CALCAREOUS NANNOPLANKTON RESPONSE TO THE LATEST CENOMANIAN 
OCEANIC ANOXIC EVENT 2 PERTURBATION

GIULIA FAUCHER1*, ELISABETTA ERBA1, CINZIA BOTTINI1 & GABRIELE GAMBACORTA1

1*Corresponding author. Department of  Earth Sciences, Università degli Studi di Milano, 20133 Milan, Italy. E-mail: giulia.faucher@unimi.it

To cite this article: Faucher G., Erba E., Bottini C. & Gambacorta G. (2017) - Calcareous nannoplankton response to the latest Cenomanian 
Oceanic Anoxic Event 2 perturbation.  Riv. It. Paleontol. Strat., 123(1): 159-176.

Rivista Italiana di Paleontologia e Stratigrafia 
(Research in Paleontology and Stratigraphy)

vol. 123(1): 159-176.  March 2017

Abstract. Morphometric analyses were performed on Biscutum constans, Zeugrhabdotus erectus, Discorhabdus rota-
torius and Watznaueria barnesiae specimens from five sections spanning the Cenomanian-Turonian boundary interval 
including Oceanic Anoxic Event (OAE) 2 (~ 94 Ma). The study provides evidence for size fluctuations and dwar-
fism of  B. constans during OAE 2, followed by a partial recovery at the end of  the event: this taxon appears to be 
the most sensitive species, with similar and coeval size trends in all the analyzed sections. Conversely, morphometry 
shows negligible or unsystematic coccolith variations in Z. erectus, D. rotatorius and W. barnesiae. The comparison of  
OAE 2 data with those available for the early Aptian OAE 1a and latest Albian OAE 1d, indicates that B. constans 
repeatedly underwent size reduction and temporary dwarfism, possibly implying that the same paleoenvironmental 
factors controlled calcification of  B. constans during subsequent OAEs although the amplitude of  B. constans cocco-
lith reduction is significantly larger for OAE 1a than OAE 2.

Paleoceanographic reconstructions suggest that ocean chemistry related to the amount of  CO
2
 and toxic 

metal concentrations played a central role in B. constans coccolith secretion, while temperature and nutrient availa-
bility do not seem to have been crucial. Contrary to OAE 1a, Z. erectus, D. rotatorius and W. barnesiae appear to be 
substantially unrelated to OAE 2 paleoenvironmental stress, possibly because of  different degrees of  perturbation. 

Received: November 15, 2016; accepted: January 15, 2017

Key words: morphometry; coccoliths; Oceanic Anoxic Event 2; ocean acidification.

IntroductIon

The geological record of  the Cretaceous 
world documents profound changes in the ocean-
atmosphere system, including volcanic injection 
of  large amounts of  CO

2
, super-greenhouse con-

ditions, oceanic anoxia and eutrophication (e.g. 
Schlanger & Jenkyns 1976; Erba 2004; Hay 2009; 
Jenkyns 2010; Föllmi 2012; Bottini et al. 2015; Erba 
et al. 2015). Intervals of  prolonged global anoxia, 
known as Oceanic Anoxic Events (OAE)s (Schlan-
ger & Jenkyns 1976) were characterized by burial of  
unusually large amounts of  organic matter during 
profound perturbations of  the ocean-atmosphe-
re system, similarly to current (and future) global 
changes.

The latest Cenomanian OAE 2 (~94 Ma) is 
arguably regarded as the most extreme paleoenvi-
ronmental stress related to the warmest climate of  
the past 150 My, characterized by an accelerated 
hydrological cycle, enhanced production and bu-
rial of  organic matter, very high concentrations of  
volcanically-produced CO

2
 and altered chemistry 

and structure of  the oceans (see review provided by 
Jenkyns 2010). In the time interval encompassing 
OAE 2, calcareous nannoplankton were forced to 
face anomalous paleoceanographic and paleoclima-
tic conditions that induced extinctions and origina-
tions (e.g. Bralower 1988; Leckie et al. 2002; Erba 
2004). Quantitative studies of  nannofossil assembla-
ges in various geological settings revealed differen-
tial abundance patterns of  fertility-related species, 
in particular of  Biscutum constans and Zeugrabdothus 
erectus. In general, an eutrophication episode was re-
constructed at low latitudes (Hardas & Mutterlose 
2007) while a shift to oligotrophic conditions was 
evidenced at mid-latitudes (Gale et al. 2000; Linnert 
et al. 2010, 2011). In the Western Interior Seaway 
(WIS) local changes controlled the trophic level 
across OAE 2 (Corbett & Watkins 2013). 

In this work, we focus on size variations of  
four species, namely Biscutum constans, Discorhabdus 
rotatorius, Watznaueria barnesiae and Zeugrabdothus erec-
tus in the Cenomanian-Turonian boundary interval 
(CTBI), and specifically across OAE 2. These taxa 
were previously studied through the early Aptian 
OAE 1a (Erba et al. 2010; Lübke et al. 2015; Lübke 
& Mutterlose 2016), the latest Albian OAE 1d (Bor-



Faucher G., Erba E., Bottini C. & Gambacorta G.160

nemann & Mutterlose 2006) and the CTBI (Linnert 
& Mutterlose 2012) providing insights into cocco-
lith size changes across OAEs. In particular, Erba 
et al. (2010) demonstrated that calcareous nanno-
plankton was extremely sensitive to ocean acidifica-
tion associated to OAE 1a at low latitude sites in 
the Tethys and Pacific Oceans, allowing separation 
of  most-, intermediate-, and least-tolerant taxa: 
dwarfism of  B. constans, Z. erectus and D. rotatorius 
coccoliths was documented during OAE 1a but no 
significant changes in W. barnesiae dimension were 
detected, although more elliptical and malformed 
specimens were identified (Erba et al. 2010). Dwarf-
ism of  B. constans and Z. erectus was documented also 
across OAE 1a at higher latitudes (North Sea and 
Lower Saxony Basin, Lübke & Mutterlose 2016), 
but explained as the response to decreased light in 
surface waters under conditions of  intense run off. 
In the same sections, W. barnesiae remained stable 
without significant size variations and interpreted 
as a robust species with respect to changes of  sun-
light penetration. 

During OAE 1d, morphometry of  B. constans 
specimens attested a decrease in mean length, while 
the average size of  W. barnesiae coccoliths remained 
constant (Bornemann & Mutterlose 2006). Linnert 
& Mutterlose (2012) investigated nannofossil mor-
phometry at two Deep Sea Drilling Project (DSDP) 
sites from Goban Spur in the Cenomanian-Turonian 
interval, although hiatuses across OAE 2 hampered 
the reconstruction of  detailed size variations in the 
CTBI. However, slightly smaller Biscutum specimens 
were observed in the lower Turonian compared to 
the upper Cenomanian interval, while no significant 
changes in size were detected for genus Watznaueria.

Sections from various oceanic basins were se-
lected on the basis of  their stratigraphic character-
ization, ensuring relatively high resolution and cor-
relation at supra-regional scale. The main objectives 
of  this study are: i) the assessment of  size variations 
of  B. constans, D. rotatorius, W. barnesiae and Z. erectus 
across OAE 2; ii) the evaluation of  timing and type 
of  reactions of  phytoplankton calcification through 
progressively stressing conditions and their demise; 
iii) the identification of  global, regional and local 
response to paleoenvironmental perturbations; iv) 
the evaluation of  synchroneity or diachroneity of  
nannoplankton variations versus paleoenvironmen-
tal changes; v) implementation of  paleoecological 
reconstructions of  abiotic and biotic parameters 

influencing coccolith secretion across OAEs.  In 
particular, we want to test the following hypotheses: 
(1) did short-term fluctuations in coccolith mor-
phometry follow transient changes in climate and 
ocean chemistry across OAE 2?;  (2) did B. constans, 
D. rotatorius, W. barnesiae and Z. erectus respond to 
OAE 2 perturbations similarly to other OAEs?; (3) 
were single or concomitant paleoenvironmental 
factors influencing calcareous nannoplankton calci-
fication?; (4) were changes in coccolith size abrupt 
or gradual, especially at the onset and demise of  
OAE 2?; (5) were the paleolatitudes discriminating 
for coccolith size ?

