benthic foraminiferal assemblages and morphological abnormalities as pollution proxies in two...

Benthic foraminiferal assemblages and morphologicalabnormalities as pollution proxies in two Egyptian bays

A.M. Samira,*, A.B. El-Dinb

aGeology Department, Faculty of Science, Alexandria University, P.O. Box 21526, Alexandria, EgyptbOceanography Department, Faculty of Science, Alexandria University, Alexandria, Egypt

Received 3 March 2000; accepted 28 November 2000

Abstract

A detailed comparative study of Recent benthic foraminiferal populations was conducted at two bays (El-Mex and Miami)

located along the Mediterranean coast of Alexandria, Egypt. Nine samples from each bay were studied and a total of 78 benthic

foraminiferal species belonging to 19 families were identi®ed. Porcellaneous forms were dominant, comprising 65% and 68%

of the total population in El-Mex and Miami bays, respectively. El-Mex is one of the most metal-polluted areas along the

Alexandrian coast. It is contaminated by industrial wastes, chie¯y heavy metals, as well as agricultural and domestic ef̄ uents.

Increasing pollution results in low species diversity and population density, associated with an increase in tolerant or oppor-

tunistic species. The extent to which population was found to be impoverished corresponded to the degree to which the

sediment was contaminated. In this contaminated environment, foraminiferal tests were stunted and aberrant tests were

frequently found. Species diversity and population density were higher in Miami Bay (domestic sewage) and deformed

forms were scarce. X-ray microanalysis reveals that living deformed specimens contain higher levels of heavy metals (Pb,

Zn, Cu, Cr, and Cd) than non-deformed ones. This strongly suggests that heavy metals are responsible for the abnormalities in

foraminiferal tests. The study illustrates that the mode of test deformation depends upon the degree of pollution and type of

pollutants. Benthic foraminifera re¯ect human-induced environmental perturbation and they can be used as bioindicators for

monitoring coastal pollution. q 2001 Elsevier Science B.V. All rights reserved.

Keywords: Benthic; Deformities; Proxies; Type; Degree; Pollution; Egypt

1. Introduction

Foraminifera are very sensitive to environmental

stress and have been increasingly used for pollution

studies in the last 30±40 years. Studies of pollution

effects on benthic foraminiferal tests and their use as

proxy indicators were initiated by Zalesny (1959),

Resig (1960), and Watkins (1961).

Deformed tests appear to increase dramatically in

areas subjected to different types of pollutants, e.g. oil

slicks (VeÂnec-PeyreÂ, 1981); sewage discharge

(Watkins, 1961); agrochemicals (Bhalla and Nigam,

1986); high organic matter content (Caralp, 1989),

and heavy metal contamination (Shari® et al., 1991;

Alve, 1991; Yanko et al., 1994, 1998). Abnormal test

shapes have also been reported from areas subjected

to natural environmental stresses such as: (1) abnor-

mal salinity (Hofker, 1971; Brasier, 1975); (2)

reduced nutrition levels (Heron-Allen and Earland

1910; Murray, 1963); and (3) rapidly changing

environmental conditions (Scott and Medioli, 1980).

A comprehensive review of deformities and their

Marine Micropaleontology 41 (2001) 193±227

0377-8398/01/$ - see front matter q 2001 Elsevier Science B.V. All rights reserved.

PII: S0377-8398(00)00061-X

www.elsevier.nl/locate/marmicro

* Corresponding author.

probable causes is given by Boltovskoy et al. (1991)

and Alve (1995).

Despite the number of published papers discussing

the aspects of morphological variability such as size,

different modes of deformation and the dominant occur-

rence of aberrant forms in relation to pollution, little

attention has been paid to the possible connection

between the mode of deformation and environmental

properties. The principal objectives of this study are:

(1) to investigate the distribution and abundance of

benthic foraminiferal species in the two studied bays;

(2) to elucidate the relationship between foraminiferal

assemblages and marine pollution; and (3) to ascertain

the connection between the modes of deformation, the

degree of pollution, on one hand, and type of pollutants.

Coastal water pollution in Egypt is an environmen-

tal problem (Nasr, 1995). In general, the source of

pollution by trace metals in the country has been

attributed to growing industrialization, improper

management and disposal of industrial wastes, and

agricultural runoff into marine water. Analysis carried

out on water samples or sur®cial bottom sediments of

the Alexandria coastal region reported the presence of

high concentrations of heavy metals (Pb, Zn, Cu and

Cr) as well as progressive enrichment in their levels

(e.g. El-Sayed et al., 1979; Rifaat, 1982; Abd El-

Hakim, 1990; El-Nady, 1996a,b; El-Rayis et al.,

1997; Fahmy et al., 1997).

In comparison to the large body of published work

regarding the chemistry of sediments and water, little

A.M. Samir, A.B. El-Din / Marine Micropaleontology 41 (2001) 193±227194

Fig. 1. Location map of the study area and stations sampled. E� Eastern Harbor; W�Western Harbor.

concern has been paid to the study of benthic forami-

nifera from the beaches of Alexandria (e.g. Said and

Kamel, 1954, 1957; El-Halaby, 1975; Abu El-Enien,

1979; El-Menhawey, 1998). No attempts have been

made thus far to elucidate the effect of pollution on

benthic foraminiferal communities.

1.1. Area description

The studied areas include two bays which are

located along the Alexandria coast, Egypt (Fig. 1).

El-Mex Bay, one of the most polluted areas, is ellip-

tical in shape, extends for about 15 km between El-

Agami to the west and the Western Harbour (WH) to

the east, and from the shoreline seaward to a depth of

20 m. In general, the shoreline is rocky with narrow

sandy beaches surrounding the embayments. There

are pronounced differences in both the direction and

intensity of marine currents in the bay near the outlets.

Land-derived ef̄ uent from the Umum Drain causes

the transport of surface water in a northernly direc-

tion. The bay is also characterized by the presence of

an eddy current affecting most of its parts, especially

at stations 4 and 5 (Fig. 1).

Miami Bay, a small bay located southwest of Abu

Qir city, is protected from the westward currents by a

rocky platform and from the northward currents by a

relatively large island (Gebel El Kor). It is widely

open to the sea from the northeast area where it

reaches its maximum depth ( < 6.5 m). Predominant

currents ¯ow into the bay northwesterly over the

rocky platform, which constitutes the main inlet of

marine currents into the bay. The northwest winds

generally cause the formation of shallow currents

inducing transportation of coastal sediments to the

east (El-Halaby, 1975). The shallower parts of the

bay, mainly to the south, are strongly affected by

wave action.

1.2. Pollution

El-Mex District is an industrial zone west of Alex-

andria City. As a consequence of growing heavy

industries (chlor-alkali plant, petrochemicals, pulp,

metal plating, industrial dyes, textiles) and the uncon-

trolled disposal of the resulting wastes, coastal water

of El-Mex Bay receives huge amounts of untreated

industrial wastes (Fe, Mn, Cu, Zn, Cd, Pb and Ni) as

revealed by sediment analysis (Shriadah and Emara,

1996) and water analysis (Fahmy et al., 1997). These

A.M. Samir, A.B. El-Din / Marine Micropaleontology 41 (2001) 193±227 195

Table 1

Physiographic parameters at sampled stations in El-Mex (E) and Miami (M) bays (after El-Sabrouti et al., 1997)

Water analysis Sediment analysis

Stations Depth

(m)

Temp.

(8C)

pH mg O2/l Salinity Corg

(%)

TOM

(%)

CaO

(%)

MgO

(%)

CaCO3

(%)

E1 6 18 7.91 5.75 29.45 0.188 0.34 19.194 0.32 34.275

E2 9 18.2 7.92 2.49 13.76 0.223 0.4 19.996 0.64 35.707

E3 14 18 8.05 4.22 19.19 1.058 1.9 20.343 0.85 36.327

E4 19 17.8 8.16 5.08 39.75 0.24 0.43 21.68 0.68 38.714

E5 10 17.6 8.12 4.98 15.25 0.18 0.32 23.177 0.78 41.387

E6 5 17.9 8.07 5.94 16.83 0.138 0.25 19.461 0.97 34.751

E7 2.5 17.6 7.51 3.83 7.89 0.257 0.46 18.392 0.82 32.843

E8 16 18.2 7.65 5.18 39.96 1.466 2.6 21.33 0.97 38.089

E9 16 18.2 7.62 6.33 38.12 1.74 3.15 18.766 0.78 33.511

M1 1 20.2 8.05 4.15 39.28 0.702 1.26 18.151 1.59 32.412

M2 1 19.4 8.05 4.42 39.75 0.781 1.4 20.851 0.77 37.234

M3 4 19.3 8 3.74 38.91 0.257 0.46 17.884 0.67 31.936

M4 1 19.4 7.92 4.61 39.44 0.18 0.32 17.135 0.37 30.598

M5 1 19.4 8.03 3.84 39.96 0.233 0.42 17.242 0.43 30.789

M6 3.5 18.8 7.95 3.63 38.86 0.9 1.62 19.033 0.68 33.987

M7 6.5 18.8 8.05 5.63 39.54 0.497 0.9 19.648 1.08 35.086

M8 2.5 18.6 8.13 4.83 38.7 0.069 0.12 18.124 0.62 32.124

M9 2 19 8.16 6.66 38.39 0.109 0.2 17.055 0.54 30.455

wastes, which contain potentially toxic metals, are

dumped directly into the bay via a pipeline in its

southern part (nearby stations 1 and 2, Fig. 1). More-

over, about 2.6 million m3/year discharges into the

bay through the Umum Drain from Lake Maryut, a

watermass highly polluted by agrochemicals, indus-

trial and domestic wastes (Samir, 1994). Therefore,

stations 1, 2, 6, and 7 are more likely to receive higher

concentrations of trace metals due to their proximity

to the Umum Drain (stations 6 and 7) and pipeline

discharging the industrial wastes (stations 1 and 2).

