Quaternary Science Reviews 149 (2016) 269e278
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Quaternary Science Reviews
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Beginning of a new age: How did freshwater gastropods respond to the Quaternary climate change in Europe?
* Elisavet Georgopoulou a, b, , Thomas A. Neubauer a, Giovanni Strona c, Andreas Kroh a, Oleg Mandic a, Mathias Harzhauser a a Geological-Paleontological Department, Natural History Museum Vienna, Burgring 7, 1010 Vienna, Austria b Institute for Earth Sciences, University of Graz, Heinrichstraße 26, 8010 Graz, Austria c European Commission, Joint Research Centre, Institute for Environment and Sustainability, Forest Resources and Climate Unit, 21027 Ispra, Italy article info abstract
Article history: The well documented fossil record of European Quaternary freshwater gastropods offers a unique Received 19 October 2015 resource for continental-scale biogeographical analyses. Here, we assembled a dataset including 338 Received in revised form freshwater gastropod taxa from 1058 localities across Europe, which we used to explore how freshwater 14 July 2016 gastropod communities varied in space and time across six distinct time intervals of the Quaternary, i.e. Accepted 27 July 2016 Gelasian, Calabrian, Middle Pleistocene, Last Interglacial, Last Glacial and Holocene. We took into Available online 10 August 2016 consideration both species richness and qualitative structural patterns, comparing turnover rates be- tween time intervals and examining variations in community nestedness-segregation patterns. Species Keywords: fi Pleistocene richness differed signi cantly between time intervals. The Early Pleistocene showed the highest di- Holocene versity, likely because of the contribution of long-lived aquatic systems like the lakes Bresse and Tiberino Species richness that promoted speciation and endemism. The rich Middle to Late Pleistocene and Holocene assemblages Species turnover were mostly linked to fluvial and/or lacustrine systems with short temporal durations. We identified a Overlap-segregation major turnover event at the Plio-Pleistocene boundary, related to the demise of long-lived lakes and of Range-through approach their rich, endemic faunas at the end of the Pliocene. In the subsequent intervals, little or no turnover Geographical ranges was observed. We also observed a pattern of high segregation in Early Pleistocene communities, asso- ciated with the abundance of endemic species with small distribution ranges, and reflecting the pro- vincial character of the aquatic freshwater systems at that time. This structured pattern disintegrated gradually towards the Middle Pleistocene and remained unstructured up to present. In particular, spatial patterns of community nestedness-segregation in the Last Interglacial and Holocene suggest a random recolonization of freshwater habitats mostly by generalist species following deglaciation. © 2016 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
1. Introduction tectonic activity (e.g. Antonioli et al., 2009; Gabris and Nador, 2007; Stocchi et al., 2005; Zagwijn, 1989). Changes in species diversity The Quaternary Period (2.588e0 Ma; Gibbard et al., 2010), patterns during the Quaternary are usually affiliated with the which can be considered short in a geological perspective, is recurrent glaciations (e.g. Colwell and Rangel, 2010; Dynesius and characterised by successive glacial episodes and distinctly lower Jansson, 2000; Hewitt, 1999; Jansson and Dynesius, 2002), and temperatures compared to the preceding Neogene Period (Lisiecki particularly with the last Ice Age (e.g. Hewitt, 1999, 2000). Qua- and Raymo, 2005). During this time, Europe attained its present ternary ice house conditions affected different animal groups in shape, with extensive changes in shorelines and inland waters different ways as shown, for example, by European insect faunas, occurring mainly because of glacio-isostatic movements and which do not show high extinction rates during the Quaternary, but instead display shifts in their geographical ranges (Coope, 1994). Similarly, changes in species geographical ranges (which, in turn, affected local species richness and composition) have been recor- * Corresponding author. Geological-Paleontological Department, Natural History ded for the Late Pleistocene and Holocene land snail faunas of Museum Vienna, Burgring 7, 1010 Vienna, Austria. north-western Europe (Limondin-Lozouet and Preece, 2014). As E-mail addresses: [email protected], georgelisavet@yahoo. gr (E. Georgopoulou). shown by Neubauer et al. (2015b), the freshwater gastropods of http://dx.doi.org/10.1016/j.quascirev.2016.07.034 0277-3791/© 2016 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). 270 E. Georgopoulou et al. / Quaternary Science Reviews 149 (2016) 269e278
Europe experienced a major turnover at the Plio-Pleistocene divisions were chosen to fit the formal Quaternary subdivisions boundary, and a severe decline in their diversity. The main expla- proposed by Gibbard et al. (2010), hence facilitating comparability, nations of this event have been identified in deteriorating climate, and pinpointing the main glacial event of the Late Pleistocene (i.e. and in the disappearance of long-lived lakes (Neubauer et al., the Last Glacial). All localities extracted from the literature were 2015b). assigned to one of the six TIs based on their stratigraphic age, as While, the distribution of freshwater gastropods during the updated and attributed by Georgopoulou et al. (2015) (see Quaternary is reasonably documented at a regional scale (e.g. Supplementary Table 2). Localities with age ranges crossing a TI's Alexandrowicz, 1999; Esu and Girotti, 1975; Kennard and age boundary were excluded from the dataset except for those Woodward, 1917, 1922; Lo zek, 1964; Mania, 1973; Sanko, 2007; where 90% or more of the interval fell within one of the two TIs. Settepassi and Verdel, 1965), a detailed breakdown of trends in Localities with too coarse stratigraphic attributions (e.g. “Early freshwater gastropod biodiversity and biogeography is entirely Pleistocene” or “Late Glacial to Holocene”) were excluded from the missing on a larger scale. Beyond that, a limited number of studies analyses. deal with regional biogeographical patterns, time intervals or taxa, focusing mostly on the terrestrial gastropods (e.g. Limondin- 2.2. Species richness Lozouet and Preece, 2014; Meijer and Preece, 1996). In contrast, the biogeographical relationships of Neogene lacustrine gastropods We examined patterns of species richness across the six TIs. on a pan-European scale have recently been investigated Because of the incomplete fossil record and heterogeneity in (Harzhauser and Mandic, 2008; Neubauer et al., 2015a). These sampling effort, localities included in the dataset are unevenly works identified a trend towards increasing provincialism during distributed and geographically clustered (Fig. 1). Thus, in all TIs, the Neogene, resulting from the formation of large, long-lived lakes information on species distribution is well available in some areas, with highly endemic faunas. By the onset of the Pleistocene, while it is sparse or lacking in others. To cope with the potential however, nearly all of these major hotspots had vanished. confounding effect of this pattern, we created 100 100 km equal- A recent investigation of modern gastropod distribution in Eu- area grid cells in ArcGIS 10 (Esri Inc., 1999e2010) in Behrmann ropean lakes indicates that lacustrine snails still carry the imprint of projection. To ensure that species richness was not overestimated the last Ice Age (Georgopoulou et al., 2016). Here we aim at in areas represented in the dataset by