1998 - Carbon Isotopic Fractionation by Plankton in the Southern Indian Ocean - Relationship Between...

8/11/2019 1998 - Carbon Isotopic Fractionation by Plankton in the Southern Indian Ocean - Relationship Between 13C of Particulate Organic Carbon and Dissolved

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.Journal of Marine Systems 17 1998 3958

Carbon isotopic fractionation by plankton in the Southern IndianOcean: relationship between d

13C of particulate organic carbon

and dissolved carbon dioxide

I. Bentaleb a,f,1, M. Fontugne a,), C. Descolas-Gros b, C. Girardin c, A. Mariotti c,C. Pierre d, C. Brunet e, A. Poisson e

aCentre des Faibles Radioactiites, Laboratoire mixte CNRSr CEA, Domaine du CNRS, 91198 Gif-sur-Yette Cedex, France

bUniersite Montpellier II URA 1355, CC 093, 34095 Montpellier Cedex 05, France

c Uniersite P. and M. Curie, INRA, Laboratoire Biogeochimie des Isotopes Stables, 4, place Jussieu, 75252 Paris Cedex 05, France d

LODYC, Uniersite P. and M. Curie, 4, place Jussieu 75252 Paris Cedex 05, Francee

LPCM, Uniersite P. and M. Curie, 4, place Jussieu 75252 Paris Cedex 05, Francef

Department of Enironmental Chemistry, CID-CSIC, 1826 Jordi Girona, 08034 Barcelona, Spain

Received 15 October 1995; accepted 15 April 1996

Abstract

.Simultaneous measurements of chlorophyll a, carboxylase activities Rubisco and bcarboxylases in phytoplankton, 13 .organic carbon content and isotopic composition d C of suspended particulate organic matter, and partial pressure ofPOC .

carbon dioxide in surface seawater were performed during the end of summer 1992, in the South Indian Ocean. Results

.indicate that plankton populations display different carbon metabolisms on both sides of the subtropical convergence STC .North of STC, planktonic communities appeared to be dominated by mixorheterotrophs, while south of STC, physiological . .bCrR ratio or biomass C rChl parameters are characteristic of autotrophic phytoplankton. The isotopic fractionationPOC . . 13 between dissolved CO and SPOM is different for these two populations. Only d C values of flora dominated byp 2diatoms south of the STC part showed a strong correlation with dissolved CO concentrations which permitted a relationship2between these parameters for the Southern Ocean.

Resume

.Des mesures simultanees de chlorophylle, des activites des carboxylases Rubisco etbcarboxylases du phytoplancton, de 13 .la teneur et de la composition isotopique d C de la matiere organique particulaire en suspension et les pressions`POC .

partielles de CO dans les eaux de surface ont ete effectuees a la fin de lete 1992 dans le sud de locean Indien. Les ` 2

.resultats indiquent que, de part et dautre de la convergence subtropical STC , les populations phytoplanctoniquespresentent des metabolismes dassimilation du carbone differents. Au nord de la convergence, les communautes sont

.dominees par les organismes mixorheterotrophes alors quau sud les parametres physiologiques rapports bCrR et de `

)Corresponding author. Laboratoire des Sciences de Climat et de lEnvironnement, UMR 1572 CEA rCNRS, Domaine du CNRS, 91198

Gif sur Yvette Cedex, France. Tel.: q33-1-6982-3525; Fax:q33-1-6982-3568; E-mail: [email protected]

Present address: University of Wales, Bangor, School of Ocean Sciences, Marine Science Laboratories, Menai Bridge, Gwynedd LL59

5EY, UK.

0924-7963r98r$ - see front matter q 1998 Elsevier Science B.V. All rights reserved. .P I I : S 0 9 2 4 - 7 9 6 3 9 8 0 0 0 2 8 - 1


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( )I. Bentaleb et al.rJournal of Marine Systems 17 1998 39 58 41

have been attributed to variations in bcarboxylation .capacity Falkowski, 1991 .

In contrast, mixotrophic andror heterotrophic or-

ganisms fix inorganic carbon but also use metabo-

lites synthesized by other pathways in the cell orfrom external medium as energy sources Descolas-

.Gros and Oriol, 1992 . In that case, the bcarboxylase

activities are high as compared to the Rubisco. The

wide range in the observed bCrR ratios confirms

that in phytoplankton, there may exist a continuumbetween autotrophy and heterotrophy Lewitus and

.Caron, 1991a,b; Descolas-Gros and Oriol, 1992 .

When heterotrophy predominates, it is probable that13 w .xany relationship between d C and CO aq isPOC . 2

possible since the carbon source is derived partly

from organic substances. .Although CO aq is 200 times less abundant than2

bicarbonate, it is the species of inorganic carbon .utilized by Rubisco Cooper et al., 1969 . The low

.CO aq concentration of seawater may be biologi-2cally limiting, so triggering acclimative mechanisms

.in phytoplankton such as concentrating CO aq2mechanisms, active transport of the HCOy and the3

.reconversion in CO aq by the carbonic anhydrase2

Fig. 1. Map of transects of Minerve 17 cruise in the Southern Ocean, Indian Ocean sector.


