GEOLOGICA CARPATHICA
, JUNE 2017, 68, 3, 207 – 228
doi: 10.1515/geoca-2017-0016
www.geologicacarpathica.com
Calcareous nannoplankton and foraminiferal response to
global Oligocene and Miocene climatic oscillations:
a case study from the Western Carpathian
segment of the Central Paratethys
KATARÍNA HOLCOVÁ
Institute of Geology and Palaeontology, Charles University, Albertov 6, 128 43 Praha 2, Czech Republic; holcova@natur.cuni.cz
(Manuscript received August 23, 2016; accepted in revised form November 30, 2016)
Abstract: The reactions of foraminiferal and calcareous nannoplankton assemblages to global warming and cooling
events in the time intervals of ca. 27 to 19 Ma and 13.5 to 15 Ma (Oligocene and Miocene) were studied in subtropical
epicontinental seas influenced by local tectonic and palaeogeographic events (the Central Paratethys). Regardless of
these local events, global climatic processes significantly influenced the palaeoenvironment within the marine basin.
Warm intervals are characterized by a stable, humid climate and a high-nutrient regime, due primarily to increased
continental input of phytodetritus and also locally due to seasonal upwelling. Coarse clastics deposited in a hyposaline
environment characterize the marginal part of the basin. Aridification events causing decreased riverine input and
consequent nutrient decreases, characterized cold intervals. Apparent seasonality, as well as catastrophic climatic events,
induced stress conditions and the expansion of opportunistic taxa. Carbonate production and hypersaline facies
characterize the marginal part of the basins. Hypersaline surface water triggered downwelling circulation and mixing of
water masses. Decreased abundance or extinction of K-specialists during each cold interval accelerated their speciation
in the subsequent warm interval. Local tectonic events led to discordances between local and global sea-level changes
(tectonically triggered uplift or subsidence) or to local salt formation (in the rain shadows of newly-created mountains).
Keywords: climate, foraminifera, calcareous nannoplankton, Oligocene, Miocene, Central Paratethys.
Introduction
The major Miocene cooling events in the Early and the late
Middle Miocene can be correlated with two episodes of
deci duous tree appearances in the Western Carpathian area
(Planderová 1990):
(1) A brief event at the Oligocene/Miocene boundary, with
increases of Ulnus, Alnus and Betula, which coincides with the
global Mi-1 event, lasting approximately 250 ka around the
Oligocene/Miocene boundary (23.03 Ma) (Zachos et al. 2001).
The stomatal index data indicate a rapid increase in atmo-
spheric carbon dioxide at 22.95 Ma, followed by a more
gradual decrease (Kürschner et al. 2008). The cooling was
connected with an increase in seasonality, as shown by palaeo-
climate analysis based on plant macrofossils. In the study area
(the Pannonian domain), cooling, especially of the coldest
months, was documented by Erdei et al. (2007), who finds
sub-zero winter temperatures. Aridity is indicated, based on
leguminous elements (Erdei et al. 2007). The subsequent
warming corresponds to the reappearance of palms from the
genera Arecipites, Myricipites, etc. (Planderová 1990).
Ozdínová & Soták (2014) documented this warming in the
NP25 calcareous nannoplankton zone from foraminiferal and
calcareous nannoplankton assemblages. Grunert et al. (2015)
interpreted the following cooling to coincide with the NN1
and lower part of the NN2 Zones (to the FO of H. ampliaperta)
based on oscillations in stable oxygen isotope values.
(2) The Middle Miocene event represents the beginning of
the Middle and Late Miocene gradual environmental and
climatic changes known as the MMCT (= Middle Miocene
Climate Transition) (Holbourn et al. 2005). The cooling can be
correlated with the Mi-3 global events (Mi-3a event 14.3 Ma,
Mi-3b event 13.8 Ma; Gradstein et al. 2012). In terrestrial
climates, the transition from the MMCO (= Middle Miocene
Climate Optimum 15 Ma; Gradstein et al. 2012) to the MMCT
is characterized by an increase in the mean annual range of
temperatures, primarily due to decreasing cold month tem-
peratures (Bruch et al. 2010), and increased seasonality is
principally expressed in the seasonality of precipitation
(Doláková et al. 2014). In the study area, climatic instability
was connected with the appearance of small carbonate bodies
(Holcová et al. 2015) as a consequence of the Langhian aridi-
fication events, which were described from the Mediterranean
area at 15.074 Ma and 14.489 Ma (Hüsing et al. 2010). Fin-
dings of pollen grains of herbs and heliophilous plants, such as
Poaceae, Asteraceae, Caryophyllaceae, Chenopodiaceae,
Olea, Buxus and Ephedra, also indicate the existence of more
open and drier areas at that time in the studied area.
Regardless of these climatic fluctuations, the studied area
was located in the subtropical zone during the latest Oligocene
to Middle Miocene (Planderová 1990; Böhme et al. 2010).
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In epicontinental seas, the impact of global climatic changes
may be influenced by local palaeogeographic events triggered
by local tectonic and volcanic processes. The following local
processes may have influenced global climatic oscillations in
the study area: during the middle part of the Oligocene, the
Paratethys returned to open marine conditions. Tropical water
incursion from the Indian Ocean, which was described around
the Oligocene/Miocene boundary (Rögl 1999), could locally
minimize the impacts of global cooling.
The culmination of the MMCO was characterized by a large
marine transgression affecting the entire circum-Mediterra-
nean area, including the Central Paratethys (Rögl 1999; Popov
et al. 2004; Kováč et al. 2007; Piller et al. 2007). The trans-
gression enabled the incursion of warm Indo-Pacific water
into the Paratethys. Moreover, the Central Paratethyan Basin
was at that time strongly influenced by the so-called “Styrian
phase” of tectonic and volcanic activity (Rögl 1998).
The aim of this work is to analyse the specific imprint of
global climatic events on the subtropical epicontinental sea,
as characterized by local oscillations in sea-water chemistry
and/or nutrient content. In littoral to upper bathyal environ-
ments, sensitivity of ecosystems to sea-level oscillations can
be expected; however, local sea-level cycles can differ from
global ones due to tectonic influence. It is also expected that
tectonic and volcanic activity can change geomorphology,
seafloor topography and seaways connecting the Central
Paratethys with surrounding areas, which could influence
regional atmospheric circulation, the origin and circulation of
water masses, and eventually local mesoclimate.
To determine climatic events based on oxygen and carbon
isotopic data in the study area is problematic due to the small
water body of the Paratethys and its restrictions in circulation
to the world ocean causing local oscillations in water chemis-
try. In the Middle Miocene of the Carpathian Foredeep, the
stable isotope record reflects more salinity than temperature
oscillations (Scheiner 2015). Furthermore, the foraminiferal
tests from the Oligo-Miocene “Schlier” are recrystallized and
unsuitable for isotopic analysis. Therefore, two pronounced
cooling events (the Oligo-Miocene and Middle Miocene
cooling) were identified from the palaeobotanical interpre-
tation (mainly palynological data; e.g., Planderová 1990;
Doláková et al. 2014). Foraminiferal and calcareous nanno-
plankton events were used to increase resolution of the record
based on the terrestrial plants around these cooling events by
providing further subdivision of the time interval of the cooling
event. Statistically significant differences in the composition
of foraminiferal and calcareous nannoplankton assemblages
were defined and used for palaeoenvironmental interpre tation.
