506
Bijmaetal.
composition by 3.2 to 3.8 %0, respectively, when fed
GSL and SFB artemia.
Symbiont Effect
Our experimental results have separated the influence of symbiont photosynthesis from the influence
of the carbonate chemistry on the shell isotopic
composition calcification. The observed l3C-enrichment and 180-depletion in HL 0. universa
relative to specimens maintained in the dark are
clearly a function of symbiont photosynthesis
and have been reported before. With respect to
l3C-enrichment, a mechanism has been proposed
whereby RUBISCO preferentially removes 12C0 2
during photosynthesis and subsequently enriches
the calcifying environment with l3C (Spero 1992;
Spero and DeNiro 1987; Spero and Lea 1993;
Spero et al. 1991; Spero and Williams 1989).
Because it is generally assumed that
photosynthesis per se does not affect the 0 18 0
of the photosynthate nor that of the residual
~0-C02-HCO;pool (Swart 1983), 180-depletion
in symbiotic systems were tentatively explained
as the result of light-enhanced calcification
rates (Bouvier-Soumagnac et al. 1986; Spero 1992;
Spero and Lea 1993). However, as discussed before, our data suggest that calcification rate may
not explain the oxygen isotope fractionation observed in this study. In the rest of this section we
propose an alternative mechanism based on local
pH changes induced by carbon fixation of the
symbionts.
Since the symbiotic algae increase the pH of the
foraminiferal microenvironment to as much as 8.8
during photosynthesis(J0rgensen et al. 1985)
the local [COn will be elevated as well (Wolf~
Gladrow et aI.1999). The observed differences in
0 18 0 between HL and dark range from
0.35 %0 for 0. universa (Spero 1992) to 0.63 0/00
for G. sacculifer (Spero and Lea 1993). If we
assume that this difference is solely due to the
symbiont induced shift in the ambient carbonate
chemistry, and further that the 0180/[COn and a
ol3C/[COn slopes are -0.002 %0 and -0.0065 %0
respectively (Table 1), a simultaneous shift of
1.1 %0 and 2.0 %0 towards more negative Ol3C
values at HL can be calculated for 0. universa
and G. sacculifer, respectively. On the contrary,
we found a positive shift of 1.1 %0 for 0. universa
and others have shown that compared to specimens
grown in the dark, ODC of 0. universa and G.
sacculifer kept above saturation light levels, is
enriched by 1.7 %0 (Spero 1992) and 1.4 %0 (Spero
and Lea 1993), respectively. Consequently, if we
take the kinetic effect on 013C and 0 18 0 (induced
by local changes in the carbonate chemistry) into
account, we have to invoke an additional
mechanism to explain a concomitant enrichment in
ODC between 2.2 to 2.8 %0 for 0. universa and
even 3.4 %0 for G. sacculifer.
RUBISCO has always been the first choice to
explain shell enrichment in the light. However, this
mechanism requires that sufficient CO 2 is available
to enrich the residual CO 2 pool or, ifHCO~is the
carbon source, that not all CO 2 (once converted
from HCOJ if fixed by RUBISCO and that some
diffuses to the site of calcification. Numerical
experiments (Wolf-Gladrow et al. 1999) have demonstrated that the symbionts are CO 2 limited, even
at low photosynthetic rates, and therefore use
HC0 3 -as their main carbon source. These experiments have also demonstrated that a steep CO 2
gradient exists between the shell surface and the
symbiont halo, probably acting as an efficient barrier against CO 2 diffusion towards the shell. As the
HCO;pool is very large and hardly affected by photosynthetic carbon fixation, and theo l3 C ofHCO;
is very close to the ODC of LC0 2 , we argue that
RUBISCO is probably not responsible for the
HL:dark shift. This conclusion is supported byexperiments carried out at constant pH (Fig. 3e). As
CO 2 availability increases, shells get lighter instead
of heavier, suggesting that enzyme mediated DC_
enrichment of the ambient environment plays a
subordinate role, if at all.
As an alternative hypothesis to explain the observed positive shift between the HL and dark
experiments we propose scavenging of respired
12C0 2 by the symbionts. In the previous section we
have shown that respired CO 2 can lower shell O\3C
by 3.2 to 3.8 %0 (depending on the food source),
enough to explain the required enrichment in the
light of up to 3.4 %0. The decrease in shell ODC
with increasing [C0 2 aq] at constant pH can now
be explained by a decrease in the scavenging efficiency of respired CO 2 as bulk CO 2 increases. Thus
Bijmaetal.
composition by 3.2 to 3.8 %0, respectively, when fed
GSL and SFB artemia.
