Mediterranean-like “fall dump” events in the Baltic Sea

Abstract

In the Mediterranean Sea, organic carbon-rich sapropels have been deposited periodically over the last fifteen million years. Some sapropels are characterized by high contents of the mat-forming, planktonic diatom Pseudosolenia calcar-avis and the planktonic diatom Thalassionema nitzschioides as a result of their mass sinking in autumn (the so-called “fall dump”). The present study shows that fall dump events also occurred in the brackish Baltic Sea around 6300–5800 calibrated years before present (cal yr BP; present = AD 1950). In sediments from the northern Baltic Sea these events are evidenced by high contents of a lipid specific for P. calcar-avis (a C_25:2 highly branched isoprenoid alkene) and corroborated by fossil remains of both P. calcar-avis and T. nitzschioides. A biomarker index based on long-chain alkyl diol lipids indicates that mat-forming Proboscia diatoms were also present. High contents of calanoid resting eggs further suggest that the copepod population was stressed being unable to feed on such large diatoms. The fall dump events occurred during a complete stratification of the water column and euxinic conditions, as reflected by the redox-sensitive trace metal uranium, allowing upward diffusion of nutrients and the growth of rhizosolenid mat-forming diatoms in a deep chlorophyll maximum. Synchronous remains of P. calcar-avis in the central Baltic Sea further suggest that these events occurred on a basin-wide scale.

Keywords

alkyl diols Bothnian Sea calanoid resting eggs diatom microfossils highly branched isoprenoid alkene Holocene Thermal Maximum Pseudosolenia calcar-avis Proboscia diatoms redox-sensitive uranium Thalassionema nitzschioides

Introduction

Sapropels are organic-rich deposits known for example from the Mediterranean Sea and the Black Sea, as the semi-enclosed nature of their basin causes their systems to be very sensitive to climatic perturbations (Rohling et al., 2015; Wegwerth et al., 2018). In the Mediterranean Sea, sapropels are thought to have formed when river discharge and runoff into the marginal basins increased. The low-density fresh water formed a lid at the surface that reduced or even prevented overturning circulation and deep water formation. As a result, the supply of oxygen to the deep water diminished, potentially causing anoxia and even euxinia (sulphidic conditions) and favoring organic matter preservation. Nutrient input increased with river outflow as well, thereby increasing primary production, the export of organic carbon to deep water and, consequently, oxygen consumption (Rohling et al., 2015). Although sapropels have been studied thoroughly, the processes involved in the formation of such organic-rich layers are still not fully understood. While some sapropels have been studied in detail in terms of primary productivity using diatom microfossils (Kemp et al., 1999, 2000; Koizumi and Masamichi, 2006), diatom frustules easily undergo differential dissolution when sinking through the water column and in the sediment (Barker et al., 1994), that may result in incomplete or biased palaeoenvironmental information. Studying sapropels formed in different environments and applying alternative proxies may improve understanding of these peculiar events.

The Baltic Sea (Figure 1a) is a semi-enclosed basin and is the world’s second-largest brackish sea after the Black Sea. Saline waters from the North Sea entering the Baltic Sea in its south-western part via the Skagerrak are increasingly diluted by riverine freshwater input. As a result, the Baltic Sea is characterized by both a south-western to north-eastern horizontal salinity gradient from 25 to <2 g kg⁻¹ at the surface and a strong vertical stratification (Figure 1b; Snoeijs-Leijonmalm and Andrén, 2017). In the deep East Gotland Basin (EGB; 249 m), a stable pycnocline located currently between 50 and 100 m water depth separates surface waters with salinity around 7 g kg⁻¹ from deeper waters with salinity >11 g kg⁻¹. This pronounced vertical stratification limits the vertical exchange of water masses, resulting in oxygen-depleted and even euxinic bottom waters. Sapropelic sediments were deposited in these deep basins during relatively warm periods: since ca. 1950 CE, during the Medieval Warm Period (700–1800 cal yr BP) and between 4000 and 7000 cal yr BP, that is during most of the Holocene Thermal Maximum (Jilbert et al., 2015; Reinholdsson et al., 2013; Zillén et al., 2008). The deposition of these sediments was most likely related to both increased stratification and primary production (Jilbert et al., 2015). In the present study, the analyses of diatom-specific lipid biomarkers combined with diatom microfossils, calanoid resting eggs, and trace metals allowed characterizing the formation, structure and biological effects of two Mid-Holocene events resembling Mediterranean sapropels, but in a brackish environment.

Figure 1.