Finally, points at which palaeoenvironmental changes and
global climatic events coincide, are paid further attention in
the discussion.
Regional setting
The area of the Central Paratethys examined in this study
includes the Pannonian Basin system and the Carpathian Fore-
land basins (Seneš 1961; Fig. 1).
The Late Oligocene/Early Miocene climatic oscillations
have been studied in the northern region of the Buda Basin
(local geomorphological unit called the “South Slovak Basin”),
which is a part of the Pannonian basin system. The strati-
graphy, lithostratigraphy and sedimentology of this area were
summarized in Vass (1995), Vass et al. (1979, 1993) and Vass
Fig. 1. Locations of studied sections.
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& Elečko (1989). The succession starts with dark grey siltstones
to claystones with evenly distributed CaCO
3
(14.2–18.3 %).
They are overlain by monotonous calcareous siltstones to fine
sandstones with mica and phytodetritus at dominant bedding
surfaces (“Schlier”) within the basin infill. Glauconite-rich
intercalations and horizons with increased CaCO
3
were recor-
ded in the transitional intervals between these lithotypes. In the
marginal part of the basin, lagoonal evaporites (dolomite,
anhydrite) were deposited (Vass et al. 1979). The overlying
siltstones vary in silt and clay content, shell debris, intensity of
bioturbation, and CaCO
3
content, which oscillates between 1.1
to 49.2 % (Vass et al. 1979, 1993; Vass & Elečko 1989). More
variegated lithology was recorded in marginal facies, where
organodetrital carbonate bodies are replaced by conglomerates
and deltaic deposits (Vass et al. 1979, 1993; Vass & Elečko
1982, 1989; Šutovská-Holcová et al. 1993; Vass 1995).
The Middle Miocene samples have been collected from
sections in the Carpathian Foredeep. The Early to Middle
Miocene Carpathian Foredeep is a peripheral foreland basin
that developed from the subsurface loading of the Alpine–
Carpathian orogenic belt on the passive margin of the Bohemian
Massif. The Carpathian Foredeep exhibits striking lateral
varia tions in basin width, depth, and stratigraphy of deposits,
along with variations in the pre-Neogene basement composi-
tion and tectonic subsidence. The basin continued to the south
(the Alpine Foredeep/Alpine Molasse Zone) and to the NE
(Polish part of the Carpathian Foredeep) (Oszczypko 1998;
Nehyba & Šikula 2007; Nehyba et al. 2008). The pelitic sedi-
ments (“Tegel”) with sandstone intercalations and biohermal
bodies strongly dominate the basin volumetrically. These
mudstones vary in silt and clay content, shell debris, intensity
of bioturbation and sedimentary structure. The mudstones are
interpreted as dominantly outer shelf deposits or hemipela-
gites (Papp et al. 1978; Nehyba et al. 2008).
Materials and methods
The studied material originates from six boreholes from the
South Slovak Basin (Oligocene/Miocene interval): LR-9,
LR-10 (Šutovská 1987), LR-2, EH-1, EH-2, ČO-1 (marginal
deltaic facies; Šutovská-Holcová et al. 1993), two parastrato-
type sections (Budikovany and Bretka) of the local Egerian
stage (Báldi & Seneš 1975), five boreholes from the Carpa-
thian Foredeep (Middle Miocene): RY-1 (Kopecká 2012),
ZIDL-1 and ZIDL-2 (Doláková et al. 2014), LOM-1 (Holcová
et al. 2015), OV-1 (Nehyba et al. 2016) and one from the
Danube Basin: ŠO-1 (Papp et al. 1978) (Fig. 1). Lithology,
location and biostratigraphical correlation of the studied
sections are given in Fig. 2. In total, 182 samples from the
Lower Miocene and 246 samples from the Middle Miocene
were analysed.
Foraminifera were studied in the 63 to 2000 μm fractions.
Approximately 200 to 300 specimens of foraminifera from
each sample were determined and their abundances were used
for statistical analysis. The calcareous nannoplankton was
studied in the same samples as the foraminifera. The abun-
dance of nannoplankton was expressed semiquantitatively as
the number of specimens in the visual field of the microscope
(Zágoršek et al. 2007). Approximately 200 to 500 specimens
of calcareous nannoplankton were determined from individual
samples and used for further statistical analysis.
Foraminiferal, as well as calcareous nannoplankton assem-
blages were statistically analysed using the software PAST
developed for palaeontologists (Hammer et al. 2001). For
grouping samples non-metric multidimensional scaling
(n-MMDS) was used; Kruskal-Wallis tests were applied for
testing differences between biostratigraphically distinguished
intervals, and relations among individual taxa were quantified
by Spearman’s correlation coefficient.
Results
Calcareous nannoplankton and planktonic foraminiferal
biostratigraphical events
Biostratigraphical events around the Oligocene/Miocene
boundary
The succession of bioevents from the broader Oligocene/
Miocene boundary interval in the study area was synthesized
by Holcová (2001, 2005), Ozdínová & Soták (2014) and
Grunert et al. (2015).
(1) The interval between the last occurrence (LO) of Globo-
rotalia opima (dated at 26.9 Ma in the global ocean; Gradstein
et al. 2012) and the first occurrence (FO) of Globigerinoides
primordius (dated at 26.1 Ma in the global ocean; Gradstein et
al. 2012) can be correlated in the study area with lithological
change from dark-grey claystones to light grey siltstone to
sandstone (“Schlier”).
In contrast to the biostratigraphic events, the change in
litho logy is very distinct and can be used as a correlation
horizon if the position of the FO Globigerinoides primordius
is unclear. Though dates of biostratigraphical events in the
Central Paratethys may not exactly coincide with the record of
the global ocean, this interval likely corresponds to the period
of global warming between 26.5 and 25.2 Ma (Pekar et al.
2005; Villa & Persico 2006). This warming event from the
same level was also described by Ozdínová & Soták (2014) in
the studied area.
(2) The last common occurrence (LCO) of Reticulofenestra
bisecta. The LO of this species is often used to approximate
the Oligocene/Miocene boundary (Berggren et al. 1995; Young
1998; Ozdínova & Soták 2014). However, rare reworked speci-
mens of R. bisecta occur commonly in the Lower Miocene of
the Pannonian Basin (NN2 to NN4 Zones; Holcová 2005).
Therefore, only the last continuous occurrence of R. bisecta
was used as a biostratigraphical marker. The event is dated to
23.1 Ma in the global ocean agreeing with the global Mi-1
cooling event (23.2 Ma; Gradstein et al. 2012). Though the age
of the LCO of R. bisecta in the Central Paratethys may differ
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from the world ocean, the cooling around this event has been
established by Planderová (1990) in the South Slovak Basin.
(3) The FO of Helicosphaera scissura and the FO of
Discoaster druggii are isochronous events in the Central Para-
tethys (Holcová 2005). Helicosphaera scissura is, however,
more abundant and its FO is more easily determined.
(4) The FO of Helicosphaera ampliaperta is a well defined
event in the Central Paratethys (Holcová 2002, 2005). I
n the
Fig. 2a. Biostratigraphic correlations, lithology and sampled intervals of studied sections — Oligocene–Miocene boundary interval.