numerous localities, for each unravelling the trends in diversity and spatial structure of the Eu- TI, we calculated the number of species within each grid cell ropean freshwater gastropod fauna throughout the Pleistocene and including at least one locality. Given that the selected grid size Holocene, i.e. the last 2.6 Ma, in order to provide the missing links reflects the explicit character of species distribution records and between the well-resolved patterns of Neogene and modern maintains their spatial accuracy, this procedure should ensure that freshwater gastropod biogeography. For this we compiled a sampling errors related to variation in area sizes are avoided (Kreft comprehensive dataset including available information on the oc- and Jetz, 2010). Average species richness in each TI was defined as currences of European Quaternary freshwater gastropods. We used the quotient of the total number of species divided by the number this dataset to explore how species richness and composition of grid cells with occurrence data. Differences in average species changed throughout six different time intervals, providing the first, richness between TIs were investigated using ANOVA with a detailed biogeographical study of Quaternary freshwater snails at a Dunnett-Tukey-Kramer pairwise multiple comparison post hoc test continental scale. adjusted for unequal variances and sample sizes (see Lau, 2013)or, as in our case, for unequal number of grid cells with occurrence 2. Methods data. In order to explore potential biases related to the uneven spatial 2.1. Taxonomic evaluation and temporal subdivision structure of the dataset, we performed a resampling procedure to check whether observed differences in average species richness Occurrence data of freshwater gastropods of the European between the defined TIs were affected by the different number of Quaternary were obtained after comprehensive literature search grid cells included in each TI (see Fig. 2). For this, we randomly (see Supplementary Table 1). Owing to the heterogeneity of the selected for each TI a number of grid cells equal to the minimum reviewed bibliography (e.g. different authors, publication periods, number of occupied grid cells across all TIs (i.e. 26 grid cells, and taxonomic approaches), species names were validated using Gelasian) and performed the ANOVA again. This procedure was updated scientific sources prior to the analyses; subspecies were repeated 1000 times. If the majority of the ANOVAs resulting from not considered unless the parent species was not represented in the the 1000 replicates are significant, then we assume that the dataset. We followed primarily the systematic approaches of observed differences in the average species richness are not Welter-Schultes (2012) and of de Jong (2012), supplemented where controlled by spatial bias. necessary with information from Gloer€ (2002). The taxonomic To verify whether the dataset was affected by collection biases, updates mainly concerned different opinions on synonymy, taxo- we performed a correlation test between species richness and the nomic level, generic attribution and spellings, and aimed at mini- number of grid cells with occurrence data per TI. The null hy- mizing the effect of taxonomic biases in the dataset. For early pothesis is that species richness of each TI is independent of sam- Quaternary species, we adopted the systematic approach of pling intensity. To evaluate the effect of time, a second correlation Neubauer et al. (2014 and references therein). test between the TIs' species richness and their temporal duration The geographical frame of the dataset is the European continent, was performed. All correlations were assessed using non- extending as far as the eastern shores of the Black Sea and the Volga parametric Spearman's rank test. Upland. Preservation issues, mostly because of glacial erosion during the Ice Ages, constrained data availability in certain regions 2.3. Species temporal turnover and range-through assumption like Scandinavia. The dataset was divided into six time intervals (TIs hereafter): Species turnover among TIs was assessed using the bjtu Gelasian (2.588e1.806 Ma), Calabrian (1.806e0.781 Ma), Middle dissimilarity measure (Baselga, 2012). This index was selected Pleistocene (0.781e0.126 Ma), Last Interglacial (0.126e0.115 Ma), because of its independency from differences in species richness Last Glacial (0.115e0.0117 Ma) and Holocene (0.0117e0 Ma). These (Baselga, 2012). To evaluate the turnover rate at the E. Georgopoulou et al. / Quaternary Science Reviews 149 (2016) 269e278 271
Fig. 1. Localities with Quaternary freshwater gastropods for the six time intervals Gelasian, Calabrian, Middle Pleistocene, Last Interglacial, Last Glacial and Holocene.
PlioceneePleistocene boundary, we included the Late Pliocene 2.4. Range sizes and range overlap-segregation (Piacenzian) European freshwater gastropod species from the dataset of Neubauer et al. (2015b). In order to correct for missing We measured each species’ geographical range and the total records, we adopted the range-through assumption, i.e. we area occupied by all species for each TI as the area of the smallest assumed that all species had continuously existed from their first to polygon enclosing all species occurrences using the Minimum last recorded occurrence (Hammer and Harper, 2006). To avoid Bounding Geometry Tool in ArcGIS. We then plotted species range biasing the real first and last appearance dates of the species by sizes as the proportion of the total area they occupy against the using only Pliocene to Quaternary records, we completed the cur- cumulative number of species in order to observe if the proportion rent data by integrating Neogene and modern records as well of restricted to widespread species ranges changes throughout the (Georgopoulou et al., 2016; Neubauer et al., 2015b). The analysis Quaternary. was repeated a second time excluding singletons, i.e. species pre- We investigated how spatial patterns of species distribution sent in only one TI, in order to evaluate their effect on the temporal varied throughout the Quaternary by assessing the structure of turnover. species-area presence-absence matrices, which map the occur- We applied a resampling procedure in order to ensure that the rence of each species in the equal-area grid cells per TI. To assess observed patterns of turnover were not influenced by preservation matrix structure, we used the recently established measure of node or spatial bias. For this, we calculated the average turnover rate overlap and segregation (Ɲ) introduced by Strona and Veech (2015), from 25% of randomly selected species of each TI over 1000 which permits testing if nodes in a network tend to share more or replicates. less interacting partners than expected by chance. Although the method was formulated for ecological networks, it 272 E. Georgopoulou et al. / Quaternary Science Reviews 149 (2016) 269e278
