Marine Micropaleontology 51 (2004) 23 38

www.elsevier.com/locate/marmicro

Planktonic foraminiferal biostratigraphy and mechanisms in the

$
extinction of Morozovella in the late middle Eocene
Bridget S. Wade *
Institute of Earth Sciences, School of GeoSciences, University of Edinburgh, West Mains Road, Edinburgh EH9 3JW, UK
Received 21 May 2002; received in revised form 21 August 2003; accepted 11 September 2003

Abstract
The muricate planktonic foraminiferal genera Morozovella and Acarinina were abundant and diverse during the upper
Palaeocene to middle Eocene and dominated the tropical and subtropical assemblages. A significant biotic turnover in
planktonic foraminifera occurred in the latest middle Eocene with a notable reduction in the acarininid lineage and the
extinction of the morozovellids. These genera are extensively employed as palaeoclimatic and biostratigraphic markers and,
therefore, this turnover episode is an important event in the record of the Cenozoic planktonic foraminifera. Sediments from the
western North Atlantic (Ocean Drilling Program Site 1052) were examined in order to investigate these extinction events, in
terms of both timing and mechanisms. Biostratigraphic events of the middle and late Eocene have been examined with a
sampling resolution of approximately 3 kyr. These have been calibrated to the magneto- and astrochronology to accurately
define the timing of key biostratigraphic events, particularly the extinction of Morozovella spinulosa which is a distinct
biomarker for late middle Eocene sediments. High-resolution biostratigraphy reveals that the extinctions in the muricate group
occurred in a stepwise form. The large acarininids (Acarinina praetopilensis) terminate 10 kyr prior to the extinction of M.
spinulosa and small acarininids (Acarinina medizzai and Acarinina echinata) continue into the upper Eocene.
High-resolution stable isotope analyses have been conducted on planktonic and benthic foraminifera from the western North
Atlantic to reconstruct sea surface temperatures (SSTs) and deep water temperatures and the structure of the water column
around this major biotic turnover. Whilst the extinctions of M. spinulosa and A. praetopilensis occur during a long-term cooling
trend, the biotic turnover in the muricate group does not appear to be related to significant climatic change. Sea surface
temperatures decrease slowly prior to the extinction events, and there is no evidence for a large-temperature shift associated
with the faunal changes. The turnover event was therefore probably related to the increased surface water productivity and the
deterioration of photosymbiotic partnerships with algae.
D 2003 Elsevier B.V. All rights reserved.
Keywords: extinction; eocene; planktonic foraminifera; biostratigraphy; temperature; stable isotopes

1. Introduction
B Supplementary data associated with this article can be found
at doi:10.1016/j.marmicro.2003.09.001.
* Tel.: +44-131-650-8524; fax: +44-131-668-3184.
E-mail address: bwade@glg.ed.ac.uk (B.S. Wade).
0377-8398/$ - see front matter D 2003 Elsevier B.V. All rights reserved.
doi:10.1016/j.marmicro.2003.09.001

The muricate genera Morozovella and Acarinina

are an extinct group of planktonic foraminifera that
dominated the tropical and subtropical oceanic
sediments from the upper Paleocene to the latest

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B.S. Wade / Marine Micropaleontology 51 (2004) 2338

middle Eocene. The diversity of muricate foraminifera decreased throughout the middle Eocene
with a major faunal turnover in planktonic foraminifera during the late middle Eocene (magnetochron C17n.3n). This saw the extinction of the
Morozovella lineage and a major decline in the
Acarinina lineage. The extinction of Morozovella
and large acarininids is a major event in the
history of the Cenozoic planktonic foraminifera.
These genera are extensively utilised as palaeoclimatic studies and are important markers in Eocene
planktonic foraminifera biostratigraphy, and, therefore, their last occurrence (LO) is an important
datum to constrain.
Whilst previous research has established that
Morozovella and Acarinina were prominent surface
dwellers for approximately 20 million years within
the tropical and subtropical fauna (Pearson et al.,
1993; Norris, 1996), the reason for the extinction of
the muricate planktonic foraminiferal genus Morozovella has not been studied at a high resolution.
Previous workers (e.g., Toumarkine and Luterbacher, 1985; Mancin and Pirini, 2001) have noted
that the extinction was abrupt, although the exact
timing of events was not known. This work details
the middle Eocene extinction of morozovellids at a
high temporal resolution (3 kyr sampling) and thus
enables the rate and timing of biotic turnover to be
defined. The excellent recovery coupled with the
magneto- and cyclostratigraphic framework for
Ocean Drilling Program (ODP) Site 1052 (Norris
et al., 1998; Palike et al., 2001) is used to accurately reconstruct the timing of middle and late
Eocene biostratigraphic events and to refine the
biochronology. Of particular interest is the extinction of Morozovella spinulosa which is the biomarker for the top of the late middle Eocene
planktonic foraminiferal Zone P14.
The second objective of this paper is to address
the causal mechanisms that resulted in the near
synchronous extinctions of the morozovellids and
Acarinina praetopilensis. Stable isotopic analysis of
several species of foraminifera permits the local
water column structure and sea surface temperatures
(SSTs) to be determined and provides the opportunity to investigate whether the extinction of Morozovella was in response to Eocene climatic
deterioration.

2. Methods
2.1. Geological setting
Ocean Drilling Program Leg 171B drilled five sites
on the Blake Nose (western North Atlantic; Fig. 1).
This study focuses on samples from Site 1052
(29j57VN, 76 j37VW). This is the shallowest site in
the depth transect, at approximately 1345 m below sea
level, and comprises an expanded Eocene sequence of
siliceous nannofossil ooze (Norris et al., 1998). Palaeodepth estimated from benthic foraminiferal assemblages was 600 1000 m during the middle Eocene
(Norris et al., 1998) with a palaeolatitude of 29jN
(Ogg and Bardot, 2001).
2.2. Biostratigraphic calibration
Biostratigraphic analysis has been conducted on
middle and late Eocene samples from the astronomically dated ODP Site 1052, with the objective of
defining and dating the major planktonic foraminiferal
bioevents. Site 1052 is ideal to document this biotic
turnover due to the expanded middle Eocene sequence, relatively well-preserved planktonic foraminifera and the clear magneto- and astrochronology
(Norris et al., 1998; Palike et al., 2001). This enables
the investigation of the timing and mechanisms that
resulted in the biotic turnover of planktonic foraminifera in the latest middle Eocene. Sedimentation rates
are high (34 m/m.y.) which permits detailed (3 kyr)
biostratigraphic analysis. Samples were analysed for
planktonic foraminiferal biostratigraphic purposes every 10 cm, between 17 and 133 m composite depth
(mcd; Chrons C16n to C18n). Additional biostratigraphic analysis was performed on late Eocene samples from Site 1053 (29j59VN, 76j31VW).
2.3. Stable isotope investigation
Stable isotope analyses were conducted on late
middle Eocene foraminifera from Site 1052 in order
to investigate the origin of the extinction in response
to palaeoceanographic history and climatic change.
Six species of planktonic foraminifera and one species of benthic foraminifera (>250 Am size fraction)
were selected from below, within and above the
extinction interval. These were the inferred mixed

B.S. Wade / Marine Micropaleontology 51 (2004) 2338

25

Fig. 1. Location map showing drill locations and bathymetry (m) of Ocean Drilling Program Leg 171B, Sites 1049 1053 and the Blake Plateau
(inset; Kroon et al., 1998).

layer dwellers Morozovella crassata, M. spinulosa,

Acarinina praetopilensis, Globigerinatheka mexicana; the thermocline dwellers Turborotalia cocoaensis and Subbotina utilisindex; and the benthic
foraminifer Nuttalides truempyi.
Sample weights were typically 0.17 F 0.03 mg.
Prior to analysis, specimens were sonicated in methanol to remove attached calcite particles. Ultrasonic
cleaning was repeated when visual examination
proved this to be necessary. Samples were analysed
isotopically using a VG Isogas Prism III mass spec-

trometer at the University of Edinburgh, Scotland.

