www.elsevier.com/locate/marpolbul
Marine Pollution Bulletin 48 (2004) 91–96
Foraminifers as indicators of marine pollution: a cultureexperiment with Rosalina leei
R. Saraswat *, Sujata R. Kurtarkar, A. Mazumder, R. Nigam
National Institute of Oceanography, Dona Paula, 403 004 Goa, India
Abstract
In order to develop a viable foraminiferal proxy for heavy metal pollutants, juvenile specimens of Rosalina leei were subjected to
different mercury concentrations (0–180 ng/l). Initially considerable growth was observed in specimens kept in saline water having a
mercury concentration up to 100 ng/l. But with the gradual increase in concentration of mercury the growth rate started decreasing.
Total growth achieved was significantly lower in case of specimens kept at relatively higher mercury concentrations then those
maintained in normal saline water. The most significant result of this experiment was the addition of abnormal chambers in the
specimens kept at higher mercury concentration. Later the specimens kept at highest concentration (180 ng/l) were subjected to
progressively increasing concentration of mercury to see the further effects and it was found that the specimens were still living at as
high a mercury concentration as 260 ng/l although there was no growth.
� 2003 Elsevier Ltd. All rights reserved.
Keywords: Mercury pollution; Foraminifers; Culture experiment; Abnormalities; Rosalina leei
1. Introduction
To effectively monitor the introduction as well as
increase or decrease in the concentration of pollutants it
is essential to delineate certain parameters, the change in
which can be used as a viable tool for such purposes.Most of the unicellular marine microorganisms are very
sensitive to environmental changes. That is why they are
the most common group of marine organisms used for
pollution studies. Many marine pollution studies make
use of bacteria (Rasmussen and Sorenson, 1998) as they
are almost ubiquitous and also can easily be cultured in
the lab. However because of negligible fossilization po-
tential, bacteria are of little help to decipher pollutionthrough time.
For such studies foraminifers (unicellular almost ex-
clusively marine protists), are more useful than other
marine microorganisms as a hard and thick calcium
carbonate covering known as the test that protects their
single cell, incorporates all the physico-chemical char-
acteristics of the ambient environment during the life of
*Corresponding author. Tel.: +91-832-2456700x4358; fax: +91-832-
2456702/703.
E-mail addresses: [email protected], rajeev_saraswat@rediff-
mail.com (R. Saraswat).
0025-326X/$ - see front matter � 2003 Elsevier Ltd. All rights reserved.
doi:10.1016/S0025-326X(03)00330-8
the foraminifers and gets preserved after the death of the
organism. Scott et al. (2001) have also pointed out the
importance of foraminifers in monitoring coastal envi-
ronments. The use of foraminifers to monitor marine
pollution started with the studies conducted by Zalesny
(1959), Resig (1960) and Watkins (1961). After thesestudies foraminifers have extensively been used to
monitor marine pollution particularly in coastal areas
(V�enec-Peyr�e, 1981; Ellison et al., 1986; Nagy and Alve,
1987; Caralp, 1989; Alve, 1991; Sharifi et al., 1991;
Yanko et al., 1994, 1998; Samir, 2000; Debenay et al.,
2001; Samir and El-Din, 2001; Geslin et al., 2002). In
India also, the foraminiferal proxies have, a number of
times been applied to monitor marine pollution (Setty,1976, 1982; Rao and Rao, 1979; Setty and Nigam, 1984;
Naidu et al., 1985; Bhalla and Nigam, 1986; Rao, 1996;
Jayaraju and Reddy, 1996; Nigam et al., 2002).
Most of above studies relied on the reported occur-
rence of increased percentage of certain species and
deformed foraminiferal tests in polluted areas. But there
has been a difference of opinion whether the deforma-
tion of tests is due to pollution or because of some otherreasons, as deformed tests have also been reported from
areas subjected to environmental stress like low salinity,
less food supply etc. (Heron-Allen and Earland, 1910;
Murray, 1963; Hofker, 1971; Brasier, 1975; Scott and
92 R. Saraswat et al. / Marine Pollution Bulletin 48 (2004) 91–96
Medioli, 1980; Boltovskoy et al., 1991; Cadre et al.,
2003). The reported occurrence of abnormalities in tests
from almost all types of environments irrespective of
their location and physico-chemical characteristics(Seiglie, 1964; Closs and Maderia, 1968; Yanko et al.,
1998; Geslin et al., 1998, 2002) further aggravates the
problem. The most effective method to solve this prob-
lem could be laboratory culture experiments through
which foraminiferal response to various types and con-
centrations of pollutants can be observed. In the present
experiment an attempt has been made in this direction
where the inner shelf benthic foraminiferal species Ro-
salina leei has been subjected to various concentrations
of mercury, one of the most harmful heavy metal pol-
lutant almost invariably present in the world oceans,
contributed to oceanic waters by both natural as well as
anthropogenic sources.
