Historical Biology

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The Pleistocene flora of Bezhan, southeast

Albania: early appearance of extant tree species

Thomas Denk, H. Tuncay Güner, Johannes Martin Bouchal & Mădălina-Elena

Kallanxhi

To cite this article: Thomas Denk, H. Tuncay Güner, Johannes Martin Bouchal & Mădălina-Elena
Kallanxhi (2021) The Pleistocene flora of Bezhan, southeast Albania: early appearance of extant
tree species, Historical Biology, 33:3, 283-305, DOI: 10.1080/08912963.2019.1615061

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HISTORICAL BIOLOGY
2021, VOL. 33, NO. 3, 283–305
https://doi.org/10.1080/08912963.2019.1615061

ARTICLE

The Pleistocene flora of Bezhan, southeast Albania: early appearance of extant tree
species
a a,b a
Thomas Denk , H. Tuncay Güner , Johannes Martin Bouchal and Mădălina-Elena Kallanxhic
a
Department of Palaeobiology, Swedish Museum of Natural History, Stockholm, Sweden; bFaculty of Forestry, Department of Forest Botany,
Istanbul University Cerrahpaşa, Istanbul, Turkey; cFaculty of Biology and Geology, Department of Geology, Babeş-Bolyai University, Cluj-Napoca,
Romania

ABSTRACT ARTICLE HISTORY

The piggyback basin of Bezhan, southeastern Albania, was formed during the late Neogene and Received 13 February 2019
contains Pliocene/Pleistocene deposits. These continental deposits consist of marls, siltstones and Accepted 1 May 2019
clays separated by a thin series of lignite-seams alternating with clays (Bezhan formation). We investi- KEYWORDS
gated leaf fossils and dispersed pollen from marls of the upper portion of this formation. Fifty-two plant Plant macrofossils; pollen;
taxa comprising algae, gymnosperms, and angiosperms were recovered. Of these, at least 19% belong Quercus cerris; sub-
to extant species and less than 16% belong to taxa today extinct in western Eurasia. Tsuga is Mediterranean vegetation
represented by three pollen taxa with affinities to modern Chinese, Japanese, and North American belt; extant tree species;
species. Herbaceous taxa indicative of steppe (Artemisia, Amaranthaceae) occur in low quantities (≤1%) Calabrian
suggesting an interglacial setting. Four vegetation units are recognised: Wet riparian and aquatic
vegetation, mesic oak forest, dry sub-Mediterranean woodland, and montane conifer forest. A compar-
ison of the Bezhan flora with well-dated Pliocene and Pleistocene floras of Italy suggests a Calabrian
(late early Pleistocene) age for the upper unit. This estimate is based on the abundance of extant taxa,
the absence of subtropical taxa, and threshold values of particular taxa (Tsuga, Carya). The findings are
in agreement with age estimates for extant tree species from molecular studies.

Introduction within the variability of comparable parts in modern species

and being unique to this modern species. By doing so,
Climate cooled gradually over the past 5 million years (Ma)
Gelasian-Calabrian carpological material of Quercus from
(Ravelo et al. 2004) punctuated by a short warm episode at
northern Italy was referred to as Quercus cf. robur L. and
3 Ma (Haywood et al. 2000) after which continued cooling led
clearly distinguished from older Pliocene material lacking the
to the climate cyclicity (glacial/interglacial) seen in the
diagnostic characters of the modern species.
Pleistocene (Suc et al. 1997; Head et al. 2008). The palaeobo-
In general, the Plio-Pleistocene transition in the
tanical record shows clear signs of vegetation change in the
Mediterranean region was accompanied by a re-organisation
Mediterranean Basin over the past 4 million years
of the flora that involved extinction of many plants from
(Combourieu-Nebout et al. 2015). Here, Pliocene assemblages
older periods and the early appearance of modern forms
were dominated by subtropical plant taxa, which disappeared
(Velitzelos et al. 2014; Martinetto 2015).
progressively following latitudinal gradients from north to
While the geographical patterns and temporal sequence of
south in Italy (Bertini 2010; Combourieu-Nebout et al.
these changes are well recorded for the Italian peninsula
2015; Magri et al. 2017). As a consequence, temperate oak
(Bertini 2010; Bertini et al. 2014; Bertini and Martinetto
forests and conifer forests composed of Tsuga, Abies,
2014; Pini et al. 2014; Russo-Ermolli and Bertini 2014)
Cathaya, Picea and Pinus haploxylon expanded, and
based on a great number of fossil-bearing strata with good
Mediterranean-type forest developed.
age control, the chronology of late Neogene and Quaternary
During recent years, a substantial number of studies have
terrestrial deposits in the Albanids is not well constrained
focussed on patterns of plant extinctions (woody angiosperms
(Meço and Aliaj 2000).
and gymnosperms) during the Pleistocene in western Eurasia
Here, we investigated plant macrofossils and dispersed
(e.g. Follieri et al. 1986; Svenning 2003; Bertini 2010; Magri
pollen in Pleistocene lacustrine deposits of southeastern
2012; Bertini et al. 2014; Biltekin et al. 2015; Combourieu-
Albania. Using the ecological range of the taxa encountered,
Nebout et al. 2015; Magri et al. 2017; Martinetto et al. 2017).
we reconstructed palaeoenvironments. To establish the age of
In contrast, only a few studies investigated the early appear-
the investigated plant assemblage, in absence of other age
ance of modern tree species in western Eurasia (e.g. Magri
constraint\s (palaeomagnetism, mammal fauna, tephra), we
2010; Martinetto 2015). Martinetto (2015, p. 70) considered
correlated the pollen and macrofloras with those from Italy.
fossil specimens to represent modern species when they
Furthermore, we assessed whether and to which extent leaf
exhibited a diagnostic suite of characters all of which falling

CONTACT Thomas Denk thomas.denk@nrm.se Department of Palaeobiology, Swedish Museum of Natural History, Box 50007, Stockholm 10405, Sweden
Supplemental data for this article can be accessed here.
© 2019 Informa UK Limited, trading as Taylor & Francis Group

Published online 20 May 2019

284 T. DENK ET AL.

and pollen assemblages contained morphotypes that closely northwest direction from Thessaly in Greece to southeast-
match modern species and discussed first appearance dates of ern Albania. During the Paleogene and Miocene, the ATHB
modern species in the sub-Mediterranean vegetation belt of developed transgressively on the Mirdita Zone (Figure 1). It
western Eurasia. is filled by a ca. 4500 m thick sedimentary succession of
shallow marine molasse deposits, which rest unconform-
ably on a Mesozoic basement. Molasse deposits are overlain
Material and methods by late Miocene to Pleistocene lacustrine and fluvial-lacus-
trine deposits including lignites (Pashko 2018). These
Geological background
deposits formed during the uplifting of the ATHB from
The Albanides thrust belts are located between the middle Miocene to the present and occur scattered within
Dinarides to the north and the Hellenides to the south. the ATHB (Meço and Aliaj 2000; Pashko 2018). Basin fills
They are folded and overthrusted westward as tectonic of these depressions comprise terrigenous conglomerates
nappes that formed since the Jurassic because of the colli- from surrounding mountain ranges and limnic pelites
sion of the African and Euro-Asiatic plates. The Albanides including lignites (Meço and Aliaj 2000).
thrust belts include the Apulia Foreland (Sazani Zone), The small intermontane depression of Kolonjë-Bezhan was
several orogenic tectonic nappes, the Peri-Adriatic formed during the Pliocene. It contains the lignite-bearing
Depression, and one intramontane depression (Meço and Bezhan Formation (Meço and Aliaj 2000), which discordantly
Aliaj 2000; Xhomo et al. 2002; Pashko 2018; Figure 1). The overlies Eocene Gramos flysch (Figure 2). Above the flysch, the
Albanian-Thessalian intermontane basin (ATHB) repre- lower unit of the Bezhan Formation begins with 7–8 m of basal
sents a narrow marine trough and extends in a southeast- conglomerate consisting of pebbles of fine-grained sands scattered
into a greyish silt-clay matrix. Above the conglomerates, a 50–70
m thick rather homogeneous siltstone succession occurs, which is
overlain by a 20–25 m thick series with lignite seams. Above this
succession, the upper unit consists of 45–70 m of marly siltstone
and clay comprising plant macrofossils (Pashko et al. 1973). The
macrofossils described here were collected from the discontinued
Bezhan lignite mine from marls overlying the lignite seams
(Kleinhölter 2004); no further stratigraphically relevant informa-
tion was provided by Kleinhölter (2004) and Meço et al. (2004).
Using the borehole sections B7 and B12 of Pashko et al. (1973) as a
reference, the macrofossils probably originated from the lower
part of the upper unit. Meço et al. (2004) based their ‘late Pliocene’
age of the Bezhan Formation on an unpublished palynological
report by Gjani. According to this report, only a single sample
originating from the lower part of the upper unit comprises 90%
conifer pollen (Pinaceae). The remaining 10% were angiosperms
with only a minor contribution of herbaceous plants
(Amaranthaceae). According to Gjani in Meço et al. (2004), the
palynoflora indicated a ‘late Pliocene’ age for these sediments.
Unfortunately, Meço et al. (2004) did not provide any information
about the sampled section nor did they provide a pollen diagram.
As such, their palynological data cannot be used for any strati-
graphic correlation.
Finally, younger Quaternary sediments consisting mainly
of coarse gravels rest discordantly on top of Pliocene and
Pleistocene basin fill (Meço and Aliaj 2000; Figure 2).