Normal corrections were applied, and the results of
stable isotope measurements are expressed in x
relative to the Pee Dee Belemnite (PDB) standard
reference carbonate (Craig, 1957). Silver Mine (SM)
and MAB2B calcite powdered standard as well as an
in-house standard were measured concurrently
(mean = 0.20 mg) to record analytical precision and
instrument calibration. Replicate analyses of standards yielded standard deviations of < 0.09x for
d18O and < 0.05xfor d13C.

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B.S. Wade / Marine Micropaleontology 51 (2004) 2338

3. Results
All of the samples analysed contained abundant planktonic foraminifera. The fauna at Site
1052 is distinctive of subtropical environments of
the middle and late Eocene. The samples are

typically characterised by M. spinulosa, M. crassata, A. praetopilensis, S. utilisindex, G. mexicana, G. index, Turborotalia cerroazulenis and
Catapsydrax unicavus, indicating planktonic foraminiferal Zones P14 and P15 (middle and upper
Eocene).

Fig. 2. New and revised planktonic foraminifera biostratigraphic data for the middle and late Eocene (Ocean Drilling Program Site 1052) against
the magnetochronology of Cande and Kent (1995). : last occurrence; : first occurrence; : events in previous published chronologies that are
found to extend into the late Eocene at Site 1052.

B.S. Wade / Marine Micropaleontology 51 (2004) 2338

27

or 37.81 Ma for the CK95 and PSR01 time-scales,

respectively. With the extinction of A. praetopilensis,
the acarininid group exhibits a significant decrease in
test size. The extinction of A. praetopilensis does not
represent the LO of the genus. The small acarininid
species Acarinina medizzai (Plate 2a 2d and 2n 2q)
and Acarinina echinata (Plate 2e 2m) continue in the
< 250 Am size fraction until the top of Site 1052
(magnetochron C16n). The small A. medizzai are low
in abundance and not consistently present in the
samples. Acarininids were not seen in the >250 Am
size fraction beyond 37.81 Ma (PSR01 time-scale).
The LO of the large A. praetopilensis at 92.77 mcd
therefore represents a crucial change in the biota.
The first occurrence (FO) of Globigerinatheka
semiinvoluta was determined at 91.67 mcd (1052B,
11H-4, 3 6 cm) within Chron C17n.3n. This depth
corresponds to an age of 38.00 Ma for CK95 (Fig. 2)
or 37.78 Ma for PSR01 (Table 1). Planorotalites
capdevilensis (Plate 1a and 1b) was not present in
sediments above 38.32 mcd (1052B, 5H-2, 33 36
cm). This datum calibrates to 36.24 on the CK95
time-scale and 36.35 Ma on the PSR01 chronology.
Orbulinoides beckmanni is the marker for planktonic
foraminiferal Zone P13. The Shipboard Scientific
Party (Norris et al., 1998) documented the LO of this
species at 135.69 mcd (1052A, 15H-CC, 14 16 cm).
This results in an age of 39.98 and 39.72 on the timescales of CK95 and PSR01, respectively.
Several foraminiferal biostratigraphic data published in previous chronologies, such as Berggren et
al. (1995), have not been revised. These are the last
occurrences of Acarinina collactea, Acarinina primitiva and Subbotina frontosa. This was because A.
collactea and A. primitiva were rare within the samples

3.1. New and revised biostratigraphic events and

calibration to the orbital time-scale
The orbital chronology of Palike et al. (2001) and
the high-resolution biostratigraphic analysis applied
here allowed a number of new and existing data to be
constrained to within 3 kyr (based on average sedimentation rates). For clarity and to enable comparison
with oceanic records elsewhere, the middle and late
Eocene planktonic foraminiferal biostratigraphic
events have been calibrated to both the magnetochronology of Cande and Kent (1995) and the astrochronology of Palike et al. (2001) (referred to as CK95 and
PSR01 from herein). The existing and revised biostratigraphic data and ranges of key planktonic foraminiferal species are shown in Fig. 2 and listed in
Table 1. Planktonic foraminiferal species of biostratigraphic significance are shown in Plate 1. Plate 2
shows the range of variation in the middle and late
Eocene acarininids from the < 250 Am size fraction.
Both M. crassata (Plate 1j 1l) and M. spinulosa
(Plate 1m 1o) terminate at the same horizon and were
not found in sediments above 92.37 mcd (1052B, 11H4, 73 76 cm). This is within Chron C17n.3n and is
calibrated at 38.02 Ma on the magnetochronology of
CK95 or 37.80 Ma for PSR01 (Table 1). Morozovella
are abundant within the fauna from Site 1052 to 38.30
Ma. Qualitative observations indicated a decline in the
abundance of morozovellids in sediments younger than
38.30 Ma, 500 kyr prior to the extinction. No change
was seen in the size of morozovellids at Blake Nose.
The extinctions of A. praetopilensis (Plate 1g 1i)
and the morozovellids are not synchronous. The LO of
A. praetopilensis occurred 10 kyr (40 cm) prior to the
morozovellid event and corresponds to an age of 38.03

Table 1
New and revised planktonic foraminifera biostratigraphic data
Datum

Hole

Core

Interval
(cm)

Depth
(mbsf)

Depth
(mcd)

Age (Ma)
Berggren et al. (1995)

Revised age
(Ma) to CK95

Revised age (Ma) to

Palike et al. (2001)

S. linaperta (T)
M. spinulosa (T)
M. crassata (T)
A. praetopilensis (T)
G. semiinvoluta (B)
P. capdevilensis (T)
O. beckmanni (T)

1053A
1052B
1052B
1052B
1052B
1052B
1052A

3H-4
11H-4
11H-4
11H-4
11H-4
5H-2
15H-CC

105 108
73 76
73 76
113 116
36
33 36
14 16

24.55
86.75
86.75
87.15
86.05
35.35
129.67

24.60
92.37
92.37
92.77
91.67
38.32
135.69

37.7
38.1

38.4
38.5
40.1

< 34.59
38.02
38.02
38.03
38.00
36.24
39.98

37.80
37.80
37.81
37.78
36.35
39.72

Mbsf: metres below sea floor; mcd: metres composite depth; : Nocchi et al. (1986); : no previous age assignment; <: younger than; T: top; B: base.

ki d

28

fil
i

B.S. Wade / Marine Micropaleontology 51 (2004) 2338

Plate 1. Late and middle Eocene planktonic foraminifera of biostratigraphic significance. All scale bars represent 100 Am, except in (a) and (b)
where scale bars are 50 Am. (a) P. capdevilensis umbilical view, sample 171B-1052F-10H-4, 73 76 cm. (b) P. capdevilensis spiral view, sample
171B-1052F-10H-4, 73 76 cm. (c) G. semiinvoluta (?), specimen does not show strong thickening around the apertures, sample 171B-1052B-11H
4, 143 146 cm. (d) S. linaperta umbilical view, sample 171B-1052C-2H-2, 93 98 cm. (e) S. linaperta spiral view, sample 171B-1052B-5H-2,
33 36 cm. (f) S. linaperta edge view, sample 171B-1052B-10H-1, 83 86 cm. (g) A. praetopilensis umbilical view, sample 171B-1052B-14H-4,
23 26 cm. (h) A. praetopilensis spiral view, sample 171B-1052B-14H-4, 23 26 cm. (i) A. praetopilensis edge view, sample 171B-1052B-11H-5,
43 46 cm. (j) M. crassata umbilical view, sample 171B-1052F-13H-4, 53 56 cm. (k) M. crassata edge view, sample 171B-1052F-13H-4, 53 56
cm. (l) M. crassata spiral view, sample 171B-1052F-13H-4, 53 56 cm. (m) M. spinulosa umbilical view, sample 171B-1052F-13H-5, 93 96 cm.
(n) M. spinulosa edge view, sample 171B-1052F-13H-5, 93 96 cm. (o) M. spinulosa spiral view, sample 171B-1052F-13H-5, 93 96 cm.

