Introduction
Deep, ancient lakes are of global importance for palaeoclimate research, and
diatom records from these lakes can provide powerful insights into
mechanisms of climate and environmental change over long timescales (Mackay
et al., 2010). Lake Ohrid (Macedonia and Albania) is a rare example of a deep,
ancient Mediterranean lake (Roberts and Reed, 2009). It is thought to be the
oldest lake in Europe, and probably the most biodiverse lake in the world
(Albrecht and Wilke, 2008; Levkov and Williams, 2012). It is therefore a key
site for palaeoclimate research in the northeastern Mediterranean region
(Wagner et al., 2014). As most Mediterranean lakes are relatively shallow
and demonstrate a strong diatom response to shifts in moisture availability
(Zhang et al., 2014), the diatom record in Lake Ohrid may provide an
important means by which to disentangle temperature and precipitation
effects in Mediterranean climate research.
Temperature reconstructions during the Lateglacial and Holocene in the
northeastern Mediterranean region are rare and rely mainly on pollen data
(e.g. Bordon et al., 2009; Dormoy et al., 2009; Pross et al., 2009). Using
pollen as a temperature proxy in this region is controversial. Renssen et al. (2012) suggested that pollen-based temperature reconstruction may be
unreliable since precipitation rather than temperature is the main climatic
control on Mediterranean vegetation distribution, while Mauri et al. (2015)
argued instead that pollen transfer functions can provide robust results for
temperature reconstruction in this region. Quantitative climate
reconstruction methods have their own strengths and weaknesses (Birks et al.,
2010; Juggins and Birks, 2012), and pollen-based temperature reconstructions
can show different patterns and amplitudes of change depending on the
technique used (Dormoy et al., 2009; Peyron et al., 2013). Deep Lake Ohrid,
for which no major lake-level change during the Lateglacial and Holocene has
been reported (Wagner et al., 2009; Reed et al., 2010), is arguably an ideal
site for using palaeolimnological proxies such as diatoms to improve
understanding of temperature change in this region.
To date, diatom-based palaeoclimate research in Lake Ohrid has focused on
low-resolution analysis of response to the last glacial–interglacial cycle
(Wagner et al., 2009; Reed et al., 2010; Cvetkoska et al., 2012, 2015).
Fluctuations in diatom composition between glacial or stadial and interglacial or interstadial stages have suggested a strong and simple response
to temperature-induced changes in lake productivity. Here, we focus on the
analysis of diatom response to Lateglacial and Holocene limnological,
climate and environmental change, testing the response of diatoms in greater
detail than has been achieved previously. Core Co1262, in the western part
of the lake, is chronologically well constrained and is the longest and most
continuous Holocene sequence yet retrieved from the lake. Diatom results are
compared with sedimentological and geochemical data from the same core
(Wagner et al., 2012; Lacey et al., 2015). We also compare core Co1262 diatom results with
low-resolution diatom data from core Lz1120 (southeastern Lake Ohrid; Wagner
et al., 2009), core Co1202 (northeastern Lake Ohrid; Reed et al., 2010;
Cvetkoska et al., 2012), the DEEP site (central Lake Ohrid; Cvetkoska et
al., 2015) and core 9 (north-central Lake Ohrid; Roelofs and Kilham, 1983) and with palynological data from the region (Wagner et al., 2009;
Panagiotopoulos et al., 2013).
Site description
Lake Ohrid (40∘54′–41∘10′ N,
20∘38′–20∘48′ E; 693 m a.s.l.; Fig. 1) is an ancient graben lake with a continuous
> 1.2 Myr sedimentary record (Wagner et al., 2014; Francke et al., 2016). The lake is
about 30 km long, 15 km wide, and has a surface area of 358 km2 and a
maximum water depth of 293 m (Albrecht and Wilke, 2008; Wagner et al.,
2012). The lake basin has a relatively simple tub-shaped morphometry with
steep slopes along the western and eastern sides and less inclined shelves
in the northern and southern parts. It is surrounded by the Galičica
Mountain (2256 m a.s.l.) to the east, the Mali i Thatë Mountain (2276 m a.s.l.) to the southeast, the Jablanica Mountain (2225 m a.s.l.) to the
northwest, and the Mokra Mountain (1512 m a.s.l.) to the west. Geological
formations around the lake comprise Palaeozoic metamorphics to the
northeast, karstified Triassic limestones to the east, southeast and
northwest, Jurassic ophiolites to the west, Tertiary molasse deposits to the
southwest and south, and Quaternary fluviolacustrine deposits in the
Struga, Ohrid and Starovo plains to the north, northeast and south,
respectively (Hoffmann et al., 2010; Reicherter et al., 2011). The local
climate belongs to the Mediterranean regime with minimum precipitation
occurring in June–August, and it is also influenced by the continental
regime as it is surrounded by high mountains (Watzin et al., 2002).
North–south winds prevail in the lake basin (Stanković, 1960; Matzinger
et al., 2006a). The catchment vegetation is distributed mainly in
altitudinal belts as, in ascending order, mixed deciduous oak forest, beech
forest, coniferous forest, and subalpine and alpine meadows (Lézine et
al., 2010; Panagiotopoulos et al., 2013).