Fig. 2. Maps showing the geographical distribution of species richness for the six TIs based on 100 100 km grids (Behrmann projection). Species richness per grid cell is colour- coded, with equal scale across all figures (based on the grid cell richness of the Calabrian). The number indicated by the arrow in the richness bar corresponds to the maximum species richness per grid cell of the respective TI. can be directly applied to presence-absence species-area matrices, minimum values recorded for the six matrices, i.e. 26 cells (Gela- since these correspond to bipartite networks where species are sian) and 57 species (Last Interglacial). We then computed Ɲ for all connected to the localities where they occur. In such context, Ɲ can null matrices, in order to test if (and to what extent) the variation in measure both the tendency of species to co-occur in the same grid structure observed in the complete matrices between different TIs cell (range overlap) and the tendency of the localities to host similar was biased by differences in species richness or the number of faunas (beta similarity). Ɲ varies between 1 (maximum segrega- occupied grid cells. We also used a non-parametric Spearman's tion) and 1 (maximum overlap/nestedness), while values close to rank test to explore potential relationships between the number of 0 indicate randomness. first and last occurrences and TI duration and the average degree of A general problem in the analysis of non-random patterns in range overlap-segregation (Ɲ) across the TIs. species-area matrices is that differences in matrix properties (most Analyses were carried out in R 3.1.1 (R Development Core Team, notably matrix size and fill) can hamper comparisons (Strona et al., 2014) using packages DTK (Lau, 2013), sampling (Tille and Matei, 2013; Strona and Fattorini, 2014). To cope with this problem, which 2015) and betapart (Baselga et al., 2013). The analysis of node was particularly compelling in our study due to the large variability overlap-segregation was implemented in Python (Van Rossum and in both the number of occupied grid cells and species, we per- Drake, 1995). formed a bootstrapping procedure similar to that described in Strona et al. (2013). For this, 100 random matrices were created for 3. Results each species-area matrix by extracting at random a number of columns (i.e. grid cells) and rows (i.e. species) equal to the Our dataset included occurrence records for 338 species and E. Georgopoulou et al. / Quaternary Science Reviews 149 (2016) 269e278 273 subspecies, classified into 78 genera and 16 families, from 1058 (Gelasian and Calabrian) in contrast to the Late Pleistocene (Last localities of the European Quaternary (Fig. 1, Table 1). The number Interglacial and Last Glacial), where most of the species were wide- of grid cells with occurrence data varied between 26 (Gelasian) and ranged (Fig. 3, Table 3). 141 (Holocene) (Fig. 2). We detected no significant collection bias Ɲ was negatively correlated with TI duration (rho ¼ 0.94, between TIs, with the numbers of grid cells per TI largely uncor- P ¼ 0.005), indicating that species overlap is lower in TIs with related with species richness (rho ¼ 0.086, P ¼ 0.87). Similarly, longer duration. There was no correlation between Ɲ and the species richness was not correlated with TI duration (rho ¼ 0.71, number of first (rho ¼ 0.54, P ¼ 0.27) or last occurrences P ¼ 0.11). Although ANOVA revealed significant differences in (rho ¼ 0.26, P ¼ 0.62). The Quaternary trends of species richness, average species richness across TIs (F5,393 ¼ 5.283; P < 0.0001), not turnover and overlap-segregation are summarized in Fig. 4. all pairwise comparisons between TI species richness were signif- icant (Supplementary Table 3). In particular, average species rich- ness, which was highest during the Last Interglacial, dropped significantly to the Last Glacial and increased markedly to the Ho- locene (Supplementary Table 3). Average richness was also higher in the Middle Pleistocene and Calabrian compared to the Last Glacial (Supplementary Table 3). Finally, the majority of the repli- cate ANOVAs (90.4%) was significant, i.e. P-values were below the significance level 0.05 (see Supplementary Fig. 1), indicating that our results are not affected by the uneven spatial extend of the dataset. Average species temporal turnover resulting from random resampling (Table 2) was in agreement with the original turnover rates (see Supplementary Table 4). Dissimilarity due to species replacement (bjtu) varied from 0 between the Last Interglacial and the Last Glacial to 0.91 ± 0.03 between the Piacenzian and the Holocene (Table 2). Considering consecutive TIs, species turnover was exceptionally high between the Piacenzian and the Gelasian (0.80 ± 0.10), followed by the CalabrianeMiddle Pleistocene (0.35 ± 0.07) and GelasianeCalabrian (0.33 ± 0.06), while it remained low for the remaining pairs, i.e. Middle PleistoceneeLast Interglacial (0.14 ± 0.07) and Last GlacialeHolocene (0.17 ± 0.07). The lack of species replacement between the Last Interglacial and Last Glacial reflects the high similarity in species composition of the two TIs. The exclusion of singletons lowered the compositional Fig. 3. Proportion of species' geographical ranges of gastropod species per TI. The dissimilarity between the pairwise comparisons (see Table 2), so vertical axis represents the percentage of the study area covered by a species range. that the average bjtu dropped from 0.51 ± 0.29 to 0.35 ± 0.26. Geographical ranges of all TIs are scaled and the relative differences in between the TIs Small-ranged species prevailed in the Early Pleistocene are shown.
Table 1 Summary statistics for the 1058 Quaternary localities. Numbers of singletons, i.e. species that occur only in one time interval, for the range-through approach are given in parentheses. Standard deviation is provided for the mean grid cell richness. For the complete dataset see Supplementary Table 1.
Holocene Last glacial Last interglacial Middle pleistocene Calabrian Gelasian
Species richness 134 60 57 135 141 130 Genus richness 54 34 33 51 54 41 Range-through richness 158 (42) 128 (2) 124 (0) 169 (23) 195 (7) 205 (35) No. of localities 439 99 86 186 158 90 No. of occupied grid cells 141 53 50 83 46 26 Mean grid cell richness 12.22 ± 8.08 7.09 ± 5.82 13.64 ± 8.30 12.49 ± 9.35 12.83 ± 10.24 7.69 ± 8.14 Interval duration (myr) 0.0117 0.1033 0.011 0.655 1.025 0.782 No. of first occurrences 42 4 9 37 41 138 No. of last occurrences 158 12 0 54 63 51
Table 2
Species turnover rates between the six Quaternary TIs and the Piacenzian, computed with the bjtu index of species turnover. Results were generated from a 25% randomly selected subset of the data and averaged over a 1000 replications. Numbers in parentheses refer to turnover rates with singletons removed and were calculated with the same resampling approach as before. Turnover rates between stratigraphically consecutive TIs are shown in bold. Turnover rates between Quaternary TIs are marked with grey.
Holocene Last glacial Last interglacial Middle pleistocene Calabrian Gelasian
Last Glacial 0.17 ± 0.07 (0) Last Interglacial 0.14 ± 0.07 (0.03 ± 0.01) 0 (0) Middle Pleistocene 0.49 ± 0.07 (0.17 ± 0.03) 0.19 ± 0.07 (0.16 ± 0.02) 0.14 ± 0.07 (0.13 ± 0.02) Calabrian 0.58 ± 0.07 (0.34 ± 0.03) 0.35 ± 0.08 (0.33 ± 0.03) 0.31 ± 0.08 (0.31 ± 0.03) 0.35 ± 0.07 (0.18 ± 0.03) Gelasian 0.69 ± 0.06 (0.54 ± 0.03) 0.56 ± 0.08 (0.56 ± 0.03) 0.54 ± 0.08 (0.55 ± 0.03) 0.58 ± 0.07 (0.49 ± 0.02) 0.33 ± 0.06 (0.17 ± 0.02) Piacenzian 0.91 ± 0.03 (0.76 ± 0.03) 0.88 ± 0.04 (0.75 ± 0.03) 0.87 ± 0.04 (0.75 ± 0.01) 0.89 ± 0.03 (0.67 ± 0.01) 0.85 ± 0.04 (0.38 ± 0.01) 0.80 ± 0.04 (0) 274 E. Georgopoulou et al. / Quaternary Science Reviews 149 (2016) 269e278