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Fig. 2b. Biostratigraphic correlations, lithology and sampled intervals of studied sections — Middle Miocene.
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Mediterranean region, the event was dated to approximately
20 Ma (Fornaciari
&
Rio 1996).
Events (3) and (4) approximately correlate with the dis-
appearance of deciduous forests in the study area (Planderová
1990) which can be interpreted as warming. Elsewhere in the
Central Paratethys area (the North Alpine Foreland Basin),
a carbon isotope excursion indicating the cooling event was
recorded between the FO of Helicosphara carteri and the
FO of H. scissura (Grunert et al. 2015), supporting the use
of the FO of H. scissura as a marker of the beginning of
warming.
Based on these events, the studied sections were subdivided
into the following intervals (Fig. 2a):
The Oligocene interval Oli-1 ranges from the base of the
studied sections to the FO of Globigerinoides primordius
whereas lithology changes from dark claystones to light silt-
stones marking the beginning of the interval Oli-2 that ends
with the LCO of Reticulofenestra bisecta. The top of the
Miocene interval Mio-1 is defined by the FO of Helicosphaera
scissura and/or the FO of Discoaster druggii and is overlain
by interval Mio-2 ending with the FO of Helicosphara ampli-
aperta. Intervals Oli-2 and Mio-1 are lithologically uniform.
Around the Mio-1/Mio-2 boundary, the marginal limestone
bodies ware replaced by marginal coarse clastics.
The early Middle Miocene biostratigraphical events
The dates of the Middle Miocene bioevents in the world
ocean (Gradstein et al. 2012) differ from the astronomically
calibrated dates from the Mediterranean area (Abdul Azis et
al. 2008). Due to the communication of the Central Para-
tethyan Sea with the Mediterranean (Rögl 1998), correlation
with the Mediterranean dates is more suitable.
(1) The FO of Orbulina suturalis is dated in the Mediterra-
nean area to 14.5–14.6 Ma; (Iaccarino et al. 2011) and in the
Central Paratethys to 15.03–14.2 Ma (Hohenegger et al.
2009a; Selmeczi et al. 2012; de Leeuw et al. 2013). Although
some dating may not be fully accurate, all these ages
correspond to a period slightly after the culmination of the
MMCO.
(2) The use of the LCO of Helicosphaera waltrans was prio-
ritized over using of its LO due to the common occurrence of
reworked individuals. Dating of the event to 14.38 Ma can be
approximated from the base of the Soos drill in which
H. waltrans was not recorded (Hohenegger et al. 2009b).
On the other hand, H. waltrans was recorded in a horizon
radiometrically dated to 14.39 Ma (the Styrian Basin;
Hohenegger et al. 2009a), which indicates that the event had to
occur at approximately 14.38 Ma which agrees with the dating
of this event in the Mediterranean (14.357 Ma; Abdul-Azis et
al. 2008). The upper boundaries of all studied sections are
erosive. However, Sphenolithus heteromorphus occurs in all
samples, which indicates an age younger than 13.5 Ma for the
upper boundary of the studied interval.
In the Middle Miocene, two intervals were studied (Fig. 2b):
the MM-1 interval is defined by the FO of Orbulina (base) and
LCO of Helicosphaera waltrans (top) and the MM-2 interval
ended with the erosive boundary with Sphenolithus hetero-
morphus occurrence.
Distribution of foraminiferal and calcareous nannoplankton
taxa in biostratigaphically defined intervals
The Late Oligocene/Early Miocene results of the n-MMDS
showed differences between Oligocene and Miocene calca-
reous nannoplankton assemblages (Fig. 3a) which statistically
significantly differ in the values of the first coordinate
(Fig. 3b). The “core” samples from the Mio-2 interval indicate
high similarity among the majority of assemblages from this
interval (Fig. 3a).
Benthic foraminiferal assemblages from the Miocene are
highly variable in comparison with Oligocene ones (Fig. 3c).
The values of the first coordinate differentiate assemblages
from the Mio-2 interval from older ones (Fig. 3d).
The box plots supported by Kruskal-Wallis tests (Fig. 3e)
show that assemblages from the Oli-1 interval differ in having
higher abundances of Uvigerina spp., the Gyroidina–Gyroido-
inoides-group, and miliolids. In both Oligocene intervals, the
highest relative abundances of Helicosphaera euphratis and
Cyclicargolithus floridanus were recorded. The Oli-2 interval
is characterized by abundant Coccolithus pelagicus, Pullenia,
and Melonis, monoserial lagenids, and tubular agglutinated
foraminifera. The Mio-1 interval differs from other intervals
by an increase in Bolivina spp. without sculpture; markedly
increased Reticulofenestra minuta, and the Cassidulina–
Globo cassidulina group also remained high in the Mio-2
interval. In this interval, the variability of cibicidoid abun-
dances also increased, relative abundances of Cyclicargolithus
floridanus decreased and large Helicosphaera euphratis nearly
disappeared. The Mio-2 interval is characterized by increases
in the abundances of large endemic Reticulofenestra excavata,
Discoaster spp., Helicosphaera scissura, and the benthic
foraminiferal genera Ammonia, Elphidium, and Porosonion.
The Oli-1 and Mio-1 intervals are associated with increased
abundances of Lenticulina spp., while abundances of Nonion
commune and Pontosphaera multipora increased in the Mio-2
and Oli-2 intervals.
Relations between taxa characteristic for the Oligo-Miocene
intervals were enumerated using statistically significant
correlations among relative abundances of taxa (Fig. 4):
(1) Hoeglundina, Uvigerina and Gyroidina co-occur with
Reticulofenestra bisecta and characterize the Oli-1 interval.
Lenticulina spp. also correlates with this group, but the genus
occurs in the Oli-1 and Mio-1 intervals.
(2) Miliolids, abundant in the Oli-1 interval, positively
correlate with Braarudosphaera bigelowi.
(3) Melonis, Pullenia, monoserial lagenids, and tubular
agglutinated foraminifera co-occur with Coccolithus pela-
gicus, Helicosphaera euphratis and Pontosphaera multipora;
this group of taxa dominated in the Oli-2 interval. Relative
abundances of Nonion commune also correlate with this group,
though the species is abundant also in the Mio-2 interval.
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Fig. 3. Differences between late Oligocene to early Miocene benthic foraminiferal and calcareous nannoplankton assemblages from bio-
stratigrafically defined Oli-1, Oli-2, Mio-1 and Mio-2 intervals: a — classification of calcareous nannoplankton assemblages using non-Metric
Multidimensional Scaling (n-MMDS), b — statistically significant differences of values of the first coordinate from plot a; c — classification
of benthic foraminifera assemblages using n-MMDS, d — statistically significant differences of values of the first coordinate from plot c;
e — statistically significant differences in relative abundances of benthic foraminiferal and calcareous nannoplankton taxa from Oli-1, Oli-2,
Mio-1 and Mio-2 intervals.
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(4) Bolivina spp., characteristic of the Mio-1 interval,
correlate with taxa abundant in both Miocene intervals:
Cassidulina, Reticulofenestra minuta and R. haqii. Bolivina
spp. are also contemporary with Lenticulina spp., which
dominates in the Oli-1 and Mio-1 intervals.
(5) The group of genera Elphidium, Ammonia, Porosononion
and Thoracosphaera spp. characterizes the Mio-2 interval.