Map showing the location of Lake Ohrid (Macedonia and Albania) and the
coring sites Co1262 (this study; Wagner et al., 2012; Lacey et al., 2015),
Lz1120 (Wagner et al., 2009), Co1202 (Vogel et al., 2010; Reed et al., 2010;
Cvetkoska et al., 2012), DEEP site (Wagner et al., 2014; Francke et al.,
2015; Cvetkoska et al., 2015) and Core 9 (Roelofs and Kilham, 1983). Arrows indicate main river flows (C: Cerava River; K: Koselska
River; S: Sateska River; D: Crni Drim River), and asterisks indicate major springs
(N: Sveti Naum; T: Tushemisht; B: Biljana; V: Dobrá Voda). Modified from
Reed et al. (2010).
Lake Ohrid is fed mainly by karstic springs (53 %, comprising 27 %
surface springs and 26 % sublacustrine springs), with 24 % of water
input from river inflow and 23 % from direct precipitation on the lake
surface. Direct outflow is via the Crni Drim River (66 %), with 34 %
evaporative loss (Matzinger et al., 2006a). The largest surface springs are
those of Sveti Naum and Tushemisht at the southeastern edge of the lake,
with smaller complexes comprising the Biljana spring in the northeastern
part and the Dobrá Voda spring in the northwest (Albrecht and Wilke, 2008).
Sublacustrine springs are located mainly on the eastern shore of the lake,
with one in the northwestern corner (Matter et al., 2010). An important
source of karstic springs is the Lake Prespa underground outflow, which
provides 21 % of total Lake Ohrid water input (Matzinger et al., 2006b).
The karst aquifers are also charged by the infiltration of precipitation on
the Galičica and Mali i Thatë mountains. There is no major inflow close to
the Lin Peninsula in the western part of the lake. The top 150–200 m of
the water column is mixed every winter, and a complete circulation of the
entire water column occurs roughly every seventh winter (i.e. it is
oligomictic; Stanković, 1960; Matzinger et al., 2006a). Lake Ohrid is
alkaline, with pelagic water pH 8.0–8.9 (measured in 2004–2006; Tasevska
et al., 2012) and ionic composition dominated by bicarbonate and calcium
(Stanković, 1960). It is highly oligotrophic, with total phosphorus and
total nitrogen concentration throughout the water column at the lake centre
of 4.6–6.8 and 171–512 µg L-1, respectively
(measured in 2000–2001; Watzin et al., 2002) and low dissolved silica
concentration of < 0.2 mg L-1 in the trophogenic zone in summer
(in 1957; Stanković, 1960). It is typically fresh and clear, with low
water conductivity of 195–239 µS cm-1 in the littoral zone (in
2009–2010; Schneider et al., 2014) and a high Secchi depth of 11–21 m (in
2000–2003; Petrova et al., 2008).
Material and methods
Following detailed hydro-acoustic surveys carried out between 2004 and 2009
on lake bathymetry and sediment architecture (Wagner et al., 2012; Lindhorst
et al., 2015), a 1008 cm long core, Co1262, was recovered in June 2011 from
260 m water depth off the Lin Peninsula at the western margin of
Lake Ohrid, using UWITEC gravity and piston coring equipment from a floating
platform (www.uwitec.at). Excluding a 200 cm thick mass wasting
deposit and three smaller ones (< 20 cm) identified by coarse grain
size and low water content (Wagner et al., 2012), the undisturbed composite
sediment sequence is 785 cm long.
The age model of core Co1262 was described in detail by Lacey et al. (2015).
Radiocarbon dating, tephrostratigraphy and cross correlation of calcite and
organic matter content with other sediment cores from Lake Ohrid and the
hydraulically linked adjacent Lake Prespa were used to provide a chronological
control for core Co1262. The age model was calculated based on five calendar
ages of terrestrial plant remains, three well-dated tephras (Somma-Vesuvius
AD 472/512 tephra, Mount Etna FL tephra and Somma-Vesuvius Mercato tephra;
Sulpizio et al., 2010; Damaschke et al., 2013) and five correlation points,
using the smoothing spline method (smoothing: 0.1) with the software
package Clam 2.2 (Blaauw, 2010). One radiocarbon age of fish remains is
apparently too old and was excluded, as the fish remains are probably
affected by a reservoir effect or they are redeposited (Wagner et al.,
2012). The radiocarbon and tephra chronologies are shown in Table 1, and the
correlation of core Co1262 with other sediment cores was described in detail
by Wagner et al. (2012). The age model shows that core Co1262 covers the
past 12 300 years (Fig. 2), spanning the Lateglacial and Holocene period.
Age–depth model of core Co1262 (modified from Lacey et al., 2015).
Diatom analysis was carried out on 104 samples in the 785 cm long master
sequence, taken every 8 cm but at a higher resolution of 4 cm around
putative abrupt events at ca. 8200 and 4200 cal yr BP. The age resolution
is ca. 80–110 years for the top 120 cm, ca. 40–70 years between
240–120 cm (ca. 2200–1400 cal yr BP), ca. 100–200 years between
350–240 cm (ca. 4400–2200 cal yr BP), ca. 270–350 years between
435–350 cm (ca. 7800–4400 cal yr BP) and ca. 90–120 years for the
lower sequence. The relatively low age resolution in the middle of the
core is a result of low
sedimentation rate.