B.S. Wade / Marine Micropaleontology 51 (2004) 2338

29

Plate 2. Middle and late Eocene specimens of Acarinina. All scale bars represents 40 Am. (a) A. medizzai umbilical view, sample 171B1052F-10H-4, 73 76 cm. (b) A. medizzai umbilical view, sample 171B-1052F-10H-4, 73 76 cm. (c) A. medizzai umbilical view, sample
171B-1052B-12H-4, 113 116 cm. (d) A. medizzai edge view, sample 171B-1052B-12H-4, 113 116 cm. (e) A. echinata umbilical view,
sample 171B-1052F-13H-4, 53 56 cm. (f) A. echinata spiral view, sample 171B-1052F-13H-4, 53 56 cm. (g) A. echinata edge view,
sample 171B-1052F-13H-4, 53 56 cm. (h) A. echinata umbilical view, sample 171B-1052B-5H-2, 33 36 cm. (i) A. echinata edge view,
sample 171B-1052B-5H-2, 33 36 cm. (j) A. echinata spiral view, sample 171B-1052B-5H-2, 33 36 cm. (k) A. echinata umbilical view,
sample 171B-1052B-5H-2, 33 36 cm. (l) A. echinata edge view, sample 171B-1052B-5H-2, 33 36 cm. (m) A. echinata spiral view, sample
171B-1052B-5H-2, 33 36 cm. (n) A. medizzai umbilical view, sample 171B-1052F-13H-4, 53 56 cm. (o) A. medizzai edge view, sample
171B-1052F-13H-4, 53 56. (p) A. medizzai spiral view, sample 171B-1052F-13H-4, 53 56 cm. (q) A. medizzai spiral view, sample 171B1052F-10H-4, 73 76.

studied, whilst S. frontosa graduated to Turborotalia

spp. which prevented the last occurrence being defined. Subbotina linaperta was present at the top of the

section studied (1053A, 3H-4, 105 108 cm; 24.60

mcd). The range of this species therefore continues
into the late Eocene beyond 35.40 Ma (Fig. 2).

30
B.S. Wade / Marine Micropaleontology 51 (2004) 2338
Fig. 3. Stable isotope results of various monospecific foraminifera over the extinction of Morozovella. (a) Oxygen isotope results (Wade and Kroon, 2002); (b) Carbon isotope results.
( ): Morozovella crassata; (5): Morozovella spinulosa; (Z): Morozovella spp.; (
): Acarinina praetopilensis; (o): Turborotalia cocoaensis; ( w ): Globigerinatheka mexicana; (+):
Subbotina utilisindex; (n): Nuttalides truempyi. Sea surface temperatures were calculated using the equation of Erez and Luz (1983) with 0.5xice volume effect (Lear et al., 2000)
and adjusted for latitudinal gradients in evaporation as per Zachos et al. (1994). Spliced L*a*b color code L (after Norris et al., 1998), magnetochronology and biostratigraphic zones
are shown on the right. This interval corresponds to the Bartonian and North American land mammal age Late Duchesnean.

B.S. Wade / Marine Micropaleontology 51 (2004) 2338

3.2. Stable isotope results

The results of isotopic analyses for planktonic and
benthic foraminifera are illustrated in Fig. 3. Carbon
isotope results from Morozovella and Acarinina show a
large variability (~1.7x) close to the extinction events
(Fig. 3b) and range from 2.2xto 3.9x(Appendix
B1). Globigerinatheka mexicana d13C values are heavier than those of Morozovella and Acarinina but lighter
than the thermocline dwellers and range from 1.0xto
2.6x. The d13C values recorded by S. utilisindex and
T. cocoaensis are very similar to each other and vary
between 1.0xand 1.7xPDB. The shift in d13C to
lower values at 92.37 mcd (Fig. 3b) is an artefact due to
the measurements of G. mexicana recording lighter
d13C values in comparison to morozovellids. Carbon
isotopes at the extinction episode are not significantly
different to those earlier in the record. Oxygen isotopic
data for planktonic foraminifera at Site 1052 are
presented in Wade and Kroon (2002).
Benthic foraminiferal (N. truempyi) stable isotope
values fluctuate between 0.9xand 0.2xfor d18O
and 0.5xand 1.1xfor d13C (Fig. 3; Appendix B).
A correction factor of + 0.4xwas applied to the
oxygen isotope results to account for vital and habitat
preferences as per Shackleton et al. (1984).
4. Discussion
4.1. Calibration of planktonic foraminiferal
biostratigraphy
The extinction of Morozovella within Chron
C17n.3n is consistent with previous studies from the
tropics and subtropics (e.g., Berggren et al., 1995), but
approximately 400 kyr later than in Mediterranean
sections (e.g., Nocchi et al., 1986; Premoli Silva and
Boersma, 1988; Mancin and Pirini, 2001). The continued development of the astronomical time-scale will
allow the diachrony of datum events to be assessed.
Qualitative observations indicated a decrease in
abundance of Morozovella from 38. 3 Ma (PSR01
time-scale), suggesting a period of increased ecological stress for the morozovellids. However, qualitative
observations did not indicate a decline in the abundance of A. praetopilensis until 37.813 Ma, suggest1

For Appendix B see online version of this article.

31

ing that the demise of A. praetopilensis was rapid and

occurred within 5.7 kyr.
Acarinina medizzai and Acarinina echinata continue
to the top of Site 1052 ( < 34.59 Ma, magnetochron
C16n). The persistence of small acarininids into the
upper Eocene was also noted in high latitudes at Sites
702 and 703 (South Atlantic) by Nocchi et al. (1991) and
Sites 738 and 744 (Kerguelen Plateau) by Huber (1991).
The acarininid lineage thus extends after the major
biotic turnover in the latest middle Eocene. The smaller
acarininid forms were probably less specialised and are
therefore more resilient to environmental change.
The FO of G. semiinvoluta within Chron C17n.3n.
is younger than previously indicated by Berggren et al.
(1995), where the FO of G. semiinvoluta is close to the
base of C17r and is older than the LO of M. spinulosa.
This difference was also found by several other workers (e.g., Benjamini, 1980; Nocchi et al., 1986; Pearson
and Chaisson, 1997; Norris et al., 1998) suggesting that
the diachronism of the FO of G. semiinvoluta should be
investigated further. Specimens here intergraded from
Globigerinatheka spp. (Plate 1c) making the actual FO
difficult to determine.
The extended range of P. capdevilensis to 36.24/
36.35 Ma (CK95 and PSR01 time-scales, respectively)
is in contrast to previous work that has suggested an
extinction of Planorotalites spp. within Zone P14 at
38.5 Ma (Schmidt and Raju, 1973; Toumarkine and
Luterbacher, 1985; Nocchi et al., 1986; Mancin and
Pirini, 2001). This discrepancy is probably due to
Planorotalites spp. size, as this genus generally falls
into the 63 125 Am size fraction.
Subbotina linaperta extends into younger sediments
in the North Atlantic subtropics. The LO of S. linaperta
was reported by Berggren et al. (1995) to be within
C17n.2n (37.7 Ma) based on the calibration of data
from Maud Rise (Weddell Sea, Antarctica) and to
approximately 37.2 Ma at Sites 702 and 703 by Nocchi
et al. (1991). Here, the LO of S. linaperta (Plate 1d 1f)
was found at Blake Nose to be younger than 34.6 Ma
(CK95 time-scale) because this species was present at
the top of Site 1052 and also in samples analysed from
Site 1053 (1053A, 3H-4, 105 108 cm; magnetochron
C13r). Jenkins (1971) and Blow (1979) reported that S.
linaperta persisted into the late Eocene (Zone P16).
Although this study does not incorporate sediments of
Zone P16, the duration of S. linaperta does extend
beyond that shown in Berggren et al. (1995).

