Paleoecological evidence for a multi-trophic regime shift in a perialpine lake (Lake Joux, Switzerland)
Graphical abstract
Introduction
Lake ecosystems are changing at an increasing rate as a consequence of global climate change, as well as regional and local environmental and anthropogenic disturbances (Jenny et al., 2020). Threats to lake ecosystems arise from the accumulation of local and global human stressors, but also from their potentially non-linear and sudden responses to the stressors after years of relative stability. Such transitions are referenced as regime shifts, and can occur without easily detectable early-warning signals (Scheffer et al., 2001). Regime shifts typically occur at multiple trophic levels, after exposure to discrete or continuous stressors (Bestelmeyer et al., 2011; Randsalu-Wendrup et al., 2016). That happens abruptly and has prolonged consequences on ecosystem structure and function (McGowan et al., 2005) that would delay the efficiency of management actions (Andersen et al., 2009; Randsalu-Wendrup et al., 2016; Scheffer et al., 2001). Detecting the occurrence and quantifying the strength of such major shifts in lakes is fundamental to identify causes of catastrophic changes and to help develop management strategies for the protection and the conservation of freshwaters.
Regime shifts raise important management issues, yet there are few documented records of true regime shifts, especially for deep lakes. Our ability to detect regime shifts and to determine their underlying causes is currently limited by the lack of long-term high-resolution data (Smol, 2010; Taranu et al., 2018). Lacustrine sediments provide unique archives of climatic, environmental and ecological changes that constitute an alternative option for the retrieval of information from the past (Gregory-Eaves and Beisner, 2011). Paleolimnological records archive evidence for major events such as regime shifts through community changes. Therefore, paleolimnological approaches have potential to shed light on the dynamics of environmental and biological change over decadal to millennial time scales.
Subfossil-based paleolimnological proxies that are readily preserved in the sediment over thousands of years include diatoms, cladocerans and chironomids (Leavitt and Hodgson, 2001; Watts and Maxwell, 1977). Used widely to track various facets of lake histories, such as primary production (Deshpande et al., 2014; Leavitt and Hodgson, 2001; Makri et al., 2019), these proxies can support assessment of long-term responses of biological communities to key environmental drivers. These drivers include changes in nutrient regime (eutrophication and re-oligotrophication) (Hall et al., 1999) or pH (Battarbee, 1991), climate change (e.g., Walker et al., 1991; Perga et al., 2015; Bruel et al., 2018) and human impacts (Battarbee and Bennion, 2011; Dubois et al., 2017).
More recently developed molecular-based proxies have further opened sedimentary archives to ecologists by enabling the investigation of all organisms across the tree of life. Such proxies include those that do not leave identifiable morphological remains or fossils, such as microbes and microeukaryotes (Capo et al., 2021; Domaizon et al., 2017; Taberlet et al., 2012; Thomsen and Willerslev, 2015). Sedimentary DNA (sedDNA) approaches applied to lakes have led to successful ecological reconstructions of primary producers at deeper taxonomic resolutions compared to photosynthetic pigments. They have made possible the estimation of their genetic diversity (Capo et al., 2016; Coolen et al., 2006; Domaizon et al., 2013; Monchamp et al., 2018, 2019a). Further, studies combining both sedDNA and other paleolimnological proxies have proven useful to validate temporal trends in lake biodiversity (Coolen et al., 2006; Stoof-Leichsenring et al., 2012; Tse et al., 2018; Wirth et al., 2013).
Both paleoecological and neolimnological studies on the changing dynamics of systems usually cover a limited range of diversity or trophic levels (for example, pigments (Makri et al., 2019); cladocerans (Bruel et al., 2018)). Processes leading to an ecosystem-wide shift, on the other hand, result from intricate relationships at multiple trophic levels. The coupling of molecular genetics and more classical paleolimnological approaches can help evaluate the evolutionary response of aquatic organisms to changing environments and to uncover trophic interactions (Ellegaard et al., 2020). So far, multi-trophic assessments of biodiversity dynamics at a lake scale have not been available.
Lake Joux, a mountain lake located in the Swiss Jura, is particularly well suited to paleoecological work. The history of human activities in the catchment, back to the early settlement of humans (∼300 CE), is well known. Regular monitoring of the lake since the 1980s provides decades of valuable information on biological communities and water quality. Similar to other perialpine lakes (Tolotti et al., 2018), Lake Joux has undergone eutrophication over the second half of the 20th century (max. 35 μg total phosphorus (TP)/L), with consequences on the zoobenthos and phytoplankton composition documented by contemporary monitoring.