Table 3 (compare Jansson and Dynesius, 2002 and references therein). Summary results of range overlapesegregation analysis and summary statistics of Exceptionally rich assemblages during the Last Interglacial were species ranges for the six TIs. Ɲ, average range overlapesegregation; mean SR, mean found in central Germany (Mania, 1973), southern and eastern species ranges in km2; max SR, maximum species ranges in km2. England (Sparks, 1964; Sparks and West, 1959; West and Sparks, TI Ɲ Mean SR Max SR 1960), and Belarus (Sanko, 2007). The increased average richness Holocene 0.054 ± 0.15 936563.84 7427516 may be attributed to optimum climatic conditions that enabled Last Glacial 0.159 ± 0.10 488625.06 3154710 molluscs to expand their ranges towards north-eastern Europe (see ± Last Interglacial 0.195 0.07 515164.69 1724436 Sanko et al., 2011 and references therein). On the other hand, the Middle Pleistocene 0.144 ± 0.16 615122.27 3801977 Calabrian 0.396 ± 0.11 198196.47 2715862 Last Interglacial was characterised by the lowest species diversity Gelasian 0.703 ± 0.04 34278.51 1523283 among all TIs, even when the range-through approach was considered. This could be partially related to processes dating back to the Middle Pleistocene, e.g. climate continentalisation in 4. Discussion southeast and central Europe (Buggle et al., 2013), which promoted a decrease in species richness (cf. Alexandrowicz et al., 2014a; cf. 4.1. Patterns of species richness Alexandrowicz and Alexandrowicz, 2010). It should be noted, however, that data for the Last Interglacial were only available for a Following the latest phase of the Pliocene with ca. 450 species restricted latitudinal zone in central and northern Europe. (after Neubauer et al., 2015b), European lacustrine gastropod spe- During the Last Glacial, both species diversity and local richness cies richness continuously declined throughout the Pleistocene. were restricted. The fossil deposits of this TI indicate the existence Our results indicate that differences in richness, which are unre- of small, short-lived water bodies inhabited by few but widespread lated to unequal temporal duration or to uneven spatial sampling, species (e.g. Alexandrowicz, 2013a; Apolinarska and Ciszewska, can be largely explained by how the availability of freshwater 2006; Hoek et al., 1999; Kossler and Strahl, 2011; Sümegi et al., habitats varied across the Quaternary. The majority of the Gelasian 2011). For example, during the Late Glacial, gastropod faunas of species was bound to a handful of diverse and often highly endemic (palaeo-) lakes in northern Poland were poor and consisted mainly aquatic systems, e.g. the fluvio-lacustrine Bresse Basin in south- of species with wide ecological preferences (Alexandrowicz, eastern France with 44 species, the East Anglian Crag in eastern 2013a). In addition, temperature had considerably declined (see England with 21 species, Lake Kos in Greece with 19 species, and Lisiecki and Raymo, 2005), and the advancing ice sheets from the Lake Tiberino in central Italy with 38 species (e.g. see Neubauer middle Weichselian to the Last Glacial Maximum had covered large et al., 2015b; Schlickum and Puissegur, 1978; Willmann, 1981). parts of northern Europe and the Alpine region (Mangerud et al., The Lakes Bresse and Tiberino persisted into the Calabrian (Esu and 2004). Nevertheless, local richness maxima were detected above Girotti, 1975; Schlickum and Puissegur, 1977, 1978) and may qualify or near the permafrost line as reconstructed by Frenzel et al. (1992), as long-lived lakes (following Gorthner, 1992). Additionally, during while the few available southern localities were much poorer. the Calabrian new centres of diversity evolved in the Hungarian As shown by a series of molecular analyses (e.g. Benke et al., fluvial basins and fluvio-lacustrine systems in south-western Ger- 2009; Cordellier and Pfenninger, 2008, 2009), refugia for fresh- many and the Netherlands. On the Iberian Peninsula and in eastern water gastropods existed during the Late Pleistocene glaciations in Europe only small aquatic bodies with less diverse faunas were northern and central Europe. Thus, local richness maxima can be present during the Early Pleistocene. Thus, during the entire Early partly explained by the availability of northern refugia and by the Pleistocene, the majority of freshwater deposits bearing gastropods increased proportion of widespread species. Although fossil data of seemed to be associated with long-lived aquatic systems which freshwater gastropods from the southern regions of Europe is less offered stable environmental conditions and facilitated speciation complete than the Central European record, the existence of (Wesselingh, 2007). Our results on increased speciation rates (see species-poor southern localities as opposed to relative rich local- Table 1) further support this hypothesis. ities in northern (excluding Scandinavia) and central Europe sug- On the contrary, in the Middle Pleistocene, Late Pleistocene and gests that local richness is not a function of temperature alone (see Holocene, the highest richness was mostly found in smaller and Fig. 2 and Supplementary Table 2). short-lived freshwater habitats. Examples of such fluvial and/or During the Holocene, examples of rich gastropod assemblages lacustrine systems with highly diverse fauna can be found in were associated with freshwater deposits in Belarus (Sanko, 2007), central-eastern England (Horton et al., 1992; Kennard and Belgium (Kuijper, 2006) and the Netherlands (Meijer, 1988). The Woodward, 1922) and south-western Germany (Bibus and Rahle,€ three main reasons for the observed high species richness during 2003). the Holocene are i) the increased availability of suitable habitats in Although several long-lived lakes existed at that time, including postglacially developing lakes triggering successive recolonization the still existing Lake Ohrid (Wagner et al., 2014; Wilke et al., 2016), of formerly glaciated areas (Georgopoulou et al., 2016); ii) the the Caspian Sea (Albrecht et al., 2014), and the Black Sea resulting increase in speciation rates, mostly in southern European (Wesselingh, 2007), there is little information available on their species (see Hewitt, 1999, 2000); iii) the higher preservation po- freshwater gastropod faunas prior to the Holocene. Lake Lirino in tential for the geologically young deposits. central Italy may also qualify as a long-lived lake, as suggested by its well-constrained temporal duration of ca. 200 kyr (Manzi et al., 4.2. Temporal turnover 2010), and supported indirectly by its quite diverse fauna consist- ± ing of 30 species (Settepassi and Verdel, 1965). A substantial species turnover (0.80 0.04) marked the Plio- e Despite the continuous climatic deterioration, an expansion of cene Pleistocene boundary, constituting one of the major tipping the climatic periodicity from 41 kyr to 100 kyr between 0.9 and 0.4 points in European freshwater gastropod diversity. Species Ma resulted in longer warm (interglacial) and shorter cold (glacial) replacement at the time was entirely controlled by singletons intervals up to the Late Pleistocene (Lisiecki and Raymo, 2005). (Table 2), which were mainly associated with long-lived lakes. The Thus, the increased climatic stability may partly explain the strong turnover resulted from the demise of large, long-lived and increased species richness observed for the Middle Pleistocene diverse lakes such as Dacia, Slavonia and Transylvania, and from the disappearance of their highly endemic faunas. A comparable E. Georgopoulou et al. / Quaternary Science Reviews 149 (2016) 269e278 275
Fig. 4. Species richness, turnover and range overlapesegregation trends throughout the Quaternary. Standard deviations of species turnover, average richness and over- lapesegregation are shown, respectively. a. Average richness was calculated based on the equal-area grid cells. b. Species richness is based on the range-through assumption. c.
Turnover is based on the range-through assumption. Shown are the values of the bjtu index of species turnover (dark grey line) and the values of the bjtu index of species turnover after the exclusion of singletons (light grey dashed line). Notice that the species turnover after the exclusion of singletons is very low. d. Range overlapesegregation was calculated based on the equal-area grid cells. Hol, Holocene; LG, Last Glacial; Lint, Last Interglacial; MP, Middle Pleistocene; Cal, Calabrian; Gel, Gelasian.