The eastern part of the bay receives brackish water


Fig. 2. Graphic mean size distribution (in phi) of bottom sediments in El-Mex and Miami bays (data from El-Sabrouti et al., 1997).

( < 90.000 m3/day) from the Nubaria Canal loaded

with tanneries wastes through the WH outlet. Close

proximity of a cement factory contributes signi®cant

amounts of cement dust to the bay water. Shipping

activities along the main trade harbour (Western

Harbour) contribute to bay pollution.

Miami Bay, unlike El-Mex Bay, has no industrial

activity on the adjacent coast. Only domestic wastes

contribute through an outfall to the bay, which do not

carry signi®cant amounts of heavy metals (Nasr,

1995; Table 1, Sample 10). Therefore, it was selected

as a consite because it is free from industrial pollution.

1.3. Environmental parameters of the studied areas

To assess the impact on the biota, comparisons

between the unpolluted and the polluted areas might

be useful if the areas in focus have comparable and

relatively homogeneous hydrographical and physical

characteristics. The oceanographic (depth, tempera-

ture, salinity, hydrogen ion concentration ªpHº,

dissolved oxygen ªDOº), as well as the geochemical

parameters (the concentrations of CaO, MgO, CaCO3,

organic carbon ªCorgº content, total organic matter

ªTOMº) are almost the same for the two bays based

on measurements on the same samples made by El-

Sabrouti et al. (1997). Their results of analyses on

both water and sediments are summarized in Table

1. However, there are notable differences in the

measured surface water salinities in the two bays.

The surface water salinity in El-Mex Bay ¯uctuates

widely. The water mass in front of the Umum Drain

has estuarine salinity strati®cation, a brackish surface

layer with low salinity (7.98%). This depends primar-

ily on the amount of brackish water discharged

through the drain. Below this layer, the salinity

increases with depth Ð the deeper bottom waters

have salinities up to 38.2%. In Miami Bay, by

contrast, no brackish water has been discharged into

the bay and consequently surface water salinities

exhibited normal values (ranges between 38.4 and

39.7%). The Corg varies in El-Mex Bay, gradually

increasing in a seaward direction. The corresponding

TOM ranges between 0.25 and 3.15% with a mean

value of 1.82%. The distribution of TOM is closely

related in El-Mex Bay to the grain-size distribution

(El-Sabrouti, et al., 1997). In Miami Bay, by contrast,

there is no appreciable difference in the Corg; it ranges

from 0.07 to 0.9%. The corresponding TOM varies

between 0.12 and 1.62% with a mean value of

0.7%. The distribution of the TOM is not clearly

related to the grain-size distribution. The zonal distri-

bution of the TOM coincides with the distribution of

the seagrasses on the ¯oor of the bay.

1.4. Grain-size distribution

Generally, the grain-size in El-Mex Bay decreases

seaward. According to the data published by El-

Sabrouti et al. (1997), sediments of El-Mex Bay

consist mainly of coarse sand (stations, 1, 2, 5, 6, 7;

Fig. 2). The outer margin of the bay (stations 8 and 9)

is covered by coarse silt, whereas the deepest part of

the bay (stations 3 and 4) is covered by ®ne sand.

In Miami Bay, 6 sedimentological zones can be

differentiated (Fig. 2). The western part is character-

ized by a very coarse sand with abundant seagrasses

(station 2). The middle part of the bay (stations 3, 6,

8), as well as the northeastern entrance of the bay

(station 7) are covered by coarse sand. The southwes-

tern and southeastern coastal parts (stations 1 and 9)

are made up of medium sand. The last zone, situated

between the southeastern and southwestern coastal

parts (stations 4 and 5), is covered by ®ne sand.

2. Materials and methods

Sampling was completed during March 1994 using

a Petterson grab sampler. Sediment samples were

taken from 18 stations; nine from each bay (Fig. 1).

From each grab sample, only the top 1±2 cm of undis-

turbed sediments were retained and preserved in 20%

formalin solution. This part was used because it

includes faunas that have been impacted by the

prevailing polluted conditions and not representing

different age ranges (and different discharge

histories). In the laboratory, a constant volume

(about 50 cm3) was stained with buffered rose Bengal

dye (1 g of rose Bengal in 1 l of distilled water) for

48 h to differentiate between living and dead forami-

nifera following Walton's technique (1952). Wet

samples were washed through 63 mm screen and

oven dried at 608C. Three hundred specimens from

all size fractions together (250±500, 125±250, and

63±125 mm) were picked and identi®ed following

the generic classi®cation of Loeblich and Tappan


(1988). All deformed tests, whenever present, were

picked from each sample and morphologically exam-

ined. Live and dead foraminifera were studied sepa-

rately. As the living individuals were present in low

numbers (mostly 1±6 in the 300 picked specimens) in

the two bays, the dead foraminifera were used for

statistical purposes because: (1) they provided a larger

data base; (2) the total (living and dead) populations

are often statistically identical and only diverge when

living/total becomes large (Murray, 1976, 1991).

Consequently, there are no obvious differences in

the population parameters between the living and

dead assemblages (e.g. Buzas, 1965; Scott and

Medioli, 1980; Yanko et al., 1994). To qualitatively

estimate the heavy metals within the foraminiferal

tests, analyses were made on living normal and aber-

rant tests using an energy dispersive spectrometer

(Link ISIS Oxford Analyzer) attached to SEM

(JEOL JSM 5300). X-ray spectra were obtained at

20 kV accelerating potential and measured in counts

(live counting time of 100 s). Prior to chemical analy-

sis, the analyzed tests were carefully cleaned in an

ultrasonic cleaner, washed thoroughly with distilled

water and oven dried at 608C to minimize the prob-

ability for the loss of volatile metals (Siegel et al.,

1994). Since results from juvenile tests are inconclu-

sive, the analysis was carried out on the adult speci-

mens (.125 mm). To eliminate variations in the vital

effect attributable to different foraminiferal species all

the analyzed specimens belonged to the same species

(Ammonia beccarii formae). Due to the heterogeneous

distribution of trace metals (Severin, 1990), at least

three points on each test were measured to check for

internal variability of the shell composition. Care was

taken to avoid edges and pores of specimens to mini-

mize the possibility of contamination in the data

obtained. Ca, Mg and Al were measured along with

the heavy metals Zn, Cu, Pb, Cr and Cd. To measure

heavy metal concentrations in sediments of El-Mex

Bay, samples were frozen immediately after

sampling. In the laboratory 0.5 g of each dry sample

(63 mm fraction) was dissolved in a mixture of 5:1

perchloric and hydro¯uoric acids (v/v), respectively,

following the method of Tessier et al. (1979). The

concentrations were measured using the ¯ame atomic

absorption spectrophotometer (Perkin±Elmer Mode

2380). The precision (^8%) was checked by dupli-

cate analysis, whereas accuracy (^5%) was checked

using sensitivity check standards for the analyzed

elements (Pb, Zn, Cu, Cr and Cd).

2.1. Statistical treatment

The relative frequencies of foraminiferal species

from 18 stations were treated in Q-mode cluster analy-

sis using the Statistical Package for Social Sciences

(SPSS/Pc1) Package Computer program (Version 4.0,

Norusis, 1990). Although, there are a wide variety of

techniques, the average linkage methods are the most

widely used in ecology (Pielou, 1984). Of the average

linkage methods we prefer to use the unweighted

(UPGMA) pair group than the weighted pair group

(WPGMA) method. This is because the latter is

more sensitive to minor differences between the

assemblages, and tend to form many groups, rather

than a few distinct groups as in the UPGMA (Kovach,

1987). The resulting dendrogram clusters the samples

into groups, each one is characterized by the presence

of certain dominant taxa. The rare taxa have little

effect on the formation of the main groups, particu-

larly when these taxa occur in low abundances in

samples with more abundant taxa (Kovach, 1987,

1989). Species diversity was estimated using the

following parameters: (1) species diversity (number

of species in a sample, Murray, 1991); (2) percentage

dominance (highest percentage abundance of forami-

niferal species in a sample (Walton, 1964), also the

number of species forming 80%; (3) population

density (number of specimens per 1 g dry sediments);

and (4) a -Fisher index (relationship between the

number of species and the number of individuals in

an assemblage, Murray, 1973).

3. Results

3.1. Sediments

Since sediments are the ®nal host of contaminants

in the marine environment, it is possible to pollution

by means of sediment analyses. Sediments are prefer-

able to other components of the marine environment,

as they are not mobilized as fast as biota or water.

Geochemical analyses of Cu, Zn, Pb, Cr and Cd

from El-Mex Bay are shown in Fig. 3A±E. The distri-

bution patterns for Cu, Pb, Zn, and Cd are similar:

maximum concentrations are present in the vicinity


of stations 1 and 2 (near to the pipe discharging the

industrial wastes) and to some extent stations 6 and 7

(close to the ef¯uent of the contaminated water

coming through the Umum Drain). Unlike those for

Cu, Zn, Pb and Cd, the greatest concentration of Cr is

at stations 8 and 9 which are located near the WH

outlet discharging wastes rich in chromate or dichro-

mate resulting from the leather tanning industries.