To improve ability to detect and to quantify the consequences of regime shifts over the entire ecosystem, this study addressed the following questions. First, how did ecological communities change in Lake Joux during the last millennium. Second, to what extent do identified changepoint(s) qualify as critical transitions or regime shifts? What is the character of the changes? For example, were the changes restricted to some biological compartments or did it spread/ripple across all trophic levels? In brief, we aimed at qualifying and quantifying biological change attributable to local human activities, specifically land use and pollution in the watershed.
Section snippets
Study area
Lac de Joux (Lake Joux) is located in the Swiss Jura at 1004 m above sea level (m a.s.l.). It is the largest of four lakes that lie in the Joux Valley, which is flanked by 1300−1600 m a.s.l. mountains (Fig. 1a). Table 1 lists the lake’s main morphological and limnological features.
Methods
To pursue the research questions posed, we used an integrated approach combining paleolimnological and sedDNA proxies to reconstruct the multi-trophic dynamics (i.e., decomposers; bacteria, primary producers; photosynthetic plankton, primary consumers; cladocerans and chironomids, and secondary consumers; fish) over a period of ∼1000 years in Lake Joux. We then used a change-point analysis to identify major shifts in communities and tested for the occurrence of regime shifts using a modelling
Results
As detailed below, the data analysis revealed significant changes in communities at multiple levels across the food web. These changes reflect the ecosystem’s response to human and climate changes, including the physical and chemical properties of the lake. The shift from oligotrophic to eutrophic status, (Bosset, 1961) and the following re-oligotrophication of the lake (Lods-Crozet et al., 2006) reported in the literature, is partly reflected in the concentrations of total phosphorus measured
Dynamics of the transition and regime shift
The paleolimnological data from this study provided distinctive biostratigraphic signatures that suggests resilience of the lake over several hundreds of years followed by an ecosystem-level response to environmental forcing (González Sagrario et al., 2020). These changes are consistent with a possible transition from the Holocene to a proposed Anthropocene, with a stratigraphic signal around the mid-20th century of the Common Era. This transition marks an intensification of human impacts
Conclusions
The analyses presented above provide answers to the three research questions asked in this paper. First, our unique multi-level paleoreconstruction dataset compiles important biological change over the last 1000 years in Lake Joux and reveals enhanced human impact on the ecosystem over the second half of the 20th century, mainly linked to cultural eutrophication. Consequently, there was a rapid turnover in community composition in phytoplankton, Cladocera, and chironomid assemblages, with taxa
Data availability
The sequence data produced in this study have been deposited in the European Nucleotide Archive (ENA) with the study accession number PRJEB36317.
Funding
This work was made possible thanks to an Eawag Discretionary Fund and the financial contribution of Piet Spaak and Francesco Pomati at the Department of Aquatic Ecology, Eawag. M-E. Monchamp received support through a postdoctoral fellowship funded by GRIL, Liber Ero, and McGill University. M. Muschick was supported by the SNSF Sinergia grant CRSII5_183566.
CRediT authorship contribution statement
Marie-Ève Monchamp: Conceptualization, Data curation, Formal analysis, Investigation, Writing - original draft, Writing - review & editing, Visualization, Project administration, Funding acquisition. Rosalie Bruel: Formal analysis, Investigation, Visualization, Writing - review & editing. Victor Frossard: Investigation, Writing - review & editing, Resources. Suzanne McGowan: Investigation, Writing - review & editing, Resources. Marlène Lavrieux: Visualization, Writing - review & editing. Moritz
Declaration of Competing Interest
The authors report no declarations of interest.
Acknowledgements
We thank I. Brunner, A. Lück, and M. Thali for their work in the laboratory and M. Reyes and A. Zwyssig for sediment coring. We are grateful to J-C. Walser (Genetic Diversity Centre, ETH Zürich) for help with bioinformatics. We also thank Z.E. Taranu and S.R. Carpenter for their contribution to the statistical analyses. We thank A. L. Banderet, E. Jemmi, J. Kneubühler, I. Candolfi, S. Gerber, E. Herzog and T. Meyer zu Westram for helping with sieving core samples and screening for fish remains.
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Department of Biology, McGill University, Montreal, Quebec, Canada.
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Groupe de recherche interuniversitaire en limnologie (GRIL), Quebec, Canada.
- 3
Sorbonne University, UPEC, CNRS, IRD, INRAE, Institute d'Ecologie et des Sciences de l'Environnement de Paris, iEES-Paris, Paris, France.