pattern, albeit to a lesser extent, characterised the GelasianeCala- At the end of the Middle Pleistocene, several genera and species brian boundary. It corresponds mostly to the diminution of aquatic typical for the Neogene to early Quaternary disappeared from basins, such as Lake Kos, the East Anglian Crag and Patras Graben Europe's inland aquatic systems, e.g. the genera Neumayria (see (see Doutsos et al., 1988), and the appearance of typical Calabrian Girotti, 1972) and Pseudodianella (see Neubauer et al., 2013) and species, such as Microcolpia wuesti (Meijer, 1990), a species char- species like Borysthenia goldfussiana (Wüst, 1901), Lithoglyphus acteristic of the Bavelian stage (1.2e0.86 Ma) but with no associa- jahni (Urbanski, 1975), Tanousia runtoniana (Sandberger, 1880) and tion to such long-lived lakes (Meijer and Preece, 1996). Species Tanousia stenostoma (Nordmann in Madsen and Nordmann, 1901) turnover between the Calabrian and the Middle Pleistocene was (see Meijer and Preece, 1996). In addition, few modern taxa mainly caused by the presence of singletons. Typical Calabrian appeared during the ensuing Last Interglacial [e.g. Bythinella aus- faunas, such as those of the Lakes Bresse and Tiberino, were triaca (Frauenfeld, 1857); Benke et al., 2009, 2011]. The rather low replaced in the Middle Pleistocene by faunas of aquatic basins in turnover rate was unaffected by singletons, reflecting the lack of southern and eastern Europe like Lirino (Liri Valley, Italy), Larymna- long-lived systems promoting speciation and endemism during Malesina (Atalanti Basin, Greece), Don (Don River Basin, Russia), these periods. As some of the abovementioned species have been and the Black Sea, some of which can be considered as long-lived linked with temperate climatic conditions (see Meijer and Preece, lakes sensu Gorthner (1992). Climate conditions during the Ear- 1996), their disappearance may be linked to the further deterio- lyeMiddle Pleistocene transition have been regarded as a potential rating climate and climate continentalisation (Buggle et al., 2013). cause of faunal turnover in western Palaearctic mammals (Kahlke However, despite the fundamental climate changes following the et al., 2011), and may have also contributed to the freshwater transition into the Last Glacial, there was no species turnover be- gastropod turnover. tween the Last Interglacial and Last Glacial. Turnover between the 276 E. Georgopoulou et al. / Quaternary Science Reviews 149 (2016) 269e278
Last Glacial and the Holocene was moderate, and again explained the Caspian Sea still exist in Europe e paralleled the decline of by the abundance of singletons. endemic species and provincialism per se, and the decrease in Consequently, climate cannot be regarded as the main driving species turnover (see Fig. 4). The rise and demise of these long-lived force for species turnover in the Quaternary. Although climatic systems and their associated fauna are rooted in the tectonic ac- fluctuations apparently affected the spatial distribution of modern tivity and geodynamic evolution of Europe (Neubauer et al., 2015b). lacustrine gastropods (Georgopoulou et al., 2016), their effect on Climate seems to be only a secondary force in shaping species temporal turnover seems to be limited. As a general rule, turnover turnover in the Quaternary. rates are controlled by rare species, mostly related to the existence Conversely, climate change or, more precisely, the repeated cy- and demise of long-lived lakes. This implies that there was little cles of glaciation and deglaciation, had a strong effect on gastro- temporal turnover in “normal” short-lived aquatic systems, which pods’ geographical ranges. The node overlap and segregation comprise the vast majority of Quaternary freshwater systems. analysis indicated that the present-day and Last Interglacial pat- terns resulted from random recolonization of formerly glaciated 4.3. Nested patterns of species ranges areas following deglaciation after, respectively, the Last Glaciation Maximum ca. 19 kyr BP (Clark et al., 2009; see also Georgopoulou The distinction between the provincial faunas of the Early et al., 2016) and the late Middle Pleistocene Glaciation ca. 125 kyr Pleistocene and the following, short-lived type of fauna is also re- BP (Kukla, 2000). The climatically induced local extirpation and flected in the range overlap-segregation analysis. During the following recolonization was likely an iterative process shaping Gelasian and Calabrian, our analysis revealed an overall tendency freshwater gastropod distributions throughout the glacial cycles. towards segregation (Table 3), with low overlap in species distri- The high proportion of species with wide geographical ranges in butions and low species co-occurrence, possibly because of the the Late Pleistocene and Holocene indicates that the majority of average small species ranges observed in that period. These results surviving species were generalists. may indicate that at a European scale the biogeographical con- Other aspects that have been considered to influence patterns of nections of freshwater gastropods were low. freshwater gastropod distributions are local environmental condi- Although species ranges were larger during the Middle Pleis- tions (Alexandrowicz, 2013a) and the increasing human activity tocene, the Last Interglacial, the Last Glacial and the Holocene (see during the last ca. 100 kyr (e.g. Alexandrowicz, 2008; Sanko et al., Fig. 3), species/site overlap did not increment significantly, with the 2011). Local conditions, such as resource availability, habitat di- patterns in species distribution tending instead towards a general versity, topography and vegetation richness, have been docu- lack of structure (Table 3). According to Briers (2003), resource mented to influence the successful establishment and diversity of availability and species’ ability to exploit them affect range sizes of fossil freshwater mollusc faunas (Alexandrowicz, 2013a; freshwater gastropods. The increased proportion of wide-ranged Alexandrowicz et al., 2014b; Sümegi et al., 2011). Similarly, species from the Middle Pleistocene onwards suggests that the increasing human impact in the Late Pleistocene and Holocene led majority of surviving species were generalists, able to explore a to the impoverishment of assemblages, disappearance of species considerable amount of resources, which is consistent with our and changes in composition (e.g. Alexandrowicz, 2008, 2013a, b; results (i.e. Ɲ values close to 0). Sümegi, 2007). Although human impact has been mostly consid- The lack of clear structure in freshwater gastropod distribution ered to negatively affect freshwater gastropod faunas, the observed after the Early Pleistocene may be also related to the rapidly expansion of range sizes