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B.S. Wade / Marine Micropaleontology 51 (2004) 2338

The high-resolution biostratigraphic examination of

Site 1052 has therefore led to a number of species
ranges being refined. The extinctions of P. capdevilensis, S. linaperta and the acarininid lineage were all
previously documented within the middle Eocene.
These have all been found to continue into the late
Eocene at Site 1052.
4.2. Causal mechanisms of the biotic turnover
During the early Paleogene, the morozovellids and
acarininids were immensely successful shallow
dwelling groups. The near synchronous extinction of
the morozovellids and the large acarininids would
suggest a connected causal mechanism. Near simultaneous extinction events are also exhibited by the
terminations of the planktonic foraminiferal genera
Turborotalia and Hantkenina in the uppermost Eocene (Pomerol and Premoli Silva, 1986) and Dentoglobigerina altispira/Menardella multicamerata in the
Pliocene (Chaisson and Pearson, 1997). However, the
cause of these multiple extinctions remains unknown.
It is difficult to envisage the mechanisms relating to
the near synchronous extinction of Morozovella and
Acarinina without clear climatic control. The closely
spaced extinctions of related taxa suggest some kind
of change in oceanic circulation or reorganisation of
current systems related to ocean basin geometry or
expansion of the cryosphere. The high-resolution
biostratigraphy at Site 1052, in conjunction with the
multispecies stable isotope data, provide significant
insights into palaeoceanographic conditions at the
turnover events. The possible hypotheses that resulted
in the near synchronous extinction of the morozovellids and large acarininids are discussed below.
4.2.1. Temperature
The morozovellids and acarininids typically record
the lightest d18O values and heaviest d13C values
compared to other Eocene planktonic foraminifera
(Pearson et al., 1993; Norris, 1996; Pearson et al.,
2001). Surface dwelling warm water-adapted species
were the primary ecological group that declined or
terminated in the latest middle Eocene (Keller et al.,
1992). Long-term evolutionary trends in planktonic
foraminifera appear to correspond to temperature
(Berggren, 1969). The extinction of the surface water
group without a decline in forms that inhabited deeper

waters does suggest that surface water cooling was a

possible forcing factor. The extinction of the muricate
genera has therefore often been linked with decreasing
SSTs and global cooling (Berggren, 1969; Keller,
1983; Boersma and Premoli Silva, 1991; Keller et al.,
1992; Pearson, 1996).
Other marine and terrestrial faunal and floral groups
also indicate a biotic turnover in the latest middle/early
late Eocene. Extinctions around the Bartonian/Priabonian boundary have been found in land mammals
(Wilson, 1986; Stucky, 1990; Prothero, 1999; Alroy
et al., 2000), bivalves, gastropods (Hansen, 1987) and
larger foraminifera (Hottinger, 1960; Schaub, 1981;
Hallock et al., 1991). The majority of species becoming
extinct were highly diversified tropical species (Berggren and Prothero, 1992), suggesting a causal link
between climatic deterioration and biotic turnover.
The highly fluctuating d18O values of surface
dwelling planktonic foraminifera indicate environmental instability and considerable temporal variation in
SSTs and middle Eocene subtropical climate (Wade
and Kroon, 2002). There is an increase in the Subbotina
d18O immediately following the termination of the
morozovellids (Fig. 3). This could represent an abrupt
cooling of the thermocline; however, the time series
here is not of great enough length to determine whether
this was a long-term climatic trend in the structure of
the water column. A decrease in abundance prevented
the acquisition of isotopic data for both Morozovella
and Acarinina in the 6 kyr prior to their extinction.
However, any significant change in SSTs would be
detected in the oxygen isotopic results of G. mexicana.
Benthic foraminiferal results (Fig. 3) are comparable
with previous studies (Zachos et al., 2001 and references therein).
There is a possible ~6 jC decrease in SSTs over the
400 kyr prior to the extinction events (~1.5 jC / kyr;
Fig. 3a); however, this does not appear to represent a
long-term shift in climate. Although both Morozovella
and Acarinina became extinct during a cooling trend
and within an SST low (21 jC), evidence for major
cooling and direct SST control to explain the extinct
events is insufficient, particularly as populations survived a similar SST low 471 kyr earlier at 38.3 Ma (Fig.
3a). This suggests that surface water cooling was not
the primary forcing factor for the extinction episode.
The data here do not support ideas that significant
reductions in SST caused the extinction events, and

B.S. Wade / Marine Micropaleontology 51 (2004) 2338

surface water cooling alone, therefore, cannot account

for the extinction of the morozovellids and the decline
in acarininid diversity.
The extinction of the Morozovella lineage may have
been in response to habitat destruction and niche
elimination. Whilst there is no major climatic shift at
the extinction events, the gradual decrease in SSTs
(Fig. 3a) resulted in a marked reduction of the thermal
gradient. The isotopic gradient of the water column at
the extinction events is only ~1.5x, indicating a
thermal gradient possibly as low as 6 jC (~0.25x/1
jC; Epstein et al., 1953). The reduction in foraminiferal
diversity may thus be associated with a decrease in the
surface to benthos thermal gradient. Significant
changes in thermocline depth and productivity may
have permitted asymbiotic deep dwellers, such as
Subbotina, Turborotalia and Hantkenina, to encroach
and occupy the mixed layer and thrive. There is an
indication that the genera Hantkenina and Subbotina
decreased their depth habitat through the Eocene
(MacLeod et al., 1990; Coxall et al., 2000), but it is
difficult to ascertain whether this habitat change was
related to the extinction of Morozovella. Hantkenina
and Subbotina species may have exerted enhanced
competitive pressure on zooplankton communities by
competing for a niche that was no longer optimal for the
morozovellids. The reduced stratification of the water
column could also have critical implications for reproductive strategies in planktonic foraminifera. Variations in the structure of the water column such as
depth of the thermocline or the chlorophyll maximum
may have provoked failure of synchronisation in
gametogensis and thus extinction.
Blake Nose is situated in the subtropics (29jN) in
the western North Atlantic. Whilst no significant temperature change is evident from the foraminifera record
at this location, there is evidence for temperature shift
around this time elsewhere (Douglas and Savin, 1973,
1975; Shackleton and Kennett, 1975; Boersma and
Shackleton, 1977; Oberha nsli and Toumarkine,
1985). Global cooling through the middle Eocene
would have decreased the morozovellids habitat (and
population size) by the reduction of tropical and subtropical biogeographical provinces. The increased environmental stress caused by the reduction in habitat
may thus have contributed to their demise. High-latitude cooling is likely to have had an effect on circulation and eutrophication (discussed below) and,

33

therefore, temperature may be involved indirectly rather than directly.