Moreover, Cassidulina co-occurs with these genera but is
common in both Miocene intervals.
In the Oligocene-Early Miocene interval planktonic fora-
minifera are rare (up to 20 %) and poorly preserved; assem-
blages can therefore be characterized only qualitatively.
Globigerinoides primordius appeared at the beginning of the
Oli-2 interval, dominated by 4-chambered Globigerina spp.
The Mio-1 interval is characterized by small 5-chambered
globigerinids. In the Mio-2 interval, four-chambered globige-
rinids reappeared and the FO of Globigerinoides trilobus is
observed.
The Middle Miocene climatic events
The n-MMDS showed a larger variability of benthic, as well
as planktonic foraminiferal and calcareous nannoplankton
assemblages during the MM-2 interval in comparison with the
MM-1 interval (Fig. 5a–c). The MM-2 interval is charac-
terized by a bimodal distribution of assemblages whereas
assemblages from the MM-1 interval are less dispersed.
The most pronounced similarity is found for planktonic fora-
minifera from the MM-1 interval, which are concentrated into
a compact “core” group in the plot of the n-MMDS coor-
dinates (Fig. 5b).
Box plots supported by Kruskal-Wallis tests (Fig. 5d)
showed higher relative abundances of monoserial lagenids,
Melonis, Pullenia, Nonion commune, Bulimina spp., 4-cham-
bered Globigerina bulloides-G. praebulloides group, Globi-
gerinella regularis, and large Helicosphaera spp. (>7 µm)
in assemblages from the MM-1 interval. Asterigerinata
planorbis, Elphidium spp., Cibicidoides spp., Cassidulina,
Globocassidulina, miliolids, large foraminifera (mainly
Amphistegina spp.), Ammonia spp., biserial agglutinated,
Paragloborotalia mayeri, 5-chambered Globigerina ottnan-
giensis and Turborotalita quinqueloba, Reticulofenestra haqii,
Umbilicosphaera jafari, and reworked Palaeogene taxa
reached higher abundances in the MM-2 interval, while
relative abundances of Reticulofenestra minuta were more
varied (Fig. 5d).
The Spearman coefficient enables us to express the follo-
wing relations among relative abundances of foraminifera and
calcareous nannoplankton taxa (Fig. 6):
(1) Strong positive correlations among Asterigerinata
planorbis, Elphidium spp., large foraminifera, Cassidulina
spp., Cibicidoides spp., Ammonia sp., and miliolids from the
MM-2 interval. Reticulofenestra minuta, 5-chambered Turbo-
rotalita quinqueloba and Globigerina ottnangiensis, plexus of
very small Globigerina spp. (<100 µm), Globorotalia mayeri,
and Bolivina spp. can also be added to this group.
(2) The MM-1 interval is characterized by a group com-
posed of Nonion commune, 4-chambered Globigerina prae-
bulloides–G. bulloides group, Globigerinella regularis, and
large Helicosphaera spp. (mainly H. waltrans and H. carteri).
(3) A group of taxa positively correlated with Globigeri-
noides spp. and Orbulina suturalis–Praeorbulina circularis
was recorded in both intervals, and co-occurs with: (i) Globo-
rotalia bykovaye, Uvigerina spp. and Lenticulina spp. in both
intervals; (ii) monoserial lagenids, Melonis, Pullenia, and
Coccolithus pelagicus in the MM-1 interval; and (iii) aggluti-
nated foraminifera (biserial), Hansenisca, Umbilicosphaera
jafari and Reticulofenestra haqii in the MM-2 interval.
Calcareous nannoplankton events in relation to climatic
oscillations
The most prominent changes during the Mio-1 interval
(Fig. 7) included a decrease in Cyclicargolithus floridanus and
an increase of Reticulofenestra minuta. Extinctions of the
largest reticulofenestrids (Cyclicargolithus abisectus and
Reticulofenestra bisecta) can be correlated with the beginning
Fig. 4. Statistically significant (p < 0.05) correlations among relative
abundances of benthic foraminiferal and calcareous nannoplankton
taxa, enumerated by Spearman correlation coefficient, from the late
Oligocene to early Miocene. Groups of taxa with high correlation
coefficients and their affinities to Oli-1, Oli-2, Mio-1 and Mio-2 inter-
vals are indicated.
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of the Mio-1 interval, although the exact extinction level is
hard to determine due to reworking. During the subsequent
Mio-2 interval, the extinct large reticulofenestrids are substi-
tuted by large endemic Reticulofenestra excavata, and the
abundance of R. minuta declined (Fig. 7b). The percentage of
large Helicosphaera euphratis also decreased during the
Mio-1 interval, whereas that of the new taxon H. carteri
increased. In the following Mio-2 interval, new large helico-
sphaeras appeared: first H. scissura, then H. ampliaperta
(Fig. 7b).
Changes in calcareous nannoplankton assemblages during
the Middle Miocene are less prominent than in the Oligocene/
Miocene interval. Similarly to the Mio-1 interval, abundances
of large reticulofenestrids (R. excavata, C. floridanus) decrea-
sed during the MM-2 interval (Fig. 8a, b). Additionally, abun-
dance of large helicosphaeras, characteristic for the MM-1
interval (alternating horizons with H. waltrans and H. carteri),
gradually subsided and abundance of small H. walbersdor-
fensis increased in the MM-2 interval (Fig. 8c, d).
Interpretation and discussion
Transition between the Oli-1 and Oli-2 intervals (ca 26.5Ma;
Fig. 9a)
As was discussed above, the Oli-1/Oli-2 boundary interval
may be correlated with the global late Oligocene warming
recognized by an increase in temperate-water taxa starting at
26.5 Ma (Vila & Persico 2006) or the appearance of a warm
deep-water mass between 26.5 and 25.2 Ma (Pekar et al.
2005). Then the Oli-1 interval represents the end of the
Oligocene cooling.
In the study area, nanno- and microfossils together with the
dark claystones of the Oli-1 interval enable the interpretation
of high nutrients and an O
2
-depleted environment at the sea
floor during the cold interval. The genera Uvigerina and
Gyroidina, characteristic of this lithotype, typify regions of
high organic productivity and a sustained flux of organic
matter to the sea floor as the most important factor controlling
their distribution (Caralp 1989; Hermelin 1992; Sjoerdsma &
van der Zwaan 1992; Miao & Thunell 1993; Sen Gupta &
Machain-Castillo 1993; Rathburn & Corliss 1994). Moreover,
Uvigerina is a traditional indicator of oxygen-depleted
water (Kaiho 1994; Murray 2006). Gyroidina is interpreted as
an epifaunal detritivore occurring at the sediment-water inter-
face (Murray 2006). Oxygen and carbon stable isotopic values
(Scheiner 2015) showed a similarity between the life habitats
of Gyroidina and that of Melonis, both preferring high organic
productivity areas (Thomas et al. 1995). Large Lenticulina
spp., another abundant benthic genus, are considered to be
a high-oxygen-consuming epifaunal element (Kaiho 1994;
van der Zwaan et al. 1999). However, the oxygen require-
ments of Lenticulina are classified inconsistently: after the
morphotype analysis of Rosoff & Corliss (1992) and Kouwen-
hoven & Van der Zwaan (2006) Lenticulina species were con-
sidered oxyphilic, while Kaiho (1994) classified Lenticulina
spp. as suboxic indicators. This discrepancy agrees with its
opportunistic character, as interpreted since the Jurassic (Peryt
& Lamolda 1996; Reolid & Martínez-Ruiz 2012), and
Lenticulina may live in oxic, as well as dysoxic, environments.
