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Hydrobiologia

, Volume 824, Issue 1, pp 1–32 | Cite as

European large perialpine lakes under anthropogenic pressures and climate change: present status, research gaps and future challenges

  • Nico Salmaso
  • Orlane Anneville
  • Dietmar Straile
  • Pierluigi Viaroli
LARGE AND DEEP PERIALPINE LAKES Review Paper

Abstract

The aim of this review is to introduce and critically comment the main research topics considered in a selection of papers on the European large perialpine lakes (LPL) presented at the XXXIII congress of the International Society of Limnology in 2016. Besides highlighting ongoing research advancements in the LPL, the review provides a critical overview of the scientific information available on the large lake’s ecosystems, identifying a few emerging research topics (e.g., aquatic ‘omics’ and high frequency monitoring). Many limnological investigations are linked to the concept of scientific monitoring, following a “problem solving” approach connected with the management of water resources. Experimental studies and modeling are restricted to specific niches. Overall, the scientific knowledge is quite scattered, showing hot-spots of specialized or integrated research in specific lakes and areas. The advancement of new knowledge in the LPL should rely on a better integration of scientific disciplines using multidisciplinary approaches, and on the continuous adoption of new advanced technologies and tools, contributing, besides basic research, to the next generation monitoring approaches. Finally, the preservation of LPL has to rely on water protection policies addressed towards the sustainable development of both terrestrial and aquatic ecosystems, following the “green” and “blue” infrastructure concepts.

Keywords

Large deep lakes Anthropogenic pressures Climate change Research gaps Research perspectives 

Introduction

The large lakes located in the perialpine region are among the most important world water resources. Besides representing highly frequented and well renowned tourist destinations, these lakes are intensively exploited for water supply in agriculture, industry and for drinking purposes, and for commercial and angling fishing. Hence, these lakes provide critical ecosystem services for the Alpine regions, which have one of the highest gross domestic products (GDP) in Europe (Iammarino et al., 2018). For example, the four largest perialpine lakes in Italy (i.e., Garda, Maggiore, Como, and Iseo) provide 50% of the annual water flow in the Po river, whose catchment alone contributes 40% of Italy’s GDP (Alpine Convention, 2009). It is not surprising how the long historical and cultural tradition characterizing the Alpine region set the stage for the birth of limnology (Egerton, 2014) and for a lively and rich number of long-term investigations on the largest lakes.

In the Large Lake’s book by Tilzer & Serruya (1990), the distinction between large and smaller world’s lakes was set at 500 km2. This limit allowed including 253 of the thousands of lakes in the planet. Of these, only two lakes were located in the Alpine area, i.e., Geneva and Constance. The former, along with the lakes Como, Maggiore and Garda, was also included among the 50 largest lakes by depth, whereas Geneva was the only one included in the 50 largest lakes by volume. If not connected with distinctive functional properties, the criteria used to set a limit distinguishing large and small lakes is however somewhat arbitrary. It is widely recognized that most key ecosystem patterns and processes scale with lake size (Håkanson, 2004; Downing et al., 2006; Nõges et al., 2008; Cael & Seekell, 2016; Woolway et al., 2017b), so different operational limits can be set depending on the focus of investigations and processes examined. For example, to delimit shallow lakes, Scheffer (1998) took into consideration only water bodies that can be largely colonized by macrophytes and that do not stratify for long periods in summer. This way, this category can also include lakes of several square km. Conversely, with a major focus on the ecological quality of water resources and human health, the size typology based on surface area defined in the Water Framework Directive (2000) includes (large) lakes with area greater than 0.5 km2.

In this special issue (SI) we did not establish any strict pre-set limit to distinguish large and small lakes. Nevertheless, based on the contribution of the authors (e.g., Tolotti et al., 2018: Table 1), the lakes included in this SI have surface, depth, and volume ranges between around 10 and > 500 km2, 68 and 410 m, and 0.5 and 89 km3, respectively. These ranges allow suggesting an operational demarcation of “large lake”, which is defined by surface, maximum depth, and volume limits set at > 10 km2, > 50 m, and > 0.5 km3. Therefore, in the perialpine region, with a few exceptions (e.g., Neusiedler See, Austria and Hungary), the large perialpine lakes (LPL) have to share not only high surfaces, but also high water volumes and maximum depths. These physical features have important implications, setting the stage for the hydrology, thermal properties, geochemical and biogeochemical cycles and the biological processes depending on them (Tilzer & Serruya, 1990). The general features of the LPL are summarized in Table 1. Besides the prevalence of the pelagic zone compared to the littoral or bottom zones, a few other distinguishing characteristics are the almost absence of ice during the winter season, the oligomixis of most lakes, and susceptibility to meromixis. These characteristics are dependent on geographical location and long-term climatic changes (Dokulil et al., 2006, 2010; Rempfer et al., 2010; O’Reilly et al., 2015). Further, the shores of the large perialpine lakes are densely populated, often hosting large villages and cities and a large tourist population, especially during summer.
Table 1

Distinguishing features of large and deep lakes compared to shallow lakes

Characteristic

Typical feature

Physiographic and hydrological characteristics

 

 Water retention time

Area and volumes of lakes are large in relation to the watershed area. The lower proportional annual inflow causes a higher theoretical retention time. The actual retention time can be even greater in the deeper layer of oligomictic and meromictic lakes

 Internal water movements

Deeper mixing of surface water layer even during stratification due to increasing wind fetch. Oscillation of water masses

 Horizontal heterogeneities

Presence of physical heterogeneities and forcing over the whole surface and between littoral and pelagic zones

 Heat budget

Large heat storage capacity and low susceptibility to freeze; low probability of complete ice cover

 Spring vertical mixing

Greater susceptibility to oligomixis and meromixis

Biogeochemical cycles

 

 Internal cycling and nutrient retention

Higher internal cycling of organic matter and nutrients and less susceptibility of biogeochemical processes to short-term perturbations. Owing to longer retention times, nutrients remain longer in the lake bottom

 Nutrient removal by settling particles

Nutrients are removed from the trophogenic layers by settling autotrophic particles and organic matter, as well as adsorption on inorganic particles. Sediment resuspension is of lesser importance

 Hypolimnetic storage of nutrients

Hypolimnetic and mixolimnetic waters can store large quantities of nutrients

Trophic structure

 

 Pelagic and benthic communities

Ratio of pelagic to benthic biovolume or production is large

 Horizontal and vertical heterogeneity of biota

Heterogeneous distribution of surface blooms due to physical heterogeneities and gradients, and wind. Heterogeneous vertical distribution of phytoplankton in the trophogenic layer, and prokaryoplankton along vertical oxygen and redox gradients

 Trophic state

Owing to the lower ratio between watershed area and lake volume, nutrient loads are lower and, in the absence of relevant anthropogenic pressures, the general natural condition approaches oligotrophy

 Bloom formation

Presence of surface blooms is possible only during calm weather (and sometimes after storms and rainy days); small breezes can concentrate pelagic blooms along the shores and harbors

 Seasonality in plankton community

Vertical dilution in winter, and light limitation; enhanced growth in spring due to supply of nutrients from the mixed hypolimnion contributes to the high seasonal amplitude of plankton biomass, and species seasonality; sometimes, recurrent annual cyclical patterns are recognizable. Hydrostatic pressure acts as a selective factor (e.g., collapse of gas vesicles in cyanobacteria below, e.g., 100 m; selection of smaller and resistant gas vesicles in deeper lakes)

 Seasonality in benthos

Reduced variability of environmental conditions at the bottom of deep lakes cause lesser variations in the benthic organisms

 Fish

Existence of pelagic fish populations foraging for food

Monitoring

 

 Equipment

Requires larger motor boats and dedicated equipment

 Monitoring

Depending on the research/monitoring objectives, may require a larger number of monitoring stations and sampling depths along the water column. Characteristics of the surface/upper epilimnion can be evaluated by satellite measurements

Management

 

 Recovery from eutrophication

Can be exclusively based on the abatement of external nutrients. Other measures are not/poorly feasible

 Cross-border lakes

The management of large cross-border lakes requires specific agreements between countries and/or regions

The characters listed apply to the deep LPL. Adapted from Tilzer & Serruya (1990)

The aims of this review are: (i) to introduce and critically comment the main research topics considered in a selection of papers on the European large perialpine lakes presented at the XXXIII congress of the International Society of Limnology in 2016 and (ii) to evaluate the state of the art, emerging trends and gaps in knowledge and research, and to assess future research needs and directions in relation to the functionality of these ecosystems and to the most critical traditional and emerging environmental stressors.

The state of knowledge

Physical and chemical limnology

Traditionally, studies of physics, hydrology, chemistry, and plankton of large perialpine lakes contributed to found and foster the modern limnological science. Since the 1960s, there was also a growing number of investigations dealing with water deterioration due to eutrophication, which allowed to implement long-term studies in many lakes, among others lakes Constance (Güde et al., 1998), Geneva (Anneville et al., 2002), Lucerne (Bührer & Ambühl, 2001), Bourget (Jacquet et al., 2005), Maggiore (Mosello & Ruggiu, 1985), Lugano (Barbieri & Mosello, 1992) and Garda (Gerletti, 1974). In most LPL, the eutrophication peaks were generally reached between the late 1960s and early 1980s. Since then, the measures systematically adopted to reduce nutrient loads (mainly phosphorus) caused a progressive decline of nutrient concentrations, in some lakes—but not in all—approaching phosphorus concentrations typical for oligotrophic water bodies (Mosello et al., 1997; Massol et al., 2007; Salmaso et al., 2007; Jochimsen et al., 2013; Fastner et al., 2016; Rogora et al., 2018).

