Register      Login
Environmental Chemistry Environmental Chemistry Society
Environmental problems - Chemical approaches
RESEARCH ARTICLE

Dynamics of halocarbons in coastal surface waters during short term mesocosm experiments

Anna Orlikowska A B , Christian Stolle A , Falk Pollehne A , Klaus Jürgens A and Detlef E. Schulz-Bull A
+ Author Affiliations
- Author Affiliations

A Leibniz Institute for Baltic Sea Research Warnemünde (IOW), Seestraße 15, D-18119 Rostock, Germany.

B Corresponding author. Email: anna.orlikowska@io-warnemuende.de

Environmental Chemistry 12(4) 515-525 https://doi.org/10.1071/EN14204
Submitted: 30 September 2014  Accepted: 29 January 2015   Published: 11 June 2015

Environmental context. Halocarbons are trace gases important in atmospheric ozone chemistry whose biogenic production – among other factors – depends on light-induced stress of marine algae. Several studies have confirmed this effect in laboratory experiments but knowledge in natural systems remains sparse. In mesocosm experiments, which are a link between field and laboratory studies, we observed that the influence of natural levels of ultraviolet radiation on halocarbon dynamics in the marine surface waters was either insignificant or concealed by the complex interactions in the natural systems.

Abstract. The aim of the present study was to evaluate the influence of different light quality, especially ultraviolet radiation (UVR), on the dynamics of volatile halogenated organic compounds (VHOCs) at the sea surface. Short term experiments were conducted with floating gas-tight mesocosms of different optical qualities. Six halocarbons (CH3I, CHCl3, CH2Br2, CH2ClI, CHBr3 and CH2I2), known to be produced by phytoplankton, together with a variety of biological and environmental variables were measured in the coastal southern Baltic Sea and in the Raunefjord (North Sea). These experiments showed that ambient levels of UVR have no significant influence on VHOC dynamics in the natural systems. We attribute it to the low radiation doses that phytoplankton cells receive in a normal turbulent surface mixed layer. The VHOC concentrations were influenced by their production and removal processes, but they were not correlated with biological or environmental parameters investigated. Diatoms were most likely the dominant biogenic source of VHOCs in the Baltic Sea experiment, whereas in the Raunefjord experiment macroalgae probably contributed strongly to the production of VHOCs. The variable stable carbon isotope signatures (δ13C values) of bromoform (CHBr3) also indicate that different autotrophic organisms were responsible for CHBr3 production in the two coastal environments. In the Raunefjord, despite strong daily variations in CHBr3 concentration, the carbon isotopic ratio was fairly stable with a mean value of –26 ‰. During the declining spring phytoplankton bloom in the Baltic Sea, the δ13C values of CHBr3 were enriched in 13C and showed noticeable diurnal changes (–12 ‰ ± 4). These results show that isotope signature analysis is a useful tool to study both the origin and dynamics of VHOCs in natural systems.

Additional keywords: Baltic Sea, δ13C-signature, Raunefjord, UV-light, volatile halocarbons.


References

[1]  Scientific Assessment of Ozone Depletion: 2006, Global Ozone Research and Monitoring Project Report number 50, 2007 (World Meteorological Organization: Geneva, Switzerland).

[2]  A. M. Wuosmaa, L. P. Hager, Methyl chloride transferase: a carbocation route for biosynthesis of halometabolites. Science 1990, 249, 160.
Methyl chloride transferase: a carbocation route for biosynthesis of halometabolites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXls1Oktbc%3D&md5=96e30f3bd640a13fca0e651ae62bd880CAS | 2371563PubMed |

[3]  S. Amachi, Y. Kamagata, T. Kanagawa, Y. Muramatsu, Bacteria mediate methylation of iodine in marine and terrestrial environments. Appl. Environ. Microbiol. 2001, 67, 2718.
Bacteria mediate methylation of iodine in marine and terrestrial environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt1Cit7Y%3D&md5=b3d95fbcf19c1fbae1539ebe4e0b6c48CAS | 11375186PubMed |

[4]  R. Theiler, J. C. Cook, L. P. Hager, J. F. Siuda, Halohydrocarbon synthesis by bromoperoxidase. Science 1978, 202, 1094.
Halohydrocarbon synthesis by bromoperoxidase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXot1yitg%3D%3D&md5=b276e0d79bde079a4b17ddedaf89441fCAS | 17777960PubMed |