2. Mercury pollution: an insight
Out of various heavy metal pollutants present in sea,
mercury received a great deal of attention after the death
of 46 people, residing around Minamata Bay in Japan in
the year 1956, which were attributed to consumption of
fishes having alarmingly high concentration of mercury
in their muscle tissues (Nakahara et al., 1977). Both
natural as well as anthropogenic sources contribute mer-cury to the environment. The natural sources of mercury
in the environment include different ores of mercury, e.g.
cinnabar (red HgS), metacinnabar (black HgS), liv-
ingstonite (HgSb4S7), mercury containing sulphide
minerals such as tetrahydrite (6Cu2S Æ Sb2S3) etc. Nat-
ural sources are estimated to release about 2.5 · 104 to
5.0 · 105 tons year�1 of mercury, by degassing of the
earth�s atmosphere (Weiss et al., 1971). Anthropogeni-cally mercury is contributed to the environment as a
byproduct of chloralkali, agriculture, paint, pharma-
ceutical and paper and pulp industries as well as in the
form of disinfectants, fungicides etc. The mercury con-
tribution by human beings to the environment is sup-
posed to be about 2 · 104 to 7 · 104 tons year�1
(Summers and Silver, 1978).
In the oceans mercury occur both in inorganic {Hg(OH)2 and HgCl2} as well as organic form. The con-
centration of dissolved mercury in open oceans vary
from 0.2 to 1 ng/l, occasionally reaching up to 2 ng/l
(Mason and Fitzerald, 1996), while in case of conti-
nental margins it varies from 50 to 1000 ng/kg of sus-
pended matter. The common organic form of mercury is
methylmercury, which is also the most toxic form as it
becomes bioaccumulated and biomagnified up the foodchain, resulting in manifold concentration of mercury in
higher marine organisms such as fish, as compared to its
concentration in oceanic water. Despite worldwide
concern, mercury pollution has not received enough
attention in India. Therefore information about the
distribution of mercury in Indian waters is almost neg-
ligible (Singbal et al., 1978). But, in recent years efforts
have been taken to quantify the distribution of mercuryin parts of the Indian Ocean bordering India (Krish-
nakumar and Bhat, 1998; Kaladharan et al., 1999).
Based on the reported minimum (26 ng/l) and maximum
(187 ng/l) concentration of mercury in the region off
Goa, in the Arabian Sea along the west coast of India
(Singbal et al., 1978), and keeping in view the gravity of
mercury pollution situation, as evident from a recent
article in ‘‘The Times of India’’ (Mago, 2003), it wasdecided to find out the effects of mercury pollution on
benthic foraminifers.
3. Materials and method
Material for obtaining live specimens of benthic fo-
raminiferal species R. leei for the present study wascollected from the waters off Goa. This included both
sediment samples and marine algae comprising Sargas-
sum sp., Spatoglossum asperum and Stoechospermum
marginatum. The floating as well as attached (to rocks
submerged in seawater) algal material was collected
along with seawater and then soon after bringing on
shore, it was transferred to a plastic tub having filtered
seawater, and shaken vigorously to detach foraminifersfrom the algal substrate. After vigorous shaking the
whole of the material was transferred on to the sieves of
size 1000 lm and then over to 63 lm, kept over a funnel.
These sieve sizes were chosen as most of the juvenile as
well as mature benthic foraminifers are believed to have
their size within this limit. The choice of this sieve size
helped in concentrating the foraminifers and getting rid
of extraneous material. The plus 63 lm material wascollected in beakers along with some seawater and
brought to the laboratory. If enough seaweed sample
was not available, sediment sample in the form of upper
one cm of sediments, from near the rocks was scrapped
off and stored in beakers along with seawater and
brought to the laboratory as a source of live specimens.