However, horizons with large Lenticulina wedged between
sediments dominated by Uvigerina and Gyroidina may indi-
cate perhaps an increase in oxygen content followed by its
decrease. In any case, the oxygen content at the sea floor
varied, though a hypoxic palaeoenvironment rich in nutrients
prevailed with occasional episodes of oxygen increase.
In the surface water, Cyclicargolithus floridanus dominant
during the Oli-1 interval (together with Cyclicargolithus
abisectus), was previously considered to be an indication of
temperate water (Wei & Wise 1990). However, its temperature
affinity was questioned by Persico & Villa (2004). The species
was more likely eurytopic, thriving under a large spectrum of
environments (Shcherbinina 2010). It also confirms the obser-
vations of Sachsenhofer et al. (2010), who recorded blooms of
Cyclicargolithus floridanus in both the organic-rich zone and
the overlying organic-poor formation. The characteristic
calca reous nannoplankton genus Thoracosphaera is a general
proxy for oligotrophy or stratification (Höll et al. 1998; Vink
2004). Isotopic ratios for the common planktonic foraminifera
group paragloborotaliids indicate that Oligocene represen-
tatives calcified in the upper-thermocline depth (Poore &
Matthews 1984
;
Wade et al. 2009). All these data confirm
stratification of the water column with oscillation of palaeo-
environmental parameters in the surface layer. A clear indi-
cator of the quantity of nutrients in the upper part of the water
column is absent.
Marginal facies are characterized by miliolids, mainly Quin-
queloculina spp., representing epifaunal genera often living on
plants and tolerating salinity increases (Murray 2006). Milio-
lids are accompanied by Braarudosphaera bigelowi, which
also indicates fluctuating salinity conditions (Bartol et al.
2008). It agrees well with the occurrence of evaporites (Vass et
al. 1979), all of which confirm salinity increase in the margi nal
part of the basin, probably as a consequence of low rainfall.
Aridity is also expected from the high abundance of micro-
fossils in the sediment, caused rather by low terrigenous input
than by high primary productivity.
The lithological change from dark grey claystones to light
grey siltstones with glauconite-rich and carbonate intercala-
tions at the base (Vass et al. 1993) can be correlated with
a change in the abundance and preservation of foraminiferal
tests at the Oli-1/Oli-2 interval boundary. Abundant, large,
well-preserved tests with pyrite infilling were substituted
by less abundant, smaller foraminifera (Holcová 2001).
The absence of pyrite infilling reflects an increase of oxygen
content in the sediment caused by a regional palaeogeographic
change from an isolated to an open marine basin (Báldi 1986;
Rögl 1998; Popov et al. 2004). Glauconite and carbonate
accumu lation at the base of siltstones already indicates oxyge-
nated to mildly reducing marine environments and continuing
very low sedimentation rates (McRae 1972; Odin & Matter
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Fig. 5. Differences between the Middle Miocene foraminiferal and calcareous nannoplankton assemblages from biostratigraphicaly defined
MM-1 and MM-2 intervals; a–c: classification of assemblages using non-metric multidimensional scaling (n-MMDS): a — calcareous
nannoplankton, b — planktonic foraminifera; c — benthic foraminifera; d — statistically significant differences in relative abundances of
foraminiferal and calcareous nannoplankton taxa from MM-1 and MM-2 intervals.
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1981; Amorosi 1997). The subsequent decrease in forami-
niferal abundance might reflect increased sediment input
caused by climatic change from an arid to a humid climate.
Oli-2 interval (26.5 to 23.1 Ma; Fig. 9b)
Based on local palynological data, the Oli-2 interval repre-
sents a warm subtropical condition without arctotertiary
elements (Planderová 1990). Though timing of biostrati-
graphic events marking the boundaries of this interval in the
world ocean and the Central Paratethys can differ, correlation
with the global late Oligocene warming is generally expected
(26.5 to 23.1 Ma; Pekar et al. 2005; Gradstein et al. 2012).
Helicosphaera spp., with a peak at the base of the interval,
has an affinity to warm mesotrophic to oligotrophic water and
high light intensities (Knappertsbusch 1993; Ziveri et al. 1995,
2004; Haidar & Thierstein 2001). The horizon may indicate
a palaeogeographic event — an influx of warm, oceanic water
after the reopening of communication between the Paratethys
and the Indo-Pacific realm (Rögl 1998) connected with the
oxygenation of the bottom water. Rögl (1998, 1999) dated this
incursion to the Oligocene/Miocene boundary; our data show
a slightly older age for this event (upper Oligocene, NP25
Zone). Later, the abundance of the high-nutrient marker
Coccolithus pelagicus (Okada & McInyre 1979; Winter et al.
1994; Cachao & Moita 2000) increased. This may correspond
to an increase in terrigenous nutrients as a result of increased
precipitation.
The quality of the surface water is also indicated by the
planktonic foraminifera. The Upper Oligocene Globigerina
bulloides-like tests, dominating the studied samples, have
δ
18
O values among the lightest of the assemblage, indicating
a shallow mixed layer habitat for these foraminifera as well.
However, the δ
13
C signal suggests a symbiotic association
with dinoflagellates (Poore & Matthews 1984
); therefore the
Upper Oligocene Globigerina bulloides group may not neces-
sarily
indicate strongly eutrophic areas as the
modern plank-
tonic foraminifera Globigerina ex gr. bulloides (Schiebel et al.
1997).The isotopic ratios of the new species Globigerinoides
primordius are very similar to those of Globigerina cf.
bulloides in the same size fraction, pointing to a similar
mixed-layer and symbiotic life habit (Poore & Matthews 1984
;
Wade et al. 2009). Therefore, the coexistence of these species
in the upper Oligocene cannot indicate seasonal alternation of
mixed and stratified water, as in Recent assemblages, and only
mixed water can be inferred. The appearance of new globi-
gerinid forms with secondary apertures on the spiral side is
considered to be a response to the Late Oligocene warming
(Jenkins 1973).
Melonis, Pullenia, and Nonion commune, characterizing
sea-floor conditions during the Oli-2 interval, indicate a high
supply of organic material to the sea floor (Caralp 1989;
Hermelin 1992; Sjoerdsma & van der Zwaan 1992; Miao &
Thunell 1993; Sen Gupta & Machain-Castillo 1993; Rathburn
& Corliss 1994). Their classification as oxic vs. suboxic taxa
varies (Kaiho 1994, 1999; Schönfeld 2001; Kouwenhoven &
Van der Zwaan 2006), which might reveal that these genera
can live under oxic conditions as well as tolerating dysoxic
and suboxic pore-water. The co-occurrence of high-nutrient
markers, planktonic Coccolithus pelagicus and benthic
Melonis, Pullenia, and Nonion commune, might indicate
an upwelling regime, but the absence of other upwelling
indicators, as well as the symbiotic life habitat of the Upper
Oligocene Globigerina bulloides group, strongly challenges
this hypothesis; the mixing of water may have been caused,
instead, by riverine input.