[5]  R. S. Beissner, W. J. Guilford, R. M. Coates, L. P. Hager, Synthesis of brominated heptanones and bromoform by a bromoperoxidase of marine origin. Biochemistry 1981, 20, 3724.
Synthesis of brominated heptanones and bromoform by a bromoperoxidase of marine origin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXktlOqsLc%3D&md5=f0b678843f0fc4ded45d82c0ab3af643CAS | 7272274PubMed |

[6]  C. Y. Lin, S. L. Manley, Bromoform production from seawater treated with bromoperoxidase. Limnol. Oceanogr. 2012, 57, 1857.
Bromoform production from seawater treated with bromoperoxidase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXptlCgsg%3D%3D&md5=26baf1d0d724aa2e3c7b39440ce53eddCAS |

[7]  T. Urhahn, K. Ballschmiter, Chemistry of the biosynthesis of halogenated methanes: C1-organohalogens as pre-industrial chemical stressors in the environment? Chemosphere 1998, 37, 1017.
Chemistry of the biosynthesis of halogenated methanes: C1-organohalogens as pre-industrial chemical stressors in the environment?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlt1eiu7Y%3D&md5=473f5287218f200979eb8937b8ce71d5CAS |

[8]  R. M. Moore, O. C. Zafiriou, Photochemical production of methyl iodide in seawater. J. Geophys. Res. 1994, 99, 16415.
Photochemical production of methyl iodide in seawater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXms1ars7c%3D&md5=e3342470790e927b6f67cad53395316dCAS |

[9]  C. E. Jones, L. J. Carpenter, Solar photolysis of CH2I2, CH2ICl, and CH2IBr in water, saltwater, and seawater. Environ. Sci. Technol. 2005, 39, 6130.
Solar photolysis of CH2I2, CH2ICl, and CH2IBr in water, saltwater, and seawater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVWjurw%3D&md5=f37c93459f8e4c3faf302ed49ca019b6CAS | 16173573PubMed |

[10]  K. Ballschmiter, Pattern and sources of naturally produced organohalogens in the marine environment: biogenic formation of organohalogens. Chemosphere 2003, 52, 313.
Pattern and sources of naturally produced organohalogens in the marine environment: biogenic formation of organohalogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsVGnsLg%3D&md5=61e3cf9aaf5aa9aa8ec0b25ff4eefa02CAS | 12738255PubMed |

[11]  M. Martino, P. S. Liss, J. M. Plane, The photolysis of dihalomethanes in surface seawater. Environ. Sci. Technol. 2005, 39, 7097.
The photolysis of dihalomethanes in surface seawater.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvFynu7s%3D&md5=55a95a1a4d27db47ecd1ea294fea7227CAS | 16201634PubMed |

[12]  K. Goodwin, M. E. Lidstrom, R. S. Oremland, Marine bacterial degradation of brominated methanes. Environ. Sci. Technol. 1997, 31, 3188.
Marine bacterial degradation of brominated methanes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmt1eksrk%3D&md5=7d272be068707cf8b9a4fd4d62353cf0CAS |

[13]  K.-C. Ma, D. Mackay, S. C. Lee, W. Y. Shiu, Halogenated aliphatic hydrocarbons, in Handbook of Physical-Chemical Properties and Environmental Fate for Organic Chemicals. Halogenated Hydrocarbons Vol. II 2006, pp. 921–1256 (CRC Press: Boca Raton, FL, USA). 10.1201/9781420044393.CH5

[14]  S. Klick, Seasonal variations of biogenic and anthropogenic halocarbons in seawater from a coastal site. Limnol. Oceanogr. 1992, 37, 1579.
Seasonal variations of biogenic and anthropogenic halocarbons in seawater from a coastal site.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXisVSht70%3D&md5=5ee16dabe9dcf6d67910e6013afe70a2CAS |

[15]  S. D. Archer, L. E. Goldson, M. I. Liddicoat, D. G. Cummings, P. D. Nightingale, Marked seasonality in the concentrations and sea-to-air flux of volatile iodocarbon compounds in the western English Channel. J. Geophys. Res. 2007, 112, C08009.
Marked seasonality in the concentrations and sea-to-air flux of volatile iodocarbon compounds in the western English Channel.Crossref | GoogleScholarGoogle Scholar |

[16]  A. Orlikowska, D. E. Schulz-Bull, Seasonal variations of volatile organic compounds in the coastal Baltic Sea. Environ. Chem. 2009, 6, 495.
Seasonal variations of volatile organic compounds in the coastal Baltic Sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhslGjsbk%3D&md5=d27023e8965aa9c1a69a9d62600a9440CAS |

[17]  M. Pedersén, J. Collén, K. Abrahamsson, A. Ekdahl, Production of halocarbons from seaweeds: an oxidative stress reaction? Sci. Mar. 1996, 60, 257.