Rifaat and Deghedy (1996) studied a natural unpol-

luted beach located west of Alexandria. They found

that sediments of their study area contained lower

average concentrations of metals when compared to


Fig. 3. Contour maps showing the distribution of measured heavy metals (ppm%) and deformed forms percent (D.f.) in sediments of El-Mex

Bay.

other areas in the Mediterranean Sea (El-Sayed et al.,

1988; Rifaat et al., 1992; El-Sayed and Rifaat, 1993),

the Red Sea (El-Sayed, 1984; Montaggiont et al.,

1986; Rifaat, 1994) as well as different seas (Wede-

pohl, 1978). Their values were considered in the

present study as the background levels (Table 2).

Compared with the levels of metals encountered in

the current study (Table 2), it is obvious that El-

Mex Bay exhibits severe pollution conditions: Cu is

53.3 times, Pb is 15.7 times, Zn is 24.9 times, Cr is

14.5 times, and Cd is 41.4 times higher than back-

ground levels. Furthermore, the results obtained

showed progressive enrichment in heavy metal

concentrations over time when compared to that

detected by Rifaat (1982) from the same sites

(Table 2).

3.2. Foraminifera

3.2.1. Characteristics of foraminiferal assemblages

The dead foraminiferal assemblages of the two

studied bays were composed almost entirely of benthic

species. Due to the shallow water in the two bays, plank-

tic species were very rare, represented by members of

the suborder Globigerinina (family Globigerinidae), e.g.

Globigerina bulloides (0.7%) in El-Mex Bay (station

5) and Globigerinoides ruber (0.03%) and G.

bulloides (0.07%) in Miami Bay (station 6).


Table 2

Values of heavy metal concentrations and enrichment levels in sampled sediments of El-Mex Bay as measured by the FAAS

St Zn

(ppm)

Cu

(ppm)

Pb

(ppm)

Cr

(ppm)

Cd

(ppm)

E1 123.3 355.8 157.7 73.2 49.5

E2 109 280.9 129.8 62.5 43.4

E3 80 170.9 24.2 43.4 23.6

E4 55.1 118.5 40.9 64 30.2

E5 70.5 162.3 97 58.1 34.7

E6 82.75 306 106.5 73.6 39.6

E7 90 202.1 113.8 87.9 41.8

E8 71.4 143.6 23.1 127.8 47.2

E9 81.4 131 39.3 152.6 26.1

Mean (1994) 84.8 207.9 81.4 82.5 37.3

(Present study)

Minimum 55.1 118.5 23.1 43.4 26.1

Maximum 123.3 355.8 157.7 152.6 49.5

Mean (1982)a 68 176 Not determined 3.2

Backgroundb 3.4 3.9 5.2 5.7 0.9

Enrichmentc 1.25 1.12 ± ± 1.17

Enrichmentd 24.94 53.31 15.65 14.47 41.44

a Date after Rifaat (1982).b Data after Rifaat and Deghedy (1996).c Enrichment�Mean of 1994/mean of 1982.d Enrichment�Mean of 1994/background values.

Table 3

Characteristic species restricted to each bay

Miami Bay El-Mex Bay

Adelosina cliarensis Textularia truncata

A. duthiersi Neopateoris cumanaensis

Spiroloculina angulosa Pseudotriloculina laevigata

S. excavatum Wellmanellinella striata

Miliolinella labiosa Parrina bradyi

Pseudolachlanella slitella Ammonia beccarii forma beccarii

Pyrgo striolata Ammonia beccarii forma tepida

Articulina carinata Haynesina depressula

Amphisorus hemprichii Elphidium excavatum

Amphistegina radiata

Elphidium serrulatum

Reussella spinulosa

Globulina gibba

Ammonia beccarii forma

parkinsoniana

A total of 78 benthic species belonging to 41 genera

were identi®ed from the two studied bays. Fifty-seven

species were found in common, whereas 9 and 14

species were restricted to El-Mex and Miami bays,

respectively (Table 3). The suborder Miliolina was the

most dominant, representing 62.5 and 69.5% of the total

assemblages in El-Mex and Miami bays, respectively. It

was represented, in decreasing order, by the families

Haurinidae, Peneroplidae, Spiroloculinidae, Soritidae

and Fisherinidae (Fig. 4). Forty species of these families

were found in common, whereas four were restricted to

El-Mex Bay (Neopateoris cumanaensis, Pseudotrilocu-

lina laevigata, Wellmanellinella striata and Parrina

bradyi), and nine species to Miami Bay (Adelosina

cliarensis, A. duthiersi, Spiroloculina angulosa, S.

excavata, Milionella labiosa, Pseudolachlanella

slitella, Pyrgo striolata, Articulina carinata and Amphi-

sorus hemiprichii).

Members of the suborder Rotaliina comprised the

second most important component in the recorded

foraminiferal assemblages, comprising 34.55 and

30.2% of the total assemblages in El-Mex and Miami

bays, respectively. Major families present (in decreas-

ing order) were: Cibicididae, Rotaliidae, Rosalinidae,

Elphidiidae, and Asteriginidae. Families recorded in

low frequency were: Bolivinidae, Planorbulinidae,

Buliminidae, Reussellidae, Eponididae, and Nonioni-

dae. The Amphisteginidae (1.5%) were restricted to

Miami Bay. The families Planorbulinidae, Amphiste-

ginidae, Rosalinidae, Cibicididae, and Elphidiidae

showed similar distribution patterns throughout

Miami Bay. In El-Mex Bay their frequency varied,

exhibiting lower values at stations 4 and 5 (Fig. 5).

Family Rotaliidae, represented mainly by Ammonia

beccarii formae (tepida and beccarii), was more abun-

dant in El-Mex Bay. This could be attributed to their

ability to tolerate lower salinities (Walton and Sloan,

1990) and to colonize in polluted areas as will be

discussed later. Family Cibib ididae presented in

higher percentages in Miami than El-Mex Bay due to

their intimate association with seagrasses which are

widespread in Miami Bay.


Fig. 4. Histogram showing the distribution of foraminiferal families in the bays studied.

Minor components of the recorded assemblages

were represented by members belonging to the subor-

ders Lagenina and Textulariina. Suborder Lagenina,

represented by family Polymorphinidae, constituted

0.1 and 0.2% of the total assemblages in El-Mex

and Miami bays, respectively. Globulina gibba was

restricted to Miami Bay, while Guttulina problema

was recorded in both bays. The only representatives

of the suborder Textulariina were represented by the

family Textulariidae (0.1%) and restricted to El-Mex

Bay, e.g. Textularia truncata which was recorded

from stations 5 and 9. Due to heavy metal pollution,

living species (Ammonia beccarii forma tepida and

Elphidium excavatum) were few and sporadic in

their occurrence in El-Mex Bay (Table 4; Fig. 6).

They were represented by 1, 3, and 4 individuals in

stations, 3, 8, and 9, respectively.

In Miami Bay, the majority of the living population

consisted of Ammonia beccarii forma parkinsoniana,

Sorites orbiculus, Peneroplis pertusus, Reussella

spinulosa, Rosalina globularis, R. macropora, Aster-

igerina mamilla, and Amphistegina radiata. Despite

of the fact that Miami Bay is not polluted by heavy

metals (which have deleterious effects on benthic

foraminifera), the number of living individuals is

low, falling within the range of 1±6 except in station

6 where it reached 20 (Table 4; Fig. 6). This may be

due to the coarse±very coarse sandy nature of the

bottom sediments that leads to the prevalence of

oligotrophic conditions. This is in accordance with

the ®ndings of Phleger (1960), Murray (1968),

Antony (1968), Mohamed (1972), and Zazou

(1977). These authors ®nd that the ®ne sand and

silty sand substrata yield high numbers of living

species and individuals. In contrast coarse±very

coarse sand or clay which have lower numbers. More-

over, the ®ne-grained sediments generally contain

higher percentages of organic matter, and thus more

potential food, than coarse-grained sediments. These

conditions might be attributed to the continuous


Fig. 5. Distribution of the suborder Rotaliina (Rotaliidae, Elphidiidae, Rosalinidae and Cibicididae) in the two bays.

winnowing of the ®ne particles by the prevailing

current action in the west-easterly direction as

detected by El-Halaby (1975).

3.2.2. Foraminiferal diversity

Species diversity was higher in Miami than El-Mex

Bay. Simple diversity values ranged between 34 and

49 in Miami Bay, while in El-Mex Bay it ¯uctuated

between 13 and 41 (Fig. 6). In El-Mex Bay, the high-

est values occurred at stations 3, 4, and 8, intermediate

values were found in the middle part of the bay

(stations 5, 6 and 7), and lowest values at stations 1

and 2.

Percentage dominance values show the reverse

pattern to species diversity; ¯uctuating in El-Mex

more than in Miami Bay. The number of species form-

ing 80% was low, in general, in El-Mex Bay, particu-

larly at stations 1 and 2 (6 and 5 species, respectively),

as well as stations 6 and 7 (8 and 13, respectively). In

Miami Bay, they fall within the range of 14±21,

except for station 9 (12).

The a -Fisher index values in the two studied bays

fall within the range of the values found by Murray

(1973) for shelf seas �a . 5� with the exception of

station 2 in El-Mex Bay which registered a lower

value �a � 3�: The value at station 1 was just above

the boundary �a � 5:8�: Conversely, in Miami Bay

the values ranged between 10 and 17.

Population density (the number of specimens per

1 g dry sediments) is lower in El-Mex than in

Miami Bay. It ranged between 12±459 and 55±446

in El-Mex and Miami bays, respectively (Fig. 6).

Outstanding population density occurred at station 1

in Miami Bay (1636). Since this station is located

relatively far away from arti®cial beach nourishment

(which affect the other near-beach stations 6, 7 and

12), it is not affected by sediment dilution.