Age estimates for core Co1262. The calibration of radiocarbon ages
into calendar ages is based on Calib 7.0.2 (Stuiver and Reimer, 1993) and
IntCal13 (Reimer et al., 2013) and on a 2σ uncertainty.
Core depth
Lab code
Material
Radiocarbon age
Calendar age
(cm)
(14C yr BP)
(cal yr BP)
17
COL 1251.1.1
terrestrial plant remains
164 ± 20
140 ± 145
122
the AD 472/512 tephra
1478/1438
240
COL 1735.1.1
terrestrial plant remains
2176 ± 46
2190 ± 140
315
the FL tephra
3370 ± 70
318
COL 1736.1.1
terrestrial plant remains
3280 ± 45
3510 ± 110
335
COL 1737.1.1
terrestrial plant remains
3581 ± 40
3850 ± 130
368
COL 1738.1.1
terrestrial plant remains
4370 ± 44
5030 ± 190
503
the Mercato tephra
8890 ± 90
548
COL 1243.1.1
fish remains
10 492 ± 37
12 400 ± 190
(rejected)
Standard techniques in Battarbee et al. (2001) were adopted for preparation
of diatom slides. Approximately 0.1 g dry weight sediment samples were
heated in 25–30 mL 30 % H2O2 to oxidise organic matter, and a
few drops of concentrated HCl were added to remove carbonates and remaining
H2O2. The residue was suspended in distilled water, centrifuged
and washed four to five times to remove clay and remaining HCl. The suspension was
diluted to an appropriate concentration, and known quantities of plastic
microspheres were added to allow calculation of absolute diatom
concentration. Diatom slides were mounted using Naphrax™.
Diatoms were counted along transects at ×1000 magnification under
oil immersion on an OLYMPUS BX51 light microscope. More than 500 valves per
slide were counted. Diatom identification was based on a range of standard
literature (Krammer and Lange-Bertalot, 1986, 1988, 1991a, b;
Lange-Bertalot, 2001; Krammer, 2002; Houk et al., 2010, 2014) and the
dedicated Lake Ohrid works, which reflect ongoing revision and improvement of
diatom taxonomy (Levkov et al., 2007; Levkov and Williams, 2011; Cvetkoska
et al., 2012, 2014a), adopting the nomenclature of the Catalogue of Diatom
Names (on-line version; Fourtanier and Kociolek, 2011). The endemics,
Cyclotella fottii Hustedt and the smaller taxon Cyclotella hustedtii Jurilj were previously separated (Hustedt,
1945; Jurilj, 1954). They are now combined as C. fottii but we split morphotypes
into size classes to investigate additional subspecies response (cf. Reed et
al., 2010; Cvetkoska et al., 2012). Cyclotella minuscula (Jurilj) Cvetkoska is a new species
identification (Cvetkoska et al., 2014a), which was previously identified as
Discostella stelligera (Cleve & Grunow) Houk & Klee (Roelofs and Kilham, 1983; Wagner et
al., 2009) or briefly combined with Cyclotella ocellata Pantocsek (Reed et al., 2010; Cvetkoska
et al., 2012). Cyclotella ocellata morphotypes were split according to number of ocelli. Stephanodiscus transylvanicus Pantocsek is
another improvement of species identification (Cvetkoska et al., 2012),
which was previously identified as Stephanodiscus astraea (Ehrenberg) Grunow (Roelofs and Kilham,
1983), Stephanodiscus neoastraea Håkansson & Hickel (Wagner et al., 2009) or Stephanodiscus galileensis Håkansson
& Ehrlich (Reed et al., 2010). Diatom results were displayed using Tilia
version 1.7.16, and zone boundaries were defined based on relative abundance
data according to constrained incremental sum of squares (CONISS) cluster
analysis (Grimm, 2011).
To assess the quality of diatom preservation, the F (fractional) index of
Ryves et al. (2001) was used to calculate the dissolution of the dominant
endemic taxon C. fottii which consists of a range of morphotype cell sizes. The
F index is the ratio of pristine valves to all valves (sum of pristine and
partially dissolved valves), where F= 1 indicates perfect preservation
(Ryves et al., 2001). Unconstrained ordination techniques were used to
explore the variance in the diatom relative abundance data using Canoco for
Windows 4.5 (Ter Braak and Šmilauer, 2002). Detrended correspondence
analysis (DCA) gave the largest gradient length of 1.85 SD units, and thus
the linear ordination method principal components analysis (PCA) was
selected (Ter Braak, 1995; Lepš and Šmilauer, 2003). Diatom
concentration data can be influenced both by differences in cell sizes of
diatom species and by changes in sedimentation rates, and diatom biovolume
accumulation rate (BVAR) data provide a more robust interpretive tool for
productivity than concentration data (Battarbee et al., 2001; Rioual and
Mackay, 2005). However, the necessary diatom cell biovolume data and dry
sediment bulk density data were not available. Instead, we assessed
qualitatively the potential influence of sedimentation rates and valve
sizes of main planktonic taxa (including size classes of C. fottii) on diatom
concentration.
Results
A total of 99 diatom species was identified, consisting of 9 planktonic
species, 5 facultative planktonic species and 85 benthic species. In
spite of low diversity of plankton, its relative abundance is > 90 % throughout the record. Six major diatom assemblage zones can be
defined based on diatom relative abundance data, which match well with
changes in absolute diatom concentration (Fig. 3). F index values for the
endemic Cyclotella fottii are > 0.75 throughout the record, with
> 500 valves counted on each slide and > 2 × 107 valves g-1 concentration per sample, and diatom preservation quality is high.
