Palaeogeography, Palaeoclimatology, Palaeoecology 586 (2022) 110722

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Palaeogeography, Palaeoclimatology, Palaeoecology

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Deep-water paleoenvironmental changes based on early-middle Miocene

benthic foraminifera from Malta Island (Central Mediterranean)
Bianca Russo a, *, Luciana Ferraro b, Cecilia Correggia a, Ines Alberico b, Luca Maria Foresi c,
Mattia Vallefuoco b, Fabrizio Lirer b
a
Dipartimento di Scienze della Terra, dell’Ambiente e delle Risorse - DiSTAR, Università “Federico II”, Complesso Universitario di Monte Sant’Angelo (Edificio 10), Via
Vicinale Cupa Cintia, 21, 80126 Napoli, Italy
b
Istituto di Scienze Marine (ISMAR), CNR Napoli, Calata Porta di Massa, Porto di Napoli, 80133 Napoli, Italy
c
Dipartimento di Scienze Fisiche, della Terra e dell’Ambiente, Università degli Studi di Siena, Via Laterina 8, 53100 Siena, Italy

A R T I C L E I N F O A B S T R A C T

Editor: A Dickson A detailed quantitative, statistical and isotopic study on benthic foraminiferal assemblages from the upper
Burdigalian - lower Langhian of Malta Island (St. Peter’s Pool section) was carried out in order to gain more
Keywords: insights on paleoenvironmental changes that affected the central part of the Mediterranean Basin during the
Early-middle Miocene early-middle Miocene. The most abundant and/or palaecologically significant taxa were grouped into Group A
Benthic foraminifera
(oxic/oligotrophic and oxic/oligo-mesotrophic opportunistic behaving) and Group B (hypoxic/eutrophic) and,
Oxic and hypoxic taxa
on the base of their microhabitat in superficial microhabitat taxa (epifaunal + epifaunal to shallow infaunal
Oxygen and Carbon stable isotopes
Paleoecology taxa), intermediate microhabitat taxa (shallow infaunal + shallow to intermediate infaunal taxa) and deep
Malta microhabitat taxa (deep infaunal species). The changes in the structure of the benthic foraminiferal assemblages,
Central Mediterranean Basin together with isotopic data and statistical analysis results, identify five main intervals SPP1-SPP5, testifying the
evolution of bottom water conditions between 16.12 and 15.36 Ma, corresponding to warm climate conditions
due to the onset of the Miocene Climatic Optimum (MCO). The main benthic foraminiferal turnover occurred
between 16.01 and 15.91 Ma. It has been recorded in both the palaecological and geochemical data and can be
related to the Miller’s Mi2 cooling event. This turnover correlates to a sea level falling that we believe caused an
increase of the primary productivity due to runoff intensification. We suggest that the fluctuations of superficial
microhabitat oxic/oligo/oligo-mesotrophic Group A, opposite to those of intermediate and deep microhabitat
hypoxic/eutrophic Group B, and the occurrence of the superficial microhabitat, oxic/oligo-mesothrophic
opportunistic behaving species are indicative of increased seasonality, which in turn affect food flux and
oxygenation at the sea-floor. Moreover, the calculation of %P and the well-defined depth distribution range of
some significant species allowed us to estimate a middle bathyal paleodepth, ranging from 600 m to 1000 m for
the entire composite section.

1. Introduction
The global oceanographic system, from the Indo-Pacific to Atlantic
through the Tethys Ocean, was affected by a complex and dynamic
climatic history mostly due to ocean reorganization during the Late
Oligocene-Miocene time interval (Miller et al., 1991; Zachos et al., 2001,
2008).
The Miocene epoch (23.03–5.33 Ma) was a time interval of global
warmth, relative to today. Continental configurations and mountain
topography transitioned towards modern conditions, and many flora
and fauna evolved into the same taxa that exist today. Miocene climate
was dynamic: long periods of early and late glaciation bracketed a ~ 2
Myr greenhouse interval, the Miocene Climatic Optimum (MCO). Floras,
faunas, ice sheets, precipitation, pCO2, and ocean and atmospheric cir­
culation mostly (but not ubiquitously) covaried with these large changes
in climate. With higher temperatures and moderately higher pCO2
(~400–600 ppm), the MCO has been suggested as a particularly
appropriate analog for future climate scenarios, and for assessing the
predictive accuracy of numerical climate models, the same models that
are used to simulate future climate (Steinthorsdottir et al., 2021). The

* Corresponding author.
E-mail address: bianca.russo@unina.it (B. Russo).

