Palaeogeography, Palaeoclimatology, Palaeoecology 178 (2002) 197^210

www.elsevier.com/locate/palaeo

Changes in coiling direction of Cibicidoides pseudoacutus

(Nakkady) across the Cretaceous^Tertiary boundary of
Tunisia: palaeoecological and biostratigraphic implications
Simone Galeotti  , Rodolfo Coccioni
Istituto di Geologia and Centro di Palinologia dell’Universita', Campus Scienti¢co, Localita' Crocicchia, 61029 Urbino, Italy
Received 10 September 1999; accepted 9 August 2001

Abstract

The analysis of coiling direction preference in the benthic foraminifera Cibicidoides pseudoacutus (Nakkady) has
been carried out across the Cretaceous^Tertiary boundary (K^T boundary) from four Tunisian sections representing a
palaeobathymetric transect from a middle^outer neritic to lower upper bathyal depositional setting. Our study reveals
that C. pseudoacutus developed a preference for sinistral coiling in a short time period during the lowermost Danian.
The comparison of the coiling ratio (number of sinistral vs. dextral individuals) record with isotope data and
dinoflagellate cyst assemblage distribution suggests that the development of sinistrally coiled populations of
Cibicidoides pseudoacutus might be related to a short-term cooling of both surface and bottom waters which occurred
at the K^T boundary and lasted for some 7 kyr.
The continuous occurrence and the high abundance of Cibicidoides pseudoacutus through the K^T boundary in
neritic to upper bathyal depositional environments around southern Tethys make identification of the shift in its
coiling ratio relatively easy. The development of a sinistrally coiled population in this benthic foraminiferal species is
regarded as a potential marker for the base of planktonic foraminiferal Zone P0 in Tethyan shallow water
settings. ß 2002 Elsevier Science B.V. All rights reserved.

Keywords: benthic foraminifera; coiling ratio; biostratigraphy; palaeoecology; Cretaceous^Tertiary boundary; Tunisia

1. Introduction ferent and impossible to compare as a conse-

The use of biota-based sea surface temperature
proxies across the Cretaceous^Tertiary boundary
(K^T boundary), such as foraminiferal assem-
blage-based transfer functions, is unfortunately
hampered as most calcareous plankton groups be-
low and above the boundary are completely dif-
* Corresponding author. Fax: +39-722-304273.
E-mail address: s.galeotti@uniurb.it (S. Galeotti).
quence of the mass extinction event. However,
the e¡ect of the K^T boundary event on benthic
foraminifera was relatively minor with few species
extinctions at this chronohorizon (see reviews in
Kuhnt and Kaminski, 1996 and Coccioni and Ga-
leotti, 1998) and therefore a comparison of Maas-
trichtian versus Danian assemblages is possible.
Nevertheless, examination of benthic foraminifera
as potential stratigraphic and palaeoclimatic indi-
ces across the K^T boundary has been very lim-
ited possibly also because this group is generally

0031-0182 / 02 / $ ^ see front matter ß 2002 Elsevier Science B.V. All rights reserved.
PII: S 0 0 3 1 - 0 1 8 2 ( 0 1 ) 0 0 3 9 6 - 0