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( )I. Bentaleb et al.rJournal of Marine Systems 17 1998 39 5842

Table 1

Location of the samples analyzed during Minerve 17 cruise in the Southern Indian Ocean

13w .x w x w xNumber Longitude Latitude pCO T S CO aq d C POC Chl2 2 PO C.y1 y1 . . . . . . . . .of sample 8E 8S ppm 8C mM mg l mg l

1 115.40 y20.13 361 27.4 35.2 9.6 y22.86 75

2 113.55 y21.24 357 27.2 35.3 9.7 y23.91 57 0.09

3 112.50 y21.85 344 26.3 35.4 9.4 y24.08 48 0.07

4 111.66 y22.42 343 25.5 35.6 9.5 y23.25 43 0.085 110.86 y22.91 342 25.2 35.0 9.6 y23.89 30 0.07

6 109.81 y23.51 337 25.2 35.2 9.5 y22.72 48 0.06

7 108.95 y23.99 332 24.5 35.4 9.5 y23.46 54 0.07

8 108.11 y24.51 332 23.8 35.5 9.6 y23.41 36 0.09

9 107.21 y25.06 333 23.8 35.5 9.7 y23.27 41 0.09

10 106.39 y25.56 323 22.4 35.5 9.8 y23.01 44 0.10

11 105.57 y26.02 325 22.6 35.5 9.7 y23.73 53 0.10

12 104.62 y26.59 323 22.3 35.5 9.8 y23.79 50 0.09

13 103.89 y27.02 320 21.9 35.6 9.7 y23.52 40 0.07

14 103.00 y27.30 23.2 35.7 y23.78 44 0.07

15 102.00 y28.00 21.8 35.8 y23.77 42 0.05

16 101.38 y28.49 328 21.3 35.8 10.2 y23.47 34 0.05

17 100.10 y29.19 328 21.3 35.8 10.2 y23.15 26 0.06

18 99.16 y29.74 333 20.7 35.8 10.4 y23.50 34 0.0619 98.23 y30.26 327 20.7 35.9 10.3 y22.91 34 0.06

20 97.33 y30.81 335 19.4 35.9 10.9 y23.68 26 0.07

21 96.41 y31.31 331 19.5 35.8 10.8 y23.21 27 0.08

.T: sea surface temperature 8C . .S: sea surface salinity .

w .x y1 .CO aq : molecular CO concentration mmol l .2 213 .d C : isotopic composition of particulate organic carbon .POC .

y1 .POC: particulate organic carbon content mg l . y1 .Chl: Chlorophyll concentration mg l .

y1 y1.Enzymatic activity of RUBP, PEPC, PEPCK and PYR nmol CO l h l .213 .d C : measured isotopic composition of dissolved inorganic carbon .DIC .13 .d C : interpolated values of isotopic composition of dissolved inorganic carbon .

DIC . calc. . . : Fractionation factor measured .p . . : Fractionation factor interpolated values .p

Raven, 1970; Graham and Smillie, 1976; Badger

and Andrews, 1982; Badger et al., 1985; Kerby and

Raven, 1985; Paneth and OLeary, 1985; Patel and

Merrett, 1986; Moroney et al., 1987; Dixon and

Merrett, 1988; Badger and Price, 1989; Munoz and

Merrett, 1989; Thielman et al., 1990; Kaplan et al.,.1991 . These mechanisms may have also an effect on

isotopic composition of phytoplankton. Although the

conversion by carbonic anhydrase is in isotopic equi- .librium OLeary et al., 1992 , it needs more detailed

studies to estimate the influence of active transport

on the carbon isotopic fractionation. .The occurrence of CO aq limitation has been2

observed in very high phytoplanktonic biomass or

during high phytoplankton growth rates Deuser,

1970; Fry and Wainright, 1991; Bentaleb, 1994;.Laws et al., 1995 . In such conditions, phytoplank-

ton, due to the high productivity, do not fractionate

according to the theoretical scheme predicting that

the isotopic fractionation increases with increasing .Rubisco activities or increasing CO aq concentra-

2tions. This can be the result of disequilibria of the

aqueous carbonate system. As the rate of the photo-

synthetic carbon fixation surpasses the rate of iso-

topic equilibria in the process of generation of new

carbon dioxide, both fractionations between cell car-

bon and carbon dioxide and between carbon dioxide

and bicarbonate decrease. This raises the problem of


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13 13 13 . .RUBP PEPC PEPCK PYR d C d C d C , ,DIC . DIC . DIC . p p . . . , calculated calculatedq measured calculated

1.45 1.24 1.45 15.6 15.59

0.6 0.2 0.5 0.6 1.39 1.26 1.39 16.6 16.55

1.34 1.30 1.34 16.6 16.58

0.8 0 0.4 0.3 1.37 1.34 1.37 15.7 15.69 1.44 1.35 1.44 16.4 16.37

0.6 0 0.6 0 1.31 1.36 1.31 15.1 15.06

1.31 1.39 1.31 15.7 15.73

1.4 0.3 0.2 0.1 1.29 1.43 1.29 15.6 15.58

1.37 1.43 1.37 15.5 15.52

0.6 0 1.6 0 1.21 1.50 1.21 14.9 -14.94

1.31 1.49 1.31 15.8 15.78

0.7 0 0.8 1.2 1.51 1.51 16.01

1.53 1.53 15.71

0.7 0 1.1 0.3 1.18 1.46 1.18 15.8 15.77

1.53 1.53 15.96

1 0 0.7 0.4 1.56 1.56 15.62

1.48 1.56 1.48 15.2 15.23

1.59 1.59 15.62 1.59 1.59 15.03

1.3 0.8 1.6 0.8 1.64 1.65 1.64 15.7 15.70

1.65 1.65 15.25

.the CO aq limitation, since it appears that the high2carbon demand decreases the supply of free carbon

dioxide available for the photosynthesis.