https://doi.org/10.1016/j.palaeo.2021.110722
Received 23 January 2021; Received in revised form 7 October 2021; Accepted 15 October 2021
Available online 30 October 2021
0031-0182/© 2021 Elsevier B.V. All rights reserved.
B. Russo et al.
middle Miocene represents an important time interval for the climate
evolution (i.e., Shackleton and Kennett, 1975; Woodruff and Savin,
1989, 1991; Holbourn et al., 2005; Verducci et al., 2009), which grad­
ually moved from warm MCO, termed by the Middle Miocene Climate
Transition (MMCT), to cooler conditions due to major environmental
changes (Miller and Kent, 1987; Miller et al., 1991; Zachos et al., 2001),
mostly driven by orbital forcing (Holbourn et al., 2007, 2013b, 2015).
During this period, δ18O data on open ocean benthic foraminifera reveal
three prominent enrichments that reflect increased glaciation, known as
Mi2a, Mi3a and Mi3b Miller’s events (Miller et al., 1991). In particular,
the Mi3b event represents the most prominent δ18O excursion associated
with the major expansion of the East Antarctic Ice Sheet at ~13.8 Ma, in
the uppermost part of MMCT interval (Miller et al., 1991). In addition, a
long-lasting positive excursion in δ13C benthic signal (“Monterey
Excursion” between 17 and 13.5 Ma; Zachos et al., 2001) is documented
from Langhian deep ocean (i.e., Holbourn et al., 2007, 2013a,b, 2015
and reference therein) to shallow water Mediterranean records (Bran­
dano et al., 2021 and reference therein).
In terms of Miocene proto-Mediterranean, significant paleogeo­
graphic and paleoenvironmental changes interested this area. In
particular, the counter-clockwise rotation of Africa and Arabia caused a
collision with the Anatolian plate during the late Burdigalian. Then, in
the early-middle Miocene, the Indo-Pacific connection closed and the
Tethyan Seaway transformed in a series of semi-enclosed basins similar
to the present-day situation (Rögl and Steininger, 1983; Rehault et al.,
1985; Steininger et al., 1985; Woodruff and Savin, 1989; Ramsay et al.,
1998; Harzhauser et al., 2007; Karami et al., 2011; De La Vara and
Meijer, 2016).
According to this paleoclimatic and paleoceanographic framework,
the upper Burdigalian-Langhian St. Peter’s Pool section in Malta Island
(Foresi et al., 2011) is a key area to analyse the deep-water paleo­
environmental changes over the MCO interval. Moreover, using benthic
foraminifera and stable isotope signatures, δ18O excursion related to
Mi2a event will be identified for the first time.
Benthic foraminifera are useful tool to detect and monitor the
modern and past deep water-mass ocean circulation (e.g. Bernhard and
Sen Gupta, 1999; Jorissen, 1999; Loubere and Fariduddin, 1999; Kou­
wenhoven and van der Zwaan, 2006; Sarkar and Gupta, 2009; Mourik
et al., 2011; Eichler et al., 2016; Rathburn et al., 2018; Xue et al., 2019)
and relationship with chemical and physical features of deep water
masses was highlighted by several authors (e.g. Smart and Ramsay,
1995; Schmiedl et al., 1997; Yasuda, 1997; Bellanca et al., 2002; Spro­
vieri et al., 2004; Jorissen et al., 2007; Russo et al., 2007; Pérez-Asensio
et al., 2012). Benthic foraminifera are closely related to oxygen con­
centration in the bottom waters and in the sediment, as well as to the
organic matter input from the surface waters (e.g. Moodley and Hess,
1992; Sen Gupta and Machain-Castillo, 1993; Gooday, 1994; Kaiho,
1994; van der Zwaan et al., 1999; Sander Ernst and van der Zwaan,
2004; Murray, 2006; Pucci et al., 2009; Caulle et al., 2013, 2015; Drinia
et al., 2018).
Previous studies on Miocene benthic foraminiferal assemblages from
Maltese Archipelago were carried out by Bellanca et al. (2002) on Ras il-
Pellegrin section. The authors provide significant results obtained from
isotope and benthic foraminiferal data, suggesting a direct relationship
between surface and intermediate Mediterranean water masses during
the Langhian-Serravallian. Ostracods from the Langhian-Serravallian of
Ras il-Pellegrin composed section were studied by Bonaduce and Barra
(2002) to define changes in palaeoenvironmental conditions at the sea-
floor. Benthic foraminifera from St. Peter’s Pool section were roughly
analyzed by Foresi et al. (2011), in order to estimate the paleodepth of
the marine sedimentary record.
In this paper the benthic foraminifera together with Oxygen and
Carbon stable isotopes have been used as proxy to evaluate the main
palaeoecological changes of the bottom water masses occurred in the
proto-Mediterranean during the upper Burdigalian - lower Langhian.
The results obtained from the quantitative and statistical study of
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Palaeogeography, Palaeoclimatology, Palaeoecology 586 (2022) 110722
benthic foraminifera and of the benthic δ18OH. dutemplei and δ13CH. dutemplei
isotope records of the St. Peter’s Pool section (Malta Island, Central
Mediterranean) are presented.
2. Study area: The Maltese Archipelago
2.1. Geological setting
The Maltese Archipelago is located in the Central Mediterranean,
approximately 80 km South of Sicily and 320 km North of North Africa
(Fig. 1), close to the actual boundary between the Malta Platform and
the Pantelleria Rift (Finetti, 1982).
The archipelago extends for 45 km in a NW-SE direction and consists
of 3 main islands: Malta, Gozo and Comino (Fig. 1), and several small
uninhabited islets which include Cominotto, Filfola, St. Paul’s Islands,
Fungus Rock and few other minor rocks.
According to the geological literature (Hyde, 1955; Giannelli and
Salvatorini, 1972, 1975; Felix, 1973; Pedley, 1976, 1978; Pedley et al.,
1976, 1978; Mazzei, 1985; Föllmi et al., 2008; Foresi et al., 2008;
Gruszczynski et al., 2008; Baldassini et al., 2013; Foresi et al., 2014;
Baldassini and Di Stefano, 2017), the stratigraphy of the Maltese Ar­
chipelago has been exhaustively investigated thanks to the extensive
and well-exposed sedimentary successions. Sedimentary sequences
include five formations characterized by different lithological, sedi­
mentological and paleontological features: 1) the Lower Coralline
Limestone Formation (LCLf) - late Oligocene; 2) the Globigerina Lime­
stone Formation (GLf) - Chattian-Langhian, subdivided into three
members, the Lower (LGLm), Middle (MGLm) and Upper Globigerina
Limestone (UGLm) (Rizzo, 1932); 3) the Blue Clay Formation (BCf) -
Serravallian-Tortonian; 4) the Greensand Formation (GSf), early Mes­
sinian, and 5) the Upper Coralline Limestone Formation (UCLf) - pre-
evaporitic, early Messinian.
2.2. St. Peter’s pool section
The St. Peter’s Pool section outcrops on the eastern coast of the
Delimara Peninsula (Fig. 1) and is representative of the Upper Globi­
gerina Limestone member (Foresi et al., 2011).
The section is 31 m thick and lies on the C2 phosphate-rich bed
(Fig. 2).
The sedimentary record is characterized by a cyclic alternation of
calcareous marl, marly limestone and jutting bioturbated hardened
limestone. In the middle part of the section a thick dark-grey interval,
recognizable in the whole Delimara Peninsula, occurs between 10.2 and
11.9 m (Fig. 2). The lower part of the section, from the C2 phosphate-
rich bed to the dark-grey interval, consists of light beige coloured
rhythmic alternations of calcareous marl, marly limestone and dark
beige hardened limestone that are rich in echinoid rests, molluscs and
fossil tracks. Conversely, the upper part of the section, from the dark-
grey interval to the top, is characterized by a marked change in colour
from light beige to dark beige, which is associated to a progressive
decrease of the calcareous marl thickness and to an equivalent increase
in prominent hardened limestone. At 28.4 m, calcareous marl and marly
limestone change colour again and become whitish (Fig. 2). For a more
detailed description of the section, see Foresi et al. (2011).
The integrated bio-magnetostratigraphic study proposed by Foresi
et al. (2011) allowed the authors to attribute the section to the upper­
most Burdigalian to lower Langhian, spanning from planktonic forami­
nifera biozones MMi3 to MMi4c pp. (Foresi et al., 2011; Lirer et al.,
2019) and the calcareous nannofossil zones MNN4a to MNN5a (Foresi
et al., 2011) (Fig. 2). The age model for S. Peter’s Pool section bases on
calcareous plankton biovents by Foresi et al. (2011) and astronomical
ages proposed by Turco et al. (2017) in the La Vedova section (Conero
Area, Central Italy). The age-depth profile has been produced by linear
interpolation between the identified biostratigraphic tie-points (Fig. 2).
B. Russo et al.
Fig. 1. Location and geological map of the study area (modified from Foresi et al., 2011); geology of Delimara Peninsula from Oil Exploration Directorate (1993).
3. Material and methods
3.1. Sample preparation and classification of benthic foraminifera
A total of 135 samples for benthic foraminiferal analyses were
collected from the investigated section (Appendix A) and processed
using standard laboratory procedures. Specifically, they were dis­
aggregated in normal water, washed and sieved into two size fractions
(mesh sizes 63 μm and 125 μm). The fraction >125 μm was splitted by an
Otto microsplitter to obtain a representative fraction, containing
approximately 300 benthic foraminiferal specimens. All specimens were
picked out, identified at specific or supraspecific level, counted and
stored in Chapman slides. The taxonomic identification was based for
genera on Loeblich and Tappan (1964, 1988), and for species on Van
Morkhoven et al. (1986), Holbourn et al. (2013a). Some online data­
bases, such as Foraminifera.eu (https://foraminifera.eu/) and Worms
(https://www.marinespecies.org/; Hayward et al., 2018) have also been
used.
3.2. Ecological preferences of benthic foraminiferal taxa
According to Sgarrella et al. (2012) Recent deep-sea benthic fora­
minifera are dependent on food availability, in terms of productivity
exported to the sea floor, essential to meet their energy requirements
(Loubere and Fariduddin, 1999), and on oxygen bottom water content
(e.g. Corliss, 1985; Gooday, 1988, 1993; Herguera and Berger, 1991;
Barmawidjaja et al., 1992; Jorissen et al., 1995; Jorissen and Wittling,
1999; De Rijk et al., 2000; Schmiedl et al., 2000; Fontanier et al., 2002,
3
Palaeogeography, Palaeoclimatology, Palaeoecology 586 (2022) 110722
2003, 2006). Moreover there is a general consensus that oligotrophic