Horizons with agglutinated foraminifera gradually expanded
in the upper part of the interval. In general, agglutinated fora-
minifera may reflect an oligotrophic character in the benthic
ecosystem (Jorissen et al. 1998). This finding challenges the
observations of Kaminski et al. (1988), Jones (1999), Kender
et al. (2005), Jones (2006) and Kender et al. (2008) who
recorded exceptionally high abundances of agglutinated fora-
minifers in delta fan environments with high sedimentation
rates and strong terrestrial input. The recorded rounded plani-
spiral (Haplophragmoides, Cyclammina) and tubular uni-
locular (Bathysiphon) morphotypes are considered epifaunal
Fig. 6. Statistically significant (p < 0.05) correlations among relative
abundances of foraminiferal and calcareous nannoplankton taxa,
enumerated by Spearman correlation coefficient, from the Middle
Miocene. Groups of taxa with high correlation coefficients and their
affinities to MM-1 and MM-2 intervals are indicated.
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Fig. 7. Variability of calcareous nannoplankton assemblages in Oli-1, Oli-2, Mio-1 and Mio-2 intervals. a — Variability in relative abundances
of reticulofenestrids and helicosphaeras in LR-9, LR-2, EH-1 boreholes and Budikovany and Bretka sections; b — Histograms summarizing
abundances of reticulofenestrids and helicosphaeras in Oli-1, Oli-2, Mio-1 and Mio-2 intervals.
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Fig. 8. Variability of calcareous nannoplankton assemblages in MM-1 and MM-2 intervals. a — Variability in relative abundances of
reticulofenestrids in LOM-1, OV-1, RY-1 and ZIDL-1, 2 boreholes; b — Histograms summarizing abundances of reticulofenestrids in
MM-1 and MM-2 intervals; c — Variability in relative abundances of helicosphaeras in LOM-1, OV-1, RY-1 and ZIDL-1, 2 boreholes;
d — Histograms summarizing abundances of helicosphaeras in MM-1 and MM-2 intervals.
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to shallow infaunal active deposit and suspension feeders
(Tyszka 1994; Van den Akker et al. 2000; Kaminski et al.
2005; Reolid et al. 2008; Nagy et al. 2009). The frequent abun-
dance of Bathysiphon filiformis indicates a high nutrient flux
of shelf-derived organic matter to the seafloor (Gooday 1993,
1996; Kaminski et al. 2005; Murray 2006; Kender et al. 2008).
For Early Miocene Bathysiphon-rich deposits, the TOC/S
ratios suggest oxygen-depleted conditions with degraded
organic material (Grunert et al. 2013). Similarly to oscillations
of CaCO
3
content in siltstones (Vass et al. 2007), varying
abundances of agglutinated foraminifera in these deposits
indicate variance in the influx of terrigenous material, corre-
sponding to variance in continental nutrient input. Hyposaline
Ammonia spp. in the marginal part of the basin (Vass et al.
2007) also reveal a rather humid climate with salinity oscilla-
tions as a consequence of high riverine influx.
Generally, mixed water with high nutrients can be
inferred for the probably warm Oli-2 period. Disturbances,
including varying terrigenous input and varying quantity and
quality of nutrients, can be expected in the upper part of the
interval.
Mio-1 interval (ca 23 Ma; Fig. 9c)
In the uppermost Oligocene, organodetritic limestones
appeared in the marginal part of the basin, for which
strontium isotope dating provides an age of 23.39 Ma (Less et
al. 2015). The production of limestones points to decreased
terrigenous input before the Mi-1 cooling event. Besides large
herbivo rous oligotrophic foraminifera (Miogypsina, Lepido-
cyclina, Hetero stegina; Murray 2006), the limestones
contain the small opportunistic suspension feeder Cibici doides
sp. which may indicate episodic input of nutrients in
suspension.
In the central part of the basin, no lithological change was
observed. In biota, the LCO of Reticulofenestra bisecta is con-
nected with occurrence of arctotertiary elements (Planderová
1990). Also protist assemblages changed: Lenticulina spp.,
also characteristic of the Oli-1 (cold) interval, reappeared.
Low-oxygen and high-nutrient Uvigerina and Melonis,
accompanying Lenticulina spp. during the Oli-1 interval, were
substituted by smooth-walled Bolivina spp. In contrast to
Uvigerina and Melonis, Bolivina is
highly adaptable and tole-
rant of a wide range of different factors or combinations of
environmental factors (e.g., Camacho et al. 2015) and the sub-
stitution of taxa points to an unstable environment.
A new
feeding strategy is represented by the Cassidulina group,
which reveals an influence of seasonal phytodetritus pulses
(Gooday 1993). Planktonic assemblages are characterized by
substitution of
large reticulofenestrids by small ones,
indica-
ting environmental stress with quick changes within that
environment, including oscillations of salinity (Wade &
Brown 2006) and nutrient content (Flores et al. 1997;
Wells & Okada 1997; Kameo 2002). However, other authors
recorded abundant s
mall Reticulofenestra in high-nutrient
conditions (Okada
&
Honjo 1973;
Takahashi
&
Okada 2000;
Bauman
&
Freitag 2004). Therefore, there are two explana-
tions: unstable conditions or a high-nutrient environment.
Due to the absence of other high-nutrient markers, instability
is the preferred explanation. The common planktonic fora-
miniferal species
Turbo rotalita quinqueloba, which substi-
tuted for four-chambered Globigerina spp., is a shallow-
dwelling marker of cold, non-stratified waters (Rohling et
al. 1993).
Generally, instability, decreased nutrients, phytodetritus
pulses, and decreased terrigenous input due to aridity are
expected for the cold interval. This interpretation is corro-
borated by palaeoclimate analysis based on plant macrofossils
(Erdei et al. 2007), which inferred cooling, seasonality increase
and aridity in the Pannonian domain.
Mio-2 event (19–22 Ma; Fig. 9d)
The reappearance of palms from the genera Arecipites,
Myricipites, etc. (Planderová 1990) indicate warming during
this interval.
Expansion of the shallow-water coarse clastic facies,
including the deltaic one, reflects the local palaeogeographic
and palaeotectonic event: tectonically triggered shallowing
(Vass et al. 1993). High-tide markers indicate changes of basin
configuration leading to high tides (Sztanó & de Boer 1995).
The gradual substitution of marginal limestones by coarse
clastics of the Bretka Formation is well documented and dated
to 22.4–21.9 Ma by strontium isotopes (Less et al. 2015) and
indicates an increase in humidity. Shallowing-influenced com-
position of the benthic foraminifera assemblage primarily
consists of increase in the relative abundances of Elphidium,
Ammonia and Porosononion. In addition, these genera indi-
cate a salinity decrease, which can also be correlated to
increased precipitation. In the central part of the basin, abun-
dances of Cassidulina and Nonion commune rose, showing
enrichment in nutrients mainly due to the strong influence of
seasonal phytodetritus pulses (Gooday 1993; Murray 2006).