In Zone D-1 (785–639 cm; ca. 12 300–10 600 cal yr BP), planktonic C. fottii is
dominant at > 80 % abundance, diatom PCA Axis 1 scores are
low, and diatom concentration is very low. In Subzone D-1a (785–743 cm; ca.
12 300–11 800 cal yr BP), facultative planktonic taxa, mainly comprising
Staurosirella pinnata (Ehrenberg) Williams & Round and Pseudostaurosira brevistriata (Grunow) Williams & Round, are
present at ca. 8 % abundance. Subzone D-1b (743–639 cm; ca.
11 800–10 600 cal yr BP) is marked by a slight increase in the abundance of planktonic
C. minuscula, and facultative planktonic taxa decrease slightly to < 5 %.
Summary diatom diagram of relative abundance of planktonic and
facultative planktonic species from core Co1262, showing lithostratigraphy
(modified from Wagner et al., 2012), diatom concentration, C. fottii
F index values, and principal component analysis (PCA) Axis 1
scores.
Zone D-2 (639–551 cm; ca. 10 600–9500 cal yr BP) shows a decline in the
abundance of C. fottii (and its large morphotypes in particular) and a shift to
relatively high diatom PCA Axis 1 scores. Cyclotella ocellata increases to ca. 10–30 % in
Subzone D-2a (639–607 cm; ca. 10 600–10 200 cal yr BP), and
Stephanodiscus transylvanicus appears, with a peak in diatom concentration. In Subzone D-2b
(607–551 cm; ca. 10 200–9500 cal yr BP), C. minuscula increases to ca. 20–40 % at the expense of
C. ocellata and S. transylvanicus, while diatom concentration is relatively low.
In Zone D-3 (551–449 cm; ca. 9500–8200 cal yr BP), C. ocellata is abundant throughout
(ca. 20–60 %), with high diatom PCA Axis 1 scores and diatom
concentration. In Subzone D-3a (551–511 cm; ca. 9500–9000 cal yr BP), C. ocellata
shows sustained peak abundance (ca. 30–60 %), including non-classic
morphotypes with ≥ 4 ocelli at the valve centre. Subzone D-3b
(511–449 cm; ca. 9000–8200 cal yr BP) is characterised by an increased abundance of S. transylvanicus,
and C. ocellata consists mainly of the classic morphotype (three ocelli).
In Zone D-4 (449–269 cm; ca. 8200–2600 cal yr BP), C. fottii is at high abundance
(ca. 60–85 %), S. transylvanicus is consistently present at ca. 5–10 % abundance, and
C. ocellata is at relatively low abundance (ca. 10–20 %), with a decline in diatom
PCA Axis 1 scores and diatom concentration.
In Zone D-5 (269–214 cm; ca. 2600–2000 cal yr BP), C. ocellata shows renewed high
abundance (ca. 50–60 %), with an increase in diatom PCA Axis 1 scores.
Diatom concentration is relatively high.
In Zone D-6 (214–0 cm; ca. 2000 cal yr BP–present), C. ocellata is abundant (ca.
25–60 %), and there is increased but fluctuating abundance of C. minuscula, showing
a sharp peak (ca. 35 % abundance) at the lower zone boundary. Diatom PCA
Axis 1 scores are high, but diatom concentration is low.
Interpretation
The limnological interpretation of diatoms rests in part on previous studies
(Stanković, 1960; Allen and Ocevski, 1976; Ocevski and Allen, 1977),
which found that endemic C. fottii occupies the hypolimnion throughout the year in
Lake Ohrid. Cyclotella fottii is described as oligothermic and oligophotic, and it is thought to
be an opportunistic species which extends its growth into the epilimnion
during periods of low temperature in winter and early spring (Stanković,
1960). Stephanodiscus transylvanicus probably has similar ecological preferences to other intermediate-
to large-sized Stephanodiscus species by virtue of their morphological similarity
(Bradbury, 1991) and has been described as hypolimnetic (Stanković,
1960; Allen and Ocevski, 1976) and mesotrophic (Wagner et al., 2009).
Cyclotella ocellata (and by inference C. minuscula) adopts an epilimnetic life habit in Lake Ohrid, thrives
mainly in late spring and summer, and is described as eurythermic
(Stanković, 1960). It has been described as mesotrophic (Wagner et al.,
2009) and is taken as an indicator of nutrient enrichment in this highly
oligotrophic lake compared to C. fottii (Lorenschat et al., 2014). Cyclotella ocellata is also found to
be favoured by high nitrogen concentration in shallower, mesotrophic Lake
Prespa, the sister lake of Lake Ohrid (Kocev et al., 2010). Cyclotella minuscula is very small
(3–5 µm diameter), and probably has a similar ecological niche as
other small-celled Cyclotella sensu lato species (Saros and Anderson, 2015), which have low
nutrient and light requirements, high growth rates and low sinking rates,
owing to their high ratio of surface area to volume (Winder et al., 2009;
Finkel et al., 2009).