4.2.2. Eutrophication and upwelling
The demise of the muricates may have been in
reaction to variations in the location and intensity of
upwelling and eutrophication of surface waters. Allmon
(2001) concluded that nutrient conditions were a prominent forcing factor in patterns of extinction in the
western North Atlantic during the late Cenozoic. There
is evidence of high productivity of surface waters in the
latest middle and late Eocene (McGowran, 1989) with a
greater spatial range of upwelling provinces (Boersma et
al., 1987) and abundant biosiliceous sediments throughout the Gulf of Mexico, and equatorial and subtropical
Atlantic (Berger and von Rad, 1972; McCoy and Zimmerman, 1977; Tucholke and Vogt, 1979; Premoli Silva
and Boersma, 1986; Ehrmann and Thiede, 1986). Initiation of biosiliceous sedimentation at Site 689 (Maud
Rise) also occurred in the latest middle Eocene, indicating that the fertility of surface waters significantly
increased (Diester-Haass, 1995). Eutrophic waters at
Blake Nose during the latest middle Eocene are indicated by the abundant siliceous microfossils (Norris et al.,
1998), protoperidinioid dinoflagellate cysts and Prasinophyte algae (van Mourik et al., 2001).
Both isotopic analyses and modelling studies suggest that the Blake Nose region was sensitive to
upwelling during the Eocene (Bice et al., 2000; Huber
and Sloan, 2000; Wade et al., 2000, 2001; Sloan and
Huber, 2001a,b). Upwelling and the eutrophication of
surface waters would have had a notable impact on
thermocline depth, nutricline dynamics and interspecies competition in marine communities, resulting in a
shallow nutrient-enriched mixed layer and cool SSTs.
This would require species to have adapted to varying
temperatures and nutrient levels. Changes in nutrient
regimes would have caused habitat disturbance and
enhanced extinction as suggested by Allmon (2001) for
the Plio-Pleistocene. A period of environmental stress
is also reflected in the dwarfing of calcareous nannoplankton assemblages from this site (Govan, 2003).
The decrease in size in nannofossils coupled with the
extinction of M. spinulosa and A. praetopilensis suggest significant stress in the surface waters at this time
and perhaps a major change in nutrient pathways and
food web dynamics. Mechanisms of eutrophication
rather than temperature control have also been sug-

34

B.S. Wade / Marine Micropaleontology 51 (2004) 2338

gested to explain the extinction of the long ranging

nannofossil genus Discoaster in the late Pliocene
(Chapman and Chepstow-Lusty, 1997).
The loss of oligotrophic habitats would have
affected competition and trophic resources for many
marine organisms. Extinctions also occur within the
large benthic foraminifera at this time, with a decrease
in the diversity of the nummulitid group and extinction of the alveolinid group (Hottinger, 1960; Schaub,
1981; Hallock et al., 1991). Large benthic foraminifera, like the muricate planktonic foraminifera, are
indicated to have thrived in the photic zone and
include forms with dependence on endosymbionts
and/or a tendency towards a k-strategy scenario,
suggesting decreases in oligotrophic habitats on both
the shelf and open ocean (Hallock et al., 1991). It is
possible that the continued increase in surface water
nutrient levels caused habitat disturbance and thus
extinction. However, it is difficult to invoke stratification breakdown and nutrification on a global scale.
Detailed biostratigraphy of the larger foraminifera will
help to determine whether these events are coeval
with those in the planktonic foraminiferal record.
4.2.3. Symbiont elimination
Within the planktonic foraminiferal assemblage, the
muricate forms are distinct from all other planktonic
foraminifera. Previous studies have suggested that
Morozovella and Acarinina had similar ecological
preferences, occupying the warm, shallow, mixed layer
of the oceans, and had a symbiotic relationship with
algae (Pearson et al., 1993; DHondt et al., 1994; Kelly
et al., 1996; Norris, 1996). This valuable adaptation
would have allowed them to thrive in oligotrophic
habitats and niche space not available to the rest of
the assemblage. However, this adaptation may have
also enhanced their susceptibility to extinction. Many
modern species of planktonic foraminifera (e.g., Orbulina universa and Globigerinoides sacculifer) have a
symbiotic relationship with algae, usually chysophycophytes or dinoflagellates (Hemleben et al., 1989).
The muricate genera Morozovella and Acarinina are
analogous in ecological terms to the modern planktonic
foraminifer genus Globigerinoides. In the modern species G. sacculifer, photosymbionts play a critical role in
calcification and growth rate (Be et al., 1982). Like G.
sacculifer, acquiring algal symbionts may have been
essential for the successful life cycle of the muricate

foraminifera. This would have left the muricates susceptible to both environmental factors influencing
themselves and factors affecting their algal symbionts.
Symbiotic forms are largely absent after the extinction of Globigerinatheka until the Miocene radiation.
The biotic turnover in the late middle Eocene therefore
represents a significant reduction in the numbers of
planktonic foraminifera hosting algal symbionts and
constitutes a major change in the surface water ecology.
The evolution of symbiotic relationships with algae
was probably an adaptation to oligotrophic environments, where photosymbiont activity may be of evolutionary or ecological benefit (Haynes, 1965; Lee et
al., 1979; Norris, 1996). The appearance of photosymbiosis has been suggested to enhance diversification (Kelly et al., 1996; Norris, 1996). The loss of
symbiotic relationships therefore has the potential to
trigger extinctions and decrease diversity. Multiple
alterations in environmental conditions such as pronounced upwelling and surface water eutrophication
possibly led to the destruction of the symbiotic relationships in both Morozovella and Acarinina and thus their
demise. Eutrophication has been documented to have a
negative effect on other photosymbiotic organisms
(e.g., corals; Hallock and Schlager, 1986; Edinger
and Risk, 1994). The closely spaced extinctions of
Morozovella, A. praetopilensis and the alveolinids
could therefore feasibly be related to diminished photosymbiotic activity. Perhaps all of these groups possessed a common algal symbiotic relationship? The
elimination of this common symbiont due to eutrophication could thus have directly contributed to the
demise of the muricate group.
The deterioration of symbiotic relationships is therefore proposed as a mechanism to account for the near
synchronous extinctions of large acarininids and Morozovella and the turnover seen in the large benthic
foraminifera. This scenario has also been put forward
to explain the extinction of the Morozovella velascoensis lineage in the late Paleocene (Kelly et al., 2001).
Future high-resolution work from other locations will
substantially enhance the understanding of environmental change at this time.
4.3. Summary
Previous work (e.g., Cifelli, 1969; Lipps, 1970,
1986; Keller et al., 1992) has proposed that the biotic

B.S. Wade / Marine Micropaleontology 51 (2004) 2338

turnover in planktonic foraminifera was attributed to

global cooling and habitat destruction. The lack of a
distinct shift in temperature at the near synchronous
extinction events suggests that factors other than sea
surface temperatures were a significant mechanism
behind the biotic turnover. The data obtained from Site
1052 indicate that niche elimination or food web
collapse and perhaps the demise of symbiotic associations caused by increased upwelling and surface water
eutrophication were primary forcing factors. Temperature decline may have been a contributing cause for the
turnover events rather than a direct influence. The
gradual decrease in SSTs probably affected the depth
and stability of the mixed layer causing eutrophication
of surface waters as suggested by Hallock et al. (1991).
Enhanced upwelling and collapse of the thermocline
may have initiated the deterioration in symbiotic partnerships. Any of these factors may have decreased
Morozovella populations beyond a critical threshold.