LocatIon/studIed sectIons

We studied five stratigraphic sections cove-
ring the CTBI (Figs 1 and 2), including Eastbourne 
(East Sussex, England), Clot Chevalier (Vocontian 
Basin, France), Novara Di Sicilia (northeastern Si-
cily, Italy), Rock Canyon (Pueblo, Colorado, USA) 
and Cuba (northern-central Kansas, USA) sections 
from the WIS. These sections were chosen based 
on availability of  integrated stratigraphy granting a 
good time control derived from C-isotopic strati-
graphy and biostratigraphy.

Eastbourne is the thickest section covering 
the CTBI in the Anglo-Paris Basin (Gale 1995, 
1996; Gale et al. 1999; Paul et al. 1999). The stu-
died outcrop was sampled at Gun Gardens and 
consists of  a 27 m-thick section comprising th-
ree lithological units: Grey Chalk (rhythmically 
bedded marly chalk), Plenus Marls (greenish grey 
marls and clay-rich chalk) and White Chalk (coc-
colith and calcisphere-dominated nodular limesto-
ne). Samples analyzed were collected during the 
CT-Net Project and nannofossil biostratigraphy 
combined with chemostratigraphy was published 
in Tsikos et al. (2004): OAE 2 is constrained by 
the last occurrences of  Corollithion kennedyi and 
Axopodorhabdus albianus and the first occurrence of  
Quadrum gartneri at OAE 2 onset and end, respecti-
vely. These nannofossil events are consistent with 
more recent biostratigraphic data by Linnert et al. 
(2011).

The Novara di Sicilia section consists of  a 19 
m-thick stratigraphic interval measured through 
an olistolith within a melange of  the Argille Vari-
colori (Scopelliti et al. 2008). From a lithological 



Oceanic Anoxic Event 2 161

point of  view, the succession can be divided into 
three parts: a lower part with alternations of  thick 
marly limestone with light and dark marlstone, an 
intermediate portion with thinner light-colored 
strata and an upper part of  black shale alternating 
with dark marlstone and claystone. The nannofos-
sil and planktonic foraminiferal biostratigraphy, in-
tegrated with C-isotopic stratigraphy (Scopelliti et 
al. 2008) indicate that the Novara di Sicilia section 
contains only the lower part of  the Bonarelli Level 
equivalent and the underlying interval. Specifically, 
the outcrop ends shortly above δ13C

org
 peak B in-

dicating that only the onset and early part of  OAE 
2 are represented.

The Clot Chevalier section is located in the 
Vocontian Basin (southeastern France) that was 
a part of  the hemipelagic intrashelf  basin of  the 
European Tethyan passive margin (Wilpshaar et al. 
1997). The 35 m analyzed section consists of  an 
alternation of  dark grey marlstone and light grey 
limestones (Falzoni et al. 2016). The local equiva-
lent of  the “Bonarelli Level” in the Clot Cheva-
lier section is represented by the “Thomel Level”, 
which is characterized by laminated organic-rich 
sediments (from 3 to 31 meters from the base of  
the section) (Falzoni et al. 2016). At the base of  
Th1 unit, the presence of  a borrowed sharp sur-
face reveals the existence of  a hiatus in the lower 
part of  the section. Furthermore, within units Th1 
and Th2, a condensed stratigraphic level has been 
observed and interpreted as an interval of  very 
low sedimentation rate or sedimentation interrup-
tion. Nannofossil biostratigraphy was achieved by 
Russo (2014).

The Rock Canyon-Pueblo and the Cuba sec-
tions are both from the WIS where the Cenoma-

nian/Turonian boundary lies within the Bridge 
Creek Limestones Member of  the Greenhorn 
Formation. The Rock Canyon section is located in 
southern-central Colorado near Pueblo, along the 
Arkansas River; it was ratified as the global bound-
ary stratotype section and point (GSSP) for the 
base of  the Turonian Stage (Kennedy et al. 2005). 
Here, the Bridge Creek Limestones consist of  al-
ternating pelagic chalk and limestone and C

org
-rich 

beds (marlstone and calcareous shale), mainly bio-
turbated, with laminated and sublamintated units. 
The Rock Canyon section has been intensively 
investigated for litho-, bio-, chemo- stratigraphy 
and for paleoecological and paleoenvironmental 
reconstructions (Leckie 1985; Pratt 1985; Pratt et 
al. 1993; Bralower 1988; Kennedy 2000; Keller & 
Pardo 2004; Snow et al. 2005; Sageman et al. 2006; 
Corbett & Watkins 2013). The analyzed interval 
goes from 0.3 m to 10.2 m: samples from the pre-
OAE 2 interval were not available.

The Cuba section in northern-central Kan-
sas, is about 600 km East of  the Rock Canyon 
section. Equivalent strata around Cuba consist of  
more fine-grained calcareous to chalky shale within 
the Jetmore Chalk and Pfeifer Shale Members of  
the Greenhorn Formation. These two members 
are dominated by marlstone and calcareous shale 
(Bowman & Bralower 2005). At the Cuba section 
the stratigraphic control is based on integrated li-
tho-, chemo-, bio- stratigraphy (Hattin 1975, 1985; 
Bowman & Bralower 2005; Eleson & Bralower 
2005; Desmares et al. 2007; Corbett & Watkins 
2013; Corbett et al. 2014). The analyzed samples 
were previously investigated for chemo- and bio-
stratigraphy by Bowman & Bralower (2005) and 
Eleson & Bralower (2005).

CC

E

NdS

Western Tethys

WIS

proto 
North 

Atlantic

P

C

Caribbean 
Plateau

0

30°

30°

60°

60°

Fig. 1 - Paleo-location of  the studied 
sections at ~ 94 Ma (late Ce-
nomanian). E = Eastbourne, 
CC = Clot Chevalier, NdS = 
Novara di Sicilia, P = Pueblo 
and C = Cuba, WIS = We-
stern Interior Seaway. The 
paleo-map is from Du Vivier 
et al. (2014).



Faucher G., Erba E., Bottini C. & Gambacorta G.162

Methods 

Calcareous nannofossils were investigated in smear slides un-
der light polarizing microscope, at 1250X magnification. Smear slides 
were prepared using standard techniques (Bown & Young 1998) wi-
thout centrifuging and/or ultrasonic cleaning in order to retain the 
original sediment composition. A small fraction of  sediment was 
powdered in an agate mortar with bidistillate water; a few drops of  
the suspension were extracted with a pipette and spread over a slide, 
leaving to dry on a hot plate. The dried suspension was sealed on a 
glass slide with Norland Optical adhesive.

The nannofossil preservation was carefully assessed in or-
der to avoid diagenetically altered material. In fact, partial dissolution 
and/or overgrowth have the potential to artificially decrease or en-
large the coccolith size, respectively. This is particularly relevant for 
the delicate Biscutum, Zeugrhabdotus and Discorhabdus coccoliths that are 
diagenetic-prone (e.g. Thierstein 1980). Accurate screening of  pre-
servation was achieved under light polarizing microscope to ascertain 
the degree of  etching and/or overgrowth. Moreover, individual B. 
constans, Z. erectus, D. rotatorius and W. barnesiae coccoliths considered 
for morphometry were selected based on their complete and conti-
nuous outline and lack of  crimping due to etching or overgrowth. 
We also tested the potential control - and its degree - of  lithology 
on coccolith preservation, because marlstones normally contain the 
best preserved nannofossil assemblages, while coccoliths are often 
affected by overgrowth in limestones and by etching in carbonate-
poor lithotypes (Thierstein & Roth 1991).

