Early postglacial recolonisation,refugial dynamics and the origin of a major biodiversity hotspot. A case study from the Malá Fatra mountains,Western Carpathians,Slovakia

Abstract

While general trends in Central European postglacial recolonisation dynamics are relatively well known, we often lack studies on intermediate (meta-population, landscape) scales. Such studies are needed to increase our understanding of, for example, the location of refugia; emergence of endemism, rates and trajectories of postglacial migrations; and anthropogenic landscape changes. Here, we focused on the outer Western Carpathian mountain chain Malá Fatra, which is currently characterised by high biodiversity and endemism and is thus considered a likely refugium of the Last Glacial period for the temperate biota of Eastern–Central Europe. We used molluscs and vascular plants as reference taxonomic groups and supported palaeoenvironmental interpretations of their (sub)fossil assemblages using high-resolution geochemical data. Generally, postglacial biotic successions from the study region fit the standard developmental pattern well in Middle and Eastern European uplands. Nevertheless, we found important biogeographically based peculiarities. In total, more than 50 species per (sub)fossil community at the reference site Valča, including 30 woodland species and 11 Carpathian endemites, make site of the highest known Holocene mollusc species diversity in Europe. Our palaeoecological analysis of this long-term biodiversity hotspot suggests that the Western Carpathians were likely an important source of the postglacial recolonisation of Central Europe by forest biota and, at the same time, an area of refugium-based endemism.

Keywords

climatic changes forest history Gastropoda Holocene late Glacial palaeofaunistics plant macrofossils pollen analysis stable isotopes

Introduction

The late Glacial period and the following first few millennia of the Holocene witnessed major climatic changes on a global scale, which have been connected to general trends in biotic development in periglacial Central Europe. These regional trends are relatively well known (e.g. Finsinger et al., 2017; Firbas, 1949, 1952; Giesecke et al., 2011; Ložek, 1964; and many others), at least in comparison with the rest of the world. In particular, mollusc successions have probably been best documented in the Czech and Slovak Republics (e.g. Horáčková et al., 2015; Juřičková et al., 2014b; Ložek, 1964, 1982), though some other Central European countries have also been relatively well studied (e.g. Alexandrowicz, 1987; Frank, 2006; Fuhrmann, 1973; Füköh, 1993; Füköh et al., 1995; Mania, 1972, 1973; Meyrick, 2001; Sümegi, 2005).

However, biotic reactions to climatic changes can differ locally and may show marked deviations from general trends. For instance, Ložek (1982) described this phenomenon based on mollusc successions of 15 Central and Eastern European landscape types. More recently, Abraham et al. (2016) and Jamrichová et al. (2017) confirmed striking local differences in vegetation development trajectories based on analyses of a large number of pollen successions from the same area (i.e. currently Czechia and Slovakia). Based on these studies, it seems plausible that the general trend of postglacial development consists of interacting patterns of many specific and partly independent local histories shaped by different geographical settings connected to glacial refugia and postglacial migration routes.

Molluscs as a tool for uncovering local biogeographic histories

We believe that the time is now ripe for puzzling out some of these local histories, with the aim to elucidate the processes behind the emergence of general biogeographic patterns. Mollusc (sub)fossil assemblages currently seem to be the best proxy for this task. Mollusc shells can be identified to species level, whereas the most commonly used palaeoecological proxy, pollen, is only partly identifiable into the comparably exact taxonomic level. Importantly, shells are usually deposited where the animal actually lived, unlike pollen or vertebrate bones (e.g. Davies, 2008; Evans, 1972; Ložek, 1964, 2000; Sümegi, 2005).

Just as biogeography or ecology cannot exist without precise faunistic and floristic knowledge, palaeofaunistic and palaeofloristic analyses are fundamental not only for palaeontology but also for understanding the shaping of recent ecosystems. While palaeofloristic approaches have dealt with data covering a majority of Europe (e.g. Brewer et al., 2016), mollusc palaeofaunistics have just emerged during the past two decades with studies of more than one succession per particular landscape domain (Gedda, 2001; Girod, 2011; Juřičková et al., 2013a, 2013b, 2014c; Limondin-Lozouet et al., 2013; Limondin-Lozouet and Preece, 2004; Meyrick, 2001). Studies in Central Europe have repeatedly confirmed Ložek’s (1982) division of the Holocene landscape development into (1) a zonal part with fully developed woodland faunas (Juřičková et al., 2014b), (2) an alpine area (Juřičková et al., 2014c) with reduced forest faunas and late-Holocene human impact and (3) a chernozem lowland zone where woodlands and their faunas were never fully established during the Holocene due to middle-Holocene (Neolithic) anthropogenic influences and their late-Holocene acceleration (Juřičková et al., 2013a, 2013b; Pokorný et al., 2015). However, there are still substantial differences between individual chernozem lowlands heavily impacted by prehistoric agriculture (Juřičková et al., 2013a, 2013b; Pokorný et al., 2015) and little-impacted lowlands (Břízová and Juřičková, 2011), where by contrast fully developed woodlands occurred. In Western Europe, that is, the edge of the continent with oceanic climatic influences, other conditions were established (Gedda, 2001; Limondin-Lozouet and Preece, 2004; Meyrick, 2001), and only few canopy forest species occurred during the Holocene climatic optimum (Holocene thermal maximum sensu; Renssen et al., 2009). In the Mediterranean, progressive desiccation was a driving factor of Holocene successions (Girod, 2011; Limondin-Lozouet et al., 2013).