[18]  R. M. Moore, M. Webb, R. Tokarczyk, R. Wever, Bromoperoxidase and iodoperoxidase enzymes and production of halogenated methanes in marine diatom cultures. J. Geophys. Res. 1996, 101, 20 899.
Bromoperoxidase and iodoperoxidase enzymes and production of halogenated methanes in marine diatom cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xmtlyqu7w%3D&md5=e6c6a9a8c947cf79f602d07fd4296ea6CAS |

[19]  K. Goodwin, W. J. North, M. E. Lidstrom, Production of bromoform and dibromomethane by giant kelp: factors affecting release and comparison to anthropogenic bromine sources. Limnol. Oceanogr. 1997, 42, 1725.
Production of bromoform and dibromomethane by giant kelp: factors affecting release and comparison to anthropogenic bromine sources.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjtlejsrk%3D&md5=edfca8d350bf2baa1ce9c5f3597272d6CAS |

[20]  A. Ekdahl, M. Pedersén, K. Abrahamsson, A study of the diurnal variation of biogenic volatile halocarbons. Mar. Chem. 1998, 63, 1.
A study of the diurnal variation of biogenic volatile halocarbons.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnslKitLY%3D&md5=76ee28e7953758315dedce32df191193CAS |

[21]  S. L. Manley, P. E. Barbero, Physiological constraints on bromoform (CHBr3) production by Ulva lactuca (Chlorophyta). Limnol. Oceanogr. 2001, 46, 1392.
Physiological constraints on bromoform (CHBr3) production by Ulva lactuca (Chlorophyta).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnsVSktbg%3D&md5=9571b2b0f87e110311178a9a5628e7fcCAS |

[22]  C. Hughes, G. Malin, P. D. Nightingale, P. S. Liss, The effect of light stress on the release of volatile iodocarbons by three species of marine microalgae. Limnol. Oceanogr. 2006, 51, 2849.
The effect of light stress on the release of volatile iodocarbons by three species of marine microalgae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlWltbvO&md5=79b4e951853d9ea49bd49040ed38ca3cCAS |

[23]  M. G. Scarratt, R. M. Moore, Production of chlorinated hydrocarbons and methyl iodide by the red microalga Porphyridium purpureum. Limnol. Oceanogr. 1999, 44, 703.
Production of chlorinated hydrocarbons and methyl iodide by the red microalga Porphyridium purpureum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjs1yjs7c%3D&md5=d43836f3965b0dc60f62c462bc55f910CAS |

[24]  F. Laturnus, T. Svensson, C. Wiencke, G. Öberg, Ultraviolet radiation affects emission of ozone-depleting substances by marine macroalgae: results from a laboratory incubation study. Environ. Sci. Technol. 2004, 38, 6605.
Ultraviolet radiation affects emission of ozone-depleting substances by marine macroalgae: results from a laboratory incubation study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovFSmtbk%3D&md5=b415b4e469d7b488638d026df3316232CAS | 15669318PubMed |

[25]  C. Hughes, D. J. Franklin, G. Malin, Iodomethane production by two important marine cyanobacteria: Prochlorococcus marinus (CCMP 2389) and Synechococcus sp. (CCMP 2370). Mar. Chem. 2011, 125, 19.
Iodomethane production by two important marine cyanobacteria: Prochlorococcus marinus (CCMP 2389) and Synechococcus sp. (CCMP 2370).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlslWmsr4%3D&md5=ed5dd33b657a2d73033d6e30367b7bcdCAS |

[26]  D. Smythe-Wright, C. Peckett, S. Boswell, R. Harrison, Controls on the production of organohalogens by phytoplankton: effect of nitrate concentration and grazing. J. Geophys. Res. Biogeosci. 2010, 115, G03020.
Controls on the production of organohalogens by phytoplankton: effect of nitrate concentration and grazing.Crossref | GoogleScholarGoogle Scholar |