Geography and salinity gradients of the Baltic Sea. (a) Location of sediment core Pos435/10-4. (b) Salinity change along a transect from the Skagerrak to the Bothnian Bay via the East Gotland Basin (EGB). Salinity data from World Ocean Atlas 2018 plotted with the Ocean Data View software.

Methods

Sediment core Pos435/10-4 (62°52.2′N, 19°02.6′E; 952 cm long; 214 m water depth) was retrieved from a deep basin located in the north-western Bothnian Sea using a gravity corer (Figure 1a). The age model of the core has been published in Häusler et al. (2017). The present study focuses on sediments from the depth interval 771–893 cm dated 5084–6989 cal yr BP. The age model for this interval is constrained by seven radiocarbon dates of bulk sediment and calanoid resting eggs with error bars of ±30 yr. After total sediment digestion with a mixture of HNO₃, HF, and HClO₄ as described in Dellwig et al. (2021), the contents of Al and Mn were measured by inductively coupled plasma–optical emission spectroscopy (ICP-OES; iCAP 6400 Duo; Thermo Fisher Scientific) and U by ICP–mass spectrometry (ICP-MS; iCAP Q; Thermo Fisher Scientific). Diatom frustules were determined quantitatively with a transmitted light microscope (Zeiss Axioscope A1) after treating the dry sediments with HCl and H₂O₂ (Kaiser et al., 2016). Highly branched isoprenoid (HBI) alkenes and long chain alkyl diols (LCD) were extracted, purified, and analyzed by gas chromatography mass spectrometry (GC-MS; Agilent Technologies 7890B GC system and 5977B Mass Selective Detector) and GC-FID (flame ionization detection; Thermo Scientific TraceUltra GC) as described in Kaiser et al. (2016). LCDs were detected using single ion monitoring of mass-to-charge ratios (m/z) 299 (C₂₈ 1,14-alkyl diol), 313 (C₂₈ 1,13-alkyl diol), 327 (C₃₀ 1,14-alkyl diol), and 341 (C₃₀ 1,13-alkyl diol) ions (Willmott et al., 2010). The content of the C_25:2 HBI alkene was normalized to TOC to account for the potential effect of organic matter degradation. The diol index (DI) was calculated as defined by Willmott et al. (2010): DI = (C₂₈ + C₃₀ 1,14-diols)/[(C₂₈ + C₃₀ 1,14-diols) + (C₂₈ + C₃₀ 1,13-diols)]. The identification of diatom valves and the ecological information on the species are based on Snoeijs and Kasperovičienė (1996).

Results and discussion

During the Holocene Thermal Maximum (HTM), sapropelic sediments with a TOC content between 5% and 20% (Figure 2a) were deposited in the Bothnian Sea (Häusler et al., 2017; Jilbert et al., 2015). The time interval between 6300 and 6000 cal yr BP is characterized by high contents of C_25:2 HBI alkene (up to 275 µg gTOC⁻¹; Figure 2b), a lipid specific for the diatom P. calcar-avis (Kaiser et al., 2016). A second increase occurred between 5900 and 5800 cal yr BP. P. calcar-avis is a large (up to 1 mm in length) planktonic diatom thriving in temperate to warm waters with salinities between 8 and 18 g kg⁻¹ (Karpinsky, 2010). As other Rhizosolenids, P. calcar-avis is a mat-forming diatom adapted to stratified, oligotrophic conditions reproducing rapidly under low light conditions characteristic of the lower part of the surface mixed layer, or deep chlorophyll maximum (DCM; Goldman and McGillicuddy, 2003). Both individual cells and mats of rhizosolenid diatoms can regulate their buoyancy to migrate between deep nitrate pools (as deep as 140 m) and shallower waters to photosynthesize (Pilskaln et al., 2005). Relatively high DI values (Figure 2c) indicate the presence of Proboscia diatoms (de Bar et al., 2018; Willmott et al., 2010). These latter are large (up to 1 mm in length) rhizosolenid diatoms adapted to oligotrophic, cold to temperate waters with a salinity between 15 and 35 g kg⁻¹, and bloom mainly in summer and fall (Lange et al., 1992). As for P. calcar-avis, Proboscia diatoms are adapted to exploit a deep nutricline in a stratified water column (Kemp et al., 2000). Therefore, the presence of both P. calcar-avis derived C_25:2 HBI alkene and 1,14-alkyl diols produced by Proboscia diatoms suggest a salinity around 15–18 g kg⁻¹ that is about 10–13 g kg⁻¹ above modern values, oligotrophic conditions and a stratified water column in the Bothnian Sea between 6300–6000 and 5900–5800 cal yr BP.

