Erschienen in: Hydrobiologia ; 824 (2018), 1. - S. 291-321 https://dx.doi.org/10.1007/s10750-018-3677-x

Large and deep perialpine lakes: a paleolimnological perspective for the advance of ecosystem science

Monica Tolotti . Nathalie Dubois . Manuela Milan . Marie-Elodie Perga . Dietmar Straile . Andrea Lami

2 Abstract The present paper aims at reviewing with zmax C 100 m and lake area C 10 km , and on 4 general knowledge of large European perialpine lakes shallower perialpine lakes representing hotspots of as provided by sediment studies, and at outlining the extensive neo- and paleo-limnological research. By contribution, from several lines of evidence, of pinpointing temporal and spatial differences in pale- modern paleolimnology in both interpreting past lake olimnological studies conducted in the Alpine coun- ecological evolution and forecasting lake responses to tries, the review identifies knowledge gaps in the future human impacts. A literature survey mainly perialpine area, and shows how sediment-based based on papers published in international journals reconstructions represent a powerful tool, in mutual indexed on ISI-Wos and Scopus from 1975 to April support with limnological surveys, to help predicting 2017 has been conducted on the 20 perialpine lakes future scenarios through the ‘‘past-forward’’ principle, which consists in reconstructing past lake responses to conditions comparable to those to come. The most Guest editors: Nico Salmaso, Orlane Anneville, Dietmar Straile & Pierluigi Viaroli / Large and deep perialpine lakes: recent methodological developments of sediment ecological functions and resource management

M. Tolotti (&) M.-E. Perga Department of Sustainable Agro-ecosystems and Institute of Earth Surface Dynamics, Geopolis, University Bioresources, Research and Innovation Centre (CRI), of Lausanne, Quartier UNIL-Mouline, 1015 Lausanne, Fondazione Edmund Mach (FEM), Via Mach 1, Switzerland 38010 S. Michele all’Adige, Italy e-mail: [email protected] M.-E. Perga CARRTEL, INRA-University Savoie-Mont Blanc, N. Dubois 74203 Thonon-les-bains Cedex, France Geological Institute, Department of Earth Sciences, ETH Zu¨rich, Sonneggstrasse 5, 8092 Zu¨rich, Switzerland A. Lami Istituto per lo Studio degli Ecosistemi, ISE-CNR, Largo N. Dubois V. Tonolli 50, 28922 Verbania, Italy Department of Surface Waters Research and Management, Eawag, U¨ berlandstrasse 133, 8600 Du¨bendorf, Switzerland

M. Milan Á D. Straile Limnological Institute, University of Konstanz, Mainaustrasse 252, 78464 Konstanz, Germany

Konstanzer Online-Publikations-System (KOPS) URL: http://nbn-resolving.de/urn:nbn:de:bsz:352-2-1sugv88nloavf2 292 studies show the potential to cope with the increasing population still represents a major human threat for ecosystem variability induced by climate change, and several LDPLs. Perialpine lakes are still exposed to to produce innovative and crucial information for point-source pollution (e.g. from productive activi- tuning future management and sustainable use of ties), but airborne NOx (Rogora et al., 2006), persistent Alpine waters. organic pollutants (POPs) from agriculture, urban and industrial areas (Guzzella et al., 2018), as well as Keywords Perialpine lakes Á Lake sediments Á ‘‘new’’ pollutants, such as microplastics (Faure et al., Human impact Á Eutrophication Á Paleoclimate Á 2012; Imhof et al., 2013) and drugs inducing antibiotic Global change resistance (Di Cesare et al., 2015), currently represent the most widespread contamination threat. Alien species, which easily spread also in relation to tourist transfer (Gherardi et al., 2008), are becoming a crucial Introduction issue for the conservation of biodiversity and ecosys- tem services of LDPLs. According to the classification by Timms (1992), large Nevertheless, the sensitivity of LDPLs to climate and deep perialpine lakes (LDPLs) are distinguished change currently represents a hot issue due to the tight from the other two major categories of alpine lakes relation existing between LDPL physiography, their (i.e. high alpine and alpine) based on their piedmont peculiar thermal dynamics (i.e. holomixs with com- position and their tectonic-glacial origin, which is plete thermal circulation only after cold and/or windy related to the past dynamics of large Alpine glaciers winters, Ambrosetti et al., 2003) and major atmo- occupying ancient and deep canyon-valleys (Bini spheric circulations (Salmaso et al., 2014). These et al., 1978). factors together represent key drivers of transport LDPLs represent a key water resource for the processes in water and sediments, and of water densely populated Alpine region. For example, the chemistry, nutrient availability, water transparency five largest Italian subalpine lakes represent * 80% and biological dynamics of LDPLs (e.g. Manca et al., of the total Italian freshwater resources (Salmaso & 2000; Straile et al., 2003; Jankowski et al., 2006; Mosello, 2010), while L. Geneva and L. Constance George, 2010; D’Alelio et al., 2011). Water temper- provide drinking water for [ 800,000, respec- ature is increasing in many lakes of the northern tively * 5 million people (CIPEL, Commission hemisphere, including perialpine lakes (O’Reilly internationale pour la protection des eaux du Le´man, et al., 2015), but the evidence that global warming is www.cipel.org, Petri, 2006). LDPLs are extensively more pronounced in mountain regions (Gobiet et al., used also for irrigation and industry, and represent key 2014) is of particular concern, as the LDPL catch- regional resources for tourism, while waters within the ments extend to the glacial Alpine ranges. The LDPL catchments are intensively used for hydropower progressive Alpine deglaciation and the changing production since the 1930s (Wu¨est et al., 2007; Sal- precipitation pattern predicted for the twenty first maso & Mosello, 2010). Concern about the sustain- century (Beniston, 2006; IPCC, 2013; Radic´ et al., ability of these ecosystem services among 2014) have the potential to strongly affect the stakeholders and end-users stimulated the launching of hydrological regime of perialpine lake catchments, long term monitoring programmes of some key and to produce negative ecological and socio-eco- LDPLs already in the 1950/1960s. Intensification of nomic effects related to water scarcity. the research activity at local and regional level took The present context of multiple stressors and place at some sites in the late 1990s (e.g. within the superimposed global warming is challenging the European Long Term Ecological Research Network, sustainable management of LDPLs, especially in LTER, http://www.lter-europe.net), with the objective connection to the insufficient knowledge of the of assessing future vulnerability of perialpine lakes complex interactions between local human impacts and outlining common developing trends within the and climate variability, and of the related lake modern context of multiple and trans-boundary human ecological responses. On the other hand, the present impacts. The results of these studies pinpointed that environmental and socio-economic context of LDPLs nutrient enrichment related to resident and tourist makes the need for better capacity to predict future 293 lake development increasingly urgent. According to paleolimnological research to the knowledge of LDPL the EU Water Framework Directive (European Com- responses to human stressors at secular-scale, and to mission, 2000), current lake ecological quality and the assessment of perialpine lake sensitivity to present restoration targets have to be defined as the degree of and future human impacts. By pinpointing spatial and deviation from good pre-impact quality, i.e. from temporal differences in paleolimnological research ecological reference conditions (European Commis- conducted in the different Alpine countries, this work sion, 2003), which characterize less or not impacted has the additional objective of identifying knowledge reference lakes or past periods in the development of a gaps in the study of lacustrine sediment in the certain lake. However, due to the variety and spatial perialpine area, and of exploring the potential of distribution of human perturbations on lacustrine modern methodological approaches to answer open ecosystems, reference lakes are in reality rare or basic and applied limnological research questions. scarcely representative for the majority of lake According to geography and bedrock geology five categories (Buraschi et al., 2005). Furthermore, high major sub-groups of LDPLs are recognized (Fig. 1): quality long term limnological data are available only (1) Savoyan lakes (F) located on calcareous bedrock for a few key perialpine lakes, such as for Lakes and with waters of middle hardness, (2) lakes of the Lucerne and Constance since the early twentieth Swiss Plateau (CH, D, A) receiving waters form the century (Wolff, 1966; Grim, 1968), L. Geneva since crystalline mountain ranges of the Central Alps, (3) 1957 (Monod et al., 1984), Lakes Maggiore and lakes of the Southern Alps (I, CH) mainly located at Lugano since 1973 (http://www.cipais.org/index.asp). lower altitude (average = 245 m a.s.l., Table 1)in Smaller lakes usually received attention only after calcareous regions and with watershed basins extend- symptoms of cultural eutrophication became evident ing in the crystalline Central Alps, (4) Bavarian in the 1960s–1970s (e.g. Alefs & Mu¨ller, 1999; Gar- (D) and (5) Salzkammergut (A) lakes located at ibaldi et al., 1999). Although the decadal-scale data altitudes between * 400 and 500 m a.s.l. in calcare- are crucial for lake quality control and management, as ous watersheds. The present contribution focuses on well as for understanding ecological processes, this the 20 largest and deepest perialpine lakes, with 2 lack of long temporal perspective hampers the defi- zmax C 100 m and lake area C 10 km (Fig. 1; nition of lake-specific reference conditions and Table 1). Four additional perialpine lakes shallower restoration targets, as well as the prediction of future than 100 m have also been included in the review as lake ecological trends (Bennion et al., 2011). hotspots of extensive limno- and paleolimno-logical Paleolimnology—the reconstruction of past lake research (Table 1). environmental conditions and ecological status based The review of the paleolimnological literature was on the study of proxies stored in lake sediments— mainly based on papers published on international represents the most powerful tool, in mutual comple- journals indexed on Web of Science (ISI-WoS, mentarity with limnological surveys, to close the Thomson Scientific’s Institute for Scientific Informa- knowledge gaps between present and past lake eco- tion, http://www.webofknowledge.com) and Scopus logical conditions. Paleolimnological reconstructions (http://www.scopus.com) from 1975 to April 2017. allow using each lake as a reference site for itself, The databases were searched for each selected lake while the extension of the limnological perspective (keywords: ‘‘lake name’’ AND ‘‘sediment’’ NOT back to pre-impact periods, when lake dynamics were ‘‘geology’’) as a topic (word included at least in title, mainly controlled by climate, can help discriminating abstract, or keywords), and contributions on surface between natural and anthropogenic variability (Mills lake sediment, geology or sedimentology were then et al., 2017). The comparison with lake conditions manually eliminated. Papers published in not indexed during past stages of major climate change (such as the journals and unpublished PhD theses were identified Little Ice Age or the Holocene Climatic Optimum) can through a final search in Google Scholar (https:// help disentangling climate effects from other impacts, scholar.google.com) using the same key words. The and can sustain the prediction of future trends within a paleolimnological achievements are organized in four context of climate change (Battarbee et al., 2012). major thematic sections: sedimentology, past lake The present review paper aims at providing a chemical conditions, past climate variability and past synthetic summary of the contribution of lake ecological conditions. Finally, most recent and 294