[27]  F. Keppler, R. M. Kalin, D. B. Harper, W. C. McRoberts, J. T. G. Hamilton, Carbon isotope anomaly in the major plant C1 pool and its global biogeochemical implications. Biogeosciences 2004, 1, 123.
Carbon isotope anomaly in the major plant C1 pool and its global biogeochemical implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpsFWgu7s%3D&md5=03e7c9a79caea587950477d284914d56CAS |

[28]  C. Hughes, G. Malin, C. M. Turley, B. J. Keely, P. D. Nightingale, P. S. Liss, The production of volatile iodocarbons by biogenic marine aggregates. Limnol. Oceanogr. 2008, 53, 867.
The production of volatile iodocarbons by biogenic marine aggregates.Crossref | GoogleScholarGoogle Scholar |

[29]  H. Piazena, D. P. Häder, Penetration of solar UV irradiation in coastal lagoons of the southern Baltic Sea and its effect on phytoplankton communities. Photochem. Photobiol. 1994, 60, 463.
Penetration of solar UV irradiation in coastal lagoons of the southern Baltic Sea and its effect on phytoplankton communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitVamtrk%3D&md5=eeaf3f4b7822e17d81aa42872a15d554CAS |

[30]  K. Grasshoff, M. Ehrhardt, K. Kremling, T. Almgren, M. O. Andreae, R. Dawson, J. C, Duinker, D. Dyrssen, S. Fonselius, H. P. Hanses, T. Hillebrand, B. Josefsson, F. Koroleff, G. Liebezeit, J. Olafsson, P. J. Statham, P. J. LeB. Williams, Methods of Seawater Analysis, 2nd edn (Eds K. Grasshoff, M. Ehrhardt, K. Kremling) 1983 (Verlag Chemie: Weinheim, Germany).

[31]  N. R. Auer, B. U. Manzke, D. E. Schulz-Bull, Development of a purge and trap continuous flow system for the stable carbon isotope analysis of volatile halogenated organic compounds in water. J. Chromatogr. A 2006, 1131, 24.
Development of a purge and trap continuous flow system for the stable carbon isotope analysis of volatile halogenated organic compounds in water.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVGjtbjM&md5=84abc41d533351d046b83e14a04522f9CAS | 16899248PubMed |

[32]  H. Utermöhl, Zur Vervollkommnung der quantitativen Phytoplankton-Methodik (Ed. C. H. Mortimer) 1958 (Schweizerbart: Stuttgart, Germany).

[33]  Guidelines Concerning phytoplankton Species Composition, Abundance and Biomass. Manual for Marine Monitoring in the COMBINE Programme of HELCOM, Part C (HELCOM) 2014. Available at http://www.helcom.fi/Documents/Action%20areas/Monitoring%20and%20assessment/Manuals%20and%20Guidelines/Manual%20for%20Marine%20Monitoring%20in%20the%20COMBINE%20Programme%20of%20HELCOM_PartC_AnnexC6.pdf [Verified 8 May 2015].

[34]  N. Wasmund, I. Topp, D. Schories, Optimising the storage and extraction of chlorophyll samples. Oceanologia 2006, 48, 125.

[35]  D. Marie, X. L. Shi, F. Rigaut-Jalabert, D. Vaulot, Use of flow cytometric sorting to better assess the diversity of small photosynthetic eukaryotes in the English Channel. FEMS Microbiol. Ecol. 2010, 72, 165.
Use of flow cytometric sorting to better assess the diversity of small photosynthetic eukaryotes in the English Channel.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvVamsL8%3D&md5=cda331c95e367af7d1ab4c7f57250d05CAS | 20236325PubMed |

[36]  G. Chin-Leo, D. L. Kirchman, Estimating bacterial production in marine waters from the simultaneous incorporation of thymidine and leucine. Appl. Environ. Microbiol. 1988, 54, 1934.
| 1:CAS:528:DyaL1cXkvFygtLk%3D&md5=7adcc29cc0efaac2989d6a6e0b24da1bCAS | 16347706PubMed |

[37]  B. Riemann, P. Koefoed Bjørnsen, S. Newell, R. Fallon, Calculation of cell production of coastal marine bacteria based on measured incorporation of [3H]thymidine. Limnol. Oceanogr. 1987, 32, 471.
Calculation of cell production of coastal marine bacteria based on measured incorporation of [3H]thymidine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXkt1Slt78%3D&md5=b67400e82a66d3b9061e47b2c78efa68CAS |

