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Primary and Secondary Controls on Carbon-Isotopic Compositions of Sedimentary Organic Matter
PRIMARY AND SECONDARY CONTROLS ON CARBON-ISOTOPIC COMPOSITIONS OF SEDIMENTARY ORGANIC MATTER RAY TAKIGIKU1, BRIAN N. POPP1, MARCUS W. JOHNSON1, J.M. HAYESI*, PIERRE ALBRECHT2, HENRY J. CALLOT2 and RUBEN OCAMPO2 1Biogeochemical
Laboratories, Departments of Chemistry and Geology, Geology Building, Indiana University, Bloomington, IN 47405-51 01, U.S.A. 2Laboratoire de Chimie Organique des Substances Naturelles, Departement de Chimie, University Louis Pasteur, 67008 Strasbourg, France
ABSTRACT We have investigated the carbon-isotopic compositions of porphyrins (degradation products of chlorophyll) in sedimentary strata from greatly different environments of deposition and propose that they provide a basis for estimation of the isotopic composition of primary organic matter. Isotopic differences between primary organic matter and total organic carbon remaining in sediments must derive from secondary processes occurring in the water column or in sediments. Total organic carbon in the lacustrine Messel Shale (Eocene) is depleted C in these sediments is probably due in large part in 13C by 4 to 6%a relative to porphyrins. This depletion of 13C to the recapture of methane carbon, depleted in 13C, by methane-oxidizing bacteria. On the other hand, total or F mation (mid-Cretaceous) is enriched in C by up organic carbon in the marine sediments of the Greenhorn to 3.5%o relative to primary inputs. This enrichment in 13C most likely resulted from intensive aerobic reworking of organic matter by heterotrophic organisms. Keywords: porphyrin, 13C, heterotroph, methanogen, diagenesis, Eocene, lake, Cretaceous, pelagic.
INTRODUCTION
The biological community at and below the sediment—water interface is sustained by primary producers which synthesize an important portion of the organic matter reaching the sediments. A great deal happens to that primary organic matter before its reworked residues show up in fossil fuels or other forms of organic material in sedimentary rocks. Chemical effects of this avalanche of secondary processes are so diverse that resolution ofpaleoenvironmen-
* Corresponding author
tat signals and recognition of specific secondary processes is often difficult. In terms of processes and complexity, the pathway of carbon following primary synthesis of organic matter can be compared to the pathway of carbon in metabolism. In respiring heterotrophs, consistent metabolic patterns result in a fixed relationship between isotopic compositions of diet and feeding organism: the organism is enriched in 13C by approximately one permil relative to its diet (DeNiro and Epstein, 1978; Fry et al., 1983, 1984). In contrast, we have found that
4
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
total organic carbon (TIC) in the Messel Shale is depleted in 13C by at least 4%0 and possibly 6% relative to primary inputs (Hayes et al., 1987), and that TIC in North American midcontinental sedimentary rocks of Cretaceous (Cenomanian—Thr onian) age is enriched in 13C by up to 3.5% relative to primary inputs (Hayes et a1.,1989). Obviously, isotopic relationships between inputs and biomass in sediments are less uniform than those in respiring heterotrophs. The comparison between metabolism and geochemistry fails because secondary processes in natural environments are less uniform than metabolic processes. These secondary processes are affected by diverse factors, including productivity in the water column, rate of inorganic sedimentation, and 12 content of bottom water, among many others. Acting in response to them, different processes will predominate in different environments. As secondary processes change, so do patterns of carbon flow and, hence, isotopic fractionations. Observed variations in isotopic compositions of sediments must include signals indicative of these changes in secondary processes. Here, we report progress on the extraction and interpretation of those signals. If isotopic signals related to secondary processes are to be recognized, it is necessary to have some means of determining the isotopic composition of the primary organic material in any paleoenvironment under study. Mindful that primary organic material in most environments is of photosynthetic origin, we have introduced the hypothesis that tetrapyrrole pigments derived from chlorophyll can serve as "isotopic biomarkers" for primary producers (Takigiku et al., 1986; Hayes et al . , 1987, 1989) . Through knowledge of the isotopic composition of the tetrapyrrole portion of chloro-
phyll, the isotopic composition of numerous primary molecular species can be reconstructed. MATERIALS AND METHODS
Samples, geological setting Messel Shale. The sediments that now comprise the Messel Shale (Matthes,1968) accumulated 47 ± 2 Ma ago in anaerobic waters at the bottom of a lake (Von Koenigswald, 1980). Subsequent depths of burial have not exceeded 300 m, nor has the temperature of the shale exceeded 40° C (Arpino et al., 1972). Contents of organic carbon reach 25%, and preservation of molecular structures has been excellent (Chappe et al., 1981; Dastillung et al., 1980). Sixteen different geoporphyrins, including two derived from bacteriochlorophylls of the d series and thus indicative of the existence in the lake of an anaerobic photic zone, have been isolated and identified (Icampo et al., 1984, 1985a,b). Greenhorn Formation. Sediments (middle Cretaceous; Cenomanian—Turonian) sampled for this study are from an 18-m interval of a core drilled by Plains Resources and identified as the #1 Schoeck—Errington hole, Sherman County, northwestern Kahsas. These marine sediments, now buried about 700 m beneath the surface, include the Bridge Creek member and the upper portion of the Hartland Shale. The interval is dominated by many shale beds and punctuated by thinner, chalky to crystalline limestone beds. There is abundant evidence that the degree of oxygenation of bottom water during deposition of the Greenhorn Formation varied widely and repeatedly (e.g., Pratt, 1984; Zelt, 1985).
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
Analytical procedures Conventional techniques were employed for preparation of kerogen (Wedeking et al., 1983). Total extractable organic matter was obtained by Soxhlet extraction with 50/50 (v/v) dichloromethane-methanol for 72 h. Abundance of carbonate was determined by weight loss after acid leach (N 6 M HC1) and total organic carbon was determined from the yield of CO2 from combustion. Extract from the Messel Shale was further separated by chromatography on silica-gel (pre-packed, "Baker-10 disposable", extraction columns); n-hexane was used to elute saturated hydrocarbons, toluene to elute aromatic hydrocarbons, and methanol was used to elute the remaining polar sub-fractions. Geoporphyrins (Ocampo et a1.,1984; Ocampo et al., 1985a, b; Ocampo, 1980) and other biomarkers (Dastillung et al., 1980; Matter et al., 1970; Albrecht and Ourisson, 1969) were isolated and characterized in the course of earlier investigations. Ether-linked polyisoprenoids characteristic of archaebacteria were isolated by treatment of the polar subfraction with aqueous HI to form polyisoprenoid-iodidies, which were purified by chromatography on silica gel, chloroform eluent. Purity was assessed by comparison of chromatograms and mass spectra with authentic standards prepared from Methanobacterium thermoautotrophicum. Sub-fractions enriched in geoporphyrins were prepared from total extracts from the Greenhorn Formation samples using a prepacked "Bond-Slut" silica-gel column (Analytichem, Intl) . A 2% solution of methylene chloride in petroleum ether (b.p. 30-60° C) was used to elute saturated hydrocarbons and some aromatic compounds. Ethyl acetate was used to elute a
5
fraction containing both nickel- and vanadylgeoporphyrins, and compounds of intermediate polarity. The geoporphyrin subfractions were applied to silica gel 60 TLC plates (E. Merck) and eluted using hexane/ toluene/ethyl acetate (14/10/1, by volume). Approximately 1-cm wide bands containing nickel-geoporphyrins (Rf -- 0.84) and vanadyl-geoporphyrins (Rf - 0.16) were scraped from the plate, and collected by washing with methylene chloride. Geoporphyrins were further purified by repeating this procedure. The isotopic composition of carbonate was determined by analysis of CO2 evolved by reaction with phosphoric acid at 50° C (McCrea, 1950; Wachter and Hayes, 1985). Samples of CO2 for isotopic analysis were prepared by combustion of organic materials in sealed quartz tubes (Wedeking et al., 1983). Analytical uncertainty for all carbon and oxygen isotopic analyses was less than 0.1%0. All carbon-isotopic compositions are reported in parts per thousand relative to the PDB standard (Craig, 1957; Urey et al., 1951) . RESULTS AND DISCUSSION Messel shale The 13C contents of carbon fractions are summarized in Table 1. Structures of porphyrins and other biomarkers are shown in Fig. 1; probable sources, abundances, and isotopic compositions of these compounds are shown in Table 2. Hayes et al. (1987) have reviewed evidence indicating that these compounds are representative of primary inputs from dinoflagellate algae (with possible additions from brown algae and diatoms) and green photosynthetic bacteria. Porphyrins derived from oxygenic
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
6
~
2
1
R = CH2CH3
4 R=H
R' = CH3 ~
R = CH3
COON
I
COON
R = R = CH2CH3 R = CH2CH2CH3 R' = CH2CH3
9
14
Fig. 1. Structures of compounds for which isotopic compositions are reported. For methods of isolation see references cited in Table 2.