In addition to describing local biotic and landscape developments, palaeofaunistics and palaeofloristics may contribute to testing hypotheses of general significance. Even in times of increasingly sophisticated phylogeographic reconstructions, the location of glacial refugia, postglacial recolonisation processes and evaluations of landscape changes caused by various forms of human impact cannot be studied without precise (sub)fossil data. For example, while the presence of Central European glacial refugia for temperate species has been frequently discussed (and both accepted and refused) during last two decades (for the Western Carpathians, e.g. Jamrichová et al., 2014, 2017; Jankovská and Pokorný, 2008; Juřičková et al., 2014a; Ložek, 2006; Tzedakis et al., 2013), their location remains unclear, because they likely formed small patches in the landscape matrix (and have thus been termed cryptic refugia). Even if we find some such refugia, the question remains how large they were, how fast temperate organisms spread from them (if at all) and to what extent they contributed to colonisation on the (sub)continental scale. Without a doubt, these questions are essential for predicting the impact of biotic changes under currently ongoing climatic changes. Mollusc palaeofaunistics can, therefore, provide new independent data for this debate.

The study area

We used a Quaternary mollusc database of Central Europe (Horáčková et al., 2015) to select a landscape of important biogeographical situation and simultaneously covered by a sufficient network of sampled Holocene mollusc successions. Our previous palaeofaunistic studies focused on an azonal chernozem area (Břízová and Juřičková, 2011; Juřičková et al., 2013a; Pokorný et al., 2015) as well as an azonal mountain area of the Bohemian Massive (Juřičková et al., 2014c). This study aims to extend this approach to the key area of the Western Carpathian mountains where the presence of Last Glacial Maximum (LGM) refugia of temperate species has repeatedly been hypothesised (Jamrichová et al., 2014, 2017; Juřičková et al., 2014a; Willis and Van Andel, 2004).

Such a view is strongly supported by current biogeographic research: At present, the Western Carpathians are an important interface between biogeographically contrasting regions of Europe, and the area harbours highly diverse biota that reflects both climatic and edaphic variability. These characteristics have been demonstrated to have played a major role in the Quaternary survival of contrasting biotic elements (Jamrichová et al., 2017; Mráz and Ronikier, 2016). As the result, the area is currently a biodiversity hotspot of continental significance and displays a high degree of endemism. Among vascular plants, the Western Carpathians are the richest in endemic taxa with the narrowest distribution ranges (Kliment et al., 2016). High endemism is also known for many animal groups (e.g. Bálint et al., 2011; Barkasi, 2016). The highest Central European snail endemism has been found in the Alps as well as Carpathians with the Western Carpathians being the northernmost situated area of endemism (Welter-Schultes, 2012). The survival of some endemic snail species during the LGM in the Western Carpathians has already been documented by Ložek (2006) and Juřičková et al. (2014a). However, endemic species are only rarely encountered in fossil records, so we have hardly any information about fluctuation of their ranges.

While studying of species range dynamics in mountain areas, it is always important to study timberline fluctuations, whose dynamics markedly differ between Central European Hercynian mountains (Treml et al., 2006) and the Southern Carpathians (Feurdean et al., 2016). These fluctuations could have especially affected the survival of alpine zone species during the Holocene climatic optimum.

For this study, we selected one of the mountain ranges of the Western Carpathians – the Malá Fatra mountains – a relatively temperate area with an especially high degree of endemism, indicating a potential for the presence of a temperate species glacial refugium. From 24 Western Carpathian endemic snail species, 19 currently live in the Malá Fatra (Welter-Schultes, 2012). Over the past several decades, we have been able to assemble a complex fossil record of this area, comprising multi-sited mollusc data, plus one complex reference record that provides, in addition to mollusc data, high-resolution vegetation (pollen and plant macrofossils) and geochemical (stable isotopes) proxies.

Material and methods

Site characteristics

The six sampled sites are situated in the southern part of the Malá Fatra mountains (Lúčanská Fatra) in north-western Slovakia (Figure 1). This mountain chain is built of a mosaic of granite and Mesozoic carbonaceous rocks (limestones and marlstones, respectively). At present, the mountain slopes and ridges are covered by beech forests with an herb-rich undergrowth (Eu–Fagenion) and some patches of calciphilous beech woods (Cephalantero–Fagenion). The vegetation cover is influenced by the proximity of the warm Upper Nitra and Turiec Basins, as documented, for example, by the common occurrence of the thermophilous shrub Clematis vitalba in altitudes well above 700 m a.s.l.

Figure 1.

Location of the study area in Central Europe and situation of studied successions in the Malá Fatra mountains (Slovakia). The large red circle shows the reference site Valča, while smaller black circles show the supporting sites.