In contrast to the hypothesis of a linear response to temperature suggested
in earlier, low-resolution diatom studies (Roelofs and Kilham, 1983; Wagner
et al., 2009; Reed et al., 2010; Cvetkoska et al., 2012), we think that
variations in the relative abundance of these taxa may be a direct response
to shifts in temperature-induced lake productivity, but we should also
consider the possible influence of temperature-related
stratification or mixing regime, wind forcing, catchment mediation, light
limitation, and/or spring inflow. It should be noted that temperature here
is mean annual epilimnetic water temperature (“water temperature”
hereafter). Lake Ohrid is still highly oligotrophic and exceptionally
transparent (Matzinger et al., 2006a, 2007), and hypolimnetic diatoms can be
found at > 200 m water depth (Stanković, 1960), so light
limitation can be assumed to be insignificant. Although Lorenschat et al. (2014) suggested that karstic springs from Lake Prespa have a strong
influence on the nutrient budget of Lake Ohrid, it is apparent that spring
inflow and associated nutrient transport do not reach the site of core
Co1262 in the westernmost part of the lake (Matzinger et al., 2006a), and
thus the direct influence of springs is probably negligible.
Comparison of diatoms in core Co1262 with sedimentological and
geochemical data from the same core. Calcite (CaCO3) content and
potassium (K) concentration are from Wagner et al. (2012), and total organic
carbon (TOC) content, hydrogen index (HI) and oxygen index (OI) are from
Lacey et al. (2015).
From the results of this study, the complacency in C. fottii F index values and high
quality of diatom preservation (Fig. 3) indicate that major shifts in diatom
composition are not related to the taphonomic effects of dissolution but
represent real ecological shifts. Diatom PCA Axis 1 scores clearly vary
according to the relative abundance of the epilimnetic taxa, with high
positive scores associated with the dominance of epilimnetic taxa and high
negative scores in zones of low-diversity C. fottii dominance. To strengthen
interpretation, the diatom results of core Co1262 are compared with calcite
(CaCO3) and organic matter (i.e. total organic carbon, TOC) content and
Rock Eval pyrolysis data (hydrogen index, HI; oxygen index, OI) from the
same core (Fig. 4; Wagner et al., 2012; Lacey et al., 2015). Calcite content
in particular has proved to be a strong proxy for temperature-induced
productivity in this lake (Vogel et al., 2010; Wagner et al., 2010). Diatom
shifts in core Co1262 are well correlated with those of core Lz1120 (Fig. 5;
Wagner et al., 2009), validating diatom interpretation of core Co1262 as
representative of basin-wide response. The possible influence of catchment
dynamics and nutrient delivery is assessed through comparison with
sedimentological potassium (K) intensity and sedimentation rate data from
the same core (Fig. 4; Wagner et al., 2012; Lacey et al, 2015), with
palynological data from previous lake sediment cores in Lake Ohrid (Fig. 5;
Wagner et al., 2009) and Lake Prespa (Panagiotopoulos et al., 2013), and
with calcite δ18O data from existing sediment cores in Lake
Ohrid (Leng et al., 2010; Lacey et al., 2015).
The Lateglacial (ca. 12 300–11 800 cal yr BP)
During the Lateglacial or Younger Dryas (Subzone D-1a; ca. 12 300–11 800 cal yr BP), the low-diversity dominance of hypolimnetic, oligothermic and
oligophotic C. fottii indicates low lake productivity in relation to low water
temperature, as during Marine Isotope Stage 2 (MIS 2) in core 9 (Roelofs and
Kilham, 1983), core Co1202 (Reed et al., 2010), and the DEEP site (Cvetkoska
et al., 2015). This corresponds to low calcite content, and this is also
consistent with low organic matter content, low HI and high OI, which suggest
low algal organic matter contribution and/or high organic matter degradation
(Lacey et al., 2015). The regularly-distributed (ca. 8 % relative
abundance) pioneering, facultative planktonic fragilaroid taxa S. pinnata and P. brevistriata are
probably related to cold water and winter lake ice cover (Mackay et al.,
2003; Schmidt et al., 2004), which is consistent with the deposition of
ice-rafted debris inferred from the occurrence of gravel grains (“silt with
dropstones” in “lithostratigraphy” in Fig. 3; Wagner et al., 2012). These
taxa are also probably related to physical disturbance (Anderson, 2000),
which is consistent with intense lake circulation as a result of low water
temperature and strong winds (see below). Low water temperature would have
resulted in the high frequency and long duration of complete lake
circulation which usually occurs in severe winters or following intense wind
action in less severe winters in this lake today (Stanković, 1960). If
subject to winter lake ice cover, this lake would have been dimictic or
monomictic rather than currently oligomictic. Low water temperature during
the Younger Dryas in this lake is consistent with pollen-based air
temperature reconstruction in Lake Maliq (Albania; Bordon et al., 2009), and
SL152 (northern Aegean Sea; Kotthoff et al., 2011), with alkenone- and
foram-inferred low sea surface temperature (SST) in MNB3 (northern Aegean
Sea; Gogou et al., 2007; Geraga et al., 2010), and with the globally stacked
proxy surface temperature record (Shakun et al., 2012). Intense wind action
may have occurred during this cold period (Vogel et al., 2010), in accordance
with the observation that average wind speed in winter is higher than in
summer today (Stanković, 1960). Thus, the capacity for mixing-induced
upward nutrient supply would have been high. High sedimentation rate, high K
intensity (i.e. high clastic content), and low calcite and organic matter
content (i.e. low authigenic matter content) suggest high catchment erosion.