Since the late 1900s, a significant and growing number of limnological studies investigated the long-term water temperature changes in the large perialpine lakes. The interest was fostered by the concerns raised by several studies carried out at a global level, which documented a progressive temperature rise (Houghton et al., 1990), and by the growing number of evidences of the impact of global warming on ecosystems (Tegart et al., 1990).

The first wider and comprehensive investigations documented a clear overall increase by about 0.1–0.2°C per decade in the hypolimnetic temperatures in a group of LPL and deep lakes in Northern Europe (Dokulil et al., 2006). These changes were supported by a number of studies carried out on single lakes (e.g., Livingstone, 2003; Straile et al., 2003a; Gillet & Quétin, 2006) or at wider scale in the perialpine area (Ambrosetti & Barbanti, 1999; Salmaso & Mosello, 2010; Woolway et al., 2017a). In a synoptic study based on the long term temperature analysis of the surface waters of 235 globally distributed lakes, the warming trend documented in a few LPL between 1985/1991 and 2009 was coherent with the overall increasing trends found at the global level (O’Reilly et al., 2015; Sharma et al., 2015). Coherently with the predictions of global warming trends (IPCC, 2015), the most recent investigations in the southern perialpine region confirmed the tendency of the large lakes to warm (Pareeth et al., 2017). The maximum water temperatures observed below 100 m depth in Lake Garda between 2015 and 2016 were the highest temperatures ever measured since the beginning of modern limnological observations (Salmaso et al., 2018b).

Besides the analyses of long-term trends, some studies also investigated the role of extreme climate events such as summer heat waves (Jankowski et al., 2006; Anneville et al., 2010; Dokulil et al., 2010; Gallina et al., 2011; Bergkemper & Weisse, 2018) or extremely warm winters (Rempfer et al., 2010; Straile et al., 2010) on characteristics of LPL. These analyses suggest different susceptibilities to extreme events due to e.g., differences in trophic state (Anneville et al., 2010) or lake morphology (Dokulil et al., 2010), but also that consequences of extreme events in LPL likely will differ from consequences of continuous warming due to the slow response of these large and deep lakes (Straile et al., 2010).

In deep lakes, the increase of water temperatures and intensification of thermal stratification cause a reduction in the intensity of winter and spring vertical deep mixing processes. The reduction in the extent of the mixing layer has important consequences on the depletion of oxygen in deep hypolimnetic waters and nutrient supply to the trophogenic layers. Using a modeling approach, Peeters et al. (2002) showed an increase in thermal stability in Lake Zurich in response to temperature rise scenarios, with a reduction in the frequency of complete mixing episodes. The higher vertical temperature gradients induced by warming in the lakes Irrsee, Mondsee and Hallstätter (Salzkammergut lake district, Austria), caused a significant prolongation of the stratification period (by between 28 and 37 days), expanding seasonal hypoxia and anoxia, and increasing phosphorus concentrations in bottom-water layers (Ficker et al., 2017). The effects of a persistent stratification of the water column (meromixis) can lead to a permanent hypoxia and anoxia in the deeper layers, and accumulation of nutrients and reduced compounds, as in the case of lakes Lugano, Iseo and Idro (Barbieri & Mosello, 1992; Garibaldi et al., 1997, 1999; Rogora et al., 2018). In Lake Idro, the meromixis was favored by the geographical position of the lake, which is engraved in a narrow valley, and by the effects of warming and solutes, which induced a density stratification of the water column (Viaroli et al., 2018). An important role in the stabilization of meromixis was supposed to depend on the supply of calcium and magnesium sulfate from groundwater springs. The stratification became progressively stronger due to the increasing eutrophication that, enhancing primary productivity, stimulated calcite precipitation in the trophogenic layer, and successive deposition and dissolution in the monimolimnion (Garibaldi et al., 1997). Paradoxically, the establishment of meromixis, circumventing the mixing of the nutrient rich monimolimnion with the trophogenic layer, contributes to decrease the trophic state of the surface waters. In this regard, in mero- and oligomictic lakes, Salmaso et al. (2003b) distinguished between potential and observed trophic status, which were determined by the overall content of nutrients in the water column, and by the actual nutrients made available by mixing processes in the trophogenic layers, respectively (Fig. 1).
Fig. 1

Temporal variations in observed (dashed line) and potential (continuous line) trophic status in (A) oligomictic and (B) meromictic large and deep lakes. In oligomictic lakes, potential and observed trophic status will coincide during periods of complete mixing and vertical homogenization of nutrients (blue arrows). In meromictic lakes, phosphorus is trapped in the monimolimnion and cannot be exchanged with the mixolimnion; in the absence of vertical mixing, diffusive fluxes upwards can be negligible. The two examples assume a progressive decrease in trophic status, mostly determined by the content of nutrients (principally P) in the water column. In holomictic lakes, observed and potential trophic status will tend to coincide.

Adapted from Salmaso et al. (2003b)

The consistent long-term increase of water temperatures during the winter period in many LPL is characterized by large interannual variations strongly related to the variability in winter air temperatures. In many lakes located in the northern perialpine regions and in Central and Northern Europe, the interannual variations have been shown to be significantly linked to the winter (December–March) North Atlantic Oscillation (NAODM) (Straile et al., 2003b; George, 2010). Conversely, in the large lakes south of the Alps, the interannual temperature fluctuations are mainly linked to a different teleconnection index, i.e., the winter (December-February) East Atlantic (EADF) pattern (Salmaso, 2012; Salmaso & Cerasino, 2012; Salmaso et al., 2014, 2018b; Rogora et al., 2018). In both cases, years with higher/positive NAODM and EADF values are associated to warm/mild winters and to the persistence of water temperature gradients that impede a complete vertical mixing due to incomplete cooling of the water column. In turn, this causes an incomplete upward mixing of nutrients, which accumulate in the hypolimnion. Conversely, during the lower/negative phase, NAODM and EADF are associated with more extended mixing or complete overturn events, and higher supply of nutrients to the trophogenic layers. The year-to-year fluctuations in the teleconnection indices and winter air temperatures trigger complex cascade events that have a strong impact on the biological communities (Supplemental Fig. 1) (Anneville et al., 2002; Straile et al., 2003a, 2003b; Molinero et al., 2007; George, 2010; Salmaso & Cerasino, 2012; Manca et al., 2014). The impact of the large-scale atmospheric patterns on the lakes Lugano and Garda have been further addressed and updated in this SI. In Lake Lugano, the effects of negative EA phases and/or cold winters on primary producers were mediated by the size of the two sub-basins of the lake (deep and shallow) (Lepori et al., 2018a), and by grazing of herbivores (Lepori et al., 2018b). In Lake Garda, recent results (Salmaso et al., 2018b) confirmed the cascading effects triggered by the higher/lower EADF phases on mixing, total phosphorus (TP) supply and development of cyanobacteria and diatoms found in previous works (Salmaso & Cerasino, 2012). The essential role of vertical mixing in the control of productivity in the LPL has been recently confirmed also in Lake Zurich (Yankova et al., 2017). Repeated lack (1977) and complete stop (2013) of holomixis caused severe epilimnetic phosphorus depletions and absence of phytoplankton spring blooms. On the other hand, reduced winter mixing was suggested to result in larger summer blooms of Planktothrix rubescens (De Candolle ex Gomont) Anagnostidis & Komàrek in the same lake, presumably due to less damage of Planktothrix gas vesicles in winters with reduced deep-water mixing (Posch et al., 2012).

The decrease of water temperatures and frequency of more extended or full mixing episodes in lakes located at the northern and southern side of the Alps has been associated to the persistence of more or less long negative phases in both NAODM and EADF, respectively; (Straile et al., 2003a; Dokulil et al., 2006; Salmaso et al., 2014, 2018b). The analyses of the long-term data available demonstrated that these two teleconnection indices are actually characterized by a tendency to a shift towards positive phases (Fig. 2), allowing to hypothesize a more complex connection between lake mixing intensity and global warming, which would be mediated by large scale atmospheric circulation patterns over the Atlantic area and the European continent/NW Africa. In the short term, this would lead to an improvement in the quality of surface waters, especially in lakes between oligo-mesotrophy and eutrophy, decreasing the supply of nutrients to the trophogenic layers (Supplemental Fig. 1). In the long term, however, the risk of triggering longer meromictic phases or continuous meromixis would increase. The occurrence of complete mixing after a prolonged period of meromixis was demonstrated to have important or even dramatic effects due to e.g., the sudden drop in oxygen concentrations and fish kill in the surface waters of Lake Lugano (CIPAIS, 2006), or the marked increase of nutrients and phytoplankton in surface layers of Lake Iseo (Salmaso et al., 2003b).
Fig. 2

Long-term changes of the mean winter values of the (A) East Atlantic pattern (from December to February, EADF) and North Atlantic Oscillation (from December to March, NAODM) from 1951 to 2018. The years refer to the months of January and February/March, e.g., the 1951 EADF average includes the values recorded in December 1950, and January and February 1951. The blue curve and the dashed-green lines indicate the LOESS smoothing and the linear trend (Sen’s slope), respectively. Annual increase values (Sen’s slopes) of EADF and NAODM are 0.023 and 0.019, respectively (P < 0.001). EA and NAO values were obtained from NOAA-CPC (www.cpc.ncep.noaa.gov). Methods to estimate trends are described in (Salmaso et al., 2018b). (A) modified and updated from (Salmaso et al., 2018b)

Besides the numerous works dealing with nutrients and eutrophication, a few papers focused on specific aspects of lake’s chemistry, including the analysis of water chemistry parameters of photochemical significance in lakes Iseo, Garda, Geneva and Piburger See (Minella et al., 2011, 2016). Moreover, confirming a tendency documented in the European Alpine area (Müller & Gächter, 2012; Zobrist et al., 2018) and in many other regions worldwide (Dugan et al., 2017; Kaushal et al., 2018), the increasing trends in chloride and sodium in lakes Maggiore, Lugano, Como, Iseo and Garda was substantiated by Rogora et al. (2015). A brief account on geochemistry investigations can be found in Salmaso & Mosello (2010) and references therein.