The most complex, multi-proxy fossil record used in this study is from the Valča calcareous tufa deposit, and it was thus used as a reference site. This site is situated at the bottom of a deep mountain valley, Slovianska dolina, approximately 3.5 km west of the village Valča (N 49°00′3.8″; E 18°47′44.9″; 550 m a.s.l.). The valley sides at the profile consist of Lower Cretaceous and Jurassic marlstones and marly limestones forming the bedrock. Higher upstream, a resurgence with H₂S-rich water is located directly in the stream channel. The spring area of the Sloviansky brook is situated near the central mountain ridge, which rises here up to 1218 m. The depositional sequence developed in the tufa swamp at the valley bottom, which was repeatedly dammed by travertine terraces so that in certain phases, the sedimentation proceeded in shallow pools where very fine detritus of muddy character, rich in organic particles, was accumulated. Such sediments alternated with tufaceous horizons precipitated in running water or marshland vegetation, including a clastic admixture coming from the slopes built of marlstone bedrock. In light of the position of the site, the fossil assemblages may also include specimens transported from up to 3 km away, the length of the upper part of the Slovianska dolina valley. The malacofauna of tufas in Valča has been preliminary studied and published (Lisický, 1969; Šilar and Ložek, 1988). For the lithology of this reference profile, see Supplementary 1 (available online). The lower part of the profile (below layer 33B) has been excavated and analysed only recently. This tufa complex is rich not just in mollusc shells but also in plant macrofossils and pollen – a complex preservation that is rarely seen elsewhere. Pollen and plant macrofossil data were obtained just recently.

The Laskár tufaceous footslope accumulation is situated near the village Valentová on the eastern bank of the middle part of the Turiec river (N 48°57′43″; E 18°52′37″; 430 m a.s.l.). Alluvium of this small river is situated in the open agricultural landscape recently. All layers contain tufa or tufa admixtures together with malacofauna in all layers, along with vegetation remains in certain layers. The lowest part of the profile contains limnic sediments, a fen complex of strata with tufaceous admixture is above (see Supplementary 2, available online). Preliminary information about this site has been published before but lacking detailed processing and radiocarbon dating (Ložek, 1997). The accumulation basin of this deposit is relatively high, and fossil assemblages may include species of flood debris transported from the approximately 3-km² area of the Turiec basin.

The Kozol site is a pit on the south footslope of the Kozol hill (1119 m a.s.l.) situated in the Medzihorská dolina valley (N 49°06′37″; 18°45′10″; 690 m a.s.l.) near the village Rajec. The vast gravel pit expose footslope sediments from which eastern part of the pit was sampled (see Supplementary 2, available online). The area is covered by deciduous forest recently. The mollusc succession was previously published in a regional collection (Ložek, 1986). Shells could have been transported from only a small area of approximately 150 m².

The Repeš site lies near the village Kl’ačno (N 48°56′15″; E18°41′50″; 600 m a.s.l.). This tufa accumulation (see Supplementary 2, available online) is situated in the south-oriented alluvium of a small brook. The area is covered by deciduous forest recently. Shells may have been transported from an approximately 0.5-km-long section of the Tmavá dolina valley. The Vyšehradné site is situated in the Hadvická dolina valley near the village Nitrianské Pravno (N 48°53′44″; E18°41′18″; 470 m a.s.l.). This thick tufa accumulation (see Supplementary 2, available online) is situated in the south-oriented alluvium of a small brook, and shells may have been transported from an approximately 0.5-km-long section of the Hadvická dolina valley. The area is covered by cultural forests and agricultural landscape recently. Both deposits were sampled in 1961, mentioned in Ložek (1982), but the resulting material has been studied only recently.

The last site lies on the rocky top of the Fačkovský Kľak peak (N 48°58′55″; E18°38’25”; 1300 m a.s.l.). The top of the hill is covered by oak shrubs and meadows recently, the profile is situated under the rocky calcareous cliff. Profile was sampled, processed and published in a local journal (Ložek, 1962; for lithology, see Supplementary 2, available online). Unfortunately, this old material was not preserved for later radiocarbon dating. Thus, the malacospectra from this exposed profile are just summarised here in order to complete the information from the area. For the lithology of all supporting profiles, see Supplementary 2 (available online).

Sampling and analyses of fossil molluscs

All mollusc successions were sampled by standard methods (Ložek, 1964) – 8 dm³ of space–discrete samples of the sediment were taken from the central part of each macroscopically distinguishable layer, marked in Supplementary 1 (available online), within 80-cm-wide excavation pits (Repeš and Fačkovský Kľak) or from naturally eroded exposures, which were only cleaned. Mollusc shells were extracted from the sediments by a combination of floating and sieving. After careful drying, each sample was disaggregated in water and then, if necessary, in hydrogen peroxide. Floating snails were repeatedly decanted into a 0.5-mm sieve and dried under laboratory conditions. Afterwards, the sediment was dried and sorted by sieving. Shells were systematically removed from the sediment and examined under a dissecting binocular microscope. Ecological groups were used sensu Juřičková et al. (2014b); the nomenclature follows Horsák et al. (2013). Mollusc diagrams (Figure 2) show the relative proportions of the total number of species belonging to particular ecological groups (MSS malacospectra) in separated layers. We use the relative proportion of species because of the evident local overrepresentation of the spring prosobranch Bythinella austriaca.

Figure 2.

Comparison of MSS of all six mollusc successions of the Malá Fatra mountains. Ecological groups sensu Juřičková et al. (2014b). On the left side of spectra are radiocarbon data of particular layers (cal. yr BP; see Table 1). Chronozones sensu (Jäger, 1969) are marked in grey.

Pollen and plant macrofossil analyses

Besides the palaeomalacological analyses, the reference site Valča was sampled and analysed for (sub)fossil plant remains. Plant macrofossils were extracted directly from already processed mollusc samples (see the processing method above). For pollen analysis, the profile was newly sampled in the field in intervals ranging from 10 to 40 cm. A standard acetolysis method (Erdtman, 1960) in combination with 10% HCl treatment was used for preparation of pollen slides. Pollen grains were stained using 0.1% safranin for better identification. During analysis, the minimum terrestrial taxa pollen sum of 500 grains (usually 700, maximum 800) was reached. Pollen nomenclature follows the standards of the Czech Quaternary Palynological Database (PALYCZ; Kuneš et al., 2009; available online at http://botany.natur.cuni.cz/palycz/).