Fig. 1 Map of the Alpine region with the large and deep perialpine lakes (LDPLs) considered in this paper, with indication of the geographical latitude and longitude (Greenwich). The lakes included in different, often transnational, districts are indicated with different colours. Green: Savoyan lakes, brown: lakes of the Swiss Plateau, blue: subalpine lakes, black: Bavarian lakes, violet: lakes of the Salzkammergut region

novel paleolimnological approaches potentially con- reliable chronologies and the estimation of sedimen- tributing to the advance of large lake ecosystem sci- tation rates on the basis of varve counts (Lambert & ence are discussed. Hsu¨, 1979; Wolff et al., 2006), magnetic susceptibility (Thompson & Kelts, 1974; Creer et al., 1975) and radioactive isotopes such as 210Pb and 137Cs (Fig. 3; Sedimentology Dominik et al., 1981; Lister et al., 1984; Von Gunten et al., 1987). The majority of these studies were Geophysical and sedimentological studies conducted on lakes of the Swiss Plateau (Fig. 2). Of particular interest is the artificial radioisotope 137Cs, The earliest studies of LDPL sediments aimed at the which attracted the interest of European scientists after physical characterization of deep sediment deposits, the Nuclear Accident of Chernobyl in 1986, when while ecological implications were considered margin- huge amounts of this highly toxic metal isotope and ally. Typical sedimentological approaches were applied other radioactive elements were released in the to the Swiss lakes (Fig. 2;Mu¨ller & Gees, 1970; atmosphere. After the accident, numerous studies Schindler, 1976; Niessen et al., 1992), where Hsu¨ & were conducted all over Europe in order to determine Kelts (1985) first studied sediment turbidites from a dynamics and ranges of atmospheric transport of limno-geological point of view, and to a few subalpine radioactive caesium and its deposition on soils and Italian lakes (Finckh et al., 1984;Binietal.,2007). More aquatic environments (e.g. Santschi et al., 1988). The recent sedimentological studies rely on high-resolution studies conducted on sediments of those perialpine seismic profiling of lake bottom sediments (Mu¨ller, lakes which received higher amounts of Cs fallout due 1999;Becketal.,2001; Schnellmann et al., 2005), and to contingent atmospheric circulation patterns (Irl- aim at studying processes visible on the lake floor weck, 1991; Schuler et al., 1991; Bollho¨fer et al., morphology, such as mass movements and moraine 1994; Putyrskaya et al., 2009) contributed to the ridges (Hilbe & Anselmetti 2014; Hilbe et al., 2016). validation and improvement of the 210Pb based dating of lakes sediment records by pinpointing the sedi- Sediment chronology mentary 137Cs peaks marking 1963 (when strato- spheric testing of nuclear weapons was banned) and Tightly related to sedimentological investigations are 1986, the Chernobyl Accident (Fig. 3). the development of methods for the establishment of Table 1 Geographical position, key morphometric features, current thermal regime and trophic condition of the 20 large and deep perialpine lakes (LDPLs) included in this study (with maximum depth C 100 m and lake area C 10 km2) and of four smaller lakes (not numbered, but indicated by a code), which have been additionally included since they represent key sites for the development of sediment studies on perialpine lakes

N Ac Lakes Countries Altitude L WZmax Zmean Area C. A. Vol tw Mix. T. S. (m a.s.l.) (km) (m) (m) (km2) (km2) (km3) (years)

1 G Geneva (Le´man) F–CH 372 72.0 13.0 310 153 582 7,975 89 11.4 me–ol o–m 2 B Bourget F 232 18.0 3.5 145 80 42 560 3.6 10.0 mo o–m An Annecy F 447 14.6 3.2 82 41 27 251 1.1 n.a. mo o 3 Th Thun CH 558 18.3 3.8 217 135 48 2,404 6.4 1.8 ol o 4 Br Brienz CH 564 14.2 2.8 259 173 30 1,108 5.2 2.6 ol o 5 L Lucerne (Vierwaldsta¨ttersee) CH 434 39.2 3.3 214 104 114 2,124 11.8 3.5 ol o 6 Zu Zug CH 414 14.6 4.3 198 83 38 212 3.2 17.0 me e 7Z Zu¨rich (lower) CH 406 40.6 3.8 136 51 65 1,757 3.4 1.4 ol m 8 Wa Walen CH 419 15.4 2.0 145 105 24 1,037 2.5 1.5 me o 9 C Constance (Bodensee) CH–D–A 539 63.0 14.0 252 101 493 10,900 48.0 4.7 ol o 10 O Orta I 290 13.1 2.5 143 72 18 116 1.3 8.9 mo o 11 M Maggiore I 193 64.4 10.0 370 178 213 6,599 37.5 4.1 ol o 12 Lu Lugano I–CH 271 35.0 4.3 288 171 28 297 4.69 12.4 me m–e 13 Co Como I 198 45.7 4.3 410 154 146 4,508 22.5 4.5 ol o–m 14 I Iseo I 186 25.0 4.4 251 123 62 1,842 7.6 4.1 me m–e 15 Id Idro I 368 8.3 1.9 124 77 11 617 0.9 1.2 me o–m 16 Ga Garda I 65 51.9 17.5 350 133 368 2,290 49.0 26.6 ol o–m Am Ammer D 533 16.2 5.3 81 38 46.6 993 1.8 2.7 mo m 17 S Starnberger D 584 20.2 4.7 128 53 56 315 3.0 21.0 mo o–m Ch Chiem D 518 12.8 6.2 73 25 80 1,399 2.1 1.4 mo m Mo Mondsee A 481 11.0 1.5 68 36 14 247 0.5 1.7 di–mo o–m 18 W Wolfgang A 538 10.3 2.0 114 47 14 123 0.7 3.6 di o 19 A Atter A 469 20.1 3.3 171 85 46 464 3.9 7.1 di o 20 T Traun A 422 12.2 2.9 189 91 26 1,417 2.3 1.0 ol o

Length (L) and width (W) are intended as the maximum dimensions of each lake. Zmax and Zmean = maximum and mean lake depth, respectively. The information reported in table has been collected from the literature cited in the text, data for L. Idro as in Viaroli et al. (2018); data for Mondsee as in Ficker et al. (2017). Numbers for L. Constance refer to Upper Lake Constance

