 2013.
78. McClelland, J. W. and Montoya, J. P.: Trophic relationships and the nitrogen isotopic composition of amino acids in plankton, Ecology, 83, 2173-2180, doi:10.1890/0012-9658(2002)083[2173:TRATNI]2.0.CO;2, 2002. (Pubitemid 36524756)
79. Michener, R. M. and Lajtha, K. (Eds.): Stable isotopes in ecology and environmental science, Blackwell Scientific, Oxford, 2007.
80. Middelburg, J. J.: Chemoautotrophy in the ocean, Geophys. Res. Lett., 38, L24604, doi:10.1029/2011GL049725, 2011.
81. Middelburg, J. J. and Herman, P. M. J.: Organic matter processing in tidal estuaries, Mar. Chem., 106, 127-147, 2007. (Pubitemid 47211577)
82. Middelburg, J. J., Barranguet, C., Boschker, H. T. S., Herman, P. M. J., Moens, T., and Heip, C. H. R.: The fate of intertidal microphytobenthos carbon: An in situ C-13-labeling study, Limnol. Oceanogr., 45, 1224-1234, 2000.
83. Minagawa, M. and Wada, E.: Stepwise Enrichment of N-15 Along Food-Chains - further Evidence and the Relation between Delta- N-15 and Animal Age, Geochim. Cosmochim. Ac., 48, 1135-1140, doi:10.1016/0016-7037(84)90204-7, 1984.
84. Miyatake, T., MacGregor, B. J., and Boschker, E.: Stable Isotope Probing Combined with Magnetic Bead Capture Hybridization of 16S rRNA: Linking Microbial Community Function to Phylogeny of Sulfate-Reducing Deltaproteobacteria in Marine Sediments, Appl. Environ. Microbiol., 75, 4927-4935, 2009.
85. Miyatake T., Macgregor, B. J., and Boschker, H. T.: Depth-related differences in organic substrate utilization by major microbial groups in intertidal marine sediment, Appl. Environ. Microbiol., 79, 389-392, 2013.
86. Molari, M., Manini, E., and Dell'Anno, A.: Dark inorganic carbon fixation sustains the functioning of benthic deep-sea ecosystems, Global Biogeochem. Cy., 27, 212-221, doi:10.1002/gbc.20030, 2013.
87. Moodley, L., Middelburg, J. J., Boschker, H. T. S., Duineveld, G. C. A., Pel, R., Herman, P. M. J., and Heip, C. H. R.: Bacteria and Foraminifera: key players in a short-term deep-sea benthic response to phytodetritus, Mar. Ecol.-Prog. Ser., 236, 23-29, doi:10.3354/meps236023, 2002. (Pubitemid 34780677)
88. Moodley, L., Middelburg, J. J., Soetaert, K., Boschker, H. T. S., Herman, P. M. J., and Heip, C. H. R.: Similar rapid response to phytodetritus deposition in shallow and deep-sea sediments, J. Mar. Res., 63, 457-469, doi:10.1357/0022240053693662, 2005. (Pubitemid 40900022)
89. Moore, J. W. and Semmens, B. X.: Incorporating uncertainty and prior information into stable isotope mixing models, Ecol. Lett., 11, 470-480, doi:10.1111/j.1461-0248.2008.01163.x, 2008. (Pubitemid 351499224)
90. Nomaki, H., Ogawa, N. O., Takano, Y., Suga, H., Ohkouchi, N., and Kitazato, H.: Differing utilization of glucose and algal particulate organic matter by deep-sea benthic organisms of Sagami Bay, Japan, Mar. Ecol.-Prog. Ser., 431, 11-24, doi:10.3354/meps09144, 2011.
91. Norrman, B., Zweifel, U. L., Hopkinson, C. S., and Fry, B.: Production and utilization of dissolved organic carbon during an experimental diatom bloom, Limnol. Oceanogr., 40, 898-907, 1995. (Pubitemid 26451986)
92. Oakes, J. M., Eyre, B. D., Middelburg, J. J., and Boschker, H. T. S.: Composition, production, and loss of carbohydrates in subtropical shallow subtidal sandy sediments: Rapid processing and long-term retention revealed by C-13-labeling, Limnol. Oceanogr., 55, 2126-2138, doi:10.4319/lo.2010.55.5.2126, 2010.