Morphometric analyses were performed on a total of  53 
samples from Eastbourne, 37 from Clot Chevalier, 40 from Novara 
di Sicilia, 21 from Pueblo and 18 from Cuba sections. For each sam-
ple 30 specimens of  B. constans, Z. erectus and D. rotatorius and 50 speci-
mens of  W. barnesiae were digitally photographed in random fields of  
view. Samples containing less than 30 specimens of  selected species 
were not included in the analyses. Morphometry of  W. barnesiae was 
conducted with a lower sampling resolution.

Images of  coccolith specimens were taken using a camera 
mounted on a Leitz Laborlux light microscope. Length and width 
(the diameter for D. rotatorius) of  coccolith distal shield were mea-
sured on digital images using ImageJ64 software. A total of  4740 of  
B. constans, 4500 of  Z. erectus, 4770 of  D. rotatorius and 7500 of  W. 
barnesiae were measured. The error of  measurements is of  ± 0.08 µm.

Data were statistically elaborated, using R software, to obtain 
mean, median, maximum and minimum values, 25% and 75% per-
centile, 95% confidence intervals, standard deviations, Pearson cor-
relation coefficient (r) and the linear regression function. Moreover, 
the analyses of  variance (ANOVA) and Tukey post hoc tests were 
performed with R software in order to determine if  size variations 
are statistically significant.

resuLts

In all studied samples preservation is mod-
erate and only very minor indications of  etching 
and overgrowth were sporadically detected. Our 
diagenetic estimates are in agreement with evalua-
tion of  dissolution and overgrowth previously pub-
lished for nannofossil assemblages. In particular, at 
Pueblo, Bralower (1988) and Corbett et al. (2014) 
documented moderate preservation as assessed in 

this study. Similarly, Linnert et al. (2011) and Sco-
pelliti et al. (2008) observed moderately preserved 
assemblages at Eastbourne and Novara di Sicilia, 
respectively. Good to excellent preservation was 
documented for nannofloras of  the Cuba section 
(Eleson & Bralower 2005). 

Samples analyzed from the five sections ran-
domly consist of  various lithologies, all yielding 
very similar degree of  preservation and there is no 
correlation between coccolith size and carbonate 
content. Diagenetic modifications were certainly 
different for the studied sections were deposited at 
different paleo-water depths and in various geologi-
cal settings, under diverse sedimentation regimes. 
However, similar patterns in nannofossil assemblag-
es with coexistence of  delicate and robust species 
points to negligible diagenetic influence. Moreover, 
we underline that morphometric data were gathered 
only for complete specimens without signs of  cor-
rosion or overgrowth in the outline.

The adopted stratigraphic framework is based 
on the δ13C curve integrated with nannofossil bio-
stratigraphy (Fig. 2).  Specifically, peaks A, B and C 
of  δ13C curve (Pratt et al. 1985; Tsikos et al. 2004; Jar-
vis et al. 2006; Gambacorta et al. 2015) are taken as 
key-levels for dating and correlations. As discussed 
by Jarvis et al. (2006, 2011), peak A represents the 
acme of  the first shift towards δ13C positive values. 
It is followed by a trough and a subsequent increase 
culminating at δ13C peak B marking the onset of  the 
so-called plateau. The end of  the OAE 2 C-isotopic 
anomaly correlates with  δ13C peak C followed by 
the decrease back toward pre-excursion δ13C values 
(Tsikos et al. 2004). In the next sub-chapters, the 
size fluctuations of  B. constans, Z. erectus, D. rotatorius 
and W. barnesiae coccoliths are presented for every 
section (Fig. 3, Supplementary Tab. 1). Since the 
correlation of  length and width of  B. constans, Z. 
erectus and W. barnesiae coccoliths evidences a high 
Pearson correlation coefficient (Supplementary Fig. 
S1, S2, S3), only the length is plotted and used for 
tracing size changes.

Eastbourne
Coccoliths of B. constans, Z. erectus and D. ro-

tatorius show similar size trends through the East-
bourne section (Fig. 3a). Specifically, at the OAE 2 
onset, B. constans, Z. erectus and D. rotatorius evidence 
a decrease in size becoming smaller than the mean 
values (blue line). Subsequently, a slight increase 



Oceanic Anoxic Event 2 163

in coccolith size is detected and higher values are 
reached across δ13C peak A. Successively, cocco-
liths display a reduction in size reaching minimum 
values around δ13C peak B. In the uppermost part 
of  the section, coccoliths evidence an increase in 
size becoming slightly larger than the mean size. W. 
barnesiae is rather constant through the event (see 
Supplementary Tab. 1), although a minor increase in 
size is observed in the interval between δ13C peaks 
C and D (Fig. 3a). 

Clot Chevalier
In the Clot Chevalier section, the interval pre-

ceding OAE 2 is rather thin and only a few samples 
were available for the analyses. Size trends are well 
expressed in B. constans and D. rotatorius (Fig. 3b). 
From the base, B. constans and D. rotatorius show 
a relative increase in size compared to the mean 
length-diameter. B. constans and D. rotatorius main-
tain bigger sizes in the lowermost part of  OAE 2 
and then sizes progressively decrease just after δ13C 
peak A, reaching relative minimum values around  
δ13C peak B. B. constans displays values close to aver-
age in the upper part of  δ13C plateau up to peak C 
where, along with D. rotatorius, there’s a minor in-
crease in size. Size fluctuations are less evident in Z. 

erectus and W. barnesiae that do not show significant 
trends through the event. However, Z. erectus shows 
a minor increase in size just after δ13C peak C. 

Novara di Sicilia
In the Novara di Sicilia section, only the pre-

OAE 2 interval and the first part of  the event are 
represented (Fig. 3c). In the pre-OAE 2 interval size 
values of  B. constans, Z. erectus and D. rotatorius are 
erratic (Fig. 3c) with successive increases and de-
creases in size trends. In the first part of  OAE 2, 
after a basal interval barren of  calcareous nanno-
fossils, B. constans shows coccoliths larger than the 
mean size and subsequently a trend towards smaller 
coccoliths, followed by a recovery in size around 
δ13C peak A. A final size decrease ends with a rela-
tive minimum around δ13C peak B.

Z. erectus and D. rotatorius coccoliths display er-
ratic values through OAE  2 and W. barnesiae speci-
mens show values around average through the stud-
ied interval. 

Cuba
In the lowermost portion of  this section, 

only a few samples were available to characterize the 
pre-OAE 2 interval (Fig. 3d). Maximum coccolith 

C
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B

C

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C

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C
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Fig. 2 - Stratigraphic ranges of  the 
studied sections through the 
late Cenomanian-early Turo-
nian time interval. Nanno-
fossil zonations discussed in 
Gambacorta et al. (2015). 1 
= Sissingh (1977); 2 = Bur-
nett (1998), 3 = Gambacorta 
et al. (2015).



Faucher G., Erba E., Bottini C. & Gambacorta G.164

Fig. 3 - Variations of B. constans, Z. erectus and W. barnesiae length, and D. rotatorius diameter against  δ13C curve during OAE 2 at Eastbourne, 
Clot Chevalier, Novara di Sicilia, Pueblo Rock Canyon and Cuba. δ13C and nannofossil zones at Eastbourne after Tsikos et al. 
(2004); Clot Chevalier  δ13C curve after Falzoni et al. (2016), nannofossil zones after Russo (2014); δ13C and nannofossil zones at 
Novara di Sicilia after Scopelliti et al. (2008); δ13C at Pueblo Rock Canyon after Snow et al. (2005), nannofossil zones after Russo 
(2014); Cuba δ13C after Bowman and Bralower (2005), nannofossil zones after Eleson and Bralower (2005) integrated following 
Gambacorta et al. (2015). 