Radiocarbon dating

Radiocarbon analyses were performed in the Poznań Radiocarbon Laboratory, Poland; Izoptech Zrt., Debrecen, Hungary; and the Center for Applied Isotope Studies of the University of Georgia, USA. Mollusc shells were measured by the accelerator mass spectrometry (AMS) method and calibrated for variable initial ¹⁴C concentration using the OxCal v4.3 calibration programme (Bronk Ramsey, 2009; see Table 1). Because shells can potentially contain dead carbon, which can lead to an over-estimation of their age (Goodfriend and Stipp, 1983), we used an amalgam of small species shells for radiocarbon dating, because 78% of these do not contain any dead carbon (Pigati et al., 2010). The lithology was used as another proxy to control for the undisturbed development of particular sites. In the reference site Valča, terrestrial plant macrofossils were also used for radiocarbon dating in the Poznań Radiocarbon Laboratory, Poland. Results from these confirmed the validity and precision of radiocarbon measurements from mollusc shell samples.

Table 1.

Results of AMS radiocarbon age determination. Calibration was performed in the OxCal programme version 4.3 (Bronk Ramsey, 2009).

Sample name and layer	Material dated	Measured radiocarbon age	Age (cal. BP; 95.4% int.)	Laboratory code
Laskár 3	Plicuteria lubomirskii shell	3019 ± 31BP	3211	DeA-10021
Laskár 6	Plicuteria lubomirskii shell	4282 ± 33BP	4850	DeA-10022
Laskár 8	shell amalgam	6800 ± 30BP	7636	UGAMS 7671
Laskár 10	Oxyloma elegans shell	8349 ± 40BP	9374	DeA-10023
Laskár 12	Oxyloma elegans shell	8362 ± 36BP	9386	DeA-10024
Laskár 15	Monachoides incarnatus shell	9481 ± 46BP	10828	DeA-10025
Laskár 18	Monachoides incarnatus shell	12400 ± 30BP	14468	UGAMS 7672
Repeš 3	Shell amalgam	3480 ± 30BP	3743	UGAMS 9658
Repeš 9	Shell amalgam	4850 ± 25BP	5567	UGAMS 9659
Valča 3 (190–200 cm)	Shell amalgam	4730 ± 25 BP	5456	UGAMS 9650
Valča 10 (475–485 cm)	Shell amalgam	5800 ± 25 BP	6589	UGAMS 9651
Valča 18 (685-695 cm)	Plant remain (Picea abies needles)	5985 ± 35 BP	6834	Poz-56441
Valča 25 (875–885 cm)	Plant remain (Picea abies needles)	7215 ± 35 BP	8060	Poz-56440
Valča 30 (1085–1095 cm)	Plant remain (Picea abies needles, Tilia fruit, Corylus avellana nutshell)	7950 ± 40 BP	8816	Poz-56439
Valča 33B (1295–1305 cm)	Plant remain (Picea abies needles, Sambucus nigra seeds, Alnus glutinosa fruits)	8170 ± 40 BP	9120	Poz-56438
Valča 37 (1425–1435 cm)	Plant remain (Corylus avellana nutshells)	8300 ± 60 BP	9298	Poz-63251
Vyšehradné 5	Shell amalgam	2145 ± 30BP	2156	Poz-77698
Vyšehradné 10B	Shell amalgam	3580 ± 30BP	3878	UGAMS29906
Vyšehradné 13	Shell amalgam	3780 ± 40BP	4142	UGAMS29907

Geochemical and stable isotope analyses from the Valča site

Samples for x-ray fluorescence (XRF) and stable isotope analyses were taken in 5-cm intervals from the cleaned wall. XRF measurements were performed on approximately 30 g of bulk sediment using a NITON XL3t 950 GOLDD + (Thermo Scientific) spectrometer with a 50-kV Ag tube and large-area SD detector. We included data on the elemental concentrations of strontium (Sr) and calcium (Ca). A total of 5–8 g of dried bulk sediment was leached in 30% hydroxide peroxide to remove any organic carbon in the sample. Stable carbon and oxygen isotope compositions of carbonate samples were determined using isotope relative mass spectrometry (IRMS). Finely powdered (milled) samples (200–300 µg) were decomposed with anhydrous phosphoric acid (~100 µL) in tightly sealed 12-mL vials made from borosilicate glass, using helium for the atmosphere inside the vials. Evolved carbon dioxide was transferred through a gas sampling system (GasBench II; Thermo Finnigan, Bremen, Germany) into a continuous flow stable isotope ratio mass spectrometer (Deltaplus XL; Thermo Finnigan) for analysis. Isotope compositions of the samples were initially compared with the known composition of a working standard (carbon dioxide). Final results were then expressed with respect to the International Atomic Energy Agency (IAEA) standard Vienna Pee Dee Belemnite (VPDB; IAEA, Vienna, Austria). Relative isotope abundances δ (δ¹³C for carbon and δ¹⁸O for oxygen) were calculated according to the formula δ = (R_sample/R_standard − 1)1000 (‰), where R stands for the ratios of isotope amounts ¹³C/¹²C or ¹⁸O/¹⁶O. Standard deviations of both the isotope abundances δ¹³C and δ¹⁸O, determined using a laboratory standard barium carbonate, were mostly smaller than 0.2‰. We also included results on carbon isotope composition (δ¹³) of n-alkanes of the spruce Picea abies, which is usually used as a proxy indicator of local variability in water availability. The n-alkanes in pine waxes were analysed following the method of Eley et al. (2012, 2014).