Live specimens of R. leei were picked with the help of
a mouth pipette, from the material brought from thefield and kept in �Nunclan� multiwell dishes, untill they
reproduced. Juvenile specimens of R. leei produced as a
result of reproduction were subjected to different con-
centrations of mercury, prepared by dissolving water-
soluble mercuric chloride in normal saline water. The
observations of pseudopodial response, shape and ori-
entation of newly added chambers as well as measure-
ments regarding the maximum diameter, number ofchambers, was taken under a Leica inverted microscope
(Model Leitz Fluovert FU) and Carl Zeiss Stemi 2000 C
stereomicroscope. Food was provided in the form of
diatom the Isochryses. All the specimens were kept
y = -0.0003x + 0.0543Correlation= -0.82276
0.00
0.04
0.08
0.12
0.16
0 30 60 90 120 150 180
Mercury Concentration (ng/l)
Max
imu
m G
row
th (
mm
)
Fig. 2. The graph shows maximum growth attained at different Hg
concentrations for R. leei. Growth shows negative correlation
(–0.82276) with Hg concentration.
R. Saraswat et al. / Marine Pollution Bulletin 48 (2004) 91–96 93
under a 12 h light/12 h dark cycle. In order to study the
effect of mercury on foraminifers, ten sets of different
culture medium were prepared with varying mercury
concentrations. First set was maintained, in normalseawater without the addition of any mercury, as contol.
The mercury concentration in remaining nine sets was
increased gradually in steps of 20 ng/l, every alternate
day, by maintaining one set at each concentration. To-
wards the end of the experiment when growth at almost
all concentrations stabilized, the specimens kept at 180
ng/l mercury concentration were subjected to further
higher mercuric concentration in order to find out themaximum tolerance limit. The level of significance of
correlation between growth and mercury concentration
has been determined from Table 7 of Fisher and Yates
(1964).
4. Results
From the onset of experiment untill 12–15 days, ex-
tensive psuedopodial activity was noticed in all the
specimens. During this period considerable growth was
also reported in most of them. With the gradual increase
of mercury concentration, the pseudopodial extensions,
from the specimens, kept at progressively higher mer-
cury concentration, started decreasing. The same was
reflected in the growth rate also, as in case of specimensat higher than 80 ng/l mercury concentrations growth
almost ceased after about 24–26 days (Fig. 1). The
concentration of mercury affected not only the growth
rate but also the maximum size attained (Fig. 2).
Pseudopodial activity almost ceased just 4–5 days after
subjecting the specimens to 100 ng/l mercury concen-
tration, though the specimens were alive and accumu-
lating food near their last chamber very slowly. Themost important result of this experiment was the addi-
0 20 40 60 80 1000.00
0.04
0.08
0.12
0.16
Gro
wth
(m
m)
Number of Days
0 ng/l20 ng/l40 ng/l60 ng/l80 ng/l
100 ng/l120 ng/l140 ng/l160 ng/l180 ng/l
Legend
Fig. 1. Relationship between growth of R. leei and mercury concen-
tration. The growth is adversely affected by increasing Hg concentra-
tion.
tion of abnormal chambers in the specimens kept at
higher mercury concentration (Fig. 3). The abnormali-
ties included larger than normal chamber as well as
unusual orientation of the added chambers.
The maximum growth attained showed negative
correlation ðr ¼ �0:82276Þ with the mercury concen-tration (Fig. 2), as the specimens kept at progressively
higher Hg concentration showed lower maximum
growth. The correlation value was remarkably high at
99% level of significance ðr ¼ 0:7646Þ. The maximum
size achieved by juvenile specimens under different
mercury concentrations was lower than the normal size
of the specimens collected from the field. Though the
growth almost ceased after about 40 days at all con-centrations the specimens were surviving at as high
mercury concentration as 260 ng/l.
5. Discussion
Despite a number of studies documenting foramini-
feral characteristics from environments affected by var-ious types of pollutants (Alve, 1995), the potential utility
of foraminifers to monitor marine environments is
hampered by the fact that similar foraminiferal charac-
teristics have almost invariably been reported from the
areas subjected to natural ecologically stressed envi-
ronments (Boltovskoy et al., 1991). There has been, the
need to characterize and differentiate foraminiferal
characteristics of anthropogenically polluted environ-ments from that of ecologically stressed environments
with the help of further field studies and especially
through culture studies (Yanko et al., 1998; Samir, 2000;
Geslin et al., 2002; Scott et al., 2001). The present study
wherein an attempt has been made to find out the spe-
cific response of R. leei, a nearshore benthic foramini-
feral species, to mercury, one of the most toxic heavy
metal pollutants, addresses the present concern.The comparatively lower growth rate of juvenile
specimens subjected to varying concentrations of mer-
cury, than the ones maintained at normal seawater
Fig. 3. Abnormalities in the newly added chambers (A, B) in the specimens subjected to Hg pollution as against a normal specimen (C) kept at
normal seawater. Fig. A shows larger than normal chamber, while figure B shows unusual orientation of the newly added chambers as well as a
comparatively larger last chamber.