primary producers have isotopic compositions near —22% o; those from obligately anaerobic photosynthetic bacteria have isotopic compositions near —24%.
In order to develop an estimate of the isotopic composition of the organic carbon produced by the photoautotrophs which synthesized the porphyrin precursors, we
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
7
TABLE 1 Isotopic compositions of carbon fractions in the Messel Shale 13' CPD B,%0
Sample Identification Total Carbonate Kerogen Total Extractable Organic Material Total extract fractionated on Si02 column Hexane eluent Toluene eluent Methanol eluent Alkyl porphyrin fraction (Strasbourg) Total porphyrins (Bloomington) Acid porphyrin fraction (Strasbourg)
+7.34±0.12 -28.21±0.03 - 29.72±0.10 -33.66±0.14 -29.66±0.03 - 28.30±0.07 - 22.60±0.08 - 23.43±0.06 - 23.91±0.04
TABLE 2 Carbon isotopic compositions of individual biomarkers Structures
Molecular Precursorb
Reference` Related Organismd
2 5 4 3 1 6 8
Bchl d
1 3 3
7
Bchl d
3
9 10
Phytanyl ether Biphytanyl ether
e e
Chlc
1 2 Algae 2 Algae 1 Algae Algae Mixture Photosynthetic bacteria Photosynthetic bacteria Methanogen Methanogen
Abundance (ng/g)
d1 CRDB, o
1 2 1 4 5 12 3
-19.50±0.05 -21.58±0.13 -21.89±0.15 -21.92±0.08 -22.15±0.03 -23.12±0.04 -23.92±0.05
1
-23.96±0.06
-8 -16
-29.74±0.14 -29.88±0.12
aIdentified
in Fig. 1. in reference cited. `Initial report of isolation and structure and where possible on structural grounds, assignment of specific precursor. References are as follows: (1) Ocampo et al., 1984; (2) Ocampo et al., 1985a; (3) Ocampo et al., 1985b. dldentified by reference to natural distribution of biomarkers among organisms. Italicized assignments derive from Hayes et al., 1987. eHayes et al., 1987.
bldentified
note that the tetrapyrrole nucleus of chlorophyll is commonly enriched in 13C by about 0.5%0 relative to the total plant. Specifically, Park and Dunning (1961) reported that the chlorin nucleus of chlorophyll from
tomato leaves was enriched in 13C by 0.5%0 relative to the whole leaf. At Indiana (unpublished results of investigations by R. Takigiku, G. Vasquez, H. Gest, and J.M. Hayes), we have found that the chlorin nu-
8
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
cleus from Rhodopseudomonas capsulate is depleted in 13C by 0.01 %0 relative to total cells and that, in Chromatium vinosum, the chlorin nucleus is enriched by 0.73%0. In leaves from a beech tree, the enrichment was 0.66%. The inferred isotopic compositions (whole-organism averages) of the algae and photosynthetic bacteria in the Messel Lake are, therefore, approximately — 22.5 and —24.5%. The isotopic compositions of compounds synthesized by a C-3 photoautotroph typically cover a range of 8%0 or less. The "heaviest" components are enriched in 13C by approximately 3% relative to the average, and the "lightest" components, usually lipids, are depleted by approximately 5 % 0 (Deines, 1980) . The range of primary compositions expected within the Messel Shale is thus —19.5 to —29.5%0. The total concentration of porphyrins derived from oxygenic photoautotrophs is approximately 19 ng/g: that of porphyrins derived from photosynthetic bacteria is approximately 10 ng/g. If this is taken as indicating that two thirds of the primary organic material had an isotopic composition near —22.5% while the remaining third had an isotopic composition near —24.5%, it is concluded that the average isotopic composition of all primary inputs was near —23.2%0. This value exceeds that of preserved total organic material (Table 1) by 5.0%oo. By what secondary processes has the preserved TIC been depleted in 13C by 5%o relative to primary inputs? Selective loss of 13 C-enriched components can be excluded as the sole mechanism, even though the final value (-28.2%) is within the range probably covered by input compounds (-19.5 to — 29.5%o). If the loss of 13C-enriched components were the sole mechanism of isotopic fractionation, no materials lighter than — 29.5%o would be expected, and the
preservation of compounds with isotopic compositions heavier than about —27.5% would have to be minimized. As a result, a narrow range of isotopic compositions would be expected. Instead, it is found (Tables 1 and 2) that the materials present cover an isotopic range that has been broadened, not narrowed, relative to that in primary inputs. We conclude that at least some portion, and perhaps all, of the isotopic shift is due to addition by secondary processes of organic compounds depleted in 13C relative to primary inputs. Given the presence of biomarkers characteristic of methanogenic bacteria (9, 10), detailed consideration of the isotopic characteristics of bacteria involved in methane cycles had led us to conclude (Hayes et al., 1987) that the isotopic shift is probably due in large part to recapture of methane carbon, highly depleted in 13C, by methane-oxidizing ("methylotrophic") bacteria. Greenhorn formation Results of carbon-isotopic analyses of carbonates, porphyrins, and TIC are plotted as a function of depth in Fig. 2. The excursion in isotopic composition of marine carbonate already noted by others (recent review: Schianger et al., 1987) is evident just below the apparent C enomanian Turonian boundary. Except within that excursion, the isotopic compositions of carbonate and porphyrins appear well correlated. Correlations with d(TOC) are less clear, and, in order to examine this problem without prejudice imposed by subjectively placed curves, crossplots have been prepared (Fig. 3) . On this basis, it is evident that the correlation between d(porphyrins) and d(carbonate) is considerably better than that between d(TOC) and d(ca bonate). The correlation between isotopic compositions of carbonate and por-
9
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
Ni -GEOPORPHYRIN
TOTAL ORGANIC CARBON
TIC abundance
o <1% 1%<
D <2%
2%< 0 <4%
TURONIAN FORMATION
4%<. O filled = shales
Z
~ O
Z CENO MANIAN
w w cc
O
PRIMARY ORGANIC MATTER
•
•
I 0
CALCAREOUS SHALE~tt MARLY SHALE -' MARLSTONE
G
i
~
+
+2
i
+3 -28
.
i
LIMESTONE
.