and low temporal turnover could also changing and progressively unstable climatic conditions (see result from human-induced transport or changes in available hy- Dynesius and Jansson, 2000 and references therein). Species ranges drological connections (e.g. Gaigalas et al., 2007; Sanko et al., 2011). generally diminish in every glacial cycle and expand as a response More research on individual drivers needs to be carried out in the to favourable climatic conditions during interglacial phases future to understand their contributions to the observed patterns. (Dynesius and Jansson, 2000; Limondin-Lozouet and Preece, 2014; Rousseau, 1989). If the warm phases are short, species assemblages Acknowledgements do not have enough time to evolve detectable structural patterns, for example, due to ecological processes, such as competitive We thank Tom Wilke for fruitful discussion and ideas on Late exclusion, or biogeographical ones, such as dispersion, colonization Quaternary gastropods, Stelios Simaiakis for his advice on statistical and local extinction (e.g. see Georgopoulou et al., 2016). issues and Witold Alexandrowicz and two anonymous reviewers for their constructive comments on a previous version of this 5. Conclusions manuscript. This contribution was financed by the Austrian Science Fund and is part of the FreshGEN-project (FWF project no. P25365- The massive erosion due to advancing and retreating ice sheets B25: “Freshwater systems in the Neogene and Quaternary of constrained the availability of surface outcrops and preserved Europe: Gastropod biodiversity, provinciality, and faunal faunas in northern Europe (Molnar, 2004; Sternai et al., 2012), gradients”). while certain geographic areas have been surveyed by scientists more intensely than others. Although our results were affected to Appendix A. Supplementary data some extent by the incomplete nature of the fossil record, the consistent outcomes of multiple complementary analyses, and the Supplementary data related to this article can be found at http:// lack of correlation between total species richness and the number dx.doi.org/10.1016/j.quascirev.2016.07.034. of the grid cells per TI provide robustness to our conclusions and suggest that the observed patterns were not driven by data References availability. Our results point towards a gradual loss of the Neogene pro- Albrecht, et al., 2014. Evolution of ancient lake bivalves: the Lymnocardiinae (Car- vincialism during the Quaternary. After the demise of the big diidae) of the Caspian sea. Hydrobiologia 739, 85e94. lacustrine diversity hotspots at the end of the Pliocene only few, Alexandrowicz, W.P., 1999. Evolution of the malacological assemblages in north Poland during the Late Glacial and Early Holocene. Folia Quat. 70, 39e69. smaller long-lived lakes survived to the Early Pleistocene. The Alexandrowicz, S.W., 2008. Malacofauna of Late Quaternary lacustrine deposits at continuous decline of such systems e today only Lake Ohrid and Osłonki (Kujawy, Central Poland). Folia Quat. 78, 51e69. E. Georgopoulou et al. / Quaternary Science Reviews 149 (2016) 269e278 277
Alexandrowicz, W.P., 2013a. Late Glacial and Holocene molluscan assemblages in Gibbard, P.L., Head, M.J., Walker, M.J.C., the Subcommission on Quaternary Stra- deposits filling palaeolakes in northern Poland. Stud. Quat. 30 (1), 5e17. tigraphy, 2010. Formal ratification of the Quaternary System/Period and the Alexandrowicz, W.P., 2013b. Molluscan communities in late Holocene fluvial de- Pleistocene Series/Epoch with a base at 2.58 Ma. J. Quat. Sci. 25, 96e102. posits as an indicator of human activity: a study in Podhale basin in south Girotti, O., 1972. Il genere Neumayria Stefani 1877 (Gastropoda, Prosobranchia). Poland. Ekologia Bratisl. 32 (1), 111e125. Geol. Romana 11, 115e136. Alexandrowicz, W.P., Alexandrowicz, S.W., 2010. Molluscs of the Eemian interglacial Gloer,€ P., 2002. Die Tierwelt Deutschlands, 73. Teil: Die Süßwassergastropoden in Poland. Ann. Soc. Geol. Pol. 80, 69e87. Nord- und Mitteleuropas. Bestimmungsschlüssel, Lebensweise, Verbreitung. Alexandrowicz, W.P., Łanczont, M., Boguckyj, A.B., Kulesza, P., Dmytruk, R., 2014a. ConchBooks, Hackenheim. Molluscs and ostracods of the Pleistocene loess deposits in the Halych site Gorthner, A., 1992. Bau, Funktion und Evolution komplexer Gastropodenschalen in (Western Ukraine) and their significance for palaeoenvironmental re- Langzeit-Seen Mit einem Beitrag zur Palaobiologie€ von Gyraulus “multiformis” constructions. Quat. Sci. Rev. 105, 162e180. im Steinheimer Becken. Stuttg. Beitrage€ zur Naturkd. Ser. B 190, 1e173. Alexandrowicz, W.P., Szymanek, M., Rybska, E., 2014b. Changes to the environment Hammer, Ø., Harper, D.A.T., 2006. Paleontological Data Analysis. Blackwell Pub- of intramontane basins in the light of malacological research of calcareous tufa: lishing, Oxford. Podhale Basin (Carpathians, Southern Poland). Quat. Int. 353, 250e265. Harzhauser, M., Mandic, O., 2008. Neogene lake systems of Central and South- Antonioli, F., Ferranti, L., Fontana, A., Amorosi, A., Bondesan, A., Braitenberg, C., Eastern Europe: faunal diversity, gradients and interrelations. Palaeogeogr. Dutton, A., Fontolan, G., Furlani, S., Lambeck, K., Mastronuzzi, G., Monaco, C., Palaeoclimatol. Palaeoecol. 260, 417e434. Spada, G., Stocchi, P., 2009. Holocene relative sea-level changes and vertical Hewitt, G.M., 1999. Post-glacial re-colonization of European biota. Biol. J. Linn. Soc. movements along the Italian and Istrian coastlines. Quat. Int. 206, 102e133. 68, 87e112. Apolinarska, K., Ciszewska, M., 2006. Late Glacial and Holocene lacustrine molluscs Hewitt, G., 2000. The genetic legacy of the Quaternary ice ages. Nature 405, from Wielkopolska (central Poland) and their environmental significance. Acta 907e913. Geol. Pol. 56 (1), 51e66. Hoek, W.Z., Bohncke, S.J.P., Ganssen, G.M., Meijer, T., 1999. Lateglacial environmental Baselga, A., 2012. The relationship between species replacement, dissimilarity changes recorded in calcareous gyttja deposits at Gulickshof, southern derived from nestedness, and nestedness. Glob. Ecol. Biogeogr. 21, 1223e1232. Netherlands. Boreas 28, 416e432. Baselga, A., Orme, D., Villeger, S., De Bortoli, J., Leprieur, F., 2013. Betapart: Parti- Horton, A., Keen, D.H., Field, M.H., Robinson, J.E., Coope, G.R., Currant, A.P., tioning Beta Diversity into Turnover and Nestedness Components. R Package Graham, D.K., Green, C.P., Phillips, L.M., 1992. The Hoxnian interglacial deposits Version 1.3. http://CRAN.R-project.org/package¼betapart. at Woodston, Peterborough. Philosophical Trans. R. Soc. Lond. B 338, 131e164. Benke, M., Brandle,€ M., Albrecht, C., Wilke, T., 2009. Pleistocene phylogeography and Jansson, R., Dynesius, M., 2002. The fate of clades in a world of recurrent climatic phylogenetic concordance in cold-adapted spring snails (Bythinella spp.). Mol. change: Milankovitch oscillations and evolution. Ann. Rev. Ecol. Evol. Syst. 33, Ecol. 18, 890e903. 