94 R. Saraswat et al. / Marine Pollution Bulletin 48 (2004) 91–96
condition in the present experiment, leads to the con-
clusion that the presence of heavy metal pollutant
mercury in the ambient environment, retards the growth
rate, confirming the possibilities expressed by Boltov-
skoy and Wright (1976), who noted that, ‘‘the presence,
absence, disequilibria or inter-relations of some of thetrace elements in individual organisms can retard or stop
normal growth, can provoke abnormal development
(monstrosities) and can even induce death’’. Significant
growth was observed only as long as the specimens were
under a mercury concentration of 60–80 ng/l (Fig. 1),
and for 35–40 days, after which the growth at all con-
centrations almost ceased, reflecting the inability of
specimens to cope with the persistent mercury concen-tration. At this stage the average size of the specimens
was comparatively smaller than the specimens collected
from the field, implying that under the influence of
mercury the average size of specimens decreased and
thus confirms numerous field based observations where
stunted foraminiferal tests has been reported from the
areas subjected to pollution (Yanko et al., 1994, 1998;
Samir and El-Din, 2001).Though the abnormalities in foraminiferal tests in
both field (Alve, 1991; Samir and El-Din, 2001), as well
as laboratory cultures (Stouff et al., 1999) is a common
phenomena, but the addition of abnormal chambers, in
a number of specimens, only at higher mercury con-
centrations in the present laboratory culture study
points toward the role of pollutants in the reported oc-
currence of abnormal tests from the areas subjected to
various types of pollution (Bhalla and Nigam, 1986;Alve, 1991; Debenay et al., 2001; Geslin et al., 2002).
The present result gives credence to the conclusions
drawn by Yanko et al. (1999), that there is a positive
correlation between abundance of deformed tests and
heavy metals. The reported occurrence of stunted spec-
imens despite the presence of ample food, provided
regularly in the form of Isochryses, argues against the
suggestions of Boltovskoy and Wright (1976) that thegrowth of individuals may be impaired because of lack
of phytoplankton, a nutrient source for foraminifera,
resulting from the adverse effect of trace elements on the
growth and thus productivity of phytoplankton.
As far as the pathway for the delitrious effects of
mercury on the foraminifers is concerned, the cytoplasm
seems to be the immediately affected part as evident
from the decreased pseudopodial activity in case ofspecimens subjected to comparatively higher mercury
concentrations. Similar views were expressed by Aschan
and Skullerud (1990), who opined that heavy metals
R. Saraswat et al. / Marine Pollution Bulletin 48 (2004) 91–96 95
have a definite adverse effect on the benthic fauna, es-
pecially the foraminifers. Yanko et al. (1998) also noted,
that ‘‘in extreme cases of heavy metal pollution, the
organism devotes its energy to protect itself. As a result,such an individual has little ability left for protein syn-
thesis. This inhibits its energy budget, reproduction
cycle, and also harms its cytoskeleton’’. Therefore the
adverse effect of mercury on the normal functioning of
cytoplasm of the foraminifers is probably responsible
for the abnormalities in the chambers added, in the
specimens of R. leei maintained at higher mercury con-
centrations, in the present culture experiment.Since in the present study, except for the variation in
mercury concentration, all other ecological parameters
were same for all the specimens, the occurrence of
stunted and deformed tests in specimens subjected to
various mercury concentrations can be attributed only
to mercury pollution.
6. Conclusion
The present study was conducted in order to decipher
the response of benthic foraminifer R. leei to one of the
most harmful heavy metal pollutant, that is mercury. On
the basis of this study it can be confirmed that the in-
troduction of pollutants in the ambient environment of
benthic foraminiferal community results in the mor-phological abnormalities as well as restricting the size of
the foraminifers and further that these characteristics of
foraminifers can be used to decipher the introduction,
increase or decrease of this pollutant in any area.
Acknowledgements
The authors are grateful to Dr. E. Desa, Director,
National Institute of Oceanography for providing the
infrastructure facilities and permission. We are indebted
to Dr. N.H. Hashimi, Scientist, National Institute of
Oceanography, for reviewing the manuscript and sug-
gesting improvements. The authors express their sincere
thanks towards Mr. Jay Sankar De, for fruitful discus-
sions regarding mercury pollution and providing nec-essary literature. R. Saraswat and A. Mazumder
thankfully acknowledge the Council of Scientific and
Industrial Research, New Delhi for the financial grant
availed in the form of Junior Research Fellowship and
Senior Research Fellowship, respectively.
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