PALAEO 2755 1-5-02

198 S. Galeotti, R. Coccioni / Palaeogeography, Palaeoclimatology, Palaeoecology 178 (2002) 197^210
believed to be of use only for local correlations
due to its facies dependence. An unambiguous
correlation between temperature and coiling di-
rection in Recent benthic foraminifera has been
claimed by Collins (1990) although this parameter
has been suggested to be also related to mode of
reproduction (FÖyn, 1936, 1937; Myers, 1940;
Lee et al., 1963; Nigam and Rao, 1989; Nigam
and Khare, 1992). This parameter has, therefore,
two potential applications: data from species in
which the coiling ratio is environmentally con-
trolled can be used as a proxy for sea £oor pa-
laeotemperature estimates while inheritable coil-
ing patterns may be useful in establishing
phylogenetic relationships among species.
In this paper we explore the possibility that
variations in the coiling direction preference with-
in the benthic foraminifera Cibicidoides pseudo-
acutus (Nakkady) (Fig. 1) may be the response
to a short-term bottom water temperature change
following the K^T boundary event.
With this aim four sections have been studied
from the shallow water setting of Tunisia where
rich Cibicidoides pseudoacutus populations contin-
uously occur across the K^T boundary. Results
are then compared to previously published data
on the dino£agellate-based sea surface tempera-
ture curve (Brinkhuis et al., 1998) and the oxygen
isotope record (Keller and Lindinger, 1989) from
the El Kef section.
Fig. 1. Microphotographs of Cibicidoides pseudoacutus (sample K^T boundary +60 cm from the Elles section).
PALAEO 2755 1-5-02
2. Material
El Haria Tunisian K^T boundary transition
series are among the most complete in marine
settings (e.g. Smit and Romein, 1985; Brinkhuis
and Zachariasse, 1988; Keller, 1988a,b; Pospi-
chal, 1994; Keller et al., 1995; Smit et al., 1997;
Adatte et al., 1998; Dupuis et al., 1998; Stinnes-
beck et al., 1998). In particular, the ‘El Kef I
section’ was established as the K^T boundary
‘Global Stratotype Section and Point’, the bound-
ary being placed at the base of the so-called
boundary clay layer (Cowie et al., 1989).
For this study, four sections (Elles, Ain Settara,
El Kef, and El Melah; Figs. 2 and 3) from the
NW Tunisian Trough have been studied across
the K^T boundary which falls within the El Haria
Formation. In each of the studied sections the
lowermost Danian is characterised by CaCO3 -im-
poverished lithologies with the deposition of a
dark grey clay layer underlain by a thin red layer
containing an Ir anomaly, Ni-rich spinels, and
shocked quartz which marks the K^T boundary
(Smit et al., 1997; Robin et al., 1998; Stinnesbeck
et al., 1998). The studied sites represent a north^
south palaeobathymetric transect from the mid-
dle^outer neritic Elles section to the lower upper
bathyal El Melah section. Palaeobathymetric as-
sessment of the studied sections is based on either
literature data (Burollet, 1967; Keller, 1988a,
 S. Galeotti, R. Coccioni / Palaeogeography, Palaeoclimatology, Palaeoecology 178 (2002) 197^210
Fig. 2. Palaeogeographic sketch of Tunisia at K^T time (re-
drawn from Adatte et al., 1998) with location of the studied
sections indicated by diamonds.
1992; Speijer and van der Zwaan, 1994; Adatte et
al., 1998; Stinnesbeck et al., 1998) or new data
from the El Kef section which have been inter-
preted following Sliter (1972), Sliter and Baker
(1972); Nyong and Olsson (1983/4), Olsson and
Nyong (1984) and van Morkhoven et al. (1986).
2.1. Elles K^T boundary transition
The Elles section contains one of the most com-
plete K^T boundary transitions in Tunisia, and is
similar to the El Kef stratotype section (Smit et
al., 1997; Kouwenhoven et al., 1997). The upper-
most Maastrichtian is characterised by grey marls,
siltstones and shales deposited in a middle^outer
neritic environment (Adatte et al., 1998; Stinnes-
beck et al., 1998). The lowermost Danian is rep-
PALAEO 2755 1-5-02
199
resented by a 50 cm thick boundary clay layer.
Upsection, the lithology changes to black ¢ssile
shales rich in organic matter (Stinnesbeck et al.,
1998). According to Keller et al. (2002), the
studied stratigraphic interval comprises the upper-
most part of the planktonic foraminiferal Plum-
merita hantkeninoides Zone, the entire P0 Zone
(28 cm thick), and the lowermost part of Zone
P1a (Fig. 4).
The Cibicidoides pseudoacutus coiling ratio was
calculated from 22 samples collected from 1 m
below to 1 m above the K^T boundary. Sampling
resolution is higher in proximity to the K^T
boundary where samples were collected at 1^3-
cm intervals.
2.2. Ain Settara K^T boundary transition
The Ain Settara deposits characterise a transi-
tion zone situated between the Tunisian Trough
to the north and the emergent Kasserine Island to
the south (see Fig. 2). The uppermost Maastricht-
ian consists of bluish grey marls with burrows
in¢lled with black clay at the top. The K^T
boundary transition is characterised by a complex
succession of CaCO3 -impoverished lithologies
from black and grey bioturbated clay to grey car-
bonate rich silt. Upwards in the sequence there is
a return to CaCO3 -enriched facies with the depo-
sition of grey marls. As also reported by Dupuis
et al. (1998), 15 cm below the K^T boundary
there occurs a concentration of small bivalves,
brachiopods, and solitary corals, probably due
to an episode of winnowing related to a relative
sea level fall. At the K^T boundary, a 60 cm thick
clayey layer occurs, which represents the base of
the Sidi Nasseur Marl and overlies the Maas-
trichtian deposits (Dupuis et al., 1998).
Our study focused on 23 samples spanning 1 m
below to 1 m above the K^T boundary. Samples
were taken at 2^10-cm intervals with higher sam-
pling rate close to the K^T boundary. According
to Luciani (2002), the studied stratigraphic inter-
val comprises the uppermost part of planktic for-
aminiferal Plummerita hantkeninoides Zone, the
entire Zone P0 zone (2 cm thick), and the lower
half of Zone P1a (Fig. 4). It must be mentioned
that, according to Molina et al. (1998), ¢rst speci-
200 S. Galeotti, R. Coccioni / Palaeogeography, Palaeoclimatology, Palaeoecology 178 (2002) 197^210

Fig. 3. Palaeodepth of K^T boundary sections in Tunisia. Modi¢ed after Adatte et al. (1998).

mens of Parvularugoglobigerina eugubina occur
only some 60 cm above the K^T boundary at
Ain Settara, therefore implying that Zone P0
might be much more expanded than reported by
Luciani (2002). Such a di¡erence of results can, at
least partly, be attributed to di¡erent methodolo-
gies as Molina et al. (1998) studied the fraction
greater than 63 Wm whereas Luciani (2002) ana-
lysed the fraction greater than 45 Wm.
2.3. El Kef K^T boundary transition
The El Kef K^T boundary transition is located
in a marly section that occupies the relatively
steep side of a small stream. Most previous pub-
lished studies on the El Kef section are in agree-
ment with regard to its o¡shore, outer neritic^
upper bathyal setting at K^T boundary time
(e.g. Keller, 1988a,b; Speijer and Van der Zwaan,
1994, 1996; Coccioni and Galeotti, 1998; Galeot-
ti, 1998). Previous studies also indicate that
benthic foraminifera are abundant and well-pre-
served in this section (Keller, 1988b; Speijer and
Van der Zwaan, 1994; Coccioni and Galeotti,
1998; Galeotti, 1998) also allowing a comparison
with a previously established N18 O record (Keller
and Lindinger, 1989).
The present study is based on a composite rec-
ord from El Kef I and El Kef II sections (see
Keller et al., 1995 and Smit et al., 1997 for de-
tails). For this study, 33 samples (17 from El Kef
I section and 16 from El Kef II section) were
analysed from 1 m below to 1 m above the K^T
boundary. Sampling resolution is higher in prox-
imity to the K^T boundary where samples were
collected at 1^2-cm intervals. According to Smit
in Brinkhuis et al. (1994), the studied stratigraphic
interval comprises the uppermost part of plank-
tonic foraminiferal Abatomphalus mayaroensis
Zone, or the Plummerita hantkeninoides Zone in
Keller et al. (1995). Zone P0 spans the ¢rst 58 cm
of the boundary clay layer according to the latter,
but Smit in Brinkhuis et al. (1994) discovered rare
tiny Parvularugoglobigerina eugubina 23 cm above
the K^T boundary and hence Zone P0 is reduced
to the ¢rst 23 cm of the boundary clay layer
(Fig. 4). The rest of the studied stratigraphic in-
terval represents the lower third of Zone P1a.

Fig. 4. Variations of Cibicidoides pseudoacutus coiling ratio at Ain Settara, Elles, and El Kef. Planktonic foraminiferal zonation
after Smit in Brinkhuis et al. (1994) for El Kef, Luciani (2002) for Ain Settara, and Keller et al. (2002) for Elles.