C. A. catchment area, tw estimated retention time, Mix. mixing regime, mo monomictic, di dimictic, ol oligomictic, me meromictic, T. S. trophic status, o oligotrophic, m mesotrophic, o–m oligo–mesotrophic, m–e meso–eutrophic, e eutrophic 295 296

Fig. 2 Total amount, and absolute and percent distribution to the lake districts indicated in Fig. 1, and to eight major (histogram and pie plots, respectively) of sediment studies thematic categories. SA Savoyan lakes, SP Swiss Plateau, SU conducted on the 24 perialpine lakes selected for the present subalpine lakes, BA Bavarian lakes, SK Salzkammergut lakes. contribution (see Fig. 1), as resulting from the literature survey The low number of studies conducted on Bavarian lakes conducted for the period 1975–April 2017. The studies include depends on the fact that Lake Constance (D, CH, A) has been both ISI and not indicized papers and are distributed according considered as geographically belonging to the Swiss Plateau

Catchment processes in the Alpine region (Siegenthaler et al., 1987; Beck, 2009; Strasser et al., 2013), and as a model for Lake catchment processes are affected essentially by: understanding stability of submerged lacustrine slopes (1) internal geodynamics phenomena including earth- (Strupler et al., 2017) and ocean margins in regions of quakes and volcanic eruptions, (2) climate-related high seismic activity (Strasser et al., 2007). In factors, such as the action of meteoric waters and addition, it has been shown that major past earth- winds on rock weathering, soil erosion and transport, quakes in the Alpine region started landslides, which bio-geochemical cycles and land cover (see further induced tsunami-like waves when reaching perialpine down) and (3) human-related activities able to modify lakes. The extensive study of these pre-historical and land cover and hydrology within the lake’s catchment, historical catastrophic events in Swiss and French such as deforestation and land clearance, agriculture, LDPLs (Fig. 2) contributed to highlight the risk for urbanization, water diversion and hydroelectric tsunamis in the perialpine area (Chapron et al., 1996; exploitation (Fig. 4). Schnellmann et al., 2006; Kremer et al., 2012, 2014). The study of effects of casual geodynamic events Not surprisingly, studies aimed at tracking effects on past LDPL conditions, which is tightly related to of past volcanic activity are rare in the Alpine region, the sedimentological approach, puts high attention to with the exception of the studies by Moscariello & the effects of earthquakes. In fact, seismic activity can Costa (1987), Wessels (1998) and Schnellmann (2004) reduce underwater slope stability and induce mass which revealed ash layers (tephras) of the Laacher movements and anomalous accumulations, which in Volcano (Eifel Mountains, Germany) in sediments of turn interfere with the chronology of lake sediment western perialpine lakes during the Late Glacial. records (Chapron et al., 1999; Brauer & Casanova, Similar to many other lakes in fertile European 2001; Fanetti et al., 2008). These mass movement regions (Dubois et al., 2018), the majority of the records were used to reconstruct past seismic activity LDPLs have a long history of human presence, which 297

Fig. 3 Fallout radionuclide concentrations in the cores col- activity and the supporting 226Ra reach equilibrium depth lected from the deepest point (350 m depth) of L. Garda in 2009 at * 35 cm the Garda core, and at * 50 cm in the Lugano and from L. Lugano (Melide, ca. 180 m depth) in 2015. Left, core. Unsupported 210Pb activities, calculated by subtracting central and right panels show, respectively, total 210Pb activity, 226Ra activity from total 210Pb activity, decline irregular with unsupported 210Pb activity, and 137Cs and 241Am concentrations depth in both cores. The sharp dips in unsupported 210Pb versus sediment depth (analyses performed by Handong Yang at activities around 20 cm (L. Garda) and 27 cm (L. Lugano) Ensis Ltd., University College London, UK). The 210Pb method suggest stages of rapid sediment accumulation from floods or relies on the fact that the gas 226Ra produced in the U decay slumpings. The 137Cs activity showed two well-resolved peaks series escapes to the atmosphere where it naturally decays to in both cores, with the deepest one marking the termination of 210Pb (Appleby & Oldfield, 1978). Unsupported 210Pb consists the atmospheric tests of nuclear weapons in the Pacific in 1963, in atmospheric particle-reactive 210Pb attached to aerosol, which and the upper one the Chernobyl Accident in 1986. The are deposited over the lake catchments and incorporated into the shallower depth of the 137Cs peaks in L. Garda reflects the lower sediments. As most lake sediments contain U and 226Ra, 210Pb is sedimentation rate in this less productive lake respect to the also naturally produced in situ (‘‘supported’’ 210Pb). Total 210Pb meso–eutrophic L. Lugano 298