Compared to the traditional scientific monitoring and statistical assessment, the numerical applications analyzing the thermal regime and water movements in the LPL have appeared successively, since the 1990s. At the northern border of the Alps, modeling approaches to simulate water temperature and thermal structure dynamics were applied, e.g., in lakes Constance (Hollan et al., 1990), Geneva (Perroud et al., 2009; Soulignac et al., 2018), Zürich (Peeters et al., 2002), Ammersee (Weinberger & Vetter, 2012), and Bourget (Vinçon-Leite et al., 2014). These studies contributed to better identify the forcing factors of the observed temporal variability (Schmid & Köster, 2016), whereas applications at the southern border of the Alps were less numerous (e.g., Piccolroaz, 2016). A more recent interest in the evaluation of future susceptibility of the lake thermal structure to the overall effects of different climate change scenarios stimulated the application of several 1D and 3D modeling approaches. At the northern side of the Alps, simulations of long-term changes were carried out, e.g., in lakes Annecy and Ammersee (Danis et al., 2004), Geneva (Perroud & Goyette, 2010), and Constance (Wahl & Peeters, 2014), whereas in the southern LPL, simulations were carried out in lakes Iseo (Valerio et al., 2015) and Maggiore (Fenocchi et al., 2018). Depending on the lake size and climate change scenarios adopted, the results showed an overall tendency of lakes to warm and to reduce the extent of vertical mixing in the next decades, with important effects on the degree of oxygenation in the hypolimnetic waters (Schwefel et al., 2016). On shorter time scales and using three-dimensional hydrodynamic models including Coriolis effect, Pilotti et al. (2018) highlighted the importance of Earth rotation on the inflow of the main tributaries and oxygen distribution in Lake Iseo.

Owing to the necessity and difficulty to adapt the models and parameters to the dominant species, the application of coupled physical and ecological models to simulate and predict biogeochemical processes and biotic assemblages was much less frequent (e.g., Omlin et al., 2001; Rinke et al., 2009; Dietzel et al., 2013; Kerimoglu et al., 2013, 2017; Frassl et al., 2014; Schlabing et al., 2014).

Phytoplankton, including oxygenic photosynthetic cyanobacteria, and zooplankton

Along with the physical and chemical investigations, the studies of the planktonic communities in the LPL contributed to open several research lines mainly focused on taxonomy and ecology. The interest for phytoplankton, including cyanobacteria, was fostered by its high biodiversity and capability to adapt to a wide variety of environmental conditions, so much as to represent one of the most adopted biological model used to test basic ecological theories (Tilman, 1977; Sommer et al., 1993; Padisák, 2004). Further, different species and groups of phytoplankton are differently selected along trophic (and other environmental) gradients, representing useful biological elements to be used in the assessment of water quality.

The contributions on phytoplankton presented in this SI well exemplify the importance and significance of this component in ecological studies and bioindication. Using a Bayesian approach and wavelet analysis, Anneville et al. (2018) showed how the decrease in phosphorus concentrations in Lake Geneva appeared to play a major role in the inter-annual replacement of species assemblages and how seasonal periodicity in some species could be affected by changes in large zooplankters. The impact of extreme meteorological events on phytoplankton of Lake Maggiore was the focus of the contribution by Morabito et al. (2018b). Among the algal groups, a positive relationship between precipitation and phosphorus was found, indicating an enrichment of nutrients related to runoff on short-term temporal scales (weeks). Among phytoplankton groups, cyanobacteria showed the strongest relationship with precipitation, supporting the hypothesis of a close link between meteorological events at short time scale and the stimulation of phytoplankton growth in summer, when epilimnetic waters are usually nutrient depleted (Callieri et al., 2014). The importance of the effects of short term meteorological events (heavy rain) and seasonal climatic characteristics (heat waves) on phytoplankton, and the implications for water quality assessment, were the object of the work by Bergkemper & Weisse (2018). The authors showed how many short-term phytoplankton changes could be missed by adopting the low-frequency sampling required by the EU Water Framework Directive (WFD). In particular, the data collected in Lake Mondsee allowed to associate heat wave and heavy rain episodes with species-specific changes, including an increase of chlorophytes and potentially toxic cyanobacteria (P. rubescens) during the heat wave. The impact of oligotrophication and interannual climatic changes on the phytoplankton of Lake Garda was analyzed by Salmaso et al. (2018b). The long-term data showed a strong impact of mixing dynamics and spring epilimnetic TP supply mediated by EADF. Specifically, the reduction of nutrient loadings to the lake and the decrease in the frequency of deep mixing events connected with higher EADF phases caused a reduction of cyanobacteria (especially the microcystins producer P. rubescens), and an increase of mixotrophic species (see also below).

The availability of numerous data collected during long-term scientific studies fostered the cooperation between research groups and/or the comparative analysis of the available phytoplankton collected in several LPL (Morabito et al., 2018a). Synchrony in phytoplankton changes was detected in five LPL at the northern side of the Alps (Anneville et al., 2004, 2005). During the examined period (1970–1990s), the lakes Geneva, Constance, Walen and Lower and Upper Zurich showed a clear reduction of phosphorus and tendency to oligotrophication. Despite differing absolute P-concentrations and local seasonal specific assemblages, the statistical analyses identified long-term changes in phytoplankton composition occurring coherently in all lakes. Phytoplankton species favored by oligotrophication included mixotrophic species (e.g., Dinobryon, Ceratium) and/or species indicative of oligo-mesotrophic conditions (e.g., Cyclotella). Furthermore, in some lakes that were recovering from eutrophic to mesotrophic states, long-term changes in phytoplankton communities were characterized by the increase of unexpected large species such as Planktothrix rubescens and Mougeotia gracillima (Hassall) Wittrock, i.e., low light tolerant species adapted to (oligo-)mesotrophic conditions (Tapolczai et al., 2015). In Lake Geneva, the change towards a community dominated by low light tolerant species came with the deepening of the chlorophyll-a maximum (Anneville & Leboulanger, 2001) and the occurrence of more frequent deep chlorophyll-a maxima associated with metalimnic populations. Finally, coherence between lakes was detected even when biomasses fluctuated asynchronously, suggesting that phytoplankton community composition can be considered a more sensitive proxy of the effects of regional-scale processes than biomass (Anneville et al., 2005). In the largest lakes at the southern border of the Alps, the communities were characterized by similar assemblages, but with important differences due to the strong development or presence of Aphanizomenon flosaquae Ralfs ex Bornet & Flahault in lakes Lugano and Maggiore, respectively, and the occurrence of oligotrophic blooms of Dolichospermum lemmermannii (Richter) P.Wacklin, L.Hoffmann & J.Komárek in lakes Garda, Iseo, Como and Maggiore (Salmaso et al., 2003a; Salmaso & Mosello, 2010). Further, Lake Lugano differed from other southern LPL due to the absence of Tychonema bourrellyi (J.W.G.Lund) Anagnostidis & Komárek, a recent dominant cyanobacterium able to produce anatoxin-a (ATX-a) (Salmaso et al., 2016). The results obtained within the framework of the investigations carried out in the 1990s and 2000s in the southern LPL were used to propose new ecological indices based on phytoplankton, with applicability to WFD (Salmaso et al., 2006). Nevertheless, as shown by Kaiblinger et al. (2009), phytoplankton indices alone may not be sensitive enough, confirming the need to take into account other biological elements, such as fish, zooplankton, macrophytes, periphytic diatoms, and macrozoobenthos, partially suggested by the WFD.

The potential greater development of cyanobacteria under future warming scenario was further highlighted in a comprehensive long-term (1970–2000s) investigation by Gallina et al. (2011, 2013). Extreme heat waves events were associated with high cyanobacterial biomass, whereas extreme cold events were characterized by low biomass. Besides increasing cyanotoxins and impairing water quality (Mantzouki et al., 2018), the increase of large filamentous and colonial cyanobacteria decreases dramatically the fraction of edible algae and energy transfer, though the measured effects were shown to depend on zooplankton specific responses in diverse cyanobacterial communities (Urrutia-Cordero et al., 2016). Nevertheless, changes in water temperature and stratification have effects over the whole food-web and specific feeding strategies (Ullah et al., 2018). A concurrent effect of increasing water temperatures and decreasing nutrients was considered beneficial for the development of flagellated mixotrophs in Lake Garda (Salmaso et al., 2018b). Higher temperatures might boost the rates of bacterivory in mixotrophic flagellates (Wilken et al., 2018), while the decrease of phosphorus and nitrogen can increase the growth of algae able to rely on multiple sources of nutrients and food.