5. Conclusions
Planktonic foraminiferal biostratigraphic events
have been examined with a sampling resolution of 10
cm from Ocean Drilling Program, Leg 171B, Site 1052,
with additional analyses from Site 1053. The new and
revised biostratigraphic data of the middle and late
Eocene have been calibrated to the astronomical timescale of Palike et al. (2001) and the magnetochronology
of Cande and Kent (1995) to accurately define planktonic foraminiferal bioevents. M. crassata and M.
spinulosa terminate at the same horizon whilst A.
praetopilensis terminated 10 kyr prior to the morozovellids. Qualitative observations indicate a decline in
the abundance of morozovellids from 500 kyr before
the extinction. In the acarininid lineage, the youngest
stratigraphic occurrence comprised of the small ( < 125
Am) A. medizzai and A. echinata.
The high-resolution biostratigraphic and stable isotopic analyses at Site 1052 permits the cause of the
biotic turnover to be examined at a much greater
resolution than in previous studies and test the hypothesis of extinction and climate change. Multispecies
stable isotope results reveal that decreases in SSTs
were not the primary cause of the stepwise biotic
turnover in planktonic foraminifera at this time, and
there seems to be no direct climatic event associated

35

with the extinctions. The results of this study favour the

eutrophication of surface waters and the demise of
symbiotic relationships as the principle causal mechanisms behind this key biotic turnover.
Acknowledgements
William Berggren, Kate Darling, Dick Kroon and
Paul Pearson are warmly thanked for discussions on
planktonic foraminiferal taxonomy and valuable comments on earlier versions of this manuscript. I thank
Brian Huber for an enlightening discussion on the
acarininids and use of the SEM facility at the
Smithsonian National Museum of Natural History. I
am grateful to Heiko Palike for the time-scale data,
Colin Chilcott for assistance with the mass spectrometer and Richard Hesketh for picking benthic foraminifera. Brian McGowran and H. Oberhansli are thanked
for their constructive reviews of this manuscript. The
Ocean Drilling Program (ODP) provided the samples
from Blake Nose. The ODP is sponsored by the U.S.
National Science Foundation and participating countries under management of Joint Oceanographic
Institutions. This research was supported by UK
Natural Environment Research Council reference
number GT 04/97/93/ES and NER/I/S/2000/00954
and the University of Edinburgh.
References
Allmon, W.D., 2001. Nutrients, temperature, disturbance, and evolution: a model for the late Cenozoic marine record of the
western Atlantic. Palaeogeography, Palaeoclimatology, Palaeoecology 166, 9 26.
Alroy, J., Koch, P.L., Zachos, J.C., 2000. Global climate change and
North American mammalian evolution. Paleobiology 26 (Suppl.
4), 259 288.
Be, A.W.H., Spero, H.J., Anderson, O.R., 1982. Effects of symbiont elimination and reinfection on the life processes of the
planktonic foraminifer Globigerioides sacculifer. Marine Biology 70, 73 86.
Benjamini, C., 1980. Stratigraphy and foraminifera of the Qeziot
and Har Aqrav formations (latest middle to late Eocene) of the
western Negev, Israel. Israel Journal of Earth-Sciences 29,
227 244.
Berger, W.H., von Rad, U., 1972. Cretaceous and Cenozoic sediments from the Atlantic ocean. Initial Reports of the Deep Sea
Drilling Project, U.S., vol. 14. U.S. Government Printing Office,
Washington, DC, pp. 787 886.
Berggren, W.A., 1969. Rates of evolution in some Cenozoic planktonic foraminifera. Micropaleontology 15, 351 365.
Berggren, W.A., Prothero, D.R., 1992. Eocene oligocene climatic

36

B.S. Wade / Marine Micropaleontology 51 (2004) 2338

and biotic evolution: an overview. In: Prothero, D.R., Berggren,

W.A. (Eds.), Eocene Oligocene Climatic and Biotic Evolution.
Princeton University Press, New Jersey, pp. 1 28.
Berggren, W.A., Kent, D.V., Swisher III, C.C., Aubry, M.-P. 1995.
A revised Cenozoic geochronology and chronostratigraphy. In:
Berggren, W.A., Kent, D.V., Aubry, M.-P., Hardenbol, J. (Eds.),
Geochronology, Time Scales and Global Stratigraphic Correlation: A Unified Temporal Framework for an Historical Geology,
vol. 54. Society of Economic Paleontologists and Mineralogists,
Tulsa, OK, pp. 129 212. Special Publication.
Bice, K.L., Sloan, L.C., Barron, E.J., 2000. Comparison of early
Eocene isotopic paleotemperatures and the three-dimensional
OGCM temperature field: the potential for use of model-derived
surface water d18O. In: Huber, B.T., MacLoed, K.G, Wing, S.L.
(Eds.), Warm Climates in Earth History. Cambridge Univ. Press,
Cambridge, pp. 79 131.
Blow, W.H., 1979. The Cenozoic Globigerinida E.J. Brill, Leiden 3
volumes. 1413 pp.
Boersma, A., Shackleton, N.J., 1977. Tertiary oxygen and carbon
isotope stratigraphy, Site 357 (mid latitude South Atlantic) Initial Reports of the Deep Sea Drilling Project, U.S., vol. 39. U.S.
Government Printing Office, Washington, DC, pp. 911 924.
Boersma, A., Premoli Silva, I., 1991. Distribution of Paleogene
planktonic foraminiferaanalogies with the recent? Palaeogeography Palaeoclimatology, Palaeoecology 83, 29 48.
Boersma, A., Premoli Silva, I., Shackleton, N.J., 1987. Atlantic
Eocene planktonic foraminiferal paleohydrographic indicators
and stable isotope paleoceanography. Paleoceanography 2,
287 331.
Cande, S.C., Kent, D.V., 1995. Revised calibration of the geomagnetic polarity timescale for the Late Cretaceous and Cenozoic.
Journal of Geophysical Research 100, 6093 6095.
Chaisson, W.P., Pearson, P.N., 1997. Planktonic foraminifer biostratigraphy at Site 925: middle Miocene Pleistocene. In: Shackleton, N.J., Curry, W.B, Richter, C., Bralower, T.J. (Eds.),
Proceeding of the Ocean Drilling Program. Scientific Results,
vol. 154, pp. 3 31.
Chapman, M.R., Chepstow-Lusty, A.J., 1997. Late Pliocene climatic changes and the global extinction of the discoasters: an
independent assessment using oxygen isotope record. Palaeogeography, Palaeoclimatology, Palaeoecology 134, 109 125.
Cifelli, R., 1969. Radiation of Cenozoic planktonic foraminifera.
Systematic Zoology 18, 154 168.
Coxall, H.K., Pearson, P.N., Shackleton, N.J., Hall, M.A., 2000.
Hantkeninid depth adaptation: an evolving life strategy in a
changing ocean. Geology 28, 87 90.
Craig, H., 1957. Isotopic standards for carbon and oxygen correction factors for mass spectrometric analysis of CO2. Geochimica
et Cosmochimica Acta 12, 133 149.
DHondt, S., Zachos, J.C., Schultz, G., 1994. Stable isotopic signals
and photosymbiosis in late Paleocene planktic foraminifera. Paleobiology 20, 391 406.
Diester-Haass, L., 1995. Middle Eocene to early Oligocene paleoceanography of the antarctic ocean (Maud Rise, ODP Leg
113, Site 689): change from low to a high productivity
ocean. Palaeogeography, Palaeoclimatology, Palaeoecology
113, 311 334.