[38]  S. Lee, J. A. Fuhrman, Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Appl. Environ. Microbiol. 1987, 53, 1298.
| 1:CAS:528:DyaL2sXksVGrtr4%3D&md5=449fba67df8ea76026abcda45b175a77CAS | 16347362PubMed |

[39]  F. Laturnus, T. Svensson, C. Wiencke, Release of reactive organic halogens by the brown macroalga Saccharina latissima after exposure to ultraviolet radiation. Polar Res. 2010, 29, 379.
Release of reactive organic halogens by the brown macroalga Saccharina latissima after exposure to ultraviolet radiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltlGku7s%3D&md5=e2322a4e5564471780303e7096c1a6ccCAS |

[40]  P. D. Nightingale, G. Malin, P. S. Liss, Production of chloroform and other low-molecular-weight halocarbons by some species of macroalgae. Limnol. Oceanogr. 1995, 40, 680.
Production of chloroform and other low-molecular-weight halocarbons by some species of macroalgae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXos1GmsLs%3D&md5=2cb64aec84570c06e6f20d85c94479fdCAS |

[41]  A. Karlsson, N. Auer, D. Schulz-Bull, K. Abrahamsson, Cyanobacterial blooms in the Baltic- A source of halocarbons. Mar. Chem. 2008, 110, 129.
Cyanobacterial blooms in the Baltic- A source of halocarbons.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsFahsr8%3D&md5=6252ad18870c12f50262ad8f89db73a1CAS |

[42]  Bromochloromethane Testing Rationale, Tech. Rep. CAS 74-97-5 (NTIS 201-16826A) 2009 (US Environmental Agency: Washington, DC, USA).

[43]  W. C. Keene, M. A. K. Khalil, D. J. Erickson, A. McCulloch, T. E. Graedel, J. M. Lobert, M. L. Aucott, S. Ling Gong, D. B. Harper, G. Kleimann, P. M. Midgley, R. M. Moore, C. Seuzaret, W. T. Sturges, C. M. Benkowitz, V. Koropalov, L. A. Barrie, Y. F. Li, Composite global emissions of reactive chlorine from anthropogenic and natural sources: reactive chlorine emissions inventory. J. Geophys. Res. 1999, 104, 8429.
Composite global emissions of reactive chlorine from anthropogenic and natural sources: reactive chlorine emissions inventory.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjtFyluro%3D&md5=613bad9542849d000b36cbbe884fbd06CAS |

[44]  Chloroform, CICAD 58 2004 (World Health Organization: Geneva, Switzerland).

[45]  Toxicological Profile for Chloroform 1997 (Agency for Toxic Substances and Disease Registry: Atlanta, GA, USA).

[46]  T. Fujimori, Y. Yoneyama, G. Taniai, M. Kurihara, H. Tamegai, S. Hashimoto, Methyl halide production by cultures of marine proteobacteria Erythrobacter and Pseudomonas and isolated bacteria from brackish water. Limnol. Oceanogr. 2012, 57, 154.
Methyl halide production by cultures of marine proteobacteria Erythrobacter and Pseudomonas and isolated bacteria from brackish water.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XivVars70%3D&md5=01e3a1dd021924570087795e4bbc739dCAS |

[47]  K. Abrahamsson, A. Lorén, A. Wulff, S.-Å. Wängberg, Air–sea exchange of halocarbons: the influence of diurnal and regional variations and distribution of pigments. Deep Sea Res. Part II Top. Stud. Oceanogr. 2004, 51, 2789.
Air–sea exchange of halocarbons: the influence of diurnal and regional variations and distribution of pigments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVChu7zN&md5=c5f778d99a1d8939d6b1346ed73c97c3CAS |

[48]  C. Leblanc, C. Colin, A. Cosse, L. Delage, S. La Barre, P. Morin, B. Fiévet, C. Voiseux, Y. Ambroise, E. Verhaeghe, D. Amouroux, O. Donard, E. Tessier, P. Potin, Iodine transfers in the coastal marine environment: the key role of brown algae and of their vanadium-dependent haloperoxidases. Biochimie 2006, 88, 1773.
Iodine transfers in the coastal marine environment: the key role of brown algae and of their vanadium-dependent haloperoxidases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1Cis7vO&md5=ed5a576e0113bebeef8008eebdd11086CAS | 17007992PubMed |