93. Oakes, J. M., Eyre, B. D., and Middelburg, J. J.: Transformation and fate of microphytobenthos carbon in subtropical shallow subtidal sands: A C-13-labeling study, Limnol. Oceanogr., 57, 1846-1856, doi:10.4319/lo.2012.57. 06.1846, 2012.
94. Pace, M. L., Cole, J. J., Carpenter, S. R., Kitchell, J. F., Hodgson, J. R., Van de Bogert, M. C., Bade, D. L., Kritzberg, E. S., and Bastviken, D.: Whole-lake carbon-13 additions reveal terrestrial support of aquatic food webs, Nature, 427, 240-243, doi:10.1038/nature02227, 2004. (Pubitemid 38112038)
95. Pace, M. L., Carpenter, S. R., Cole, J. J., Coloso, J. J., Kitchell, J. F., Hodgson, J. R., Middelburg, J. J., Preston, N. D., Solomon, C. T., and Weidel, B. C.: Does terrestrial organic carbon subsidize the planktonic food web in a clear-water lake?, Limnol. Oceanogr., 52, 2177-2189, doi:10.4319/lo.2007. 52.5.2177, 2007. (Pubitemid 47612140)
96. Pacella, S. R., Lebreton, B., Richard, P., Phillips, D., DeWitt, T. H., and Niquil, N.: Incorporation of diet information derived from Bayesian stable isotope mixing models into mass-balanced marine ecosystem models: A case study from the Marennes-Oléron Estuary, France, Ecol. Model., 267, 127-137, 2013.
97. Parnell, A. C., Inger, R., Bearhop, S., and Jackson, A. L.: Source Partitioning Using Stable Isotopes: Coping with Too Much Variation, Plos One, 5, e9672, doi:10.1371/journal.pone.0009672, 2010.
98. Pel, R., Hoogveld, H., and Floris, V.: Using the hidden isotopic heterogeneity in phyto- and zooplankton to unmask disparity in trophic carbon transfer, Limnol. Oceanogr., 48, 2200-2207, 2003. (Pubitemid 37538070)
99. Peterson, B. J. and Fry, B.: Stable Isotopes in Ecosystem Studies, Annu. Rev. Ecol. Syst., 18, 293-320, doi:10.1146/annurev.ecolsys.18.1.293, 1987.
100. Phillips, D. L.: Converting isotope values to diet composition: the use of mixing models, J. Mammal., 93, 342-352, doi:10.1644/11-MAMM-S-158.1, 2012.
101. Phillips, D. L. and Gregg, J. W.: Uncertainty in source partitioning using stable isotopes, Oecologia, 127, 171-179, doi:10.1007/s004420000578, 2001. (Pubitemid 32449368)
102. Phillips, D. L. and Gregg, J. W.: Source partitioning using stable isotopes: coping with too many sources, Oecologia, 136, 261-269, doi:10.1007/s00442-003-1218-3, 2003. (Pubitemid 36933259)
103. Phillips, D. L. and Koch, P. L.: Incorporating concentration dependence in stable isotope mixing models, Oecologia, 130, 114-125, doi:10.1007/ s004420100786, 2002. (Pubitemid 36064143)
104. Phillips, D. L., Newsome, S. D., and Gregg, J. W.: Combining sources in stable isotope mixing models: alternative methods, Oecologia, 144, 520-527, doi:10.1007/s00442-004-1816-8, 2005. (Pubitemid 41218802)
105. Polis, G. A., Anderson, W. B., and Holt, R. D.: Toward an integration of landscape and food web ecology: The dynamics of spatially subsidized food webs, Annu. Rev. Ecol. Syst., 28, 289-316, doi:10.1146/annurev.ecolsys.28.1.289, 1997. (Pubitemid 28012294)
106. Post, D. M.: Using stable isotopes to estimate trophic position: Models, methods, and assumptions, Ecology, 83, 703-718, doi:10.2307/3071875, 2002. (Pubitemid 36524158)
107. Riebesell, U., Revill, A. T., Holdsworth, D. G., and Volkman, J. K.: The effects of varying CO2 concentration on lipid composition and carbon isotope fractionation in Emiliania huxleyi, Geochim. Cosmochim. Ac., 64, 4179-4192, 2000. (Pubitemid 32185381)
108. Rose, K. A., Allen, J. I., Artioli, Y., Barange, M., Blackford, J., Carlotti, F., Cropp, R., Daewel, U., Edwards, K., Flynn, K., Hill, S. L., HilleRisLambers, R., Huse, G., Mackinson, S., Megrey, B., Moll, A., Rivkin, R., Salihoglu, B., Schrum, C., Shannon, L., Shin, Y., Smith, S. L., Smith, C., Solidoro, C., St John, M., and Zhou, M.: End-To-End Models for the Analysis of Marine Ecosystems: Challenges, Issues, and Next Steps, Marine and Coastal Fisheries, 2, 115-130, doi:10.1577/C09-059.1, 2010.