.
-27
-26 13 L ~
~_,
~so
i
i -29 G
1 ~~
...........~'
• -28
-27
, -26
-25
-24
~
-23
)
Fig. 2. Carbon-isotopic compositions of carbonate, Ni-geoporphyrins and total organic carbon as a function of depth in the Greenhorn Formation. Increments in depth scale are 1 m. Symbols represent individual isotopic analyses. The points designated by open inverted triangles in the carbonate column represent samples with both (i) contents of Sr approximately two-fold lower than all other samples in the section (less than 600 ppm — often lower — whereas average is near 1100 ppm), and (ii) textures indicative of extensive recrystallization. As noted in the legend, symbols in the total organic carbon column indicate abundance of TIC, with open symbols representing bioturbated beds and filled symbols representing laminated beds. The heavy line drawn through carbonate points (visual fit) is intended to represent principal variations. In other plots, a lighter line has been employed for the same purpose. The heavy line in the porphyrin column is congruent with the carbonate line and has been shifted in order to bring it into the closest possible agreement with the porphyrin trend (the shift is –28.76%0). Variations in the isotopic composition of primary organic matter were inferred from that of Ni-geoporphyrins according to the relationship shown in Fig. 1.
phyrins is expected due to the isotopic relationships summarized in Fig. 4. Note that, if (i) there are no post-depositional shifts in isotopic compositions of carbonate and
chlorophyllides (D1 = 0, DCP = 0), and (ii) eP is constant, a constant isotopic difference is expected between sedimentary carbonates and tetrapyrroles.
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
10
t
y = 0.15c + -26.765 r2 = 0.024 i •
i
i
-25.5
•
% ~~-26.0
•
-
a-
• •
~ -26.5
~,~~ ~~ -27.0
.
•
•• .
•
~
•
• •
. ' ~~ • •
• -27.5
~
I
1
I
1
+1.5
+1.0
+0.5
d
13
I
+2.0
'-'CARBONATE
y = 0.703c + -28.44
r2 = 0.51
-26.5
-28.0
+0.5
+1.0
d13C CARBONATE o~oo
+1.5 (PDB)
+2.0
Fig. 3. Data from Fig. 2 replotted in order to allow examination of correlations between isotopic compositions of carbon phases for samples outside the isotopic excursion (711.5 - 715.0 m).
There is, of course, no guarantee that primary isotopic compositions have been preserved. As noted (Fig. 2) there is independent evidence that diagenetic processes have altered isotopic compositions of carbonate in some limestones. Although, for other samples, there is no independent evidence of diagenetic alteration, it is logical to suggest
that a portion of the scatter in the remaining carbonate points results from diagenetic processes that have not affected concentrations of trace elements or textural indicators significantly. The generally good correlation (except within the excursion) between the carbonate and porphyrin trend lines then suggests that diagenetic shifts of isotopic
11
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
i /
Diagenesis
H+
Cat+ f
_
3 ~i.n
3
i
DI
p~
H+
Cá +
~
"bicarbonate pumping" H+ H2O k J
t
7b
~-
+2.0%
'
Photosynthetic Fixation
3' ~.N2
H+ H2 0 +8.89'°°
+10.8%0
Fractionation of 13C by equilibrium isotope effects
Secondary Processes
*1.00
Cprimary er
= chlorophyllide—.. geoporphyrin
~
-- +0.5%o
D cp
D2
~
Fractionation of 13C by kinetic isotope effects
Fig. 4. Isotopic relationships associated with carbonate system and with fixation and burial of organic carbon. The equilibrium carbon isotopic fractionation among carbonate species is a function of temperature, pH and pCO2. Calculation of isotopic equilibrium and experiments performed at 25° C have yielded the following results. O'Leary (1984) determined e[CO2(aq)/CO2(g)] = —1.1%0. Values for e[HCO3-(aq)/CO2(g)] range from +6.2%0 (look et al., W74) to +8.3%0 (Abelson and Hoering,1961). Emrich et al. (1970) determined e[HCO3-(aq)/CaCO3] = —2%o at 25 ° C. Values for e[CaCO33CO2(g)] range from +8.9%0 (Vogel, 1959) to + 10.0%0 (Baertschi, 1957). The symbols er, D2, Dcr and Di are introduced to represent, respectively, the isotopic fractionation accompanying photosynthetic fixation of carbon by primary producers, the isotopic shift in TIC associated with reworking of primary organic material by all secondary processes (biological and thermal), the isotopic shift (if any) associated with production of geoporphyrins from primary chlorophyllides, and the carbon-isotopic shift (if any) associated with diagenetic stabilization of carbonate materials.
compositions of porphyrins have not been significantly larger than those of carbonates. Within the carbon-isotopic excursion, the failure to maintain a constant isotopic difference between carbonates and porphyrins might be due either to significant post-depositional shifts or to variations in er. We favor the latter alternative because the same pattern of varying levels of oxygenation evident elsewhere in the section persists within the excursion, and there are no changes in composition of kerogen or pristane—phytane ratio that suggest diagenetic effects occurring here were different than elsewhere in the section. Further, because the misfit between the porphyrin and carbonate records after the peak of the excursion is approximately constant, the observed deviations of almost 20 points within that interval could be explained by the single requirement that er temporarily decreased by approximately 0.45%0.
It is indicated in Fig. 4 that an isotopic fractionation (noted as D2) may accompany secondary processes (= all processes after primary production, including those occurring in the water column as well as diagenetic processes in sediments). Because the correlation between isotopic compositions of TIC and carbonate is poorer than that between those of nickel-geoporphyrins and carbonate, we conclude that secondary effects on the isotopic composition of TIC are significantly larger than those affecting the isotopic compositions of porphyrins and carbonates. It follows that variations in d(porphyrins) are more likely to record variations in d(primary organic matter) than are variations in d(TOC). The shaded region between the primary organic matter and TIC curves in Fig. 2 is representative of D2 (Fig. 4), the isotopic shift associated with secondary processes.