Plant material
The plant material used for the present study is housed at the
Swedish Museum of Natural History (S182016–S182085). It
was collected in 1999 by Kleinhölter (2004). Kleinhölter
(2004) described 21 carpological and leaf taxa from Bezhan.
For the present study, we re-investigated the macrofossil
Figure 1. Map of Albania showing main geological features (based on Meço and (mainly leaves) material from Bezhan and investigated dis-
Aliaj 2000). (a) Sazani Foreland, (b) Ionian Zone, (c) Kruja Zone, (d) Krasta-Cukali persed pollen from the layer that yielded the leaf fossils
Zone, (e) Albanian Alps (Karst), (f) Gashi Zone, (g) Mirdita (Subpelagonian) Zone,
(h) Korabi (Pealogonian) Zone, (i) Albanian Thessalian Basin, (j) Peri-Adriatic
(Figure 2). At the moment, the exact stratigraphic position
Depression. Asterisk indicates the Kolonje-Bezhan Basin. within the upper unit of the Bezhan Formation cannot be
 HISTORICAL BIOLOGY 285

Age constraints
Oligocene to Miocene molasse basins of Albania are well-
dated using calcareous nannofossils (e.g. Kallanxhi et al.
2016; Kallanxhi and Ćorić 2017), foraminifera, and molluscs
(e.g. Buli et al. 2001; Pashko 2018). In contrast, several
Pliocene/Pleistocene lacustrine basins are more difficult to
date. Pashko et al. (1973) considered the Neogene sediments
of Bezhan as Tortonian (late Miocene) overlain by alluvial
sediments of Quaternary age based on lithostratigraphy
(Figure 1). Later, Gjani (unpublished) attributed lacustrine
sediments of Bezhan to the late Pliocene (corresponding to
Gelasian, early Pleistocene according to the currently used
chronostratigraphy) based on palynology. Here, we investi-
gated macrofossils (leaves) and dispersed pollen. The
palaeobotanical evidence was compared with that from
selected localities from Armenia, Greece and Italy spanning
a time period form Messinian to Middle Pleistocene
(Figure 3).

Results
Systematic palaeobotany
Thirty-six taxa are woody plants. Of these, most are trees, but
one liana and at least six shrubs are included as well. Six taxa
are elements of riparian vegetation and 29 occur in various
types of well-drained lowland and upland forests. Thirteen
herbaceous taxa include six aquatic and seven ecologically
indifferent plants. Of the latter, Amaranthaceae,
Caryophyllaceae, Artemisia, and Asteroideae also occur in
steppe vegetation but do not make up more than 1% in the
pollen record.
In the following, the plant taxa (Figures 4–11) recognised
are illustrated and briefly discussed. Six fruit taxa described
by Kleinhölter (2004) are not included here but listed in Table
1. The sequence of taxa starts with algae and continues with
gymnosperms and angiosperms. The sequence of angios-
perms follows APG IV (2016).

Superdivision Charophyta Migula 1897 sensu Leliaert et

Figure 2. Lithological logs from boreholes B7 and B12 of the Bezhan Formation al. 2012
(modified from Pashko et al. 1973; Meço et al. 2004). The shaded portion above the
coal seam indicates the approximate position of the leaf horizon investigated for Class Zygnematophyceae Round 1971
the present study. From the same layer, dispersed pollen was investigated. Family Zygnemataceae Kützning 1843
Genus Spirogyra Link in C.G.Nees 1820
established. Pollen sample processing followed the protocol Spirogyra sp./Ovoidites elongatus (Hunger, 1952) Krutzsch
described in Halbritter et al. (2018). Pollen grains were inves- 1959 (Figure 9(a))
tigated with both light microscopy (LM) and scanning elec-
tron microscopy (SEM) using the single grain technique
(Zetter 1989). The pollen sample originates from the slab Remarks
containing specimen S182078. Residue and SEM-stubs are Ovoidites elongatus is a fossil-species used for psilate aplanos-
housed under accession numbers S182078-01 and S182078- pores/zygospores commonly produced by Spirogyra, indicat-
02 at the Swedish Museum of Natural History. Three hundred ing shallow, stagnant, oxygen-rich fresh water and lake
and fifty pollen grains were counted to establish the pollen margins (Van Geel 2001; Worobiec 2014). Kleinhölter
abundance values presented in Table 1. For climate inference (2004) reported a single gyrogonite of the fossil-genus
and comparison to extant vegetation, the Köppen-Geiger Tectochara N.Grambast and L.Grambast (Characeae) that
system is used (Kottek et al. 2006; Peel et al. 2007) also belongs to Charophyta.
286 T. DENK ET AL.

Table 1. Plant taxa recorded from the Pleistocene of Bezhan.