3.2.3. Cluster analysis

Q-mode cluster analysis performed to study simila-

rities between the stations; relationships were

displayed as dendrograms. The resulting dendrograms

(Fig. 7) represent the grouping of the stations accord-

ing to the relative abundance of benthic foraminiferal

species in each one. The clusters are regarded as

biotopes and are interpreted as representing different

ecological conditions. Samples from El-Mex Bay

were grouped into two main clusters (I and II), each

with two subclusters, whereas those of Miami Bay

were grouped into three clusters (I, II and III).


Table 4

Statistical parameters at sampled stations in El-Mex (E) and Miami (M) bays

St. Species

diversity

%

Dominance

No. of spp.

forming 80%

Population

density

a-Fisher

index

Living individuals

per 300

Deformed

%

E1 23 36.2 6 34 5.8 0 2.1

E2 13 38.7 5 12 3 0 25.7

E3 36 19.7 15 213 10.5 1 0.5

E4 41 12.5 19 446 12.5 0 0.5

E5 33 18.5 16 95 9.5 0 2

E6 24 37.3 8 99 6 0 0.3

E7 24 30.7 13 62 6 0 0.7

E8 30 11.5 13 459 8.2 3 1.1

E9 41 9.7 19 401 12.5 4 0.8

M1 34 23 21 1636 10 4 0

M2 46 12.4 21 55 15 3 0.7

M3 46 13.6 18 162 15 4 0

M4 37 27.3 14 321 11.5 5 0

M5 37 31.8 14 464 11.5 3 0

M6 42 11.8 16 403 13 20 0

M7 34 20.3 12 63 10 1 0

M8 38 13.8 16 264 11.8 5 0

M9 49 27.7 18 445 17 6 0

A.M

.S

am

ir,A

.B.

El-D

in/

Ma

rine

Micro

paleo

nto

logy

41

(2001)

193

±227

20

4

0 2.5 5

Deformed %

0 2.5 5

0 10 20

Living Ind. /300

0 10 20

0 5 10 15

- Fisher index

0 10 20

0 250 500

PopulationDensity

0 250 500

0 10 20

No. of spp.forming 80%

0 10 20 30

0 20 40

% Dominance

0 20 40

0 25 50

E1

E2

E3

E4

E5

E6

E7

E8

E9

Species Diversity

0 25 50

M1

M2

M3

M4

M5

M6

M7

M8

M9

S

t

a

t

i

o

n

s

1636

25.7

α

Fig. 6. Statistical parameters used to relate the foraminiferal assemblages to the environmental conditions in El-Mex (top) and Miami (bottom) bays.

A.M. Samir, A.B. El-Din / Marine Micropaleontology 41 (2001) 193±227 pp. 205±208

Fig. 7. Frequencies of common foraminiferal species, biotope relationship (de®ned by cluster analysis) and environmental considerations in

El-Mex (E) and Miami (M) bays.

Fig. 7 shows the characteristic assemblage of each

biotope together with the ecological interpretation. In

case of El-Mex Bay, Cluster I represents the high

energy, near-shore biotope (2.5±9 m). Stations of

this cluster have a signi®cant statistical difference

from those of cluster (II) since their foraminiferal

assemblage is less diversi®ed due to the prevalent

conditions of environmental stress. Cluster I includes

sub-biotopes (A) and (B), respectively.

Sub-biotope (A) includes stations 6 and 7, located

adjacent to the Umum Drain and has an assemblage

consisting of 30 species. The assemblage is dominated

by Peneroplis pertusus (33.7%) Rotalia macropora

(13%), Asterigerina mamilla (9.3%), Quinquelocu-

lina auberiana (8.7%), and Elphidium crispum

(4.9%). Samples of this sub-biotope appear to be

under stressful environmental conditions due to the

in¯ow of the contaminated water of the Umum

Drain, although not as severe as in samples of sub-

biotope (B) described below.

Sub-biotope (B), which is made up of two stations

(1 and 2) located in the immediate vicinity of the

pipeline discharging the industrial wastes, represents

the highly polluted sub-biotope. The foraminiferal

assemblage was less diversi®ed, consisting of 25

species, 19 of them are the same as in sub-biotope

(A). Eighty percent of the assemblage was composed

of Quinqueloculina auberiana (34.7%), Q. disparilis

(22%), Q. annectens (5.4%), Q. vulgaris (4.2%),

Triloculina tricarinata (7.7%), and Adelosina medi-

terranensis (3.3%). The basic changes distinguishing

this sub-biotope from the preceding one are a reduc-

tion in the diversity of the assemblage and the predo-

minance of Quinqueloculina species; associated with

a decrease in Peneroplis pertusus, Rosalina macro-

pora, and Asterigerina mamilla.

Cluster II represents the low energy off-shore

biotope. It occupies the deepest part of the bay

(10±19 m), away from the direct effect of pollution.

It is characterized by having a comparatively diversi-

®ed foraminiferal assemblage which indicates a return

to nearly normal conditions. Two sub-biotopes can be

recognized within this biotope, and although closely

related, each indicates slightly different environmen-

tal conditions.

Sub-biotope (C) is formed of three stations (3, 8 and

9). Samples of these stations consist of silt or sandy

silt and were characterized by organic-rich substrates.

The recorded assemblage was composed of 51

species, predominated with Quinqueloculina seminu-

lum (13.1%), Q. tropicalis (8.4%), Sigmoilinita spp.

(5.8%), Ammonia beccarii forma tepida (11.2%),

Rosalina globularis (9.3%) and Elphidium excavatum

(4.5%).

Sub-biotope (D) encompasses stations 4 and 5. The

distribution of this sub-biotope re¯ects the in¯uence

of brackish water in¯ow discharged from the Umum

Drain into the bay. The total assemblage consists of 53

species, 77.4% of which are the same as in sub-

biotope (C). Sub-biotope (D) differs from sub-biotope

(C) in the increase of Quinqueloculina disparilis

(from 0.4 to 13.2%), Peneroplis planatus (from 0.6

to 10.1%), Sorites orbiculus (from 0.5 to 8.2%); and

the decrease of Q. tropicalis (from 8.4 to 0.0%), Q.

seminulum (from 11.2 to 1.1%), Sigmoilinita spp.

(from 5.8 to 1.1%), and Ammonia beccarii forma

tepida (from 11.2 to 1.1%). Samples containing this

assemblage were made up of ®ne sand.

In Miami Bay, cluster analysis differentiates

between three biotopes. The distribution of these

biotopes has a signi®cant relationship with depth,

organic matter, and seagrasses (Fig. 8).

Cluster I, which consists of four (1, 4, 5 and 9)

stations, represents the near-shore (1±2 m water

depth) biotope, with high energy environmental

conditions. The foraminiferal assemblage of this

biotope consists of 54 species. The most abundant

species are Peneroplis pertusus (27.5%), Lachlanella

planciana (8.1%), Asterigerina mamilla (8.3%), and

Rosalina macropora (5.9%). Sediments bearing this

assemblage vary in composition from medium sand

(stations 1 and 9) to ®ne sand (stations 4 and 5) with

a low organic matter content and scarce occurrence

of seagrasses. Peneroplis pertusus lives as symbiont

on red soft algae (Leutenegger, 1984; Reiss and

Hottinger, 1984) that needs a quiet environment

with high light intensity (Murray, 1991). Their occur-

rence with a high percentage in this high-energy

environment suggests that they have been trans-

ported, most probably from the sediments of Cluster

II (described below) and resedimented in this

biotope.

Cluster II includes samples 2, 3, 6, and 8 located

at intermediate depths of the bay (1±4 m) and char-

acterized by the abundant occurrence of seagrasses.

These samples consist of very coarse sand which


decreased gradually in size in a west±east direction.

The foraminiferal assemblage of this biotope is

diverse, consisting of 63 species and dominated

by Peneroplis pertusus (11.8%), Quinqueloculina

auberiana (9%), Q. inaequalis (5.6%), and Triloculina

tricarinata (8%).

Cluster III is a disjunct cluster, representing the off-

shore biotope. It is formed of one sample (7), which is


Plate I. All scales are 100 mm unless noted otherwise.

(1)±(3) Quinqueloculina disparilis d'Orbigny. (1) and (2) Side view and apertural view of normal specimens, both views from M7. (3)

Apertural view of deformed specimen, E1. Note the double apertures.

(4)±(8) Adelosina mediterranensis (Le Calvez). (4) Side view of normal specimen, E5. (5)±(8) Side views of deformed specimens show

distorted chamber arrangement, all specimens from E1.

(9)±(17) Deformed forms of miliolids. (9) Side view shows creases of the chambers, scale 500 mm, E6. (10)±(13) and (16) Side views show

abnormal growth, (10)±(12) scale 500 mm, the ®rst three specimens from E2, the others from E1. (14) Oblique side view shows

double apertures, E5. (15) Apertural view shows twisted of pen-ultimate chamber, E2. (17) Side view shows lateral asymmetry of

the apertural position, E4.

Fig. 8. Energy dispersal X-ray analyses show the qualitative elemental composition as measured in counts in living deformed (A, C) and non-

deformed (B, D) tests of Quinqueloculina disparilis (top) and Q. seminulum (bottom).

located at the deepest part of the bay (6.5 m). The

foraminiferal assemblage of this biotope is less diver-

si®ed (34 species), probably due to winnowing by

tidal currents. The distinctive foraminiferal species

are Quinqueloculina auberiana (20.3%), Q. disparilis

(12.2%), Triloculina tricarinata (13.2%), and

Elphidium crispum (12.2%). Sediments of this

biotope are formed of coarse sand and a moderate

concentration of organic matter.