Results

Mollusc successions of six profiles in the Malá Fatra were studied (Figure 2, Supplementary materials 3, 4, 5, and 6, available online). Two of them, Valča and Laskár, contained malacofauna of time spans from the late Glacial to the Epiatlantic and the Pre-Boreal to the Sub-Boreal (sensu Jäger, 1969). The remaining four profiles contained only middle- to late-Holocene snail assemblages. Other proxies (pollen, plant macrofossils, oxygen and carbon stable isotopes) were available only for the Valča reference site (Figures 3 and 4, Supplementary materials 7, 8, and 9, available online).

Figure 3.

Pollen diagram of Valča (Slovakia).

Figure 4.

Graphs of δ¹⁸O (proxy for temperature), δ¹³C, Sr/Ca (proxy for precipitation amount) and variation of arboreal pollen at the Valča site plotted by age (ka) and compared with the δ¹⁸O record from North Greenland Ice Core Project (NGRIP Members, 2004).

Valča – Reference site of the Malá Fatra

Malacofauna

The mollusc succession of the Valča site can be divided in two main biostratigraphic zones (Figure 2, Supplementary materials 3, 4, 5, and 6, available online). The underlying complex of strata (layers 38–26; 1485–925 cm depth) was dominated by indifferent species (ecogroup C: 7–8) and wetland species (ecogroup D: 9–10) with an admixture of some more tolerant woodland species in very low numbers. Of particular importance is the high abundance of Discus ruderatus (9100 cal. yr BP) as well as of the demanding terrestrial prosobranch Platyla polita (ca. 9300 cal. yr BP) in association with Aegopinella pura and Clausilia pumila, which may indicate a favourable woodland environment already in this early-Holocene (Pre-Boreal) period. This interpretation is also supported by the higher abundances of the hygrophilous species Carychium tridentatum and Vitrea crystallina, which occur in humid woodland leaf litter. However, it is difficult to determine whether these scattered records indicate a minor climatic oscillation or temporary change in the sedimentary environment. In contrast, the whole upper group of strata (layers 22–1; 925–0 cm depth) was characterised by a dramatic increase in species richness, predominantly due to the expansion of woodland species (ecogroups 1–3) and partially by inhabitants of canopy forest (ecogroup 1). Their arrival began, however, already 8100 cal. yr BP (layer 25), with dispersed occurrences of several woodland elements in low abundances. The early occurrences of Cochlodina orthostoma, Isognomostoma isognomostomos and Petasina unidentata (layer 26) indicate a canopy forest still during the late-Holocene. There was a dramatic boom of silvicolous (canopy forest) species in the middle-Holocene (Atlantic period), where from almost one layer to the next, the number of these species doubled (11 woodland species in layer 23 vs 34 ones in layer 21) and their abundances multiplied (33 woodland specimens in layer 23 vs 1407 ones in layer 21). Of particular interest is the late (late Atlantic; Epiatlantic) occurrence of the dead wood dwelling Carpathian endemic species Argna bielzi on the westernmost border of its range. The appearance of Discus perspectivus indicates warming during the second half of the Atlantic period (6800 cal. yr BP). Wetland species (ecogroup 9) disappeared during the late Atlantic (Epiatlantic) period (5450 cal. yr BP) and on the contrary the steppe species Chondrula tridens emerged. Subsequently, the rapid sedimentation and formation of tufa ended.

Pollen and plant macrofossil records

The state of pollen preservation enabled successful pollen analyses from the lowest sedimentary layer (1470 cm) to the level of 390 cm. The pollen diagram (Figure 3) shows a fully developed temperate broadleaf forest already for the oldest recorded period, between ca. 9300 and 9000 cal. yr BP (from the bottom-up to the 1200 cm depth), dominated by hazel (Corylus avellana). Despite the elevated position of the area (the sampling site is located at 550 m a.s.l., while surrounding slopes reach much higher altitudes up to 1000 m a.s.l.), this forest already had a thermophilous character in this early period, as indicated by the regular occurrence of Hedera helix and Viscum pollen grains. Towards the end of this period, hazel progressively declined and Norwegian spruce (Picea abies) expanded.

In the oldest phases of the record, pollen grains of beech (Fagus) already occurred in low quantities. Such an early occurrence could either be the result of early immigration from LGM refugia located in the south, or the result of LGM refugia in the proximity, as proposed for the area of the Western Carpathians by Magri et al. (2006).

At the level of 1090 cm (radiocarbon-dated to 8800 cal. yr BP), maple (Acer) expanded and became another important element of regional forests (note that maple is a relatively very low pollen producer; Broström et al., 2008). Shortly after, other broadleaf thermophilous tree taxa (mainly Ulmus and Quercus) reached their absolute maxima. The very high pollen percentages of spruce (Picea) and alder (Alnus glutinosa-type) can be attributed to local overrepresentation caused by their presence in the wetland or around its edges. This interpretation was verified by the results of the plant macrofossil analysis (Supplementary materials 7 and 8, available online) that shows abundant findings of these two taxa. Shortly after 8000 cal. yr BP, the abundance of silver fir (Abies alba) started to increase.