62
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6a

6b
U

C
7

5a
N

C
 1

3*
*

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C

 1
2*

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16
m

δ13Ccarb δ13Corg

8

9

10

11

12

13

14

15

Tu
ro

ni
an

 C
en

om
an

ia
n

-2 4

A

B
C

-23-29

N
C

 1
1

O
A

E
 2

Diameter μm1.5 4.0 Length μm
B. constans Z. erectus D. rotatorius W. barnesiae

6.0 4.5

6.06.0

4.5

4.5

4.5

6.0

6.0

6.0 2.0 4.51.5

1.5

1.5

1.5

1.5

2.0

2.0

2.0

2.0

L
ith

o
lo

g
ic

a
l 

u
n

its

1.5 4.0

1.5 4.0

1.5 4.0

1.5 4.0

2.0 9.0

2.0 9.0

2.0 9.0

2.0 9.0

2.0 9.0

'

Length μmLength μm

±1 standard deviation sample mean length

total mean length

pre-OAE mean length

 95% confidence interval

O
A

E
 2

O
A

E
 2

O
A

E
 2

O
A

E
 2

Barren Interval 



Oceanic Anoxic Event 2 165

values of  B. constans are observed around δ13C peak 
A followed by a decrease in size reaching minimum 
values around δ13C peak B. In the upper part of  the 
section, above δ13C peak C, an increase in coccoliths 
is observed with values similar to the mean.

 Coccoliths of  D. rotatorius display a well-de-
fined size peak at the onset of  OAE 2 around δ13C 
peak A, whereas Z. erectus dimensions are very simi-
lar to the mean size values with a gradual increase 
towards larger coccoliths recorded after δ13C peak 
C. W. barnesiae doesn’t show significant size changes, 
although an increase was observed in the lower part 
of  OAE 2. 

Pueblo 
In the lowermost part of  OAE 2 at Pueblo, 

an increase in size is observed in B. constans and D. 
rotatorius showing larger coccoliths around δ13C peak 
A (Fig. 3e). Both B. constans and D. rotatorius display 
a decrease in size, reaching minimum values around  
δ13C peak B and remaining small through the upper 
part of  OAE 2 and overlying interval. A return to 
larger coccoliths was recorded after δ13C peak D.  Z. 
erectus and W. barnesiae show minor changes in size; 
however, smaller coccoliths of  Z. erectus were ob-
served at the end of  the isotopic plateau and a slight 
decrease in size of  W. barnesiae specimens correlates 
with δ13C peak B.

Coccolith morphometry 
Among analyzed species, B. constans shows 

distinct and coeval size fluctuations through OAE 
2 in all studied sections, while D. rotatorius, Z. erec-
tus and W. barnesiae, record only minor and isola-
ted size variations at different stratigraphic levels. 
Mean length of  B. constans (Supplementary Tab. 1) 
varies depending on latitude: coccoliths are bigger 
at highest latitude (i.e. Eastbourne) and progressi-
vely decrease southwards, reaching minimum values 
at lowest latitude sections (i.e. Novara di Sicilia). 
Within the studied sections, the main size features 
of  B. constans can be summarized as follow: 

larger coccoliths characterize the pre-OAE 2 
interval;

a minor decrease in size correlates with the 
onset of  OAE 2; 

an increase in size trend reaches a maximum 
around δ13C peak A;

a decrease in size trends culminates with 
dwarf  coccoliths at δ13C peak B;

a relative recovery in size marks the post – 
OAE 2 interval, although without reaching pre-
event sizes.

The ANOVA and Tukey post hoc test were 
applied to coccolith morphometric data in order 
to evaluate if  B. constans means are significantly dif-
ferent in the ten intervals identified within the δ13C 
curve (Supplementary Tab. 2, Fig. S4): 1) pre-pos-
itive excursion; 2) initial rise; 3) peak A; 4) trough 
between peak A and peak B; 5) peak B; 6) plateau; 7) 
peak C; 8) decreasing values after peak C; 9) peak D; 
10) further decrease after peak D. Statistical analyses 
evidence that, in every section, B. constans is always 
significantly smaller (p < 0.05, Supplementary Tab. 
2) in interval number 5 corresponding to δ13C peak 
B compared to interval number 1 (pre-OAE 2) and 
interval number 3 (δ13C peak A). 

dIscussIon

Calcareous nannoplankton calcification 
and OAE 2 perturbation

Morphometric and statistical analyses indicate 
consistent and significant changes in coccolith size 
of  B. constans in all studied sections. We exclude a 
diagenetic control since the investigated successions 
yield rather homogenous moderate preservation, 
belong to different settings and underwent diverse 
diagenetic paths. Measured coccoliths are complete 
with no evidence of  corrosion or overgrowth in the 
outline and the co-occurrence of  incoherent size 
variations in different taxa is further evidence for 
disregarding diagenetic modifications.

Our morphometric data highlight latitude-re-
lated changes in B. constans size, being its coccoliths 
bigger at highest latitude (Eastbourne section) and 
progressively smaller southwards, with minimum 
values at lowest latitude (Novara di Sicilia section). 
Such findings are consistent with patterns observed 
in Cenozoic (Herrmann & Thierstein 2012) and 
Holocene (Herrmann et al. 2012) assemblages in-
dicating changes in coccolith size across latitudes.

In order to understand the role of  complex 
environmental stress of  OAE 2 on B. constans size 
variations, we first take under consideration the 
multiproxy data available for the WIS and East-
bourne sections (Fig. 4). The record of  pCO

2
 con-

centrations derived from stomata in fossil leaves 



Faucher G., Erba E., Bottini C. & Gambacorta G.166

of  the WIS area is limited to the first part of  the 
C-isotopic anomaly (Barclay et al. 2010) associated 
with a long-term increase in pCO

2 
interrupted by 

two relative lows. It was hypothesized that volcanic 
activity started to influence atmospheric CO

2
 levels 

before the OAE 2 onset (Fig. 4a; Barclay et al. 2010): 
an increase by 20%, equivalent to a rise of  60-300 
ppm, was attributed to a massive magmatic episode 
occurring some 500 kyrs in advance of  the positive 
C-isotopic excursion that defines OAE 2 (Barclay et 
al. 2010). A distinct low in atmospheric CO

2
 of  about 

25-26% (Barclay et al. 2010; Sinninghe Damstè et al. 
2008) was documented at the stratigraphic level of  
δ13 C peak A, followed by a further increase up to the 
middle part of  OAE 2 (Barclay et al. 2010). 

Osmium isotopic signature moves towards less 
radiogenic values approximately 30-40 kyrs before 
OAE 2 onset and was attributed to an input of  unra-
diogenic Os from a mantle source, thus suggestive of  
an intense submarine volcanism continuing through 
the first phase of  OAE 2 (Du Vivier et al. 2014).

In the Pueblo section, Snow et al. (2005) 
documented a first relative increase and then a peak 
in trace metals at the onset of  OAE 2 and at δ13C 
peak B, respectively (Fig. 4a). The presence of  these 
metal abundance anomalies needs an explanation 
other than influx of  terrigenous input and the most 
reliable hypothesis is the release of  magmatic fluids 
in event plumes (Snow et al. 2005). The metal-rich 
intervals are more abundant in the less volatile and 
more reactive elements (such as Sc, Co, Mn and Fe) 
and this is in good agreement with the position of  
the Caribbean Plateau, which was proximal to the 
WIS area. Cuba and Pueblo sections are, as expected, 
rich in a wide range of  near-field and far-field ele-
ments. In the Eastbourne section, a relative increase 
in chromium (Cr/Al) was documented at the onset 
of  OAE 2 (Fig. 4b) and a maximum precedes δ13C 
peak B (Pearce et al. 2009). Shape and stratigraphic 
levels of  both Cr enrichments at Eastbourne and 
Pueblo point to the Caribbean hydrothermal events 
(Pearce et al. 2009) associated with OAE 2.

a

B

A

Tu
ro

ni
an

C
en

om
an

ia
n

-2
00

δ13C

C

D
ep

th
 (c

m
 a

bo
ve

 b
as

e)

m 80
0

60
0

40
0

20
0

0

N
C

11
N

C
12

a*
NC

12
b*

*
Q

. g
ar

tn
er

i
R.

 a
sp

er
H

. c
hi

as
tia

S.
g

N
.j.

