Spatial differences in dissolved silicon utilization in Lake Baikal, Siberia: Examining the impact of high diatom biomass events and eutrophication

Recent research has highlighted how Lake Baikal, Siberia, has responded to the direct and indirect effects of climate change (e.g., ice-cover duration), nutrient loading, and pollution, manifesting as changes in phytoplankton/zooplankton populations, community structure, and seasonal succession. Here, we combine and compare analyses of chlorophyll a (an estimate of total algal biomass), carotenoid pigments (biomarkers of algal groups), and lake water silicon isotope geochemistry (dSiDSi) to differentiate spatial patterns in dissolved silicon (DSi) uptake at Lake Baikal. A total of 15 sites across the three basins (south, central, and north) of Lake Baikal were sampled in August 2013 along a depth gradient of 0–180 m. Strong, significant correlations were found between vertical profiles of photic zone DSi concentrations and dSiDSi compositions (r520.81, p<0.001), although these are strongest in the central basin aphotic zone (r520.98, p<0.001). Data refute the hypothesis of DSi uptake by picocyanobacteria. Algal biomass profiles and high surface dSiDSi compositions suggest greater productivity in the south basin and more oligotrophic conditions in the north basin. dSiDSi signatures are highest at depth (20 m) in central basin sites, indicating greater (10–40%) DSi utilization at deep chlorophyll maxima. DSi limitation occurs in the pelagic central basin, probably reflecting a high diatom biomass bloom event (Aulacoseira baicalensis). Meanwhile in the more hydrologically restricted, shallow Maloe More region (central basin), both high dSiDSi compositions and picocyanobacteria (zeaxanthin) concentrations, respectively point to the legacy of an “Aulacoseira bloom year” and continuous nutrient supply in summer months (e.g., localized eutrophication). World-wide, climate warming is impacting freshwater ecosystems (e.g., O’Reilly et al. 2015) and, in many cases, its effects are superimposed upon anthropogenic catchment alteration, nutrient loading, and pollution (Jeppesen et al. 2011; Moss et al. 2011; Izmest’eva et al. 2016). Lake Baikal, the world’s deepest and most voluminous lake (containing up to 20% of the world’s unfrozen freshwater; Sherstyankin et al. 2006) is no exception. Over the past 60 yrs, surfacewater temperatures of Lake Baikal have increased up to 2.48C (Hampton et al. 2008; Shimaraev and Domysheva 2013), resulting in earlier lake ice-off dates and later ice-on dates, particularly in the southern basin (Todd and Mackay 2003; Hampton et al. 2008). Ice formation and retreat, plays an essential role in the thermal regime of Lake Baikal, promoting water column mixing and upper water column nutrient renewal in the spring, after ice-off. As such, late 20 Century climate change has altered the water column thermal structure, which in turn has altered the spatial patterns of phytoplankton biomass (Fietz et al. 2007) and food web structure (Hampton et al. 2008). Eutrophication has also been noted in the coastal and shallow bay regions of Lake Baikal (Kobanova et al. 2016), resulting in increases in cryptophyte blooms, toxin-forming cyanobacteria blooms and thick mats of the benthic, *Correspondence: [email protected] Additional Supporting Information may be found in the online version of this article. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 1 LIMNOLOGY and OCEANOGRAPHY Limnol. Oceanogr. 00, 2018, 00–00 VC 2018 The Authors Limnology and Oceanography published by Wiley Periodicals, Inc. on behalf of Association for the Sciences of Limnology and Oceanography doi: 10.1002/lno.10792 filamentous chlorophyte Spirogyra spp., and the non-native macrophyte Elodea canadensis (Kravtsova et al. 2014; Kobanova et al. 2016; Timoshkin et al. 2016). The combined effects of climate and eutrophication on food web structures across pelagic and shallow regions need to be addressed in Lake Baikal (O’Donnell et al. 2017). This is of particular importance, as bottom up controls (e.g., nutrient availability and temperature) on phytoplankton productivity, are not well understood. The limnological characteristics of Lake Baikal and importance of silicon stable isotope geochemistry Assessment of the internal fluxes of nutrients in Lake Baikal are an important prerequisite for evaluating the consequences of climate and anthropogenic changes (M€ uller et al. 2005). Spring pelagic upwelling lasts c. 35 days and between 20% and 60% of the lake area mixes vertically (Shimaraev et al. 2012). Complete deep-water surface renewal is within the range of every 8–19 yrs (Weiss et al. 1991; Hohmann et al. 1997; Peeters et al. 1997; M€ uller et al. 2005). Instead, the top 200–300 m of the Lake Baikal water column convectively mixes twice each year (Shimaraev et al. 1994). Dissolved silicon (DSi) is a vital nutrient for biomineralization in Lake Baikal (particularly in “Aulacoseira bloom years”: “Phytoplankton succession at Lake Baikal and seasonal nutrient uptake” section) and estimations of silicate residence time are between 100 yr and 170 yr (Falkner et al. 1997; Shimaraev and Domysheva 2004). Long-term export of DSi to Lake Baikal sediments (modelled to be 20–24%) is greater in the south than the north basin (Panizzo et al. 2017) due to better below-ice conditions (e.g., less snow cover and greater transparency), longer-ice free seasons, and subsequent enhanced diatom productivity. Surface-water DSi concentrations in Lake Baikal are predominantly derived from upwelling (630 mmol yr), rather than riverine inputs (312 mmol yr), and net sedimentation is estimated at c. 1170 mmol m yr (M€ uller et al. 2005). Silicon isotope geochemistry provides the unique opportunity to model DSi uptake across the lake, identify productivity “hotspots” and explore drivers of these trends. Silicon (Si), the second most abundant element in the earth’s crust (Epstein 1999), plays a key role in global biogeochemical cycling. The dissolved phase or DSi, also known as orthosilicic acid (Si(OH)4), is an important nutrient in aquatic systems and has such been found to have an intimate relationship with the carbon cycle (via the oceanic biogeochemical pump; Pondaven et al. 2000). Si has three stable isotopes (Si, Si, and Si), which are reported via the delta notation dSi as the ratio between Si/Si (or previously dSi as the ratio between Si/Si) compared to the same ratio in the standard reference material NBS 28. These three isotopes of Si permit the method to be used as a proxy for constraining the silicon cycle due to the significant fractionations that occur during different processes. For example, silicon isotope ratios of DSi in waters (referred to as dSiDSi hereafter) can be used as a tracer of multiple processes including weathering congruency (Fontorbe et al. 2013; Hughes et al. 2013; Frings et al. 2015), biological uptake and land-use changes (Delvaux et al. 2013), and anthropogenic catchment impacts (Hughes et al. 2012). In lakes, dSiDSi traces DSi nutrient utilization by siliceous organisms (Alleman et al. 2005; Opfergelt et al. 2011; Panizzo et al. 2016, 2017). Lake Baikal summer dSiDSi water column compositions have been demonstrated to provide a proxy for spring diatom utilization (Panizzo et al. 2016, 2017). For example, diatoms discriminate against the heavier Si isotope during DSi uptake with the lighter Si isotope incorporated via biomineralization, leading to the residual DSi pool becoming enriched in Si. Panizzo et al. (2016) identified the progressive isotopic enrichment of diatoms (dSidiatom) during spring bloom development, so that summer compositions (when stratification ensues) reflect the legacy of this spring diatom bloom. Here, we explore similarities and differences in biogeochemical cycling across the upper water column (0–180 m) of Lake Baikal. We present the first lake system comparisons of phytoplankton biomass [chlorophyll a (Chl a) concentrations], phytoplankton composition (algal chlorophyll and carotenoid pigments), and seasonal DSi utilization (dSiDSi). Combined, these proxies provide the opportunity to test the hypothesis that picocyanobacteria do not substantially alter the DSi pool, when their populations dominate the summer phytoplankton (“Phytoplankton succession at Lake Baikal and seasonal nutrient uptake” and “Examining main drivers behind DSi uptake at Lake Baikal” sections). Our second objective is to better understand how internal cycling of DSi varies spatially across Lake Baikal (both in pelagic and more shallow regions) (“Spatial patterns of DSi utilization at Lake Baikal” section). Finally, the novel approach of silicon isotope geochemistry will be used to quantify seasonal DSi utilization at depth and explore episodes of localized nutrient exhaustion, as a response to both these natural and anthropogenic pressures (“Quantifying sub-surface DSi utilization at central basin sites in Lake Baikal” section). Phytoplankton succession at Lake Baikal and seasonal nutrient uptake Annually, the first phytoplankton (diatom) blooms in Lake Baikal occur in spring under ice, and thus lake-ice duration and transparency are crucial to their development (Jewson et al. 2009; Moore et al. 2009). Seasonal succession of phytoplankton blooms is linked to the timing of ice-off (end of May–June) when a rapid period of diatom cell-division occurs, as a result of the turbulent mixing of the water column to a depth of c. 100 m (Popovskaya 2000; Fietz et al. 2005a). In autumn (after October), as summer stratification breaks down, a second peak in diatoms (including Cyclotella minuta species) occurs due to turbulent mixing and cell Panizzo et al. Melosira blooms and eutrophication in Lake Baikal