3.3. Test deformities

Out of 78 species found in the present study, only 18

species (23%) exhibit morphological deformities. The

deformities were restricted mainly to the families Haur-

inidae, Peneroplidae, Soritidae and Cibicidade.

Deformed specimens were mainly present in El-Mex

Bay where they comprised up to 25.7% of the total

assemblage. In severe cases, test deformation is so

extreme that taxonomic identi®cation becomes very

dif®cult (Pl. I, ®gs. 9±17). Maximum numbers of

deformed specimens were recorded at stations 1 and 2

(2.1 and 25.7%, respectively; Fig. 3F) which are closest

to the pipeline discharging industrial wastes. Morpho-

logical deformities in El-Mex Bay were manifest as:

double apertures (Pl. I, ®gs. 3 and 14; Pl. III, ®gs. 8

and 9), protuberances of one chamber (Pl. II, ®g. 9;

Pl. III, ®g. 2), abnormal growth (Pl. I, ®gs. 5±8, 10±

13, 16; Pl. II, ®gs. 7, 13±15, 17; Pl. III, ®gs. 4±7),

twisted or distorted chamber arrangement (Pl. I, ®g.

15; Pl. III, ®gs. 11±13), compressed tests (Pl. III, ®g.

20), spiroconvex tests (Pl. III, ®gs. 14±16), wrong

direction of coiling (Pl. II, ®g. 2), aberrant chamber

shape and size (Pl. III, ®gs. 3 and 19), and overdeve-

loped chambers (Pl. III, ®gs. 17 and 18). Some speci-

mens accumulate more than one deformation (double

apertures, siamese twins, Pl. III, ®gs. 8 and 9). In Miami

Bay, on the other hand, deformed specimens were

recorded only from station 2 (0.7%), represented by

siamese twins (Pl. II, ®gs. 11 and 12) and reduction in

the size of one or more chambers (Pl. III, ®g. 10). It is

believed that morphological abnormalities detected

from El-Mex Bay were caused by stressed conditions

on the sea bottom related to heavy metal contamination.

Nevertheless, to eliminate the effect of natural environ-

mental stresses as a possible reason for test deformities,

X-ray analyses were performed on living deformed and

non-deformed individuals of Quinqueloculina dispari-

lis (costate, calcareous imperforate wall), Q. seminulum

(smooth, calcareous imperforate wall),and Ammonia

beccarii s.l. (smooth, calcarperforate wall). The results

obtained (Figs. 8 and 9) revealed that deformed tests

contain rather higher concentrations of Cu, Zn and Cr

compared to the non-deformed tests independent of life

habitat, surface ornamentation as well as wall structure,

except that Cr is not able to incorporate within tests with

calcareous imperforate wall.

4. Discussion

4.1. Diversity indices

Species diversity can be viewed as a gross measure

of the effect of environmental stresses on benthic

foraminiferal communities. Low species diversity is


Plate II. All scales are 100 mm, except 16 � 200 mm:

(1) and (2) Quinqueloculina seminulum (Linnaeus). (1) Side view of normal specimen, E3. (2) Side view of deformed specimen shows change

in the direction of the axis of coiling and multiple apertures, E1.

(3) and (4) Peneroplis pertusus (Forskal). (3) Side view of normal specimen, M5. (4) Side view of deformed specimen shows the tendency of

uncoiling chamber arrangement, E9.

5)±(9) Peneroplis planatus (Fichtel and Moll). (5) and (6) Side views of normal specimens, M3. (7)±(9) Side views of deformed speci-

mens. (7) Note the abnormal growth of the last formed chamber, E3. (8) Deformed side view shows reduction in the size of the last

formed chambers, E4. (9) Deformed side view with protuberances, E8.

(10)±(12) Amphisorus hemprichii Ehrenberg. (10) Side view of normal specimen, M1. (11) and (12) Deformed specimens show siamese

twinns, both views from M2.

(13)±(15) Deformed forms of Lobatula lobatula (Walker and Jacob), all specimens from E2. Note the abnormal growth of the tests.

(16) and (17) Elphidium excavatum (Terquem). (16) Side view of normal specimen, E8. (17) Side view of deformed specimen shows axial

elongation of the test, E9.

characteristic of polluted environments (Bretsky and

Lorenz, 1970; Schafer et al., 1991; Yanko et al.,

1998). Although, many benthic species respond favor-

ably and could bene®t from organic wastes as a source

of nutrients (Watkins, 1961; Yanko et al., 1994),

heavy metals and chemicals are unlikely to favor

any particular species. In the present investigation,

the foraminiferal assemblage was most diverse and

dense in Miami Bay. Except for the low surface

water salinity values (Table 1) in some stations of

El-Mex Bay (especially station 7), there were no

apparent differences in the measured oceanographic

and sedimentological parameters in the two studied

bays. However, as the salinity values in these stations

increase with depth (up to 38.2½; El-Sabrouti et al.,

1997), it could be speculated that the presence of

heavy metals was the only variable responsible for

the adverse population response. There was a marked

negative population response to the presence of a

signi®cant concentration of heavy metals. The extent

to which population was found to be impoverished

corresponded to the degree to which the sediment

was contaminated. The most impoverished foraminif-

eral population was found in stations 1 and 2 (34 and

12, respectively) where the sediments have higher

concentrations of heavy metals than at any other

stations of the bay. The higher concentration of

heavy metals is due to the presence of the pipe

discharging industrial wastes. Stations 6 and 7 also

exhibited somewhat lower values (62) due to the

proximity of the contaminated water out¯ow from

the Umum Drain.

The species diversity trend was concordant with the

population density values. In other words, lower

diversity values were recorded at stations 1, 2, 6 and

7 (23, 13, 24 and 24, respectively). Highest values

were observed at stations 4, 8 and 9, located away

from the direct effect of pollution.

Change in species diversity as a response to estuar-

ine pollution are discussed by Schafer (1973) in

Chaleur Bay, eastern Canada. In that area, the diver-

sity is reduced close to the ef̄ uent sources re¯ecting

adverse environmental conditions. In their study of

the Chesapeake-Elizabeth outfall on the southern

shore of Chesapeake Bay, Bates and Spencer (1979)

record an increase in foraminiferal diversity and

density away from the pollution source. Moreover,

Schafer et al. (1991) recognize that species diversity

and the total foraminiferal number per cubic centi-

meter is much lower in stressed environments.

Accordingly, it could be speculated that heavy metal

pollution has a detrimental effect on both population

density and species diversity. It acts as a limiting

factor for certain foraminiferal species.

Percentage dominance shows an inverted pattern to

species diversity. Increased pollution leads to a poor

community consisting of few opportunistic species in

high numbers (Murray, 1973; Pearson and Rosenberg,

1976). This could explain the highest values of

percentage dominance at stations 1, 2, 6 and 7 in El-

Mex Bay.

The a -index was ®rst described by Fisher et al.

(1943). It shows the relationship between the number

of species and the number of individuals in an assem-

blage. The a -Fisher index had lower values (3±12.5)

in El-Mex than in Miami (10±17). Lower values in El-

Mex Bay were recorded at stations 1, 2, 6, and 7 (5.8,

3, 6, and 6, respectively) located adjacent to the dump

site and out¯ow of the Umum Drain. Values then

increased seawards (8.2±12.5) at stations 3, 4 and 8

located away from pollutants. The higher values at

Miami Bay, as well as the deeper parts of El-Mex


Plate III. All scales are 100 mm.

(1) Ammonia beccarii forma tepida (Cushman). Umbilical view of normal specimen, E8.

(2)±(20) Deformed specimens of Ammonia beccarii formae. (2) Umbilical view shows protuberances in the form of bulla-like chamber

covering the umbilicus, E8. (3) Aberrant chamber shape (broken), E8. (4)±(7) Umbilical views show abnormal growth, all speci-

mens from E2. (8) and (9) Peripheral views show siamese twins and double apertures, E4 and E1, respectively. (10) Umbilical view

shows reduction in the size of chambers, M2. (11)±(13) Peripheral views show twisting of the entire test ((11) and (12)), or the last

whorl only (13), ®rst two specimens from E2 and the other from E1. (14)±(16) Peripheral views show abnormal high spire giving

spiroconvex test, all specimens from E9. (17) and (18) Umbilical views. Note the overdeveloped chamber(s), both specimens from

E8. (19) Umbilical view shows aberrant chamber shape and size, E1. (20) Umbilical view shows extreme compression, E2.

Bay were the result of more stable environmental

conditions.

4.2. Foraminifera as bioindicators of pollution

4.2.1. Indicator or opportunistic species

Speci®c studies done by several authors led to the

differentiation between pollution-tolerant and pollu-

tion-sensitive taxa. At lower latitudes (Mediterranean,

Caribbean, and Arabian Seas), Ammonia beccarii

forma tepida has been reported to dominate in areas

close to outfalls discharging sewage (Seiglie, 1971),

chemical and thermal ef¯uents (Seiglie, 1975), ferti-

lizer byproducts (Setty, 1976), caustic soda and chlor-

ine complex (Setty and Nigam, 1984), and heavy

metals (Nagy and Alve, 1987; Alve, 1991; Shari® et

al., 1991; Yanko et al., 1994). In temperate regions,

Elphidium excavatum shows particular tolerance to

most kinds of contaminants. The results obtained

from the studies of Schafer (1973), Buckley et al.

(1974) Bates and Spencer (1979), and Schafer et al.