741e777. Benke, M., Brandle,€ M., Albrecht, C., Wilke, T., 2011. Patterns of freshwater biodi- Kahlke, R.-D., García, N., Kostopoulos, D.S., Lacombat, F., Lister, A.M., Mazza, P.P.A., versity in Europe: lessons from the spring snail genus Bythinella. J. Biogeogr. 38, Spassov, N., Titov, V.V., 2011. Western Palaearctic palaeoenvironmental condi- 2021e2032. tions during the Early and early Middle Pleistocene inferred from large Bibus, E., Rahle,€ W., 2003. Stratigraphische Untersuchungen an molluskenführen- mammal communities, and implications for hominin dispersal in Europe. Quat. den Terrassensedimenten und ihren Deckschichten im mittleren Neckarbecken Sci. Rev. 30, 1368e1395. (Württemberg). Eiszeitalt. Ggw. 53, 94e113. Kennard, A.S., Woodward, B.B., 1917. The Post-Pliocene non-marine Mollusca of Briers, R.A., 2003. Range size and environmental calcium requirements of British Ireland. Proc. Geologists’ Assoc. 28, 109e190. freshwater gastropods. Glob. Ecol. Biogeogr. 12, 47e51. Kennard, A.S., Woodward, B.B., 1922. The Post-Pliocene non-marine Mollusca of the Buggle, B., Hambach, U., Kehl, M., Markovic, S.B., Zoller,€ L., Glaser, B., 2013. The east of England. Proc. Geologists’ Assoc. 33, 104e142. progressive evolution of a continental climate in southeast-central European Kossler, A., Strahl, J., 2011. The Late Weichselian to Holocene succession of the lowlands during the Middle Pleistocene recorded in loess paleosol sequences. Niedersee (Rügen, Baltic Sea) e new results based on multi-proxy studies. E&G Geology 41, 771e774. Quat. Sci. J. 60 (4), 434e454. Clark, P.U., Dyke, A.S., Shakun, J.D., Carlson, A.E., Clark, J., Wohlfarth, B., Kreft, H., Jetz, W., 2010. A framework for delineating biogeographic regions based Mitrovica, J.X., Hostetler, S.W., McCabe, A.M., 2009. The last glacial maximum. on global species distributions. J. Biogeogr. 37, 2029e2053. Science 325 (5941), 710e714. Kuijper, W.J., 2006. Flora en fauna in en rond een Scheldegeul bij Kallo op het einde Colwell, R.K., Rangel, T.F., 2010. A stochastic, evolutionary model for range shifts and van het atlanticum (Beveren, prov. Oost-Vlaanderen). Relicta 1, 29e48. richness on tropical elevational gradients under Quaternary glacial cycles. Kukla, G.J., 2000. The last interglacial. Science 287, 987e988. Philosophical Trans. R. Soc. B 365, 3695e3707. Lau, M.K., 2013. DTK: Dunnett-Tukey-Kramer Pairwise Multiple Comparison Test Coope, G.R., 1994. The response of insect faunas to glacial-interglacial climatic Adjusted for Unequal Variances and Unequal Sample Sizes. R Package Version fluctuations. Philosophical Trans. R. Soc. B 344, 19e26. 3.5. http://CRAN.R-project.org/package¼DTK. Cordellier, M., Pfenninger, M., 2008. Climate-driven range dynamics in the fresh- Limondin-Lozouet, N., Preece, R.C., 2014. Quaternary perspectives on the diversity water limpet Ancylus fluviatilis (Pulmonata, Basommatophora). J. Biogeogr. 35, of land snail assemblages from northwestern Europe. J. Molluscan Stud. 80, 1580e1592. 224e237. Cordellier, M., Pfenninger, M., 2009. Inferring the past to predict the future: climate Lisiecki, L.E., Raymo, M.E., 2005. A Pliocene-Pleistocene stack of 57 globally modelling predictions and phylogeography for the freshwater gastropod Radix distributed benthic d18O records. Paleoceanography 20, PA1003. http:// balthica (Pulmonata, Basommatophora). Mol. Ecol. 18, 534e544. dx.doi.org/10.1029/2004PA001071. de Jong, Y.S.D.M., 2012. Fauna Europaea Version 2.5. http://www.faunaeur.org. Lo zek, V., 1964. Quartarmollusken€ der Tschechoslovakei. Rozpravy Úst redního Doutsos, T., Kontopoulos, N., Poulimenos, G., 1988. The Corinth-Patras rift as the Ústavu Geologickeho 31, Praha. initial stage of continental fragmentation behind an active island arc (Greece). Madsen, V., Nordmann, V., 1901. Det interglaciale Nematurella ler ved gudbjerg paa Basin Res. 1, 177e190. fyn. Meddelelser fra Dan. Geol. Foren. 8, 23e30. Dynesius, M., Jansson, R., 2000. Evolutionary consequences of changes in species' Mangerud, J., Jakobsson, J., Alexanderson, H., Astakhov, V., Clarke, G.K.C., geographical distributions driven by Milankovitch climate oscillations. Proc. Henriksen, M., Hjort, C., Krinner, G., Lunkka, J.-P., Moller,€ P., Murray, A., Natl. Acad. Sci. U. S. A. 97, 9115e9120. Nikolskaya, O., Saarnisto, M., Svendsen, J.I., 2004. Ice-dammed lakes and Esri Inc, 1999e2010. ArcGIS for Desktop: Release 10. Environmental Systems rerouting of the drainage of northern Eurasia during the last glaciation. Quat. Research Institute, Redlands, CA. Sci. Rev. 23, 1313e1332. Esu, D., Girotti, O., 1975. La malacofauna continentale del Plio-Pleistocene dell’Italia Mania, D., 1973. Palao€ okologie,€ Faunenentwicklung und Stratigraphie des Eiszei- centrale. I. Paleontologia. Geol. Romana 13, 203e294. talters im mittleren Elbe-Saalegebiet auf Grund von Molluskengesellschaften. Frauenfeld, G. von, 1857. Über die Paludinen aus der Gruppe der Paludina viridis Geol. Beih. 21 (78/79), 1e175. Poir. Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften. Naturwiss. Manzi, G., Magri, D., Milli, S., Palombo, M.R., Margari, V., Celiberti, V., Barbieri, M., Cl. 22 (2), 569e578. Barbieri, M., Melis, R.T., Rubini, M., Ruffo, M., Saracino, B., Tzedakis, P.C., Frenzel, B., Pesci, M., Velichko, A.A., 1992. Atlas of Paleoclimates and Paleoenvir- Zarattini, A., Biddittu, I., 2010. The new chronology of the Ceprano calvarium onments of the Northern Hemisphere. Late PleistoceneeHolocene. Hungarian (Italy). J. Hum. Evol. 59, 580e585. Academy of Sciences/G. Fischer, Budapest/Jena. Meijer, T., 1988. Mollusca from the borehole Zuurland-2 at brielle, The Netherlands Gabris, G., Nador, A., 2007. Long-term fluvial archives in Hungary: response of the (an interim report). Meded. Werkgr. Tert. Kwartaire Geol. 25 (1), 49e60. Danube and Tisza rivers to tectonic movements and climatic changes during the Meijer, T., 1990. Notes on Quaternary freshwater Mollusca of The Netherlands, with Quaternary: a review and new synthesis. Quat. Sci. Rev. 26, 2758e2782. descriptions of some new species. Meded. Werkgr. Tert. Kwartaire Geol. 26 (4), Gaigalas, A., Sanko, A., Pazdur, A., Pawlyta, J., Michczynski, A., Budenait_ e,_ S., 2007. 145e181. Buried oaks and malacofauna of Holocene oxbow lake sediments in the Vala- Meijer, T., Preece, R.C., 1996. Malacological evidence relating to the stratigraphical kupiai section, Lithuania. Geologija 58, 34e48. position of the Cromerian. In: Turner, C. (Ed.), The Early Middle Pleistocene in Georgopoulou, E., Neubauer, T.A., Kroh, A., Harzhauser, M., Mandic, O., 2015. An Europe. A.A. Balkema, Brookfield, Rotterdam, pp. 53e82. outline of the European Quaternary localities with freshwater gastropods: data Molnar, P., 2004. Late Cenozoic increase in accumulation rates of terrestrial sedi- on geography and updated stratigraphy. Palaeontol. Electron. 18.3.48A, 1e9. ment: how might climate change have affected erosion rates? Annu. Rev. Earth Georgopoulou, E., Neubauer, T.A., Harzhauser, M., Mandic, O., Kroh, A., 2016. Dis- Planet. Sci. 32, 67e89. tribution patterns of European lacustrine gastropods: a result of environmental Neubauer, T.A., Mandic, O., Harzhauser, M., Hrvatovi c, H., 2013. A new Miocene factors and deglaciation history. Hydrobiologia 775, 69e82. http://dx.doi.org/ lacustrine mollusc fauna of the Dinaride Lake System and its palaeobiogeo- 10.1007/s10750-016-2713-y. graphic, palaeoecologic, and taxonomic implications. Palaeontology 56 (1), 278 E. Georgopoulou et al. / Quaternary Science Reviews 149 (2016) 269e278