12
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
It is evident that D2 has not changed sharply in response to significant changes in bottom-water oxygenation indicated by changes in size and density of burrows. This suggests that an important component of these secondary processes may be occurring in the water column. Total organic carbon in the Greenhorn Formation is consistently enriched in 13C by about 0.8% relative to coexisting porphyrins (except in the excursion, where enrichments larger than 3%o are found). This difference reverses in sign and exceeds in magnitude the 0.5% depletion (TIC vs chlorophyllide) observed in fresh organic matter. The cause of this reversal is not known with certainty, but we suggest that it is a signal of oxidative reworking (details below) of primary organic matter prior to its immobilization in lithifried sediments. The Cenomanian–Turonian isotopic excursion has been ascribed to enhanced rates of burial of organic carbon in deep ocean basins during an oceanic anoxic event (Scholle and Arthur, 1980). Enhanced burial of organic carbon associated with a shift in the isotopic composition of marine carbonate indicates that the enhancement represented a shift in the overall balance of the global carbon cycle. As a consequence of increased burial of organic carbon, the global rate of production of 02 must also have increased, and that oxidant must have accumulated and/or been consumed at an enhanced rate by oxidizable materials other than organic carbon (Fe2+, sulfide). To whatever extent 12 accumulates at the same time ventilation of the deep ocean basins lags (a characteristic of an oceanic anoxic event), a strongly oxidizing surface environment is expected. Accordingly, we suspect that the larger values of A2 observed within the isotopic excursion are an indica-
tion of particularly intensive oxidative reworking of organic matter in shallow seas during that interval, at least at the location sampled by our core. We associate the isotopic shifts (primary material - sedimentary TIC) with effects of oxidative reworking because aerobic heterotrophs are enriched in 13C relative to their food source (DeNiro and Epstein, 1978; Fry et al., 1983, 1984). Investigations, both with laboratory cultures (e.g., DeNiro and Epstein, 1978; Monson and Hayes, 1983), and with organisms collected in the wild (e.g., Eadie, 1972; Millis et al., 1983; McConnaughey and McRoy, 1979; Fry et al., 1983, 1984), have demonstrated that heterotrophic activity results in an enrichment of . 1%0 (in total biomass) per trophic level. We observed a correlation between enrichment of 13C in TIC and the degree of bioturbation. In limestone samples with abundant evidence of bioturbation, indicating aerobic conditions, TIC is enriched in 13 C by + 1.3 ± 0.6% relative to Ni-porphyrins. In marly shale samples, which show a higher degree of lamination and have higher content of TIC, the enrichment is ±0.8 ± 0.5% . TIC in calcareous shale samples has the lowest enrichment, +0.7 ± 0.3%0, suggesting that it has been proportionately least affected by processes of aerobic heterotrophy a result expected based on the fine lamination and high carbon content of these shales. We are cautious about appealing to oxidation as an explanation of the observed enrichment of 13C in TIC because each stage of oxidative heterotrophy results in substantial losses of organic carbon. The pervasive nature of such effects in the modern ocean has, however, recently been noted (Cole et al., 1987), and it may be that this problem is not overwhelming.
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
13
CONCLUSION
REFERENCES
We have obtained results and developed hypotheses indicating that the carbonisotopic composition of primary organic matter in ancient environments can be determined by isotopic analyses of porphyrins. Further, it appears that isotopic differences (= D2, Fig. 4) between primary inputs and total organic carbon carry information about secondary processes affecting the organic carbon, and, thus, about the paleoecology of the water column and sediments. Specifically, total organic carbon in Messel Shale sediments is depleted in 13C relative to porphyrins known to derive from oxygenic photoautotrophs as well as those derived from photosynthetic bacteria. The wide range of isotopic compositions found in organic extract from these sediments, and the presence of biomarkers characteristic of methanogenic bacteria suggest that the recapture of methane carbon by methylotrophic bacteria most likely produced the observed isotopic shift. In the Greenhorn Formation, total organic carbon is consistently enriched in 13C relative to primary material. Respiring heterotrophs appear to be the organisms responsible for the secondary enrichment of 13C in TIC because variations in the extent of enrichment are well correlated with other paleoenvironmental indicators.
Abelson, P.H. and T.C. Hierin, 1961. Carbon isotopic fractionation in formation of amino acids by photosynthetic organisms. Proceedings of the National Academy of Science USA, 47:623-632 Albrecht, P. and G. Ourisson, 1969. Triterpene alcohol isolation from oil shale. Science, 163:1192-1193. Arpino, P., P. Albrecht and G. Ourisson, 1972. Studies on the organic constituents of lacustrine Eocene sediments. Possible mechanisms for the formation of some geolipids related to biologically occurring terpenoids. In: H.R. von Gaertner and H. Wehner (Editors), Advances in Organic Geochemistry, 1971. Pergamon Press, Oxford, pp. 173-187. Baertschi, P., 1957. Messung and Deutung relativer 0 and ~3 Haufi g keitsvari a otien n C in Karvon 180 bonatgesteninen and Mineralen, Schweizer. Mineralog. Petrog. Mitt., 37:73-152. Chappe, B., W. Michaelis and P. Albrecht, 1981. Molecular fossils of archaebacteria as selective degradation products of kerogen. In: A.G. Douglas and J.R. Maxwell (Editors), Advances in Organic Geochemistry, 1979. Pergamon Press, Oxford. pp. 265-274. Cole, J.J., S. Honjo and J. Erez, 1987. Benthic decomposition of organic matter at a deep-water site in the Panama Basin. Nature, 327:703-704. Craig, H., 1957. Isotopic standards for carbon and oxygen and correction factors for mass spectrometric analysis of carbon dioxide. Geochim. Cosmochim. Acta, 12:133-149. Dastillung, M., P. Albrecht and G. Ourisson, 1980. Aliphatic and polycyclic alcohols in sediments: hydroxylated derivatives of hopane and of 3methylhopane. J. Chem. Res., (S):166-167. Deines, P., 1980. The isotopic composition of reduced organic carbon. In: P. Fritz and J.C. Fontes (Editors), Handbook of Environmental Geochemistry: The Terrestrial Environment, Vol. 1. Elsevier, Amsterdam, pp. 329-406. Deniro, M.J. and S. Epstein, 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta, 42:495-506. Sadie, B.J., 1972. Distribution and fractionation of stable carbon isotopes in the Antarctic ecosystem. PhD. Thesis, Texas A&M University, College Station, Texas. Enrich, K., D.H. Shalt and J.C. Vogel, 1970. Carbon isotope fractionation during the precipitation of calcium carbonate. Earth Planet. Sci. Lett., 8:363-371. Fry, B., R.S. Scalan and P.L. Parker, 1983. 13C/12C ratios in marine food webs of the Torres Strait, Queensland. Austr. J. Mar. Freshwater Res., 34:707-715.
ACKNOWLEDGEMENTS
We are grateful for support from the NationalAeronautics and Space Administration (NGR 15-003-118). We thank S.A. Studley for technical assistance, L.M. Pratt and the U.S. Geological Survey for help in obtaining samples of the Schoeck—Errington core, and to J.L. Reichelderfer for Rock-Eval analyses.