Figure 2.

Sediment records from core Pos435/10-4 (Bothnian Sea). (a) Total organic carbon (TOC) content (Häusler et al., 2017). (b) Content of C25:2 highly branched isoprenoid (HBI) alkene. (c) Diol Index (DI). (d) Diatom assemblage. (e) U/Al. (f) Mn content. (g) Content of calanoid resting eggs (Häusler et al., 2017).

The assemblage of the most abundant planktonic diatoms (Figure 2d) suggests a brackish and eutrophic to mesotrophic environment before 6300 cal yr BP as indicated by relatively high abundances of Cyclotella choctawhatcheeana (relative abundance of 50–70%; salinity tolerance: 2–9 g kg⁻¹; temperate species) and Thalassiosira hyperborea (2–6%; 2–9 g kg⁻¹; cold). P. calcar-avis first appears around 6500 cal yr BP. Between 6300 and 5950 cal yr BP, Thalassionema nitzschioides (2–58%; 8–34 g kg⁻¹; warm to temperate) and Thalassiosira levanderi (6–30%; 18–30 g kg⁻¹; temperate to cold) imply brackish to marine waters beside P. calcar-avis (8–25%), but mesotrophic conditions. After 5850 cal yr BP, T. nitzschioides disappears while Pauliella taeniata increases (30–40%; 18–30 g kg⁻¹; temperate to cold), what suggests both a gradual cooling trend and more mesotrophic conditions. Interestingly, Fragilariopsis cylindrus (3–5%; 9–18 g kg⁻¹; cold), which is most abundant between 6300 and 6000 cal yr BP, indicates cold and mesotrophic conditions and the presence of winter sea ice. Therefore, increased stability of the water column and stratification could have favored species such as T. nitzschioides and T. levanderi in the mesotrophic conditions of the spring bloom (Andrén et al., 2020) and the presence of P. calcar-avis in summer oligotrophic conditions (Kemp et al., 1999).

Astonishingly, the diatom assemblage of the Bothnian Sea between 6300 and 6000 cal yr BP closely resembles the assemblage found in some Mediterranean sapropels, which is also dominated by P. calcar-avis (40%) and T. nitzschioides (10%) (Kemp et al., 1999; Koizumi and Masamichi, 2006; Schrader and Matherne, 1981). Kemp et al. (1999, 2000) suggested that large rhizosolenid diatoms such as P. calcar-avis can proliferate in a DCM of stratified waters in summer contributing to sediment accumulation from a fall dump linked to winter mixing and mass sedimentation of diatoms. This fall dump could rival or exceed the spring bloom (T. nitzschioides). The Baltic Sea biomarker record suggests that Proboscia diatoms, which are present together with other rhizosolenid diatoms in modern summer sediment traps of the Skagerrak (Lange et al., 1992), were also involved in fall dump events, but their remains were mainly not preserved in the sediments (Koizumi and Masamichi, 2006). Kemp et al. (1999, 2000) further proposed that the enhanced productivity characterizing fall dump events was driven by increased nutrient input from terrestrial runoff, but these nutrients were trapped at depth in a nutricline.