Order Genus, frequency (pollen, spores) Pollen count % Element Life form Ecology
Zygnematales Spirogyra 4 ca. 1% Cyst Aquatic algae Eutrophic lake
Charales Tectocharaa,c Gyrogonite Aquatic algae Freshwater, lake, ponds
Ephedrales Ephedra sp. 1 ≤0.3% Pollen Shrub Edaphically dry forest or woodland
Pinales Papillate Cupressaceae pollen (split)d 13 3.7% Pollen Tree Various forest types
Pinales Abies sp. 23 6.6% Pollen Tree Upland forest
Pinales Cedrus sp. 18 5.1% Pollen Tree Upland forest
Pinales Picea sp. 8 2.3% Pollen Tree Upland forest
Pinales Picea sp. Seed Tree Upland forest
Pinales Pinus subgen. Pinus 128 37.0% Pollen Tree Various forest types
Pinales Pinus subgen. Strobus 10 2.9% Pollen Tree Various forest types
Pinales Pinus sp. Seed Tree Various forest types
Pinales Pinus sp. (3-needled)d Leaf fascicle Tree Upland forest; edaphically dry forest or woodland
Pinales Pinus sp. (5-needled) Leaf fascicle Tree Upland forest; edaphically dry forest or woodland
Pinales Tsuga sp. 1d, 35 10.0% Pollen Tree Upland forest
sp. 2d, sp. 3d
Pinales Pinaceae gen. indet. Seed (scales) Tree Upland forest
Alismatales Potamogeton sp. 3 ≤1% Pollen Aquatic herb Freshwater, lake, ponds
Poales Carex sp.a Fruit Aquatic herb Reed belt
Poales Phragmites sp. Leaf Aquatic herb Reed belt
Poales Scirpus sp.a Fruit Aquatic herb Reed belt
Ranunculales Ranunculus aquatilis L.a Fruit Aquatic herb Freshwater, lake, ponds
Ranunculales Ranunculus sp.a Fruit Herb Indifferent
Saxifragales Liquidambar sp. 2 ≤0.6% Pollen Tree Riparian forest
Saxifragales Myriophyllum sp.a Fruit Aquatic herb Freshwater, lake, ponds
Vitales Parthenocissus sp. d
1 ≤0.3% Pollen Liana On trees
Rosales Crataegus sp. (aff. nigra Waldst. & Kit.) Leaf Shrub Various forest types or woodland
Rosales Rhamnaceae gen. indet. 1 ≤0.3% Pollen Shrub/tree Various forest types or woodland
Rosales Ulmus vel Zelkova sp. 1, sp. 2 7 2.0% Pollen Tree Various forest types
Rosales Ulmus aff. minor Mill. Leaf Tree Various forest types
Fagales Castanea sp. 1 ≤0.3% Pollen Tree Lowland forest
Fagales Quercus aff. cerris L. Leaf Tree Edaphically dry forest or woodland
Fagales Quercus sect. Ilex 10 2.8% Pollen Tree Sclerophyllous forest and woodland
Fagales Quercus aff. coccifera L. Leaf Shrub/tree Sclerophyllous forest and woodland
Fagales Quercus sp. (section Quercus) Leaf Tree Various forest types
Fagales Quercus sp. Lb 24 6.8% Pollen Tree Various forest types
Fagales Pterocarya sp. 6 1.7% Pollen Tree Riparian forest
d
Fagales Carya sp. 17 4.9% Pollen Tree Various forest types
Fagales Alnus sp. 5 1.4% Pollen Tree Riparian forest
Fagales Betula sp. 13 3.7% Pollen Tree Upland forest
Fagales Betula sp. Seed Tree Upland forest
Fagales Betula sp. Leaf Tree Upland forest
Fagales Carpinus sp.a Fruit Tree Lowland forest
Cucurbitales Coriaria aff. myrtifolia Niss ex L. 1 ≤0.3% Pollen Shrub Edaphically dry forest or woodland; forest edges
Malpighiales Populus aff. alba L. Leaf Tree Riparian forest
Malpighiales Salix sp. Leaf Tree Riparian forest
Myrtales Lythraceae aff. Decodond 1 ≤0.3% Pollen Shrub Edaphically dry forest or woodland; wetlands
Sapindales Acer sp. 1, sp. 2 5 1.4% Pollen Tree Various forest types
Sapindales Acer aff. monspessulanum L. Leaf Tree Edaphically dry forest or woodland; forest edges
Sapindales Acer sp. 1 (section Platanoideae) Leaf Tree Upland forest
Caryophyllales Caryophyllaceae 3 ≤1% Pollen Herb Indifferent but including steppe
Caryophyllales Amaranthaceae 3 ≤1% Pollen Herb Indifferent but including steppe
Ericales Erica aff. arborea L. 1 ≤0.3% Pollen Shrub Sclerophyllous forest and woodland
Lamiales Olea aff. europaea L. 1 ≤0.3% Pollen Tree Sclerophyllous forest and woodland
Lamiales Fraxinus sp. 1 ≤0.3% Pollen Tree Riparian forest
Apiales Apiaceae sp. 1, sp. 2 4 1.0% Pollen Herb Indifferent but including steppe
Asterales Artemisia sp. 4 1.0% Pollen Herb Indifferent but including steppe
Asterales Asteroideae 2 ≤0.6% Pollen Herb Indifferent but including steppe
Incerta sedis Leguminophyllum sp. Leaf Shrub Various forest types
Incerta sedis Dicotylophyllum sp. Leaf Shrub/tree Various forest types
a
Kleinhölter (2004); specimens not seen.
b
For the pollen counts, large pollen of Quercus was treated uniformly whereas distinct Cerris and Quercus types were differentiated using SEM.
c
Extinct genus.
d
extinct in western Eurasia.
Bold = likely representing an extant species.
 HISTORICAL BIOLOGY 287

Genus Cedrus Trew 1757

Cedrus sp. [pollen, Figure 9(h)]

Remarks
Cedrus sp. is similar (thickened cappa, sacci half-spherical, low
sacci attachment angle) to extant pollen of this genus (Beug 2004).

Genus Picea A.Dietr. 1824

Picea sp. [pollen, Figure 9(i)]

Remarks
Picea sp. is similar (e.g. sacci half-spherical, low sacci attachment
angle, low sacci height) to extant pollen of this genus (Beug 2004).

Figure 3. Geographic position of Messinian to Middle Pleistocene localities

discussed in this study. Messinian: (a) Vegora; Piacenzian: (b) Meleto;
Picea sp. [seed, Figure 9(d)]
Calabrian: (c) Pietrafitta, (d) Camerota, (e) Montalbano Jonico, (f) Oriolo, (g)
Ohrid lake section; Middle Pleistocene: (h) Megalopolis.
Material – S182024

Superdivision Tracheophyta Sinott 1935 ex Cavalier- Remarks

Smith 1998 Nearly identical seeds occur in modern Picea. Close simila-
Subdivision Spermatophyta Willkomm 1854 rities of the fossil seed are with the extant P. omorika (Pančić)
Gymnosperms Purkyne 1887 endemic to a small area in Serbia and Bosnia
Subclass Gnetidae Pax in Prantl 1894 and Herzegovina (Farjon 1990).
Order Ephedrales Dumort. 1829
Family Ephedraceae Dumort. 1829 Genus Pinus L. 1753
Genus Ephedra L. 1753 Pinus subgenus Pinus L. 1753
Ephedra sp. [pollen; Figure 9(b,c)] Pinus subgenus Pinus sp. [pollen, Figure 9(j)]

Remarks
Remarks
The present Ephedra pollen shows unbranched pseudosulci, a
Pollen of Pinus subgenus Pinus sp. (diploxylon type) is charac-
feature typical of an extant basal grade of Mediterranean spe-
terised by narrowly attached, spherical sacci (Halbritter et al. 2018).
cies of this genus (Bolinder et al. 2016).

Subclass Pinidae Cronquist, Takht. & Zimmerm. 1966 Pinus subgenus Strobus Lemmon 1895
Order Pinales Gorozh. 1904 Pinus subgenus Strobus sp. [pollen, Figure 9(k)]
Family Cupressaceae Rich. ex Bartling, 1830
Papillate Cupressaceae pollen [pollen; Figure 9(d–f)] Remarks
Pollen of Pinus subgenus Strobus sp. (haploxylon type) is
characterised by broadly attached, half-spherical sacci and
Remarks dotted thickenings in the leptoma area (Halbritter et al. 2018).
Split papillate Cupressaceae pollen is commonly assigned to
Inaperturopollenites dubius, similar pollen is produced by extant
members of subfamilies Sequoioideae and Taxodioideae (Kedves Pinus sp. [seed, Figure 4(c)]
1985; Miyoshi et al. 2011). Modern species of these subfamilies Material – S182023
occur both in swamp forests and on well-drained soils.

Kleinhölter 2004, Pinus sp., p. 105

Family Pinaceae Spreng. ex F.Rudolphi 1830
Genus Abies Mill. 1754 Remarks
Small seeds with small asymmetrical wings are typical of the
Abies sp. [pollen, Figure 9(g)]
modern species P. sylvestris L. Extant Mediterranean and Balkan
species (e.g. P. pinea L. 1753, P. pinaster Aiton. 1789, P. peuce
Remarks Griseb. 1846, P. heldreichii H.Christ 1863, P. halepensis Mill. 1808,
Abies sp. pollen from Bezhan corresponds (e.g. crest, sacci and P. canariensis C.Sm. ex DC. 1829) have much larger seeds and/
nearly spherical, size) to extant pollen of this genus (Beug 2004). or wings. Extant Pinus nigra J.F.Arnold 1785 and P. brutia Ten.
288 T. DENK ET AL.

Figure 4. Macrofossils from Bezhan. Picea to Betula.