In the LPL, zooplankton was the object of numerous studies mainly focused on the characteristics of food-webs and impact of eutrophication, oligotrophication and climatic fluctuations (e.g., de Bernardi & Giussani, 1975; Balvay et al., 1984; Einsle, 1988; Güde, 1988; De Bernardi et al., 1989; Nauwerck, 1991; Angeli et al., 1995; Straile & Geller, 1998a, b; Salmaso & Naselli-Flores, 1999; Molinero et al., 2006; Anneville et al., 2007, 2010; Straile, 2015). These studies showed that the crustacean zooplankton was strongly affected by eutrophication resulting in striking dominance shifts, extinction of species and invasion of taxa better adapted to eutrophic conditions (Straile & Geller, 1998b). With oligotrophication, changes were partially reversible as e.g., some species which went extinct were able to re-establish (Stich, 2004). As oligotrophication in most LPL occurred more or less synchronous with recent warming, it is still a major issue to disentangle effects of these two drivers on zooplankton. Previous work, e.g., Seebens et al. (2007) as well as work in this issue (Lepori et al., 2018b), suggests that effects of both drivers on zooplankton will be season-specific and that also indirect effects will be involved.

Since temperature increases in the epilimnion can influence life cycle, growth and feeding rates of zooplankton species (Schindler, 2001), warming can induce phenological alterations and decoupling of the growth phases of prey and predator populations. Phenological changes may deeply influence planktonic food webs, possibly resulting in a decrease of energy transfer efficiency and, ultimately, a loss of ecosystem productivity (Manca & DeMott, 2009). Conversely, changes in phenology may sometimes improve the temporal match between predators and preys, as it was observed in Lake Geneva where the climate-induced better match between spring zooplankton growth and whitefish (Coregonus lavaretus L.) larvae hatching contributed to the increase in whitefish yield (Anneville et al., 2017). There are also species with life cycles adapted to large seasonal variability of their food sources and which are, consequently, able to shift e.g., their reproductive period with climate induced advances of the phytoplankton spring bloom (Seebens et al., 2009). Recent modeling studies for Lake Constance additionally suggest that no strong mismatches should be expected with seasonally homogenous warming, but only when warming will be seasonally heterogeneous (Straile et al., 2015). Signals of possible effects of temperature increase on trophic status were detected in Lake Maggiore in the hot spring–summer 2003, when the zooplankton community was typical of mesotrophic conditions, although nutrient concentrations were below the threshold for oligotrophy (Visconti et al., 2008).

More recently, a number of studies demonstrated the efficacy of stable isotope analysis (SIA) to define ecological roles of freshwater zooplankton, space and time changes in trophic links between organisms, and functional diversity in lakes (Perga & Gerdeaux, 2006; Leoni, 2017; Visconti et al., 2018). Further, the role of zooplankton as vector of microcystin to whitefish in Lake Hallwil was examined by Sotton et al. (2014).

Diversity and ecology of bacteria, including cyanobacteria, and archaea

During the last decade, microbial ecology experienced the greatest progresses fostered by the development and adoption of new technologies, in particular those linked to the advancement of ‘omics’ domains. This revolution is also affecting the study of microbial communities in the LPL.

Traditionally, a number of seminal papers dealing with the constituents of the microbial loop (Weisse et al., 1990; Callieri & Heinimaa, 1997) focused on heterotrophic (HPP) and autotrophic (APP) picoplankton (Callieri et al., 1995, 2012) mostly examined by epifluorescence techniques. Further, in Lake Maggiore, using traditional culture-independent approaches, Denaturing Gradient Gel Electrophoresis (DGGE) techniques allowed to identify different ecotypes with different photosynthetic characteristics and seasonal occurrence patterns (Callieri et al., 2007). Sequencing of the most prominent gel bands allowed identifying different Synechococcus strains. In general, results were consistent with the coexistence of different ecotypes along the water column, rapidly acclimating and performing differently in the microhabitats. Using fingerprinting and cloning-sequencing, Pollet et al. (2011) identified a strong spatial and seasonal variations of Planctomycetes in lakes Annecy and Bourget linked to environmental conditions and mostly due to a small number of dominant phylotypes. In Lake Bourget, studies of the phylum Verrucomicrobia with multiple approaches (qPCR and cloning) identified 71 operational taxonomic unit (OTUs) belonging to particle-associated bacteria and 59 OTUs part of the free-living fraction, therefore providing strong evidence for the importance of substrate-attached bacteria (Parveen et al., 2013). The distribution of Thaumarchaeota in the deep hypolimnion of Lake Maggiore and in a wider number of large southern perialpine lakes was formerly studied with culture independent approaches and CARD-FISH (Coci et al., 2015; Callieri et al., 2016). The first comprehensive account of the diversity of major bacterial groups in the southern LPL using CARD-FISH technique has been provided in this SI by Hernández-Avilés et al. (2018). The study showed a common pattern, with a first appearance of the large sized “opportunistic” bacteria in spring, followed in summer by ultramicrobacteria, less vulnerable to predation. Significant correlations between a few phytoplankton and bacterial groups suggested the existence of functional interactions between photosynthetic prokaryotes/eukaryotes and heterotrophic prokaryotes. Conversely, using a culture-dependent approach, Callieri et al. (2013) studied the phylogenetic diversity of picocyanobacteria isolated from a few southern LPL and several other water bodies in Mexico and Argentina. Most of the isolates belonged to Synechococcus and Cyanobium clades, i.e., the same as those successively identified by the application of high throughput sequencing (HTS) techniques (see below). Similar studies allowed discovering new bacterial species, including Limnohabitans (Hahn et al., 2010), a new genus found in Lake Mondsee and successively identified also in other LPL.

A challenging issue is represented by the risk for human health caused by induced antibiotic resistance in lake bacteria. As shown in this SI, the presence of antibiotic resistance genes (ARGs) within the resident microbiome of lakes Geneva and Maggiore was correlated with anthropogenic impacts (Eckert et al., 2018). Nevertheless, abiotic factors and the food-web structure were influential in controlling the survival of specific bacterial genotypes and thus the resistance genes they harbor.

Besides ecological investigations of single species, e.g., P. rubescens (Posch et al., 2012; Jacquet et al., 2014), the study of isolated and cultured toxigenic and non-toxigenic cyanobacteria strains in a few LPL provided relevant information not only for the risk assessment and management of lakes, but also for the taxonomy, autecology, physiology, metabolomics, and toxicology of the dominant cyanobacteria. These culture-dependent approaches were used to study the distribution of toxigenic and non-toxigenic strains of Planktothrix spp. (Kurmayer & Gumpenberger, 2006; Kurmayer et al., 2011; Ostermaier et al., 2012; D’Alelio et al., 2013; Salmaso et al., 2016), the diversity and selection of genes encoding gas-vesicles of greater strength in populations of P. rubescens living in the deeper lakes (D’Alelio et al., 2011), and the biogeography of potentially toxic populations. As for this latter topic, numerous populations of D. lemmermannii isolated in Europe along a North–South gradient were shown to be able to express toxicity only in the Central and Northern regions (Salmaso et al., 2015; Capelli et al., 2017). The increasing development of T. bourrellyi to detectable abundances was recognized for the first time in Lake Maggiore using microscopic determinations (CNR-ISE Sede di Verbania, 2007), and in Lake Garda using a polyphasic approach (Shams et al., 2015). Successively, besides Lake Garda, the presence of ATX-a producing populations of T. bourrellyi was proved also in lakes Iseo, Como and Maggiore using genetic, phylogenetic and metabolomic profiling approaches (Salmaso et al., 2016). The expansion of this toxigenic species in other LPL north of the Alps (and in other smaller perialpine lakes) is still awaiting confirmation. If not linked to any other known cyanobacterial producer (Bernard et al., 2017), the detection of ATX-a in environmental samples could suggest to test explicitly samples (Kurmayer et al., 2017) for the potential presence of toxigenic populations of T. bourrellyi. The draft genome sequence of a strain of T. bourrellyi isolated from Lake Garda was analyzed and described by Pinto et al. (2017).

Owing to the problems caused by the presence of toxigenic cyanobacteria in the exploitation of water resources used for drinking and recreational purposes, a few techniques based on real-time PCR were devised to discriminate quantitatively microcystins (MCs) and non-MCs producing populations of P. rubescens (Garneau et al., 2015), or, as shown in this SI, the abundance of the ATX-a producer T. bourrellyi (Capelli et al., 2018). Further, the determination of the distribution of cyanotoxins in environmental samples or in strains isolated from the LPL was carried out by Cerasino & Salmaso (2012) and Cerasino et al. (2017). In Lake Bourget, the effects of P. rubescens blooms on C. lavaretus were examined by Sotton et al. (2011). Filaments of P. rubescens were observed in intestinal tracts of whitefish, and the presence of microcystin-LR detected in the intestine and liver, leading to potential adverse effects on the health of whitefish.