Fig. 4 Schematic representation of a perialpine lake and its re-dissolution) occurring in the lake sediments are shown. The catchment, with indication of major climate and human-related schematic sediment cores indicate the normal sequence of catchment processes, which can directly or indirectly affect lake seasonal biochemical and clastic varvae, as well as perturbations ecological dynamics (drawing by M. Tolotti). Principal physical by volcanic activity (tephras), and turbidites due to major and chemical processes (i.e., sliding, resuspension, bioturbation, hydrological events (floods, slumps) dates back at least to the Neolithic Age (ca. (WWII). During the last century, the establishment of 5900–4500 cal years BP, Menotti, 2004). However, hydroelectric power plants represented, together with impacts of human activities on lake catchments urbanization, one of the major anthropogenic impacts remained negligible for most of the Holocene thanks on LDPL catchments. Between the 1930s and the to the size-related buffering capacity of LDPLs, which 1950s, the hydrological regime of many LDPLs was tends to absorb and minimize moderate external modified due to construction of reservoirs, impound- perturbations. Effects of early human activities, such ments, water diversions and plants for forced water as pile dwellings on lakeshores, agriculture develop- pumping aimed at power production (Wu¨est et al., ment and the related soil clearance, were demonstrated 2007; Lappi, 2008). Reservoirs and impoundment for L. Constance (Ro¨sch, 1993), but especially for decreased the input of suspended material of riverine smaller LDPLs, such as Mondsee since the Late origin to LDPLs (Anselmetti et al., 2007), as was Neolithic (Swierczynski et al. 2013a) and L. Bourget revealed by the increasing proportion of organic since the Bronze Age (Jacob et al., 2009). material deposited in sediments of some lakes (e.g. Human activities increased rapidly since the Indus- Milan et al., 2015). This may erroneously suggest an trial Revolution and at an enhanced velocity since the early increase in lake productivity, while in other economic and demographic boom after World War II lakes, as in L. Brienz, the reduced input of riverine 299 material decreased the allochthonous nutrient input, their occurrence in perialpine lakes is related to and thus inducing the lake’s oligotrophication (Wu¨est exacerbated by nutrient increase (De Candolle, 1825). et al., 2007; Thevenon et al., 2013). Past abundance of cyanobacteria in LDPLs has been usually inferred from concentrations of taxonomically specific subfossil pigments preserved in sediments Past lake chemical conditions (Zu¨llig, 1956, 1989; Guilizzoni et al., 1983; Neukirch, 1990), although different degradation rates related to Natural chemical composition of surface waters both molecular structure and lake environmental largely depends worldwide on the geology of water- conditions can hamper the estimation of original sheds. Nowadays, rivers and lakes receive a great abundance (Leavitt, 1993; Milan et al., 2015). In variety of anthropogenic contaminants, including recent years the quantification of endospore (akinetes) nutrients and numerous non-nutrients pollutants, such formed by Nostocales provided reliable information as heavy metals, organic synthetic chemicals, phar- on lake colonization by cyanobacterial populations maceuticals, hormones or radionuclides. Toxicity, and lake trophic development (Wunderlin et al., 2014; transport, persistence, and accumulation of contami- Salmaso et al., 2015). nants in water, sediments and organisms depend on Remains of other aquatic organisms, such as their intrinsic chemical properties and on complex Cladocera, revealed great potential as qualitative interactions between pollutants and natural lake indicators of past trophic condition of perialpine lakes chemical and biological components, which are still (e.g. Nauwerck, 1988; Hofmann, 1998), but diatoms far from being completely understood (Nellier et al., were widely preferred (e.g. Klee & Schmidt, 1987; 2015). Schmidt, 1991; Alefs & Mu¨ller, 1999; Wessels et al., 1999), due to their ubiquitous abundance and good Eutrophication: reconstructing the evolution preservation in lake sediments, as well as to their of anthropogenic lake nutrient enrichment reliability as trophic indicators (Hall & Smol, 2010). Statistical models for quantitative reconstruction of Paleolimnological studies of perialpine lakes were past total phosphorus (TP), and secondarily of photo- triggered during the 1980s by the symptoms of cultural synthetic pigments, which represent the most widely eutrophication, which became evident in numerous used variables for lake trophic classification (Vollen- temperate lakes of the Alpine region during the 1960s. weider & Kerekes, 1982), developed during the 1980s, Several works explored the possibility to track effects in parallel with tools for inferring lake acidification in of lake nutrient enrichment on lake productivity N-Europe and N-America (Smol, 2008). However, as through the study of sediment aspect (Nipkow, 1920) the direct determination of phosphorus concentration and bio-geochemical indicators, such as the sediment in lake sediment is not reliable due to a set of complex content of organic matter and algal pigments (Ravera chemical interactions (Engstrom & Wight, 1984), & Parise, 1978; Guilizzoni et al., 1982), stable isotopes models aimed at an indirect reconstruction of past lake (Giger et al., 1984), biogenic silica (Schelske et al., TP based on biological proxies, especially subfossil 1987) or lipids (Buchholz et al., 1993). These early diatoms (Birks, 2010), were developed. Sediment eutrophication studies concentrated on lakes that were records from numerous perialpine lakes were used to the main study object of Research Institutes and quantify ecological optima and tolerance of diatom Universities and were considered as reference lakes at species, which were combined with species abun- country level (e.g. Geneva, Zu¨rich, Constance, Mond- dances to develop transfer functions for inferring past see and Maggiore). TP in Alpine and perialpine lakes (Wunsam & As the relation between organisms and water Schmidt, 1995; Lotter et al., 1998). The development nutrient level was already known for long (e.g. of these statistical tools is considered as a sort of Kolkwitz & Marsson, 1908), the studies rapidly ‘‘Rosetta stone’’ (Smol, 2008), as it allowed extending focussed on the use of lacustrine species composition the temporal perspective provided by lake surveys and diversity as qualitative indicators of eutrophica- from decades to centuries. tion symptoms. Cyanobacteria were the first biological Although regional studies are still rare (e.g. Berthon indicators used, in relation to the early recognition that et al., 2013) and no supra-regional integrated study has 300 been conducted yet, the available diatom-based the Italian subalpine lakes have been investigated only reconstructions outline a coherent secular-scale evo- after 2010 (Milan et al., 2015). lution of the lake trophic status in perialpine lakes Furthermore, the quantitative approach to infer past north and south of the Alps. The majority of the lakes lake TP is currently undergoing a stage of critical remained in oligo- to mesotrophic conditions until the revision, as it shows some biases which are mainly late 1940s, while TP levels increased very rapidly in related to the set of ecological and statistical assump- the 1960s in relation to the input of untreated waste tions involved in paleoenvironmental reconstructions waters originating especially from the rapidly expand- (Juggins, 2013). In particular, the models for diatom- ing resident and tourist population during the post-war base lake TP reconstruction show scarce spatial economic boom. The lake nutrient enrichment was replicability in relation to the strong geographical accompanied by the substitution of small oligotrophic connotation of the training sets, and the inclusion of centric diatoms [i.e. Cyclotella spp. (Ku¨tzing) Bre´bis- numerous taxa without significant relations to TP (e.g. son] by colony forming pennate taxa [primarily many benthic TP-tolerant Fragilariaceae). The relation Fragilaria crotonensis Kitton, Asterionella formosa between diatom and TP may be strongly affected or Hassall, Tabellaria flocculosa (Roth) Ku¨tzing], which confounded by secondary variables, such as water prefer mesotrophic conditions (Marchetto & Bet- chemistry, depth and climate conditions (Juggins tinetti, 1995; Wessels et al., 1999; Marchetto et al., et al., 2013). Finally, LDPLs are strongly under- 2004; Berthon et al., 2013; Milan et al., 2015). The represented in the existing European calibration sets. maximum eutrophication stage, which was usually Only four LDPLs (i.e. Ammer, Atter, Como and reached in the 1970/1980s, was characterized by high Garda) are included in the Central European dataset, proportions of Stephanodiscus parvus Stoermer & which was calibrated on 86 lakes south and north of Ha˚kansson and Aulacoseira spp. Thwaites. the Alps (Wunsam & Schmidt, 1995), while the Swiss Paleolimnological reconstructions corroborate and dataset (Lotter et al., 1998) includes only small lakes. underscore the neo-limnological evidence of a hetero- This situation often results in poor estimates of TP geneous trophic development of LDPLs in the last few concentrations measured in the lake water column, or decades, in relation to different timing and success of in the necessity to rely on more general calibration sets restoration measures, catchment features, lake size (such as the Comb-EU TP, Battarbee et al., 2001), or and morphology or local economic issues. Several on sets calibrated to different European regions, as lakes north of the Alps (e.g. Dokulil & Teubner, 2005; reported for example by Milan (2016). Another critical Berthon et al., 2013; Jochimsen et al., 2013) and L. aspect regards the general scarcity of long monitoring Maggiore (Mosello et al., 2010) represent examples of records, which hampers the validation of trophic particularly successful lake restoration, and are now reconstructions based on comparison between paleo- tending to pre-1960s trophic status (Table 1). Other and neo-limnological data. In the Alpine area, this has lakes still show enhanced trophic status due to been possible for Mondsee (Bennion et al., 1995; secondary internal P-load, such as Zu¨rich and Lugano Dokulil & Teubner, 2005), Maggiore (Manca et al., (Lepori & Roberts, 2017), or to incomplete and/or late 2007) and Geneva (Berthon et al., 2013). The relia- restoration measures, such as Iseo and Garda (Salmaso bility of the taphonomic diatoms assemblages repre- & Mosello, 2010; Tolotti, unpublished data). Despite sents a further important issue for reconstructions the general stimulus that the EU FWD provided to based on biological remains. Comparison between sediment studies in Europe since the 2000s (Bennion living and sediment communities aimed at outlining et al., 2011), sediment-based reconstructions of past diagenetic processes has been conducted only in a few lake TP still remain rather heterogeneous for the lakes (Marchetto & Musazzi, 2001; Jankowski & LDPLs. Research concentrated on a few key lakes, Straile, 2003; Berthon et al., 2013). while the definition of reference conditions continues Possibly also in connection to these issues, the to be mainly based on historical limnological data and existing diatom-based transfer functions did not expert judgment. At present, past trophic development undergo any updating process after their development has not yet been reconstructed at secular-scale for in the 1990s, so that they still rely on a taxonomical some Swiss lakes, while sediments of the majority of stand, which is out of date and does not take in account recent taxonomical revisions and new auto-ecological 301 knowledge. As a result, although diatom-based TP suitable trophic indicators are contained in the lake reconstructions still represent a fundamental and sediments (Marchetto & Musazzi, 2001; Guilizzoni common step for sediment investigations, paleolim- et al., 2012). nology is currently moving on towards more compre- Subfossil Cladocera remains have also been suc- hensive and ecological approaches (see below). cessfully used as quantitative indicator of lake trophic Subfossil photosynthetic pigments represent an level. As Daphnia has strong stoichiometric require- alternative proxy for inferring past lake TP in ments for P, changes in its past abundance could be perialpine lakes. Due to higher post-depositional directly related to changes in lake TP level and a degradation rates of pigments relative to diatoms, Daphnia-inferred TP transfer function was developed pigment-inferred TP often underestimates diatom- for the Savoyan LDPLs (Berthon et al., 2013). inferred nutrient levels (Fig. 5), especially in olig- Daphnia-inferred TP has been shown to track early otrophic well-oxygenated lakes (Guilizzoni et al., enrichment in TP below 10 lgPl-1 that was so far 2011). However, pigment-inferred TP values are undetectable through diatom-based methods, but usually sufficiently robust to provide a reliable recon- becomes inefficient for TP concentra- struction of major past lake nutrient trends, and are tions [ 100 lgPl-1 (Bruel et al., 2018). However, especially useful when subfossil diatoms are domi- as the growth of aquatic animals is strongly affected by nated by nutrient-tolerant taxa, or when no other both bottom-up and top-down factors, Cladocera