(a) cf. Abies sp., winged seed, S182020, (b) cf. Picea sp., seed scale, S182021, (c) Pinus sp., winged seed, S182023, (d) Picea sp., winged seed, S182020, (e) Pinus sp., 5-needled fascicle,
S182018, asterisks indicate needle position, (f) Pinus sp., 3-needled fascicle, S182019, asterisk indicate needle position, (g,h) Monocotyledonae sp. 1, (g) node and internode section,
S182026, (h) apical part of a large leaf, S182030, (i,j) Ulmus aff. Minor, (i) leaf, S182050, (j) leaf fragment, S182043, (k) Leguminophyllum sp., leaf fragment, S182045, (l) Indet. leaf 1, S182046,
(m) cf. Quercus aff. coccifera, leaf, S182047, (n) Quercus sp. (sect. Quercus), leaf, S182036, (o) Betula sp., leaf, S182054.Scale bars: 1 cm (b–d) and 2 cm (a, e–g).
 HISTORICAL BIOLOGY 289

1815 have slightly smaller winged seeds than the previous species Pinaceae gen. indet. [seeds or seed scales; Figure 4(a,b)]
but still larger than the fossil seed and extant P. sylvestris L. 1753
Material – S182020, S182021, S182022, S182025
(Farjon 2005).

Pinus sp. [5-needled fascicle; Figure 4(e)] Kleinhölter 2004, Picea sp., p. 105
Material – S182018
Remarks
Kleinhölter 2004, Pinus sp. (three-needle pine), p. 105 A number of further Pinaceae seeds/seed scales are difficult to
assign to a particular genus. Specimen S182020 (Figure 4(a))
has a large seed (7 mm long) and wing (15 mm long).
Remarks Somewhat similar seeds occur in Abies [e.g. A. cilicica
Five-needle pines occur in subgenus Strobus. Among the (Antoine & Kotschy1854) Carrière 1855; Farjon 1990].
European representatives of Strobus is the Balkan endemic Specimen S182021 [Figure 4(b)] possibly is a seed scale of
Pinus peuce (www.conifers.org). Picea; similar seed scales occur in P. omorika (see above).

Pinus sp. [3-needled fascicle; Figure 4(f)] Subclass Magnoliidae Novák ex Takht. 1967
Material – S182019 Monocots

Kleinhölter 2004, Pinus sp. (three-needle pine), p. 105 Order Alismatales R.Br. ex Bercht. & J.Presl 1820
Family Potamogetonaceae Bercht. & J.Presl 1823
Genus Potamogeton L. 1753
Remarks
Three-needle pines typically occur in subgenus Pinus (www.con Potamogeton sp. [pollen; Figure 9(x–z)]
ifers.org). Extant species with fascicles in three occur in the
Americas.
Remarks
When investigated with LM, this pollen is reticulate. SEM investi-
Genus Tsuga Carrière 1847 gation reveals a reticulum crested with nanoechini [Figure 9(z)].
Pollen with similar sculpturing occurs, for example, in extant
Tsuga sp. 1 [pollen; Figure 9(l–o)] Potamogeton natans L. 1753 and P. nodosus Poir. 1816 (Sorsa
1988).
Remarks
Tsuga sp. 1 is similar to pollen of extant Tsuga forrestii Downie Order Poales Small 1903
1923 and T. chinensis (Franch.) E.Pritzel 1900 with echinate sculp- Family Poaceae Barnhart 1895
turing and a broad monosaccus (LM, SEM; Sivak 1973). Genus Phragmites Adans. 1763
Phragmites sp. [leaf, axis; Figure 4(g,h)]
Tsuga sp. 2 [pollen; Figure 9(p–s)]
Material – S182026, S182030

Remarks
Kleinhölter 2004, Monocotyledonae sp. 1, p. 108, pl. 2,
Pollen similar to Tsuga sp. 2 (narrow monosaccus, long echini) is
Figure 7
produced by the extant Japanese Tsuga sieboldii Carrière 1855
(Sivak 1973).
Remarks
Tsuga sp. 3 [pollen; Figure 9(t–w)] Leaf and axis remains of Poaceae are difficult to assign to particular
genera. We tentatively refer the axis with nodes and internodes
[Figure 4(g)] and the apical part of a large leaf [Figure 4(h)] to the
Remarks genus Phragmites. Extant Phragmites is a typical element of lake-
The extant eastern North American Tsuga canadensis Carrière shores.
1855 produces monosaccate pollen without detectable echini
(LM, SEM), similar to Tsuga sp. 3 (Sivak 1973; Kurmann 1990). Superrosids
290 T. DENK ET AL.

Order Saxifragales Bercht. & J.Presl 1820 with (micro)rugulate exine sculpturing within their
Family Altingiaceae (Horan. 1841) Lindl. 1846 Lasiodiscus-type.
Genus Liquidambar L. 1753
Liquidambar sp. [pollen; Figure 10(a,b)] Family Ulmaceae Mirbel 1815
Genus Ulmus L. 1753/Zelkova Spach 1841
Remarks Ulmus vel Zelkova sp. 1 [pollen; Figure 10(i)], Ulmus vel
The figured specimen is pantoporate and shows porate, Zelkova sp. 2 [pollen; Figure 10(j)]
nanoechinate exine sculpturing and distinct pore membranes
(SEM). These characters are characteristic of extant pollen of
Remarks
this genus (Bogle and Philbrick 1980; Ickert-Bond and Wen
Ulmus and Zelkova produce oblate pollen with rugulate sculp-
2013).
turing (LM and SEM) (Takahashi 1989; Stafford 1995). Ulmus
Rosids
vel Zelkova sp. 2 differs by smaller size and more distinct
rugulate sculpturing from Ulmus vel Zelkova sp. 1.
Order Vitales Juss. ex Bercht. & J.Presl 1820
Family Vitaceae Juss. 1789 Ulmus aff. minor L. 1753 [leaf; Figure 4(i,j)]
Genus Parthenocissus Planch. 1887
Material – S182028, S182043, S182050, S182072
Parthenocissus sp. [pollen; Figure 10(c–e)]

Kleinhölter 2004, Ulmus sp., p. 107, pl. 2, Figure 3

Remarks
Similar pollen (reticulate, distinct costae) occurs in the North
American Parthenocissus heptaphylla (Planch.) Britton 1903 and Remarks
the eastern Asian P. tricuspidata (Siebold & Zucc.) Planch. 1887 The leaf material at hand is identical to modern Ulmus minor
(Lu et al. 2012; Halbritter and Weber 2016). (see e.g. herbarium E, http://data.rbge.org.uk/herb/
E00080246, E00075698, E00080250, E00405665).

Order Rosales Bercht. & J.Presl 1820

Order Fagales Engler 1892
Family Rosaceae Juss.
Family Fagaceae Dumort. 1829
Genus Crataegus Tourn ex. L.
Genus Castanea Mill. 1754
Crataegus sp. [leaf; Figure 8(a–c)]
Castanea sp. [pollen; Figure 10(k)]
Material – S182085

Remarks
Remarks Similar pollen of extant Castanea was figured in Praglowski
A single leaf belongs to Rosaceae. Among Rosaceae, closest (1984).
similarities are with Crataegus based on the leaf size, denti-
tion, and leaf shape. The extant species C. nigra Waldst. &
Kit. 1799 appears to be the closest match with the fossil leaf Genus Quercus L. 1753
(margin at leaf base dentate, overall leaf shape; https:// Quercus subgenus Cerris sect. Cerris Oerst 1866
science.mnhn.fr/all/search/form). This species is native in Quercus sect. Cerris sp. [pollen; Figure 10(l,m)]
central-eastern Europe and the northern Balkans growing
mainly on floodplains. Records of Albania date back to 1955
(Mitrushi 1955) and would need confirmation (Bartha Remarks
2017). Tectum ornamentation within sections of Quercus is highly
consistent and thus provides a diagnostic character to assign
dispersed oak pollen to infrageneric groups when investigated
Family Rhamnaceae Juss. 1798 with SEM (Denk and Grimm 2009; Denk et al. 2017). Pollen
Rhamnaceae gen. indet. [pollen; Figure 10(f–h)] of Quercus sect. Cerris displays weakly rugulate ornamenta-
tion (rugulae masked by secondary sporopollenin) and char-
acteristic agglomerations of rodlets [SEM; Figure 10(m)].
Remarks
This pollen is tentatively assigned to Rhamnaceae based on its
Quercus aff. cerris L. [leaf; Figures 5(a–h) and 6(a–g)]
exine sculpture (SEM), shape, and colpus configuration.
Schirarend and Köhler (1993) included Rhamnaceae pollen Material – S182056 to S182070, S182072 to S182084
 HISTORICAL BIOLOGY 291