The use of traditional culture independent approaches (e.g., DGGE, CARD-FISH, cloning and sequencing), besides being time-consuming and costly, allows the determination of only the most abundant or representative taxa, disregarding most of the diversity. The advent of next-generation sequencing (NGS) technologies and the use of full shotgun metagenomics and marker gene amplification metagenomics (Oulas et al., 2015) have provided an impressive impulse to aquatic ecology, allowing to investigate the bacterial and eukaryotic biodiversity of freshwater ecosystems at an unprecedented detail. In the LPL, NGS approaches have been recently used to assess lake benthic diatoms diversity and ecological status of Lake Bourget using standardized DNA barcode and massive sequencing, and identifying species using a DNA reference library (Rivera et al., 2018). Nevertheless, as demonstrated by the authors, floristic inventories of species may differ significantly from the classical microscopic determinations due to the incompleteness of the DNA reference library. Hence, DNA metabarcoding for biomonitoring purposes will provide reliable results in the near future, only when the constraints due to incomplete reference DNA libraries will be solved. With an approach more focused on prokaryotic and/or bacterial and eukaryotic diversity, a few studies were carried out in deep large and smaller lakes, such as Fuschlsee (Medinger et al., 2010) and Bourget and Pavin (Debroas et al., 2015; Lepère et al., 2016). Recently, Salmaso et al. (2018a) identified a characteristic and recurrent cyclical pattern in the development of the bacterial community in Lake Garda; an in depth analyses of sequences obtained by HTS allowed also to identify oxygenic photosynthetic cyanobacterial species never detected before by using the traditional microscopic methods, as well as two new recently described non-photosynthetic cyanobacterial groups adapted to live in aphotic environments, namely ML635J-21 clade and Melainabacteria.

Fish

Fish communities were the object of many investigations in single water bodies, especially in the northern LPL. Among the others, investigations were focused on the effects of large-scale meteorological factors on the long-term dynamics of species of economic interest such as Coregonus lavaretus in lakes Constance and Geneva (Straile et al., 2007; Anneville et al., 2009); the importance of density-dependent effects on whitefish growth compared to that of eutrophication in Lake Constance (Thomas & Eckmann, 2007); microcystins (MCs) accumulation in whitefish (Coregonus lavaretus) of Lake Bourget during Planktothrix rubescens dominance (Sotton et al., 2011); the management of fish resources in Lake Maggiore (Grimaldi, 1996).

A number of synoptic studies allowed obtaining information of general importance, useful for understanding the ecology and distribution of fishes in the perialpine region, as well as their management. The knowledge of conservation units delimited by genetic and morphological criteria is essential for the correct management of water resources. Using genetic data across six microsatellite DNA loci and morphological characters, Douglas & Brunner (2002) demonstrated that undocumented stocking of Coregonus during the last 100 years in the Central Alpine region has further added confusion to the naturally occurring cryptic and sibling species living in the LPL. From a management perspective, the authors proposed to view the Alpine Coregonus lineage as an ‘‘evolutionarily significant unit’’, and each population a specific ‘‘management unit’’. The results were confirmed by Gum et al. (2014) in Lake Constance, where the appearance of new alleles in the gene pool since the 1970s suggested an admixture with other Coregonus forms in the lake or with stocked allochthonous forms. The effects of stocking was also apparent in the genus Esox in Northern Italy, including Lake Garda. Gandolfi et al. (2017) demonstrated the existence of introgressive hybridization between the native E. flaviae Lucentini et al. and the exotic E. lucius L. species in Northern Italy; the dispersal of the invader seemed to be promoted by stocking actions.

By analyzing historical and contemporary data of whitefish radiations from several LPL, Vonlanthen et al. (2012) reconstructed changes in genetic species differentiation through time. Results suggested that anthropogenic eutrophication has led to speciation reversal in whitefish radiations by increasing gene flow between previously ecologically differentiated species.

The effects of the oligotrophication process that characterized the LPL since the 1970–1980s on the fish communities and yields were investigated by Gerdeaux et al. (2006). During the eutrophication phase, fish communities were dominated by cyprinids and perch, whereas, during oligotrophication, while the total yield remained nearly the same, coregonids were dominant. In lakes where TP went below 5 μg l−1, the total yield decreased rapidly, with strong negative effects on fish production. The best mean annual yields for coregonids were recorded for TP concentrations between 20 and 40 μg l−1. Using a similar dataset from the same group of lakes, Massol et al. (2007) showed that fish abundance was affected by phosphorus concentration at the species level, suggesting a control mediated by recruitment rather than by adult survival, and by interspecific interactions depending on species position in the trophic chains. Models indicated that roach and trout were positively related to increases in TP; pike responded slightly negatively and whitefish had a peak of abundance at transitional TP values (40–50 μg l−1); finally, perch was not affected by TP at all. In a recent study, Nõges et al. (2017) analyzed the long-term limnological and fisheries data from five European lake basins and found that oligotrophication induced different fish responses. In the deep lakes Geneva and Maggiore their study suggests cascading top-down effects, emphasizing the importance of careful ecosystem-based fisheries management for maintaining high water quality.

In contrast to a strong effect of oligotrophication, Massol et al. (2007) did not find any significant effect of temperature increase on fish abundances in LPL during the period 1970–2000. Conversely, in recent decades strong and fast changes were observed in the response of fish to the warming along a wide north–south European gradient (Jeppesen et al., 2012). The importance of raising water temperature and synergic effects between global warming and P-reduction on fish populations of Lake Geneva was addressed by Anneville et al. (2017). Reduction of P-loadings was beneficial for the recovery of whitefish spawning areas, slowing the increase of percid and cyprinid communities. At present, rising spring water temperatures are favoring the growth rates of the larvae of whitefish, improving its recruitment. Nevertheless, in Lake Geneva, whitefish is already living at the upper end of its thermal tolerance range, whereas water temperatures exceeding 8°C during the spawning season are expected to cause a decline in whitefish reproductive success (Anneville et al., 2013).

Important changes in the biomass of typical and common species can not be only due to long-term changes in trophic state, but also due to invasion of neobiota. In Lake Constance, the pelagic zone of the upper lake underwent a massive invasion of the non-native three-spined stickleback (Gasterosteus aculeatus L.) since 2013. Concurrently, pelagic whitefish (Coregonus wartmanni Bloch) showed a strong decrease, implying direct effects of Gasterosteus on Coregonus, possibly due to interspecific competition for food inducing reduced growth and survival, and stickleback predation on whitefish eggs and larvae (Rösch et al., 2018). The dimension of the invasion of non-native fishes on the LPL has been further scrutinized in 8 southern perialpine lakes of various size (Volta et al., 2018). Out of 34 fish species, 20 were native, 7 introduced historically and 7 introduced recently. In terms of abundances, non-native species contributed between 4 and 72% to standardized catches by numbers, and between 5 and 65% by biomass. Overall, the present harvest is dominated by non-native species.

Benthos and macrophytes

Overall, benthos and littoral vegetation were the object of studies carried out on single LPL. However, no new contributions were proposed in this SI which may indicate that research on these communities is still underrepresented, especially as these communities are important biological elements in the application of WFD. In this respect, benthic diatoms have been the object of several studies based both on microscopic determination (e.g., Spitale et al., 2011; Rimet et al., 2015) and HTS analyses (Visco et al., 2015; Rivera et al., 2018).

Recent investigations on macrobenthic communities showed an alarming increase of introduced and invasive species in many lakes. In Lake Garda, Ciutti et al. (2011) identified almost 40 species of non-indigenous fish (see also Volta et al., 2018), invertebrates, and macrophytes. The introductions were particularly important for invertebrates and macrophytes. Besides Dreissena polymorpha (Pallas, 1771) a few other recently introduced bivalves showed a fast colonization rates in the Alpine hydrographic network such as, among others, the Asian clam Corbicula fluminea (O.F. Müller, 1774), the Chinese pond mussel Sinanodonta woodiana (Lea, 1824), and the quagga mussel Dreissena bugensis Andrusov (Werner & Rothhaupt, 2008; Ciutti et al., 2011; Kamburska et al., 2013). Gergs & Rothhaupt (2015) demonstrated a large impact of invasive species on the composition of benthic macroinvertebrates in Lake Constance. Some widespread invasive species are potential competitors and predators of ecologically important native species, strongly impacting food webs (David et al., 2017). With regard to the most impacting species (e.g., Dikerogammarus villosus Sowinsky), Rewicz et al. (2017) suggested to actively implement safety programs procedures to stop or slow down spreading among the Alpine lakes, preventing additional long distance transport.

The study of macrophytes took new impulse with their inclusion among the biological indicators considered in the evaluation of the lake ecological status by the WFD (Water Framework Directive, 2000; Stelzer et al., 2005). The role of this biological element is essential for a wide spectrum of ecological services, including sustaining biodiversity and food webs, sediment resuspension/trapping etc. (see below).