W
.d

V
.b

P.f

M
. m

os
by

en
se

M
. n

od
os

oi
de

s

-28

10
00

δ13Corg

Pratt et al., 1993

cm

5.52.0
B. constans

μm-22
δ44Ca

Bralower al., 2003 
unpublishised data.

Pratt et al., 1993

O
A

E
 2

Trace Metals

Element/Zr

0 9

Laurus nobilis

Hypodaphnis zenkeri

95% CI

95% CI

pCO2 

ppmv ppmv0 400 

pCO2 calibration pCO2 

400

0.0 1.0
(187Os/188Os)initial

-1.6 -1.3

Co/Zr x10
Cu/Zr x 2
W/Zr x100

800

b -5 -2

-5 -2
δ

18O

Plenus 
Cold 
Event

Thermal 
Maximum

T
u

ro
n

ia
n

C
e

n
o

m
a

n
ia

n

Q
. g

.
R

. c
.

A
.a

.

W
. d

.
M

. g
.

C
. g

.
N

C
11

*
N

C
12

**
N

C
13

**F
. c

.
N

. j
.

2.0 5.5
B. constans length

0 0.45
δ44Ca

m

10

15

20

25

-24-27
δ

13Corg(‰ VPDB)

Holywell Event

28 29
Δ

13C(‰VPDB)

A

B

C
D

δ13Ccarb 62

0 40 0 28

Biscutum 
spp. %

Productivity 
index

Watnaueria 
spp. %

0 2.2 0.5 1.5

Cr/Al (mM/M)

Onset of Caribbean
Volcanism

O
A

E
 2

Fig. 4 - Synthesis of  major geological events in the late Cenomanian – early Turonian interval a) WIS δ13C curve (Snow et al. 2005); pCO
2
 recon-

struction (Barclay et al. 2010); trace metals (Snow et al. 2005); osmium-isotope signature (Du Vivier et al. 2014); calcium-isotope signa-
ture (Du Vivier et al. 2015); composite B. constans morphometric curve (this study): pre-OAE 2 interval data from Cuba section, OAE 
2 and post OAE 2 interval from Pueblo Rock Canyon; b) Eastbourne section δ13C curve (Tsikos et al. 2004) and  δ13C curve (Jarvis 
et al. 2011); δ18O (Tsikos et al. 2004), cooler pulses during Plenus Cold Event (Jenkyns et al. 2016); relative abundance of  Watznaueria, 
Biscutum and productivity index (Linnert et al. 2011); Cr/Al (Pearce et al. 2009); calcium-isotope signature (circle = δ44/42Ca, Blättler et 
al. 2013; diamonds = δ44/42Ca Du Viver et al. 2015); B. constans morphometric curve (this study).



Oceanic Anoxic Event 2 167

At Eastbourne, temperature fluctuations 
were reconstructed using the O-isotopic record 
(Pearce et al. 2009; Jarvis et al. 2011): a relative 
warming correlates with the onset of  OAE 2 and 
is interrupted by the Plenus Cold Event (Fig. 4b) 
associated with a temporary spread southwards of  
North boreal biota (including the index belemnite 
Praectinocamax plenus) (Pearce et al. 2009; Jarvis et al. 
2011; Jenkyns et al. 2016). The middle-late part of  
OAE 2 is then characterized by increased paleotem-
perature culminating with the “early Turonian ther-
mal maximum” just after δ13C peak D (Jarvis et al. 
2011). A shift towards lower δ44Ca and δ7Li values 
indicates accelerated weathering at the beginning of  
the OAE 2 C-isotopic anomaly (Blättler et al. 2011; 
Pogge von Stradmann et al. 2013), reaching a maxi-
mum around  δ13C peak B, some 200-300 kyrs after 
the volcanism onset (Pogge von Stradmann et al. 
2013).

At Eastbourne and in the WIS areas, Du 
Vivier et al. (2015) documented a transient increase 
of  δ44Ca at the beginning of  δ13C anomaly: CO

2
-

induced ocean acidification during the Caribbean 
LIP eruption was proposed as the potential cause 
of  such δ44Ca positive shifts (Du Vivier et al. 2015).

Previous studies of  nannofossil assemblages 
of  the Eastbourne (Linnert et al. 2011) (Fig. 4b) and 
WIS (Corbett & Watkins 2013) sections showed par-
tially contrasting data. Yet, a general picture of  sup-
pressed abundances of  the fertility-taxa B. constans 
and Z. erectus was derived for mid-latitude shelf  and 
epeiric settings through OAE 2 (Corbett & Watkins 
2013). However, in the Cuba section, an increase of  
the higher-fertility nannofossil species was detected, 
suggesting local meso- to eutrophic conditions in 
the eastern margin of  the WIS (Corbett & Watkins 
2013). Paleoenvironmental perturbations in the 
CTBI reconstructed at Eastbourne and in the WIS 
are consistent with results gathered in other sec-
tions and used for global characterization of  OAE 
2 (Jenkyns 2010) in terms of  paleoCO

2
 fluctuations, 

climate moving to global warming, enhanced pri-
mary productivity due to increased nutrient fluxes 
and upwelling as well as ocean acidification. 

Our nannofossil morphometric data may 
provide insights into the comprehension of  type 
and rate of  reactions of  phytoplankton calcification 
through progressively stressing conditions and their 
demise. 

We notice that short-term fluctuations in 

morphometry follow transient changes in climate 
and ocean chemistry. In particular, the reconstruct-
ed early increase in pCO

2
 shortly prior to and at the 

beginning of  OAE 2, associated with initial volca-
nism, correlates with the first decrease in size of  
B. constans coccoliths (Fig. 4 and Supplementary Fig. 
S4). A short-lived return to relatively larger cocco-
liths falls around  δ13C peak A, in the interval of  the 
Plenus Cold Event and reconstructed lower pCO

2
. 

The subsequent decrease in B. constans size 
culminating in dwarfism across δ13C peak B (Fig. 
4 and Supplementary Fig. S4) correlates with met-
al enrichments and a significant temperature rise. 
Only a partial return to pre-OAE 2 sizes was ob-
served in B. constans coccoliths after δ13C peak D, 
suggesting the persistence of  stressing conditions 
in the earliest Turonian characterized by high paleo-
temperatures known as the “early Turonian thermal 
maximum” (Jarvis et al. 2011). 

As for living coccolithophores (Riebesell et al. 
2000; Beaufort et al. 2011; Müller et al. 2011, 2012; 
Hoffmann et al. 2012; Sett et al. 2014), the main 
paleoenvironmental factors influencing calcareous 
nannoplankton calcification in the Cretaceous were 
presumably nutrient availability, sea surface temper-
ature, carbonate chemistry, ocean acidification, toxic 
trace metals, competition with other organism and 
salinity (Erba 2004, 2006; Mutterlose et al. 2015). 
Linnert & Mutterlose (2012) highlighted a decrease 
in size of  Biscutum specimens during OAE 2 at oce-
anic sites from northeastern Atlantic Ocean. The 
associated decrease in abundance of  Biscutum sug-
gested that the reduction in size occurred under oli-
gotrophic conditions (Linnert & Mutterlose 2012). 
We found a similar relationship at Eastbourne and 
Pueblo (Figs 3, 5), but in the Cuba (Corbett & Wat-
kins 2013) and Novara di Sicilia (Scopelliti et al. 
2008) sections, the analogous decrease in B. constans 
coccolith size and dwarfism around δ13C peak B, oc-
curred under high nutrient availability (Scopelliti et 
al. 2008; Corbett & Watkins 2013). Therefore, the 
trophic level of  surface water cannot be ascribed as 
the trigger of  reduced calcification.