Kleinhölter 2004, Quercus sp. 1, p. 106, pl. 2, Figures 1 and 4 teeth usually have minute bristle-like extensions. Leaves may
Kleinhölter 2004, Quercus sp. 2, p. 106, pl. 2, Figure 6 be narrow elliptic with shallow lobes, or coarse teeth (Figure 7
(a–c,f,g)), or lobes may be more pronounced and roundish
mimicking the leaves of white oaks (Quercus sect. Quercus;
Remarks Figure 7(d,e,h,i)). In addition, complex deeply lobed leaves
Quercus cerris leaves in the lignite-bearing Bezhan Formation occur. Among these, lobes may be simple, narrow triangular
are identical to modern leaves of this species. Quercus cerris is with acute apices (Figure 7(j,k,s–v)) or they may be with sec-
remarkable in its leaf polymorphism. Apices of leaf lobes or ondary lobes (Figure 7(l–r)). Finally, extreme forms consist of a

Figure 5. Macrofossils from Bezhan. Quercus aff. cerris.

(a–h) Quercus aff. cerris, leaves and leaf fragments, (a) S182070, (b) S182072, (c) S182078, (d) S182074, (e) S182081, (f) S182065, (g) S182060, (h) S182062.Scale bars: 2 cm (a–h).
292 T. DENK ET AL.

Figure 6. Macrofossils from Bezhan. Quercus aff. cerris.

(a–g) Quercus aff. cerris, leaves and leaf fragments, (a) S182057, (b) S182063, (c) S182067, (d) S182058, (e) S182061, (f) S182068, (g) S182048.Scale bars: 2 cm (a–g).
 HISTORICAL BIOLOGY 293

Figure 7. Modern leaf variability in Quercus cerris.

(a–c) 2007158 [I], (d, e) 2006243 [T], (f,g) 2006005 [T], (h) 2006009 [T], (i) 2006016 [T], (j) 2006233 [T], (k) 2006158 [T], (l) 2007119 [I], (m) 2006018 [T], (n,o) 2006110 [T], (p) 2007035 [I], (q)
2007156 [I], (r) 2006170 [T], (s) 2006303 [T], (t) 2007155 [I], (u) 2007027 [I], (v) 2006159 [T]. Scale bars: 2 cm (a–v).See electronic supplement for detailed voucher information.
294 T. DENK ET AL.

rhachis-like middle part of the lamina and few narrow, pointed Genus Pterocarya Kunth 1824
lobes (Figure 7(t–v)). The leaf variability in the fossil material
Pterocarya sp. [pollen; Figure 10(u)]
exactly matches the one found in the modern leaves.
Lobed leaves with secondary lobes and reduced lamina with
but a few narrow lobes are also found in a number of species of Remarks
sect. Quercus such as Q. pyrenaica Willd. 1805, Q. vulcanica Boiss. A polygonal outline and stephanoporate (4–7) apertures are
ex Kotschy 1859, Q. kotschyana O.Schwarz 1935, Q. alba L. 1753 characteristic of Pterocarya pollen (Stone and Broome 1975).
(e.g. Schwarz 1936, 1937; Krüssmann 1962) but here lobes are
usually not acute and lack the bristle-like extensions. In addition,
these species do not produce shallowly lobed leaves at all. Family Betulaceae Gray 1822
Genus Alnus Mill. 1754
Quercus subgenus Cerris sect. Ilex Loudon 1730 Alnus sp. [pollen; Figure 10(r)]
Quercus sect. Ilex sp. [pollen; Figure 10(n,o)]
Remarks
Remarks Alnus pollen has characteristic arci spanning between adja-
Pollen of Quercus sect. Ilex is markedly smaller than pollen of cent pores (Blackmore et al. 2003).
other sections and displays characteristic microrugulate orna-
mentation [SEM; Figure 10(o); Denk and Grimm 2009].
Genus Betula L. 1753
Betula sp. [pollen; Figure 10(s)]
Quercus aff. coccifera L. [leaf; Figure 4(m)]
Material – S182047
Remarks
The figured specimen displays a distinct atrium, a typical feature of
Remarks
the Betula pubescens type of Blackmore et al. (2003).
A single specimen resembles this Mediterranean oak by its
small, dentate leaf with secondary veins departing from pri-
mary veins at wide angles. Betula sp. [leaf; Figure 4(o)]
Material – S182054
Quercus subgenus Quercus sect. Quercus Loudon 1730
Quercus sect. Quercus sp. [pollen; Figure 10(p,q)] Remarks
A single small betulaceous leaf might belong to Betula. Deeply
cordate leaves are typically found in seedling leaves (see, for exam-
Remarks ple, herbarium P, MNHN-P-P00503957). In addition, a few
The sculpture of pollen belonging to Quercus sect. Quercus impressions of seeds are found in the fossil material.
displays characteristic microverruate ornamentation [SEM;
Figure 10(q); Denk and Grimm 2009].
Order Cucurbitales Juss. ex Bercht. & J.Presl 1820
Family Coriariaceae DC. 1824
Quercus sp. [leaf; Figure 4(n)] Genus Coriaria L. 1753

Material – S182036 Coriaria aff. myrtifolia Niss ex L. 1753 [pollen; Figure 10(v,w)]

Remarks
Remarks Identical pollen is produced by the extant west Mediterranean
A single leaf with round lobes, round sinuses between lobes Coriaria myrtifolia (Halbritter and Weis 2015). The genus has
and cordate leaf base might belong to the roburoid white oaks also been reported from lacustrine sediments in southern Italy
(Quercus sect. Quercus). dated at 450–650 thousand years (ka) (Russo-Ermolli 1999).

Family Juglandaceae DC. ex Preleb 1818 Order Malpighiales Juss. ex Bercht. and J.Presl 1820
Genus Carya Nutt. 1818 Family Salicaceae Mirb. 1815
Genus Populus L. 1753
Carya sp. [pollen; Figure 10(t)]
Populus aff. alba L. 1753 [leaf; Figure 8(f,g)]
Material – S182052, S182053
Remarks
Oblate pollen with three pores off-set towards the distal pole Remarks
is characteristic of this genus (Stone and Broome 1975). The fossil leaves are identical to leaves of the modern P. alba.
 HISTORICAL BIOLOGY 295

Figure 8. Macrofossils from Bezhan.

(a–c) Crataegus aff. nigra, leaf, S182085, (d,e) Salix aff. cinerea, (d) S182048, (e) S182040, (f,g) Populus aff. alba, (f) S182052, (g) S182053, (h) Acer aff. monspessulanum, S182050, (i,j) Acer
section Platanoidea, (i) S182051, (j) S182049.Scale bars: 2 cm (a–j).
 296 T. DENK ET AL.

Figure 9. Dispersed pollen of the leaf fossil-bearing strata of Bezhan. Light microscopy (LM) and scanning electron microscopy (SEM) micrographs of algal aplanospores or
zygospores, and Gymnosperm and Potamogetonaceae pollen.
 HISTORICAL BIOLOGY 297

(a) Spirogyra sp./Ovoidites elongates; (b,c) Ephedra sp., EV, (c) unbranched pseudosulci visible; (d–f) Papillate Cupressaceae pollen, PV; (g) Abies sp., EV; (h) Cedrus sp., EV; (i) Picea sp., EV; (j)
Pinus subgen. Pinus (diploxylon pollen type), EV; (k) Pinus subgen. Strobus (haploxylon pollen type), EV; (l–o) Tsuga sp. 1, (l) PV, (m) PRV, (n) proximal face detail, (o) echinate sculpturing of
saccus detail; (p–s) Tsuga sp. 2, (p) PV, (q) DV, (r) leptoma detail, densely echinate sculpturing, (s) saccus detail, weakly echinate; (t–w) Tsuga sp. 3, (t) PV, (u) DV, (v) leptoma detail, (w) saccus;
(x–z) Potamogeton sp., (z) reticulum crested with nanoechini.PV: polar view; PRV: proximal view; EV: equatorial view; DV: distal view.LM scale bar 10 µm, SEM scale bars 10 µm (c, e, m, q, u, y),
5 µm (n, o, r, s, v, w), and 1 µm (f, z).