(1991) show that Elphidium excavatum is able to

compete successfully in polluted, near-shore environ-

ments. Besides their apparent tolerance to various

ef̄ uents, the high mobility of E. excavatum indivi-

duals (Schafer and Young, 1977) may explain their

ability to ¯ourish in contaminated areas. These

previous observations are in accordance with the

results of the present study where living individuals

recorded in El-Mex Bay belong to A. beccarii forma

tepida and E. excavatum. As the majority of deformed

tests were represented by the miliolids, it could be

speculated that they are very sensitive to pollution.

This is in agreement with the results obtained by

Rao and Rao (1979) who reported that miliolids are

less tolerant to pollution.

4.2.2. Size of foraminiferal tests

Yanko et al. (1992, 1994) have noted that the most

stunted foraminiferal tests are characteristic for areas

contaminated by heavy metals. In Miami Bay, the

total assemblage was dominated by large specimens

(.125 mm) compared to those from El-Mex Bay

where the majority of the foraminiferal assemblages

were found either in the 63 mm or the 63±100 mm

fractions. The presence of stunted adult tests indicates

that the presence of heavy metals causes a physiolo-

gical disturbance which slows normal growth.

4.2.3. Test deformities in relation to degree of

pollution and type of pollutants

Morphological abnormalities are a general feature

occurring among all benthic foraminifera. This

phenomenon occurs in both cold and warm water,

independent of latitudes, taxonomic af®nity, feeding

strategy, or test morphology (Yanko et al., 1998). The

presence of abnormal tests suggests natural environ-

mental stresses, e.g. changes in ecological parameters

(Closs and Maderia, 1968; Seiglie, 1964), extreme

environmental conditions (Zaninetti, 1982; Almogi-

Labin et al., 1992), or pollution. For a long time, it

has been dif®cult to distinguish between deformities

resulting from natural or anthropogenic stresses. For

instance Lidz (1965) has recorded up to 30%

deformed tests from Nantucket Bay and proposed

that they are either due to changing water conditions

or pollution. This is because most polluted areas are

often also naturally stressed. Subsequent studies,

however, distinguish between morphological abnorm-

alities caused by natural environmental stresses from

those caused by severe anthropogenic alterations of a

natural environment. Shari® et al. (1991) report from

their analysis on foraminiferal tests of Southampton

water that deformed specimens contain much greater

values of Cu and Zn than non-deformed specimens,

suggesting that heavy metals are responsible for test

deformities. From their study along the Mediterranean

coast of northern Israel, Yanko et al. (1998) conclude

that an increase in deformed Amphistegina lobifera,

Cibicides advenum and Pseudotriloculina subgranu-

lata indicates an increase in Cd, Cr and Ti, respec-

tively. However, they did not ®nd any correlation

between the type of morphological deformity and

heavy metal in¯uence. Geslin et al. (1998) examined

the wall texture of deformed tests in the genus Ammo-

nia. They attribute the crystalline disorganization in

the wall of deformed tests to a stress imposed to the

crystalline framework due to the introduction of alien

trace elements. The presence of empty cavities could

be caused either by a change in physical and chemical

conditions or by food shortage in the environment.

Despite of the numerous published papers on pollu-

tion and its effect on benthic foraminifera, little atten-

tion has been paid to the way in which benthic

foraminifera respond to both the type and concentra-

tion of pollutants. Still left unanswered is the ques-

tion: can benthic foraminiferal deformities in polluted


areas be related to the type and degree of pollution?

The available observations are still insuf®cient for

solving such a complicated problem. Besides, the

relationship between pollution and foraminifers is

rather dif®cult to understand, not only because the

pollutants being discharged into an environment are

very different, but also because their effect on differ-

ent species are very different. For instance, pollutants

which may be favorable for some species could be

harmful, at the same time, for others.

The variation of heavy metal content in benthic

foraminiferal tests reveals the ability of these organ-

isms to re¯ect the heavy metal contamination of their

environment, whereby a differentiation of the local

pollution effect is possible. In one species (Ammonia

beccarii s.l.), the results of our chemical analysis are

instructive. Tests of A. beccarii have been selected for

chemical analyses because of their worldwide distri-

bution, great abundance (especially, in paralic envir-

onments), and well-known biological and ecological

behavior (Murray, 1991), therefore the results are

applicable to other polluted areas. They are free-

living, thus their morphology does not vary in relation

to the substrate as in the case of epiphytic forms, e.g.

genus Lobatula which shows a wide range in test

morphology as it adjusts to the geometry of its attach-

ment surface. Moreover, A. beccarii is able to survive

in extremely low (,1½) and high (.90½) salinities

(Walton and Sloan, 1990) without undergoing

morphological changes.

X-ray analyses (Figs. 8 and 9) showed that

deformed tests (Fig. 9A±C) exhibiting higher concen-

trations of heavy metals (particularly Cu and Zn)

show higher Mg and Al (Fig. 9A±C) or Al (Fig. 8A

and C) concentrations, than those with lower heavy

metal concentrations (Fig. 9D±F), stunted (Fig. 9G),

or non-deformed tests (Figs. 8B, D and 9H). There-

fore, it could be concluded that there is a proportional

relationship between the concentration of heavy

metals (Cu, Zn) on one hand, and Mg, Al on the

other hand. This is in agreement with the results

obtained by Yanko and Kronfeld (1992, 1993).

These authors suggest that trace metal poisoning

weakens the biological barrier that differentiates

between the uptake of bivalent cations (Mg and Ca)

from seawater. The result is the substitution of Ca by

the smaller Mg-ion, provoking an increase in the Mg

concentration in the tests. The presence of high Al

concentration is due to the presence of an exogenous

layer (possibly clay minerals) covering the original

wall (CaCO3) of the deformed tests (cf. Geslin et al.,

1998).

One of the characteristic features in the results of

X-ray analyses (Figs. 8 and 9) is the great variability

in the uptake of heavy metals within the deformed

tests. The analyses showed that Cu, followed by Zn

and Cr are more easily absorbed than Pb, regardless

of their concentrations in the surrounding medium.

Rashid (1974) has shown that Cu is preferentially

absorbed by organic material, followed by Zn. Bane-

rji (1992) ®nds that Cu, Zn and Cr, in sequence, are

more easily absorbed compared to Ni and Pb. Shari®

et al. (1991) have documented that deformed speci-

mens contain much greater amounts of metals, in

particular Cu and Zn, than non-deformed specimens.

However, the analysis of their sediments (Shari® et

al., 1991, Table 1, p. 111) shows higher concentra-

tions in Pb than Cu. The explanation that Cu21 and

Zn21 are more easily absorbed than Cr61 is due to

their smaller size. The absorption of Pb by foramini-

fera, on the other hand, is very limited. This could be

explained according to the sequence of complex

stability (Irving and Williams, 1948). According to

this sequence, Pb has the highest ability to make

stable complexes such as lead carbonate. Goldberg

(1965) shows that the ability of marine organisms to

concentrate metals generally follows the Irving±

Williams succession. Moreover, Pb21 has the largest

size comparable to Cu21, Zn21 and Cr21 ions.

Consequently, Pb21 will be the least absorbed by

marine organisms like foraminifera.

Close inspection of the analyzed tests revealed that

forms with twisted, compressed, and abnormal growth

(Fig. 9A±C; Pl. III, Figs. 13, 20, and 7, respectively),

taken from stations 1 and 2, were characterized by

higher values of heavy metals than forms with

protuberances (Fig. 9D; Pl. III Fig. 10), taken from

station 8, located further away from the direct effect of

pollution. Spiroconvex forms (Fig. 9E; Pl. III, Fig. 16)

showed the presence of a signi®cant peak of Cr. This

mode of deformation was dominant at stations 8 and 9

that registered the highest organic matter content in

the two bays (Table 1). Accordingly, this type of

deformation resulted from the presence of either

high concentrations of Cr or organic matter.

Deformed specimens with reduced size of one



Fig. 9. Energy dispersal X-ray analyses show the qualitative elemental composition as measured in counts in living deformed (A±F), stunted

(G) and non±deformed (H) tests of Ammonia beccarii formae.

chamber (Fig. 9F; Pl. III, Fig. 10) from Miami Bay

have insigni®cant amounts of heavy metals, except for

a small peak of Zn. The presence of reduced size of

one chamber(s) indicates that a physiological defect

affects the growth during the formation of this cham-

ber(s). This disturbance could result from either de®-

ciency of nutrient content in water or an increase in

the concentration of Zn. Hallock (1985) has reported

on how poor nutrition may slow growth. Cedhagen

(1991) ®nds that chambers of benthic foraminifera

which are added during the winter when nutrition is

scarce, are smaller and shorter than those correspond-

ing to the summer months. The other possibility

(increase in Zn concentration) could be due to short-

term increase in the disposal of household detergent

products where most enzyme detergents contain

amounts of Zn, Fe, and Mn.

Based on the previous ®ndings of Samir (1994,

2000) from the highly polluted Lake Mariut and

Manzalah Lagoon, together with the present results,

it might be possible to establish a schematic order

for the expected mode of deformation in different

polluted areas. Deformed forms with twisted,

compressed or abnormal growth dominate in

severely polluted areas characterized by high

concentrations of heavy metals. Decreasing concen-

trations of heavy metals lead to the presence of

deformed tests with protuberances. Deformed tests

with a high spiral side could be detected in either

organically polluted sites, or sites exhibiting high

concentrations of Cr. Forms with reduced cham-

ber(s) size are characteristic for areas either polluted

by domestic sewage or containing very low levels of

heavy metals.

The aforementioned ®ndings serve as a baseline for

understanding how benthic foraminifera respond to

the type and degree of pollution. Nevertheless, future

studies including culturing the individual species and

experimentally isolating the type and degree of pollu-

tion under controlled conditions are recommended.