Although a strong relationship between d13

CPOC .w .xand CO aq has been observed, the available data2

.may be biased: 1 statistic distribution would not be .typical of a more random global sampling, 2 most

of the pCO values were not measured simultane-213 .ously with d C and 3 standardized POMPOC .

sampling was not used.

The aim of this study is to provide new data

which will permit the estimation of the respective .influence of carbon pathways and of CO aq con-2

centrations on organic carbon isotopic variations.

Data will be discussed in the context of models

describing the relationship between d13

C andPOC . .CO aq concentrations.

2

2. Materials and methods

2.1. Study area

The Minerve 17 cruise Mesure a 1Interface`Eau-aiR des Variations des Echanges de CO ,2

.MarchApril 1992 on board RV Marion Dufresne

consisted of a cruise trackPort Hedland in Aus- . .tralia 208S, 1158E Kerguelen Island 498S, 708E

. .La Reunion Island 258S, 578E Fig. 1 . The mainhydrological features in the South Indian Ocean and

particularly around the Kerguelen Plateau have been .described previously e.g., Park et al., 1991 . Al-

though some small hydrological differences may be

observed between the eastern and western basins of

the South Indian Ocean, these changes being small,

we have only considered the latitudinal variations.

Sea surface water north of the Subtropical Front . STC is characterised by high temperatures 15

.258C and high salinities corresponding to the sub- .tropical gyre 3536 whereas lower values are

.measured T-158C, S-34.5 south of the STC . .Tables 15 . The oceanic area from the STC 428S

.to the Sub-Antarctic Front SAF at 508S includes

two subsystems of the Southern Ocean: the Polar .Front Zone PFZ and the Permanently Open Ocean

. .Zone POOZ Treguer and Jacques, 1991 .The choice of the South Indian Ocean basin

was motivated by large latitudinal variations of

the d13

C , temperature, species distributionPOC .


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Table 2


13w .x w x w xNumber Longitude Latitude pCO T S CO aq d C POC Chl2 2 POC .y1 y1 . . . . . . . . .of sample 8E 8S ppm 8C mM mg l mg l

22 95.46 y31.84 328 19.0 35.8 10.8 y22.02 43 0.11

23 94.36 y32.47 335 19.1 35.8 11.0 y22.83 36 0.08

24 93.49 y32.94 329 19.3 35.8 10.8 y23.52 38 0.14

25 92.00 y33.20 18.6 35.7 y22.66 34 0.1426 90.48 y34.57 337 19.2 35.7 11.2 y22.81 53 0.13

27 90.00 y35.00 17.4 35.6 y22.27 119 0.31

28 89.41 y35.15 315 17.7 35.4 10.9 y22.58 76 0.23

29 88.95 y35.45 322 18.1 35.5 11.0 y22.89 48 0.17

30 88.44 y35.74 309 16.7 35.5 10.7 y21.22 101 0.53

31 87.76 y36.08 315 16.7 35.4 11.2 y21.64 103 0.50

32 87.32 y36.30 307 16.6 35.4 11.0 y21.15 94 0.51

33 86.81 y36.57 307 16.7 35.4 10.9 y21.48 96 0.43

34 86.35 y36.81 310 16.7 35.3 11.1 y21.93 77 0.39

35 85.69 y37.20 309 17.0 35.1 11.0 y21.63 68 0.38

36 84.89 y37.56 309 16.4 35.9 11.1 y21.26 90 0.52

37 84.29 y37.87 312 16.6 35.8 11.1 y21.67 79 0.44

38 83.59 y38.20 311 15.7 35.7 11.4 y22.25 81 0.41

39 82.87 y38.55 308 15.3 35.6 11.4 22.59 121 0.6440 82.45 y38.77 308 14.9 35.5 11.6 y21.83 139 0.74

41 81.86 y39.08 310 13.9 35.3 12.0 y21.12 123 0.65

42 81.45 y39.26 309 14.2 35.0 11.9 y21.57 152 0.75

43 80.78 y39.62 309 15.4 35.0 11.5 y21.42 103 0.49




y1 y1.Enzymatic activity of RUBP, PEPC, PEPCK and PYR nmol CO l h l .213 .d C : measured isotopic composition of dissolved inorganic carbon .

DIC .13 .d C : interpolated values of isotopic composition of dissolved inorganic carbon .DIC . calc. . . : Fractionation factor measured .p . . : Fractionation factor interpolated values .p

Fontugne and Duplessy, 1981; Fontugne et al.,. w .x1991 , and the high gradients of the CO aq Pois-2

.son et al., 1993 . At the 103 stations, total chloro-

phyll and organic carbon contents, enzyme activities,

organic and inorganic carbon isotopic composition 13 13 .d C and d C and pCO were measuredPOC . DIC . 2simultaneously. The d

13C were only measuredDIC .

for 50 stations.

