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: rajeev@darya.nio.org, 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.

References

Alve, E., 1991. Benthic foraminifera reflecting heavy metal pollution in

Sorfjord, Western Norway. Journal of Foraminiferal Research 21,

1–19.

Alve, E., 1995. Benthic foraminiferal responses to estuarine pollution:

a review. Journal of Foraminiferal Research 25, 190–203.

Aschan, M.A., Skullerud, A.M., 1990. Effects of changes in sewage

pollution on soft-bottom macrofauna communities in the inner

Oslofjord, Norway. Sarsia 75, 169–190.

Bhalla, S.N., Nigam, R., 1986. Recent foraminifera from polluted

marine environment of Velsao Beach, South Goa, India. Revue de

Paleobiology 5, 43–46.

Boltovskoy, E., Wright, R., 1976. Recent Foraminifera. Dr.W. Junk

Publishers, The Hague. pp. 515.

Boltovskoy, E., Scott, D.B., Medioli, F.S., 1991. Morphological

variations of benthic foraminiferal tests in response to changes in

ecological parameters: a review. Journal of Paleontology 65, 175–

185.

Brasier, M.D., 1975. Morphology and habitate of living benthonic

foraminiferids from Caribbean carbonate environment. Revue

Espenola Micropaleontologia 7, 567–569.

Cadre, V.L., Debenay, J.-P., Lesourd, M., 2003. Low pH effects on

Ammonia baccarii test deformation: implications for using test

deformations as a pollution indicator. Journal of Foraminiferal

Research 33, 1–9.

Caralp, M.H., 1989. Abundance of Bulimina exilis and Melonis

barleeanum: relationship to the quality of marine organic matter.

Geo-Marine Letters 9, 37–43.

Closs, D., Maderia, M.L., 1968. Seasonal variations of brackish

foraminifera in the Patos lagoon, southern Brazil. Escola de

Geologia Porto Allegre Publicaciones especial. 15, 1–151.

Debenay, J.-P., Tsakiridis, E., Soulard, R., Grossel, H., 2001. Factor

determining the distribution of foraminiferal assemblages in port

Joinville Harbour (Ile d�Yeu, France): the influence of pollution.

Marine Micropaleontology 43, 75–118.

Ellison, R.L., Broome, R., Ogilvie, R., 1986. Foraminiferal response to

trace metal contamination in the Patapsco River and Baltimore

Harbour, Maryland. Marine Pollution Bulletin 17, 419–423.

Fisher, R.A., Yates, F., 1964. Statistical tables for biological,

agricultural and medical research. Oliver and Boyd, London.

pp. 148.

Geslin, E., Debenay, J.-P., Lesourd, M., 1998. Abnormal wall textures

and test deformation in Ammonia (Hyaline Foraminifer). Journal

of Foraminiferal Research 28 (2), 148–156.

Geslin, E., Debenay, J.-P., Duleba, W., Bonetti, C., 2002. Morpho-

logical abnormalities of foraminiferal tests in Brazilian environ-

ment: comparison between polluted and non-polluted areas.

Marine Micropaleontology 45, 151–168.

Heron-Allen, E., Earland, A., 1910. On the recent and fossil

foraminifera of the shore-sands of Sesely Bill, Sussex, Part VI. A

contribution towards the aetiology of Masselina secans (d�Orbigny

sp.). Journal of Royal Microscopic Society of London, 693–695.

Hofker, J., 1971. The foraminifera of Piscadera Bay, Curacao. Studies

on the fauna of Curacao and other Caribbean Islands 35, 1–57.

Jayaraju, N., Reddy, K.R., 1996. Impact of pollution on coastal zone

monitoring with benthic foraminifera of Tuticorin, southeast coast

of India. Indian Journal of Marine Science 25, 376–378.

Kaladharan, P., Pillai, V.K., Nandakumar, A., Krishnakumar, P.K.,

1999. Mercury in seawater along the west coast of India. Indian

Journal of Marine Sciences 28, 338–340.

Krishnakumar, P.K., Bhat, G.S., 1998. Heavy metal distribution in the

biotic and abiotic matrices along Karnataka coast, west coast of

India. Indian Journal of Marine Sciences 27, 201–205.

Mago, C., 2003. India may become hot spot for mercury poisoning.

The Times of India, Mumbai. February 14.

Mason, R.P., Fitzerald, W.F., 1996. Sources, sinks and biogeochem-

ical cycling of mercury in the ocean. In: Baeyens, W., Ebinghaus,

R., Vasiliv, O. (Eds.), Global and Regional Mercury Cycles:

Sources Fluxes and Mass Balances. NATO ASI Series 2. Environ-

ment, Vol. 21, Kluwer Academic Publishers, Dordrecht, The

Netherlands, pp. 249–272.

96 R. Saraswat et al. / Marine Pollution Bulletin 48 (2004) 91–96

Murray, J.W., 1963. Ecological experiments on foraminifera. Journal

of Marine Biological Association, UK 43, 621–642.

Nagy, J., Alve, E., 1987. Temporal changes in foraminiferal faunas and

impact of pollution in Sandebukta, Oslo Fjord. Marine Micropa-

leontology 2, 109–128.