and highly oxygenated environments are relatively enriched in super­
ficially living taxa, whereas eutrophic and oxygen limited environments
are relatively dominated by deep infaunal species (Sgarrella et al.,
2012). The motile benthic deep-water foraminifera have the capability
to rapidly adapt their microhabitat to changes in food availability and
oxygenation. This dynamic adaptation is also reflected in the so-called
TROX model (TROX = TRophic OXygen model, Jorissen et al., 1995,
2007), which explains that the depth of the foraminiferal microhabitat is
controlled by food availability in oligotrophic ecosystems and oxygen
concentration in eutrophic ecosystems. In oligotrophic environments,
the microhabitat depth is limited by the low amount of food available
within the sediment, whereas in eutrophic systems, the penetration
depth of most taxa depends on the level of oxygen present in the sedi­
ment (Jorissen et al., 1995).
In Table 1 the ecological and microhabitat preferences of the
recognized benthic taxa are listed and the relative references are
reported.
3.3. Proxies based on benthic foraminifera
Generally, foraminifera are abundant and their preservation is quite
good. Then, it was possible to obtain:
- relative frequencies (%) of the most abundant and/or palae­
cologically significant taxa to describe the main paleoenvironmental
changes at the sea-floor;
B. Russo et al.
Fig. 2. The St. Peter’s Pool section: Polarity/Chron, lithology, planktonic
foraminifera and calcareous nannoplancton bioevents, and biostratigraphy
(from Foresi et al., 2011). Age-depth profile is based on calcareous plankton
ages of Turco et al. (2017). For samples references see Appendix A.
- relationship between taxa of Group A (oxic/oligotrophic taxa and
oxic/oligo-mesotrophic opportunistic behaving species) and Group B
(hypoxic/eutrophic species) (Table 2) to reconstruct the main
palaecological changes. We use the term hypoxic in analogy to sensu
Jorissen et al. (2007) for the environments, referring to the species
that prefer environments where they may potentially be influenced
by low oxygen concentrations (without referring to a precise range of
oxygen concentration). For literature references related to the
ecological characteristics of each taxon see section 3.2, Table 1;
- relative proportions of superficial microhabitat taxa (epifaunal to
shallow infaunal + epifaunal taxa), intermediate microhabitat taxa
(shallow to intermediate infaunal + shallow infaunal taxa), and deep
infaunal microhabitat taxa. Hanzawaia boueana was excluded from
the group of the superficial microhabitat taxa, because even if
epifaunal species (Spezzaferri et al., 2014), it is reported as tolerant
to high food supply and/or great preservation of organic matter at
the sea floor (Russo et al., 2002) and indicative of high productivity
(Russo et al., 2007);
∑ ∑
- paleoxygenation index - O2 index [O2 index = (1 (1) + 2 (2) +
∑ ∑
3 (3) + …. N (n))/100] where Σ(n) is the sum of the relative
abundances of taxa in group n, following Kouwenhoven and van der
Zwaan (2006). This proxy is useful to detect the trend of the oxygen
level at the sea floor. For this purpose, the benthic taxa with per­
centages >4% (with the exception of Melonis affinis because we
considered it poorly affected by the oxygen content and controlled
more by temperature than food supply - Rasmussen and Thomsen,
4
Palaeogeography, Palaeoclimatology, Palaeoecology 586 (2022) 110722
2017) were subdivided into three groups basing on their different
sensibility to oxygen content at the sea floor. The three groups
correspond to three increasing oxygen levels: low (Group 1), inter­
mediate (Group 2), and high (Group 3) level of oxygen bottom
waters.
- plankton/benthos ratio, expressed as the percentage of planktonic
specimens, %P = 100*[P/(P + B-S)], where P = number of plank­
tonic specimens, B = number of benthic specimens and S = number
of stress markers (deep infauna) (van Hinsbergen et al., 2005). This
proxy was used for paleodepth estimation. Bolivina spp., Bulimina
elongata, Cancris spp., Globobulimina affinis, Uvigerina spp. (except for
U. semiornata) have been considered as stress markers following van
Hinsbergen et al., 2005. The paleodepth estimation obtained by this
proxy was confirmed and refined by means of the co-occurrence of
depth benthic foraminiferal markers with well-defined depth distri­
bution range.
3.4. Stable isotopes
Oxygen and Carbon stable isotopes analyses were carried out to
describe the main changes of temperature and productivity of bottom
water masses. In particular, 283 samples disaggregated in normal water,
no oven dried, were analyzed to pick about 10 specimens of the benthic
foraminifera species Heterolepa dutemplei, considered indicative of oxic
bottom conditions (e.g. Russo et al., 2007). For our purpose clean in­
dividuals without concretions, overgrowth or visible diagenetic pro­
cesses on going were selected from grain size fraction ≥150 μm.
Analyses were performed at the geochemistry laboratory of the
ISMAR-CNR (Naples, Italy) with an automated continuous flow car­
bonate preparation Gas BenchII device (Spötl and Vennemann, 2003)
and a ThermoElectron Delta Plus XP mass spectrometer. Acidification of
samples was performed at 50 ◦ C. Every six samples, an internal standard
(Carrara Marble with δ18O = − 2.43‰ versus VPDB and δ13C = 2.43‰ vs.
VPDB) was used. Moreover, every 30 samples the NBS19 international
standard was measured. Standard deviations of carbon and oxygen
isotope measures were estimated at 0.1 and 0.08‰, respectively, basing
on three repetitions of ~200 samples measures. All the isotope data are
reported in δ‰ vs. VPDB.
3.5. Statistical analysis
A multivariate statistical analysis method was applied (R-mode
PCA), using SPSS statistical software (version 19) to quantify the rela­
tionship between benthic foraminiferal species recognized in 135 sam­
ples and evaluate the major changes in the benthic foraminiferal
assemblages. Starting from the original variables set, the PCA generates
a new set of uncorrelated variables named Principal Components (PCs),
resulting from a linear combination of the original ones. The PCs explain
the percentage of the system’s total variability concentrated on the first
two or three main components (Davis, 1973). Statistical analysis was
applied to the 20 taxa with an abundance >4%, out of 42 forming the
original dataset, moreover other 3 species (Anomalinoides helicinus,
Cassidulina laevigata, Globocassidulina subglobosa) with Pearson correla­
tion lower than 0.3 were not considered.
4. Results
4.1. Benthic taxa distribution patterns
Benthic foraminiferal assemblages are composed of 42 taxa, referred
to the genera Anomalinoides, Bolivina, Bulimina, Cancris, Cassidulina,
Cibicides, Cibicidoides, Cribroelphidium, Epistominella, Globobulimina,
B. Russo et al.
Table 1
Ecological and microhabitat preferences of the studied benthic taxa.
Species
Anomalinoides helicinus
Bolivina reticulata
Bolivina spathulata
Bulimina striata
Cassidulina laevigata
Cibicides pachyderma
Cibicidoides cicatricosus
Cibicidoides subhaidingerii/
Heterolepa dutemplei
Cibicidoides ungerianus
Globocassidulina subglobosa
Gyroidina spp.
Hanzawaia boueana
Lenticulina spp.
Melonis affinis
Microhabitat
Epifaunal/shallow infaunal (Pérez-Asensio et al., 2012).
Epifaunal (Sgarrella et al., 2012).
Shallow infaunal (Pérez-Asensio et al., 2012).
Deep infaunal (Violanti et al., 2011). Shallow infaunal (Singh et al.,
2015, Pascual et al., 2020).
Shallow infaunal (Grunert et al., 2018).
Shallow infaunal (Fontanier et al., 2002, Pascual et al., 2020).
Epifaunal to shallow infaunal (Pérez-Asensio et al., 2012; Spezzaferri
et al., 2014).
Epifaunal (Murray, 1991).
Epifaunal (Murray, 2006; Székely et al., 2017).
Epifaunal (Oblak, 2007). Epifaunal to shallow infaunal (Pérez-Asensio
et al., 2012).
Epifaunal to shallow infaunal (Pérez-Asensio et al., 2012).
Shallow to intermediate infaunal (Fentimen et al., 2018).
Epifaunal (Spezzaferri et al., 2014).
Epifaunal (Di Bella et al., 2015; Székely et al., 2017).
Shallow to intermediate infaunal (Fontanier et al., 2002; Grunert et al.,
2015; Singh et al., 2015; Pascual et al., 2020).
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Palaeogeography, Palaeoclimatology, Palaeoecology 586 (2022) 110722
Ecological preference
Species generally preferring oxic and/or oligotrophic environments (
Sgarrella et al., 2012).
Species belonging to Bolivina spp., reported in Székely et al. (2017) as low-
oxygen group (Spezzaferri et al., 2002), which includes some species
tolerating dysoxia (Murray, 2006); dysoxic species (Kaiho, 1994).
Species abundant in poor oxygen, rich in organic matter with elevated
productivity environments (Alavi, 1988; Martin et al., 2007; Singh et al.,
2015; Pascual et al., 2020). Species behaving as opportunistic when a great
amount of organic matter is available, and usually associated to upwelling
phenomena (Okada, 1983; Mathieu, 1986; Guerreiro et al., 2009).
Species indicating dysoxia (Kaiho, 1994; Pascual et al., 2020).
Species indicative of high productivity (Bellanca et al., 2002; Russo et al.,
2007).
Species tolerating dysoxia (Murray, 2006; Székely et al., 2017), and low
oxygen conditions (Spezzaferri et al., 2002; Székely et al., 2017) since
belonging to Bulimina spp.
Species indicative of OMZ of eastern Arabian Sea, can be used as an index
for delineating oxygen-depleted environments in Arabian Sea (Nigam et al.,
2007).
Opportunistic species adapted to high food concentration (Baas et al.,
1998; Pascual et al., 2020), related to high flux of organic carbon (Jorissen
et al., 2007; Singh et al., 2015; Pascual et al., 2020). Suboxic species (
Kaiho, 1994), related with upwelling currents (Levy et al., 1995; Pascual
et al., 2020). C. laevigata dominates the Younger Dryas (YD) and the
beginning of Lower Holocene, evidencing the occurrence of cool waters
with low-oxygen and high organic matter content (Pascual et al., 2020).
High stress, dysoxia and high organic matter tolerant species (Rögl and
Spezzaferri, 2003; Murray, 2003, 2006; Alve, 2010; Spezzaferri et al.,
2013).
C. laevigata group (including C. laevigata and Trifarina angulosa): prefers
warm and food rich conditions (Rasmussen and Thomsen, 2017). Species
belonging to Group 1, comprising Assemblages 1 and 2, which include
species that dominated during warm and mostly food-rich interstadial