 A cool-water preference was implied for B. 
constans (Lees et al. 2005) and may explain the in-
crease in size of  B. constans coccoliths around δ13C 
peak A, during the Plenus Cold Event (Jenkyns et 
al. 2016) that is a global scale SST decrease of  about 
4°C (Voigt et al. 2004; Pearce et al. 2009). Con-
versely, the abundance and size decrease recorded 



Faucher G., Erba E., Bottini C. & Gambacorta G.168

in B. constans coccoliths at δ13C peak B are associ-
ated to a SST increase of  ~ 6°C (Voigt et al. 2004; 
Pearce et al. 2009). However, it is dubious that B. 
constans calcification was directly controlled by SSTs, 
since the full recovery in size started just after δ13C 
peak D under hot conditions of  the “early Turoni-
an thermal maximum”. Indeed, the preference of  
B. constans for cooler surface-waters was previously 
questioned (e.g., Linnert & Mutterlose 2012) and, 
indeed, we notice that B. constans was very abundant 
during OAE 2 in the tropical Atlantic (Hardas & 
Mutterlose 2007) characterized by SSTs up to 35°C 
and in the earliest Turonian under the highest SSTs 
(Forster et al. 2007) recorded in the Boreal area 
(Linnert et al. 2010, 2011). 

It is feasible that some acidification of  sea-
waters postulated for the early phase of  OAE 2 
(Du Viver et al. 2015), affected B. constans calcifica-
tion. As a matter of  fact, in the studied sections, 
B. constans coccolith size fluctuations mimic CO

2
 

reconstructions (Fig. 4): a decreasing size trend is 
observed in the interval with higher CO

2
 concen-

tration and, conversely, bigger coccoliths occur 
around δ13C peak A, where a ~25% reduction in 
CO

2
 was estimated (Barclay et al. 2010; Jarvis et al. 

2011). The subsequent reduction of  B. constans coc-
colith dimensions and dwarfism correlates with a 
further rise in pCO

2
 continuing through and after 

the late phase of  OAE 2 (Jarvis et al. 2011). As pre-
viously inferred for Mesozoic times (Erba 2006), in 
the CTBI there was arguably a causal link between 
levels of  CO

2
, marine carbonate chemistry and 

calcite secretion by nannoplankton: when pCO
2
 in 

the ocean-atmosphere system was minimum, pro-
duction of  larger coccoliths was favored by high 
CaCO

3
 saturation state. Vice versa, under high CO

2
 

concentration, a drop in carbonate saturation state 
induced production of  smaller (and less calcified) 
coccoliths.

In living coccolithophorids, calcification is 
ruled by an optimum curve; low inorganic carbon 
content reduces photosynthesis that indirectly lim-
its calcification due to a deficiency of  organic mol-
ecules needed to construct coccoliths (Krug et al. 
2010). Increased inorganic carbon substrate stimu-
lates photosynthesis and calcification reaching max-
imum values; excess CO

2 
release determines low pH 

that decreases calcification rates (Krug et al. 2010; 
Bach et al. 2015). The threshold values, below or 
above, which calcification becomes metabolically 

unfavorable differ among species due to a species-
specific sensitivity to pH conditions (Krug et al. 
2010; Bach et al. 2015). 

We are conscious that CO
2 
injections during 

OAE 2 occurred during a time interval much lon-
ger than modern anthropogenic releases, thus the 
reduction in carbonate saturation should have been 
buffered by shallowing of  the calcite compensation 
depth (CCD) with only a minor effect on surface 
water chemistry. However, the construction of  the 
Caribbean Plateau was sustained for 1-2 million 
years with several pulses of  CO

2
 releases and not 

as a single volcanic eruption. Possibly, as for OAE 
1a (Méhay et al. 2009; Erba et al. 2010, 2015) the 
sum of  subsequent large and geologically brief  CO

2
 

emission was responsible for major alteration of  the 
ocean-atmosphere system.

Submarine volcanism of  the Caribbean Pla-
teau LIP introduced high concentrations of  bio-
limiting metals during OAE 2 (Snow et al. 2005) 
that possibly resulted in ocean fertilization and/or 
poisoning by toxic metals (Leckie et al. 2002; Erba 
2004) perhaps influencing coccolith calcification 
as observed on single modern coccolithophorid 
species intolerant to cadmium and copper (Brand 
1994). We speculate that B. constans was sensitive to 
metal toxicity as previously hypothesized by Erba 
(2004). Our morphometric results show that this ta-
xon was most receptive, while Z. erectus, D. rotatorius 
and W. barnesiae were more tolerant. The metal pe-
aks detected at Pueblo (Snow et al. 2005), and No-
vara di Sicilia (Duncan et al. 2013) are coeval with 
reduction and dwarfism of  B. constans coccoliths, 
remaining small after the metal enrichment around  
δ13C peak B through the earliest Turonian. Thus, 
high metal abundances were possibly a concurring 
even if  not necessarily the prime factor controlling 
B. constans calcification. 

Summarizing, in the CTBI, nutrient availa-
bility in surface waters per se does not seem to be 
crucial for coccolith calcification because B. constans 
evidence coeval size reductions in the analyzed 
sections where different trophic levels were recon-
structed. Fluctuations in paleotemperatures might 
be partly responsible for B. constans coccolith sizes 
across OAE 2, with reduced coccolith size under 
warmer conditions and vice versa, although this 
correlation does not hold in the aftermath of  OAE 
2. Morphometric data suggest that ocean chemi-
stry related to the amount of  carbon dioxide and/



Oceanic Anoxic Event 2 169

or large quantities of  toxic metals played a central 
role at species-specific level and particularly in B. 
constans coccolith size. However, excess CO

2
 in the 

ocean-atmosphere system was seemingly linked to 
volcanically-induced warming as well as metal ferti-
lization via hydrothermal plumes during (pulses) of  
submarine plateau construction.

Comparison among Cretaceous OAEs re-
cords 

Previous studies performed across other 
OAEs highlighted size variations of  selected nan-
nofossil species. During the Cretaceous, W. barne-
siae was a cosmopolitan species, common in tropical 
and subtropical regions and dominant especially in 
oceanic gyres. It is described as a r-selected oppor-
tunistic species (Hardas & Mutterlose 2007) or used 
as a low productivity indicator (Roth & Krumbach 
1986; Erba et al. 1992; Erba 1992, 2004). The data 
from the early Aptian OAE 1a (Erba et al. 2010; 
Lübke & Mutterlose 2016), latest Albian OAE 1d 
(Bornemann & Mutterlose 2006) and OAE 2 (Lin-
nert & Mutterlose 2012; this study) are showing 
that W. barnesiae remains statistically steady in size. 
However, during OAE 1a, several coccoliths of  W. 
barnesiae were affected by some malformation evi-

denced by strong ellipticity and asymmetry in the 
interval of  most extreme paleoenvironmental stress 
(Erba et al. 2010). Instead, in all studied sections, 
no signs of  stronger ellipticity or asymmetry were 
found for the OAE 2 interval. The very little varia-
bility measured in W. barnesiae specimens in both 
OAE 1a (Erba et al. 2010; Lübke & Mutterlose 
2016) and OAE 2 (Linnert & Mutterlose 2012; this 
study) possibly suggests that this taxon was most 
adaptable and only marginally affected by the pa-
leoenvironmental perturbations characterizing Cre-
taceous OAEs.