14
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
Fry, B., R.K. Anderson,13 L. Entzeroth, J.L. Bird and
P.L. Parker, 1984. C enrichment and oceanic food web structure in the northwestern Gulf of Mexico. Contrib. to Mar. Sci., 27:45-65. Hayes, J.M., R. Takigiku, R. Ocamp. H.J. Callot and P. Albrecht, 1987. Isotopic compositions and probable origins of organic molecules in the Eocene Messel Shale. Nature, 329:48-51. Hayes, J.M., B.N. Popp, R. Takigiku and M.W. Johnson, 1989. An isotopic study of biogeochemical relationships between carbonates and organbic carbon in the Greenhorn Formation. Geochim. Cosmochim. Acta, in press. Matter , G., P. Albrecht and G. Ourisson, 1970. 4Methylsterols and sterols in Messel Shale (Eocene). J. Chem. Soc., Chem. Commun., 1570-1572. Matthes, G., 1968. Les couches Eocenes dan la region du fosse rhenan septentrional. Memoire Bur. Rech. Geol. Minieres, 58:327-337. McConnaughey, T. and C.P. McRoy, 1979. Food web structure and the fractionation of carbon isotopes in the Bering Sea. Mar. Biol., 53:257-262. McCrea, J.M., 1950. On the isotopic chemistry of carbonates and a paleotemperature scale. J. Chem. Phys., 18:849-857. Millis, E.L., K. Pittman and F.C. Tan, 1983. Food web structure on the Scotian shelf, eastern Canada. A study using 13C as a food-chain tracer. ICES Rap. Proces-Verbaux Reun., 183:111-118. Monson, K.D. and J.M. Hayes, 1983. Biosynthetic control of the natural abundance of carbon 13 at specific positions within fatty acids in Saccharomyces cerevisae. Isotope fractionation in lipid synthesis as evidence for peroxisomal regulation. J. Biol. Chem., 257:5568-5575. look, W.G., J.C. Bommerson and W.H. Staverman, 1974. Carbon isotope fractionation between dissolved bicarbonate and gaseous carbon dioxide. Earth Planet. Sci. Lett., 22:169-175. Ocampo, R., 1980. Porphyrins dans le schiste de Messel: Etude structurale et signification geochimique. PhD. Thesis, University Louis Pasteur, Strasbourg, France. Ocampo, R., H.J. Callot, P. Albrecht and J.P. Kintzinger, 1984. A novel chlorophyll c related petroporphyrin in oil shale. Tetrahedron Lett., 25:2589-2592. Ocampo, R., H.J. Callot and P. Albrecht, 1985a. Identification of polar porphyrins in oil shale. J. Chem. Soc., Chem. Commun., 198-200. Ocampo, R., H.J. Callot and P. Albrecht, 1985b. Occurrence of bacteriopetroporphyrins in oil shale. J. Chem. Soc., Chem. Commun., 200-201. O'Leary, M.H., 1984. Measurement of the isotope fractionation associated with diffusion of carbon dioxide in aqueous solution. J. Phys. Chem., 88:823-825.
Park, R. and H.N. Dunning, 1961. Stable carbon isotope studies of crude oils and their porphyrin aggregates. Geochim. Cosmochim. Acta, 22:99-105. Pratt, L.M., 1984. Influence of paleoenvironemntal factors on preservation of organic matter in Middle Cretaceous Greenhorn Formation, Pueblo, Colorado. Bull. Amer. Assoc. Petrol. Geol., 68:1146-1159. Schlanger, S.O., M.A. Arthur, H.C. Jenkyns and P.A. Scholle, 1987. The Cenomanian-Turonian oceanic anoxic event, I. Stratigraphy and distribution of organic-rich beds and the marine 813C excursion. In: J. Brooks and A.J. Fleet (Editors), Marine Petroleum Source Rocks. Geological Society of London, Special Publication No. 26. Blackwell, Oxford, pp. 371-399. Scholle, P.A. and M.A. Arthur, 1980. Carbon isotope fluctuations in Cretaceous pelagic limestones: Potential stratigraphic and petroleum exploration tool. Bull. Amer. Assoc. Petrol. Geil., 64:67-87. Takigiku, R., B.N. Popp, M.W. Johnson and J.M. Hayes, 1986. Coupled variations in carbonisotopic compositions of carbonates, total organic carbon, and geoporphyrins (abstr.), Geil. Soc. America Ann. Meet., 18:769. Urey, H.C., H.A. Lowenstam, S. Epstein and C.R. McKinney, 1951. Measurement of paleotemperatures and temperatures of the upper Cretaceous of England, Denmark, and southeastern United States. Bull. Geil. Soc. America, 62:399-416. Vogel, J.C., 1959. Isotopen Trennfaktoren des Kohlenstoffs im Gleichgewichtssystem KohlendioxydBikarbonat-Karbonat. Ph.D. Thesis, Heidelberg Univ. 196 p. von Koenigswald, W., 1980. Fossilagerstatte Messel - Literaturubersicht der Forschungergebnisse aus den Jahren 1969-1979. Geil. Jb. Hessen, 108:23-38. Wachter, E.A. and J.M. Hayes, 1985. Exchange of oxygen isotopes in carbon isotopes in carbon dioxide-phosphoric acid systems. Chem. Geil. (Isotope Geoscience), 52:365-374. Wedeking, K.W., J.M. Hayes and U. Matzigkeit, 1983. Procedures of organic geochemical analysis. In: J.W. Schopf (Editor), Earth's Earliest Biosphere: Its Origin and Evolution. Princeton University Press, Princeton, pp. 428-441. Zelt, F.B ., 1985. Paleoceanographic events and lithologic/geochemical facies of the Greenhorn marine cycle (upper Cretaceous) examined using natural gamma-ray spectroscopy. In: L.M. Pratt, E.G. Kauffman and F.B. Zelt (Editors), Finegrained Deposits and Biofacies of the Cretaceous Western Interior Seaway: Evidence of Cyclic Sedimentary Processes. Society of Economic Paleontologists and Mineralogists Guidebook No. 9, pp. 49-59.
Laboratories, Departments of Chemistry and Geology, Geology Building, Indiana University, Bloomington, IN 47405-51 01, U.S.A. 2Laboratoire de Chimie Organique des Substances Naturelles, Departement de Chimie, University Louis Pasteur, 67008 Strasbourg, France
ABSTRACT We have investigated the carbon-isotopic compositions of porphyrins (degradation products of chlorophyll) in sedimentary strata from greatly different environments of deposition and propose that they provide a basis for estimation of the isotopic composition of primary organic matter. Isotopic differences between primary organic matter and total organic carbon remaining in sediments must derive from secondary processes occurring in the water column or in sediments. Total organic carbon in the lacustrine Messel Shale (Eocene) is depleted C in these sediments is probably due in large part in 13C by 4 to 6%a relative to porphyrins. This depletion of 13C to the recapture of methane carbon, depleted in 13C, by methane-oxidizing bacteria. On the other hand, total or F mation (mid-Cretaceous) is enriched in C by up organic carbon in the marine sediments of the Greenhorn to 3.5%o relative to primary inputs. This enrichment in 13C most likely resulted from intensive aerobic reworking of organic matter by heterotrophic organisms. Keywords: porphyrin, 13C, heterotroph, methanogen, diagenesis, Eocene, lake, Cretaceous, pelagic.