warm phases and interstadial cooling phases (Rasmussen and Thomsen,
2017).
Oxic/oligo-mesotrophic species (Fontanier et al., 2002; Sgarrella et al.,
2012; Spezzaferri et al., 2013; Pascual et al., 2020); opportunistic species
characteristic of a varying organic supply in relatively oligotrophic or
oligo-mesotrophic settings (Schmiedl et al., 2003; Abu-Zied et al., 2008;
Melki et al., 2009; Sgarrella et al., 2012); species able to compete in an
unstable environment (Sgarrella et al., 2012) and occurring in upwelling
areas (Licari and Mackensen, 2005).
Oxic species (Kaiho, 1994; Russo et al., 2007).
C. subhaidingerii: oxic (Corliss, 1991; Kaiho, 1994; Oblak, 2007; Russo
et al., 2007; Sgarrella et al., 2012; Székely et al., 2017) and oligotrophic
species, since belongs to Cibicidoides spp. generally preferring oxic and/or
oligotrophic environments (Sgarrella et al., 2012).
Species indicating a rather oligotrophic environment and oxic bottom
conditions (Sgarrella et al., 2012).
G. subglobosa assemblage seems to be adapted to an environment that is
characterized by low organic matter fluxes and enhanced bottom current
velocities (Schmiedl et al., 1997). Oxic indicator (Kaiho, 1999). Species
indicating relatively nutrient-poor conditions and recorded in areas of low
seasonal food supply in the North Atlantic and reported as opportunistic
species (Rasmussen et al., 2002). Species generally preferring oxic and/or
oligotrophic environments (Sgarrella et al., 2012). Oligotrophic behaving (
Spezzaferri et al., 2013).
Species with an intermediate sensibility to the presence of oxygen at the sea
floor (group 3 of a scale going from 1 -low-oxygen conditions- to 5 -normal
to well oxygenated conditions-) (Kouwenhoven and Van der Zwaan, 2006).
Suboxic indicator (Kaiho, 1999).
Species tolerant to high food supply and/or great preservation of organic
matter at the sea floor (Russo et al., 2002), and indicative of high
productivity (Russo et al., 2007).
Species with a relative low sensibility to the presence of oxygen at the sea
floor (group 2 of a scale going from 1 -low-oxygen conditions- to 5 -normal
to well oxygenated conditions-) (Kouwenhoven and Van der Zwaan, 2006).
Group reported in Székely et al. (2017) as suboxic (Kaiho, 1994; Rögl and
Spezzaferri, 2003; De Man, 2006; Grunert et al., 2012), and cold (Murray,
2006).
Cold water species (− 0.4◦ to 9 ◦ C) (Murray, 1991; Pascual et al., 2020),
tolerating high degraded organic matter content (Fontanier et al., 2002;
Pascual et al., 2020) and indicating mesotrophic conditions (Jorissen,
2003; Grunert et al., 2015; Pascual et al., 2020). The species is attracted to
(continued on next page)
B. Russo et al.
Table 1 (continued )
Species Microhabitat
Oridorsalis umbonatus Epifaunal to shallow infaunal (Pérez-Asensio et al., 2012).
Pullenia bulloides Shallow infaunal (Pérez-Asensio et al., 2012).
Siphonina reticulata Epifaunal to shallow infaunal (Pérez-Asensio et al., 2012).
Spirorutilus carinatus Epifaunal to shallow infaunal (Pérez-Asensio et al., 2012).
Uvigerina cylindrica Shallow infaunal (Stefanelli, 2004).
gaudrynoides
Uvigerina peregrina Shallow infaunal (Pérez-Asensio et al., 2012; Spezzaferri et al., 2014;
Milker et al., 2019). Shallow to intermediate infaunal (Fontanier et al.,
2002; Singh et al., 2015; Pascual et al., 2020).
Globocassidulina, Hanzawaia, Karreriella, Melonis, Neoeponides, Ori­
dorsalis, Pullenia, Saracenaria, Sigmoilina, Sigmoilopsis, Siphonina,
Sphaeroidina, Spiroplectinella, Trifarina, Uvigerina, and by other three
taxonomic units, such as Cibicidoides subhaidingerii/Heterolepa dutemplei,
Gyroidina spp. and Lenticulina spp. The list of the identified taxa is re­
ported in Appendix B.
The abundance fluctuations of the 17 species and of the taxon Cibi­
cidoides subhaidingerii/Heterolepa dutemplei with percentage > 4% are
reported in Fig. 3.
Throughout the studied section Bolivina spathulata (0.4–50%), Cas­
sidulina laevigata (0.3–27.5%), C. subhaidingerii/H. dutemplei
(0.7–39.8%), Siphonina reticulata (0.3–26.5%) and Uvigerina peregrina
(1.3–30.8%) are dominant species, together with the subordinate Buli­
mina striata, Cibicides pachyderma, Cibicidoides cicatricosus, Cibicidoides
ungerianus, Hanzawaia boueana and Melonis affinis. Further important
species include Anomalinoides helicinus, Spirorutilus carinatus and Uvi­
gerina cylindrica gaudrynoides.
In the distribution patterns described below we grouped the most
abundant and subordinate taxa, and the other important species such as
Anomalinoides helicinus, Spirorutilus carinatus and Uvigerina cylindrica
gaudrynoides into Group A (A. helicinus, C. subhaidingerii/H. dutemplei,
C. cicatricosus, C. pachyderma, C. ungerianus, S. carinatus, S. reticulata)
and Group B (B. striata, B. spathulata, C. laevigata, U. cylindrica gau­
drynoides, U. peregrina) on the base of their ecological preferences
(Table 2). The description of the patterns is mainly referred to the two
Groups together with the trend of some taxa which we considered
particularly significant for their ecological meaning.
From 16.12 to 16.01 Ma, Group A is dominant with respect to Group
B (Fig. 4c, d). C. subhaidingerii/H. dutemplei displays abundance peaks
(40%, 29%) at 16.08 and 16.03 Ma; B. spathulata shows its lowest per­
centage values starting from 16.08 Ma, B. striata displays an abundance
peak (34%) at 16.11 Ma, C. laevigata has three peaks (26%, 20%, 22%) at
16.12, 16.07 and 16.01 Ma, U. cylindrica gaudrynoides displays a peak
(16%) at 16.09 Ma, and U. peregrina shows high percentage values
(maximum value 20%) from 16.05 to 16.03 Ma (Fig. 3). Substantial
changes in the assemblage abundance and composition are observed
starting from the transitional thick dark-grey interval (16.01 to 15.96
6
Palaeogeography, Palaeoclimatology, Palaeoecology 586 (2022) 110722
Ecological preference
colder water and low food supply as included in Group 2 species that
dominated during cold and generally food poor interstadial cold phases and
stadials (Rasmussen and Thomsen, 2017). Species controlled more by
temperature than food supply (Rasmussen and Thomsen, 2017). Suboxic
indicator (Kaiho, 1994, 1999), it can occur in oxygen depleted sediments (
Jorissen et al., 1998; Pascual et al., 2020).
Suboxic indicator since belongs to Oridorsalis spp. (Kaiho, 1999).
Suboxic indicator since belongs to Pullenia spp. (Kaiho, 1999). The species
prefers colder water and low food supply as included in Group 2 species
that dominated during cold and generally food poor interstadial cold
phases and stadials (Rasmussen and Thomsen, 2017). Species controlled
more by temperature than food supply (Rasmussen and Thomsen, 2017).
Oxic species (Kouwenhoven and van der Zwaan, 2006; Russo et al., 2007;
Sgarrella et al., 2012; Pérez-Asensio et al., 2020), generally preferring
oligotrophic environments (Sgarrella et al., 2012).
High oxic conditions species (Ied et al., 2011).
Species proliferating during periods of nutrient abundance (stressed and
nutrient-rich environments) (Drinia, 2018). Suboxic species (Kaiho, 1994;
Rögl and Spezzaferri, 2003; Székely et al., 2017), indicative of high organic
matter (Rögl and Spezzaferri, 2003; Székely et al., 2017), and high primary
productivity (Spezzaferri et al., 2002; Székely et al., 2017), as belonging to
Uvigerina spp.
Species occuring in sediments rich in organic matter (Seiglie, 1968;
Schmiedl et al., 1997; Fontanier et al., 2002; Singh et al., 2015; Milker
et al., 2019; Pascual et al., 2020), indicating high productivity (Lutze,
1986; Rai and Singh, 2012; Patarroyo-Camargo and Martinez-Rodriguez,
2013; Pascual et al., 2020), meso-to eutrophic conditions (Milker et al.,
2019).
Suboxic species (Kaiho, 1994; Lutze, 1986; Singh et al., 2015; Pascual
et al., 2020).
Ma) up to 15.91 Ma, when most taxa of Group A abruptly decrease
starting to increase again at 15.92 Ma (Fig. 4c). By contrast, in the same
interval Group B abruptly increases starting to decrease at 15.92 Ma
(Fig. 4d). U. cylindrica gaudrynoides occurs almost only in this interval
(maximum value 11%), C. laevigata is present with some of its highest
percentage values (maximum value 28%) (Fig. 3).
From 15.91 to 15.86 Ma, the Group A increases (Fig. 4a), while the
Group B decreases (Fig. 4b). Conversely from 15.86 to 15.83 Ma, the
trends of these two groups are mainly reversed (Fig. 4a, b). From 15.83
to 15.71 Ma, the Group A increases or shows positive peaks (Fig. 4a)
while the Group B decreases (Fig. 4b). U. cylindrica gaudrynoides disap­
pears at 15.78 Ma (Fig. 3). From 15.71 to 15.62 Ma the Group A de­
creases (Fig. 4a) and the Group B exhibits either an increasing trend or
positive peaks (Fig. 4b). Oxic/oligo-mesotrophic opportunistic behaving
species (C. pachyderma, C. cicatricosus and C. ungerianus), which
contribute to the fluctuating trend of Group A from 15.91 to 15.62 Ma,
occur with the highest percentage values up to 15.71 Ma (Fig. 4d). From
15.62 to 15.37 Ma the Group A increases (Fig. 4a), while the Group B
shows an overall slightly decreasing trend (Fig. 4b), and the oxic/oligo-
mesotrophic/opportunistic behaving species occur with a discontinuous
trend (Fig. 4d). B. spathulata shows a decreasing trend, even if it occurs
with percentage values up to 33% from 15.55 to 15.50 Ma (Fig. 3). From
15.37 to 15.36 Ma, the Group A moderately decreases (Fig. 4a), while
the Group B slightly increases (Fig. 4b) and the oxic/oligo-mesotrophic/
opportunistic behaving species drastically reduce (Fig. 4d), and
B. spathulata increases up to 50% at 15.37 Ma (Fig. 3). C. laevigata and
M. affinis are quite abundant throughout the section and both show a
significant increasing in abundance from 16.08 to 16.06 Ma and from
16.01 to 15.91 Ma. Upwards C. laevigata has a decreasing trend up to
15.64 Ma showing high abundances percentage values up to 16.62 Ma,
and then decrease up to 15.54 Ma to increase again up to 15.37 Ma,
where decreases up to the top of the section; M. affinis shows an
increasing trend from 15.78 to 15.60 Ma, where its highest percentage
values (about 10%) are recorded (Fig. 3), from 15.60 to 15.50 Ma its
percentage abundance values decrease to slightly increase again up to
the top of the succession. H. boueana is present along the whole section
with low values (Fig. 3) and it shows an opposite trend to oxic/
B. Russo et al. Palaeogeography, Palaeoclimatology, Palaeoecology 586 (2022) 110722