Symbiont Effect
Our experimental results have separated the influence of symbiont photosynthesis from the influence
of the carbonate chemistry on the shell isotopic
composition calcification. The observed l3C-enrichment and 180-depletion in HL 0. universa
relative to specimens maintained in the dark are
clearly a function of symbiont photosynthesis
and have been reported before. With respect to
l3C-enrichment, a mechanism has been proposed
whereby RUBISCO preferentially removes 12C0 2
during photosynthesis and subsequently enriches
the calcifying environment with l3C (Spero 1992;
Spero and DeNiro 1987; Spero and Lea 1993;
Spero et al. 1991; Spero and Williams 1989).
Because it is generally assumed that
photosynthesis per se does not affect the 0 18 0
of the photosynthate nor that of the residual
~0-C02-HCO;pool (Swart 1983), 180-depletion
in symbiotic systems were tentatively explained
as the result of light-enhanced calcification
rates (Bouvier-Soumagnac et al. 1986; Spero 1992;
Spero and Lea 1993). However, as discussed before, our data suggest that calcification rate may
not explain the oxygen isotope fractionation observed in this study. In the rest of this section we
propose an alternative mechanism based on local
pH changes induced by carbon fixation of the
symbionts.
Since the symbiotic algae increase the pH of the
foraminiferal microenvironment to as much as 8.8
during photosynthesis(J0rgensen et al. 1985)
the local [COn will be elevated as well (Wolf~
Gladrow et aI.1999). The observed differences in
0 18 0 between HL and dark range from
0.35 %0 for 0. universa (Spero 1992) to 0.63 0/00
for G. sacculifer (Spero and Lea 1993). If we
assume that this difference is solely due to the
symbiont induced shift in the ambient carbonate
chemistry, and further that the 0180/[COn and a
ol3C/[COn slopes are -0.002 %0 and -0.0065 %0
respectively (Table 1), a simultaneous shift of
1.1 %0 and 2.0 %0 towards more negative Ol3C
values at HL can be calculated for 0. universa
and G. sacculifer, respectively. On the contrary,
we found a positive shift of 1.1 %0 for 0. universa
and others have shown that compared to specimens
grown in the dark, ODC of 0. universa and G.
sacculifer kept above saturation light levels, is
enriched by 1.7 %0 (Spero 1992) and 1.4 %0 (Spero
and Lea 1993), respectively. Consequently, if we
take the kinetic effect on 013C and 0 18 0 (induced
by local changes in the carbonate chemistry) into
account, we have to invoke an additional
mechanism to explain a concomitant enrichment in
ODC between 2.2 to 2.8 %0 for 0. universa and
even 3.4 %0 for G. sacculifer.
RUBISCO has always been the first choice to
explain shell enrichment in the light. However, this
mechanism requires that sufficient CO 2 is available
to enrich the residual CO 2 pool or, ifHCO~is the
carbon source, that not all CO 2 (once converted
from HCOJ if fixed by RUBISCO and that some
diffuses to the site of calcification. Numerical
experiments (Wolf-Gladrow et al. 1999) have demonstrated that the symbionts are CO 2 limited, even
at low photosynthetic rates, and therefore use
HC0 3 -as their main carbon source. These experiments have also demonstrated that a steep CO 2
gradient exists between the shell surface and the
symbiont halo, probably acting as an efficient barrier against CO 2 diffusion towards the shell. As the
HCO;pool is very large and hardly affected by photosynthetic carbon fixation, and theo l3 C ofHCO;
is very close to the ODC of LC0 2 , we argue that
RUBISCO is probably not responsible for the
HL:dark shift. This conclusion is supported byexperiments carried out at constant pH (Fig. 3e). As
CO 2 availability increases, shells get lighter instead
of heavier, suggesting that enzyme mediated DC_
enrichment of the ambient environment plays a
subordinate role, if at all.
As an alternative hypothesis to explain the observed positive shift between the HL and dark
experiments we propose scavenging of respired
12C0 2 by the symbionts. In the previous section we
have shown that respired CO 2 can lower shell O\3C
by 3.2 to 3.8 %0 (depending on the food source),
enough to explain the required enrichment in the
light of up to 3.4 %0. The decrease in shell ODC
with increasing [C0 2 aq] at constant pH can now
be explained by a decrease in the scavenging efficiency of respired CO 2 as bulk CO 2 increases. Thus