109. Rossi, F., Vos, M., and Middelburg, J. J.: Species identity, diversity and microbial carbon flow in reassembling macrobenthic communities, Oikos, 118, 503-512, doi:10.1111/j.1600-0706.2009.17112.x, 2009.
110. Salihoglu, B., Neuer, S., Painting, S., Murtugudde, R., Hofmann, E. E., Steele, J. H., Hood, R. R., Legendre, L., Lomas, M. W., Wiggert, J. D., Ito, S., Lachkar, Z., Hunt, G. L.,Jr., Drinkwater, K. F., and Sabine, C. L.: Bridging marine ecosystem and biogeochemistry research: Lessons and recommendations from comparative studies, J. Marine Syst., 109, 161-175, doi:10.1016/j.jmarsys.2012. 07.005, 2013.
111. Sarmiento, G. L. and Gruber, N.: Ocean biogeochemical dynamics, Princeton University Press, 503 pp., 2006.
112. Schell, D. M.: C-13 and C-14 Abundances in Alaskan Aquatic Organisms - Delayed Production from Peat in Arctic Food Webs, Science, 219, 1068-1071, doi:10.1126/science.219.4588.1068, 1983. (Pubitemid 13286377)
113. Schouten, S., Klein Breteler, W. C. M., Blokker, P., Schogt, N., Rijpstra, W. I. C., Grice, K., Baas, M., and Sinninghe Damsté, J. S.: Biosynthetic effects on the stable carbon isotopic composition of algal lipids: implications for deciphering the carbon isotopic biomarker record, Geochim. Cosmochim. Ac, 62, 1397-1406, 1998. (Pubitemid 28453912)
114. Semmens, B. X., Ward, E. J., Moore, J. W., and Darimont, C. T.: Quantifying Inter- and Intra-Population Niche Variability Using Hierarchical Bayesian Stable Isotope Mixing Models, Plos One, 4, e6187, doi:10.1371/journal. pone.0006187, 2009.
115. Sessions, A. L., Burgoyne, T.W., Schimmelmann, A., and Hayes, J. M.: Fractionation of hydrogen isotopes in lipid biosynthesis, Org. Geochem., 30, 1193-1200, doi:10.1016/S0146-6380(99)00094-7, 1999. (Pubitemid 29532233)
116. Smith, B. N. and Epstein, S.: Biogeochemistry of Stable Isotopes of Hydrogen and Carbon in Salt Marsh Biota, Plant Physiol., 46, 738-742, doi:10.1104/pp.46.5.738, 1970.
117. Solomon, C. T., Cole, J. J., Doucett, R. R., Pace, M. L., Preston, N. D., Smith, L. E., and Weidel, B. C.: The influence of environmental water on the hydrogen stable isotope ratio in aquatic consumers, Oecologia, 161, 313-324, doi:10.1007/s00442-009-1370-5, 2009.
118. Solomon, C. T., Carpenter, S. R., Clayton, M. K., Cole, J. J., Coloso, J. J., Pace, M. L., Vander Zanden, M. J., and Weidel, B. C.: Terrestrial, benthic, and pelagic resource use in lakes: results from a three-isotope Bayesian mixing model, Ecology, 92, 1115-1125, 2011.