Table 2
List of oxic/oligotrophic and oxic/oligo-mesotrophic opportunistic behaving taxa (Group A), and hypoxic/eutrophic taxa (Group B). The species C. cicatricosus
and C. ungerianus have been considered oxic/oligo-mesotrophic opportunistic behaving species as C. pachyderma, since they mirror the distribution pattern of
the last species. The taxa are also grouped on the base of their preferred microhabitat: superficial microhabitat taxa (epifaunal + epifaunal to shallow
infaunal), intermediate microhabitat taxa (shallow infaunal + shallow to intermediate infaunal) and deep microhabitat taxa (deep infaunal). The taxa below
the thick black line are not included in Group A and Group B because: Lenticulina spp. is an epifaunal taxa but reported as suboxic group; M. affinis is poorly
affected by the oxygen content and controlled more by temperature than food supply; the other taxa do not show any significant change along the section. For
references see section 3.2 Table 1.
Group A Group B

Oxic/oligo-mesotrophic
Oxic/oligotrophic taxa Hypoxic/eutrophic species
opportunistic behaving species

Deep microhabitat
Superficial microhabitat taxa Intermediate microhabitat taxa
taxa
Epifaunal Epifaunal to Epifaunal to shallow Shallow to
shallow Epifaunal infaunal Shallow infaunal intermediate Deep infaunal
infaunal infaunal
Anomalinoides
Bulimina striata
helicinus
Cibicidoides Cibicides pachyderma
Siphonina Cassidulina
subhaidingerii/ Cibicidoides
reticulata laevigata Bolivina spathulata
Heterolepa cicatricosus
Spirorutilus Uvigerina cylindrica
dutemplei Cibicidoides
carinatus gaudrynoides
ungerianus
Uvigerina peregrina
Globocassidulina
Bolivina reticulata Gyroidina spp.
Lenticulina subglobosa
spp. Oridorsalis
Pullenia bulloides Melonis affinis
umbonatus

oligotrophic taxa (Fig. 4c).
4.2. Benthic foraminiferal microhabitats
In Table 2 the benthic taxa with percentages >4% are also grouped
on the base of their microhabitat (for references see section 3.2, Table 1).
The distribution patterns of deep infaunal species (deep microhabitat
taxa), shallow to intermediate infaunal and shallow infaunal grouped
together (intermediate microhabitat taxa), and epifaunal to shallow
infaunal and epifaunal grouped together (superficial microhabitat taxa),
are reported in Figs. 4e-g.
From 16.12 to 16.01 Ma superficial microhabitat taxa are dominant
with mean percentage values around 45%, followed by intermediate
microhabitat taxa with mean percentage values around 25%, and by
deep microhabitat taxa which are clearly subordinate with mean per­
centage values around 8%. From 16.01 to 15.91 Ma, just below the base
of the transitional thick dark-grey interval, superficial microhabitat taxa
percentage values abruptly fall from 47% to 12% (the lowest value is
10.19% at 15.96 Ma), showing mean percentage values around 15%,
and increasing only in the uppermost part of the interval, while inter­
mediate microhabitat taxa show an opposite trend increasing up to 64%
(maximum value along the section) at 15.94 Ma and then decreasing
again up to the top of the interval; deep microhabitat taxa increases up
to 21% at 15.96 Ma followed by constant values around 10% up to the
top of the interval. From 15.91 to 15.62 Ma the three microhabitats
curves alternate increasing and decreasing trends. In particular, super­
ficial microhabitat taxa increase and become dominant in the intervals
15.91–15.86 Ma and 15.83–15.71 Ma, where deep and intermediate
microhabitat taxa decrease; between 15.86 and 15.83 Ma, and 15.71
and 15.62 Ma deep and intermediate microhabitat taxa increase, while
superficial microhabitat taxa decrease and become subordinate to in­
termediate microhabitat taxa. Upwards from 15.62 to 15.37 Ma super­
ficial microhabitat taxa increase and become dominant again with mean
values around 50%, while intermediate and deep microhabitats taxa
decrease showing mean values respectively around 25% and 10%.
Finally, from 15.37 Ma to the top of the section superficial microhabitat
taxa slightly decrease while intermediate and deep microhabitats taxa
increase.
4.3. Statistical analyses
The selected benthic taxa show a good level of correlation confirmed
by the Pearson correlation coefficient, with values between 0.3 and 0.8,
and the Kaiser-Meyer-Olkin test (KMO) values, which were higher than
0.5. All the selected benthic taxa were used to identify the PCs. The
Bartlett sphericity test (0.001) allowed us to reject the null hypothesis
(intercorrelation matrix comes from a population in which the variables
are non-collinear) and the KMO of 0.7 indicated that the extracted PCs
could account for a fair amount of variance. The first two PCs explained
about 39.2% of the variance, the magnitude of loading factors indicating
the degree of correlation that links the single variables are reported in
Table 3.
The first Principal component (PCA1) explains 25.61% of the total
variance. The highest positive loading characterizes the C. ungerianus
(0.71), C. cicatricosus (0.69), and C. pachyderma (0.68) species (Table 3),
which are plotted together in Fig. 5b, followed by H. boueana (Table 3)
and U. peregrina (Fig. 5c; Table 3). The negative loading typifies
C. subhaidingerii/H. dutemplei (− 0.63) and S. reticulata (− 0.53). The
PCA1 score plot shows a fluctuating trend with values ranging between
− 1.6 and 1.9 from the base up to the top of the section (Fig. 5a).
Nevertheless, some moderate changes can be observed in the intervals
from 16.01 to 15.91 Ma and from 15.86 to 15.83 Ma where the PCA1
negative scores shift towards higher values (respectively: − 0.7 and −
0.6) (Fig. 5a).
The second principal component (PCA2) explains 13.62% of the total
variance. The taxa C. pachyderma, C. subhaidingerii/H. dutemplei,
C. ungerianus, S. reticulata and S. carinatus, all belonging to Group A
(Fig. 5e), have positive loading (Table 3), while the species B. striata,
B. spathulata and U. cylindrica gaudrynoides, all belonging to Group B,
have negative loading (Table 3). The PCA2 score plot shows four main
intervals with positive PCA2 score: from 16.12 to 16.01 Ma, from 15.91
to 15.86 Ma, from 15.82 to 15.71 Ma and from 15.62 to 15.37 Ma,

7
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8

Palaeogeography, Palaeoclimatology, Palaeoecology 586 (2022) 110722

Fig. 3. - Vertical distribution patterns of the benthic foraminiferal taxa occurring with an abundance >4% along the St. Peter’s Pool section; for each taxon the vertical distribution pattern is plotted together with the 3
point moving average. On the left of the lithologic column the planktonic foraminifera and calcareous nannoplancton bioevents are reported. X-axis scaling is variable to better highlight the changes in abundance of the
different taxa along the section. The grey stripe corresponds to the thick dark-grey interval occurring between 10.2 and 11.9 m.
B. Russo et al. Palaeogeography, Palaeoclimatology, Palaeoecology 586 (2022) 110722

Fig. 4. From left to right curves plotted in time domain (Ma) of a: Group A (oxic/oligotrophic taxa + oxic/oligo-mesotrophic opportunisting behaving species); b:
Group B (hypoxic/eutrophic species); c: oxic/oligotrophic taxa; d: oxic/oligo-mesotrophic opportunisting behaving species; e: deep microhabitat taxa (deep infaunal
species); f: intermediate microhabitat taxa (shallow to intermediate infaunal + shallow infaunal taxa); g: superficial microhabitat taxa (epifaunal to shallow infaunal
+ epifaunal taxa); h: curve of relative oxygen level at the sea floor (O2 index) (Kouwenhoven and van der Zwaan, 2006); i: %P (van Hinsbergen et al., 2005); j-k:
oxygen (δ18O) and carbon (δ13C) stable isotopes of the benthic foraminifera H. dutemplei. For each plot the original data curve is reported together with the 3 point
moving average. The thin black lines represent the correlation between meters (lithologic column) and time (Ma). On the left of the lithologic column the planktonic
foraminifera and calcareous nannoplancton bioevents are reported. For the list of taxa belonging to Group A, Group B, and to the different microhabitats see Table 2.
The grey stripe corresponds to the thick dark-grey interval occurring between 10.2 and 11.9 m.

16.01 Ma O2 index has mean values around 1.5, moving between a

Table 3
minimum value of 1.19 (16.10 Ma) and a maximum of 1.88 (16.09 and
Factor loadings of first (PCA1) and second (PCA2) Principal Components.
16.08 Ma). From 16.01 to 15.91 Ma, just below the base of the transi­
Species PCA1 PCA2 tional thick dark-grey interval, O2 index values abruptly fall from 1.65 to
Bolivina reticulata − 0.32 − 0.19 1.00 (lowest value at 16.00 Ma), showing mean values around 1.08, and
Bolivina spathulata − 0.29 − 0.43 increasing only at the uppermost part of the interval. From 15.91 to
Bulimina striata 0.04 − 0.60 15.62 Ma O2 index values alternate increasing (15.91 to 15.86 Ma; 15.83
Cibicides pachyderma 0.68 0.44
Cibicidoides cicatricosus 0.69 0.25
to 15.71 Ma) and decreasing (15.86 to 15.83 Ma; 15.71 to 15.62 Ma).
Cibicidoides subhaidingerii/ Heterolepa dutemplei − 0.63 0.46 Upwards from 15.62 to 15.37 Ma O2 index values increase with mean
Cibicidoides ungerianus 0.71 0.57 values around 1.7. Finally from 15.37 Ma to the top of the section O2
Gyroidina spp. 0.51 − 0.26 index slightly decreases to mean values of 1.55.
Hanzawaia boueana 0.63 − 0.20
Lenticulina spp. − 0.58 0.08
Melonis affinis − 0.44 − 0.02 4.5. Plankton/benthos ratio (%P)
Oridorsalis umbonatus 0.35 0.28
Pullenia bulloides 0.53 − 0.05
Plankton/benthos ratio (%P) was calculated for all the samples, since
Siphonina reticulata − 0.53 0.34
Spirorutilus carinatus − 0.37 0.41 there was no evidence of downslope transport or reworking. As shown in
Uvigerina cylindrica gaudrynoides 0.14 − 0.64 Fig. 4i, %P values prevalently range from 74 to 92%, with lower values
Uvigerina peregrina 0.55 − 0.21 occurring respectively at 15.36 Ma (66%), 15.37 Ma (52%), 16.01 Ma
(63%), 16.09 Ma (67%) and 16.12 Ma (48%).
interbedded by four intervals, characterized by negative PCA2 scores:
from 16.01 to 15.91 Ma, from 15.86 to 15.82 Ma, from 15.71 to 15.62 4.6. Stable isotopes
Ma and from 15.37 to 15.36 Ma (Fig. 5d).
The benthic δ18OH. dutemplei and δ13CH. dutemplei isotope records are
reported in Fig. 4j and Fig. 4k, respectively. The δ18OH. dutemplei signal
4.4. Paleoxygenation index (O2 index) ranges between − 2.5 and 0.4‰. From the base of the section to 16.07
Ma, the δ18O curve does not show any noteworthy change, while from
The taxa used to calculate O2 index and their arrangement in three 16.07 to 15.96 Ma, it shows a trend towards heavier values from − 1.7‰
groups, each considered to be related to the increasing content of oxygen to about 0.5‰. Upwards to 15.64 Ma, δ18OH. dutemplei signal documents a
levels at sea floor, are reported in Table 4. cyclic trend with lighter (from 15.96 to 15.86 Ma and from 15.83 to
O2 index values fluctuate along the section (Fig. 4h). From 16.12 to 15.77 Ma) and heavier values (from 15.86 to 15.83 Ma and from 15.77

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B. Russo et al. Palaeogeography, Palaeoclimatology, Palaeoecology 586 (2022) 110722

this basal interval values increase, showing a peak at 16.01 Ma (2.2‰);

then from 16.01 to 15.77 Ma values decrease but they maintain slightly
higher than in the basal interval. From 15.77 to 15.47 Ma δ13CH. dutemplei
values decrease reaching the minimum at 15.49 Ma. In the topmost part
of the section values show low-amplitude fluctuations with no major
shifts observed.