INTRODUCTION
The biological community at and below the sediment—water interface is sustained by primary producers which synthesize an important portion of the organic matter reaching the sediments. A great deal happens to that primary organic matter before its reworked residues show up in fossil fuels or other forms of organic material in sedimentary rocks. Chemical effects of this avalanche of secondary processes are so diverse that resolution ofpaleoenvironmen-
* Corresponding author
tat signals and recognition of specific secondary processes is often difficult. In terms of processes and complexity, the pathway of carbon following primary synthesis of organic matter can be compared to the pathway of carbon in metabolism. In respiring heterotrophs, consistent metabolic patterns result in a fixed relationship between isotopic compositions of diet and feeding organism: the organism is enriched in 13C by approximately one permil relative to its diet (DeNiro and Epstein, 1978; Fry et al., 1983, 1984). In contrast, we have found that
4
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
total organic carbon (TIC) in the Messel Shale is depleted in 13C by at least 4%0 and possibly 6% relative to primary inputs (Hayes et al., 1987), and that TIC in North American midcontinental sedimentary rocks of Cretaceous (Cenomanian—Thr onian) age is enriched in 13C by up to 3.5% relative to primary inputs (Hayes et a1.,1989). Obviously, isotopic relationships between inputs and biomass in sediments are less uniform than those in respiring heterotrophs. The comparison between metabolism and geochemistry fails because secondary processes in natural environments are less uniform than metabolic processes. These secondary processes are affected by diverse factors, including productivity in the water column, rate of inorganic sedimentation, and 12 content of bottom water, among many others. Acting in response to them, different processes will predominate in different environments. As secondary processes change, so do patterns of carbon flow and, hence, isotopic fractionations. Observed variations in isotopic compositions of sediments must include signals indicative of these changes in secondary processes. Here, we report progress on the extraction and interpretation of those signals. If isotopic signals related to secondary processes are to be recognized, it is necessary to have some means of determining the isotopic composition of the primary organic material in any paleoenvironment under study. Mindful that primary organic material in most environments is of photosynthetic origin, we have introduced the hypothesis that tetrapyrrole pigments derived from chlorophyll can serve as "isotopic biomarkers" for primary producers (Takigiku et al., 1986; Hayes et al . , 1987, 1989) . Through knowledge of the isotopic composition of the tetrapyrrole portion of chloro-
phyll, the isotopic composition of numerous primary molecular species can be reconstructed. MATERIALS AND METHODS
Samples, geological setting Messel Shale. The sediments that now comprise the Messel Shale (Matthes,1968) accumulated 47 ± 2 Ma ago in anaerobic waters at the bottom of a lake (Von Koenigswald, 1980). Subsequent depths of burial have not exceeded 300 m, nor has the temperature of the shale exceeded 40° C (Arpino et al., 1972). Contents of organic carbon reach 25%, and preservation of molecular structures has been excellent (Chappe et al., 1981; Dastillung et al., 1980). Sixteen different geoporphyrins, including two derived from bacteriochlorophylls of the d series and thus indicative of the existence in the lake of an anaerobic photic zone, have been isolated and identified (Icampo et al., 1984, 1985a,b). Greenhorn Formation. Sediments (middle Cretaceous; Cenomanian—Turonian) sampled for this study are from an 18-m interval of a core drilled by Plains Resources and identified as the #1 Schoeck—Errington hole, Sherman County, northwestern Kahsas. These marine sediments, now buried about 700 m beneath the surface, include the Bridge Creek member and the upper portion of the Hartland Shale. The interval is dominated by many shale beds and punctuated by thinner, chalky to crystalline limestone beds. There is abundant evidence that the degree of oxygenation of bottom water during deposition of the Greenhorn Formation varied widely and repeatedly (e.g., Pratt, 1984; Zelt, 1985).
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
Analytical procedures Conventional techniques were employed for preparation of kerogen (Wedeking et al., 1983). Total extractable organic matter was obtained by Soxhlet extraction with 50/50 (v/v) dichloromethane-methanol for 72 h. Abundance of carbonate was determined by weight loss after acid leach (N 6 M HC1) and total organic carbon was determined from the yield of CO2 from combustion. Extract from the Messel Shale was further separated by chromatography on silica-gel (pre-packed, "Baker-10 disposable", extraction columns); n-hexane was used to elute saturated hydrocarbons, toluene to elute aromatic hydrocarbons, and methanol was used to elute the remaining polar sub-fractions. Geoporphyrins (Ocampo et a1.,1984; Ocampo et al., 1985a, b; Ocampo, 1980) and other biomarkers (Dastillung et al., 1980; Matter et al., 1970; Albrecht and Ourisson, 1969) were isolated and characterized in the course of earlier investigations. Ether-linked polyisoprenoids characteristic of archaebacteria were isolated by treatment of the polar subfraction with aqueous HI to form polyisoprenoid-iodidies, which were purified by chromatography on silica gel, chloroform eluent. Purity was assessed by comparison of chromatograms and mass spectra with authentic standards prepared from Methanobacterium thermoautotrophicum. Sub-fractions enriched in geoporphyrins were prepared from total extracts from the Greenhorn Formation samples using a prepacked "Bond-Slut" silica-gel column (Analytichem, Intl) . A 2% solution of methylene chloride in petroleum ether (b.p. 30-60° C) was used to elute saturated hydrocarbons and some aromatic compounds. Ethyl acetate was used to elute a
5
fraction containing both nickel- and vanadylgeoporphyrins, and compounds of intermediate polarity. The geoporphyrin subfractions were applied to silica gel 60 TLC plates (E. Merck) and eluted using hexane/ toluene/ethyl acetate (14/10/1, by volume). Approximately 1-cm wide bands containing nickel-geoporphyrins (Rf -- 0.84) and vanadyl-geoporphyrins (Rf - 0.16) were scraped from the plate, and collected by washing with methylene chloride. Geoporphyrins were further purified by repeating this procedure. The isotopic composition of carbonate was determined by analysis of CO2 evolved by reaction with phosphoric acid at 50° C (McCrea, 1950; Wachter and Hayes, 1985). Samples of CO2 for isotopic analysis were prepared by combustion of organic materials in sealed quartz tubes (Wedeking et al., 1983). Analytical uncertainty for all carbon and oxygen isotopic analyses was less than 0.1%0. All carbon-isotopic compositions are reported in parts per thousand relative to the PDB standard (Craig, 1957; Urey et al., 1951) . RESULTS AND DISCUSSION Messel shale The 13C contents of carbon fractions are summarized in Table 1. Structures of porphyrins and other biomarkers are shown in Fig. 1; probable sources, abundances, and isotopic compositions of these compounds are shown in Table 2. Hayes et al. (1987) have reviewed evidence indicating that these compounds are representative of primary inputs from dinoflagellate algae (with possible additions from brown algae and diatoms) and green photosynthetic bacteria. Porphyrins derived from oxygenic
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
6
~
2
1
R = CH2CH3
4 R=H
R' = CH3 ~
R = CH3
COON
I
COON
R = R = CH2CH3 R = CH2CH2CH3 R' = CH2CH3
9
14
Fig. 1. Structures of compounds for which isotopic compositions are reported. For methods of isolation see references cited in Table 2.
primary producers have isotopic compositions near —22% o; those from obligately anaerobic photosynthetic bacteria have isotopic compositions near —24%.
In order to develop an estimate of the isotopic composition of the organic carbon produced by the photoautotrophs which synthesized the porphyrin precursors, we
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
7
TABLE 1 Isotopic compositions of carbon fractions in the Messel Shale 13' CPD B,%0
Sample Identification Total Carbonate Kerogen Total Extractable Organic Material Total extract fractionated on Si02 column Hexane eluent Toluene eluent Methanol eluent Alkyl porphyrin fraction (Strasbourg) Total porphyrins (Bloomington) Acid porphyrin fraction (Strasbourg)
+7.34±0.12 -28.21±0.03 - 29.72±0.10 -33.66±0.14 -29.66±0.03 - 28.30±0.07 - 22.60±0.08 - 23.43±0.06 - 23.91±0.04
TABLE 2 Carbon isotopic compositions of individual biomarkers Structures
Molecular Precursorb
Reference` Related Organismd
2 5 4 3 1 6 8
Bchl d
1 3 3
7
Bchl d
3
9 10
Phytanyl ether Biphytanyl ether
e e
Chlc
1 2 Algae 2 Algae 1 Algae Algae Mixture Photosynthetic bacteria Photosynthetic bacteria Methanogen Methanogen
Abundance (ng/g)
d1 CRDB, o
1 2 1 4 5 12 3
-19.50±0.05 -21.58±0.13 -21.89±0.15 -21.92±0.08 -22.15±0.03 -23.12±0.04 -23.92±0.05
1
-23.96±0.06
-8 -16
-29.74±0.14 -29.88±0.12
aIdentified
in Fig. 1. in reference cited. `Initial report of isolation and structure and where possible on structural grounds, assignment of specific precursor. References are as follows: (1) Ocampo et al., 1984; (2) Ocampo et al., 1985a; (3) Ocampo et al., 1985b. dldentified by reference to natural distribution of biomarkers among organisms. Italicized assignments derive from Hayes et al., 1987. eHayes et al., 1987.