2.2. Sampling and technical procedures

Surface seawater was pumped from 5 m depth

and pre-filtered through a nitex screen in order to

eliminate cells larger than 200 mm. This pre-filtered

water was used for analyses, which included the

following determinations.

For the determination of organic carbon isotopic 13 .composition d C , the plankton was collectedPOC .

by filtering 510 l of water under vacuum through . precleaned GFrF 0.45mm glass fibre filters Ches-

.selet et al., 1981 . On board, the filters were decar-

bonated with 0.1 N HCl, dried at 608C and then

stored in the dark at 48C. In the laboratory, the filters

were rinsed with distilled water, dried at 608C.

The inorganic carbon isotopic compositions 13 .d C were determined on seawater poisonedDIC .by HgCl following conventional procedures. The2total dissolved inorganic carbon is extracted from the

.sample by acidification 2 ml phosphoric acid .


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2.7 0.7 0.8 0.6 1.69 1.68 1.69 14.0 14.05

1.67 1.67 14.85

1.4 0.2 0.8 0.7 1.66 1.66 15.55

1.70 1.70 14.651.3 0 1.8 0.6 1.67 1.67 14.83

1.96 1.76 1.96 14.4 14.38

2.7 0.3 1 0.7 1.74 1.74 14.51

1.72 1.72 14.84

5.2 0 1.9 1 1.28 1.80 1.28 12.6 12.56

6.6 0 2.4 0.8 1.80 1.80 13.50

4 0.1 1.8 1.7 1.99 1.80 1.99 13.2 13.19

3.5 0.2 2.2 0.6 1.80 1.80 13.34

6.6 0.2 3.1 0.8 1.80 1.80 13.79

7.7 0.1 2.7 1.1 1.94 1.78 1.94 13.7 13.67

6.3 0.3 1.9 1 1.81 1.81 13.10

5.9 0 1.8 0.7 1.80 1.80 13.52

2.3 0 1.1 0 1.51 1.51 13.70

7.9 0.3 3.2 1.2 1.61 1.54 1.61 14.1 14.1012.6 1.2 4 1.7 1.59 1.59 13.27

8.8 0.2 3.3 1.3 1.71 1.71 12.56

13 1 4.5 2.6 1.68 1.68 13.01

5.3 0.3 1.8 0.5 1.53 1.53 12.87

The isotopic analyses of the CO gas obtained2were analyzed using a VG ISOGAS SIRA 9 mass

spectrometer. The analytical precision was better .than "0.05. Results are reported in per mil

.relative to the international Pee Dee Belemnite PDBstandard:

d13

C s 13

Cr12

C sampler13

Cr12

C standard .y1 =10 3 ..

.Assuming that CO aq is the inorganic carbon2source for the photosynthetic processes, it is possible

to calculate the overall isotopic fractionation factor . associated with the photosynthetic inorganicp

. .carbon fixation Freeman and Hayes, 1992 : pis the difference between the d

13C and theCO aq .2

organic carbon d13

C . The former is calculatedPOC . .using the equations of Mook et al. 1974 describing

.the isotopic fractionation between bicarbonatedrb .ions and CO aq as a function of temperature:2

s 24.12 y 9866rT whereT is in K.d r b

Few paired d13

C and d13

C simultaneousDIC . POC .measurements are available, and consequently the

w .xrelationship and CO aq is poorly defined.p 2However, taking into account d

13C distributionDIC .

vs. latitude or temperature in the Southern Ocean .published by Quay et al. 1992 or GEOSECS data,

it is possible to improve our database by producinginterpolated estimates of this parameter. Using our

d13

C measurements and those of Francois et al.DIC . .1993 , we have calculated three linear fits of

13 . d C vs. sea surface temperature SST 0 toDIC .. 13108C, 10 to 158C and above 158C , allowing d CDIC .

estimates as function of SST. Comparisons between

measured values and estimates at the same location .are in good agreement rs 0.72; n s 72 .

Carboxylase activity measurements were per-

formed according to Descolas-Gros and de Billy . .1983 , Descolas-Gros and Fontugne 1985 , Desco-

.las-Gros and de Billy 1987 and Descolas-Gros and .Oriol 1992 by measuring the incorporation of ra-

dioactive carbon dioxide into acid stable product.

The results are expressed as nmol CO fixed per2 y1 y1.hour per litre of water nmol CO h l . Ru-2

bisco, PEPC and PEPCK activities were measured

on the same crude extracts after filtration of 5 to 10 l


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Table 3


13w .x w x w xNumber Longitude Latitude pCO T S CO aq d C POC Chl2 2 PO C.y1 y1 . . . . . . . . .of sample 8E 8S ppm 8C mM mg l mg l

44 80.00 y40.00 308 16.0 35 11.20 y22.00 98 0.46

45 79.78 y40.29 309 13.9 35.0 12.0 y21.06 151 0.74

46 79.41 y40.69 309 13.7 35.0 12.1 y22.12 170 0.71

47 79.12 y40.97 311 13.8 35.0 12.1 21.52 134 0.4448 78.44 y41.67 306 14.1 34.9 11.8 y22.03 120 0.71