PALAEO 2755 1-5-02

S. Galeotti, R. Coccioni / Palaeogeography, Palaeoclimatology, Palaeoecology 178 (2002) 197^210 201

PALAEO 2755 1-5-02

202 S. Galeotti, R. Coccioni / Palaeogeography, Palaeoclimatology, Palaeoecology 178 (2002) 197^210
2.4. El Melah K^T boundary transition
The uppermost Maastrichtian of the El Melah
section is characterised by the deposition of un-
structured grey marls. At the K^T boundary, a 15
cm thick boundary clay layer occurs. According
to Adatte et al. (1998), Zones P1a and P1b are
here very reduced in thickness (1.2 m) as com-
pared to Elles and El Kef ( s 10 m), suggesting
a more distal palaeo-location of this site and/or
the presence of short hiatuses (erosion and/or
condensed intervals). Accordingly, palaeogeo-
graphic reconstruction of Tunisia at K^T bound-
ary time by Burollet (1967) and palaeobathymet-
ric interpretation based on benthic foraminiferal
assemblages (Adatte et al., 1998) suggest a deeper
depositional setting of El Melah when compared
to El Kef. The El Melah K^T boundary transition
represents, therefore, the deepest depositional set-
ting among the studied sections, most likely hav-
ing been deposited in the lower part of the upper
bathyal environment. Planktonic foraminiferal
Zone P0 is also reduced in thickness as compared
to the K^T boundary stratotype spanning the
lowest 10 cm of the Danian.
In this study, only ¢ve samples from a strati-
graphic interval spanning the uppermost 47 cm of
the Maastrichtian (Zone Plummerita hantkeni-
noides) have been examined.
3. Methods
Fluctuations in coiling direction of planktonic
foraminiferal species have been used in stratigra-
phy and palaeoclimatology since the 1950s (see
Kennett, 1976; Vincent and Berger, 1981; Hemle-
ben et al., 1989, and references therein). However,
a direct control of temperature on planktonic for-
aminiferal coiling direction preference has been
more recently questioned. According to Brummer
and Kroon (1988), variation of the coiling ratio in
di¡erent species of planktonic foraminifera is re-
lated to water mass organisation and bioprovin-
cialism through reproductive isolation and sup-
pression of gene £ow across water mass bounda-
ries.
Examination of benthic foraminiferal coiling di-
PALAEO 2755 1-5-02
rection preference as a proxy for temperature es-
timation has been more limited and almost exclu-
sively carried out in shallow water settings (e.g.
Longinelli and Tongiorgi, 1960; Hallock and
Larsen, 1979; Nigam and Rao, 1989; Nigam
and Khare, 1992). A few studies have dealt with
laboratory experiments on coiling direction pref-
erence in benthic foraminifera (FÖyn, 1936, 1937;
Lee et al., 1963) while the only study that inves-
tigated the relation between coiling preference in
modern deep sea benthic foraminifera and envi-
ronmental conditions (i.e. temperature) is, prob-
ably, that of Collins (1990). Such disparities are,
at least partly, due to the di⁄culty of sampling
oceanic bottom waters compared to the simplicity
of collecting planktic samples and measuring
chemico-physical properties of surface waters.
Although the above-mentioned studies have not
de¢nitely established a clear relationship between
environmental changes and coiling direction in
benthic foraminifera, temperature seems to be
the only environmental factor in£uencing the coil-
ing ratio of this group (see review in Boltovskoy
et al., 1991). However, the coiling direction pref-
erence in benthic foraminifera is also in£uenced
by mode of reproduction (FÖyn, 1936, 1937;
Myers, 1940; Lee et al., 1963; Nigam and Rao,
1989; Nigam and Khare, 1992). This parameter
has, therefore, two potential applications: data
from species in which coiling preference is envi-
ronmentally controlled can be used as a proxy for
sea £oor palaeotemperature estimates while herit-
able coiling patterns may be useful in establishing
phylogenetic relationships among species.
In this study we explore the possibility that the
coiling ratio (number of sinistral versus dextral
individuals) in the benthic foraminifer Cibici-
doides pseudoacutus can be the response to a rapid
change of bottom water temperature following
the K^T boundary event. Cibicidoides pseudoacu-
tus was chosen for its continuous distribution and
relatively high abundance across the K^T bound-
ary. Other trochospiral taxa, although continu-
ously present across the K^T boundary, do not
occur in su⁄cient numbers to allow a thorough
evaluation of the coiling ratio record.
Sample preparation included gentle crushing,
soaking overnight in a peroxide solution, washing
 S. Galeotti, R. Coccioni / Palaeogeography, Palaeoclimatology, Palaeoecology 178 (2002) 197^210 203

Table 1
Cibicidoides pseudoacutus coiling ratio values for the studied sections and average values for speci¢c intervals

through a 63-Wm ¢ne mesh and drying at 80‡C.
All Cibicidoides pseudoacutus individuals were
picked out, glued onto micropalaeontological
slides, and counted. As reproductive mode
strongly in£uences coiling direction, only small-
sized forms (megalospheric, asexually produced)
were used in this study to avoid a genetic in£u-
ence in the calculation of the coiling ratio.
Data for the studied sections are reported in
Table 1 together with average values for speci¢c
intervals.
4. Results
The Cibicidoides pseudoacutus coiling ratio rec-
ord from the studied sections is shown in Fig. 4
next to lithostratigraphy and planktonic foramini-
feral zonation.
Mean values in the uppermost Maastrichtian
are quite similar in all sections ranging from
0.81 at El Melah to 1.05 at Elles. Rather stable
values are observed in the uppermost Maastricht-
ian of El Kef. In the uppermost Maastrichtian of
Elles, Ain Settara, and El Melah sections, the Ci-
bicidoides pseudoacutus coiling ratio record shows
larger £uctuations but it is never lower than 0.41
and never exceeds 1.56.
At Elles and El Kef, a sharp spike in the pro-
portion of sinistral specimens occurs at the K^T
boundary. At El Kef, the coiling ratio in the ¢rst
6.5 cm of Zone P0 averages 1.75 with the highest

PALAEO 2755 1-5-02

204 S. Galeotti, R. Coccioni / Palaeogeography, Palaeoclimatology, Palaeoecology 178 (2002) 197^210

PALAEO 2755 1-5-02

 S. Galeotti, R. Coccioni / Palaeogeography, Palaeoclimatology, Palaeoecology 178 (2002) 197^210 205

Fig. 5. Stable isotope and benthic foraminiferal record across K^T boundary (KTB) of El Kef. Planktonic foraminiferal zonation
after Smit in Brinkhuis et al. (1994) and Smit in Brinkhuis et al. (1998). Oxygen isotope records from Keller and Lindinger
(1989). The N18 O (¡) curve represents the ¢ne fraction ( 6 25 Wm) record while the N18 O (bf) curve represents benthic foraminifer-
al (Cibicidoides pseudoacutus) values. Faunal density expresses number of benthic foraminifera per g of dry sediment in the frac-
tion greater than 125 Wm.