bldentified
note that the tetrapyrrole nucleus of chlorophyll is commonly enriched in 13C by about 0.5%0 relative to the total plant. Specifically, Park and Dunning (1961) reported that the chlorin nucleus of chlorophyll from
tomato leaves was enriched in 13C by 0.5%0 relative to the whole leaf. At Indiana (unpublished results of investigations by R. Takigiku, G. Vasquez, H. Gest, and J.M. Hayes), we have found that the chlorin nu-
8
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
cleus from Rhodopseudomonas capsulate is depleted in 13C by 0.01 %0 relative to total cells and that, in Chromatium vinosum, the chlorin nucleus is enriched by 0.73%0. In leaves from a beech tree, the enrichment was 0.66%. The inferred isotopic compositions (whole-organism averages) of the algae and photosynthetic bacteria in the Messel Lake are, therefore, approximately — 22.5 and —24.5%. The isotopic compositions of compounds synthesized by a C-3 photoautotroph typically cover a range of 8%0 or less. The "heaviest" components are enriched in 13C by approximately 3% relative to the average, and the "lightest" components, usually lipids, are depleted by approximately 5 % 0 (Deines, 1980) . The range of primary compositions expected within the Messel Shale is thus —19.5 to —29.5%0. The total concentration of porphyrins derived from oxygenic photoautotrophs is approximately 19 ng/g: that of porphyrins derived from photosynthetic bacteria is approximately 10 ng/g. If this is taken as indicating that two thirds of the primary organic material had an isotopic composition near —22.5% while the remaining third had an isotopic composition near —24.5%, it is concluded that the average isotopic composition of all primary inputs was near —23.2%0. This value exceeds that of preserved total organic material (Table 1) by 5.0%oo. By what secondary processes has the preserved TIC been depleted in 13C by 5%o relative to primary inputs? Selective loss of 13 C-enriched components can be excluded as the sole mechanism, even though the final value (-28.2%) is within the range probably covered by input compounds (-19.5 to — 29.5%o). If the loss of 13C-enriched components were the sole mechanism of isotopic fractionation, no materials lighter than — 29.5%o would be expected, and the
preservation of compounds with isotopic compositions heavier than about —27.5% would have to be minimized. As a result, a narrow range of isotopic compositions would be expected. Instead, it is found (Tables 1 and 2) that the materials present cover an isotopic range that has been broadened, not narrowed, relative to that in primary inputs. We conclude that at least some portion, and perhaps all, of the isotopic shift is due to addition by secondary processes of organic compounds depleted in 13C relative to primary inputs. Given the presence of biomarkers characteristic of methanogenic bacteria (9, 10), detailed consideration of the isotopic characteristics of bacteria involved in methane cycles had led us to conclude (Hayes et al., 1987) that the isotopic shift is probably due in large part to recapture of methane carbon, highly depleted in 13C, by methane-oxidizing ("methylotrophic") bacteria. Greenhorn formation Results of carbon-isotopic analyses of carbonates, porphyrins, and TIC are plotted as a function of depth in Fig. 2. The excursion in isotopic composition of marine carbonate already noted by others (recent review: Schianger et al., 1987) is evident just below the apparent C enomanian Turonian boundary. Except within that excursion, the isotopic compositions of carbonate and porphyrins appear well correlated. Correlations with d(TOC) are less clear, and, in order to examine this problem without prejudice imposed by subjectively placed curves, crossplots have been prepared (Fig. 3) . On this basis, it is evident that the correlation between d(porphyrins) and d(carbonate) is considerably better than that between d(TOC) and d(ca bonate). The correlation between isotopic compositions of carbonate and por-
9
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
Ni -GEOPORPHYRIN
TOTAL ORGANIC CARBON
TIC abundance
o <1% 1%<
D <2%
2%< 0 <4%
TURONIAN FORMATION
4%<. O filled = shales
Z
~ O
Z CENO MANIAN
w w cc
O
PRIMARY ORGANIC MATTER
•
•
I 0
CALCAREOUS SHALE~tt MARLY SHALE -' MARLSTONE
G
i
~
+
+2
i
+3 -28
.
i
LIMESTONE
.
.
-27
-26 13 L ~
~_,
~so
i
i -29 G
1 ~~
...........~'
• -28
-27
, -26
-25
-24
~
-23
)
Fig. 2. Carbon-isotopic compositions of carbonate, Ni-geoporphyrins and total organic carbon as a function of depth in the Greenhorn Formation. Increments in depth scale are 1 m. Symbols represent individual isotopic analyses. The points designated by open inverted triangles in the carbonate column represent samples with both (i) contents of Sr approximately two-fold lower than all other samples in the section (less than 600 ppm — often lower — whereas average is near 1100 ppm), and (ii) textures indicative of extensive recrystallization. As noted in the legend, symbols in the total organic carbon column indicate abundance of TIC, with open symbols representing bioturbated beds and filled symbols representing laminated beds. The heavy line drawn through carbonate points (visual fit) is intended to represent principal variations. In other plots, a lighter line has been employed for the same purpose. The heavy line in the porphyrin column is congruent with the carbonate line and has been shifted in order to bring it into the closest possible agreement with the porphyrin trend (the shift is –28.76%0). Variations in the isotopic composition of primary organic matter were inferred from that of Ni-geoporphyrins according to the relationship shown in Fig. 1.
phyrins is expected due to the isotopic relationships summarized in Fig. 4. Note that, if (i) there are no post-depositional shifts in isotopic compositions of carbonate and
chlorophyllides (D1 = 0, DCP = 0), and (ii) eP is constant, a constant isotopic difference is expected between sedimentary carbonates and tetrapyrroles.
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
10
t
y = 0.15c + -26.765 r2 = 0.024 i •
i
i
-25.5
•
% ~~-26.0
•
-
a-
• •
~ -26.5
~,~~ ~~ -27.0
.
•
•• .
•
~
•
• •
. ' ~~ • •
• -27.5
~
I
1
I
1
+1.5
+1.0
+0.5
d
13
I
+2.0
'-'CARBONATE
y = 0.703c + -28.44
r2 = 0.51
-26.5
-28.0
+0.5
+1.0
d13C CARBONATE o~oo
+1.5 (PDB)
+2.0
Fig. 3. Data from Fig. 2 replotted in order to allow examination of correlations between isotopic compositions of carbon phases for samples outside the isotopic excursion (711.5 - 715.0 m).