Fig. 5 Comparison of sediment profiles of lake total phospho- carotenoid concentrations and diatom species composition and rus (TP) concentrations during the twentieth century inferred abundances. The profiles clearly indicate that pigment-inferred based on subfossil diatoms (red) and pigments (blue) in lakes of TP values are useful to reconstruct past lake phosphorus level, decreasing depth, i.e., L. Maggiore (Pallanza Basin, zmax- but tend to underestimate the highest TP values during nutrient * 100 m), L. Garda (shallower Bardolino Basin, zmax- enrichment stage. Pigment-based reconstruction of past TP level = 81 m), and L. Ledro (a small lake located close to L. Garda performs better in shallower lakes, where pigment degradation at 652 m a.s.l., zmax = 49 m). C-TP and DI-TP = lake total during sedimentation may be less pronounced than in deep lakes phosphorus concentration inferred, respectively, from subfossil 302 response to nutrients may be difficult to discriminate classes. As a consequence, most of the recent from the response to fish predations or climate paleolimnological studies on perialpine lakes in variability (Tolotti et al., 2016). Globally, subfossil France and Italy aimed at understanding how climate Cladocera are used to validate diatom-based TP variability modulates lakes response to nutrients reconstructions, and are considered as more powerful (Berthon et al., 2014; Milan et al., 2015; Tolotti, to reveal effects of multiple human impacts on LDPL unpublished data). For instance, Jenny et al. (2016) ecological dynamics and food webs (e.g. Boucherle & showed that if the appearance of bottom hypoxia has Zu¨llig, 1990; Jankowski & Straile, 2003; Manca et al., been triggered by early nutrient enrichment in the first 2007; Perga et al., 2010; Alric et al., 2013). Further- half of the twentieth century in three LDPLs, further more, subfossil Cladocera remain less extensively expansion of the hypoxic volume is now under climate investigated in LDPLs than in smaller productive control. Besides, responses of different pelagic bio- lakes with hypolimnetic anoxia, which ensures better logical compartments to climate warming are condi- remain preservation in the sediments (e.g. Sze- tioned, in magnitude and type, by the local roczyn´ska & Sarmaja-Korjonen, 2007). concentrations in TP (Perga et al., 2015). Milan et al. As lake hypoxia or hypolimnetic anoxia are usually (2017) showed that climate variability represents the caused by enhanced oxygen consumption in lakes primary driver for Cladocera under low nutrient following increases in productivity (Jenny et al., conditions, while the climate effect tends to be 2016), sediment-based reconstructions of past lake overridden under nutrient enrichment conditions. oxygenation provided indirect information on the trophic development of some perialpine lakes partic- Pollution: reconstructing the history of human- ularly affected by deep anoxia, such as L. Zu¨rich driven lake contamination (Naeher et al., 2013), Geneva and Bourget (Giguet- Covex et al., 2010; Jenny et al., 2013) and Lugano Lake anthropogenic contaminants (other than nutri- (Bechtel & Schubert, 2009). As for phosphorus, the ents) can be differentiated in two major groups: metals reconstruction of past lake oxygenation is indirect, and and industrially synthesized chemicals. Metals are based on abiotic or biological (animal) proxies. naturally present in lake waters in small quantities, Besides varve formation and geochemical composi- which originate from physical and chemical weather- tion (Jenny et al., 2013), the ratio Fe:Mn has been ing of the catchment bedrock and reach the lakes particularly used (Naeher et al., 2013), due to the through runoff or atmospheric deposition. Although relation between solubility of these ions and water essential for many metabolic processes, metals redox potential (Engstrom & Wight, 1984). Chirono- become toxic or even lethal when exceeding specific mid head capsules are the preferred animal remains in thresholds, a condition which often occurs for metal the studied LDPLs (Marchetto et al., 2004; Millet contaminants of anthropogenic origin. et al., 2010; Frossard et al., 2013), due to the high First sediment evidence of metals contamination of tolerance of several species to low oxygen concentra- European lakes dates back to the development of tions and to the good preservation of the larval head technologies for extraction of copper * 4000 years capsules in deep sediments (Walker, 2001). Ostracods BC (Mighall et al., 2002), and then of lead since the and Oligochaetes also showed good capability at Roman period (Renberg et al., 2001). To date, few tracking changes in lake oxygenation at millennial records of ancient anthropogenic metal contamination scale (Newrkla & Wijegoonawardana, 1987; Niessen are available for LDPLs, due to the scarcity of et al., 1992). paleolimnological investigations at millennial scales. Climate change can interact with anthropogenic Nevertheless, those sediment records reaching pre- nutrient enrichment in complex ways, and these industrial times show low metal concentrations in interactions may modify the behaviour of lake comparison to the high modern levels of contaminants ecosystems to a point where historically defined related to industrial emissions and fossil fuels, which restoration targets may become difficult or even dramatically increased in the early twentieth century impossible to achieve (Bennion et al., 2011). This (Wessels et al., 1995; Arnaud et al., 2004; Liechti, implies the need of resetting quality/restoration targets 2015). Stable isotopes of lead (208Pb/207Pb and and re-defining boundaries between water quality 206Pb/207Pb) in perialpine lake sediments were 303 particularly useful for the detection of pollution represented a major issue in the Alpine region, only a sources, deposition rates and pre-industrial metal few studies focussed on Hg contamination sources and contamination of lakes (Moor et al., 1996; Kober methodological issues in LDPLs (e.g. Ciceri et al., et al., 1999; Monna et al., 1999), the latter as possibly 2008). related to past mining activity, as observed for L. Recent studies on contamination of perialpine lake Lucerne during the High Middle Age (Thevenon et al., sediments tracked pollution timing and trends (Bogdal 2011). et al., 2008) in order to check the success either of the Industrially synthesized chemicals are usually ban of certain compounds (Becker-van Slooten & defined as POPs, as they are organic, often halo- Tarradellas, 1995), or of remediation strategies, such genated, toxic compounds, which are scarcely soluble as the implementation of wastewater treatment plants in waters but highly volatile, so that they can be (Thevenon & Pote´, 2012; Vignati et al., 2016). Several transported for long distances, persist for long time in of these studies revealed a coherent decrease in the environment and bio-accumulate in the food webs. deposition rates and sediment concentrations of lead Among the variety of POPs, polychlorinated biphe- and related metals since the ban of leaded fuels in nyls (PCBs) and polycyclic aromatic hydrocarbons Europe in the mid-1980s, while DDT and related (PAHs) are particularly relevant due to their large PCBs decreased in lake waters and sediments after diffusion and their significant negative effects on their European ban (79/117/CEE, Council of the human health and other organisms (Lallas, 2001). In European Communities, 1979). On the contrary, comparison to metal contamination, POPs emission in sediment records of other metals and POPs are much the environment is relatively young, as it started variable due to local factors, such as industrialization, worldwide with the massive use of dichloro-diphenyl- urbanization and long range atmospheric transport trichloro-ethane (DDT) as an insecticide, and with the following the major atmospheric circulations (Jung increasing emission of PAHs from gasoline combus- et al., 2008; Poma et al., 2014). Several recent studies tion since the * 1930s. The negative effects of DDT aimed at identifying possible factors responsible for on human and environmental health led to its ban in persisting high level of some POPs in perialpine lakes, most of the industrialized countries in the 1970s, but as in L. Thun (Bogdal et al., 2008, 2010). Naffrechoux the evidence that water and soil contamination was et al. (2015) demonstrated that the different historical steadily increasing in industrialized districts during records of recent PCBs sediment concentrations in the the 1980s and 1990s stimulated studies aimed at three major French perialpine lakes (Geneva, Bourget tracking the contaminant fate in aquatic environments, and Annecy) are related to a combination of different including LDPL sediments. The majority of studies lake catchment and hydrological features, pollution regarded the most impacted LDPLs in Switzerland, sources, as well as to differing dynamics of atmo- France and Italy (Fig. 2, http://www.cipais.org/html/ spheric transport and deposition. Bettinetti et al. lago-maggiore-pubblicazioni.asp; Naffrechoux et al., (2016) recently demonstrated that melting of Alpine 2015; Guzzella et al., 2018). Some studies provided glaciers is contributing to maintain high levels of DDT methodological improvements of extraction and in the sediments of L. Como, a legacy first revealed by detection of heavy metals and POPs (Mu¨ller, 1984; Bogdal et al. (2009) in a small high alpine lake in Arnold et al., 1998), while the majority gathered Switzerland. information on pollutants origin, dispersal and resi- Despite the amount of studies addressing spatial dence in lake ecosystems, where the sediments play an and temporal distribution of sediment contamination important role in sequestration and mobilization pro- in LDPLs, only a few paleolimnological works focus cesses (Wakeham et al., 1980; Czuczwa et al., 1985; on long term effects of pollutants on lake organisms. Wang et al., 1986; Provini et al., 1995; Wessels et al., An exception is represented by L. Orta, Italy, which 1995). For example, these studies demonstrated sig- experienced high levels of metal pollution from local nificant correlations between legacy contaminants of industry since the late 1920s and subsequent acidifi- common origin, such as Cr, Zn, Pb, Cd, Cu (e.g. cation since 1960 (Fig. 6). The effects of pollution on Monticelli et al., 2011) and PAHs from combustion of the lake biota were so dramatic (summarized in Manca fossil fuels, in particular coal (Mu¨ller et al., 1977; & Comoli, 1995) that first wastewater treatment Kober et al., 1999). As Hg contamination never started already in the late 1950s. The lake was then 304