Douglas, R.G., Savin, S.M., 1973. Oxygen and carbon isotope

analyses of cretaceous and tertiary foraminifera from the central
North Pacific. Initial Reports of the Deep Sea Drilling Project,
U.S., vol. 17. U.S. Government Printing Office, Washington,
DC, pp. 591 605.
Douglas, R.G., Savin, S.M., 1975. Oxygen and carbon isotope
analyses of Tertiary and Cretaceous microfossils from Shatsky
rise and other sites in the north Pacific Ocean. Initial Reports of
the Deep Sea Drilling Project, U.S., vol. 32. U. S. Government
printing Office, Washington, DC, pp. 509 520.
Edinger, E.N., Risk, M.J., 1994. Oligocene Miocene extinction
and geographic restriction of Caribbean corals: roles of turbidity,
temperature, and nutrients. Palaios 9, 576 598.
Ehrmann, W.U., Thiede, J., 1986. Correlation of terrigenous and
biogenic sediment fluxes in the North-Atlantic Ocean during the
past 150 my. Geologische Rundschau 75, 43 55.
Epstein, S., Buchsbaum, R., Lowenstam, H.A., Urey, H.C., 1953.
Revised carbonate-water isotopic scale. Geological Society of
America Bulletin 64, 1315 1325.
Erez, J., Luz, B., 1983. Experimental paleotemperature equation for
planktonic foraminifera. Geochimica et Cosmochimica Acta 47,
1025 1031.
Govan, V., 2003. The nannoplankton response to sea surface temperature variations during the middle Eocene at Blake Nose
Project Report. University of Edinburgh, Edinburgh, UK.
Hallock, P., Schlager, W., 1986. Nutrient excess and the demise of
coral reefs and carbonate platforms. Palaios 1, 389 398.
Hallock, P., Premoli Silva, I., Boersma, A., 1991. Similarities between planktonic and larger foraminiferal evolutionary trends
through Paleogene paleoceanographic changes. Palaeogeography, Palaeoclimatology, Palaeoecology 83, 49 64.
Hansen, T.A., 1987. Extinction of late Eocene to Oligocene mollusc: relationship to shelf area, temperature changes, and impact
events. Palaios 2, 69 75.
Haynes, J., 1965. Symbiosis, wall structure and habitat in foraminifera. Contributions from the Cushman Foundation for Foraminiferal Research 16, 40 43.
Hemleben, C., Spindler, M., Anderson, O.R., 1989. Modern Planktonic Foraminifera. Springer, New York, pp. 86 111.
Hottinger, L., 1960. Recherches sur les alveolines du Paleocene et
de lEocene. Memoires Suisses de Paleontologie 75/76, 1 243.
Huber, B.T., 1991. Paleogene and early Neogene planktonic foraminifer biostratigraphy of Sites 738 and 744, Kerguelen Plateau
(southern Indian Ocean). In: Barron, J., Larsen, B., et al.
(Eds.), Proceedings of the Ocean Drilling Program. Scientific
Results, vol. 119. Ocean Drilling Program, College Station,
TX, pp. 427 449.
Huber, M., Sloan, L.C., 2000. Modelling the Paleogene: Part II.
Paleogene wind-driven ocean circulation changes predicted
from climate modeling studies. GFF (Geological Society of
Sweden) 122, 80 81.
Jenkins, D.G., 1971. The reliability of some Cenozoic planktonic
foraminiferal datum-planes used in biostratigraphic correlation.
Journal of Foraminiferal Research 1, 82 86.
Keller, G., 1983. Paleoclimatic analyses of middle Eocene through
Oligocene planktic foraminiferal faunas. Palaeogeography, Palaeoclimatology, Palaeoecology 43, 73 94.

B.S. Wade / Marine Micropaleontology 51 (2004) 2338

Keller, G., MacLeod, N., Barrera, E., 1992. Eocene Oligocene
faunal turnover in planktic foraminifera, and Antarctic glaciation. In: Prothero, D.R., Berggren, W.A. (Eds.), Eocene Oligocene Climatic and Biotic Evolution. Princeton University Press,
New Jersey, pp. 218 244.
Kelly, D.C., Arnold, A.J., Parker, W.C., 1996. Paedomorphosis and
the origin of the Paleogene planktonic foraminiferal genus Morozovella. Paleobiology 22, 266 281.
Kelly, D.C., Bralower, T.J., Zachos, J.C., 2001. On the demise of
the early Paleogene Morozovella velascoensis lineage: terminal
progenesis in the planktic foraminifera. Palaios 16, 507 523.
Kroon, D., Norris, R.D., Klaus, A., the ODP Leg 171B Shipboard
Scientific Party, 1998. Drilling Blake Nose: the search for evidence of extreme Palaeogene Cretaceous climates and extraterrestrial events. Geology Today, 222 226 (November
December 1998).
Lear, C.H., Elderfield, H., Wilson, P.A., 2000. Cenozoic deep-sea
temperatures and global ice volumes from Mg/Ca in benthic
foraminiferal calcite. Science 287, 269 272.
Lee, J.J., McEnery, M.E., Kahn, E.G., Schuster, F.L., 1979. Symbiosis and the evolution of larger foraminifera. Micropaleontology 25, 118 140.
Lipps, J.H., 1970. Plankton evolution. Evolution 24, 1 22.
Lipps, J.H., 1986. Extinction dynamics in pelagic ecosystems. In:
Elliot, D.K. (Ed.), Dynamics of Extinction. Wiley, New York,
pp. 89 103.
MacLeod, N., Keller, G., Kitchell, J.A., 1990. Progenesis in late
Eocene populations of Subbotina linaperta (foraminifera) from
the western Atlantic. Marine Micropaleontology 16, 219 240.
Mancin, N., Pirini, C., 2001. Middle Eocene to early Miocene
foraminiferal biostratigraphy in the Epiligurian sucession (north
Apennines, Italy). Rivista Italiana di Paleontologia e Stratigrafia
107, 371 393.
McCoy, F., Zimmerman, H., 1977. A history of sediment lithofacies in the South Atlantic Ocean. In: Perch-Nielsen, K.,
Supko, P., et al., (Eds.), Initial Reports of the Deep Sea
Drilling Project, vol. 39. U.S. Government Printing Office,
Washington, pp. 1047 1079.
McGowran, B., 1989. Silica burp in the Eocene ocean. Geology 17,
857 860.
Nocchi, M., Parisi, G., Monaco, P., Monechi, S., Madile, M.,
Napoleone, G., Ripepe, M., Orlando, M., Premoli Silva, I.,
Bice, D.M., 1986. The Eocene Oligocene boundary in the
Umbrian pelagic sequences, Italy. In: Pomerol, C., Premoli
Silva, I. (Eds.), Terminal Eocene Events. Developments in
Palaeontology and Stratigraphy, vol. 9. Elsevier, Amsterdam,
pp. 24 40.
Nocchi, M., Amici, E., Premoli Silva, I., 1991. Planktonic foraminiferal biostratigraphy and paleoenvironmental interpretation on
Paleogene faunas from the subantarctic transect, Leg 114. In:
Ciesielski, P.F., Kristoffersen, Y., et al., (Eds.), Proceedings of
the Ocean Drilling Program. Scientific Results, vol. 114. Ocean
Drilling Program, College Station, TX, pp. 233 279.
Norris, R.D., 1996. Symbiosis as an evolutionary innovation in the
radiation of Paleocene planktic foraminifera. Paleobiology 22,
461 480.
Norris, R.D., Kroon, D., Klaus, A., et al., 1998. Proceedings of the