During both OAE 1a and OAE 2, B. con-
stans appears to be the most sensitive species to the 
environmental perturbation. The morphometric 
analyses conducted on B. constans and Z. erectus across 
OAE 1a in the Tethys and Pacific Oceans (Erba et 
al. 2010) as well as in the North Sea and Lower Sa-
xony Basin (Lübke & Mutterlose 2016) highlighted 
size reduction of  their coccoliths during the early 
stage of  OAE 1a in the core of  the negative carbon 
isotope excursion. Contrarily to OAE 2, B. constans 
sizes are smaller in average at higher latitudes (Lüb-
ke et al. 2015; Lübke & Mutterlose 2016) compared 
to lower latitudes (Erba et al. 2010). However, the 
drastic size decrease of  B. constans is coeval at high 

Median25%
75%

Min.

Max.

Pre OAE Post OAE δ13 C peak B interval

average length Alstӓtte1
average length North Jens-1

average length Adda - 2

Cismon core

DSPD 463

Novara di Sicilia

Clot Chevalier

Eastbourne

Cuba
Pueblo

Pre OAE Post OAEOAE 1a

7

2

B
. c

on
st

an
s 

le
ng

th

Fig. 5 - Box plots of  B. constans length across OAE 1a and OAE 2. Data for OAE 1a are from the Cismon core and DSDP Site 463 (Erba et 
al. 2010). The average length of  B. constans across OAE 1a are from Adda-2, Alstätte1 and North Jens-1 cores (Lübke & Mutterlose 
2016); data for OAE 2 are from Eastbourne, Clot Chevalier, Novara di Sicilia, Pueblo and Cuba sections. Intervals pre-OAE, OAE 1a, 
δ13C peak B, post-OAE, are based on δ13 C stratigraphy.



Faucher G., Erba E., Bottini C. & Gambacorta G.170

and low latitudes and occurred in the core of  the 
negative carbon-isotope interval (carbon isotope 
segment C3) (Erba et al. 2010; Lübke & Mutterlo-
se 2016) reaching comparable minimum B. constans 
coccolith size. The amplitude of  size reductions du-
ring the earliest phase of  OAE 1a is significantly 
different at lower and higher latitudes, of  the order 
of  ~30% versus ~17%, respectively, relative to the 
interval preceding OAE 1a.

In Fig. 5 the size measurements of  B. constans 
across OAE 1a (Erba et al. 2010; Lübke & Mutter-
lose 2016) and OAE 2 (this study) are compared. 
B. constans display very similar variations in both 
events, with a drastic decrease during OAEs. A size 
decrease of  B. constans coccoliths by 15 % on avera-
ge, occurred during OAE 2. 

The size reduction of  B. constans coccoliths 
during OAE 1d was ascribed to cooler surface-wa-
ters as indicated by nannofossil-based temperature 
(Bornemann & Mutterlose 2006). Such temperature 
influence, however, contradict the conclusions of  
Linnert & Mutterlose (2012) who observed smaller 
Biscutum coccoliths in the lower Turonian interval 
characterized by very warm surface temperature. 
Additionally, during OAE 1a dwarfism occurred 
in the core of  the negative carbon-isotope inter-
val where the highest temperature is reconstructed. 
Therefore, we do not see a correspondence betwe-
en lower temperature and smaller size, but possibly 
the opposite correlation (Fig. 4). 

The potential influence of  nutrient availabil-
ity on coccolith size, discussed for OAE 1a (Erba et 
al. 2010, 2011; Lübke et al. 2015) and OAE 1d (Bor-
nemann & Mutterlose 2006) was documented by 
general smaller sizes under enhanced fertility. This 
interpretation is in contrast with the reconstruction 
by Linnert & Mutterlose (2012) who found larger 
Biscutum coccoliths associated with higher nutrient 
concentrations in the CTBI. Nutrient availability of  
surface waters was considered by Corbett & Wat-
kins (2013) to explain changes in nannofossil as-
semblages across OAE 2 in the WIS. Indeed, the 
Cuba and Pueblo sections were analyzed and pa-
leoceanographic reconstructions suggest opposite 
conditions dominated by oligotrophy and eutrophy 
for the Pueblo and Cuba sections, respectively, dur-
ing OAE 2. Our data (Fig. 3d, e) document very 
similar sizes for B. constans coccoliths at these two 
locations and, thus, we infer that fertility was not the 
primary cause of  coccolith size control. Although 

OAE 1a was also a time of  ocean eutrophication 
(Erba 1994, 2004; Bottini et al. 2015), the time in-
terval of  dwarfism corresponds to the climax in the 
volcanic activity of  the Ontong Java Plateau as indi-
cated by Os-isotope (Tejada et al. 2009; Bottini et al. 
2012), maximum in CO

2
 (Méhay et al. 2009), trace 

metal concentrations (Erba et al. 2015) and maxi-
mum warming (Ando et al. 2008; Bottini et al. 2015) 
but not to the highest fertility (Bottini et al. 2015). 

High run-off  due to intensified continental 
weathering was supposed to have introduced more 
clastic particles and fresh waters into the sea: muddy 
and restricted photic zone reduced the availability 
of  light favoring the dominance of  small specimens 
at a regional scale (Lübke & Mutterlose 2016). How-
ever, the coeval reduction in sizes at both higher 
and lower latitudes and at highly diverse oceanic set-
tings during OAE 1a - and specifically in the carbon 
isotope segment C3 - contradict such interpretation 
and unambiguously evidences a global paleoenvi-
ronmental drive for synchronous coccolith dwarf-
ism of  B. constans.

 The data collected by Erba et al. (2010) and 
Lübke & Mutterlose (2016) indicate that minimum 
coccolith size corresponds to most extreme pertur-
bations as recorded by δ13C negative spike in the 
early part of  OAE 1a. Excess CO

2
 concentrations 

related to the volcanic activity of  the Ontong Java 
Plateau remains the most plausible explanation for 
coccolith dwarfism in B. constans, Z. erectus and D. 
rotatorius, and some malformation in W. barnesiae 
(Erba et al. 2010). Such modifications in size and 
morphology were interpreted as the species-specific 
transient response to survive progressively increas-
ing surface-water acidification. It is clear that a com-
bination of  paleoclimatic and paleoceanographic 
triggers concurred in stressing the oceanic ecosys-
tem, but, as discussed by Erba et al. (2011), ocean 
acidification under excess volcanic CO

2
 seems to be 

the requisite or determinant of  species-specific size 
reduction and malformation during OAE 1a, be-
cause coccolith dwarfism has not been documented 
during other Cretaceous cases of  high fertility inde-
pendent from OAEs.

During OAE 2, reconstruction of  pCO
2
 from 

the stomatal index suggests an increase of  about 
600 ppm reaching values of  about 900-1000 ppm 
(Barclay et al. 2010). Pogge von Strandmann et al. 
(2013) calculated the amount of  CO

2
 sequestered 

from the continental weathering (~ 4-8 x 104 Gt 



Oceanic Anoxic Event 2 171

CO
2
) in agreement with previous calculation of  the 

amount of  CO
2
 emitted in the first phase of  con-

struction of  the Caribbean Plateau (7-12 x 104 Gt 
CO

2
) (Kuroda et al. 2007). It is therefore conceiv-

able that size reduction of B. constans coccoliths (Fig. 
4), reflects a progressive acidification of  surface-
waters induced by large emissions of  volcanic CO

2
. 