Fig. 6 Age profiles of major contaminants in L. Orta (Italy) 1920s. The Cu-sed profile clearly indicates the persistence of Cu during the twentieth century. Cu-sed and Hg-sed indicate, in the lake sediments also after the termination of industrial respectively, Hg and Cu concentrations measured in a sediment contamination. The pH values dropped since the 1960s due to core collected from the lake in 2007. Other profiles indicate concomitant contamination by ammonium sulphate, (NH4)2SO4 average concentrations recorded in water samples collected and recovered after the lake liming in 1989/1990. Cr, Ni, and Hg since 1925. The Cu profile reflects the contamination since the profiles reflect the relation between contaminants concentration 1930s by a textile factory established on the lake shore in the and water pH limed to mitigate acidification in the late 1980s. Past climate variability Numerous paleolimnological studies tracked the pol- lution and recovery of L. Orta (Guilizzoni & Lami, Ecosystem processes are influenced to varying degrees 1988; Guzzella, 1996; Vignati et al., 2016), but by climate conditions, which change due to a set of especially demonstrated long term pollution-driven natural forcings operating at centennial or millennial changes in species composition and diversity of scale, such as variations in the Earth orbit, solar phytoplankton (Ruggiu et al., 1998; Guilizzoni et al., activity, volcanic emissions and ocean/atmospheric 2001), techamoebes (Asioli et al., 1996), oligochaetes interactions. Although climate directly affects lake (Bonacina et al., 1986), cladocerans (Manca & water temperature, seasonal and annual variability of Comoli, 1995) and rotifers (Piscia et al., the resulting thermal dynamics (i.e. water stability, 2012, 2016). Other studies demonstrated the contam- mixing, ice-cover) are those playing the principal role ination-driven onset of diatom teratology (Ruggiu in modulating lake environmental conditions, as well et al., 1998; Cantonati et al., 2014), and of changes in as chemical and biological processes (Adrian et al., the size distribution of the lake biota (Cattaneo et al., 2009). Moreover, many effects of climate on lake 1998). The sediment studies of L. Orta underscore the ecosystems are mediated by climate-driven hydrolog- knowledge gaps regarding effects of pollutants on the ical variability in the lake catchment and by its lake biota, and envisage the future potential develop- vegetation cover (Leavitt et al., 2009). ment of paleolimnological investigations addressing The influence of human activities on the Earth’s wide range atmospheric contamination of water carbon cycle has been growing so intensively and ecosystems. rapidly during the last * two centuries, i.e. since the 305 beginning of the Industrial Revolution, that humans Lotter, 2005) thanks to the fact that their life cycles are are currently considered the main driver of climate more affected by temperature than that of vegetal variability. In addition, human modification of lake organisms. Among algae, chrysophytes stomatocysts catchments (due to agriculture, deforestation, urban- were successfully used as proxy to infer spring and ization, hydroelectric exploitation) often exacerbates winter temperature only in smaller perialpine and climate-driven catchment processes. This poses the Alpine lakes (Kamenik & Schmidt, 2005; De Jong & necessity to rely on long term climate records in order Kamenik, 2011). However, the relations between to understand both the natural range of climate organisms and temperature are usually not straight- variability and the extent of human impacts on water forward, as organisms simultaneously respond to a ecosystems (Mills et al., 2017). Although meteoro- variety of environmental factors, which are often logical records are usually longer than limnological interconnected besides affected by climate variability. data and of better quality, they are mainly limited to a As a result, organisms-inferred past temperatures are few major cities in Europe and North America and to better in providing insight in climate trends rather than the last ca. 150 years. For example, the HISTALP in absolute values. In addition, some taxonomic database, which includes recorded and statistically groups may have better capacity to track variables extrapolated air temperature and precipitation data for that are only indirectly related to climate, such as the ‘‘Greater Alpine Region’’, covers the period water thermal stratification, oxygenation or chemistry, since * 1850 (Auer et al., 2007). As lakes accumu- rather than water temperature directly. Therefore, late records of past environmental and climatic sediment-based reconstructions of past climate vari- conditions in their sediments, the paleolimnological ability often adopt a multi-proxy approach (Birks & approach can effectively extend information on past Birks, 2006), which involves the coupled study of climate and on direct and indirect effects of climate biotic and abiotic sediment proxies related to climate variability on lake ecosystems. variability. Sediment carbon and silica content, oxy-

gen isotopes in calcite (CaCO3) and silica (SiO2), Direct and indirect reconstruction of paleoclimate organic matter or biological remains (such as lipids, based on lacustrine proxies ostracod shells and diatoms frustules) have been successfully combined to reconstruct past climate In general, LDPLs are characterized by a pronounced variability in lakes Mondsee (Drescher-Schneider & thermal inertia (Straile et al., 2010), which slows and Papesch, 1998), Lugano (Niessen et al., 1992), and smooths effects of temperature changes. However, Constance (Hanisch et al., 2009; Schwalb et al., 2013). increasing lake thermal stability due to temperature As carbonate shells or silicate frustules are secreted increase is responsible for prolonged summer strati- over a short time, their isotopic composition can store fication and reduced winter mixing of LDPLs, which information on past lake environmental conditions. in turn strongly affect nutrient distribution along the The 18O/16O ratio of ostracods and molluscs shell lake water column and plankton growth (e.g. Straile CaCO3 applied to long sediment records spanning et al., 2003; Dokulil, 2013; Salmaso et al., 2014). On over millennia allowed the reconstruction of pale- the other hand, effects of global warming may be otemperatures during the Late Glacial (ca. blurred for temperate lakes at middle to low altitude, 14700–11500 years BP) and the first half of the which are typically subject to multiple stressors often Holocene (ca. 11500–6000 years BP) of some LDPLs prevailing over climate signals. As a consequence, north of the Alps (e.g. Lister, 1988; Von Grafenstein past temperature reconstructions based on sediment et al., 1992, 1994, 1998; Anadon et al., 2006). proxies are relatively scarce for LDPLs. Temperature-inferring based on the oxygen isotopic Subfossil organism remains preserved in lake composition of diatoms frustules has been developed sediments have been used to infer past climate trends more recently, but with promising results for applica- after determining their species optima and tolerance to tion on subfossil records (Crespin et al., 2010). certain climate variables (Birks, 1998). In particular, More recently, Blaga et al. (2013) inferred temper- chironomids, and to a lesser extent Cladocera, pro- atures from L. Lucerne during the last deglaciation vided direct quantitative temperature reconstructions (14600–10600 cal. years BP) using the ‘‘organic along Alpine altitudinal gradients (revised by Heiri & geochemical paleothermometer TEX86’’ (tetraether 306 index of archaeal isoprenoid glycerol dialkyl glycerol development of plankton and fish, and can transport tetraether membrane lipids with 86 carbons, Fig. 7. nutrients and pollutants, which enter the food webs

The L. Lucerne TEX86 paleotemperature record (Leavitt et al., 2009). Due to these cascade effects, reveals remarkable resemblance with the Greenland much effort has been recently dedicated to the study of ice (NGRIP) d18O and Ammer (Germany) ostracod perialpine catchment processes as driven by climate shell d18O records, and suggests that temperature variability. The frequency and intensity of past floods changes in continental Europe were dominated during have received special interest as a proxy of past the last 15,000 years by large-scale reorganizations in climate dynamics. Flood sediment records typically the northern hemispheric climate system. consist of thick sediment layers (turbidites, Fig. 4), which can be discriminated from ‘‘normal’’ sediment Paleoclimate reconstruction based on climate- layers by their texture, geochemical composition and driven catchment processes organism remains, the latter being often scarce due to dilution by clastic material. In addition, flood layers Regional patterns of atmospheric precipitation are can be distinguished from underwater slumps espe- strongly dependent on large-scale climate dynamics cially on the basis of their peculiar geochemical and local physical features, and represent the primary content (e.g. Revel-Rolland et al., 2005; Kremer et al., driver for catchment and lake hydrological variability, 2015). which in turn can control land vegetation, soil erosion, Paleohydrological studies were typically conducted transport and accumulation of allochthonous clastic on long cores spanning over large portion of the and organic material in lakes. These materials can Holocene, or even including records of the Late increase lake water turbidity, thus affecting the Glacial, with the objective to understand natural (i.e.