49 78.00 y42.07 310 14.2 34.8 12.0 y22.19 108 0.68

50 77.35 y42.70 313 12.8 34.7 12.6 y21.85 142 0.91

51 76.79 y43.37 310 12.7 34.6 12.5 y21.74 124 0.80

52 76.44 y43.75 314 12.0 34.5 13.0 y21.20 130 0.78

53 76.20 y43.99 309 11.5 34.5 13.0 y21.50 104 0.77

54 75.84 y44.36 305 11.4 34.5 12.9 y22.79 127 0.69

55 75.60 y44.59 311 11.2 34.5 13.2 y22.01 111 1.44

56 75.33 y44.88 309 11.6 34.5 13.0 y21.73 140 0.81

57 75.07 y45.10 306 11.3 34.4 13.0 y22.00 121 0.75

58 74.76 y45.40 305 12.0 34.2 12.7 y21.54 109 0.59

59 74.46 y45.70 311 12.0 34.0 12.9 y22.57 88 0.78

60 74.02 y46.16 306 12.2 34.0 12.6 y21.68 168 1.13

61 73.68 y46.50 323 10.3 34.0 14.2 y21.95 146 1.91




y1 y1.Enzymatic activity of RUBP, PEPC, PEPCK and PYR nmol CO l h l .213 .d C : measured isotopic composition of dissolved inorganic carbon .DIC .13 .d C : interpolated values of isotopic composition of dissolved inorganic carbon .DIC . calc.

. . : Fractionation factor measured .p . . : Fractionation factor interpolated values .p

of water through GFrF glass fibre filters. Such

activity measurements reflect the carboxylating en-

zyme pool of the phytoplankton cells when sampling

occurred. .1 The total biomass and the photosynthetic pa-

rameters were estimated, respectively, by measuring:

the particulate organic carbon content with a Strohlein y1COULOMAT 702C analyzer expressed asmgC l ,.analytical precision "1 mg and the chlorophyll

concentrations by spectrofluorometry Neveux and.Panouse, 1987 .

.2 Temperature and salinity were monitored along

the cruise-track using a thermosalinograph and par-

tial pressures of CO were measured with an auto-2 .mated infrared system Poisson et al., 1993 . These

abiotic parameters give the main features of the

environmental conditions for the cells growth and

w .xpermit to calculate CO aq by using the CO2 2 .solubility coefficients established by Weiss 1974 .

3. Results and discussion

3.1. Latitudinal ariability across the Indian Ocean

Results are reported in Tables 15. The d13

CPOC .

and d13

C values range from y26.5 to y20.2DIC .and from 1.02 to 2, respectively. The partial pres-

sure of carbon dioxide varies between 300 and 360 .matm. The dissolved CO aq concentrations exhibit2

an important gradient from 20 to 508S, from 9 to 19

mmol ly1 that is proportionally reverse to that of

temperatures which decrease from 28 to 58C for the


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Table 4


13w .x w x w xNumber Longitude Latitude pCO T S CO aq d C POC Chl2 2 POC .y1 y1 . . . . . . . . .of sample 8E 8S ppm 8C mM mg l mg l

62 73.31 y46.91 323 9.3 34.0 14.7 y23.00 0.73

63 73.16 y47.09 330 5.9 34.0 16.9 y24.42 87 0.26

64 72.93 y47.28 305 4.1 33.8 16.6 y23.71 116 0.93

65 72.70 y47.50 310 4.2 33.8 16.8 y23.76 150 0.9666 72.35 y47.82 305 3.9 33.9 16.7 y24.68 131 1.02

67 72.11 y48.03 306 3.8 33.8 16.9 y25.52 130 1.40

68 71.93 y48.20 314 4.1 33.7 17.1 y26.14 118 0.96

69 71.28 y48.75 318 4.1 33.7 17.4 y23.05 117 0.79

70 70.91 y49.05 353 4.6 33.7 18.9 y26.10 82 0.68

71 70.68 y49.29 349 4.9 33.7 18.5 y24.06 107 1.14

72 70.57 y49.36 361 5.0 33.7 19.1 y22.99 76 0.63

73 70.51 y48.89 353 4.7 33.8 18.8 y23.80 101 1.04

74 70.33 y48.58 334 4.9 33.8 17.7 y20.17 172 2.01

75 70.13 y48.26 335 5.2 33.7 17.5 y21.69 156 2.14

76 69.79 y47.72 348 5.3 33.7 18.2 y23.41 258 1.71

77 69.56 y47.40 348 5.5 33.7 18.0 y24.73 251 1.58

78 68.85 y46.27 358 6.9 33.7 17.6 y25.18 82 0.22

79 68.61 y45.88 362 7.3 34.0 17.6 y25.59 77 0.2180 68.40 y45.50 331 10.6 34.1 14.4 y23.44 151 0.48

81 68.20 y45.20 326 12.2 34.2 13.5 y23.40 135 0.50

82 67.82 y44.54 327 11.8 34.5 13.6 y23.00 136 0.55

83 67.34 y43.86 332 10.5 34.9 14.4 y23.54 122 0.44

84 66.69 y42.59 300 16.1 35.0 10.9 y24.93 75 0.37

85 66.29 y42.04 299 16.0 35.1 10.9 y23.28 71 0.40

86 65.70 y41.13 309 15.2 35.1 11.6 y22.55 99 0.55

87 65.26 y40.39 308 15.6 35.2 11.4 y22.78 106 0.41


w .x y1 .CO aq : molecular CO concentration mmol l .2 213 .d C : isotopic composition of particulate organic carbon .