This is supported by sparse vegetation and unsettled soils in the catchment
during the Younger Dryas (Panagiotopoulos et al., 2013). Thus,
erosion-induced external nutrient input would also have been high. However,
Younger Dryas water temperature must have been low enough to prevent
nutrient-induced productivity increase.
Comparison of diatoms in core Co1262 with diatom and palynological
data from core Lz1120, southeastern Lake Ohrid (Wagner et al., 2009).
The earliest Holocene (ca. 11 800–10 600 cal yr BP)
After the Lateglacial, the slight increase in the relative abundance of
small, epilimnetic C. minuscula during the earliest Holocene
(Subzone D-1b; ca. 11 800–10 600 cal yr BP) is surprisingly subtle. It
is consistent with the inherent response of small planktonic diatoms to
climate warming and enhanced thermal stratification with reduced epilimnetic
nutrient availability and/or increased sinking velocities in a deep,
oligotrophic lake (Winder et al., 2009; Finkel et al., 2009; Jewson et al.,
2015). Less intense winds and prolonged calm periods may be another factor
contributing to the increase in C. minuscula in this deep,
oligomictic lake. The rarity (< 5 % relative abundance) of
facultative planktonic taxa suggests either a shorter, less intense period of
lake circulation, in accordance with the increase in C. minuscula,
or a more prolonged ice-free period, in accordance with the disappearance of
ice-rafted debris deposition after ca. 11 300 cal yr BP (Wagner et al.,
2012). The increase in the abundance of epilimnetic Cyclotella
species is also possibly related to a longer ice-free season (Smol et al.,
2005; Rühland et al., 2008). There is a gradual rather than abrupt change
in increasing organic matter content, increasing HI and decreasing OI, which
indicate relatively subtle increases in algal organic matter contribution
and/or organic matter preservation (Lacey et al., 2015). However, diatom
concentration remains as low as during the Lateglacial. Sedimentation rate
remains constant (Fig. 4), and in terms of the possible influence of diatom
cell size, an increase in the abundance of large C. fottii
morphotypes (> 20 µm) may compensate for the increase
in small C. minuscula (Fig. 3). In combination with low calcite
content, low diatom concentration thus indicates that water temperature is
still very low during this period, possibly with only intermittent
stratification. Although the diatom signature of the Lateglacial–Holocene
transition is more pronounced here than in core Co1202 (Reed et al., 2010),
the transition is remarkably muted compared to the marked diatom shifts
observed in shallower southern Balkan lakes. The distinct transition in Lake
Ioannina (northwestern Greece; Wilson et al., 2008; Jones et al., 2013), Lake
Prespa (Macedonia, Albania and Greece; Cvetkoska et al., 2014b), and Lake
Dojran (Macedonia and Greece; Zhang et al., 2014), for
example, is instead a response driven by a major increase in lake level and
moisture availability. The temperature shift was insufficient to cause a
major productivity increase in this deep lake, although high sedimentation
rate, high K intensity and low authigenic matter content probably indicate
high catchment erosion and associated nutrient delivery similar to the
Lateglacial environment. The results also confirm the potential of Lake
Ohrid's contrasting response thresholds to contribute to the separation of
temperature and precipitation change in regional palaeoclimate
reconstruction. However, muted water temperature increase in this lake is not
consistent with a distinctly increasing trend for the globally stacked proxy
mean annual surface temperature (Shakun et al., 2012; Marcott et al., 2013).
The early Holocene (ca. 10 600–8200 cal yr BP)
The early Holocene (Zones D-2 and D-3; ca. 10 600–8200 cal yr BP) is marked
by a sustained increase in the abundance of epilimnetic taxa, with an
alternation between C. ocellata and C. minuscula in Zone D-2 (ca. 10 600–9500 cal yr BP) and
dominance by C. ocellata in Zone D-3 (ca. 9500–8200 cal yr BP). Diatom PCA Axis 1
scores are correspondingly high. Since sedimentation rate is nearly
unchanged compared to Zone D-1 (Fig. 4), high diatom concentration in
Subzone D-2a and Zone D-3 might be attributed to reduced abundance of large
C. fottii morphotypes and increased abundance of relatively small C. ocellata, but high
abundance of very small C. minuscula in Subzone D-2b is associated with low rather than
high diatom concentration (Fig. 3). Thus, diatom concentration could still
indicate a real change in lake productivity during the early Holocene. High
abundance of eurythermic, mesotrophic C. ocellata between ca. 10 600–10 200 cal yr BP
(Subzone D-2a) and between ca. 9500–8200 cal yr BP (Zone D-3) corresponds
to high diatom concentration and high organic matter content, supporting an
interpretation of C. ocellata as indicative of high water-temperature-induced lake
productivity, as in core Co1202 (Reed et al., 2010). This is also consistent
with generally high HI and slightly low OI, reflecting high algal organic
matter contribution and/or better organic matter preservation (Lacey et al.,
2015). High water temperature clearly implies high air temperature, although
the converse does not necessarily apply since low water temperature occurred
during the earliest Holocene. High temperature and possibly associated low
winter wind stress would have reduced the frequency, duration and strength
of lake circulation and thus restrained nutrient availability in the
epilimnion. Nearly constant sedimentation rate (compared to Zone D-1),
generally low K intensity and high organic matter content in the diatom
zones D-2a and D-3 probably represent a decline in catchment erosion and
associated nutrient delivery rather than dilution effects. This is
consistent with dense forest and stable soils in the catchment (Wagner et
al., 2009; Panagiotopoulos et al., 2013). However, nutrient concentration
must have been insufficiently low to prevent a temperature-induced
productivity increase.