value (2.67) recorded just above the K^T bound- 5. Discussion

ary. A similar pattern is observed at Elles where
the highest value (2.45) is recorded in the basal
2 cm of the boundary clay layer and high average
values (1.5) are recorded in the lower third of
Zone P0. A second, minor spike in the Cibici-
doides pseudoacutus coiling ratio is recorded in
both the Elles and El Kef sections at 10 cm and
6.5 cm above the K^T boundary, respectively.
Upsection, the C. pseudoacutus coiling ratio aver-
age values decrease to 0.89 at El Kef and to 1.04
at Elles and therefore revert to uppermost Maas-
trichtian mean values. The spike in the proportion
of sinistral individuals which has been observed at
Elles and El Kef is absent in the Ain Settara sec-
tion where average values are 0.92 in the Maas-
trichtian and 1.13 in the Danian. In the ¢rst 1 cm
of the boundary clay layer, that is within Zone
P0, the C. pseudoacutus coiling ratio is 0.96.
A comparison with previously published data
on benthic foraminifera from El Kef (Coccioni
and Galeotti, 1998; Galeotti, 1998) indicates
that the shift of the Cibicidoides pseudoacutus coil-
ing ratio is associated with dramatic £uctuations
of benthic foraminiferal faunal parameters includ-
ing changes in the faunal density (i.e. the number
of specimens per g of dry sediment), and propor-
tion of epifaunal species (Fig. 5) as well as species
diversity and relative abundance of oxygen indi-
ces. Semi-quantitative data from Elles indicate a
comparable pattern of faunal changes in benthic
foraminiferal assemblages across the K^T bound-
ary. An increased relative abundance of C. pseu-
doacutus above the K^T boundary was observed
in all the studied sections. In the El Kef K^T
boundary transition C. pseudoacutus forms up to
60% of the whole lowermost Danian benthic for-
aminiferal assemblage with highest relative abun-
dance recorded some 15 cm above the K^T
boundary, therefore above the observed shift in
its coiling ratio (Fig. 5).
5.1. Biostratigraphic implications and completeness
of K^T boundary Tunisian transitions
Changes observed in benthic foraminiferal as-
semblages across the K^T boundary in Tunisian
sections are comparable to the observations made
in neritic to upper bathyal settings such as Brazos
River (Keller, 1992), Millers Ferry (Olsson et al.,
1996), Nye KlÖv and Stevns Klint (Schmitz et al.,
1992; Coccioni and Galeotti, 1998), and Sinai Ne-
gev (Keller, 1992). In these areas, the following
characteristic succession of benthic foraminiferal
assemblages is observed within the K^T boundary
interval: (1) late Maastrichtian foraminiferal as-
semblages are well diversi¢ed and characterised
by complex trophic structures ; (2) foraminiferal
assemblages within and directly above the bound-
ary clay layer or Fish Clay are dominated by epi-
faunal species (Cibicidoides, Anomalinoides, and
Gavelinella); (3) a slow recovery which is achieved
only 200^300 ka after the K^T boundary event
occurs in the lowermost Danian. On this basis,
Coccioni and Galeotti (1998) distinguished a low-
ermost Danian shallow water ‘epifaunal domain’
which might be of some use for stratigraphic cor-
relations across the K^T boundary transition.
However, this succession of events is only useful
for low-resolution correlations. Besides their fa-
cies dependence this is the reason why benthic
foraminifera are seen as a group of little use for
stratigraphic correlations across the K^T bound-
ary, especially if compared to other extinction
events (i.e. the Palaeocene^Eocene boundary)
The shift in the coiling ratio of Cibicidoides
pseudoacutus is a potential high-resolution corre-
lation tool probably representing an ecological
event spanning the lower part of Zone P0 which
might be traceable over shallow water settings
from the Tethys. According to the time scale of