In the upper part of the water column Globigerinoides trilobus
appeared and four-chambered Globigerina ex gr. praebul-
loides reappeared. The co-occurrence of “real” Globigeri-
noides with Globigerina praebulloides may represent seasonal
aspects: Globigerina in the colder season with mixed water,
often connected with seasonal upwelling, and Globigerinoides
in the warmer period with stratified water (Conan et al. 2002;
Peeters et al. 2002; Keigwin et al. 2005). This is in agreement
with the seasonality in phytodetritus pulses predicted from the
increase of cassidulinids. Persistent small Reticulofenestra
minuta records local and/or seasonal stress in the surface layer,
alternating with stable marine conditions inferred from the
appearance of large endemic Reticulofenestra excavata as
well as Helicosphaera scissura.
MM-1 interval (14.9–14.4 Ma; Fig. 10a)
Mg/Ca data from foraminiferal tests from the marine envi-
ronment as well as palynological analysis enable us to infer
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Fig. 9. Model of palaeobiotope distribution in the epicontinental Central Paratethys sea during the late Oligocene to early Miocene.
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a stable subtropical climate for this interval (Holcová et al.
2015; Scheiner et al. 2016).
The co-occurrence of the planktonic species Globigerina
bulloides-praebulloides, Globigerinella regularis, Globigeri-
noides spp., and Orbulina suggests a seasonal succession of
assemblages characterized by the alternation of warm seasons
with a stratified oligotrophic water and cool seasons with
a mixed upper water column (e.g., Reynold & Thunell 1985;
Rigual-Hernandez et al. 2012; Kuhnt et al. 2013; Salmon et al.
2014). Similarly, the co-occurrence of large Helicosphaera
spp. indicating warm mesotrophic to oligotrophic water
(Knappertsbusch 1993; Ziveri et al. 1995, 2004; Haidar &
Thierstein 2001) with the high-nutrient marker Coccolithus
pelagicus (e.g., Cachao & Moita 2000) suggests an alternation
of warm oligotrophic and colder eutrophic surface waters.
Seasons with cold, mixed water can be connected with local
wind-driven coastal upwelling areas (Conan et al. 2002) as
corroborated by oxygen isotopic data (Scheiner 2015) as well
as blooms of diatoms (Holcová et al. 2015). Predominance of
Globigerinella over Globigerinoides during this interval indi-
cates stable conditions in the warm season, based on the obser-
vation of Schmuker (2000), who recorded Globigerinoides
spp. in higher temperature and salinity variations, while
Globigerinella spp. bloomed in narrower temperature and
salinity ranges. Generally, this regime can be expected during
the whole interval because the planktonic foraminiferal
assemblages represent a compact group based on results of the
nMMDS.
The sea floor was settled by Bulimina spp., monoserial
lagenids, Melonis, Pullenia, Nonion commune, and Uvigerina
spp., associated with high food availability, organic carbon
content in the sediments, and traditionally low oxygen,
although they can also live under oxic conditions (Miller &
Lohman 1982; Caralp 1989; Hermelin 1992; Jorrisen et al.
1992; Sjoerdsma & van der Zwaan 1992; Miao & Thunell
1993; Sen Gupta & Machain-Castillo 1993; Rathburn &
Corliss 1994; Murray 2003). Abundant Uvigerina, Bolivina,
Bulimina, and Melonis typify regions of high organic produc-
tivity and a sustained flux of organic matter to the sea floor, for
example, under areas of upwelling (Thomas et al. 1995),
which support the interpretation of seasonal upwelling from
the planktonic assemblages.
MM-2 interval (14.4–13.8 Ma; Fig. 10b)
The base of this interval can be dated to 14.3–14.4 Ma using
the age calibration of the LCO of Helicoshaera waltrans in the
Central Paratethys (see subchapter “The early Middle Miocene
biostratigraphical events”). This age agrees well with the date
of the Mi-3a event (14.3 Ma; Gradstein et al. 2012) and the
beginning of the MMCT. This climatic change was characte-
rized by an increase in the mean annual range of temperature,
mainly due to decreasing cold-month temperatures in terres-
trial climates (Bruch et al. 2010). Along the opposite coast of
the Central Paratethys sea in Serbia, the Miocene cooling is
also connected with increased seasonality most pronounced in
winter temperatures (Utescher et al. 2007). Increased seaso-
nality, mainly seasonality of precipitation, was corroborated
by the Coexistence Approach in the study area (Doláková et
al. 2014).
The n-MMDS showed a bimodal distribution of benthic
and planktonic foraminiferal and calcareous nannoplankton
assem blages in comparison with the previous stable MM-1
interval, which may be the consequence of higher seasonal
and/or interannual variability. The surface water is characte-
rized by Paragloborotalia mayeri, Globigerinoides spp.,
Orbulina suturalis, five-chambered Globigerina ottnangiensis
and Turborotalita quinqueloba. The coexistence of these taxa
also indicates a seasonal succession of assemblages (e.g.,
Reynold & Thunell 1985; Rigual-Hernandez et al. 2012; Kuhnt
et al. 2013; Salmon et al. 2014), but substitution of Globigerina
bulloides, dominating during the MM-1 interval, by Turbo-
rotalita quinqueloba means cooling during the cold and
high-nutrient season. The lower abundance of Globigerinella
and its replacement by Globigerinoides spp. during the warm
oligotrophic season indicate more variable salinity during
summer conditions leading to hypersaline surface water are
also suggested by the occurrence of hypersaline dinoflagel-
lates (Nehyba et al. 2016) as well as isotopic data (Scheiner
2015). An increase in the calcareous nannoplankton taxon
Umbilicosphaera spp. also shows tolerance to saline water
(Ziveri et al. 2004; Boeckel et al. 2006). Moroever, Umbilico-
sphaera prefers warm, rather oligotrophic water. The unstable
conditions are corroborated by strongly dominating Reticulo-
fenestra minuta as an environmental stress indicator. Size
reduction in helicosphaeras (large Helicosphaera waltras is
gradually substituted by small Helicosphaera walbersdorfensis,
e.g., Holcová et al. 2015) is probably also a response to insta-
bility during the warm season. The lower abundance of
Coccolithus pelagicus can be explained by fewer nutrients.
The sea floor protists are characterized by Asterigerinata
planorbis, Elphidium spp., large foraminifera (mainly Amphi-
stegina spp.), and Ammonia spp., which indicate the expan-
sion of the shallow-water facies due to a sea-level drop.
Regression is corroborated by the increase in reworked
Palaeo gene calcareous nannoplankton taxa. Asterigerinata
planorbis, Elphidium spp. and large foraminifera indicate sea-
grass meadows (Murray 2006) and are independent of phyto-
detritus input as a nutrient source. On the contrary, Cibici-
doides spp., Cassidulina and Globocassidulina need those
nutrients. The riverine influxes may be either seasonal or
catastrophic and repeated in decades-long cycles. This may
correspond to the “extreme climate events” deduced from the
strongly negative excursions in δ
18
O and δ
13
C in the Ostrea
isotope archive (Harzhauser et al. 2011). The interpretation of
horizons with biserial agglutinated foraminifera (Spiroplecti-
nella, Textularia spp., Semivulvulina) is questionable because
of poor knowledge of their ecological preferences in lower
shelf-upper slope habitats. The biserial morphotypes are detri-
tivorous bacterial scavengers adapted to a shallow to deep
infaunal life strategy (Galeotti et al. 2005; Nagy et al. 2009).
Shallow-water Textularia agglutinans is an opportunistic
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species and exhibits a preference for food-enriched conditions
and a tolerance to oxygen deficiency (Barmawidjaja et al.