Genus Salix L. 1753 Kleinhölter 2004, Acer sp., p. 107, pl. 2, Figure 5
Salix sp. [leaf; Figure 8(d,e)]
Remarks
Material – S182040, S182048
The leaf remain is identical to leaves of the modern species.
Acer monspessulanum occurs in the Mediterranean and sub-
Remarks
Mediterranean regions of western Eurasia and North Africa
Leaves with eucamptodromous venation and intersecondary veins
(van Gelderen et al. 1994).
that depart at right angles are characteristic of the genus Salix. Very
similar leaves are found in the modern species Salix cinerea L.
widely distributed from Europe to western Siberia (Krüssmann Acer sect. Platanoidea [Figure 8(i,j)]
1962).
Material – S182049, S182051
Remarks
Order Myrtales Juss. ex. Bercht. & Presl 1820 Nearly identical leaf remains are found in Acer lobelii Tenore
Family Lythraceae J.St.-Hilaire 1805 native to southern Italy (cf. herbarium P, https://science.
Lythraceae aff. Decodon J.F.Gmel. 1791 [Figure 10(x–z)] mnhn.fr/all/list?specificEpithet=lobelii&genus=Acer) and A.
platanoides L. (van Gelderen et al. 1994).
Remarks
The figured specimen corresponds in size, prolate shape, Order Caryophyllales Juss. ex Bercht. & J.Presl 1820
tricolporate costate aperture (LM), microverrucate colpus Family Caryophyllaceae Juss. 1789
membrane (SEM) and rugulate fossulate exine sculpture Caryophyllaceae gen. indet. [pollen; Figure 11(a,b)]
(SEM) to Decodon pollen type 6 of Gríımsson et al. (2012),
differing only in the absence of a bridge over the Remarks
porus (SEM). The figured specimen corresponds in number and size of
pores, exine sculpture (SEM) to the Minuartia pollen type
of Beug (2004) and the Minuartia rubra type of Punt and
Order Sapindales Juss. ex Bercht. & J.Presl 1820 Hoen (1995).
Family Sapindaceae Juss. 1789
Genus Acer L. 1753
Family Amaranthaceae Juss. 1789
Acer sp. 1 [pollen; Figures 10(aa–cc)], Acer sp. 2 [pollen;
Amaranthaceae gen. indet. 1 [pollen; Figure 10(ee)] and
Figure 10(dd)]
Amaranthaceae gen. indet. 2 [pollen; Figure 10(ff)]

Remarks Remarks
In this genus, most species produce striate and colpate The two figured pantoporate specimens can securely be
pollen similar to Acer sp. 2 [Figure 10(dd)]; this type is assigned to this family (Beug 2004). Amaranthaceae gen.
more abundant in the Bezhan sample. When investigated indet. 1 differs by smaller size and fewer pores from
with SEM Acer sp. 1 [Figures 10(aa–cc)] displays rugulate Amaranthaceae gen. indet. 2.
exine sculpturing; only a single specimen of this type was
encountered. The North American species Acer negundo
L. 1753 and A. saccharinum L. 1753 produce pollen with Order Ericales Bercht. & J.Presl 1820
rugulate exine sculpturing (Biesboer 1975; Adams and Family Ericaceae Juss. 1789
Morton 1976; Clarke and Jones 1978; Philbrick and Genus Erica L. 1753
Bogle 1981). Erica aff. arborea L. 1753 [pollen; Figure 11(c–e)]
Remarks
Acer aff. monspessulanum L. [Figure 8(h)] The figured specimen is highly similar (nanoechinate verrucae and
rugulae) to the pollen of extant Erica arborea (Sarwar and
Material – S182050 Takahashi 2014; Halbritter 2016).
298 T. DENK ET AL.

Figure 10. Dispersed pollen of the leaf fossil-bearing strata of Bezhan. Light microscopy (LM) and scanning electron microscopy (SEM) micrographs of Altingiaceae,
Vitaceae, Rhamnaceae, Ulmaceae, Fagaceae, Lythraceae, Betulaceae, Juglandaceae, Coriariaceae, Sapindaceae, and Amaranthaceae pollen.
(a,b) Liquidambar sp., (b) exine and pore membrane detail; (c–e) Parthenocissus sp., (c,d) EV, (e) exine detail; (f–h) Rhamnaceae gen. indet. (f,g) EV, (h) exine detail; (i) Ulmus vel Zelkova sp. 1,
PV; (j) Ulmus vel Zelkova sp. 2, PV; (k) Castanea sp.; (l,m) Quercus sect. Cerris, (l) EV, (m) exine detail; (n,o) Quercus sect. Ilex, (n) EV, (o) exine detail; (p,q) Quercus sect. Quercus, (p) EV, (q)
exine detail; (r) Alnus sp., PV; (s) Betula sp.; (t) Pterocarya sp., PV; (u) Carya sp., PV; (v,w) Coriaria aff. myrtifolia, (v) PV, (w) exine detail; (x–z) Lythraceae aff. Decodon sp. (x,y) EV, (z) exine
detail; (aa–cc) Acer sp. 1, (aa,bb) EV, (cc) exine detail; (dd) Acer sp. 2, PV; (ee) Amaranthaceae gen. et spec. indet. 1; (ff) Amaranthaceae gen et spec. indet. 2.PV: polar view; EV: equatorial
view; DV: distal view.LM scale bar 10 µm, SEM scale bars 10 µm (d, g, y, bb) and 1 µm (b, e, h, m, o, q, w, z, cc).
 HISTORICAL BIOLOGY 299

Figure 11. Dispersed pollen of the leaf fossil-bearing strata of Bezhan. Light microscopy (LM) and scanning electron microscopy (SEM) micrographs of
Caryophyllaceae, Ericaceaem Oleaceae, Asteraceae, and Apiaceae pollen.
(a,b) Caryophyllaceae gen. et spec. indet., (b) exine detail; (c–e) Erica aff. arborea, (c) exine detail; (f–h) Fraxinus sp., (f–g) EV, (h) exine detail; (i–k) Olea aff. europaea, (i,j) EV, (k) exine detail;
(l–n) Artemisia sp., (l,m) PV, (n) EV; (o) Asteroideae gen. indet., EV; (p) Apiaceae gen. indet.1, EV; (q) Apiaceae gen. indet.2, EV.PV: polar view; EV: equatorial view; DV: distal view.LM scale bar
10 µm, SEM scale bars 10 µm (b, d, g, j, m, o) and 1 µm (e, h, k).