Ecotoxicology

Owing to the strong impact on trophic webs and aquatic organisms, and the implications for human health, the determination of chemical pollutants has been the object of a large number of investigations. In most European large lakes, including LPL, concentrations of mercury and other heavy metals, as well as persistent organic pollutants (POPs), though showing a substantial decrease, are still detectable in sediments and food webs (Nõges et al., 2008; Salmaso & Mosello, 2010). The studies carried out in the LPL were focused both on many legacy (e.g., DDT, PCB) and current-use POPs (e.g., polycyclic aromatic hydrocarbons, PAHs). Most of the investigations showed the presence of a wide array of contaminants, posing serious and challenging problems for the determination of risk assessment and management of water resources. This was well exemplified in Lake Bourget where 6 heavy metals, 15 polycyclic aromatic hydrocarbons and 7 polychlorinated biphenyls were identified, with levels of contamination varying significantly among sites (Lécrivain et al., 2018).

The long-term risks posed by POPs were fully exemplified by the sharp increase of DDT observed in 2005 in lakes Como and Iseo caused by the melting of glaciers rich in pollutants deposited during previous decades (Bettinetti et al., 2008; Miner et al., 2017). Actually, individuals of Alosa (shad) collected in Lake Como had DDT concentrations of 0.12 mg kg−1 (w.w.), i.e., a value that exceeded the Italian limit set for human consumption.

The presence of a variety of organic pollutants and biomagnification and bioaccumulation effects were widely confirmed throughout food webs (Galassi et al., 2002; Bettinetti et al., 2006; Paulus et al., 2015). The high diversity of POPs and heavy metals and biomagnification processes in large lakes have been further confirmed by Guzzella et al. (2018). In lakes Maggiore and Lugano, POPs and heavy metals deriving from past industrial activities (DDx and Hg) still exceeded Sediment Quality Guidelines in sediments and existing Quality Standards (QSs) in fish. PCBs, which were banned in Europe in 1985, showed low residual values, whereas PBDE peaks exceeded QSs for biota, probably due to recent industrial activities. Different biomagnification capacities were observed, namely Hg > DDx ≈ PBDEs. Overall, the results highlighted the existence of potential risks for the ecosystem and human health.

Paleolimnology

The LPL were the object of several studies aimed at reconstructing the ecological conditions of lakes on decadal and secular scales (Marchetto et al., 2004; Guilizzoni et al., 2012; Perga et al., 2015; Larocque-Tobler, 2017). Nevertheless, as highlighted in this SI in the review by Tolotti et al. (2018), the majority of the early studies on past catchment processes were localized in the lakes of the Swiss Plateau, whereas studies on pollution were concentrated on Swiss and subalpine lakes; reconstruction of paleoclimate and paleoecological conditions were more numerous in the Savoyan and Swiss lakes. Remarkably, owing to the much lower number of studies focused on the reconstruction of past nutrient levels, information on long-term lake trophic status at the decadal/century scale and definition of lake reference conditions have to be still completed for a large number of LPL.

Though necessitating further tuning and validation (such as the evaluation of DNA preservation in sediments; Capo et al., 2017), the application of high throughput sequencing techniques (18S rRNA gene amplicon sequencing) to sedimentary DNA showed very promising results, allowing to reconstruct past diversity for numerous planktonic eukaryotic groups (Capo et al., 2015, 2016). Further, recent application of metagenomic tools to bacterial communities (16S rRNA genes) provided a rapid and standardized way to analyze the long-term development of cyanobacteria in several perialpine lakes since the beginning of the 1900s (Monchamp et al., 2016, 2018).

An updated account of the state of paleolimnological research in the LPL is given in Tolotti et al. (2018) and references therein.

Remote sensing

Owing to the large surfaces that characterize the LPL, traditional monitoring approaches based on the collection and analysis of samples in localized areas cannot provide information about spatiotemporal variability within the lakes. Though providing information of environmental conditions largely limited to the upper epilimnetic layers, satellite remote sensing techniques proved to be widely useful to obtain synoptic spatio-temporal views on several abiotic (water temperature, hydrology, color, suspended matter) and biotic (algal blooms and phenology, submerged vegetation) elements in large lakes (Dörnhöfer & Oppelt, 2016). The application of remote sensing techniques to several LPL documented the presence or large patchiness and gradients in the surface thermal regime (Oesch et al., 2008; Pareeth et al., 2016), phytoplankton biomass distribution (Odermatt et al., 2010; Bresciani et al., 2011; Kiefer et al., 2015; Soulignac et al., 2018), and littoral vegetation (Giardino et al., 2007; Bresciani et al., 2012). Two recent regional studies allowed to confirm the long-term trends in the warming of the large perialpine lakes by using different satellite time series obtained by the retrieval and analyses of MODIS and AVHRR, and ATSR1 and A(A)TSR sensor data (Riffler et al., 2015; Pareeth et al., 2017). In particular, from 1986 to 2015 the largest lakes south of the Alps (Garda, Maggiore, Como, and Iseo) showed an increase in surface water temperatures between 0.12 and 0.20°C decade−1. Moreover, the cross-comparison of both the mean summer and annual values confirmed the high degree of temporal coherence in the long-term development of water temperatures that characterize these large water bodies.

The efficacy, spatial detail, and quality of information is expected to increase with the availability of data provided by the new generation of satellites. The combination of data collected by the sensors onboard of the new Landsat-8 (L8, launched in 2013) and Sentinel-2A/B (S2A/B, launched in 2015 and 2017) allows a multi-spectral global coverage with a pixel size of 10–30 m at a frequency of approximately three days (Yan et al., 2016). In this SI, Bresciani et al. (2018) tested the advantages in using the new optical sensors S2A and L8 in the analysis of algal blooms dynamics of lakes Maggiore, Como, Iseo, Idro, and Garda. The results showed a good relationship between in situ and remote sensing data, and confirmed the high temporal dynamicity in the temporal variation of algal biomasses in surface waters, with events characterized by an increase of biomasses from 2 to 7 mg m−3, soon followed by a drop to initial value in less than 20 days.

Research gaps, new directions, perspectives

Towards an integration of basic and applied research

This overview of research contributions on the limnology of the large perialpine lakes published in the last decades allows drawing some general considerations and recommendations (Table 2): (i) Most limnological research in the LPL were carried out following a “problem solving” approach and a strategy in the selection of tools and conceptual approaches strongly linked to the model of scientific monitoring, (ii) The fragmentation of studies in different separated topics and schools did not favor an integration of different disciplines, (iii) The integration of existing knowledge and synoptic analyses at regional and supraregional scale have been carried out including only selected specific research areas, and (iv) An additional disconnection is rapidly widening between the recent advances in specific scientific fields and the present traditional tools and approaches used in environmental monitoring programs under the criteria defined almost two decades ago by the Water Framework Directive, and other EU monitoring programs, which in turn were based on the outcomes of research carried out in the previous two decades.
Table 2

Research topics that need more intensive study and new research lines that should be activated in the study of large and deep lakes

Topic

Areas that need more intensive study or new research lines in large and deep lakes

Physical and chemical limnology

 

 Atmospheric modes of variability

The atmospheric circulation patterns as described by the two most relevant teleconnection indices for the Alpine region (i.e., NAO and EA) showed important changes and shifts. The impact of these changes on the LPL have to be further evaluated, including more lakes, using modeling approaches, and evaluating the geographic range of impacts on the Alpine and other European/Atlantic regions

 Modeling biogeochemical processes

Up to now hardly any biogeochemical models parameterized for LPL

 Extended scale of investigations

The evaluation and adoption of high frequency monitoring systems, beside traditional discrete monitoring, is advisable to extend the temporal and spatial scale of investigations, also in support to modeling

Effects of global warming

 

 Modeling long-term thermal structure and mixing

Modeling long-term thermal structures and mixing regimes based on future climate change scenarios

 Ecophysiology of aquatic organisms (plankton, benthos, nekton)

Consequences of global warming (water temperature and stratification) on lake biota, with focus of the ecophysiology of keystone species or organisms of specific interest. Impacts have to be explained at the physiological and ecological level. Interactions with other organisms and environmental factors should not be excluded

 Phenological mismatch

Decoupling prey-predators interactions

Ecotoxicology

 

 Emerging contaminants

Widening the detection, quantification, and impact of new emerging pollutants (including pharmaceuticals)

 Algal toxins

The knowledge of the producers of cyanotoxins and their distribution have to be improved; the impact of cyanotoxins on trophic webs is still insufficiently known, especially for toxins other than microcystins and anatoxins; expression mechanisms and concurrent effects have to be clarified; allelopatic effects

 Synergic effects of micropollutants

Probability of interactions, and effects of interactions between and among micropollutants (POPs, pharmaceuticals, cyanotoxins) and other environmental stressors on aquatic communities, trophic webs and human health

 Legacy from the past

Melting releases POPs and contaminants trapped in glaciers and permafrost

Plankton (including bacteria, viruses, fungi)

 

 Biodiversity

Improving the evaluation of plankton biodiversity with both culture dependent (polyphasic) and independent (analysis of environmental DNA with modern metagenomics, including marker gene amplification) approaches

 Functional diversity

Full shotgun metagenomic techniques to evaluate the functional and taxonomic diversity of plankton communities

 Ecological metabolomics

Knowledge and role of secondary metabolites in the adaptation of aquatic organisms to changing environmental conditions and extreme environments (exemplified e.g., by mycosporine-like amino acids)

 Cyanobacteria

With a few exceptions, many populations of cyanobacteria in the LPL have to be screened, clarifying their taxonomic position, genetic profiles (also at the genomic level) and toxicological characteristics