PALAEO 2755 1-5-02

206 S. Galeotti, R. Coccioni / Palaeogeography, Palaeoclimatology, Palaeoecology 178 (2002) 197^210
Berggren et al. (1995) and assuming a constant
sedimentation rate of the boundary clay layer,
the shift in C. pseudoacutus coiling ratio would,
in fact, have lasted for some 7 ka after the K^T
boundary event.
It is noteworthy that the major spike recorded
just above the K^T boundary is followed by a
second minor spike occurring at one third of
Zone P0 in both Elles and El Kef sections (see
Fig. 4). Assuming that this second spike repre-
sents the same event in these sections, a further
resolution of this event is possible. In particular,
the interval where the double spike occurs is
slightly thicker at Elles than observed in the stra-
totype section, suggesting that the basal part of
the boundary clay layer is more expanded in the
former section. Accordingly, the thickness of
Zone P0 is slightly higher at Elles (28 cm) than
observed El Kef (23 cm). The lack of a shift in
Cibicidoides pseudoacutus coiling ratio in the Ain
Settara section suggests that a stratigraphic gap
straddling at least the lower third of Zone P0
occurs in this section. Accordingly, Luciani
(2002) reports Zone P0 to be restricted to the
basal 2 cm of the boundary clay layer at Ain
Settara.
5.2. Palaeoecological implications
The development of sinistrally coiled dominat-
ed Cibicidoides pseudoacutus populations at the
K^T boundary is associated with dramatic £uctu-
ations of other benthic foraminiferal faunal pa-
rameters. In agreement with Keller (1988a) and
Speijer and van der Zwaan (1994, 1996), quanti-
tative data from El Kef (Fig. 5) can be interpreted
in terms of decreased oxygenation and organic
£uxes to the sea £oor in correspondence to the
K^T boundary. At El Kef the response of benthic
foraminiferal assemblages to the K^T boundary
event mainly occurred in terms of development
of an epifaunal-dominated assemblage associated
with a drop in the number of species (species rich-
ness) and number of specimens per sample (faunal
density). The semi-quantitative observation car-
ried out in the Elles section suggests that sudden
and marked changes comparable to those ob-
served at El Kef also occurred across the K^T
PALAEO 2755 1-5-02
boundary at this site. In particular, a drastic de-
crease of species richness and faunal density oc-
curs in response to the K^T boundary event. At
Elles and El Kef, such conditions persisted at least
up to the top of the studied intervals. On the
other hand, according to Keller (1988a) and
Speijer and van der Zwaan (1994, 1996), the com-
plete recovery of benthic foraminiferal commun-
ities is observed at El Kef only 10 m above the K^
T boundary, that is 200^300 ka after the K^T
boundary event.
However, the shift in the Cibicidoides pseudo-
acutus coiling ratio observed at El Kef and Elles
straddles the ¢rst 6.5 cm and 10 cm of Zone P0,
respectively (Fig. 4). This event therefore termi-
nated well before the end of the series of sea £oor
perturbations indicated by the benthic foramini-
feral faunal parameter record. This disparity sug-
gests that the development of sinistrally coiled
populations of C. pseudoacutus was not a direct
response to decreased organic £uxes and/or devel-
opment of dysaerobic conditions on the sea £oor.
In addition, the C. pseudoacutus coiling ratio rec-
ord does not match the record of the relative
abundance of the species on which it is calculated.
In the El Kef section, the highest relative abun-
dance of this species is, in fact, recorded 15 cm
above the K^T boundary where the coiling ratio
has already reverted to pre- K^T boundary values
(Fig. 5). It is, therefore, reasonable to assume that
the development of sinistrally coiled dominant
populations of C. pseudoacutus following the K^
T boundary was independent of changing redox
and trophic conditions, and expansion of ecolog-
ical niches particularly favourable for this species.
In Recent and fossil assemblages as well as in
laboratory cultures, coiling direction in benthic
foraminifera has been shown to be in£uenced by
reproductivity mode (FÖyn, 1936, 1937; Lee et al.,
1963; Myers, 1940; Nigam and Rao, 1989), bio-
provincialism (Hallock and Larsen, 1979) or en-
vironmental factors (Longinelli and Tongiorgi,
1960; Hallock and Larsen, 1979).
Collins (1990) claimed for the ¢rst time demon-
stration of an unambiguous correlation between
temperature and coiling direction in benthic fora-
miniferal populations. She reported that popula-
tions of predominantly dextrally coiled Bulimina
 S. Galeotti, R. Coccioni / Palaeogeography, Palaeoclimatology, Palaeoecology 178 (2002) 197^210
marginata and Bulimina aculeata in two distinct
areas (Gulf of Maine to New Jersey and Gulf of
Mexico) are strongly associated with warm tem-
peratures. However, the opposite is not true: pre-
dominantly sinistrally coiled populations are not
associated with cold temperatures.
Boltovskoy et al. (1991) reviewed the morpho-
logical variations of benthic foraminiferal tests in
response to changes in ecological parameters.
They concluded that notwithstanding some con-
tradictory evidence, changes in temperature ap-
parently result mostly in test size variation with
population of larger individuals associated with
lower temperature. However, they continue, it is
quite probable, although the evidence is still ten-
uous and more study is required, that changes in
temperature can a¡ect sinistral/dextral ratio in
some species. The coiling ratio of some benthic
foraminiferal species is therefore a potential proxy
for palaeotemperature estimates of bottom
waters.
The observed shift in the Cibicidoides pseudo-
acutus coiling ratio can be interpreted in terms
of either changing coiling preference within an
original population having a V1:1 coiling ratio
or (similarly to that suggested for Recent planktic
foraminifera) immigration of a sinistral coil-dom-
inated population from a di¡erent bioprovince.
Evidence of genotypic isolation has been, in
fact, observed in modern species of benthic fora-
minifera based on nuclear-coded ribosomal DNA