Fig. 7 Comparison of the TEX86 record (5-pt moving average) from sediments of L. Lucerne (plotted against depth) with the d18O records (5-pt moving average) of the NGRIP ice core (Rasmussen et al., 2006) across the Late Glacial Interstadial, Younger Dryas and onset of the Holocene. TEX86 values were converted into temperature (lower scale) using the lake calibration of Powers et al. (2010). Chronological tie points are provided by the Laacher See Tephra (LST, identified in the magnetic susceptibility record at 752 cm) and a fossil leaf at 650 cm depth. Figure redrawn from Blaga et al. (2013) 307 pre-human impact) climate variability. Studies on with heavily perturbed catchments, where pollen ancient flood records in French LDPLs could demon- analyses could successfully track vegetation and strate the relation between natural climate variability climate changes only during the Late Glacial and the and solar activity (Magny et al., 2010; Czymzik et al., Early Holocene (e.g. Vernet & Favarger, 1982; 2016). Sediments of L. Maggiore provided a detailed Lauterbach et al., 2012). reconstruction of past flood frequency through the Human impacts on the lake catchment occur at a application of an integrated approach combining much shorter time scale than natural climate changes instrumental monitoring data and sediment analyses. and are often more intense, but human- and climate- Microfacies analyses on thin sediment sections com- driven effects are often comparable to each other, as bined to l-XRF element scanning allowed detecting they principally affect hydrology, soil erosion and land even thin flood layers (Ka¨mpf et al., 2012). Long cores vegetation cover. Some recent studies tried to dis- from LDPLs in France (e.g. Chapron et al., criminate catchment changes driven by climate from 2002, 2005; Debret et al., 2010; Arnaud et al., 2012) those caused by pre-historical human activities and in the NE Alps (e.g. Czymzik et al., 2010; (Thevenon & Anselmetti, 2007; Gauthier & Richard, Swierczynski et al., 2013b, Fig. 2) allowed linking 2009; Hanisch et al., 2009), while others aimed at changes in frequency and intensity of runoff events understanding the effects of past hydrological vari- and debris floods to precipitation and glacier fluctu- ability on the pre-historic human settlements around ations during the Holocene. Several of the most recent the LDPLs (e.g. Magny, 2004; Magny et al., 2012; works were carried out within supra-regional projects Swierczynski et al., 2013a). Nevertheless, a holistic (e.g. DecLakes: Decadal Holocene and Late Glacial study approach has progressively developed during variability of the oxygen isotopic composition in recent years in relation to the increasing relevance for precipitation over Europe reconstructed from deep- lake management of combined climate and human- lake sediments), and joined research clusters (e.g. driven catchment processes able to affect lake abiotic PROGRESS: Potsdam Research Cluster for Georisk and biotic responses. Analysis, Environmental Change and Sustainability, REKLIM, Topic 8: Rapid climate change derived from proxy data) aimed at detecting coherent trends in Past lake ecological conditions long term climate variability at European or Alpine level (Lauterbach et al., 2012;Ka¨mpf et al., 2015). Lake ecosystems are simultaneously affected by Past climate variability has been successfully interacting anthropogenic stressors, which can reconstructed also based on sediment records of lake increase the overall vulnerability of lake ecosystems water level related to precipitation or glacial thawing. to external perturbations by making them less resistant However, since sediment signals of water level and less resilient (Dong et al., 2012). Global warming fluctuation may not be straightforward or easy to can interact with almost all anthropogenic impacts recognize, this approach usually relies on combined making environmental problems increasingly com- information from multiple proxies, such as lacustrine plex and trans-boundary, and lake management less terraces indicating past higher lake-level, seismic efficient because of the difficulty in predicting future profiles, sediment particle-size and geochemistry, trends. The necessity of addressing the complexity pollen of terrestrial and aquatic plants (e.g. Magny, posed by interlaced stressors has required a perspec- 2004; Girardclos et al., 2005; Gauthier & Richard, tive change of paleolimnological studies of LDPLs, 2009; Magny et al., 2009). It is important to pinpoint which are progressively focussing on effects of that palynological studies aimed at reconstructing past natural- and human-driven environmental changes climate through the changes in vegetation cover over on features of the lake biota and on ecological the LDPL catchments are quite scarce. In fact, since responses of perialpine lakes. pollen can be transported over long distances, paly- Several of the recent paleoecological studies adopt nological studies are useful to track regional-scale a multi-proxy approach (Birks & Birks, 2006), since changes, but are rarely valuable to reconstruct changes the simultaneous study of different biological indica- within a singular watershed (Bennet & Willis, 2001). tors characterized by different sensitivity towards This aspect is particularly limiting for those LDPLs environmental variables allows outlining different 308 timing and magnitude of ecological responses (as which allow the quantification and identification of shown in Fig. 8), thus increasing both the diagnostic subfossil DNA and RNA. For example, the application potential and the predictive reliability of sediment of molecular techniques to sediment records allowed studies (Bennion et al., 2015; Perga et al., 2015). investigating the development of cyanobacteria pop- The multi-proxy approach provided insight in the ulation in relation to lake trophic and environmental effects of climate change as superimposed over changes in Lakes Bourget (Savichtcheva et al., nutrients in subalpine and Savoyan lakes (Guilizzoni 2011, 2015; Domaizon et al., 2013) and Zu¨rich et al., 2012; Jenny et al., 2014), and allowed discrim- (Monchamp et al., 2016). In a study on 10 perialpine inating the response to climate change and nutrients by lakes, Monchamp et al. (2018) suggested that the different organisms (Fig. 8), such as diatoms (e.g. cyanobacterial communities became more homoge- Berthon et al., 2014; Milan et al., 2015), cladocerans nous across lakes due to raised temperatures strength- (Manca & Comoli, 1995; Alric et al., 2013; Milan ening the thermal stratification, which favoured et al., 2017), chironomids (Frossard et al., 2013) and cyanobacterial taxa able to regulate buoyancy. On ostracods (Namiotko et al., 2015). The comparative the other side, the microsatellite analysis of subfossil study of biological and abiotic (i.e. sediment geo- Cladocera resting eggs allowed reconstructing the chemistry) proxies outlined that lake and catchment invasion history of Daphnia pulicaria Forbes in Lower size can modulate the effects of combined climate L. Constance (Mo¨st et al., 2015). A similar approach variability and human-driven catchment processes using allozymes, applied already in the 1990s, allowed (i.e. hydropower exploitation) on the biota of peri- tracking changes in genetic architecture of Daphnia alpine lakes (e.g. Milan, 2016). spp. in Upper Lake Constance due to nutrient enrich- The multi-proxy approach is putting increasing ment (Weider et al., 1997). These studies suggest that attention to the combination of data from sediment original species composition and genetic architecture studies and limnological surveys, respectively, aiming were not restored after the lake environmental condi- not only at validating sediment-based reconstructions, tions were reestablished after peak eutrophication but also at improving process understanding and during the 1970–1980s (Brede et al., 2009). The prediction potential. Multivariate statistical microsatellite characterization of subfossil Cladocera approaches combining nutrient (either sediment-re- resting eggs from the Savoyan perialpine lakes related constructed or from monitoring records) and climatic hybridization and different evolutive trajectories of factors allow discriminating ecological responses that synoptic Daphnia species with lake nutrient level and can be attributed to local human activities from those change in fish predation pressure (Alric et al., 2016). due to climate change (e.g. Mosello et al., 2010; However, studies using cladoceran resting eggs as a Guilizzoni et al., 2012; Milan et al., 2015). In that tool need to be aware that ephippia production is matter, the varved nature of the sediments of some species-specific and may change in response to LDPLs is a clear asset as it provides the opportunity environmental change (Jankowski & Straile, 2003). for high-resolution dating up to an annual accuracy Sediment studies focussing on organisms produc- (Alric et al., 2013; Frossard et al., 2013; Jenny et al., ing cysts (Cyanobacteria, Chrysophyta) or resting 2013). eggs (Rotifera, Cladocera) can take great advantage Studies addressing organism responses to multiple from resurrection ecology techniques (Kerfoot et al., stressors are increasingly focussing on biogeography 1999), where vital propagules preserved in lake of key lacustrine taxa and on colonization by alien sediments are hatched in order to obtain pure cultures. species. Biodiversity, geographical distribution and These pure lineages can be used for genomic analyses dispersal, evolution and development trajectories of and laboratory experiments with the objective of ostracods were extensively studied in Mondsee investigating adaptation and evolutionary dynamics (Danielopol et al., 2008; Namiotko et al., 2015), while during different stages of environmental change. colonization patterns of Cyanobacteria were recon- Although the potential of combining descriptive and structed for Lakes Geneva (Wunderlin et al., 2014) experimental paleolimnology is not being fully and Garda (Salmaso et al., 2015). These studies benefit exploited yet, it has been extensively applied to from the rapid evolution of the high-throughput investigate the evolutionary response of Cladocera sequencing techniques applied to bulk sediments, and Rotifera to pollutants (Piscia et al., 2015; Sommer 309