POC . y1 .POC: particulate organic carbon content mg l . y1 .Chl: Chlorophyll concentration mg l .

y1 y1.Enzymatic activity of RUBP, PEPC, PEPCK and PYR nmol CO l h l .213 .d C : measured isotopic composition of dissolved inorganic carbon .DIC .13 .d C : interpolated values of isotopic composition of dissolved inorganic carbon .DIC . calc.

. . : Fractionation factor measured .p . . : Fractionation factor interpolated values .p

detrital carbon. The POCrChl ratio depends on light

intensity or depth, growth rate and temperature. Gei- .der 1987 reported that for laboratory phytoplankton

culture, the POCrChl ratio depends on species but is .always less than 70. Higher values )200 can be

observed for dinoflagellates Claustre and Caillau,.personal communication . The studies reported by

.Thompson et al. 1992 on the POCrChl ratio mea-

sured vs. temperature, for eight species of marine .phytoplankton marine diatoms and flagellates , show

that strictly autotrophic cells in controlled culture

conditions exhibit POCrChl ratio varying between

20 and 140. The general trend for POCrChl ratio isto decrease with increasing temperature Geider,

.1987; Thompson et al., 1992 . In marine biota, this .ratio varies over a larger range -100 to )600 ;

.lowest values -200 were generally observed atthe depth of the chlorophyll maximum Eppley et al.,

.1973; Pollehne et al., 1993 . More detailed studies of

this index are needed. From the literature data cited


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11.3 0.4 3.1 0 2.09 2.09 14.27

3.7 0.4 2.1 0.4 1.71 1.91 1.71 14.9 14.87

9.1 0.6 3.2 0.5 1.81 1.81 14.03

8.5 0.5 3.4 2.9 1.81 1.81 14.1015.7 0 6.5 2.5 1.80 1.80 14.97

26.4 0.6 2.6 0.7 1.79 1.79 15.79

1.81 1.81 16.47

4.5 0 2.3 0.1 1.81 1.81 13.38

30.3 0.4 1.4 0.4 1.71 1.84 1.71 16.4 16.38

25 0 0.6 0.9 1.85 1.85 14.53

19.3 0.2 4.6 0.4 1.76 1.86 1.76 13.4 13.39

32.6 0 5 0.6 1.84 1.84 14.24

70.4 0.4 6.6 2.3 1.78 1.85 1.78 10.6 10.57

37.3 0.1 2.3 0.2 1.87 1.87 12.22

77 0 2.9 0 1.88 1.88 13.96

36.2 0.5 2.6 0.4 1.89 1.89 15.32

2.5 0.2 1.7 0.3 1.96 1.96 16.02

2.8 0 1 0.1 1.89 1.98 1.89 16.4 16.40 2.08 2.08 14.85

5.5 1.5 1.9 1 1.90 1.90 14.82

1.94 1.94 14.42

6 0.2 1.3 0 2.03 2.10 2.03 14.9 14.88

1.83 1.83 16.75

3.8 0.2 1 0.1 1.24 1.83 1.24 14.5 14.50

9.6 0.7 2.2 0.8 1.18 1.56 1.18 13.6 13.61

8.1 0.3 0.7 0.4 1.28 1.51 1.28 14.0 14.0

above, we have assumed that a POCrChl cut-off of

200 demarks autotrophic from mixorheterotrophicpopulations: the values -200 are related to the

dominance of autotrophic cells while values )200

reflect the predominance of heterotrophic or

mixotrophic organisms or detrital carbon.

The heterotrophic features of populations, north

of STC, are supported by data of Thompson et al. .1992 because if the POCrChl ratio of the au-

totrophic organisms is roughly smaller than 200 and

always smaller in the warm waters, we should have

found low POCrChl ratios in the north of the STC if

autotrophic populations were dominant.

From physiological and biomass parameters, it

appears that mixorheterotrophic populations domi-

nate the particulate organic carbon at 5 m depth,

during the Minerve 17 cruise, north of STC. These

data do not necessarily imply a global heterotrophic

ocean in oligotrophic areas. The autotrophic organ-

isms in these low productive areas are often encoun-

.tered in deep euphotic layer Pollehne et al., 1993 ,

likely because of the proximity of the nitraclyne andbecause of the photoinhibition existing at the sea

surface.

South of the STC, POCrChl and bCrR ratios

show low values smaller than 200 and 50, respec-

tively. We also observe relatively good covariation .Fig. 3 between the POC content, chlorophyll con-

centrations and Rubisco activities, whereas no co-

variation is observed in the northern part of the STC,

because some of the organic carbon syntheses were

not photosynthetic in origin. The values of these

ratios and the parameters covariations corroborate

the autotrophic origin of the populations.