 Trophic webs

Interdisciplinary investigations (functional and modeling) aimed at clarifying trophic relationships among species and trophic levels; resilience of trophic webs to environmental impacts (including climate change); phenological mismatches; adoption of metagenomic approaches to study functional biodiversity and trophic webs

 Viruses

Functional role of viruses in the plankton community, bloom dynamics, and biogeochemical cycles

 Antibiotic resistant genes

Spread of antibiotic resistance genes in the hydrographic network

 Modeling of populations changes

Modeling of populations changes and interactions between trophic levels have to be better defined (applied at the level of functional groups or species) and tested

Aquatic biota (including fish)

 

 Fish census

Use of metagenomic techniques to provide a census of lake fish with non-invasive, rapid and cheap approaches

 Benthos

The diversity and role of benthic organisms are widely under explored

 Littoral vegetation

The function and value of littoral vegetation in ecosystem services is largely under explored

Alien species

 

 Detection and impacts

Identification of newly introduced, already established, and cryptogenic invasive species, and their effects on native biota and ecosystems; surveys carried out also making use of metagenomic approaches

Lake management

 

 Management at the lake watershed level using GIS approaches

Management and modeling of land use using GIS technologies; estimation of nutrient/pollutants loads to the lake; simulation of impacts due to land change use and climate change

 Water level oscillations

Effects of oscillation of the water levels on nutrient cycling and on benthic organisms and macrophytes in the littoral zone

 Fisheries

Improved assessment of fish stocks, evaluation and prediction of the impacts of environmental changes (reoligotrophication, climate change etc.) and fishing pressure on the abundance of exploited fish populations, promoting sustainable management strategies (Ecosystem based fisheries management)

Ecological economics

 

 Economic estimation of the value of ecosystem services

Providing economic estimates of ecosystem services provided by LPL and hydrographic networks (e.g., drinking water, tourism and recreation, wastewater treatment, fish etc.)

 Strategies to solve water conflicts

Strategies to maximize the use of water resources among users. Water quality requirements for fishing may not be the same than those expected for drinking water or tourism and recreation, requiring optimization of water use based on societal values, resource preservation, sustainability, and economic value

 Economic estimation of impacts

Defining the economic costs of impacts (e.g., eutrophication, excessive reoligotrophication, cyanobacterial blooms, POPs in trophic webs etc.) on ecosystems and human health, fisheries, treatment costs, surveillance etc.; making cost-benefits analysis of management interventions

  1. (i)

    Most of the limnological investigations carried out during the last decades in the LPL have been fostered by urgent needs to find solutions to the problems connected with eutrophication, pollution, fishery management and with the more recent threats posed by climate change. This ‘applied research’ strategy has been dictated by the need to preserve freshwater, one of the most threatened and limiting resources, from the increasing anthropogenic pollution and by the increasing demand of good quality waters. As a side effect, these programs have greatly contributed to fundamental limnology. Though very scattered and with different coverage among lakes (see next point), the main topics that have been included in the research programs in many LPL are those connected with the long-term development of trophic state, changes in the thermal structure of lakes and effects of incipient meromixis, the monitoring and fate in the food webs of persistent organic pollutants and heavy metals, monitoring of fish populations and communities, and phytoplankton changes, including toxigenic cyanobacteria and toxins. Other research fields have been largely under explored or completely overlooked. In this context, rapid adaptation of research is required to cope with new environmental emergencies. Among new topics (see Table 2), urgent investigations are needed to evaluate the impact of the past and ongoing changes in the large-scale atmospheric circulation patterns (as described by NAO and EA) on the Alpine inland waters; the consequences of global warming on the lake biota, with focus of the ecophysiology of keystone species or organisms of specific interest (Cingi et al., 2010); the identification of introduced, invasive, and cryptogenic species, sensu Kokociński et al. (2017), and their effects on food-webs and ecosystem services (David et al., 2017); the evaluation of new emerging pollutants, including pharmaceuticals (Brack et al., 2017; Glassmeyer et al., 2017) and cyanotoxins other than microcystins and anatoxins (e.g., Cerasino et al., 2017; Meriluoto et al., 2017a, b); the phenotypic, genetic and ecological characterization of the main toxigenic species of cyanobacteria in the LPL (Salmaso et al., 2016; Kurmayer et al., 2017) and other key species (Salmaso et al., 2018b); the interactions among micropollutants and other stressors and their effects on aquatic communities, trophic webs and human health (Sabater, 2017; Salo et al., 2017; Tran et al., 2018); the quantitative assessment of multiple stressors affecting aquatic biota (Gieswein et al., 2017); the spread of antibiotic resistance genes in the hydrographic network (Eckert et al., 2018; Zhao et al., 2018). From a methodological point of view, the implementation of ongoing and new studies should make full use of the new technologies (see next point), as well as of a wider spectrum of modeling approaches that, at present, have been mostly restricted to physical modeling (thermal structure and effects of future global change scenarios), with less applications to biogeochemical (Omlin et al., 2001; Dietzel et al., 2013; Schwefel et al., 2016) and biological processes (Boit et al., 2012). More in general, future progress in the ecological studies in the LPL and a better capacity to generalize results, including them in the context of general ecological knowledge, will have to be founded on the delineation of objectives defined within broader and stronger theoretical frameworks, and with testable hypotheses. What was highlighted by Harris (1999) is still valid, i.e., there is a need for fundamental information about the role of biodiversity in ecosystem function, and for understanding the interplay between environmental drivers and biodiversity in the control of materials and energy cycling within freshwater ecosystems.

     
  2. (ii)

    In his seminal paper, almost 30 years ago, Peters (1990) observed that the reductionist search for the components and functioning mechanisms of lake ecosystems has fragmented limnology into specialized and expert fields with limited interaction. Looking at the limnological contributions published in the last decade on the LPL, this view is still largely valid (cf. Salmaso & Mosello, 2010) and is further reinforced by the application of new advanced technologies requiring specialization, dedicated analytical and computational tools and jargons allowing looking at fine details but missing the whole. In this respect, a continuous fragmentation of disciplines could be further expected, therefore requiring a precise strategy addressed towards the integration of objectives and information already from the beginning of the projects, in the planning and writing phases. Actually, the most outstanding innovations in specific limnological fields were connected with the appearance and adoption of new technologies, as in the fields of the ‘omics’. The application of metagenomic approaches in marine and freshwater environments is opening new perspectives in the evaluation of microbial (Ruiz-González et al., 2017; Tessler et al., 2017), eukaryotic microplankton (Khomich et al., 2017), viral (Skvortsov et al., 2016), and benthos and nekton (Rivera et al., 2018) biodiversity, as well as functional diversity (Eiler et al., 2014; Bork et al., 2015), including the distribution of genes of specific interest (such as antibiotic resistance genes; Bengtsson-Palme et al., 2014). Massive amplicon sequencing has been used to investigate the associations between microeukaryotes and bacteria (Jungblut et al., 2012; Nitin Parulekar et al., 2017), i.e., biological compartments that usually are evaluated separately, and to reconstruct biological communities from stratified core sediments (Monchamp et al., 2016). Compared with other traditional limnological disciplines, and also considering the recent applications of these approaches, until now the objectives of the vast majority of metabarcoding studies were purely academic (Pawlowski et al., 2016). Nevertheless, favored also by the great decrease in the costs, the range of application and experiences based on HTS technologies is growing (Leese et al., 2016), including, among the others, ecological biomonitoring (Bohan et al., 2017), waterborne pathogens monitoring (Vierheilig et al., 2015; Luna et al., 2016), and census of fish communities (Thomsen et al., 2012). Similarly, the study of ecological metabolomics is providing experimental support for defining the basis of adaptation of aquatic organisms to specific environmental conditions (e.g., Ficek et al., 2013). The ‘omics’ approaches are contributing to widen the perspectives in the study of organisms; as a matter of fact, keystone groups such as cyanobacteria are no more viewed as only nuisance organisms, but also as remarkable sources of novel bioactive secondary metabolites of pharmaceutical, nutraceutical and cosmetological value (Vijayakumar & Menakha, 2015). In ecotoxicology, the use of high-resolution mass spectrometry (HRMS) can help to characterize chemical contamination using non target screening methods (Chiaia-Hernández et al., 2017). Another very promising research field that benefited from the integration and assembly of new sensors and technologies is linked to the use of satellite remote sensing and platforms equipped for the high frequency monitoring (HFM) of in situ limnological variables (Pomati et al., 2011). Such platforms allow extending the scales of observations and providing more robust basis for modeling. HFM systems have been successfully deployed in several European lakes, including some LPL, providing physical, chemical and biological information at very short time scales. In order to address both current and future water quality issues, the EU COST Action NETLAKE has recently promoted a wide networking of sites and institutions to support the development and deployment of sensor-based systems in European lakes (Marcé et al., 2016).