sequences (Tsuchiya et al., 1998). On the other
hand, as testi¢ed by benthic foraminiferal assem-
blages, sea £oor environmental changes following
the K^T boundary at El Kef were su⁄ciently dra-
matic and sudden to have hampered the adapta-
tion of an original population of C. pseudoacutus
to stressed environmental conditions. Such a
mechanism might have allowed the immigration
of a sinistral coil-dominated C. pseudoacutus pop-
ulation from a di¡erent bioprovince (possibly
from a di¡erent palaeobathymetric setting). In
agreement with Keller (1988a) such a hypothesis
would imply large sea level £uctuations in corre-
spondence to the K^T boundary at El Kef. How-
ever, the presence in the lower upper bathyal El
Melah section of C. pseudoacutus populations
with a coiling ratio similar (if not lower) to that
PALAEO 2755 1-5-02
207
observed in the shallower depositional setting of
El Kef and Elles rules out a mechanism of immi-
gration from a deeper bioprovince. The possibility
of a downward bathymetric migration also seems
unlikely. In fact, in the outer neritic Elles section,
C. pseudoacutus populations have mean Maas-
trichtian values in coiling ratios similar to that
observed in the upper bathyal setting of El Kef.
In line with observations made on Recent
benthic foraminiferal species, the observed shift
in the coiling ratio of Cibicidoides pseudoacutus
can be better interpreted as a response to a drastic
change of bottom water temperature. A general
correlation between benthic N18 O and C. pseudo-
acutus coiling ratio records cannot be traced in
the surveyed interval at Elles and El Kef also
because di¡erent sample sets have been used.
However, the development of the sinistrally coiled
population in C. pseudoacutus is associated with
sharp shifts to heavier N18 O values in both the
Elles and the El Kef sections and can be regarded
as a response to a cooling of bottom waters. In
particular, the benthic foraminiferal (C. pseudo-
acutus) N18 O record at El Kef shows a 0.5x pos-
itive excursion in the lowermost Danian, implying
a sharp bottom water cooling at the K^T bound-
ary (Keller and Lindinger, 1989; Fig. 5). More-
over, Stueben et al. (1998) have recently reported
a 1.5x increase of N18 O benthic values suggest-
ing that bottom waters signi¢cantly cooled during
the deposition of the basal 5 cm of the boundary
clay layer at Elles. Though not discussed in the
text, these authors also show an abrupt shift to
heavier values in planktic N18 O ratios at the K^T
boundary in their ¢g. 1. By contrast, ¢ne fraction
( 6 25 Wm) oxygen isotope values from El Kef
would suggest that a sea surface warming oc-
curred in the lowermost Danian (Keller and Lin-
dinger, 1989; Fig. 5). However, as pointed out by
the latter authors, diagenetic and preservational
e¡ects are variable across the K^T boundary at
El Kef with preservation generally improved in
the low-CaCO3 sediments of the boundary clay
layer. The negative shift recorded in the ¢ne frac-
tion N18 O ratio record at the K^T boundary of El
Kef might, therefore, be due to comparison with
underlying and overlying over-estimated, diage-
netically altered values. Quantitative changes in
208 S. Galeotti, R. Coccioni / Palaeogeography, Palaeoclimatology, Palaeoecology 178 (2002) 197^210
dino£agellate cyst assemblages indicate that cool-
er surface water conditions occurred in the ¢rst 10
cm of Zone P0 at El Kef (Brinkhuis et al., 1998).
These changes in the dino£agellate cyst assem-
blages correspond to the same stratigraphic inter-
val that contains the shift in the C. pseudoacutus
coiling ratio, indicating that a concomitant cool-
ing of surface and bottom waters occurred in the
earliest Danian at El Kef.
Such a short-term climatic deterioration would
generally agree with model simulation of the pri-
mary and secondary e¡ects of an extraterrestrial
impact event which postulate that a short-term
‘impact winter’ accompanied the K^T boundary
event (e.g. Pope et al., 1994; Ivanov et al., 1996).
However, a problem arises when considering the
duration of such a ‘cooling event’, the approxima-
tion of which represents a crucial point for dis-
criminating between the various scenarios of the
climate e¡ects which followed the K^T boundary
event. Impact model-derived estimates currently
available postulate that the ‘impact winter’ lasted
from several months to a decade (Pope et al.,
1994) whereas the cooling phase as indicated by
the shift in the coiling direction of Cibicidoides
pseudoacutus, invasion of boreal dino£agellate
cyst, and isotope record would have lasted some
7 ka. Following Brinkhuis et al. (1998), as an
alternative to this scenario, we must consider
that the sedimentation rate of the boundary clay
layer might have been, at least in its lower part,
extremely high, rather than the canonical view of
being extremely condensed.
6. Conclusions
The study of coiling ratios in megalospheric
individuals of the benthic foraminifer Cibicidoides
pseudoacutus across the K^T boundary from four
Tunisian sections reveals that this species devel-
oped sinistral coil-dominated populations in the
lowermost Danian at El Kef and Elles.
Such a shift in coiling direction preference co-
occurs with the invasion of cold water (boreal)
dino£agellate species and a positive shift in
benthic foraminiferal N18 O values. It is, therefore,
interpreted as a response to a short-term cooling
PALAEO 2755 1-5-02
of bottom waters which lasted for some 7 ka after
the K^T boundary event.
Besides its palaeoecological, possibly palaeocli-
matic signi¢cance, the development of sinistrally
coiled populations in Cibicidoides pseudoacutus is
a potential tool to assess the completeness of
stratigraphic sequences in Tethyan shallow water
settings just above the K^T boundary.
Acknowledgements
Alessandro Montanari and Gerta Keller are
kindly thanked for reading earlier drafts of the
manuscript. Gerta Keller is also thanked for
providing samples from the El Melah section.
We thank M.B. Hart and an anonymous reviewer
for their helpful suggestions which greatly im-