Naidu, T.Y., Rao, D.C., Rao, M.S., 1985. Foraminifera as pollution

indicators in the Vishakhapatnam harbor complex, east coast of

India. Bulletin of Geological Mining and Metallurgical Society of

India 52, 88–96.

Nakahara, H., Ishikawa, T., Sarai, Y., Kondo, I., Mitsuhashi, S., 1977.

Frequency of heavy metal resistance in bacteria from inpatients in

Japan. Nature 266, 165–167.

Nigam, R., Nayak, G.N., Naik, S., 2002. Does mining pollution affect

foraminiferal distribution in Mandovi estuary, Goa, India? Revue

de Paleobiologie 21, 673–677.

Rao, K.K., 1996. Foraminiferal fauna from the Cochin backwaters:

biological indicators of man-made changes in the environment.

Journal of Aquatic Biology 1, 9–16.

Rao, K.K., Rao, T.S., 1979. Studies on pollution ecology of

foraminifera of the Trivandrum coast. Indian Journal of Marine

Science 8, 31–35.

Rasmussen, L.D., Sorenson, S.J., 1998. The effect of long-term

exposure to mercury on the bacterial community in marine

sediment. Current Microbiology 36, 291–297.

Resig, J.M., 1960. Foraminiferal ecology around ocean outfalls off

southern California. In: Pearson, P.A. (Ed.), Waste disposal in the

marine environment. Pergamon press, London, pp. 104–121.

Samir, A.M., 2000. The response of benthic foraminifera and

ostracods to various pollution sources: a study from two lagoons

in Egypt. Journal of Foraminiferal Research 30, 83–98.

Samir, A.M., El-Din, A.B., 2001. Benthic foraminiferal assemblages

and morphological abnormalities as pollution proxies in two

Egyptian bays. Marine Micropaleontology 41, 193–227.

Scott, D.B., Medioli, F.S., 1980. Living vs. total foraminiferal

populations: their relative usefulness in paleoecology. Journal of

Paleontology 54, 814–831.

Scott, D.B., Schafer, C.T., Medioli, F.S., 2001. Monitoring in coastal

environments using foraminifera and thecamoebian indicators.

Cambridge University Press. pp. 177.

Seiglie, G.A., 1964. Sigificacion de los foraminiferos anormales de la

lagua de Unare, Lagena 1 (6).

Setty, M.G.A.P., 1976. The relative sensitivity of benthonic forami-

nifera in the polluted marine environment of the Cola Bay, Goa.

In: Proceedings, VI Indian Colloquium on Micropaleontology and

Stratigraphy, Varanasi, pp. 225–234.

Setty, M.G.A.P., 1982. Pollution effects monitoring with foraminifera

as indices in the Thana Creek Bombay area. International Journal

of Environmental Studies 18, 205–209.

Setty, M.G.A.P., Nigam, R., 1984. Benthic foraminifera as pollution

indices in the marine environment of west coast of India. Revista

Italian de Paleontologia de Stratigrafi 89, 421–436.

Sharifi, A.R., Croudace, T.W., Austin, R.L., 1991. Benthonic

foraminiferids as pollution indicators in Southampton water,

Southern England, UK. Journal of Micropaleontology 10, 109–

113.

Singbal, S.Y.S., Sanzgiri, S., Sengupta, R., 1978. Total mercury

concentrations in the Arabian Sea waters off the Indian coast.

Indian Journal of Marine Science 7, 124–126.

Stouff, V., Geslin, E., Debenay, J.-P., Lesourd, M., 1999. Origin of

morphological abnormalities in Ammonia (foraminifera): studies in

laboratory and natural environments. Journal of Foraminiferal

Research 29, 152–170.

Summers, A.O., Silver, S., 1978. Microbial transformations of metals.

Annual Review of Microbiology 32, 637–672.

V�enec-Peyr�e, M.T., 1981. Les foraminif�eres et la pollution: �etude de la

microfaune de la Cale du Dourduff (embrouchure de la rivi�ere de

Morlaix). Cahiers de Biologie Marine 22, 25–33.

Watkins, J.G., 1961. Foraminiferal ecology around the Orange

Country, California, ocean sewer outfall. Micropaleontology 7,

199–206.

Weiss, H.V., Koide, M., Goldberg, D.E., 1971. Mercury in a

Greenland ice sheet: evidence of recent input by man. Science

174, 692–694.

Yanko, V., Ahmad, M., Kaminski, M., 1998. Morphological defor-

mities of benthic foraminiferal tests in response to pollution by

heavy metals: implication for pollution monitoring. Journal of

Foraminiferal Research 28, 177–200.

Yanko, V., Kronfeld, J., Flexer, A., 1994. Response of benthic

foraminifera to various pollution sources: implication for pollution

monitoring. Journal of Foraminiferal Research 24, 73–97.

Yanko, V., Arnold, A.J., Parker, W.C., 1999. Effects of marine

pollution on benthic foraminifera. In: Sen Gupta, B.K. (Ed.),

Modern Foraminifera. Kluwer Academic Publishers, Great Bri-

tain, pp. 217–235.

Zalesny, E.R., 1959. Foraminiferal ecology of Santa Monica Bay,

California. Micropaleontology 5, 101–126.