This is the only means of gaining really accurate

answers.

5. Summary

The present study deals with the foraminiferal

distribution in Recent bottom sediments of El-Mex

and Miami bays located along the Mediterranean

coast of Alexandria, Egypt. El-Mex Bay receives

substantial amounts of heavy metals from the

surrounding industrial area, agricultural and domestic

ef̄ uents, making it one of the most polluted areas

along the Mediterranean coast of Alexandria. On the

contrary, Miami Bay is free from industrial pollution

and receives only domestic wastes. Industrial pollu-

tion, especially by heavy metals, has a deleterious

effect upon benthic foraminifera, e.g. reduced popu-

lation diversity and density, increase in percentage

dominance, stunting of the adult tests, and the

frequent presence of deformed tests. Based on

living populations, it could be speculated that

Elphidium excavatum is the most opportunistic

species, able to compete successfully in polluted,

near-shore environments followed by Ammonia

beccarii forma tepida. Miliolids, on the other

hand, are very sensitive to pollution. Chemical

analyses of living foraminiferal tests reveal that

tests of deformed forms contain values of heavy

metals higher than non-deformed ones. Deformed

forms with double apertures, compressed tests,

twisted tests, and abnormal growth are character-

ized by the highest levels of heavy metals and

largely dominate the intensively polluted sites.

Forms with protuberances contain lower concentra-

tions of heavy metals and characterize interme-

diate polluted sites. Less polluted sites are

distinguished by siamese twins. Spiroconvex tests

are a result of either high organic matter content

or high concentrations of Cr. Future studies includ-

ing culture experiments under controlled conditions

are recommended.

Acknowledgements

We wish to thank Prof. M.I. Youssef, Faculty of

Science, Ain Shams University, Egypt for thoughtful

comments and constructive criticism of the manu-

script. Thanks are also expressed to Michele

Richard for valuable suggestions and improving

the language. The authors also thank the anonymous

referees for improvement of the manuscript and

helpful suggestions.



Appendix A

Relative percentage abundances of the species in 300 counts

Species/Stations E1 E2 E3 E4 E5 E6 E7 E8 E9 M1 M2 M3 M4 M5 M6 M7 M8 M9

p Textularia truncata 0.5 0.4

Vertebralina striata 0.4 0.6 0.4 0.6 3.3 1.6 1 0.7 0.7 1.2

Adelosina c.f. carinata-striata 0.3 0.5 0.3 0.4

A. cliarensis 0.7 0.3 0.3 0.6 1.4 0.6

A. duthiersi 0.3 0.3 0.7

A. intricata 0.7 0.4 0.3 0.3 0.4 0.3

A. laevigata 1.1 1.9 1.1 1.1 2 1.5 2.3 1.6 2.4 1 0.7 0.3 0.4 0.6

A. mediterranensis 3.4 3.2 8.4 0.4 0.9 0.7 0.7 0.7 0.3 0.7 0.3 0.4

Spiroloculina angulata 0.4 0.6 0.5 1.2 0.6 1.3 0.7 0.6

S. angulosa 0.6 0.3 0.3

S. antillarum 0.4 2.2 1 1.2 1.2 1 2.9 2 2 0.3 1.7 0.3

S. excavata 0.3

S. hadai 0.6 0.3

S. mayori 0.6 0.4 3 0.3

Agglutinella compressa 0.7 0.4 0.6 0.5 0.4 1 0.4 1 2.3 0.3 0.7 1.4 2.9 0.4 1.5

Cycloforina contorta 0.7 3.2 1.1 1.7 3.2 3.5 1.2 0.7 1.6 0.7 1 1 1 0.6

C. polygona 3.2 0.4 1.1 1.2 1 1 1.7 0.3 0.3

Lachlanella planciana 0.5 3.1 2 15 6.7 4.9 5.1 6.9 4.4 2.3 2.4 5.6

L. variolata 0.4 1.1 0.5 0.4 0.3 0.3 0.3

Massilina gualtieriana 1.1 0.7 0.3

M. paronai 0.9 1.7 1.1 0.4 1.1 2.8 1.5 1 0.3 1.4 1 2.4 3

M. secans 1.1 1.1 0.8 0.3 0.7

Quinqueloculina annectens 1.1 9.7 0.6 2.8 0.4 1

Q. auberiana 36 39 14 7.6 9.8 0.8 8.6 10.4 6.1 1.7 5.9 5.7 20.3 14 3.2

Q. bradyana 0.9 0.6 0.8 0.8 1 1 2.3 1 1.6 1.4 1.2

Q. carinata-striata 1.1 0.3

Q. costata 0.7 3.3 1.1 0.3 0.6 0.3 0.3 0.3

Q. disparilis 28 16 7.9 19 2.5 3.9 0.8 3.4 4 6.5 2.7 1.3 12 3.1 1.5

Q. inaequalis 2.8 4.6 2.7 5.8 4.7 2.3 12 1.6 2.1 3.5

Q. seminulum 3.2 20 2.3 12 8.1 1 0.9

Q. tropicals 8.9 9.9 6.5 0.3 0.7 1 0.3 0.7 1.3 0.7 0.6

Q. vulgaris 4.8 3.2 5.6 5.4 3.9 1

Af®netrina planciana 1.9 1.7 5.8 3.6 1 0.7 0.7 0.7 1.5

Miliolinella labiosa 0.3

M. perplexa 0.4 3.8 1.1 0.4 4.7 4.8 0.3 0.3 0.3 0.3 0.4 0.6

Neopateoris cumanaensis 1.1

Pseudolachlanella slitella 0.3 1 0.3

Pseudotriloculina laevigata 1.1 1.1 2.1 2.4

P. brongniartiana 1.9 2.8 1.1 1.6 1.2 0.3 1.4 0.3 1.8

P. rotunda 0.9 0.3 0.3

Pyrgo striolata 0.7

Triloculina austriaca 0.4 2.8 0.5 0.3 0.3 0.4

T. tricarinata 6 9.7 3.3 10.7 3.9 3.6 3.9 5.8 3.6 4.6 8 7.4 2.4 2.6 5.4 13 11 2.7

T. trigonula 3.7 0.4 3.4 5.6 2.2 1.6 4.1 1.6 3.4 3.3 1.9 1.7 2 1.7 2.3 1 2.1

Wellmanellinella striata 0.5 0.5 0.4

Sigmoilinita costata 3.3 1.1 3.1 4 1.3 0.4 1.4 0.3

S. grata 1.1 0.4 4.2 2.8 0.7

Articulina carinata 0.3

Parrina bradyi 0.4 0.6 0.5

Laevipeneroplis karreri 1.1 1.2 0.3 0.3

Peneroplis pertusus 0.7 3.2 0.4 5 2.8 37 30.7 3.6 23 12 14 27 32 12 1.9 9.7 28


(continued)

P. planatus 4.1 3.2 0.4 13 7.3 1.1 3.1 1.2 7.4 5.7 3.2 1.4 3.3 3 2.6 1.5

Amphisorus hemprichii 2.1 1

Sorites orbiculus 0.6 10.6 5.6 0.8 1.6 1.9 0.3 2.6 3.4 2.6 1 1 5

Globulina gibba 0.7 0.3 0.3 0.3

Guttulina problema 0.5 0.5 0.3 0.3 0.3

Globigerina bulloides 0.4 0.7

Globigerinoides ruber 0.3

Brizalina difformis 0.4 0.4 0.4 0.3 0.3 0.4 0.9

Angulogerina angulosa 0.3 0.5 0.3 0.3 0.3

Reussella spinulosa 0.3 0.3 0.6

Eponides repandus 0.4 0.6 1.7 1.6 0.7 0.7 3.9 2.4 0.6

Rosalina bradyi 0.4 2.8 3.4 1.5 0.8 1.6 2.2 1.7 1 1.4 0.3 2.4 1.5

R. globularis 9.9 0.5 8.4 9.7 1.3 0.3 1.3 3.7 0.3 0.7

R. macropora 0.4 1.9 2.3 1.1 13 13 1 2.4 3.1 2.3 1.6 7.1 6.6 5.4 3.1 6.8

Cibicides refulgens 1.1 1.9 1.1 1.7 1.5 1.6 1.6 0.6 2.3 3.9 3 3.3 4.7 1.9 6.2 2.4

Lobatula lobatula 3.2 0.4 2.8 1.6 2 1.2 1 0.7 0.3 0.6 1.7 0.3

Planorbulina mediterranensis 2.4 0.6 0.5 2 0.7 1.6 0.6

P. variabilis 0.5 0.5 0.3 0.3 0.3

Asterigerina mamilla 1.9 0.6 9 9.4 1.2 1.8 1.7 3.6 16 7.9 5.7 0.6 5.9 8

Amphistegina radiata 0.3 1.3 2.3 1 1 2.4 2.9 2.4 0.3

Haynesina depressula 0.5 0.4

Ammonia beccarii tepida 13 2.3 1.5 1.2 12 8.9

A. beccarii beccarii 1.9 4.5 2.1 0.4

A. beccarii parkinsoniana 1.2 1.3 1.9 1.7 2 2.7 3.2 8.3 2.4

Elphidium advenum 2.4 2.8 1.1 1.5 0.8 3.7 7.3 1 2 1 1.4 3 1.4 0.3 1.8

E. excavatum 5.6 0.5 6.8 1.2

E. crispum 4.4 2.2 3.4 5.7 3.9 1.7 5.2 1.4 0.7 5.7 12 6.6 0.6

E. macellum 0.4 0.4 4.7 7.5 1.2 4 2.6 3 4.6 1.4 0.6 3.1 2.6

E. serrulatum 0.9 2 0.7 0.3 0.7 2.9

Appendix B

Faunal reference list

Textularia truncata Hogland Hogland, 1947, p. 175, pl. 12, Figs. 8, 9, text ®gs.