proved the manuscript. This paper benefited from
MURST 60% funding to R.C.
Appendix. Taxonomic notes
Cibicidoides pseudoacutus (Nakkady)
1950 Anomalina pseudoacuta Nakkady, p. 691, pl. 90, ¢gs.
29^32.
1988 Anomalinoides acuta (Plummer), Keller, pl. 2, ¢gs. 9,
10, 12, 13.
1994 Cibicidoides pseudoacutus (Nakkady), Speijer and Van
der Zwaan, pl. 7, Fig. 6a^c.
Test trochospirally coiled, planoconvex to bi-
convex, distinctly perforate, periphery subacute.
Some specimens show a distinct keel. The umbil-
ical side which is partially involute possesses a
pronounced knob surrounded by growths extend-
ing up to the periphery. In its original description,
Nakkady (1950) reported Cibicidoides pseudo-
acutus to be very similar to Anomalina acuta
(Plummer). However, C. pseudoacutus di¡ers
from the latter species in possessing a peripheral
aperture which does not extend towards the um-
bilicus. For its biconvex aspect and partially in-
volute spiral side C. pseudoacutus shows a re-
markable a⁄nity to the genus Anomalinoides.
However, due to the position and form of the
aperture, we assign this species to the genus Cibi-
 S. Galeotti, R. Coccioni / Palaeogeography, Palaeoclimatology, Palaeoecology 178 (2002) 197^210
cidoides in agreement with Speijer and Van der
Zwaan (1994).
References
Adatte, T., Keller, G., Liangquan, L., Stinnesbeck, W., Zagh-
nin-Turky, D., 1998. Climate and sea-level £uctuations
across the KT boundary in Tunisia: Warm and humid con-
ditions linked to deccan volcanism? International Workshop
on Cretaceous-Tertiary Transition, Volume of Abstracts, 7^
10.
Berggren, W.A., Kent, D.V., Swisher, C.C., III, Aubry, M-.P.,
1995. A revised Cenozoic geochronology and chronostratig-
raphy. SEPM Spec. Publ. 54, 129^213.
Boltovskoy, E., Scott, D.B., Medioli, F.S., 1991. Morpholog-
ical variations of benthic foraminiferal tests in response to
changes in ecological parameters: a review. J. Paleontol. 65,
175^185.
Brinkhuis, H., Zachariasse, W.J., 1988. Dino£agellate cysts,
sea level changes and planktonic foraminifers across the
Cretaceous-Tertiary boundary at El Haria, Northwest Tuni-
sia. Mar. Micropaleontol. 13, 153^191.
Brinkhuis, H., Romein, A.J.T., Smit, J., Zachariasse, W.J.,
1994. Danian-Selandian dino£agellate cysts from lower lat-
itudes with special reference to the El Kef section, NW Tu-
nisia. GFF 116, 46^48.
Brinkhuis, H., Bujak, J.P., Smit, J., Versteegh, G.J.M., Vissch-
er, H., 1998. Dino£agellate-based sea surface temperature
reconstructions across the Cretaceous-Tertiary boundary.
Palaeogeogr. Palaeoclimatol. Palaeoecol. 141, 67^83.
Brummer, G.J.A., Kroon, D., 1988. Genetically controlled
planktonic foraminiferal coiling ratios as tracers of past
ocean dynamics. In: Brummer, G.J.A., Kroon, D. (Eds.),
Planktonic Foraminifera as Tracers of Ocean-Climate His-
tory: Ontology, Relationships and Preservation of Modern
Species and Stable Isotopes, Phenotypes and Assemblage
Distribution in Di¡erent Water Masses. Free University
Press, Amsterdam, pp. 293^297.
Burollet, P.F., 1967. Tertiary Geology of Tunisia. In: Guide-
book to the Geology and History of Tunisia. Petroleum
Exploration Society, Libya, 9th Annu. Field Conf., pp.
215^225.
Coccioni, R., Galeotti, S., 1998. What happened to small
benthic foraminifera at the K/T Boundary? Bull. Soc.
Ge¤ol. France 169, 271^279.
Collins, L.S., 1990. The correspondence between water temper-
ature and coiling direction in Bulimina. Paleoceanography 5,
289^294.
Cowie, J.W., Ziegler, W., Remane, J., 1989. Stratigraphic com-
mission accelerates progress 1984^1989. Episodes 112, 79^
83.
Dupuis, C., Steurbaut, E., Matmati, M.F., 1998. The Ain Set-
tara K/T boundary section. Main results and comparison
with the El Kef stratotype. International Workshop on Cre-
taceous-Tertiary Transition, Volume of Abstracts, 67^68.
PALAEO 2755 1-5-02
209
FÖyn, B., 1936. Foraminiferenstudien I. Der Lebenszyklus von
Discorbina vilardeboana d’Orbigny. Bergens Mus. Arb. Na-
turvidensk. Rekke 2, 1^22.
FÖyn, B., 1937. Foraminiferenstudien II. Zur Kenntinis der
asexuellen Fortp£anzung und Entwicklung der Gamonten
von Discorbina vilardeboana d’Orbigny. Bergens Mus. Arb.
Naturvidensk. Rekke 2, 1^22.
Galeotti, S., 1998. Crisi Biologiche e Foraminiferi Bentonici
Attraverso i Limiti Cretaceo/Terziario, Paleocene/Eocene e
Eocene/Oligocene, Ph.D. Thesis, University of Parma, 205
pp.
Hallock, P., Larsen, A.R., 1979. Coiling direction in Amphis-
tegina. Mar. Micropaleontol. 4, 33^44.
Hemleben, C., Spindler, M., Anderson, O.R., 1989. Modern
Planktonic Foraminifera. Springer-Verlag, New York, 363
pp.
Ivanov, B.A., Badukov, D.D., Yakovlev, O.I., Gerasimov,
M.V., Dikov, Y.P., Pope, K.O., Ocampo, A.C., 1996. De-
gassing of sedimentary rocks due to Chicxulub impact: Hy-
drocode and Physical simulations. In: Ryder, G., Fastkov-
sky, D., Gartner, S. (Eds.), The Cretaceous-Tertiary event
and other catastrophes in Earth history. Geological Society
of America Special Paper 307, pp. 125^140.
Keller, G., 1988a. Extinction survivorship and evolution of
planktic foraminifera across the Cretaceous-Tertiary bound-
ary at El Kef, Tunisia. Mar. Micropaleontol. 13, 239^263.
Keller, G., 1988b. Biotic turnover in benthic foraminifera
across the Cretaceous-Tertiary boundary at El Kef, Tunisia.
Palaeogeogr. Palaeoclimatol. Palaeoecol. 66, 153^171.
Keller, G., 1992. Paleoecological response of Tethyan benthic
foraminifera to the Cretaceous-Tertiary boundary transition.
In: Takayanagi, Y., Saito, T. (Eds.), Studies in Benthic For-
aminifera. Tokai University Press, Tokyo, pp. 77^91.
Keller, G., Lindinger, M., 1989. Stable isotope, TOC and
CaCO3 record across the Cretaceous/Tertiary boundary at
El Kef, Tunisia. Palaeogeogr. Palaeoclimatol. Palaeoecol.
73, 243^265.
Keller, G., Li, L., MacLeod, N., 1995. The Cretaceous/Terti-
ary boundary stratotype section of El Kef, Tunisia: how
catastrophic was the mass extinction? Palaeogeogr. Palaeo-
climatol. Palaeoecol. 119, 221^254.
Keller, G., Adatte, T., Stinnesbeck, W., Luciani, V., Karoui,
N., Zaghbib-Turki, D., 2002. Paleoecology of the Creta-
ceous-Tertiary mass extinction in planktic foraminifera. Pa-