High C. minuscula abundance between ca. 10 200–9500 cal yr BP (Subzone D-2b), at the
expense of C. ocellata, corresponds to a major peak in calcite content. Given primarily
photosynthesis-induced calcite precipitation in this lake, with negligible
detrital calcite and minor contribution of calcite precipitated around
spring areas, the peak calcite content indicates high lake productivity and,
by inference, high water temperature (Vogel et al., 2010; Wagner et al.,
2010). However, a contrasting diatom ecological response is shown in this
subzone, with high C. minuscula abundance and low diatom concentration. Although, as
suggested above, strong stratification would support the bloom of
small-sized planktonic diatom species, low diatom concentration is not
consistent with the inferred high water-temperature-induced productivity.
Sedimentation rate is nearly unchanged compared to Subzone D-2a, and, under
a densely-vegetated catchment (Panagiotopoulos et al., 2013), high K
intensity in Subzone D-2b, along with low organic matter content and
relatively high calcite content, does not necessarily imply high catchment
erosion, possibly due to dilution effects. In contrast to Subzone D-2a and
Zone D-3, it is most likely in Subzone D-2b that, corresponding to the peak
calcite content, more nutrients such as phosphorus are lost from the
epilimnion through being absorbed onto the surface of precipitating calcite
particles (Allen and Ocevski, 1976). Epilimnetic nutrient availability in
Subzone D-2b must have been low enough to prevent a high water-temperature-induced productivity increase. The significance of this shift
was not highlighted in a previous study (Reed et al., 2010), wherein C. minuscula was
separated only as a morphotype of C. ocellata.
An increase in the abundance of hypolimnetic, mesotrophic S. transylvanicus in Subzone D-3b
(ca. 9000–8200 cal yr BP) corresponds to renewed calcite accumulation, and
the lower boundary of this subzone is also coincident with an extreme,
abrupt peak in K intensity, which originates from volcanic glass shards and
corresponds to the Mercato tephra (Wagner et al., 2012). The tephra input
would increase epilimnetic silica availability and reduce phosphorus release
from the sediment (Barker et al., 2000; Telford et al., 2004), resulting in
either an increase in diatom concentration (Lotter et al., 1995; Eastwood et
al., 2002) or a shift of diatom composition to the dominance of taxa that
require a high Si / P ratio (Abella, 1988; Cruces et al., 2006). The tephra
impact would also be short-lived, with a recovery of diatom composition
towards the pre-tephra state (Telford et al., 2004; Cruces et al., 2006). It
is apparent that the Mercato tephra has no impact on diatoms here, since S. transylvanicus
maintains its abundance over the long term and diatom concentration
maintains its maximum level. Moreover, most Stephanodiscus species prefer a low Si / P ratio
(Kilham et al., 1986), which also suggests that the tephra has no impact. It
is possible that S. transylvanicus is favoured by phosphorus release in the hypolimnion due
to the dissolution of precipitating calcite and the mineralisation of
settling organic matter from the upper layer (Stanković, 1960; Allen and
Ocevski, 1976; Matzinger et al., 2006a, 2007). In all, during the early
Holocene, high water temperature in this lake is in accordance with the
globally stacked proxy mean annual surface temperature record (Marcott et
al., 2013), and diatom species appear to respond to high water temperature
in different ways: the response of C. ocellata is direct in relation to high water-temperature-induced epilimnetic productivity, while the response of C. minuscula is
indirect in relation to nutrient limitation in the epilimnion. Lacey et al. (2015) interpreted the phase between ca. 8600–8000 cal yr BP (ca. 600
years) as a response to the abrupt 8.2 ka cooling event based on
sedimentological and geochemical data. However, based on ca. 100-year
resolution diatom data, there is no apparent diatom reversal to an
oligothermic-type flora, and the decline in diatom concentration is more a
long-term change associated with reduced sedimentation rate.