There is, of course, no guarantee that primary isotopic compositions have been preserved. As noted (Fig. 2) there is independent evidence that diagenetic processes have altered isotopic compositions of carbonate in some limestones. Although, for other samples, there is no independent evidence of diagenetic alteration, it is logical to suggest
that a portion of the scatter in the remaining carbonate points results from diagenetic processes that have not affected concentrations of trace elements or textural indicators significantly. The generally good correlation (except within the excursion) between the carbonate and porphyrin trend lines then suggests that diagenetic shifts of isotopic
11
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
i /
Diagenesis
H+
Cat+ f
_
3 ~i.n
3
i
DI
p~
H+
Cá +
~
"bicarbonate pumping" H+ H2O k J
t
7b
~-
+2.0%
'
Photosynthetic Fixation
3' ~.N2
H+ H2 0 +8.89'°°
+10.8%0
Fractionation of 13C by equilibrium isotope effects
Secondary Processes
*1.00
Cprimary er
= chlorophyllide—.. geoporphyrin
~
-- +0.5%o
D cp
D2
~
Fractionation of 13C by kinetic isotope effects
Fig. 4. Isotopic relationships associated with carbonate system and with fixation and burial of organic carbon. The equilibrium carbon isotopic fractionation among carbonate species is a function of temperature, pH and pCO2. Calculation of isotopic equilibrium and experiments performed at 25° C have yielded the following results. O'Leary (1984) determined e[CO2(aq)/CO2(g)] = —1.1%0. Values for e[HCO3-(aq)/CO2(g)] range from +6.2%0 (look et al., W74) to +8.3%0 (Abelson and Hoering,1961). Emrich et al. (1970) determined e[HCO3-(aq)/CaCO3] = —2%o at 25 ° C. Values for e[CaCO33CO2(g)] range from +8.9%0 (Vogel, 1959) to + 10.0%0 (Baertschi, 1957). The symbols er, D2, Dcr and Di are introduced to represent, respectively, the isotopic fractionation accompanying photosynthetic fixation of carbon by primary producers, the isotopic shift in TIC associated with reworking of primary organic material by all secondary processes (biological and thermal), the isotopic shift (if any) associated with production of geoporphyrins from primary chlorophyllides, and the carbon-isotopic shift (if any) associated with diagenetic stabilization of carbonate materials.
compositions of porphyrins have not been significantly larger than those of carbonates. Within the carbon-isotopic excursion, the failure to maintain a constant isotopic difference between carbonates and porphyrins might be due either to significant post-depositional shifts or to variations in er. We favor the latter alternative because the same pattern of varying levels of oxygenation evident elsewhere in the section persists within the excursion, and there are no changes in composition of kerogen or pristane—phytane ratio that suggest diagenetic effects occurring here were different than elsewhere in the section. Further, because the misfit between the porphyrin and carbonate records after the peak of the excursion is approximately constant, the observed deviations of almost 20 points within that interval could be explained by the single requirement that er temporarily decreased by approximately 0.45%0.
It is indicated in Fig. 4 that an isotopic fractionation (noted as D2) may accompany secondary processes (= all processes after primary production, including those occurring in the water column as well as diagenetic processes in sediments). Because the correlation between isotopic compositions of TIC and carbonate is poorer than that between those of nickel-geoporphyrins and carbonate, we conclude that secondary effects on the isotopic composition of TIC are significantly larger than those affecting the isotopic compositions of porphyrins and carbonates. It follows that variations in d(porphyrins) are more likely to record variations in d(primary organic matter) than are variations in d(TOC). The shaded region between the primary organic matter and TIC curves in Fig. 2 is representative of D2 (Fig. 4), the isotopic shift associated with secondary processes.
12
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
It is evident that D2 has not changed sharply in response to significant changes in bottom-water oxygenation indicated by changes in size and density of burrows. This suggests that an important component of these secondary processes may be occurring in the water column. Total organic carbon in the Greenhorn Formation is consistently enriched in 13C by about 0.8% relative to coexisting porphyrins (except in the excursion, where enrichments larger than 3%o are found). This difference reverses in sign and exceeds in magnitude the 0.5% depletion (TIC vs chlorophyllide) observed in fresh organic matter. The cause of this reversal is not known with certainty, but we suggest that it is a signal of oxidative reworking (details below) of primary organic matter prior to its immobilization in lithifried sediments. The Cenomanian–Turonian isotopic excursion has been ascribed to enhanced rates of burial of organic carbon in deep ocean basins during an oceanic anoxic event (Scholle and Arthur, 1980). Enhanced burial of organic carbon associated with a shift in the isotopic composition of marine carbonate indicates that the enhancement represented a shift in the overall balance of the global carbon cycle. As a consequence of increased burial of organic carbon, the global rate of production of 02 must also have increased, and that oxidant must have accumulated and/or been consumed at an enhanced rate by oxidizable materials other than organic carbon (Fe2+, sulfide). To whatever extent 12 accumulates at the same time ventilation of the deep ocean basins lags (a characteristic of an oceanic anoxic event), a strongly oxidizing surface environment is expected. Accordingly, we suspect that the larger values of A2 observed within the isotopic excursion are an indica-
tion of particularly intensive oxidative reworking of organic matter in shallow seas during that interval, at least at the location sampled by our core. We associate the isotopic shifts (primary material - sedimentary TIC) with effects of oxidative reworking because aerobic heterotrophs are enriched in 13C relative to their food source (DeNiro and Epstein, 1978; Fry et al., 1983, 1984). Investigations, both with laboratory cultures (e.g., DeNiro and Epstein, 1978; Monson and Hayes, 1983), and with organisms collected in the wild (e.g., Eadie, 1972; Millis et al., 1983; McConnaughey and McRoy, 1979; Fry et al., 1983, 1984), have demonstrated that heterotrophic activity results in an enrichment of . 1%0 (in total biomass) per trophic level. We observed a correlation between enrichment of 13C in TIC and the degree of bioturbation. In limestone samples with abundant evidence of bioturbation, indicating aerobic conditions, TIC is enriched in 13 C by + 1.3 ± 0.6% relative to Ni-porphyrins. In marly shale samples, which show a higher degree of lamination and have higher content of TIC, the enrichment is ±0.8 ± 0.5% . TIC in calcareous shale samples has the lowest enrichment, +0.7 ± 0.3%0, suggesting that it has been proportionately least affected by processes of aerobic heterotrophy a result expected based on the fine lamination and high carbon content of these shales. We are cautious about appealing to oxidation as an explanation of the observed enrichment of 13C in TIC because each stage of oxidative heterotrophy results in substantial losses of organic carbon. The pervasive nature of such effects in the modern ocean has, however, recently been noted (Cole et al., 1987), and it may be that this problem is not overwhelming.
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
13
CONCLUSION
REFERENCES
We have obtained results and developed hypotheses indicating that the carbonisotopic composition of primary organic matter in ancient environments can be determined by isotopic analyses of porphyrins. Further, it appears that isotopic differences (= D2, Fig. 4) between primary inputs and total organic carbon carry information about secondary processes affecting the organic carbon, and, thus, about the paleoecology of the water column and sediments. Specifically, total organic carbon in Messel Shale sediments is depleted in 13C relative to porphyrins known to derive from oxygenic photoautotrophs as well as those derived from photosynthetic bacteria. The wide range of isotopic compositions found in organic extract from these sediments, and the presence of biomarkers characteristic of methanogenic bacteria suggest that the recapture of methane carbon by methylotrophic bacteria most likely produced the observed isotopic shift. In the Greenhorn Formation, total organic carbon is consistently enriched in 13C relative to primary material. Respiring heterotrophs appear to be the organisms responsible for the secondary enrichment of 13C in TIC because variations in the extent of enrichment are well correlated with other paleoenvironmental indicators.
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ACKNOWLEDGEMENTS
We are grateful for support from the NationalAeronautics and Space Administration (NGR 15-003-118). We thank S.A. Studley for technical assistance, L.M. Pratt and the U.S. Geological Survey for help in obtaining samples of the Schoeck—Errington core, and to J.L. Reichelderfer for Rock-Eval analyses.
14
CONTROLS ON ISOTOPIC COMPOSITION OF ORGANIC MATTER
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