Order Lamiales Bromhead 1838 Order Asterales Link 1829

Family Oleaceae Hoffmanns. & Link 1809 Family Asteraceae Bercht. & Presl 1820
Genus Fraxinus L. 1753 Subfamily Asteroideae Lindl. in Loudon
Asteroideae Lindl.
Fraxinus sp. [pollen; Figure 11(f–h)]
Genus Artemisia L.
Remarks Artemisia sp. [pollen; Figure 11(l–n)]
The figured specimen falls within the morphological range of
extant Fraxinus pollen (Punt et al. 1991).
Remarks
The figured specimens fall within the morphological range of
Genus Olea L. 1753 extant Artemisia pollen (Punt and Hoen 2009).
Olea aff. europaea L. 1753 [pollen; Figure 11(i–k)]
Asteroideae gen. indet. [pollen; Figure 11(o)]
Remarks
The figured specimen closely resembles the pollen (size,
reticulum with perpendicular ridges or nanoechinate sculp- Remarks
turing) of extant Olea europaea (Nilsson 1988; Punt et al. Although the figured specimen is poorly preserved and the
1991). configuration of the aperture cannot be observed, the
300 T. DENK ET AL.

discernible morphological features (size, echini structure) are both Quercus deciduous and Juglandaceae rule out a glacial
similar to the Gnaphalium uliginosum type of Punt and Hoen environment as typically recorded in the upper part of the
(2009). Camerota section (Baggioni et al. 1981; Bernac 1984).
Four main vegetation units are recognised: Wet, mesic,
dry, and montane vegetation. Wet vegetation includes ripar-
Order Apiales Nakai 1930
ian vegetation around lakes and rivers and aquatic vegetation
Family Apiaceae Lindl. 1836
(Table 1). Among woody plants, typical riparian trees were
Apiaceae sp.1 [pollen; Figure 11(p)] Salix, Populus, Alnus, Fraxinus, and Pterocarya and
Liquidambar. Of these, the latter two are today absent from
the regional flora but have a relict distribution in southeastern
Remarks Europe and Asia Minor. A further taxon extinct from the
This specimen falls within the morphological range of the modern flora of Europe is represented by papillate cupressac-
Apium inundatum type of Punt (1984). eous pollen belonging to Taxodioideae or Sequoioideae.
These may have been riparian plants or plants of well-drained
Apiaceae sp. 2 [pollen; Figure 11(q)6 soils. All the herbaceous plants recorded in the palynological
record might have been part of riparian vegetation as well but
not restricted to this vegetation type. Likewise, the liana
Remarks Parthenocissus may have been part of riparian vegetation
Despite being poorly preserved, the figured specimen clearly and other forest types.
falls within the morphological range of the Trinia glauca type Mesic forest vegetation is mainly represented by oaks.
of Punt (1984). Mesic oaks are most common among leaf fossils and make
up 7% in the palynological assemblage. Most eye-catching is
Incertae sedis the presence of Quercus aff. cerris that might have been a
main component of a dry oak forest. Accessory elements in
Leguminophyllum sp. [Figure 4(k)] these forests may have been Crataegus and evergreen oaks, as
Material – S182045 well as conifers. Lobed oaks of section Quercus (white oaks)
are ecologically more diverse and may as well have been part
Remarks of the riparian vegetation. The same is true for Carya.
Small, sessile leaflets with entire margin are commonly Further, Acer sect. Platanoidea and Castanea formed part of
assigned to Fabaceae. However, similar leaves/leaflets also mesic forest vegetation.
occur in a wide range of other families. A substantial number of taxa recorded in the plant assem-
blage of Bezhan occur today in sub-Mediterranean and
Mediterranean woodlands. These taxa include Ulmus aff.
Indet. leaf 1 [Figure 4(l)] minor, Coriaria, Acer aff. monspessulanum, Erica aff. arborea,
Material – S182046 and Olea. It is noteworthy that such woodlands occur adja-
cent to dry beech forests in northeastern Spain (Llierca valley)
and north of Genova. Here, Erica arborea and Quercus ilex
Remarks
occur in the understorey of Castanea sativa adjacent to Fagus
We are unable to assign this apical part of a leaf with finely
stands (Genova) and Coriaria, Erica arborea, and Quercus ilex
crenulated margin to a particular family or genus.
form forest edges of light Fagus forests (Denk 1998). These
woodlands thrive under fully humid Cfa and Cfb climates,
Discussion which change into summer-dry Cs climates towards the
Mediterranean sea. This underscores the sub-Mediterranean
Palaeoenvironment
character of these woodlands.
Using ecological properties of closely related modern species, Higher up in the Bezhan area and partly interlocked with
the ecological niches of the fossil taxa recorded in the Bezhan mesic forests thrived a diverse montane conifer forest (Figure
assemblage were inferred (Table 1). 12). The pollen assemblage (Table 1) is dominated by conifers
Taxa, which are characteristic of steppe environments in (nearly 70%), of which ca. 40% belong to Pinus (subgenus
glacial periods (Artemisia), occur in very low amounts in our Pinus 37%, subgenus Strobus 2.9%). Furthermore, Abies,
sample (up to 1%). Hence, it is unlikely that these pollen Cedrus, and Tsuga spp. reach between 5% and 10%. This
grains represent extensive steppe areas but rather might ori- suggests local presence of diverse conifer forests.
ginate from small open patches in different kinds of forest
and woodlands (e.g. pine forest, open Q. cerris forest, wood-
land with Acer monspessulanum, Ephedra, Olea, Erica, etc.; Age
Figure 12).
Although our pollen data come from a single horizon, the In general, pollen spectra from intramontane basins without
composition of the pollen assemblage indicates interglacial additional age constraints (e.g. mammals, tephra) are difficult
conditions. Specifically, the very low amount of herbaceous to correlate with marine or coastal sections. For example,
taxa (including Artemisia) and relatively high percentages of Messinian sediments at Sioneri (Piemonte, Italy) record
 HISTORICAL BIOLOGY 301

Figure 12. Dry, wet, mesic, and montane habitats in the Pleistocene of Bezhan.

hinterland vegetation very similar to the one from Bezhan with according to Bertini 2010, 2013; Bertini and Martinetto 2014;
the exception of Cathaya and Sciadopitys both of which are not Fidolini et al. 2013) represents a rich leaf flora of Piacenzian
found at Bezhan. Abies, Cedrus, Picea, Sciadopitys, and Tsuga age with many exotic elements (e.g. Magnolia, Ocotea,
are considered as the main constituents of the montane vege- Trigonobalanopsis, Engelhardioideae, palms etc.) all of which
tation belt in the Messinian and Pliocene of Italy (Bertini and are absent from the Bezhan flora.
Martinetto 2011) and hence cannot be used to discriminate a The fact that the plant assemblage of Bezhan includes at least
late Miocene from a Pliocene site. If compared to various plant 19% of taxa corresponding to extant species strongly indicates an
fossil localities with well-constrained age, the Bezhan assem- age younger than Messinian or Pliocene for this flora. Reliable
blage is characterised by components closely resembling extant fossil records of modern species have usually not been reported
species (e.g. Quercus aff. cerris, Acer aff. monspessulanum). from sediments younger than Gelasian, Calabrian, and Middle
Adjacent Messinian sites, for example, Vegora, northern Pleistocene (see e.g. Martinetto 2015) and these ages are in agree-
Greece, entirely lack modern species (Kvaček et al. 2002). ment with extant species ages inferred from molecular studies
Likewise, Zanclean marine records in northern Italy include (Bagnoli et al. 2016, Quercus cerris; Gömöry et al. 2018, Fagus).
many exotic elements (Engelhardioideae, Magnolia, palms, Plant assemblages well comparable to the flora of Bezhan
Sapotaceae, etc.); palynofloras and carpofloras show a predo- are known from Pleistocene deposits of Central and southern
minantly East Asian affinity. Plant assemblages from the Italy. For example, the Pietrafitta site, Tiberino Basin, Central
Piacenzian/Gelasian boundary in northern Italy have a slightly Italy, is dated to middle Calabrian based on a rich vertebrate
cooler signature but still have distinct East Asian (Hokkaido) fauna (1.4–1.3 Ma; Martinetto et al. 2014). Pollen zones below
affinities (Bertini and Martinetto 2014). In Central Italy, only and above a lignite seam (and including the lignite seam)
moderate temperature fluctuations are recorded in the dom- show a pollen flora similar to the one recorded from Bezhan.
inating taxa (Engelhardioideae, Taxodioideae versus Cedrus, In addition, macrofossils include unambiguous leaf remains
Tsuga, Picea, Abies) in warm and cool phases during the of Quercus cerris.
Pliocene. Many exotic taxa are recorded (Symplocos, palms, From southern Italy, lacustrine floras dated to Calabrian
Sapotaceae, Sterculioideae, etc.; Bertini and Martinetto 2014). are known from the Camerota Basin (Campania; Russo-
The Meleto clay (Fischer and Butzmann 2000; age revised Ermolli 1999). The age of the Camerota succession is a matter
302 T. DENK ET AL.