The middle Holocene (ca. 8200–2600 cal yr BP)
The middle Holocene (Zone D-4; ca. 8200–2600 cal yr BP) was a phase of maximum
Holocene water temperature and lake productivity, as indicated strongly by
high calcite and organic matter content, high HI and low OI (Vogel et al.,
2010; Wagner et al., 2010; Lacey et al., 2015). This is in accordance with the
globally stacked proxy mean annual surface temperature record (Marcott et
al., 2013). However, the diatom response is complex. Anomalously, C. ocellata is at low
abundance, with reduced diatom PCA Axis 1 scores. As in Subzone D-2b, this
may be attributed to epilimnetic nutrient limitation, but to the extent that
C. minuscula is also constrained. Mixing-induced upward nutrient supply is probably low,
as a result of strong thermal stratification and probably weak winds
associated with high temperature. Erosion-induced external nutrient input is
also probably low, as indicated by a low sedimentation rate and K intensity
(i.e. clastic content). Low catchment erosion is also supported by dense
vegetation and stable soils in the catchment (Fig. 5; Wagner et al., 2009)
and by a drying trend and reducing water inflow from rising calcite δ18O values (Leng et al., 2010; Lacey et al., 2015). The effect of high
phosphorus precipitation linked to the calcite-scavenging effect (Allen and
Ocevski, 1976), and exacerbated by a low internal and external nutrient supply, could be sufficient to limit the development of C. ocellata during the middle Holocene in spite of high water temperature. The only predictable aspect of
the diatom data is the relatively high abundance of mesotrophic S. transylvanicus, which may
benefit from high water-temperature-induced productivity in the hypolimnion
and/or high nutrient availability in the hypolimnion under strong
stratification. The flora is similar to that of the middle Holocene in core
Lz1120 (Fig. 5; Wagner et al., 2009) and in the DEEP site (Cvetkoska et al.,
2015). Compared to Zone D-1, although C. fottii is similarly at high abundance, the
abundance of large C. fottii forms is much lower (Fig. 3) and fewer cells can
complete their full life cycle with sexual reproduction (Stoermer et al.,
1989), possibly linked to strong stratification during this period. Since
high calcite and organic matter content indicates high algal production, the
discrepancy between low abundance of epilimnetic diatom taxa and high algal
production suggests that Chlorophyceae, the other dominant algae in this
lake (Stanković, 1960; Miho and Lange-Bertalot, 2003), may outcompete
diatoms in the epilimnion and contribute more to algal production. Diatom
concentration is relatively high, in an interval with low rather than high
abundance of smaller valves of C. ocellata and C. minuscula, but this may be largely an artefact of
the consistently low sedimentation rate. As in other Lake Ohrid sediment
cores (Wagner et al., 2009; Vogel et al., 2010), there is no evidence for an
abrupt event at ca. 4200 cal yr BP. Overall, in contrast to Zone D-1, low
abundance of epilimnetic diatom taxa here is the response to high rather
than low water temperature; in contrast to Zones D-2 and D-3, the diatom
response here is to limited epilimnetic nutrient availability rather than
high water-temperature-induced productivity.
The late Holocene (ca. 2600 cal yr BP–present)
Between ca. 2600–2000 cal yr BP (Zone D-5), high C. ocellata abundance, along with
high diatom PCA Axis 1 scores, is consistent with that of core Lz1120 (Fig. 5; Wagner et al., 2009). There is surprisingly little change in other
limnological proxies during this phase, but high C. ocellata abundance correlates with
palynological evidence for anthropogenic catchment deforestation in core
Lz1120 (Fig. 5; Wagner et al., 2009). Relatively high diatom concentration
probably represents a response to epilimnetic productivity increase, caused
at least in part by human activity such as forest clearance and agricultural
development. At ca. 2000 or 1900 cal yr BP, the abrupt peak in C. minuscula abundance is
coeval with peak sedimentation rate and K intensity, abrupt reductions in
calcite, organic matter and HI, and a peak in OI. The peak is consistent
with previous interpretations, suggesting that it is related to
intensified human activity in the catchment during the Roman Period and
that enhanced erosion causes increased delivery of nutrients, clastic
material and organic matter that is extensively oxidised (Wagner et al.,
2009; Vogel et al., 2010; Lacey et al., 2015). It is a complex diatom
response to high nutrient availability, however. While very small
Cyclotella sensu lato species have low nutrient preferences, they may respond to nitrogen
enrichment when the N / P supply ratio is low (Saros and Anderson, 2015). There is
no abiotic mechanism for the removal of nitrogen from the epilimnion, and
phosphorus precipitation linked to the calcite-scavenging effect is low at
this time (Allen and Ocevski, 1976).
After ca. 1900 cal yr BP (Zone D-6), Lake Ohrid essentially reached its
modern state with a high abundance of epilimnetic taxa, dominated by smaller
valves of C. ocellata and C. minuscula, which is consistent with the flora of the late Holocene in
the DEEP site (Cvetkoska et al., 2015). As suggested in the previous zones,
the autecology of C. ocellata and C. minuscula is probably divergent in relation to nutrient
availability and mixing depth, which is supported by other observational and
experimental studies (e.g. Saros et al., 2012); on the other hand, C. ocellata is
relatively small and may also show synchronous change with very small
Cyclotella sensu lato species (e.g. Rühland et al., 2008). Moreover, high nitrogen
concentration may favour both C. ocellata and C. minuscula (Kocev et al., 2010; Saros and Anderson,
2015). Thus, it is not surprising that C. ocellata and C. minuscula concur to respond to enhanced
anthropogenic nutrient input during this period. There is strong
palynological evidence for catchment deforestation after ca. 1900 cal yr BP
from core Lz1120 and Lake Prespa core Co1215 (Wagner et al., 2009;
Panagiotopoulos et al., 2013). There is no definitive evidence for a diatom
response to known late-Holocene climatic events such as the Medieval Climate
Anomaly (MCA) or the Little Ice Age (LIA). If a strong MCA did occur,
anthropogenic nutrient input to the modern lake was sufficient to override
temperature-induced nutrient limitation in the epilimnion. With external nutrient input maintained at the same level, the implications for future climate warming are
that loss of epilimnetic diversity would not occur. Instead, the main threat
to Lake Ohrid is probably eutrophication, resulting in the invasion of
non-native taxa (Levkov and Williams, 2012).