The pollen record ended at 390 cm, a period roughly dated to 6500 cal. yr BP. Above this level, heavy corrosion of the pollen grains occurred, and poor preservation makes the pollen record of younger periods unreliable.

The upland plant taxa macrofossil record (Supplementary 7, available online) shows the common occurrence of temperate forest taxa – either trees or herbs of forest undergrowth – for the entire profile, further supporting the above interpretation of the pollen analyses, indicating the prevalence and continuity of the forested environment since the very start of the record (9300 cal. yr BP) to its end in the late Atlantic (Epiatlantic) period.

Palaeoclimatic interpretations of the stable isotope record

Since the variability of δ¹⁸O in calcareous tufa is driven mainly by changes in water body temperature during tufa precipitation, the δ¹⁸O value measured in this sediment can be used as a proxy for palaeotemperatures (Andrews, 2006). Tufa calcite δ¹³C reflects the relative sources of carbon that contribute to the dissolved inorganic carbon of groundwater – low δ¹³C derived from soil organic matter and higher δ¹³C carbon derived from the dissolution of the aquifer limestone (Andrews et al., 1993).

For a palaeoclimatic interpretation of the δ¹³C record, we used the following syllogism: if degassing in aquifer air pockets is enhanced during decreased recharge when groundwater levels are low, variation in δ¹³C may represent an index of recharge and, therefore, precipitation intensity (Andrews and Brasier, 2005). Decreased recharge (dry conditions) increases aquifer water residence time, allowing longer contact and the dissolution of aquifer limestone increasing δ¹³C and vice versa. As demonstrated by a number of previous studies, variation in the Sr/Ca ratio in tufa deposits is mostly controlled by the same mechanism – a higher Sr/Ca ratio has been found in calcite precipitated in an aquifer (during stagnation of groundwater circulation, i.e. dry conditions) in comparison with calcite precipitated out of the aquifer (Garnett et al., 2004; Ihlenfeld et al., 2003). A strong positive correlation detected between δ¹³C and the Sr/Ca ratio (r² = 0.7) supports the idea that δ¹³C variation in the studied profile represents a proxy for past precipitation amounts.

The Sr/Ca and δ¹³C records (Figure 4) showed a general trend towards decreasing values from the base of the deposit, suggesting decreased aquifer water residence time because of wetter conditions. Several episodes of apparently dry stable conditions (increased δ¹³C and Sr/Ca values due to increased aquifer water residence time) were found within the time intervals ca. 8900–8700, 8350–8500, 8000–7650, 7000–6650 and 6400–5800 cal. yr BP. The most significant increase in humidity occurred after ca. 7650 cal. yr BP. These changes are consistent with an increasing canopy of woodland vegetation, as was indicated by the pollen and plant macrofossil data (Figure 3, Supplementary materials 7 and 8, available online) and from the distinct increase of number in the number of forest mollusc species (Figure 2, Supplementary materials 3, 4, 5, and 6, available online). However, woodlands provided leaf litter and allowed the development of humus, increasing root respiration and microbial organic decay, which in turn increased the generation of isotopically light soil carbon.

Results on the compound-specific isotope analysis of δ¹³C from Picea abies sub-fossil needles were used as a proxy indicator of the local variability in water availability. Contrary to the above-described regional variations in the precipitation amount, the local variability in wetness showed quite stable conditions during the whole study period (see Supplementary 5, available online). This suggests that continuous wetland conditions dominated at the study sites with no significantly drier episodes and that consequently spruce benefited from the local hydrological conditions, independent of regional climatic changes.

The δ¹⁸O record showed a continuous increasing trend from the base of the profile, suggesting progressive warming from the start of the Holocene. This trend was interrupted by several short-term cool oscillations, of which the most significant occurred between ca. 8200 and 8000 cal. yr BP. This oscillation can be correlated with the 8.2 kyr event, although in the Northern Hemisphere, this period is broadly associated with significantly dry conditions (Alley and Ágústsdóttir, 2005), whereas at our site, a rather wetter environment prevailed (indicated by increased δ¹³C and Sr/Ca during this time period).

Supporting records

The succession at Laskár (Figure 2, Supplementary 3, available online) extended to the late Glacial, when aquatic and wetland malacofauna predominated (Valvata piscinalis, Gyraulus crista, Bathyomphalus contortus, Perforatella bidentata, Vertigo antivertigo, Vertigo geyeri, etc.), but a few forest (Faustina faustina, Fruticicola fruticum and Clausilia pumila), while open-country species (Vallonia costata and Vallonia pulchella) indicated a transitional mosaic landscape character. During the Pre-Boreal period, the data infer the presence of parkland with wetland, ephemeral water bodies (Anisus leucostoma and Galba truncatula) and open country with scattered forest (Discus ruderatus and Monachoides incarnatus). A boom of silvicolous species was dated to the Atlantic period (7600 cal. yr BP), but there was also forest parkland with ephemeral water bodies and calcareous seepages. During the Epiatlantic (4850 cal. yr BP), steppe species (Chondrula tridens) and even the thermophilous East-European Caucasotachea vindobonensis appeared. From the Sub-Boreal period (3200 cal. yr BP onwards), the number of forest and wetland species rapidly declined and open steppe patches prevailed. The West Carpathian endemic species Plicuteria lubomirskii occurred very early in the lowlands (from layer 13 Laskár, see Supplementary 2, available online), but appeared only sub-recently in the mountains (Fačkovský Kľak hill).