    Considering the selected examples above, it is quite probable that the future progresses in the limnological studies in the LPL (and water bodies, in general), will be strongly linked to the advancement and accessibility of new technological tools and to the planning of multi- and interdisciplinary projects founded on clear theoretical frameworks. If the perspective of further specialization in limnology could be functional to specific areas of application using a ‘problem solving’ approach, a better comprehension of the functioning mechanisms of lacustrine systems, and a better and robust definition of management objectives and targets will require an integration of different disciplines and expertise, also including areas traditionally considered outsides the scopes of limnology, such as economy. The quantitative assessment of the economic value of water resources and the loss of value when they are affected by environmental pressures should require a quantitative assessment to better address management priorities. In this regard, the quantitative evaluation of losses is well exemplified by the costs of harmful blooms of freshwater cyanobacteria in USA (Hamilton et al., 2014). For example, the cost of treatments designed specifically to remove taste/odor compounds and toxins associated with cyanoHABs for a group of water bodies in USA ranged between US$ 8.5 and 31.8 million (serving from 11,000 and 100,000 people) (Naidenko et al., 2012).

     
  3. (iii)

    As highlighted in the previous section, synoptic studies are still very few and limited to specific research areas and impacts (i.e., phytoplankton, paleolimnology, micropollutants), and regional areas. A few of these investigations were carried out within the framework of the Long-Term Ecological Research networks (LTER) (Morabito et al., 2018a), whereas other initiatives were based on more sporadic and temporary experiences (Gallina et al., 2013). The integration of new data into existing knowledge and synoptic analyses at regional and supraregional scale is however hampered by the intrinsic limitation common to all environmental studies, i.e., the lack of an official and recognized data repository like the International Nucleotide Sequence Database Collaboration (Blaxter et al., 2016) where to deposit compulsorily selected and quality checked data associated with the publication of papers. Nevertheless, the availability of data does not solve basic problems due to the comparability of methods and quality in datasets obtained in different laboratories and with, most of the time, different objectives, and the implications of ex post analyses, which dictate and limit the range of objectives and expected results. Anyway, the LTER program will ensure continuity of basic data series and offer opportunities for developing collaborative and large-scale research in even few sites, which are the minimum requirements for studying the long-term effects of climate changes and anthropogenic impacts on lake ecosystem development (Mirtl et al., 2018).

     
  4. (iv)

    In Europe, the present monitoring approaches applied in the determination of ecological status of rivers and lakes, including the LPL, are essentially still based on the criteria defined almost 20 years ago by the Water Framework Directive (2000). In the case of the assessment and management of chemical contamination, and in support of the upcoming WFD review in 2019, the criteria defined in the present directive were scrutinized, and a set of recommendations was provided to improve monitoring and consistent assessment, and to support solution-oriented management of surface waters (Brack et al., 2017). As for the biological components, the assessment of changes in the composition of species and community structure is still defined by adopting traditional tools. The discrepancy between the methods currently used in the water ecological assessment and the available metagenomic and metabolomic technologies is contributing to broaden the ‘scientific divide’ between academia and environmental agencies. The awareness of the necessity to upgrade the WFD criteria associating to the traditional methods the new ‘omics’ tools has fostered scientific initiatives funded, among the others, by EU programs COST (DNAqua-Net) (Leese et al., 2016), Interreg France-Swisse (SYNAQUA), and Interreg Alpine Space (Eco-AlpsWater).

     

Anthropogenic stressors and preservation of water resources

Scientific research is essential for planning sustainable use of resources and maintaining ecosystem services of large lakes (Kankaala et al., 2016). The uniqueness of the large lakes of the Alpine region is reflected in a common spectrum of anthropogenic pressures, which requires specific attention and support from scientific investigations, with dedicated applied research lines and technological transfer from basic science.

The main LPL are surrounded by human settlements that in the last half century have also evolved as tourist facilities (Comunità del Garda, 2013). Consequently, the populations along the lakeshores are fluctuating, attaining relevant peaks in summertime. This trend caused serious concerns on wastewater processing, which were solved adopting several approaches, including diffuse wastewater treatment plants and ring trunk sewers. In large lakes, recovery from eutrophication and maintenance of pristine conditions in the main water mass can be exclusively based on the abatement of external nutrient loads. Other measures, particularly those aimed at mitigating the effects of eutrophication, such as destratification, hypolimnetic withdrawal and oxygenation, food-web manipulation, sediment removal, algaecides etc. (Cooke et al., 2005), are ineffective or poorly feasible (Table 1). Nevertheless, the length of the shoreline and the different land uses can be the cause of several diffuse local impacts, negatively affecting water quality and pristine conditions of lakeshores. In such specific cases, the adoption of ad hoc local interventions (buffer strips upstream of the impacts, reed management and replanting littoral vegetation, sustainable urban green design etc.; Ostendorp et al., 1995; Gulati et al., 2008) increases the quality of lakeshores, which are the immediate visible zones of lakes, and those giving the first impression to visitors. Owing to their values as refuge for a wide variety of aquatic animals and as local hotspot of biodiversity, particular attention should be given to the management and conservation of wetlands (Keddy & Fraser, 2000).

Changes in water levels can represent a potential disturbance for littoral communities (Zohary & Ostrovsky, 2011) although seasonal fluctuations exceeding one meter on average are likely the natural condition for most LPL (Wantzen et al., 2008). The Italian LPL are man managed with dams at the outlet, allowing regulating water levels of 1–2 m (www.laghi.net). The regulation is aimed at exploiting water for irrigation and hydroelectric power generation, but this has important consequences due to the periodic emersion and submersion of the littoral areas, which can favor opportunistic and allochtonous species (e.g., pleustophytes), especially in the shallower areas. By contrast, perennial species can be threatened. In regulated lakes, the man made adjustment of lake water levels should take into account, besides the needs of the tourist industry and agriculture, the preservation of littoral communities.

The preservation of water quality in the LPL has a huge strategic economic value also in the light of the increasing exploitation of large lakes as sources of drinking water supply. The soils, rivers, and ground waters in the plains surrounding the Alps underwent high contamination of POPs (Di Guardo & Finizio, 2016; Di Guardo et al., 2017). Consequences are particularly serious in “hot spot” areas characterized by point source release of pollutants (Valsecchi et al., 2015). Within this context, further exploitation of the traditional sources of drinking water in the plains surrounding the Alps have to rely on the use of advanced and costly purification technologies. Nevertheless, the exploitation of the LPL as drinking water supply have to be based on a careful control of POPs contamination and removal of cyanotoxins. The elimination of risks posed by cyanobacteria in drinking water treatment plants have to rely on a detailed knowledge of the ecology (seasonality and vertical development) and toxicity of the cyanobacterial species dominant in each water body, on the qualitative and quantitative determination of the most abundant cyanotoxins, and on the adoption of reliable state of the art technologies for the elimination of cyanotoxins (Westrick et al., 2010; Szlag et al., 2015; Kurmayer et al., 2017; Meriluoto et al., 2017b).

Future approaches in the management of large lakes should consider processes and impacts occurring at the lake and watershed basin scale. A growing number of investigations evidenced the close connection between watershed land use and lake water quality (Hamilton et al., 2016). Urban land uses and agricultural practices were identified as obvious targets for implementation of nutrient load control and remediation actions. In perspective, the use of geographic information systems (GIS) and modeling approaches will allow to estimate nutrient/pollutants loads to the large lakes at very detailed spatial scales (homogeneous land parcels), providing powerful tools to simulate effects of land use changes and climate change in complex mosaic landscapes (Table 2).

The preservation of large perialpine lakes have to rely on water protection policies defined at different scales of integration, i.e., both at the European level (EU directives) and macro-regional level (Camagni et al., 2017; Alvisi & D’Alelio, 2018), through the integration of policies addressed to the sustainable development of terrestrial and aquatic ecosystems, following the “green” and “blue” infrastructure concepts (Suppakittpaisarn et al., 2017; Brears, 2018). In this context, strategically designed network of natural and semi-natural green and water linked areas will help delivering a wide range of ecosystem services, including water purification, contributing to climate mitigation in lake watersheds, and adaptation.

Notes

Acknowledgements

We would like to thank all the authors of this special issue for their efforts in preparing the papers that have contributed to establish the state of the art of limnology in the large and deep perialpine lakes. We are grateful to two anonymous reviewers for valuable comments and suggestions on an earlier version of the manuscript, and to Andrea Gandolfi (FEM) for checking the section dedicated to fish. DS was supported by the European Regional Development Fund: Interreg V-A—Germany-Austria-Switzerland-Liechtenstein (Alpenrhein-Bodensee-Hochrhein 2014–2020) under grant no. ABH060 (“SeeWandel: Life in Lake Constance—the past, present and future”).

Supplementary material

10750_2018_3758_MOESM1_ESM.tif (703 kb)
Cascading effects on the limnological characteristics of large and deep perialpine lakes originating from the year-to-year oscillations in the winter EA and NAO. In their higher value state, the two indices are associated to mild winters, which prevent the full mixing and vertical homogenization of physical and chemical characteristics along the water column. In their lower value state, the two indices are associated with harsh winters, which can cause a more extended or even a complete mixing of lakes, and a greater supply of nutrients to the surface and oxygen to the deep hypolimnion. Supplementary material 1 (TIFF 702 kb)

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© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Research and Innovation CentreSan Michele all’AdigeItaly
  2. 2.INRA, Université Savoie Mont Blanc, CARRTELThonon-les-BainsFrance
  3. 3.Limnological InstituteUniversity of KonstanzKonstanzGermany
  4. 4.Department of Chemistry, Life Sciences and Environmental SustainabilityUniversity of ParmaParmaItaly

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