5. Discussion

5.1. Deep water environmental changes

The S. Peter’s Pool section is characterized by fluctuations in abun­

dance of the superficial microhabitat oxic taxa (C. subhaidingerii/H.
dutemplei and S. reticulata), typical of oligotrophic bottom conditions, of
the deep infaunal hypoxic species B. spathulata, and of the intermediate
microhabitat hypoxic species (U. peregrina and subordinately B. striata
and U. cylindrica gaudrynoides), typical of eutrophic bottom conditions.
In addiction the occurrence of the superficial microhabitat oxic oppor­
tunistic behaving species (C. pachyderma, C. ungerianus and
C. cicatricosus), typical of oligo-mesothrophic bottom conditions, show a
significant trend. These latter three species generally show their highest
abundances when the other oxic and hypoxic species have similar total
relative abundances, testifying an increasing of organic matter flux to
Fig. 5. a: sample score pattern on the first principal component (PCA1); ver­ the sea-floor in still oxygenated bottom waters masses. In these envi­
tical distribution patterns of b: oxic/oligo-mesotrophic opportunistic behaving ronmental bottom conditions the deep infaunal species B. spathulata is
species (C. ungerianus + C. cicatricosus + C. pachyderma), c: U. peregrina; d: the only hypoxic eutrophic species which does not increase. We believe
sample score pattern on the second principal component (PCA2); e: vertical that the increased organic matter flux to the sea-floor, since in still
distribution patterns of Group A (see Table 1). For each plot the original data oxygenated bottom waters, characterizes a microhabitat where the oxic/
curve is reported together with the 3 point moving average. On the left of the
oligo-mesotrophic opportunistic behaving species are well adapted. The
lithologic column the planktonic foraminifera and calcareous nannoplancton
increasing in abundance of these species in such environmental bottom
bioevents are reported. The grey stripe corresponds to the thick dark-grey in­
terval occuring between 10.2 and 11.9 m. conditions testifies their opportunistic behavior, in agreement with
Verhallen (1991) and Frezza et al. (2005), who indicate that opportu­
nistic species increase with the increasing of the organic matter content
Table 4
and the decreasing of oxygen content at the sea floor. The bibliographic
Groups of benthic taxa arranged according to their relative increasing sensibility
to the oxygen content at the sea floor, used to construct the oxygen index references relative to ecological/palaecological meaning of the species
(Kouwenhoven and van der Zwaan, 2006). The three groups correspond to three are reported in section 3.2, Table 1.
increasing oxygen levels: low (Group 1), intermediate (Group 2), and high Distribution patterns of benthic species together with isotopic data
(Group 3) level of oxygen bottom waters. and statistical analysis results allowed us to identify five main intervals
Group 1 Group 2 Group 3
from SPP1 to SPP5 (Fig. 6) showing changes in the structure of the
benthic foraminiferal assemblage, their microhabitats and the evolution
Bolivina reticulata Cibicides pachyderma Anomalinoides helicinus
of bottom water conditions. The palaeoecological changes observed
Bolivina spathulata Cibicidoies cicatricosus Cibicidoides
Bulimina striata Cibicidoides ungerianus subhaidingerii/Heterolepa have also been related to the sea-level variations from the base to the top
dutemplei of the section (16.12–15.36 Ma) reported by Miller et al. (2020).
Cassidulina laevigata Globocassidulina Siphonina reticulata Between 16.12 and 16.01 Ma (interval SPP1) the general dominance
subglobosa
of Group A (preferring superficial microhabitat) (Fig. 6a), together with
Hanzawaia boueana Gyroidina spp. Spirorutilus carinatus
the relatively higher O2 index values (Fig. 6e), the meaningful presence
Uvigerina cylindrica Lenticulina spp. of Group B (Fig. 6a), the subordinate occurrence of the deep micro­
gaudrynoides habitat species B. spathulata (showing the lowest percentage values
Uvigerina peregrina Oridorsalis umbonatus starting from 16.08 Ma) (Fig. 6c) and the δ13CH. dutemplei values which
Pullenia bulloides
start to increase from 16.07 Ma, showing a peak at 16.01 Ma (Fig. 6g),
Data from: Alavi, 1988; Corliss, 1991; Kaiho, 1994, 1999; Schmiedl et al., 1997; suggest relatively oxygenated bottom water conditions with moderate
Fontanier et al., 2002; Spezzaferri et al., 2002, 2013; Murray, 2003, 2006; Rögl organic matter fluxes. This interpretation is also supported by 1) the
and Spezzaferri, 2003; Schmiedl et al., 2003; De Man, 2006; Kouwenhoven and fluctuation of PCA1 (Fig. 5a), which can be considered as the surface
van der Zwaan, 2006; Jorissen et al., 2007; Martins et al., 2007; Oblak, 2007; productivity trend, since it well correlate with the distribution patterns
Russo et al., 2007; Abu-Zied et al., 2008; Drinia, 2009; Melki et al., 2009; Alve,
of U. peregrina and B. spathulata (Fig. 3), and by 2) PCA2 curve (Fig. 6d),
2010; Ied et al., 2011; Grunert et al., 2012; Rai and Singh, 2012; Sgarrella et al.,
which can be interpreted as the oxygen content of bottom water trend,
2012; Singh et al., 2015; Patarroyo-Camargo and Martinez-Rodriguez, 2013;
Székely et al., 2017; Drinia, 2018; Milker et al., 2019; Pascual et al., 2020; Pérez-
since it mirrors the patterns of C. subhaidingerii/H. dutemplei, S. reticulata
Asensio et al., 2020. The ecological meaning of the different taxa is reported in (Fig. 3) and 3) O2 index (Fig. 6e). Sporadic episodes of higher oxygen
the section 3.2, Table 1. content are testified by peaks of C. subhaidingerii/H. dutemplei (Fig. 3),
and the superficial microhabitat taxa (Fig. 6c), and by relatively higher
values of O2 index (Fig. 6e). On the contrary, peaks in abundance of the
to 15.64 Ma). A gradual decreasing towards lighter values (− 2‰) is intermediate microhabitat taxa (B. striata, C. laevigata, U. cylindrica
observed from 15.64 to 15.52 Ma, followed by a trend vs. heavy values gaudrynoides, U. peregrina, Fig. 3) document short periods of enhanced
up to the top of the section. productivity in still oxygenated bottom waters, as also highlighted by
The δ13CH. dutemplei values range between 0.3 and 2.2‰. In particular δ13CH. dutemplei signal (Fig. 6g). In SPP1 interval M. affinis and C. laevigata
the curve does not show variations from the base to 16.07 Ma. Above display an increasing trend from 16.08 to 16.06 Ma, showing some of the

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B. Russo et al. Palaeogeography, Palaeoclimatology, Palaeoecology 586 (2022) 110722

Fig. 6. From left to right: a) total relative abundance curves of Group A (red) and Group B (blue); b) total relative abundance curves of oxic/oligo-mesotrophic
opportunistic behaving species (green), oxic/oligotrophic taxa (red), and hypoxic/eutrophic species (blue); c) total relative abundance curves of deep microhab­
itat taxa (black), intermediate microhabitat taxa (blue), and superficial microhabitat taxa (red); d) sample score pattern on the second principal component (PCA 2);
e) curve of relative oxygen level at the sea floor (O2 index) (Kouwenhoven and van der Zwaan, 2006); f) vertical distribution pattern of Melonis affinis; g)-h) oxygen
(δ18O) and carbon (δ13C) stable isotopes curves of the benthic foraminifera Heterolepa dutemplei; i) sea level oscillations curve (Miller et al., 2020); intervals (SPP1-
SPP5). On the left of the lithologic column, the planktonic foraminifera and calcareous nannoplancton bioevents are reported. For the list of taxa belonging to A and B
groups, oxic/oligo-mesotrophic opportunistic behaving species, oxic/oligotrophic taxa, and hypoxic/eutrophic species, deep microhabitat taxa, intermediate
microhabitat taxa, and superficial microhabitat taxa see Table 2. The grey stripe corresponds to the thick dark-grey interval occurring between 10.2 and 11.9 m. (For
interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