Together with the mollusc succession of the Kozol profile, the lithology documents the development of slope sedimentation during the Holocene in this small mountain valley. While the oldest parts (layers 10–6) showed evidence of gravel sedimentation on the partly open hill slope with typical rock dwelling species (Pyramidula pusilla and Faustina cingulella), from layer 5 sedimentation ceased and then altered into a flow of coarse scree developing into a humid talus slope forest with a fully developed canopy forest fauna (Acicula parcelineata, Cochlodina orthostoma, Daudebardia rufa, Discus perspectivus, Isognomostoma isognomostomos, Ruthenica filograna, etc.). Some parts of the footslope may have even been waterlogged, as indicated by few Carychium tridentatum and especially Bythinella austriaca shells. Small open patches, indicated by few shells of Cochlicopa lubricella and Truncatellina cylindrica, may have been the consequence of natural desiccation or pastures.

Profiles of tufaceous sediments at Repeš and Vyšehradné are younger. In both profiles, the dominance of woodland species (ecogroup 1–3) indicated a humid forest during the middle- and late-Holocene at Repeš and only from the late-Holocene at Vyšehradné. Ephemeral wetlands and small springs, with a high abundance of the spring prosobranch Bythinella austriaca, occurred at both sites. A slowing of sedimentation and the end of tufa formation in both profiles, together with the appearance of steppe species (Pupilla muscorum in Repeš and Granaria frumentum in Vyšehradné) during the late-Holocene, may indicate the influence of pastoral farming penetrating into small mountain valleys, thanks to a drying out of the landscape.

Discussion

As recently demonstrated by Feurdean et al. (2014) and Jamrichová et al. (2014, 2017), the Inner Carpathian Basin, including its northern edge in the territory of the present Slovakia, was already occupied in the first millennia of the Holocene by well-developed temperate broadleaf forests. This is probably the result of the proximity of LGM refugia for temperate forest taxa (Jankovská and Pokorný, 2008; Juřičková et al., 2014a; Ložek, 2006; Willis and Van Andel, 2004), and this view is further supported by our study that shows the dominance of a forested environment at the Valča site since the very start of the record (9300 cal. yr BP). This finding also supports the hypothesis (Jamrichová et al., 2017; Willis and Van Andel, 2004) that the early establishment of temperate forests is likely a key factor for understanding the current biogeography of Eastern–Central Europe. This early occurrence of temperate trees is unlikely to be explained only by gradual postglacial migrations from Southern Europe. Humid but relatively warm mountains might hence have acted as glacial refugia of temperate forest species, while adjacent lowlands and leeward basins might have rather acted as postglacial refugia for steppe grasslands (as shown in recent study by Jamrichová et al., 2017). Unfortunately, the existence of LGM refugia for temperate forest taxa cannot be directly demonstrated by this study, due to the lack of a sufficiently old fossil record (i.e. going back to the LGM).

Postglacial mollusc succession and climatic development of the Malá Fatra

In general, the mollusc succession of the Malá Fatra corresponds to the standard pattern of development in mid-European upland areas (e.g. Juřičková et al., 2014b; Ložek, 1964) but with some biogeographically related peculiarities. The late Glacial (starting at 14,500 cal. yr BP) occurrence of some forest species (Clausilia pumila, Faustina faustina and Fruticicola fruticum; for detail, see Supplementary 3, available online) provides early evidence of scattered woodlands in the Malá Fatra and again the likelihood of nearby or local glacial refugia for these species. In the Pre-Boreal, other woodland species completed the mollusc assemblages. Species such as Acanthinula aculeata, Aegopinella pura, Columella edentula, Discus ruderatus, Platyla polita, Vertigo pusilla and Monachoides incarnatus indicate the occurrence of a canopy forest in lowlands and mountain valleys in this transitional period. Steppe and open-country patches were characteristic of lowlands in the Turiec Basin throughout the whole Holocene, likely owing to the impact of human settlements (Veliačik, 1989; Žaár, 2015). In mountain valleys, the rare records of open-country species may likely results shell transport from nearby higher situated exposed rocky habitats. Open patches in the Slovianska dolina valley (Valča site), which are directly associated with human impacts in the Turiec Basin, appeared only later (5450 cal. yr BP), as indicated by the steppe snail species Chondrula tridens (and supported by the occasional macrofossil find of cereal remains in the same period – charred chaff of Triticum monococcum; Supplementary 7, available online). The boom of silvicolous species was dated to 7600 cal. yr BP in the lowland (Laskár) and 7400 cal. yr BP in the mountain valley (Valča) and can be associated with the mid-Holocene humidity pulse, visible in many palaeoenvironmental records throughout Central Europe (see Roberts, 2014). At the Valča site, this supraregional trend is reflected in the distinct increase of δ¹⁸O values (proxy for temperature rise) accompanied by the decrease of δ¹³C values and the Sr/Ca ratio (a proxy for precipitation decrease) that occurred here after 8000 cal. yr BP (Figure 4). The predominantly forested environment and dominance of thermophilous broadleaf trees at Valča are also supported by the pollen and plant macrofossil analyses, as well as by the presence of the highest known canopy forest mollusc diversity in the entire European Holocene record, at least to our knowledge. The desiccation (as demonstrated locally by the geochemical data, see Figure 4) started immediately after the silvicolae boom in the lowland site but culminated there around 4850 cal. yr BP. While almost all profiles contain tufa sediments, desiccation resulted in a slowing rate of sedimentation and an end of tufa formation in the Sub-Boreal period. This desiccation is also apparent from the declines in large populations of the spring species Bythinella austriaca. During this period, the Malá Fatra consisted of a mosaic of woodland, open (mostly anthropogenic) and wetland habitats.