laeogeogr. Palaeoclimatol. Palaeoecol. 178, 257^297.
Kennett, J.P., 1976. Phenotypic variation in some recent and
Late Cenozoic planktonic foraminifera. In: Hedley, R.H.,
Adams, C.G. (Eds.), Foraminifera, Volume 2. Academic
Press, San Diego, CA, pp. 111^170.
Kouwenhoven, T.J., Speijer, R.P., Vanoosterhout, C.W.M.,
Van der Zwaan, G.J., 1997. Benthic foraminiferal assem-
blages between two major extinction events ^ the Paleocene
El Kef section, Tunisia. Mar. Micropaleontol. 29, 105^
127.
Kuhnt, W., Kaminski, M.A., 1996. The response of benthic
foraminifera to the K/T boundary event ^ A review. Ge¤ol.
Afr. Atl. Sud Actes Colloq. Angers 1994, 433^442.
210 S. Galeotti, R. Coccioni / Palaeogeography, Palaeoclimatology, Palaeoecology 178 (2002) 197^210
Lee, J.J., Freudenthal, H.D., Muller, W.A., Koosoy, V.,
Pierce, S., Grossman, R., 1963. Growth and Physiology of
Foraminifera in the laboratory. Part 3, Initial studies of
Rosalina £oridana. Micropaleontology 9, 449^466.
Longinelli, A., Tongiorgi, E., 1960. Frequenza degli individui
destrogiri in diverse popolazioni di Rotalia beccarii Linneo.
Boll. Soc. Paleontol. Ital. 1, 5^16.
Luciani, V., 2002. High-resolution planktonic foraminiferal
analysis from the Cretaceous/Tertiary boundary at Ain-Set-
tara (Tunisia). Palaeogeogr. Palaeoclimatol. Palaeoecol. 178,
299^319.
Molina, E., Arenillas, I., Arz, J.A., 1998. Mass extinction in
planktic foraminifera at the Cretaceous/Tertiary boundary
in subtropical and temperate latitudes. Bull. Soc. Ge¤ol.
France 169, 351^363.
Myers, E.H., 1940. Observation on the origin and fate of £ag-
ellated gametes in multiple tests of Discorbis (Foraminifera).
J. Mar. Biol. Assoc. UK 24, 201^226.
Nakkady, S.E., 1950. A new foraminiferal fauna from the
Esna shales and upper Cretaceous Chalk of Egypt. J. Pale-
ontol. 24, 675^692.
Nigam, R., Rao, A.S., 1989. The intriguing relationship be-
tween coiling direction and reproductive mode in benthic
foraminifera. J. Palaeontol. Soc. India 34, 79^82.
Nigam, R., Khare, N., 1992. The reciprocity between coiling
direction and dimorphic reproduction in benthic foramini-
fera. J. Micropaleontol. 11, 221^228.
Nyong, E.E., Olsson, R.K., 1983/4. A paleoslope model for
Campanian to Lower Maestrichtian Foraminifera in the
North America Basin and adjacent continental margin.
Mar. Micropaleontol. 8, 437^477.
Olsson, R.K., Nyong, E.E., 1984. A paleoslope model for
Campanian-Lower Maastrichtian Foraminifera of New Jer-
sey and Delaware. J. Foraminifer. Res. 14, 50^68.
Olsson, R.K., Liu, C., van Fossen, M., 1996. The Cretaceous/
Tertiary catastrophic event at Millers Ferry, Alabama. In:
Ryder, G., Fastkovsky, D., Gartner, S. (Eds.), The Creta-
ceous-Tertiary Event and Other Catastrophes in Earth His-
tory. Geological Society of America Special Paper 307, pp.
263^277.
Pope, K.O., Baines, K.H., Ocampo, A.C., Ivanov, B.A., 1994.
Impact winter and the Cretaceous/Tertiary extinctions: Re-
sults of a Chicxulub asteroid impact model. Earth Planet.
Sci. Lett. 128, 719^725.
Pospichal, J.J., 1994. Calcareous nannofossil at the K-T
boundary, El Kef: No evidence for stepwise, gradual or
sequential extinctions. Geology 22, 99^102.
Robin, E., Rocchia, R., Lefevre, I., Pierrard, O., Dupuis, C.,
Smit, J., Zaghib-Turki, D., Karoui, N., Matmati, F., 1998.
The compositional Variation of K/T spinel in Tunisia: Evi-
dence for a global Deluge of Projectile debris. International
PALAEO 2755 1-5-02
Workshop on Cretaceous-Tertiary Transition, Volume of
Abstracts, 49^50.
Schmitz, B., Keller, G., Stenvall, O., 1992. Stable isotope and
foraminiferal changes across the Cretaceous-Tertiary bound-
ary at Stevns Klint, Denmark: Arguments for long-term
oceanic instability before and after bolide-impact event. Pa-
laeogeogr. Palaeoclimatol. Palaeoecol. 96, 233^260.
Sliter, W.V., 1972. Upper Cretaceous planktonic foraminiferal
zoogeography and ecology ^ eastern Paci¢c margin. Palaeo-
geogr. Palaeoclimatol. Palaeoecol. 12, 15^31.
Sliter, W.V., Baker, A., 1972. Cretaceous bathymetric distribu-
tion of benthic foraminifera. J. Foraminifer. Res. 2, 167^
183.
Smit, J., Romein, A.J.T., 1985. A sequence of events across the
Cretaceous-Tertiary boundary. Earth Planet. Sci. Lett. 74,
155^170.
Smit, J., Keller, G., Zargouni, F., Razgallah, S., Shimi, M.,
BenAbdelkader, O., Ben Haj Ali, N., Ben Salem, H., 1997.
The El Kef sections and sampling procedures. Mar. Micro-
paleontol. 29, 67^69.
Speijer, R.P., Van der Zwaan, G.J., 1994. Extinction and sur-
vivorship patterns in southern Tethyan benthic foraminiferal
assemblages across the Cretaceous/Paleogene boundary.
Geol. Ultraiect. 124, 19^64.
Speijer, R.P., Van der Zwaan, G.J., 1996. Extinction and sur-
vivorship of southern Tethyan benthic foraminifera across
the Cretaceous/Palaeogene boundary. In: Hart, M.B. (Ed.),
Biotic Recovery from Mass Extinction Events. Geological
Society Special Publication 102, pp. 343^371.
Stinnesbeck, W., Keller, G., Adatte, T., 1998. Lithological
Characteristics of the K/T transitions in Tunisia: Evidence
of a tsunami event? International Workshop on Cretaceous-
Tertiary Transition, Volume of Abstracts, 53^54.
Stueben, D., Kramar, U., Berner, Z., Keller, G., 1998. Trace
elements and stable isotopes in foraminifera of the Elles K/T
pro¢le: Indications for sea level £uctuations and primary
productivity. International Workshop on Cretaceous-Terti-
ary Transition, Volume of Abstracts, 55^56.
Tsuchiya, M., Kitazato, H., Pawlowski, J., 1998. Phylogenetic
relationships among three genera within the subfamily Glab-
ratellidae from Japan based on ribosomal DNA sequences.
FORAMS ’98, International Symposium on Foraminifera,
Monterrey, Mexico, July 5^12, Sociedad Mexicana de Pale-
ontologia, A.C., Special Publication 107.
van Morkhoven, F.P.C.M., Berggren, W.A., Edwards, S.A.,
1986. Cenozoic cosmopolitan deep-water benthic foramini-
fera. Bull. Cent. Rech. Explor. Prod. Elf-Aquitaine Me¤m.
11, 1^412.
Vincent, E., Berger, W.H., 1981. Planktonic foraminifera and
their use in paleoceanography. In: Emiliani, C. (Ed.), The
Oceanic Lithosphere. Sea 7, 1025^1119.