1995), while Jorissen et al. (1998) indicated that agglutinated
foraminifera reflect oligotrophy on the sea-floor. In any case,
agglutinated foraminifera may display an opportunistic
behaviour which becomes evident after environmental distur-
bances when opportunists rapidly reproduce (Hess et al. 2013).
These disturbances may be correlated with the “extreme
climate events” of Harzhauser et al. (2011). The alternation of
biserial agglutinated foraminifera with cassidulinids may
reflect alternation in the quality of organic matter. Unlike
Cassidulina, which needs fresh phytodetritus near the riverine
influx, degraded organic matter far from its source is sufficient
for agglutinated foraminifers. Miliolids accompanied by
Braarudoshaera bigelowi, occurring in the marginal part of
the basin, represent hypersaline environments (Murray 2006;
Bartol et al. 2008). Together with carbonate production indi-
cating a precipitation decrease, this agrees with the aridifi-
cation events known from the Mediterranean (14.489 Ma;
Hüsing et al. 2010) leading to the Wieliczkian salinity crisis
(
Gazdzicka 1994; Peryt 1997; Oszczypko 1998).
Common features of climatic events in the subtropical
epicontinental sea (the Oligocene and Miocene Central
Paratethys)
The studied warm intervals (Oli-2, Mio-2, MM-1) are
charac terized by enhanced humidity increasing riverine influx
bringing terrigenous nutrients. Where marginal facies are
preserved, coarse clastics, including deltaic deposits with
hypo
saline assemblages, prevail. Tectonically-triggered
shallowing may also lead to broad distribution of hyposaline
facies in warm intervals which are globally correlated with
deepening. Typical taxa characterizing warm intervals include
the high-nutrient markers Coccolithus pelagicus, four-
chambered Globigerina, Melonis, Pullenia, and low-oxic
Bulimina. In addition to an increase in nutrients due to
increased terrigenous input, seasonal upwelling was also
recorded. Its establishment probably depends on atmospheric
circulation with seasonal winds, relating to, for example, the
formation of mountain chains in coastal areas.
At the base of the warm interval, increased large Helico-
sphaera spp. (often new species replacing taxa driven extinct
in the preceding cold interval) indicate the incursion of warm,
oligotrophic surface water into the Central Paratethys. Beside
new large Helicosphaera, new large Reticulofenestra also
appeared.
These characteristics can also be recognized in another
warm interval in the Central Paratethys. Eutrophication, indi-
cated by the appearance of pyritized frustules of diatoms and
tests of pteropods, precipitation increase, interpreted from the
occurrence of deltaic deposits, and hyposaline facies were
recorded in the warm period between the Oi2 and Oi2a-events
(ca. 29–30 Ma; upper NP23–lower NP24). Monospecific asso-
ciations of Uvigerina hantkeni (the “Uvigerina bloom”) at the
base of the NP24 Zone indicate a high-nutrient environment
on the sea floor. The peak in Helicosphaera spp. is followed
by an increase of the high-nutrient marker Coccolithus pela-
gicus (Horváth 1998; Ozdínova & Soták 2014).
Cold intervals (Oli-1, Mio-1 and MM-2) are characterized
by decreased nutrient availability due to decreasing riverine
input as a consequence of aridification. The synchronous
cooling and drying approximately coincident with the Oi2b
and/or Mi1 events is also recorded in Asia, where a causal
linkage between late Oligocene global cooling and central
Asian aridity was determined (Dong et al. 2013). Riverine
input may be seasonal or episodic (decades-long cycles) based
on occurrence of markers of phytodetritus pulses. The coinci-
dence of aridification, pronounced seasonality and episodic
extreme rainfalls caused increased stress and the appearance
of r-specialists, such as small Reticulofenestra and small cibi-
didoids.
Aridity-induced seasonal salinity increase in surface water
may have triggered downwelling circulation, which agrees
with the prevalence of mixed water in cold intervals. This
regime is expected during the MMCT by Brzobohatý (1987)
and Báldi (2006). The central part of the basin is dominated by
opportunistic Lenticulina spp. and biserial agglutinated fora-
minifera. Deficiency in both terrigenous and upwelling-
introduced nutrients caused the enlargement of sea-grass
meadows in the photic zone with herbivorous foraminifera
dependent only on nutrients from the sea-grass ecosystem.
Conclusions
1. The distribution of foraminiferal and calcareous nanno-
plankton assemblages in the Central Paratethys during
time intervals ca. 27 to 19 Ma and 15 to 13.5 Ma refuted
the working hypothesis, which predicted only a marginal
impact of global climate changes on a subtropical epicon-
tinental sea influenced by local tectonic and palaeogeo-
graphic events. Global climatic cycles influenced the
palaeoenvironment in the studied subtropical epiconti-
nental seas particularly in the intervals between the most
significant tectonic events.
2. Warm intervals and associated global sea-level rises
started with the opening of communication with the
warmer Indo-Pacific and Mediterranean realms, which
accelerated the influence of global warming.
3. Warm intervals can be characterized by a generally stable
climate with weak seasonal signals, high evaporation
increasing humidity, and then riverine inflow and input of
terrigenous nutrients. Decreased salinity is expected in
marginal facies and surface water, and may have caused
stratification. Seasonal upwelling was locally established
under favourable winds and mixed water masses. Suspen-
sion feeders and eutrophic markers prevailed in basinal
assemblages.
4. Cold intervals are characterized by aridification due to
decreased evaporation and marked seasonality, warm sea-
sons having stratified water and hypersaline oligotrophic
224
HOLCOVÁ
GEOLOGICA CARPATHICA
, 2017, 68, 3, 207 – 228
water. This heavy, saline layer triggered downwelling
mixing, persisting during the cold season. Moreover,
episodic intensive rainfalls in decade-long cycles can be
expected. Instability supported expansion of stress-
tolerant, opportunistic taxa, often small-sized (Lenti-
culina, biserial agglutinated, small Cibicidoides,
Reticulo fenestra minuta). Oligotrophy triggered en-
largement of sea-grass meadows with herbivorous fora-
minifera dependent on nutrient sources from their own
ecosystem.
Local tectonic events led to certain discrepancies between
global and local sea-level cycles, local salt formation
(in the rain shadow of newly-created mountains), and
establishment of an upwelling regime (geomorphological
changes altering atmospheric circulation and creating
stable winds with a direction driving surface water away
from the coast causing upwelling).
5. Climatic change triggered nannofossil evolution. Large
reticulofenestras and helicosphaeras were reduced in size
during cool phases, which emptied habitats for new taxa
appearing in the following warm interval (both endemics
and colonists); for example, Reticulofenestra bisecta was
substituted after the Mi-1 event by endemic Reticulo-
fenestra excavata, while Helicosphaera ampliaperta and
H. scissura replaced Helicosphaera euphratis.
Acknowledgements: The study was supported by project
PRVOUK P44 and PROGRESS Q45. The author greatly
appreciates the constructive reviews of Dr. Katalin Báldi and
Prof. Michael Kaminski which improved the manuscript.
Fig. 10. Model of palaeobiotope distribution in the epicontinental Central Paratethys sea during the Middle Miocene.
225
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GEOLOGICA CARPATHICA
, 2017, 68, 3, 207 – 228
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