[49]  X. Guan, Y. Du, Y.-L. Li, W. M. Kwok, D. L. Phillips, Comparison of the dehalogenation of polyhalomethanes and production of strong acids in aqueous and salt (NaCl) water environments: ultraviolet photolysis of CH2I2. J. Chem. Phys. 2004, 121, 8399.
Comparison of the dehalogenation of polyhalomethanes and production of strong acids in aqueous and salt (NaCl) water environments: ultraviolet photolysis of CH2I2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptFGmt7c%3D&md5=f5f30e10ef22b3f2fff965e852ba7421CAS | 15511161PubMed |

[50]  W. Meier-Augenstein, GC and IRMS technology for 13C and 15N analysis of organic compounds and related gases, in Handbook of Stable Isotope Analytical Techniques (Ed. P. de Groot) 2004, pp. 153–174 (Elsevier Science Publishers B.V.: Amsterdam).

[51]  G. F. Slater, B. S. Lollar, B. E. Sleep, E. A. Edwards, Variability in carbon isotopic fractionation during biodegradation of chlorinated ethenes: implications for field applications. Environ. Sci. Technol. 2001, 35, 901.
Variability in carbon isotopic fractionation during biodegradation of chlorinated ethenes: implications for field applications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvVOntQ%3D%3D&md5=6dbd52946e8e20dc06d5de3e1cde39e1CAS | 11351533PubMed |

[52]  M. Blessing, M. A. Jochmann, T. C. Schmidt, Pitfalls in compound-specific isotope analysis of environmental samples. Anal. Bioanal. Chem. 2008, 390, 591.
Pitfalls in compound-specific isotope analysis of environmental samples.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXis1SnsA%3D%3D&md5=e8c07906845eb978f4fcfd83b06e24e2CAS | 17901949PubMed |

[53]  M. H. O’Leary, Carbon isotope fractionation in plants. Phytochemistry 1981, 20, 553.
Carbon isotope fractionation in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXltFWlsLY%3D&md5=ba2d6bb060f3d17ce2497bbd4d9c569aCAS |

[54]  H. B. A. Prins, J. T. M. Elzenga, Bicarbonate utilization: function and mechanism. Aquat. Bot. 1989, 34, 59.
Bicarbonate utilization: function and mechanism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXltlSltLs%3D&md5=dfb6b6cc2e0346d11a1b1ae1e7a3c730CAS |

[55]  M. L. Fogel, L. A. Cifuentes, Isotope fractionation during primary production, in Organic Geochemistry (Eds M. H. Engel, S. A. Macko) 1993, pp. 73–98 (Plenum Press: New York).

[56]  J. A. Raven, C. S. Cockell, C. L. De La Rocha, The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2008, 363, 2641.
The evolution of inorganic carbon concentrating mechanisms in photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtV2qs77P&md5=6657d174a312c5d9beded270f899934fCAS | 18487130PubMed |

[57]  J. R. Reinfelder, Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Annu. Rev. Mar. Sci. 2011, 3, 291.
Carbon concentrating mechanisms in eukaryotic marine phytoplankton.Crossref | GoogleScholarGoogle Scholar |

[58]  P. D. Quay, S. R. Emerson, B. M. Quay, A. H. Devol, The carbon cycle for Lake Washington – a stable isotope study. Limnol. Oceanogr. 1986, 31, 596.
The carbon cycle for Lake Washington – a stable isotope study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xks1Gqt74%3D&md5=6518b53e4eb76c5845481b99a1a0dde1CAS |

[59]  A. L. Herczeg, R. G. Fairbanks, Anomalous carbon isotope fractionation between atmospheric CO2 and dissolved inorganic carbon induced by intense photosynthesis. Geochim. Cosmochim. Acta 1987, 51, 895.
Anomalous carbon isotope fractionation between atmospheric CO2 and dissolved inorganic carbon induced by intense photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXksVGrsLs%3D&md5=cdcbfe1ea761a5803d40b5dba649660dCAS |

[60]  B. Fry, S. C. Wainright, Diatom sources of 13C-rich carbon in marine food webs. Mar. Ecol. Prog. Ser. 1991, 76, 149.
Diatom sources of 13C-rich carbon in marine food webs.Crossref | GoogleScholarGoogle Scholar |

[61]  P. G. Falkowski, Species variability in the fractionation of 13C and 12C by marine phytoplankton. J. Plankton Res. 1991, 13, 21.