of debate; Russo-Ermolli (1999) suggested an age of 1.78– key taxa to differentiate Gelasian and Calabrian pollen floras
1.48 Ma (based on nannofossils and foraminifera), while Suc in Italy. Comparing presence/absence data from Italian
and Popescu (2005) and Suc et al. (2018) consider this section Pleistocene floras with the flora from Bezhan shows that
to be slightly younger, 1.3–1.2 Ma (based on pollen stratigra- Bezhan and the Calabrian Italian sites share the presence of
phy). The pollen record of this succession can be divided into Olea and lack a number of elements that are present in the
two parts. In the lower part, Carya is dominating, Oleaceae Gelasian sites of southern Italy (Cathaya, Sequoia type, and
and Ceratonia are relatively abundant and single grains of subtropical trees). This and the finding that several taxa
warmth loving elements occur (e.g. Sapotaceae, recorded for Bezhan probably represent modern species pro-
Engelhardioideae; Bernac 1984). In the upper part, Quercus vides further evidence that the fossil-bearing layer from which
and Artemisia dominate, Amaranthaceae are more abundant the Bezhan plant assemblage derives might be of Calabrian
while Oleaceae are much less abundant and warmth-loving (1.8–0.781 Ma) age.
elements are absent (Bernac 1984; Russo-Ermolli 1999). A younger age seems unlikely. For example, a detailed
Pollen assemblages reported for the Camerota section are palynological investigation of Middle Pleistocene layers at
further characterised by Pinus, Tsuga, Cathaya, Megalopolis (southwestern Greece) shows an alternation of
‘Taxodiaceae’, and Cedrus, along with Pterocarya, Ulmus, forest and open vegetation cycles. Exotic taxa are absent from
Liquidambar, and Carpinus (Baggioni et al. 1981; Bernac the palynofloras and both forest and open vegetation cycles
1984; Russo-Ermolli 1999). The Bezhan pollen flora mainly have high percentages of herbaceous plants (Asteraceae in
corresponds in its composition and the absence of warmth open vegetation cycles, Poaceae in forest cycles; Okuda et al.
loving elements (Sapotaceae, Engelhardoideae) to the pollen 2002). Likewise, a leaf assemblage of Riano (Rome) dated at
record of the upper Camerota basin fill, but differs by rela- 450 ka is composed of modern species found today in the
tively low abundance of non-arboreal pollen and absence of region or in adjacent regions of western Eurasia (Pterocarya,
Cathaya. The presence of elements coming from different Zelkova) and is lacking exotic taxa (Follieri 1958; Bertini et al.
vertical vegetation belts indicates that the Camerota Basin 2014). The same pattern is seen in a 500 ka pollen profile
was surrounded by significant relief. Baggioni et al. (1981) from Lake Ohrid (Sadori et al. 2016).
reported a macroflora from the upper part of the Camerota
basin fill corresponding to the Bezhan macroflora by the
Disappearance of exotic taxa and origin of modern
presence of oaks with affinities to section Quercus, Acer cf.
species
monspessulanum and Carpinus orientalis (involucre), but also
including Fagus, Carya, and Zelkova. The well-dated The plant assemblage of Bezhan is characterised by a rela-
Montalbano Jonico section, 1.25–0.9 Ma (Joannin et al. tively high amount of taxa that can be referred to modern
2008), differs from the Bezhan pollen flora by a high non- species (Ranunculus aquatilis, Ulmus minor, Quercus cerris,
arboreal component. Coriaria myrtifolia, Populus alba, Acer monspessulanum, Erica
From Armenia, a middle Calabrian flora (Ollivier et al. arborea, and Olea europea). Hence, of 52 taxa recorded, ca.
2010) with radiometric dating also includes macrofossils simi- 19% represent extant European species. Given that some taxa
lar to the Bezhan assemblage (Quercus cerris, Betula, Carpinus, in the pollen record are determined only to family level, this
Populus alba, Salix spp., Ulmus minor, Crataegus, number may be even larger. For example, pollen of Apiaceae
Myriophyllum, Acer spp., Paliurus spina-christi, Phragmites). may belong to a modern species, which we could not deter-
A recent palynological investigation of a sediment core from mine because the preserved pollen features do not provide
Lake Ohrid at the border between the Republic of Macedonia sufficient diagnostic characteristics for species delimitation. A
and Albania (Donders et al. 2018) reveals strong similarity with latest Calabrian site of Central Italy that is markedly similar
our pollen spectrum from Bezhan. Specifically, 1.34–1.2 Ma to the Bezhan assemblage yielded a fruit and leaf assemblage
sediments from the Lake Ohrid are similar to the Bezhan with 80% of the species representing extant local species
pollen spectrum. (Martinetto and Sami 2001). At the same time, both these
A late Calabrian (800,000 ka) plant assemblage including localities still contain exotic elements such as Tsuga. In the
leaves and fruits from Oriolo, Ravenna province, is also Bezhan assemblage, Tsuga is relatively common (10%).
similar to the Bezhan assemblage (Martinetto and Sami According to Magri et al. (2017), values of Tsuga pollen
2001). This flora shares many taxa with Bezhan: Tsuga, dropped far below 10% at various points during the
Pinus, Abies, Salix, Populus alba, Carya, Pterocarya, Alnus, Calabrian, whereas last records of single pollen grains occur
Carpinus, Quercus cerris, Ulmus minor, Crataegus, Coriaria, around the Calabrian/Middle Pleistocene boundary (Bertini
Acer monspessulanum, and Fraxinus. However, at Oriolo, 2010). A remarkable feature of the Bezhan assemblage is the
80% of the species represent extant local species (at least presence of three different types of Tsuga pollen, including
19% at Bezhan). extant North American and East Asian types.
According to Combourieu-Nebout et al. (2015), a decrease A second prominent element in the flora of Bezhan is leaves
in Taxodium-type and increase in montane trees at the end of referable to the modern Quercus cerris. From Greece, Velitzelos
the Pliocene is followed by a decrease in Taxodiaceae and et al. (2014) reported a single leaf of Quercus aff. cerris from
increase in steppe vegetation in the Gelasian (see, for late Pliocene/Gelasian deposits from Atalanti/Zeli. The flora of
instance, Stirone, northern Italy). A comparison of numerous Atalanti/Zeli has extinct species of Quercus sect. Ilex, Alnus,
well-dated palynofloras across Italy south of 42.5°N by and Betula that are typical of late Neogene floras and it is
Combourieu-Nebout et al. (2015) identified a number of difficult to determine with certainty whether the single leaf of
 HISTORICAL BIOLOGY 303

Quercus belongs to the modern species since the leaf poly- Disclosure statement
morphism of the fossil taxon cannot be assessed with a single
No potential conflict of interest was reported by the authors.
leaf. From Calabrian deposits of Rhodes (Archangelos;
Velitzelos et al. 2014), single leaves referred to as Q. pseudo-
castanea also may belong to Q. cerris. As stated above, further
Funding
unambiguous records of Q. cerris are from Calabrian sites in
Italy (Martinetto et al. 2014) and Armenia (Ollivier et al. 2010). This study was financed by a grant of the Swedish Research Council (VR;
From these (limited) data, it appears that dates of last project no. 2015-03986) to TD. HTG was supported by The Scientific
common presence of exotic (extinct in western Eurasia) taxa and Technological Research Council of Turkey (TÜBİTAK), 2219 Post-
Doctoral Research Fellowship Program (2017/2), project no.
and of first appearances of modern taxa converge at the 1059B191700382.
Calabrian. This is in agreement with recent molecular studies
(Gömöry et al. 2018; modern Fagus sylvatica s.str.) but
younger than the inferred Gelasian divergence time for east- ORCID
ern and central population of Q. cerris (Bagnoli et al. 2016).
Thomas Denk http://orcid.org/0000-0001-9535-1206
H. Tuncay Güner http://orcid.org/0000-0001-9742-1319
Conclusions and outlook Johannes Martin Bouchal http://orcid.org/0000-0002-4241-9075

Here, we provide a comprehensive palaeobotanical assess-

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