highest percentage values recorded along the section (Fig. 6f). This
increasing trend correlates with δ18OH. dutemplei heavier values starting
from 16.07 Ma (Fig. 6h), testifying the beginning of a relative cooling of
bottom water masses.
At 16.01 Ma, the base of the thick dark-grey interval marks a drastic
change in the benthic foraminiferal assemblage, because Group A is
replaced by Group B (Fig. 6a); the intermediate microhabitat taxa
become dominant (Fig. 6c) and the deep microhabitat taxa increase
(Fig. 6c), while the superficial microhabitat taxa abruptly decrease
(Fig. 6c) with percentages values generally similar or lower (in corre­
spondence of the thick dark-grey interval) than the deep microhabitat
taxa (Fig. 6c). U. cylindrica gaudrynoides, species indicative of high pri­
mary productivity (e.g. Székely et al., 2017) and proliferating in stressed
and nutrient-rich environments (Drinia, 2018), characterizes this in­
terval. Cassidulina laevigata, a high stress, dysoxic and high organic
matter tolerant species (e.g. Spezzaferri et al., 2013), evidencing the
occurrence of cool waters with low-oxygen and high organic matter
content (Pascual et al., 2020), displays a significant increase with some
of its highest percentage values. The increase of Group B and the trends
of C. laevigata and U. cylindrica gaudrynoides may be the result of an
increased organic flux at the seafloor (e.g. Jorissen et al., 1995). In
addition, the PCA1 negative scores shift towards higher values (Fig. 5a),
while O2 index abruptly decreases and reaches its minimum values
(Fig. 6e). PCA2 becomes negative (Fig. 6d), whereas δ13CH. dutemplei
shows a peak followed by a decreasing trend but with values slightly
higher than in the SPP1 interval (Fig. 6g). All these signals evidence,
between 16.01 and 15.91 Ma (interval SPP2), the transition from a quite
oxygenated with moderate organic matter fluxes to the sea floor
(interval SPP1) to low oxygen bottom water masses with a clear increase
of the productivity. These new conditions at the sea floor are also
associated with a cooling phase testified by a marked shift vs. heavy
values in δ18OH. dutemplei signature (Fig. 6h) and by the increasing trend of
M. affinis and C. laevigata (Fig. 6f). This cooling phase should correspond
to the well-known glaciation event Mi2 (Miller et al., 1991), reflecting
substantial ice volume increases near the bases of Zones Mi2 (at about
16.1 Ma), and correlates with the sea level falling (Fig. 6i, Miller et al.,
2020). The sea level falling trend, as well as δ18OH. dutemplei (Fig. 6h) and
M. affinis trends (Fig. 6f), matches also the decreasing trend of Group A,
the opposite increasing trend of Group B (Fig. 6a), and the increasing
trend of δ13CH. dutemplei (Fig. 6g). These conditions, together with the
significant presence of U. cylindrica gaudrynoides and C. laevigata, could
be due to an increase of the primary productivity, caused by the inten­
sification of the runoff determined by the sea level fall related to the
cooling phase.
Between 15.91 and 15.62 Ma (interval SPP3) the fluctuations of the
superficial microhabitat Group A, and intermediate/deep microhabitat
Group B, which become either dominant or subordinate (Fig. 6a), imply
a transition from a more stable and eutrophic conditions (SPP2) to un­
stable oligo-mesotrophic/eutrophic conditions (SPP3). This interpreta­
tion is supported by the increase in abundance of the superficial
microhabitat, oxic/oligo-mesotrophic opportunistic behaving species
(C. pachyderma, C. cicatricosus and C. ungerianus), species more
competitive in unstable environmental conditions, from 15.91 to 15.71
Ma (Fig. 6b). These changed bottom water conditions are also docu­
mented by the trend in O2 index (Fig. 6e), PCA2 (Fig. 6d) and partially
by PCA1 curves (Fig. 5a), as well as by the trend of δ18OH. dutemplei signal

11
B. Russo et al.
(Fig. 6h), suggesting relatively more oxygenated and warmer (from
15.91 to 15.86 Ma, and from 15.83 to 15.77 Ma) or more productive, less
oxygenated and cooler (from 15.86 to 15.83 Ma and from 15.77 to
15.62 Ma) bottom water masses. In SPP3 interval M. affinis shows an
increasing trend from 15.78 to 15.62 Ma (Fig. 6f) correlating to the
δ18OH. dutemplei vs. heavier values (Fig. 6h). In SPP3 interval, the varia­
tions of the sea level correlate with changes in Group A, M. affinis and
δ18OH. dutemplei only in the upper part (from 15.71 to 15.63 Ma), where
the oxic/oligo-mesotrophic opportunistic behaving species are less
abundant than the interval 15.91–15.71 Ma (Fig. 6).
Between 15.62 and 15.37 Ma (interval SPP4) the palaecological
bottom conditions are similar to the SPP1 interval, since the superficial
microhabitat Group A (Fig. 6a) dominates again, and the oxic/oligo-
mesotrophic opportunistic behaving species occur even if with a
discontinuous trend (Fig. 6b), Group B slightly decreases, suggesting
relatively stable oxic conditions with moderate organic matter fluxes. An
increasing trend is recorded by O2 index curve (Fig. 6e), PCA2 becomes
positive (Fig. 6d), while the intermediate and deep microhabitat Group
B decreases (Fig. 6a) as well as δ13CH. dutemplei signal (Fig. 6g). These
changes suggest a partial restoring of the SPP1 palaeoecological bottom
water conditions. δ18OH. dutemplei trend initially decreases vs. lighter
values and gradually increases towards heavier values after 15.52 Ma
(Fig. 6h), in good agreement with the decreasing followed by the
increasing trends of C. laevigata (initially decreasing and then increasing
from 15.54 Ma, Fig. 3) and M. affinis (initially decreasing and then
increasing from 15.50 Ma, Fig. 6f). These trends also correlate with the
initial rising followed by the sea level fall (Fig. 6i). It is worth to point
out that δ18OH. dutemplei signal correlates with the Group A and Group B
trends only up to 15.52 Ma (lighter δ18OH. dutemplei values, Group A
increasing trend and Group B decreasing trend), but upwards to 15.37
Ma, coherently with the shift of δ18OH. dutemplei signal towards heavier
values, Group A and Group B do not invert their trends. We have not
found an explanation for this mismatch.
In the uppermost part of the section, from 15.37 to 15.36 Ma (in­
terval SPP5): 1) the slight decrease in abundance of the superficial
microhabitat Group A (Fig. 6a) - mainly due the drastic reduction of the
oxic/oligo-mesothrophic opportunistic behaving species (Fig. 6b), 2) the
moderate increase of the intermediate/deep microhabitat Group B
(Fig. 6a) - essentially due to the increase of B. spathulata (Fig. 6c), 3) the
shift of PCA2 towards negative values (Fig. 6d), 4) the slight decrease of
O2 index (Fig. 6e), suggest a little increase of the organic matter content
in relatively less oxygenated bottom water masses with respects to SPP1
and SPP4 intervals.
Summarizing, the benthic foraminiferal changes reflect different
deep water environmental conditions between 16.12 and 15.36 Ma (late
Burdigalian to early Langhian) corresponding to warm climate condition
linked to the onset of the MCO (e.g. Holbourn et al., 2015; Prista et al.,
2015).
Thomas (2007) reported that middle Miocene benthic foraminiferal
faunal turnover, occurred during episodes of global cooling, may reflect
the increased seasonality of primary productivity and increased delivery
of labile organic matter to the sea floor. According to this interpretation,
we suggest that in the St. Peter’s Pool section the fluctuations of “oxic/
oligotrophic”, “hypoxic/eutrophic” and “oxic/oligo-mesotrophic
opportunistic behaving” taxa are indicative of increased seasonality,
which in turn affect food flux and oxygenation at the sea-floor.
5.2. Paleobathymetry
Foresi et al. (2011) estimated an upper-bathyal paleodepth for St.
Peter’s Pool section deposition, based on a preliminary study of benthic
foraminifera. More detailed analyses reported in this work allowed us to
estimate the paleodepth with a greater accuracy using the %P (van
Hinsbergen et al., 2005) and marker species with well-defined depth
distribution range. The values of the %P curve, mainly ranging from
74% to 93% (Fig. 3), permit to estimate a paleodepth ranging between
12
Palaeogeography, Palaeoclimatology, Palaeoecology 586 (2022) 110722
500 and 1000 m. The co-occurrence of the depth markers C. cicatricosus
together with B. reticulata, H. dutemplei and H. boueana confirm and
refine the depth interval calculated with the %P. Cibicidoides cicatricosus
has its upper and lower bathymetric limits at 600 m and 1000 m
respectively (Katz and Miller, 1993); while the other species have their
lower limit at 1000 m (Kouwenhoven, 2000; Russo et al., 2002; Drinia
et al., 2004), then a middle bathyal paleodepth (van Morkhoven et al.,
1986), ranging from 600 m to 1000 m is estimated.
6. Conclusions
The integrated study on benthic foraminiferal assemblages and Ox­
ygen and Carbon stable isotopes were carried out on the upper Burdi­
galian - lower Langhian S. Peter’s Pool section (Malta Island, Central
Mediterranean Sea).
The micropaleontological and geochemical data collected from the
section allow us to hypothesize the following palaeoecological changes
in the bottom water masses:
- from 16.12 to 16.01 Ma (interval SPP1): relatively oxygenated
bottom conditions with moderate organic matter fluxes;
- from 16.01 (base of the thick dark-grey lithological interval) to
15.91 Ma (interval SPP2): transition to cooler bottom water masses
with lower oxygen content and a clear increase of the productivity. In
this interval is recorded the major benthic foraminiferal turnover,
that is well recognized also in the isotope records. These conditions
are associated with a sea level fall, well correlated with a cooling
phase, documented by δ18OH. dutemplei signal, M. affinis trend and the
trends of the other main palaeoecological bottom water indicators.
We believe that these conditions are related to an increase of the
primary productivity, caused by an intensification of the runoff
determined by the falling of the sea level, following the cooling;
- from 15.91 to 15.62 Ma (interval SPP3): succeeding of relatively
more oxygenated and warmer bottom water masses (from 15.91 to
15.86 Ma and from 15.83 to 15.71 Ma) with more productive, less
oxygenated and cooler water masses (from 15.86 to 15.83 Ma and
from 15.71 to 15.62 Ma);
- from 15.62 to 15.37 Ma (interval SPP4): restoring of the initial
bottom conditions recorded in the lower part (interval SPP1) of the
section, characterized by relatively oxygenated bottom water masses
with moderate organic matter fluxes. These conditions are associated
with an initial rising, followed by a falling of the sea level, well
correlated with δ18OH. dutemplei signal initially lighter and heavier
upwards;
- from 15.37 to 15.36 Ma (interval SPP5): little increase of the organic
matter content in relatively less oxygenated bottom water masses
with respects to SPP1 and SPP4 intervals.
Plankton/benthos ratio (%P) and the presence of some benthic spe­
cies with a well-defined depth distribution range allowed us to estimate
a middle-bathyal paleodepth, ranging from 600 m to 1000 m during
MCO (between 17 and 15 Ma).
It is worth to point out that the major benthic foraminiferal turnover
occurred between 16.01 (base of the thick dark-grey lithological inter­
val) and 15.91 Ma can be related to a cooling phase corresponding to the
onset of Miller’s event Mi2 (Miller et al., 1991, 2020).
Concluding, the main variations detected in the benthic foraminif­
eral assemblages suggest different paleoenvironmental conditions
characterized either by relatively oxygenated, warmer bottom water
masses and moderate organic matter fluxes, or less oxygenated, cooler
bottom water masses with an increase in productivity, correlating with
Miocene Climatic Optimum (MCO). We suggest that these paleoenvir­
onmental changes observed in the St. Peter’s Pool section are indicative
of increased seasonality, which in turn affect food flux and oxygenation
at the sea-floor.
B. Russo et al. Palaeogeography, Palaeoclimatology, Palaeoecology 586 (2022) 110722

Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
dell’Università e della Ricerca (PRIN Project 2006, Scientific coordi­
nator Silvia Iaccarino) and by Regional Committee on Mediterranean
Neogene Stratigraphy (RCMNS) fund 2009 of the Consiglio Nazionale
delle Ricerche (CNR) of Italy.
We thank Kenneth Miller (Rutgers University) for the sea level data.