et al., 2016; Zweerus et al., 2017), and of Daphnia to confirm the taxonomic identity of the cyanobacterium toxic cyanobacteria (Hairston et al., 1999), as well as Dolichospermum lemmermannii (Richter) Wacklin, to quantify past population densities and to genetically Hoffmann & Koma´rek (Salmaso et al., 2015). 310 b Fig. 8 Compared dynamics of major environmental forcing Swiss LDPLs of contrasting trophic conditions, which and ecological responses in L. Bourget during the period allowed tracking changes in heterotrophic microbial 1850–2010. a TP concentrations as inferred from diatoms (Alric et al., 2013) and Daphnia (Berthon et al., 2013). Subtle changes metabolism in relation to lake nutrient level (Carstens occurred already in the 1920s, with a significant post WWII et al., 2013), or comparing the development of lake acceleration of eutrophication. TP levels are currently getting food webs (Bechtel & Schubert, 2009). close to their initial levels. b Atmospheric temperature anomalies over the study period (HISTALP, Auer et al., 2007). Vertical lines points the threshold across which detected ecological changes are due to TP (vertical green line) and Research gaps and future perspective warming (vertical orange line). Benthic responses include changes in lake hypoxic volumes (c Jenny et al., 2016) and in Although numerous paleolimnological studies of subfossil chironomid communities at maximal (d), intermediate (e) and mid-depths (f), summarized by scores on the first LDPLs exist, the present review puts in evidence principal component of PCA analyses. At greater depths, several spatial and temporal heterogeneities. The main responses to eutrophication occurred 20 years earlier than at objectives of sediment research have been unevenly shallower depths. Pelagic responses include: subfossil diatom distributed in the different countries since the very (g Berthon et al., 2014) and cladoceran communities (i Alric et al., 2013), which are both summarized by scores on the first beginning. Sediment studies were conducted more PCA component, contribution of Synechococcus spp. Na¨geli extensively on LDPLs next to Research Institutes and (Domaizon et al., 2013) and Planktothrix rubescens (Savichtch- Universities, while research topics are distributed eva et al., 2015) to total cyanobacterial sediment DNA (h), and rather heterogeneously according to different aca- reconstructed lake surface CO2 concentrations (j Perga et al., 2016). The responses to eutrophication occurred in the 1920s for demic specializations and local environmental prob- diatoms and CO2, but appeared only in the 1940s, at a higher lems (Fig. 2). The majority of the early studies on lake TP level, for cyanobacteria and cladocerans. The absence of sedimentology and past catchment processes were reversal trajectories for all the studied compartments, except concentrated on lakes of the Swiss Plateau (including diatoms, despite the successful reduction in lake TP level, was interpreted as related to significant direct or indirect effects of the trans-boundary L. Constance), studies on lake climate warming over the last three decades pollution are concentrated on Swiss and subalpine lakes, while reconstruction of paleoclimate and past lake ecological conditions are more numerous for the Savoyan and Swiss lakes. Surprisingly, reconstruction Another innovative paleoecological approach con- of past lake nutrient level received scarcer attention sists in the use of stable isotope composition aimed at (Fig. 2), with the result that information on past lake tracking past changes in the lake food web or carbon trophic status and definition lake reference conditions cycling as affected by human impacts and climate are still to be completed, or updated, for the majority variability. At L. Annecy d15N of sediment organic of the perialpine lake districts, with the exception of matter was shown to be significantly correlated to lake the Savoyan lakes. trophic changes during the last century (Perga et al., Also the focus of sediment studies of perialpine 2010). Changes in carbon and nitrogen stable isotopes lakes evolved over time, moving from the quantifica- have been recently studied in chironomid remains tion of past changes in lake environmental features (head capsules) of Savoyan lakes in order to recon- (e.g. sedimentation rate, water level, temperature) and struct spatial and temporal differences in the contri- impacts (e.g. nutrients, pollutants) towards the under- bution of methanotrophic bacteria to the benthic standing of effects of human-driven environmental secondary production in relation to changes in lake changes and superimposed climate change on lake deep oxygenation (Frossard et al., 2015). The d13C ecological features and functions. These hetero- values of subfossil cladoceran remains were shown to geneities, besides pointing out the necessity to com- quantitatively track changes in the summer CO 2 plete the picture at regional level, indicate that the surface concentrations of LDPLs, showing that nutri- potential of sediment investigations of LDPLs is far ents and climate have considerably modified the C away from being exhausted, but could be further exchanges between perialpine lakes and the atmo- exploited to address modern ecological and manage- sphere over the last century (Perga et al., 2016). A ment issues. further example is the measurement of d15N in bulk Despite the efforts to reduce nutrient inputs to lakes sediment and in hydrolysable sediment amino-acids in from urban and productive effluents, eutrophication 311 still represents the most common water quality response, in relation to local factors, and can hardly be problem for the densely populated and highly produc- extrapolated from one lake to another (Dokulil, 2013). tive areas of the world (Smith & Schindler, 2009), The unexploited potential of sediment studies on which includes the perialpine region. As a conse- LDPLs strongly emerges when considering the recent quence, sediment studies addressing nutrient enrich- methodological developments in paleolimnology. The ment and re-oligotrophication of LDPLs are still multidisciplinary and multi-proxy approach already topical, especially in relation to the crucial need to appears to be indispensable to address the study of understand the role of superimposed climate variabil- multiple stressors within the current context of climate ity in modulating lake response to nutrients. warming. The investigation of stable isotopes in Since present climate conditions are approaching subfossil biological and biochemical remains repre- those of the Holocene Optimum (IPCC, 2013), sents a powerful method to investigate changes in the paleoecological studies of LDPLs at millennial scale lake food webs, from microbes to fishes. New could provide the reconstruction of lake ecological approaches, such as those exploiting the structural conditions during past warmer periods, thus improv- composition of the sediments (e.g. Jenny et al., 2016), ing the prediction of future lake scenarios based on the enable to evaluate the consequence of environmental study of past analogue climate stages. Alpine glaciers changes on lake functioning (e.g. hypoxia, carbon are predicted to strongly retreat, if not completely cycle). disappear, within the next few decades (Radic´ et al., Vegetal and animal resting stages preserved in the 2014). This will substantially impact the hydrological sediment allow the application of experimental pale- regimes of LDPLs, with serious consequences for olimnology to track past changes in biodiversity, to agriculture, hydropower production, drinking water, reconstruct colonization and invasion processes by tourism and navigation. Paleolimnology may support species of interest, and to understand micro-evolu- prediction of future lake trends and a conscious lake tionary trajectories and life strategies of key lacustrine management by revealing LDPL responses to major organisms. stages of glacier reduction and scarce precipitations The study of subfossil genomic material preserved during the Holocene. in lake sediments currently represents one of the most Although numerous LDPLs are directly or indi- promising developments of paleoecology. Although rectly exploited for hydropower production, a system- this approach still needs methodological improve- atic study of the resulting lake changes in hydrology, ments and is prone to degradation of subfossil DNA thermal regime and biodiversity is still missing. and RNA, especially under peculiar chemical condi- Sediment studies can provide information for a direct tions, it already allowed investigating organisms that comparison of lake ecological condition before and do not leave remains in sediments (such as the after the human-driven modification of lake hydro- majority of cyanobacteria and protists). This widens logical regime. the palette of biological information that can be The increasing importance of diffuse and long retrieved through sediment studies. At present the ranging human impacts over lake ecosystems suggests metagenomic approach is mainly aimed at the char- the opportunity to intensify supra-regional sediment acterization and quantification of past lake bacterial studies (which at present are still scarce) in order to populations, but very recent developments are target- outline temporal and spatial coherence/difference ing planktonic unicellular eukaryotes (Capo et al., between LDPLs in relation to environmental and 2015, 2016). This approach has great potential to impact gradients. The adoption of a holistic eco- substantially strengthen the knowledge of past lake regional vision may increase the strength of lake biodiversity and ecological processes through detailed management within the relatively socio-economically information on entire ecosystem compartments. homogeneous Alpine region. Such supra-regional Although regime shifts are considered as typical for comparisons appear to be particularly relevant when shallow lakes (Scheffer, 1998), there is yet some considering that lake biological and ecological evidence that especially benthic and littoral compart- responses to climate change tend to be idiosyncratic, ments have crossed critical tipping points very early in contrast to more coherent physical and chemical during the eutrophication process (at lake TP levels \ 10 lgl-1, Jenny et al., 2016; Bruel et al., 312

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