147±149.

Vertebralina striata d'Orbigny d'Orbigny, 1826, p. 283, no. 1, Fig. 81.

Adelosina cf. carinata-striata Wiesner A. milletti var. carinata-striata Wiesner, 1923, p. 77.

pl. 14, Figs. 190, 191.

Adelosina cliarensis (Heron-allen and Earland) Quinqueloculina cliarensis Heron-allen and Earland,

1930, p. 58, pl. 3, Figs, 26, 31.

A. duthiersi Schlumberger Schlumberger, 1886, p. 100, pl. 16, Figs. 16, 18.

A. intricata (Terquem) Quinqueloculina intricata Terquem, 1878, p. 73, pl.

8, Figs. 16±21.

A. laevigata d'Orbigny d'Orbigny, 1820, p. 232, pl. 158, Figs. S, T, U.

A. mediterranensis (Le Calvez) Quinqueloculina mediterranensis Le Calvez, 1958,

p. 177, pl. 4, Figs. 29±31.

Spiroloculina angulata Cushman S. grata Terquem var. angulata Cushman, 1917, p.

36, pl. 7, Fig. 5.

S. angulosa Terquem Terquem, 1878, p, 53, pl. 5, Fig. 7.

S. antillarum d'Orbigny d'Orbigny, 1839, p. 166, pl. 9, Figs. 3, 4.


(continued)

S. excavata d'Orbigny d'Orbigny, 1846, p. 271, pl. 16, Figs. 19±21.

S. hadai Thalmann Thalmann, 1933, p. 354.

S. mayori Cushman Cushman, 1924, p. 56, pl. 20, Figs. 5, 6.

Agglutinella compressa El-Nakhal El-Nakhal, 1983, p. 129, pl. 1, Figs. 1±3; pl. 2, Figs.

10, 11.

Cycloforina contorta (d'Orbigny) :Quinqueloculina contorta d'Orbigny, 1846, p. 298,

pl. 20, Figs. 4±6.

C. polygona (d'Orbigny) Q. polygona d'Orbigny, p. 198, pl. 12, Figs. 21±23.

Lachlanella planciana (d'Orbigny) Q. planciana d'Orbigny, p. 186, pl. 10, Figs. 24, 25;

pl. 11, Fig. 6.

L. variolata (d'Orbigny) Quinqueloculina variolata d'Orbigny, p. 302, no. 26.

Massilina gualtieriana (d'Orbigny) Q. gualtieriana d'Orbigny, 1839, p. 186, pl. 11, Figs.

1±3.

Q. auberiana d'Orbigny d'Orbigny, p. 193, pl. 12, Figs. 1±3.

M. paronai Martinotti Martinotti, 1921, p. 317, pl. 4, Figs. 3±4.

M. secans (d'Orbigny) Q. secans d'Orbigny, p. 303, no. 43.

Quinqueloculina annectens (Schlumberger) Massilina annectens Schlumberger, 1893, p. 220, pl.

3, Figs. 77±79.

Q. carinata-striata (Wiesner) Adelosina milletti Wiesner var. carinata-striata

Wiesner, 1923, p. 76±77, pl. 14, Figs. 190±191.

Q. costata d'Orbigny d'Orbigny, 1826, p. 301, pl. 3, Fig. 3.

Q. disparilis d'Orbigny d'Orbigny, 1826, p. 302, pl. 3, Fig. 21.

Q. bradyana Cushman Cushman, 1917, p. 52, pl. 18, Fig. 2.

Q. inaequalis d'Orbigny d'Orbigny, p. 142, pl. 3, Figs. 28±30.

Q. seminulum (Linnaeus) Serpula seminulum Linnaeus, 1758, p. 786, pl. 2,

Figs. 1a±c.

Q. tropicalis Cushman Cushman, 1924, p. 63, pl. 23, Fig. 10.

Q. vulgaris, d'Orbigny d'Orbigny, 1826, p. 302, no. 33.

Af®netrina planciana (d'Orbigny) Triloculina planciana d'Orbigny, 1839, p. 62, pl. 15,

Figs. 5±6.

Miliolinella labiosa (d'Orbigny) T. labiosa d'Orbigny, 1839, p. 178, pl. 10, Figs. 12±

14.

M. perplexa (Mcculloch) Pippinoides perplexa Mcculloch, 1977, pl. 3, p. 571,

pl. 3, Fig. 2.

Neopateoris cumanaensis Bermuetez and Seiglie Bermudez and Seiglie, 1963, p. 102, pl. 1, Fig. 2.

Pseudolachlanella slitella Langer 1992, p. 90, pl. 2, Figs. 4±6

Pseudotriloculina brongniartiana (d'Orbigny) Triloculina brongninartiana d'Orbigny, 1839, p.

176, pl. 10, Figs. 6±8.

P. laevigata (d'Orbigny) T. laevigata d'Orbigny, 1826, p. 300, no. 145.

P. rotunda (d'Orbigny) T. rotunda d'Orbigny, 1826, p. 299, no. 4.

Pyrgo striolata (Brady) Biloculina ringens (Lamarck) var. striolata Brady,

1884, p. 143, pl. 3, Figs. 7, 8.

Triloculina austriaca d'Orbigny d'Orbigny, 1846, p. 275, pl. 16, Figs. 25±27.

T. tricarinata d'Orbigny d'Orbigny, 1826, p. 299, no. 6.

T. trigonula (Lamarck) Miliolites trigonula Lamarck, 1804, p. 351, pl. 17,

Fig. 4.


(continued)

Wellmanellinella striata (Sidebottom) Planispirina striata Sidebottom, 1904, p. 21, pl. 5,

Figs. 12±14.

Sigmoilinita costata (Schlumberger) Sigmoilina costata Schlumberger, 1893, p. 203, pl. 1,

Figs. 51, 52.

S. grata (Terquem) Spiroloculina grata Terquem, 1878, p. 55, pl. 5, Figs.

14, 15.

Articulina carinata (Wiesner) Articulina sagra d'Orbigny, var. carinata Wiesner,

1923, p. 74, pl. 19, Fig. 188.

Parrina bradyi (Millet) Nubecularia bradyi Millet, 1898, p. 261, pl. 5, Figs.

6a, b.

Laevipeneroplis karreri (Wiesner) Peneroplis karreri Wiesner, 1923, p. 96, pl. 20, Fig.

285.

Peneroplis pertusus (Forskal) Nautilus pertusus Forskal, 1775, p. 125 (®de Ellis and

Messina, 1940)

P. planatus (Fichtel and Moll) P. pertusus (Forskal) var. planatus Fichtel and Moll,

1798, p. 91, pl. 16, Figs. a±h.

Amphisorus hemprichii Ehrenberg Ehrenberg, 1939, p. 134, pl. 3, Fig. 3.

Sorites orbiculus Ehrenberg Ehrenberg, 1839, p. 134.

Globulina gibba d'Orbigny d'Orbigny, 1846, p. 227, pl. 13, Figs. 13±14.

Guttulina problema d'Orbigny d'Orbigny, 1846, p. 224, pl. 12, Figs. 26±28.

Globigerina bulloides d'Orbigny d'Orbigny, 1826, p. 322, pl. 34, Figs. 1±5.

Globigerinoides ruber (d'Orbigny) Globigerina ruber d'Orbigny, 1839, p. 82, pl. 4, Figs.

12±14.

Brizalina difformis (Williamson) Textularia variabilis var. difformis Williamson,

1858, p. 77, pl. 6, Figs. 166±167.

Angulogerina angulosa (Williamson) Uvigerina angulosa Williamson, 1858, p. 67, pl. 5,

Fig. 140.

Reussella spinulosa (Reuss) Verneuilina spinulosa Reuss, 1950, p. 374, pl. 47,

Fig. 12.

Eponides repandus (Fichtel and Moll) Nautilus repandus Fichtel and Moll, 1798, p. 35, pl.

3, Figs. a±d.

Rosalina bradyi (Cushman) Discorbina globularis (d'Orbigny) var. bradyi

Cushman, 1915, p. 12, pl. 86, Figs. 8a±c.

R. globularis d'Orbigny d'Orbigny, 1826, p. 271, pl. 13, Figs. 1±4.

R. macropora (Hofker) Discopulvinulina macropora Hofker, 1951, p. 460,

Figs. 312, 313.

Cibicides refulgens Montfort Montfort, 1808, p. 123, Fig. 122 (®de Ellis and

Messina, 1940).

Lobatula lobatula (Walker and Jacob Nautilus lobatulus Walker and Jacob, 1798, p. 642,

pl. 14, Fig. 36.

Planorbulina mediterranensis d'Orbigny d'Orbigny, 1826, p. 280, no. 2.

P. variabilis (d'Orbigny) Truncatulina variabilis d'Orbigny, 1839, p. 135, pl.

2, Fig. 29.

Asterigerina mamilla (Williamson) Rotalia mamilla Williamson, 1858, p. 54, pl. 4, Figs.

109±111.

Amphistegina radiata (Fichtel and Moll) Nautilus radiatus Fichtel and Moll, 1798, pl. 8, Figs.

a±d.

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(continued)

Haynesina depressula (Walker and Jacob) Nautilus depressulus Walker and Jacob, 1798, p. 641,

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Ammonia beccarii forma beccarii (Linne) Nautilus beccarii Linne, 1758, p. 710, pl. 1, Fig. 1.

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