Acknowledgments

This work was financially supported by Ministero dell’Istruzione,

Appendix I

List of the examined samples: sample, stratigraphic position (distance in meters from the base of the section), sample spacing (distance in cen­
timeters between one sample and the next), lithology (DBHL = dark beige hardened limestone; DGML = dark grey marly limestone; DGCM = dark grey
calcareous marl; WML = whitish marly limestone; WCL = whitish calcareous limestone; DBML = dark beige marly limestone; DBCM = dark beige
calcareous marl; LBML = light beige marly limestone; LBCM = light beige calcareous marl).

Sample Stratigraphic position (m) Sample spacing (cm) Lithology Sample Stratigraphic position (m) Sample spacing (cm) Lithology

267bis 30.99 54 DBHL 126 16.13 31 DBML

264 30.45 8 WML 124 15.82 27 DBML
263 30.37 11 WML 122 15.55 9 DBML
261 30.26 23 WCL 121 15.46 25 DBHL
258 30.03 37 WCL 119 15.21 19 DBML
254bis 29.66 4 WCL 117 15.02 24 DBHL
254 29.62 38 WCL 115 14.78 23 DBML
251 29.24 29 WML 113 14.55 14 DBHL
248 28.95 30 WCL 328 14.41 66 DBML
245 28.65 6 WCL 107 13.75 9 DBHL
244 28.59 8 WCL 106 13.66 21 DBHL
242 28.51 46 WCL 104 13.45 11 DBHL
237 28.05 28 DBCM 103 13.34 9 DBML
234 27.77 41 DBCM 102 13.25 10 DBHL
231 27.36 11 DBCM 101 13.15 23 DBML
230 27.25 29 DBCM 99 12.92 13 DBHL
227 26.96 32 DBCM 98 12.79 24 DBML
224 26.64 37 DBHL 95 12.55 14 DBHL
220 26.27 8 DBCM 94 12.41 11 DBHL
219 26.19 18 DGML 93bis 12.3 23 DBHL
217 26.01 13 DBCM 91 12.07 28 DBML
216 25.88 23 DBCM 89 11.79 75 DGCM
214 25.65 31 DBCM 84 11.04 14 WML
211 25.34 14 DBCM 281 10.90 30 WML
209 25.20 27 DBHL 81 10.60 18 DGCM
207 24.93 20 DBCM 80 10.42 16 DGCM
205 24.73 33 DBCM 78 10.26 29 DGCM
203 24.40 12 DBCM 76 9.97 28 LBCM
202 24.28 39 DBCM 74 9.69 20 LBCM
199 23.89 15 DBHL 72 9.49 27 LBCM
197 23.74 16 DBHL 70 9.22 20 LBCM
196 23.58 33 DBCM 68 9.02 10 DBHL
193 23.25 26 DBCM 67 8.92 12 LBML
191 22.99 8 DBCM 66 8.80 22 LBML
190 22.91 21 DBCM 64 8.58 41 LBML
188 22.70 15 DBCM 61 8.17 35 LBCM
187 22.55 23 DBCM 59 7.82 19 LBML
185 22.32 20 DBCM 57 7.63 31 LBML
183 22.12 28 DBCM 55 7.32 7 LBCM
181 21.84 32 DBHL 54 7.25 45 LBCM
178 21.52 22 DBCM 50 6.80 18 LBCM
176 21.30 10 DBHL 48ter 6.62 44 DBHL
175 21.20 9 DBCM 342 6.18 31 LBCM
174 21.11 22 DBCM 336 5.87 20 DGML
172 20.89 20 DBCM 332 5.67 10 LBCM
171 20.69 15 DBHL 330 5.57 34 LBCM
169 20.54 8 DBCM 36 5.23 11 LBCM
168 20.46 7 DBCM 35 5.12 29 LBCM
167 20.39 21 DBHL 33bis 4.83 21 LBCM
165 20.18 21 DBCM 32 4.62 9 DBHL
162 19.97 25 DBCM 31 4.53 26 LBCM
159 19.72 14 DBCM 29 4.27 30 LBML
157 19.58 12 DBCM 26 3.97 17 LBCM
(continued on next page)

13
B. Russo et al. Palaeogeography, Palaeoclimatology, Palaeoecology 586 (2022) 110722

(continued )
Sample Stratigraphic position (m) Sample spacing (cm) Lithology Sample Stratigraphic position (m) Sample spacing (cm) Lithology

156 19.46 9 DBCM 25 3.80 26 LBCM

155 19.37 32 DBCM 23 3.54 18 LBML
365 19.05 30 DBHL 22 3.36 40 LBCM
359 18.75 10 DBHL 20 2.96 14 LBCM
357 18.65 54 DBHL 19bis 2.82 22 DBHL
141 18.11 9 DBML 18 2.60 37 LBCM
140 18.02 29 DBML 15 2.23 41 LBML
138 17.73 16 DBML 12 1.82 5 LBCM
137 17.57 21 DGML 11 1.77 40 LBCM
135 17.36 39 DBML 8 1.37 28 DGML
133 16.97 16 DBHL 6 1.09 26 LBCM
132 16.81 10 DBHL 4 0.83 36 LBML
131 16.71 10 DBML 2bis 0.47 39 DBHL
130 16.61 32 DBHL 1 0.08 8 LBCM
127 16.29 16 DBML

Appendix II - List of the classified species.

Anomalinoides helicinus (Costa) = Nonionina helicina Costa, 1857.

Bolivina reticulata Hantken, 1875.
Bolivina spathulata (Williamson) = Textularia variabilis var. spathulata Williamson, 1858.
Bulimina elongata d’Orbigny, 1846.
Bulimina striata d’Orbigny in Guérin-Méneville,1832.
Cancris auricula (Fichtel and Moll) = Nautilus auricula Fichtel and Moll, 1798.
Cancris oblongus (Williamson) = Rotalina oblonga Williamson, 1858.
Cassidulina carinata Silvestri, 1896 = C. laevigata var. carinata Silvestri, 1896.
Cassidulina laevigata d’Orbigny, 1826.
Cibicides pachyderma (Rzehak) = Truncatulina pachyderma Rzehak, 1886.
Cibicidoides cicatricosus (Schwager) = Anomalina cicatricosa Schwager, 1866.
Cibicidoides subhaidingerii (Parr) = Cibicides subhaidingerii Parr, 1950.
Cibicidoides ungerianus (d’Orbigny) = Rotalina ungeriana d’Orbigny, 1846.
Cibicidoides wuellerstorfi (Schwager) = Anomalina wuellerstorfi Schwager, 1866.
Cribroelphidium albiumbilicatum (Weiss, 1954) = Nonion pauciloculum subsp. albiumbilicatum Weiss, 1954.
Epistominella lecalvezi (Lys and Bourdon) = Pseudoparrella lecalvezi Lys and Bourdon, 1958.
Globobulimina affinis (d’Orbigny) = Bulimina affinis d’Orbigny, 1839.
Globocassidulina subglobosa (Brady) = Cassidulina subglobosa Brady, 1881.
Gyroidina spp.
Hanzawaia boueana (d’Orbigny) = Truncatulina boueana d’Orbigny, 1846.
Heterolepa dutemplei (d’Orbigny) = Rotalina dutemplei d’Orbigny, 1846.
Karreriella sp.
Lenticulina spp.
Melonis affinis (Reuss) = Nonionina affinis Reuss, 1851
Neoeponides schreibersii (d’Orbigny) = Rotalina schreibersii d’Orbigny, 1846.
Oridorsalis umbonatus (Reuss) = Rotalina umbonata Reuss, 1851.
Pullenia bulloides (d’Orbigny) = Nonionina bulloides d’Orbigny, 1846.
Pullenia quadriloba Reuss = Pullenia compressiuscula Reuss var. quadriloba Reuss, 1867.
Pullenia quinqueloba (Reuss) = Nonionina quinqueloba Reuss, 1851.
Pullenia salisburyi R.E. and K.C. Stewart, 1930.
Saracenaria italica Defrance, 1824.
Sigmoilopsis celata (Costa) = Spiroloculina celata Costa, 1855.
Siphonina reticulata (Cžjžek) = Rotalina reticulata Cžjžek, 1848.
Sphaeroidina bulloides d’Orbigny in Deshayes, 1828.
Spirorutilus carinatus (d’Orbigny) = Textularia carinata d’Orbigny, 1846.
Spirosigmoilina tenuis (Cžjžek) = Quinqueloculina tenuis Cžjžek, 1848.
Trifarina bradyi Cushman, 1923.
Uvigerina barbatula Macfadyen, 1930.
Uvigerina cylindrica gaudrynoides Lipparini, 1932.
Uvigerina peregrina Cushman, 1923.
Uvigerina rutila Cushman and Todd, 1941.
Uvigerina semiornata d’Orbigny, 1846.
Uvigerina striatissima Perconig, 1955.

14
B. Russo et al. Palaeogeography, Palaeoclimatology, Palaeoecology 586 (2022) 110722

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.palaeo.2021.110722.

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