119. Thurber, A. R., Levin, L. A., Orphan, V. J., and Marlow, J. J.: Archaea in metazoan diets: implications for food webs and biogeochemical cycling, ISME J., 6, 1602-1612, doi:10.1038/ismej.2012.16, 2012.
120. Travers, M., Shin, Y.-J., Jennings, S., and Cury, P.: Towards end-toend models for investigating the effects of climate and fishing in marine ecosystems, Prog. Oceanogr., 75, 751-770, 2007. (Pubitemid 350179941)
121. Van den Meersche, K., Middelburg, J. J., Soetaert, K., van Rijswijk, P., Boschker, H. T. S., and Heip, C. H. R.: Carbon-nitrogen coupling and algal-bacterial interactions during an experimental bloom: Modeling a C-13 tracer experiment, Limnol. Oceanogr., 49, 862-878, 2004. (Pubitemid 38730129)
122. Van den Meersche, K., Soetaert, K., and Middelburg, J. J.: A Bayesian compositional estimator for microbial taxonomy based on biomarkers, Limnol. Oceanogr.-Meth., 6, 190-199, 2008. (Pubitemid 351773931)
123. Van den Meersche, K., Van Rijswijk, P., Soetaert, K., and Middelburg, J. J.: Autochthonous and allochthonous contributions to mesozooplankton diet in a tidal river and estuary: Integrating carbon isotope and fatty acid constraints, Limnol. Oceanogr., 54, 62-74, doi:10.4319/lo.2009.54.1.0062, 2009.
124. Van den Meersche, K., Soetaert, K., and Middelburg, J. J.: Plankton dynamics in an estuarine plume: a mesocosm C- 13 and N-15 tracer study, Mar. Ecol.-Prog. Ser., 429, 29-43, doi:10.3354/meps09097, 2011.
125. Van Engeland, T., De Kluijver, A., Soetaert, K., Meysman, F. J. R., and Middelburg, J. J.: Isotope data improve the predictive capabilities of a marine biogeochemical model, Biogeosciences Discuss., 9, 9453-9486, doi:10.5194/bgd-9-9453-2012, 2012.
126. van Nugteren, P., Herman, P. M. J., Moodley, L., Middelburg, J. J., Vos, M., and Heip, C. H. R.: Spatial distribution of detrital resources determines the outcome of competition between bacteria and a facultative detritivorous worm, Limnol. Oceanogr., 54, 1413-1419, doi:10.4319/lo.2009.54.5.1413, 2009.
127. van Oevelen, D., Moodley, L., Soetaert, K., and Middelburg, J. J.: The trophic significance of bacterial carbon in a marine intertidal sediment: Results of an in situ stable isotope labeling study, Limnol. Oceanogr., 51, 2349-2359, 2006a. (Pubitemid 44520927)
128. van Oevelen, D., Soetaert, K., Middelburg, J. J., Herman, P. M. J., Moodley, L., Hamels, I., Moens, T., and Heip, C. H. R.: Carbon flows through a benthic food web: Integrating biomass, isotope and tracer data, J. Mar. Res., 64, 453-482, doi:10.1357/002224006778189581, 2006b. (Pubitemid 44404682)
129. van Oevelen, D., Van den Meersche, K., Meysman, F. J. R., Soetaert, K., Middelburg, J. J., and Vezina, A. F.: Quantifying Food Web Flows Using Linear Inverse Models, Ecosystems, 13, 32-45, doi:10.1007/s10021-009-9297-6, 2010.
130. Van Oevelen, D., Soetaert, K., and Heip, C. H. R.: Carbon flows in the benthic food web of the Porcupine Abyssal Plain: The (un)importance of labile detritus in supporting microbial and faunal carbon demands, Limnol. Oceanogr., 7, 645-664, 2012.