129e156. on node overlap and segregation. Methods Ecol. Evol. 6, 907e915. Neubauer, T.A., Harzhauser, M., Kroh, A., Georgopoulou, E., Mandic, O., 2014. The Strona, G., Stefani, F., Galli, P., Fattorini, S., 2013. A protocol to compare nestedness FreshGEN Database: Freshwater Gastropods of the European Neogene. Accessed among submatrices. Popul. Ecol. 55 (1), 227e239. at. http://www.marinespecies.org/freshgen. on 2015-10-15. Sümegi, P., 2007. Palaeoenvironmental studies in the Sarr et region. In: Zatyko, C., Neubauer, T.A., Harzhauser, M., Kroh, A., Georgopoulou, E., Mandic, O., 2015a. Juhasz, I., Sümegi, P. (Eds.), Environmental Archaeology in Transdanubia, 20. A gastropod-based biogeographic scheme for the European Neogene freshwater Varia Archaeologica Hungarica, pp. 361e383. systems. Earth Sci. Rev. 143, 98e116. Sümegi, P., Locskai, T., Hupuczi, J., 2011. Late Quaternary palaeoenvironment and Neubauer, T.A., Harzhauser, M., Georgopoulou, E., Kroh, A., Mandic, O., 2015b. palaeoclimate of the Lake Feher (Feher-t o) sequence at Kardoskút (South Tectonics, climate, and the rise and demise of continental aquatic species Hungary), based on preliminary mollusc records. Central Eur. J. Geosciences 3 richness hotspots. Proc. Natl. Acad. Sci. U. S. A. 112, 11478e11483. (1), 43e52. R Development Core Team, 2014. R: a Language and Environment for Statistical Tille, Y., Matei, A., 2015. Sampling: Survey Sampling. R Package Version 2.7. https:// Computing. R Foundation for Statistical Computing, Vienna, Austria. http:// CRAN.R-project.org/package¼sampling. www.R-project.org. Urbanski, J., 1975. Lithoglyphus jahni n. sp. aus den mitteleuropaischen€ Ablager- Rousseau, D.D., 1989. Reponses des malacofaunes terrestres quaternaires aux con- ungen des Mindel/Riss Interglazials, nebst Bemerkungen über den nordbalka- traintes climatiques en Europe septentrionale. Palaeogeogr. Palaeoclimatol. nischen L. fuscus (C. Pfeiffer 1828) (¼ L. pyramidatus Moellendorff 1873) Palaeoecol. 69, 113e124. (Gastropoda, Prosobranchia, Hydrobiidae). Bull. de la Soc. des Amis des Sci. des Sandberger, F., 1880. Ein Beitrag zur Kenntniss der unterpleistocanen€ Schichten Lettres de Poznan Serie D Sci. Biol. (15), 107e112. Englands. Palaeontographica 27 (2), 83e104. Van Rossum, G., Drake Jr., F.L., 1995. Python reference Manual. Centrum voor Sanko, A.F., 2007. Quaternary Freshwater Molluscs Belarus and Neighbouring Re- Wiskunde en Informatica, Amsterdam. gions of Russia, Lithuania, Poland (Field Guide). Institute of Geochemistry and Wagner, B., Wilke, T., Krastel, S., Zanchetta, G., Sulpizio, R., Reicherter, K., Leng, M.J., Geophysics. National Academy of Sciences, Belarus (In Russian). Grazhdani, A., Trajanovski, S., Francke, A., Lindhorst, K., Levkov, Z., Cvetkoska, A., Sanko, A.F., Gaigalas, A., Yelovicheva, Y., 2011. Paleoclimatic and stratigraphic sig- Reed, J.M., Zhang, X., Lacey, J.H., Wonik, T., Baumgarten, H., Vogel, H., 2014. The nificance of Belgrandia marginata (Michaud) in late Quaternary malacofauna of SCOPSCO drilling project recovers more than 1.2 million years of history from Belarus and Lithuania. Quat. Int. 241, 68e78. Lake Ohrid. Sci. Drill. 17, 19e29. Schlickum, W.R., Puissegur, J.-J., 1977. Die Molluskenfauna des Altpleistozans€ von St. Welter-Schultes, F.W., 2012. European Non-marine Molluscs, a Guide for Species Bernard (Departement Cote-d'Or).^ Arch. für Molluskenkd. 107 (4/6), 273e283. Identification. Planet Poster Editions, Gottingen€ . Schlickum, W.R., Puissegur, J.-J., 1978. Die Molluskenfauna der Schichten mit Wesselingh, F.P., 2007. Long-lived lake molluscs as island faunas: a bivalve Viviparus burgundinus und Pyrgula nodotiana von Montagny-les-Beaune (Dep. perspective. In: Renema, W. (Ed.), Biogeography, Time, and Place: Distributions, Cote-d'Or).^ Arch. für Molluskenkd. 109 (1/3), 1e26. Barriers, and Islands. Springer, Dordrecht, pp. 275e314. Settepassi, F., Verdel, U., 1965. Continental Quaternary Mollusca of lower Liri Valley West, R.G., Sparks, B.W., 1960. Coastal interglacial deposits of the English channel. ́ (southern Latium). Geol. Romana 4, 369e452. Philosophical Trans. R. Soc. Lond. B 243, 95e133. Sparks, B.W., 1964. The distribution of non-marine Mollusca in the last interglacial Wilke, T., Wagner, B., Bocxlaer, B., Albrecht, C., Ariztegui, D., Delicado, D., Francke, A., in south-east England. Proc. Malacol. Soc. Lond. 36 (1), 7e25. Harzhauser, M., Hauffe, T., Holtvoeth, J., Just, J., Leng, M.J., Levkov, Z., Sparks, B.W., West, R.G., 1959. The palaeoecology of the interglacial deposits at Penkman, K., Sadorim, L., Skinner, A., Stelbrink, B., Vogel, H., Wesselingh, F., Histon Road, Cambridge. Eiszeitalter und Gegenwart Quat. Sci. J. 10 (1), Wonik, P., 2016. Scientific drilling projects in ancient lakes: integrating 123e143. geological and biological histories. Glob. Planet. Change 143, 118e151. Sternai, P., Herman, F., Champagnac, J.-D., Fox, M., Salcher, B., Willett, S.D., 2012. Willmann, R., 1981. Evolution, Systematik und stratigraphische Bedeutung der € Preglacial topography of the European Alps. Geology 40, 1067e1070. neogenen Süßwassergastropoden von Rhodos und Kos/Agais.€ Palaeontogr. Abt. Stocchi, P., Spada, G., Cianetti, S., 2005. Isostatic rebound following the Alpine A174,10e235. € deglaciation: impact on the sea level variations and vertical movements in the Wüst, E., 1901. Untersuchungen über das Pliozan€ und das Alteste Pleistozan€ Thür- Mediterranean region. Geophys. J. Int. 162, 137e147. ingens, nordlich€ vom Thüringer Walde und westlich von der Saale. Abh. Strona, G., Fattorini, S., 2014. On the methods to assess significance in nestedness naturforschenden Ges. Halle 23, 19e368. analyses. Theory Biosci. 133 (3e4), 179e186. Zagwijn, W.H., 1989. The Netherlands during the Tertiary and the Quaternary: a case Strona, G., Veech, J.A., 2015. A new measure of ecological network structure based history of coastal lowland evolution. Geol. Mijnb. 68, 107e120.