The isotopic fractionation giving values aroundp14 for the autotrophic organisms in the southern

part is significantly different from those that may be .calculated in the north Fig. 2c . However, the calcu-

lated remains low as compared to the 29pobtained from in vitro Rubisco of terrestrial plants


12/20


13/20


13 13 13 . .RUBP PEPC PEPCK PYR d C d C d C , ,DIC . DIC . DIC . p p . . . , calculated calculatedqmeasured calculated

7.7 0.3 3 1.3 1.43 1.82 1.43 13.8 13.76

10.6 0.5 1.3 0.7 1.50 1.82 1.50 14.3 14.33

5.9 0.4 1.9 0.4 1.54 1.77 1.54 14.2 14.17

1.17 1.65 1.17 15.5 15.450.8 0 1.9 0 1.50 1.65 1.50 16.4 16.37

1.56 1.65 1.56 16.0 16.05

0.7 0.4 0.8 0.5 1.59 1.61 1.59 15.8 15.84

1.50 1.62 1.50 15.3 15.34

0.8 0 1.1 0 1.58 1.57 1.58 18.5 18.53

1.03 1.56 1.03 17.0 17.01

0.9 0 2 0 1.42 1.52 1.42 16.4 16.42

1.29 1.47 1.29 16.5 16.48

1.37 1.47 1.37 17.7 17.68

1.29 1.47 1.29 15.5 15.49

1.28 1.38 1.28 15.8 15.81

1.32 1.32 1.32

disequilibrium in the isotopic carbonate system or a .limitation in the CO aq availability.2

South of STC, the correlations between POC,

chlorophyll concentrations and Rubisco activities .Fig. 3 corroborate that the CalvinBenson cycle is

responsible for fixation of the inorganic carbon. This

leads to a decrease of the d13

C values whenPOC .w .xRubisco activities and CO aq increase.2

Autotrophic populations south of the STC SST-

.158C, salinity-34.5 exhibit a rather good corre- .lation n s 39; rs 0.82, Fig. 6a .

d13

C s y0.427 "0.05 . .POC .

= CO aq y 16.81. 1 . .2

.Since the data distribution of relationship 1 is

not sufficiently representative, especially for thew .x y1CO aq around 16 mmol l and higher than 192mmol ly1, we include published measurements of

13 w .x .d C and CO aq Franc

ois et al., 1993 , andPOC . 2new measurements from the Southern Ocean that

.will be published by Dehairs et al. 1997 with

POCrChl ratios below 200. As systematic physio-

logic or biomass parameters were not measured dur-

ing these experiments, we have selected only the

values obtained south of the STC with SST below

158C, considering that these data represent mainly

autotrophic cells as indicated by our data and those .of Fontugne et al. 1991 . Taking into account the

results obtained during eutrophic situations Be-.ntaleb, 1994 , we remove from this selection samples

representative of high biomass content Chl)1 mgy1 .l andror samples with significant PEPC activity.

This selection improves the statistical validity of

the relationship noticeably for lower temperatures.13 w .xThe correlation between d C and CO aqPOC . 2

.becomes strongest and highly significant Fig. 6b .

13d C s y0.588 "0.023 = CO aq . .POC . 2

y14.375 "0.431 n s 117;rs 0.925 . 2 . . .

. .The slopes of relationships 1 and 2 are not signif- .icantly different. Relationship 2 predicts the

w .x y1CO aq with a precision of 1.51 mmol l , and2indicates that only 85.5% of the d

13C variability

POC .w .xcan be explained by CO aq variations. This result2can be considered satisfactory for biological material

and its accuracy is comparable to those obtained for

calibration of most of other proxies used in palaeo-

ceanographical reconstructions.

In these conditions, for the restricted temperature

range of the high latitudes, the organic carbon iso-


14/20



15/20


Fig. 3. The d13

C variation vs. latitude south of the Subtropical Convergence following the track. Covariation of Chl, CPOC . POC .concentrations and Rubisco activity in the same area.

topic composition presents a good correlation with .external CO aq concentrations, using both direct2

. . linear rs 0.925 and inverse calculation relationX .2 .

13d C s 167.9r CO aq q 34.8 .POC . 2

n s 117;rs 0.898 . 2X

. .

The linear relationship would indicate that, for these

regions characterized by low chlorophyll and high

nutrient concentrations, the biological demand of .CO aq is essentially constant and that growth rate2

variations do not influence significantly the carbon

isotopic composition of phytoplankton. However, for

highly productive regions near the island shelves, thelinear relationship cannot account for the measured

d13

C values and growth rate must be taken intoaccount Rau et al., 1992; Francois et al., 1993;

Hayes, 1993; Jasper and Hayes, 1994; Laws et al.,.1995 .

( ) [ ( )]3.3. Fractionation factor and CO aq rela-p 2tionships

Using our d13

C measurements, those of DIC . .Francois et al. 1993 and interpolated values, we

have calculated the values. Results of these cal-pw .xculations are reported vs. 1r CO aq in Fig. 7.2

North of the STC, no correlations were found be-

tween these parameters, corroborating that we haveobserved with linear relationship between d

13CPOC .

.Fig. 2. Variation of biomass, physiological parameters and isotopic fractionation between dissolved CO aq and SPOM through the2 . . . .latitudinal gradient in the SW Indian Ocean a C rChl, b bCrR ratio and c isotopic fractionation . We have considered thePOC . p

latitudinal variation without taking into account the longitude.


16/20


13 w .xFig. 4. Correlations between d C and CO aq in the southPOC . 2 . .Indian Ocean: a Minerve 17 data only; b data from the

literature, including Minerve 17 data.

w .x and CO aq . South of the STC SST-158C and2.sea surface salinity-34.5 , we discard high

biomass data as discussed above. As observed for13 w .xd C and CO aq , the correlation between POC . 2 p

w .x w .x .and CO aq or 1r CO aq is strong Fig. 7 and2 2 . X.would permit the use of relationships 3 or 3 for

pCO reconstructions in sea surface water.2

"0.9 s 8.58 "0.56 q 0.38 "0.03 . . .p

) CO aq rs 0.804;n s 76 , . .23 .