Proxy data (e.g. Erba & Tremolada 2004; Méhay 
et al. 2009) suggest that during OAE 1a CO

2
 was 

emitted in subsequent individual volcanic pulses 
reaching a concentration of  about 1000-2000 ppm. 
In both OAEs, thus, the occurrence of  B. constans 
dwarf  coccoliths correlates with excess CO

2
 sug-

gesting that concentrations above threshold values 
possibly become adverse for calcification of  sensi-
tive Cretaceous coccolithophore species, in analogy 
to results of  laboratory experiments (Riebesell et al. 
2000; Krug et al. 2011; Bach et al. 2012; Bach et 
al. 2015). Calcification must be a beneficial process 
for coccolithophore algae because this high energy-
consuming process remained stable in coccolitho-
phore evolution from its appearance in the Triassic 
(Young & Henriksen 2003). However, during the 
most extreme intervals such as OAEs, a decrease 
of  the pH might have favored other groups other 
than coccolithophore algae (Bach et al. 2015). Dur-
ing OAE 2, in fact, in the interval characterized by 
the major perturbation (δ13C peak B) the decrease in 
B. constans is paralleled by a strong increase in calci-
sphere percentages (Pearce et al. 2009). This can be 
interpreted as an inability of  B. constans to properly 
calcify and adapt to a new carbonate chemistry con-
ditions, facilitating the spread of  other more com-
petitive functional groups such as dinoflagellates.

One potential factor that may have affected 
coccolith calcification in addition to CO

2
-induced 

ocean acidification is the concentration of  toxic 
metals. Indeed, we notice that during both OAE 1a 
(Larson & Erba 1999; Erba et al. 2015) and OAE 
2 (Snow et al. 2005; Duncan et al. 2013) there were 
large injections of  trace metals associated with hy-
drothermal plumes during the construction of  sub-
marine LIPs (Neal et al. 2008). Abnormal quanti-
ties of  biolimiting but also toxic metals might have 
had positive and negative feedbacks in coccolith 
production and, particularly, on size of  B. constans 
coccoliths. Metal toxicity is known for living nan-
noplankton: cadmium can inhibit calcification and 
copper is not tolerated by some coccolithophore 
species (Brand 1994). As speculated by Erba (2004) 

perhaps, poisoning by toxic metals affected calcar-
eous nannoplankton in the Cretaceous, inducing 
some extinctions, abundance drop and species-spe-
cific coccolith dwarfism.

concLusIons

Morphometric analyses of  selected nannofos-
sil taxa across OAE 2 in various geological settings 
revealed differential species-specific patterns. Coc-
colith size variations of  D. rotatorius, W. barnesiae and 
Z. erectus result to be minimal and substantially unre-
lated to OAE 2 paleoenvironmental stresses. Con-
versely, B. constans coccolith morphometric analyses 
identified size variations coeval with specific phases 
of  environmental pressure. Size fluctuations across 
OAE 2 are similar and synchronous in all the ana-
lyzed sections located at great distance, in different 
oceans and settings. 

The quantitative characterization of cocco-
lith size and morphology in the intervals preceding, 
coeval and postdating OAE 2 assessed the occur-
rence of  a relationship between calcification of  B. 
constans and paleoenvironmental perturbations. In 
fact, during OAE 2, B. constans coccoliths show a 
general decrease in mean size followed by a partial 
recovery at the end of  the event, but dimensions 
remained smaller than in the interval preceding the 
main perturbation. At higher resolution, coeval de-
creases and increases in coccolith size correspond 
to individual paleoenvironmental changes across 
OAE 2.  We underline that B. constans dwarfism is 
observed in complete specimens with no corrosion 
in their outline and, therefore, cannot be explained 
as an artifact of  diagenesis.

The comparison with morphometric data 
available for the early Aptian and latest Albian 
OAEs confirms that B. constans was most affected 
by stressing conditions and repeatedly underwent 
size reduction with evidence of  temporary dwarf-
ism. This suggests that presumably the same pa-
leoenvironmental factors (or the same combination 
of  ecosystem changes) controlled calcification of  
B. constans coccoliths during OAE 1a, OAE 1d and 
OAE 2. However, the amplitude of  B. constans coc-
colith reduction is different for OAE 1a and OAE 
2, being larger for the former event.

Z. erectus and D. rotatorius display a less-ex-
pressed decrease in size during OAE 1a and insig-



Faucher G., Erba E., Bottini C. & Gambacorta G.172

nificant or scattered changes across OAE 2; dwarf-
ism of  these taxa was detected only in the interval 
of  climax perturbation during the early Aptian 
Selli Event. The very little variability measured in 
W. barnesiae size indicate that this taxon was most 
adaptable and only marginally affected by the pa-
leoenvironmental stress characterizing Cretaceous 
OAEs: while pronounced ellipticity was taken as 
evidence of  malformation of  W. barnesiae cocco-
liths during OAE 1a, negligible variations in elliptic-
ity were observed across OAE 2, perhaps because 
of  an attenuated degrees of  perturbation.

Our results reinforce and implement paleo-
ecological reconstructions of  abiotic and biotic 
parameters somehow influencing coccolith secre-
tion across OAE 2, OAE 1d and OAE 1a allow-
ing the evaluation of  the factor, or combination of  
factors, inducing B. constans coccolith dwarfism in 
subsequent episodes of  paleoenvironmental per-
turbation. Temperature and nutrient availability in 
surface waters do not seem to have been decisive 
for B. constans coccolith size, but ocean chemistry 
related to the amount of  CO

2
 concentrations and 

carbonate saturation state, played a central role in 
coccolith production by B. constans with a repetitive 
reduction in size. Species-specific coccolith dwarf-
ism seems to be the response of  nannoplankton to 
ocean acidification during both OAE 1a and OAE 
2 to survive lower pH. 

Massive emissions of  volcanic CO
2
 during 

the Caribbean Plateau construction across OAE 2 
(Neal et al. 2008) arguably induced ocean acidifica-
tion that was detrimental to some calcareous nan-
noplankton species, with temporary production of  
dwarf  B. constans coccoliths. Hydrothermal plumes 
introduced biolimiting metals that fertilized the 
global ocean, but also pumped in toxic metals that 
might have disturbed the functioning of  some in-
tolerant species, thus affecting their biocalcification. 

Comparison of  our results with data available 
for OAE 1a and OAE 1d indicate that analogous 
causes have induced similar response at different 
times in the Cretaceous. The OAEs indicate that 
past oceanic perturbations were severe and that the 
species-specific production of  dwarf  coccoliths 
possibly represents adjustment of  some individual 
taxa to survive hostile ecosystems. This study fur-
ther suggests that B. constans was the mid-Cretaceous 
taxon most sensitive to ocean chemistry, while other 
species (Z. erectus, D. rotatorius and W. barnesiae) were 

affected only at highest degrees of  perturbation. 
It seems that calcareous nannoplankton have been 
resilient to pH changes, excess toxic metals, global 
warming and nutrification episodes, but it is cer-
tainly possible that the rate of  change was decisive 
for coccolithophore adaptation. The geological re-
cord indicates that, at wide spatial scale, calcareous 
nannoplankton could adjust to high pCO

2
, but past 

changes occurred over tens of  thousands of  years, 
giving enough time to adapt.

Acknowledgements. We thank Tim Bralower and Bob Duncan 
for sharing samples from the WIS sections, and Hugh Jenkyns for 
providing samples from the Clot Chevalier section. We thank the 
Editor, Isabella Raffi, and two anonymous reviewers for their valu-
able comments and suggestions on the manuscript. The research 
was funded through MIUR-PRIN 2011 (Ministero dell’Istruzione, 
dell’Università e della Ricerca–Progetti di Ricerca di Interesse Na-
zionale) to E. Erba, and through SIR-2014 (Ministero dell’Istruzio-
ne, dell’Università e della Ricerca–Scientific Independence of  young 
Researchers) to C. Bottini. G. Faucher was supported by Fondazione 
Fratelli Confalonieri. 

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