Holocene treeline shifts

The survival of a forest-free alpine belt in Central European mountains is the subject of current discussion, and the likelihood differs substantially for particular mountains (e.g. Treml et al., 2006). Sometime around the end of the late Atlantic (Epiatlantic) period, peaks of the Malá Fatra were probably completely covered by forest, as indicated by the fully developed woodland communities on the Fačkovský Kľak peak (1300 m a.s.l.; Ložek, 1962). Steppe and shrubby beech habitats occurred there recently, being approximately 100 m under the recent treeline in the Western Carpathians (approximately 1400 m a.s.l.; Kozak et al., 2007). Unfortunately, material from the Fačkovský Kľak profile was not preserved since its extraction, so radiocarbon dating of the highest altitude of the timberline is not possible. Nevertheless, the precise dating of the Holocene treeline shifts of this Carpathian area needs to be critically revised. Ložek (1981) attempted to resolve this problem using three successions in the nearby Kriváňská Fatra mountains but lacked radiocarbon dating. A succession in the profile from the Rozsutec peak (1500 m a.s.l.) in this area was considered to represent the whole Holocene (Ložek, 1978, 1981), but we have dated the base of this profile as being much younger (3700 cal. yr BP; unpublished data), so it cannot document treeline shifts during the critical period of the Holocene, that is, before grazing and other possible human influences started.

The zoogeographic border between the Bohemian Massive and the Western Carpathians

While the geological border between the Carpathians and the Bohemian Massive is quite clear, the westernmost borders of Carpathian species ranges and the easternmost borders of some Central European snail species ranges differ and shifted during the Holocene. Interestingly, while the Malá Fatra is not the westernmost mountain belt of the Carpathians, many West Carpathian endemics have their recent westernmost border there (Argna bielzi, Chondrina tatrica, Cochlodina cerata and Faustina cingulella – the last two also in the nearby Súľovské vrchy mountains). From 24 Western Carpathian endemic snail species, 19 currently live in the Malá Fatra (Welter-Schultes, 2012). In addition, the Malá Fatra represents the easternmost border of Cepaea hortensis. Together these species ranges provide evidence of the important zoogeographic position of this mountain belt for molluscs. However, some Central European species such as Alinda biplicata, Semilimax semilimax and Urticicola umbrosus that occur farther to the east are locally lacking in the Malá Fatra mollusc successions. This may help us evaluate the shifting of this border during postglacial successions. Of particular interest is the appearance of Balea perversa during the late Atlantic (Epiatlantic) in Vyšehradné, which is the second-known Holocene record of this species from Slovakia (according to Czech and Slovak Holocene mollusc database – unpublished data). A more recent occurrence of Balea perversa is not known from the Malá Fatra. The only known Holocene record of the Central–Western European species Helicodonta obvoluta in the Malá Fatra also comes from the Epiatlantic section of this profile, but this species has survived there to the present. One of the oldest records of the Western Carpathian endemic subterraneous species Alzoniella slovenica (6800 cal. yr BP) was obtained from the Valča section. Another Western Carpathian endemic species, Faustina rossmaessleri, is recently most abundant just in the Malá Fatra. This species has a documented LGM occurrence at the Farkašovo site approximately 70 km to the east (Juřičková et al., 2014a; Ložek, 2006), and thus, this part of the Western Carpathians seems to be its glacial refugium.

Conclusion

Hardly anyone doubts the role of the Western Carpathians as a glacial macro-refugium (Jamrichová et al., 2014, 2017; Mráz and Ronikier, 2016; Wielstra et al., 2015), being documented as the easternmost border of various studied species or genetic lineages being traced to the area of the Western Carpathians (Magri et al., 2006; Pinceel et al., 2005; Wielstra et al., 2015). In concordance with this evidence, and despite the pronounced early- to middle-Holocene climatic changes (in both temperature and precipitation), our data suggest that the Malá Fatra mountains could have been a glacial (LGM) refugium for several Western Carpathian endemic snail species. However, the precise location of these hypothetical LGM refugia remains a challenge. In any case, in this study, the Western Carpathians were demonstrated to have undergone substantial late Glacial and early-Holocene afforestation. Therefore, the area could have served as a significant stepping stone for the postglacial spread of closed-canopy temperate forest biota to the rest of Central Europe (at the least). The biological diversity within this type of biome has currently reached locally maximum values, clearly the result of long-term regional continuity of the forested environment.

Footnotes

Acknowledgements

We appreciate Nicole Limondin-Lozouet and an anonymous reviewer for their valuable comments on the previous version of the manuscript and David Hardekopf for the English revision. Petr Vorm is acknowledged for performing the XRF analysis.

Funding

This work was supported by the Czech Science Foundation (GAČR) grant 13-08169S and 17-05696S, and the HACIER project funded from the Norwegian Financial Mechanism 2009–2014, and the Ministry of Education, Youth and Sports under project contract no. MSMT-28477/2014. Access to instruments and other facilities was supported by the Czech research infrastructure for systems biology C4SYS (project no. LM2015055).

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