"0.9 s 21.03 "0.53 y 97.802 "8.35 . . .p

r CO aq rs 0.804;n s 76 . . .2X

3 .

X. w .xThe relationship 3 predicts the CO aq with a2precision of 1.91 mmol ly1.

However, our study limits geographically the use

of such a relationship between d13

C or andPOC . pw .xCO aq to the south of the STC. Palaeo-pCO2 2

13 w .xFig. 5. Correlations between d C and CO aq north of thePOC . 2 . .STC in the Indian Ocean: a Minerve 17 data only; b data from

the literature, including Minerve 17 data.


17/20


13 w .xFig. 6. d C CO aq calibration in the Southern IndianPOC . 2Ocean for autotrophic plankton dominating the total organic car-

. 13 . .bon: a Minerve datad C sy0.427 "0.048 =POC .w .x . . .CO aq y16.81 1 rs 0.82; ns39 ; b adding literature2

13 . .datad C s y14.375 "0.431 y 0.586 "0.023 =PO C .w .x . . .CO aq 2 rs 0.925; ns117 . The Snedecor test F-test2shows that the standard deviation of the slopes of these relation-

ships are not significantly different F s1.39-F s1.83;2r1 0.005.n s117; n s 39 . The subsequent use of the t-test shows that1 2

. . slopes 1 and 2 are not significantly different 152 degrees of.freedom at P s99.95% probability since the calculated value

w xtsy2.63 falls within the confidence range t y3.29,q3.29 .0.975

reconstructions for this regions, obtained from this .relationship Bentaleb et al., 1995 give upper

Holocene palaeo-pCO values consistent with pre-in-2 .dustrial equilibrium 270 matm values.

4. Summary and conclusion

Although the bCrR and POCrChl ratios are

quantitative parameters, they provide a means of

distinguishing qualitatively between autotrophic and

mixotrophic plankton. Our results suggest that

mixotrophic andror heterotrophic processes are gen-

erally dominant at the sea surface oligotrophic re-

gions. In these conditions, the d13

C values of sea

surface particulate organic carbon do not reflect thew .xCO aq because plankton organic carbon is partly2derived from assimilation of dissolved organic com-

pounds. The lack of correlation between d13

C orPOC .w .x and CO aq may be reinforced by speciesp 2diversity El Sayed and Jitts, 1973; Jacques et al.,

.1979; Sournia et al., 1979 , resulting in similar di-

versity in carbon assimilation pathways and conse-

quently to different levels of carbon isotope fraction-

ation. The relationship between d13 C andPOC .w .xCO aq is only reliable when typically autotrophic2C3 phytoplankton with Rubisco as fixing enzyme

dominate the POC as seen here with the diatom flora

in the Southern Ocean.

For phytoplankton carbon metabolism in the

Southern Indian Ocean, the STC constitutes a bound-

ary as already shown for hydrological and biochemi-

cal parameters, and phytoplankton species distribu-

tion. South of STC, low productivity and no limiting

conditions concerning nutrients and dissolved molec-

w .xular CO aq are encountered. Such conditions al-2low the development of autotrophic diatom flora

which represent the majority of the phytoplankton

biomass and consequently, this yields a good correla-13 w .xtion between d C , or and CO aq .POC . p 2

We proposed here another approach to understand

the isotopic fractionation mechanisms and to deter- .mine in which cases the CO aq content, among2

others parameters, is the main factor controlling the

d13

C of marine organic carbon. This work concludes

with a calibration between the d13

C or andPOC . pw .xthe CO aq restricted, at its present state, to the

2Southern Ocean south of the STC. As remarked by

.many authors see Goericke and Fry, 1994 , it will13 w .xbe difficult to establish a d C CO aq cali-POC . 2

bration from modern plankton, since the hetero-

trophic processes or particular carbon metabolisms

may hinder this relationship, especially in warm and

temperate areas. This suggests that calibration of


18/20


w .xFig. 7. Correlations between the fractionation factor, , and 1r CO aq on both sides of subtropical convergence.p 2

d13

C of specific biomarker of strictly autotrophic .phytoplankton C3 pathway must be the a priority to

reconstruct the palaeo-pCO of the sea surface and2

thus, the sources and sinks of CO for the atmo-2sphere in the past.

Acknowledgements

We thank J.C. Duplessy for comments and en-

lightening discussion, A. Johnston, G. Haddad and

M. Elliot, and anonymous reviewers, for their sug-

gestions. We thank F. Dehairs, D. Bakker, U. Bath-

mann and colleagues for allowing us to use their

pCO rd13

Crchlorophyll data before publication. We2

thank E. Kestenare, C. Blanc and P. Cuet for sam-

pling. The sampling in Indian Ocean was made

possible by Territoire des Terres Australes et Antarc-tiques Francaises Minerve 17 cruise of RrV Marion

.Dufresne with the important contribution of Y. Ba-

lut, all the crew members and Commandant Loudes.

This work was supported by the DBT program,

Centre National de la Recherche Scientifique CNRS,.France and the Commissariat a lEnergie Atomique`

.CEA, France . Centre des Faibles Radioactivites

.CFR Contribution 1778.

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