131. Vander Zanden, M. J. and Rasmussen, J. B.: Variation in delta N- 15 and delta C-13 trophic fractionation: Implications for aquatic food web studies, Limnol. Oceanogr., 46, 2061-2066, 2001. (Pubitemid 34009955)
132. Vander Zanden, M. J., Casselman, J. M., and Rasmussen, J. B.: Stable isotope evidence for the food web consequences of species invasions in lakes, Nature, 401, 464-467, doi:10.1038/46762, 1999. (Pubitemid 29470201)
133. Vanderklift, M. A. and Ponsard, S.: Sources of variation in consumer-diet delta(15)N enrichment: a meta-analysis, Oecologia, 136, 169-182, doi:10.1007/s00442-003-1270-z, 2003. (Pubitemid 36933250)
134. Veuger, B., Middelburg, J. J., Boschker, H. T. S., and Houtekamer, M.: Analysis of N-15 incorporation into D-alanine: A new method for tracing nitrogen uptake by bacteria, Limnol. Oceanogr.-Meth., 3, 230-240, 2005. (Pubitemid 43723662)
135. Veuger, B., Eyre, B. D., Maher, D., and Middelburg, J. J.: Nitrogen incorporation and retention by bacteria, algae, and fauna in a subtropical intertidal sediment: An in situ N-15-labeling study, Limnol. Oceanogr., 52, 1930-1942, doi:10.4319/lo.2007.52.5.1930, 2007. (Pubitemid 47612120)
136. Vogel, C., Mueller, C. W., Höschen, C., Buegger, F., Heister, K., Schulz, S., Schloter, M., and Kögel-Knabner, I.: Submicron structures provide preferential spots for carbon and nitrogen sequestration in soils, Nat. Commun., 5, 2947, doi:10.1038/ncomms3947, 2014.
137. Wagner, M.: Single-Cell Ecophysiology of Microbes as Revealed by Raman Microspectroscopy or Secondary Ion Mass Spectrometry Imaging, Annu. Rev. Microbiol., 63, 411-429, doi:10.1146/annurev.micro.091208.073233, 2009.
138. Witte, U.,Wenzhofer, F., Sommer, S., Boetius, A., Heinz, P., Aberle, N., Sand, M., Cremer, A., Abraham,W. R., Jorgensen, B. B., and Pfannkuche, O.: In situ experimental evidence of the fate of a phytodetritus pulse at the abyssal sea floor, Nature, 424, 763-766, doi:10.1038/nature01799, 2003. (Pubitemid 37021702)
139. Wolf, N., Carleton, S. A., and del Rio, C. M.: Ten years of experimental animal isotopic ecology, Funct. Ecol., 23, 17-26, doi:10.1111/j.1365-2435.2009. 01529.x, 2009.
140. Woulds, C., Cowie, G. L., Levin, L. A., Andersson, J. H., Middelburg, J. J., Vandewiele, S., Lamont, P. A., Larkin, K. E., Gooday, A. J., Schumacher, S., Whitcraft, C., Jeffreys, R. M., and Schwartz, M.: Oxygen as a control on seafloor biological communities and their roles in sedimentary carbon cycling, Limnol. Oceanogr., 52, 1698-1709, doi:10.4319/lo.2007.52.4.1698, 2007. (Pubitemid 47121578)
141. Woulds, C., Andersson, J. H., Cowie, G. L., Middelburg, J. J., and Levin, L. A.: The short-term fate of organic carbon in marine sediments: Comparing the Pakistan margin to other regions, Deep- Sea Ress. Pt. II, 56, 393-402, doi:10.1016/j.dsr2.2008.10.008, 2009.
142. Zhang, X., Gillespie, A. L., and Sessions, A. L.: Large D/H variations in bacterial lipids reflect central metabolic pathways, P. Natl. Acad. Sci. USA, 106, 12580-12586, doi:10.1073/pnas.0903030106, 2009.
143. Zigah, P. K., Minor, E. C., Werne, J. P., and Leigh McCallister, S.: An isotopic (Δ14C, δ13C, and δ15N) investigation of the composition of particulate organic matter and zooplankton food sources in Lake Superior and across a size-gradient of aquatic systems, Biogeosciences, 9, 3663-3678, doi:10.5194/bg-9-3663-2012, 2012.