37

Ocean Drilling Program. Initial Results, vol. 171. Ocean Drilling Program, College Station, TX, 749 pp.
Oberhansli, H., Toumarkine, M., 1985. The Paleogene oxygen and
carbon isotope history of Sites 522, 523 and 524 from the central South Atlantic. In: Hsu, K.J., Weisset, H.J. (Eds.), South
Atlantic Paleoceanography. Cambridge Univ. Press, Cambridge,
pp. 125 148.
Ogg, J.G., Bardot, L., 2001. Aptian through Eocene magnetostratigraphic correlation of the Blake Nose transect (Leg 171B),
Florida Continental Margin. In: Kroon, D., Norris, R.D., Klaus,
A. (Eds.), Proceedings of the Ocean Drilling Program, Scientific
Results, vol. 171B [Online] Available from World Wide Web:
hhttp://www-odp.tamu.edu/publications/171B_sr/171bsr.htmi.
Palike, H., Shackleton, N.J., Rohl, U., 2001. Astronomical forcing
in late Eocene marine sediments. Earth and Planetary Science
Letters 193, 589 602.
Pearson, P.N., 1996. Cladogenetic, extinction and survivorship patterns from a lineage phylogeny: the Paleogene planktonic foraminifera. Micropaleontology 42, 179 188.
Pearson, P.N., Chaisson, W.P., 1997. Late Paleocene to middle
Miocene planktonic foraminifer biostratigraphy of the Ceara
rise. In: Shackleton, N.J., Curry, W.B., Richter, C., Bralower,
T.J. (Eds.), Proceeding of the Ocean Drilling Program, Scientific
Results, vol. 154, pp. 33 68.
Pearson, P.N., Shackleton, N.J., Hall, M.A., 1993. Stable isotope
paleoecology of middle Eocene planktonic foraminifera and
multi-species isotope stratigraphy, DSDP Site 523, South Atlantic. Journal of Foraminiferal Research 23, 123 140.
Pearson, P.N., Ditchfield, P.W., Singano, J., Harcourt-Brown, K.G.,
Nicholas, C.J., Olsson, R.N., Shackleton, N.J., Hall, M.A.,
2001. Warm tropical sea surface temperatures in the late Cretaceous and Eocene epochs. Nature 413, 481 487.
Pomerol, C., Premoli Silva, I., 1986. The Eocene Oligocene transition: events and boundary. In: Pomerol, C., Premoli Silva, I.
(Eds.), Terminal Eocene Events. Developments in Palaeontology and Stratigraphy, vol. 9. Elsevier, Amsterdam, pp. 1 24.
Premoli Silva, I., Boersma, A., 1986. Paleogene biofacies in the
western North Atlantic Ocean. In: Vogt, P., Tucholke, B. (Eds.),
The Geology of North America, volume M, The Western North
Atlantic Region. Geological Society of America, pp. 527 546.
Premoli Silva, I., Boersma, A., 1988. Atlantic Eocene planktonic
foraminiferal historical biogeography and paleohydrographic indices. Palaeogeography, Palaeoclimatology, Palaeoecology 67,
315 356.
Prothero, D.R., 1999. Does climatic change drive mammlian evolution? GSA Today 9, 1 7.
Schaub, H., 1981. Nummulites et Assilines de la Tethys paleogene, taxinomie, phylogenie et biostratigraphie avec deux volumes datlas. Memoires Suisses de Paleontologie 104 106,
1 238.
Schmidt, R.R., Raju, D.S.N., 1973. Globorotalia palmerae Cushman and Bermudez and closely related species from the lower
Eocene, Cauvery Basin, south India. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, Series
B: Palaeontology, Geology, Physics and Chemistry, vol. 76.
North-Holland, The Netherlands, pp. 167 184.
Shackleton, N.J., Kennett, J.P., 1975. Paleotemperature history of

38

B.S. Wade / Marine Micropaleontology 51 (2004) 2338

the Cenozoic and the initiation of Antarctic glaciation: oxygen

and carbon isotope analyses in DSDP Sites 277, 279, and 281.
In: Kennett, J.P., Houltz, R.E., et al., (Eds.), Initial Reports of
the Deep Sea Drilling Project, vol. 29. U.S. Government Printing Office, Washington, DC, pp. 743 755.
Shackleton, N.J., Hall, M.A., Boersma, A., 1984. Oxygen and carbon isotope data from Leg 74 foraminifers. Moore, T.C., Rabinowitz, P.D., et al. (Eds.), Initial Reports of the Deep Sea
Drilling Project, vol. 74. U.S. Government Printing Office,
Washington, DC, pp. 599 612.
Sloan, L.C., Huber, M., 2001a. North Atlantic climate variability in
the early Palaeogene: a climate modeling sensitivity study. In:
Kroon, D., Norris, R.D., Klaus, A. (Eds.), Western North Atlantic Palaeogene and Cretaceous Palaeoceanography. Special Publications, vol. 183. Geological Society, London, pp. 253 272.
Sloan, L.C., Huber, M., 2001b. Eocene oceanic responses to orbital forcing on precessional time scales. Paleoceanography 16,
101 111.
Stucky, R.K., 1990. Evolution of land mammal diversity in North
America during the Cenozoic. Current Mammalogy 2, 375 431.
Toumarkine, M., Luterbacher, H., 1985. Paleocene and Eocene
planktic foraminifera. In: Bolli, H.M., Saunders, J.B., PerchNielsen, K. (Eds.), Plankton Stratigraphy, vol. 1. Cambridge
Univ. Press, Cambridge, pp. 87 154.
Tucholke, B., Vogt, P., 1979. Western North Atlantic sedimentary
evolution and aspects of the tectonic history. Initial Reports of
the Deep Sea Drilling Project, vol. 43. U.S. Government printing Office, Washington, DC, pp. 795 863.

van Mourik, C.A., Brinkhuis, H., Williams, G.L., 2001. Middle to

late Eocene organic-walled dinoflagellate cysts from ODP Leg
171B, offshore Florida. In: Kroon, D., Norris, R.D., Klaus, A.
(Eds.), Western North Atlantic Palaeogene and Cretaceous Palaeoceanography. Special Publications, vol. 183. Geological Society, London, pp. 225 252.
Wade, B.S., Kroon, D., 2002. Middle Eocene regional climate instability: evidence from the western North Atlantic. Geology 30,
1011 1014.
Wade, B.S., Kroon, D., Norris, R.D., 2000. Upwelling in the late
middle Eocene at Blake Nose? GFF (Geological Society of
Sweden) 122, 174 175.
Wade, B.S., Kroon, D., Norris, R.D., 2001. Orbitally forced climate
change in the late middle Eocene at Blake Nose (Leg 171B):
evidence from stable isotopes in foraminifera. In: Kroon, D.,
Norris, R.D., Klaus, A. (Eds.), Western North Atlantic Palaeogene and Cretaceous Palaeoceanography. Special Publications,
vol. 183. Geological Society, London, pp. 273 291.
Wilson, J.A., 1986. Stratigraphic occurrence and correlation of
early Tertiary vertebrate faunas, Trans-Pecos Texas: Agua
Fria-Green Valley areas. Journal of Vertebrate Paleontology
6, 350 373.
Zachos, J.C., Stott, L.D., Lohmann, K.C., 1994. Evolution of
early Cenozoic marine temperatures. Paleoceanography 9,
353 387.
Zachos, J.C., Pagani, M., Sloan, L., Thomas, E., Billups, K., 2001.
Trends, rhythms, and aberrations in global climate 65 Ma to
present. Science 292, 686 693.