The data from the Bothnian Sea provide further information on the environmental changes related to the formation of fall dump events. During the HTM, the Baltic Sea realm was characterized by temperatures 2°C–2.5°C above modern means (Borzenkova et al., 2015). However, around 6000 cal yr BP a cooling event occurred in the Baltic Sea realm, which was contemporaneous to a global cold event dated between 6500 and 5900 yr BP and possibly related to reduced solar activity (Wanner et al., 2011). On the one hand, assuming that periods with solar minima may cause increased rainfall in northern Europe (Martin-Puertas et al., 2012), an increased stratification of the Baltic Sea related to a surface salinity decrease during this period is conceivable. In the Bothnian Sea, surface salinity has been estimated to be 8–10 g kg⁻¹ between 6600 and 5800 cal yr BP (Widerlund and Andersson, 2011). On the other hand, available data suggest that bottom water salinity was around 13 g kg⁻¹ due to intrusions of saline waters from the North Sea into the northern Baltic Sea, which was still ca. 130 m deeper than today due to glacial loading and subsidence (Gustafsson and Westman, 2002; Jilbert et al., 2015). Therefore, it can be assumed that the Bothnian Sea water column was pronouncedly stratified during the HTM. The presence of euxinic bottom waters is indicated by elevated U/Al values (Figure 2e), which are in line with levels seen in Mediterranean and Black Sea sapropels (Brumsack, 2006) and reach values observed in the modern sapropel of the highly euxinic EGB Dellwig et al., 2021). However, two periods with Mn maxima around 6300 and 6000–5900 cal yr BP (Figure 2f) indicate the presence of Mn carbonate (Ca-rich rhodochrosite), which forms when oxygen-containing water intrudes the euxinic basin as observed in sub-recent sediments of the EGB (Dellwig et al., 2018). Therefore, these two periods were most likely characterized by more frequent or stronger intrusions of oxygenated and salty North Sea waters into the Bothnian Sea, strengthening the vertical salinity gradient on the one hand, but resulting in an unstable redox setting with hypoxic bottom waters on the other hand. During the subsequent stagnation periods, that is, between 6300 and 6000 cal yr BP and 5900–5800 cal yr BP, pronounced euxinic conditions were established at depth. In analogy to the stagnation period that occurred in the Baltic Sea during the 1980s, nitrate concentration decreased, while phosphate and NH₄ escaped from the sediments, resulting in high concentrations of these nutrients at depth (Fonselius and Valderrama, 2003; Jilbert et al., 2015). Along with the expansion of euxinic waters, the redoxcline rose up until reaching the base of the photic zone. This likely favored the growth of rhizosolenid mat-forming diatoms in a pronouncedly stratified water column and a nutrient-rich DCM. As the water column of the eastern Mediterranean Sea may have also been intermittently oxygenated during S1 sapropel (Casford et al., 2003), a similar process of increased stratification, vertical expansion of euxinic conditions, and the upward diffusion of nutrients into the deep photic zone may explain Mediterranean fall dump events.

Both periods of increased P. calcar-avis and Proboscia diatom contents correspond to the occurrence of high amounts of calanoid resting eggs (Figure 2g), which are produced by marine copepods to survive adverse environmental conditions. Temperature is most likely the primary environmental driver for resting egg production. However, other factors such as food availability, abrupt salinity changes, crowding, or oxygen deficiency can elicit egg production as well (Holm et al., 2018). While the effect of these different factors cannot be differentiated here, it has been observed in a Black Sea autumn bloom that an increase in the abundance of the relatively large diatom P. calcar-avis negatively impacted the grazing rate of copepods because these latter prefer phytoplankton cells with a smaller size range (10–40 µm; Stel’makh et al., 2009). Therefore, a drop in food availability due to a high abundance of large diatoms such as P. calcar-avis and Proboscia diatoms may have contributed to an increased production of calanoid resting eggs.

High abundances of P. calcar-avis remains in the Bothnian Sea sediments at 6300–6000 cal yr BP and 5900–5800 cal yr BP seems to have equivalents not only in the adjacent Ångermanälven River estuary (Warnock et al., 2018), but also in the central Baltic Sea considering age model uncertainties. In the EGB, two maxima in P. calcar-avis remains occurred around 6000 cal yr BP (Andrén et al., 2000). In the Landsort Deep, a single peak of P. calcar-avis is apparent around 6800 cal yr BP, but the temporal resolution of the record is relatively low (>100 years) and the dating uncertainties are relatively high (±600 years; van Wirdum et al., 2019). Up to 2 mm-thick layers consisting almost entirely of P. calcar-avis remains with about the same age were also found in Landsort Deep sediments (Sohlenius and Westman, 1998). It seems therefore that Mediterranean-like fall dump events occurred basin-wide in the Baltic Sea around 6000 cal yr BP. Assuming that these events occurred synchronously, they may represent valuable isochrones to correlate Baltic Sea Mid-Holocene sedimentary records.

Conclusions

A multi-proxy approach of Mid-Holocene sediments from the northern Baltic Sea allowed characterizing the formation of two Mediterranean-like fall dump events that occurred between 6300 and 5800 cal yr BP. A strengthened stratification, the expansion of euxinic conditions and the upward diffusion of nutrients favored the blooms of both the diatoms T. nitzschioides and T. levanderi in spring at the near-surface and the mat-forming diatoms P. calcar-avis and Proboscia in a summer DCM. Blooms of such large diatoms may have obliged copepods to produce resting eggs as surviving strategy. These fall dump events likely occurred on a basin-wide scale.

Footnotes

Acknowledgements

We would like to thank two anonymous reviewers for their helpful comments. We are greatful to Nadine Hollmann, Ines Scherff and Anne Köhler for their lab work.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Jérôme Kaiser

References

Andrén

Kunzendorf

(2000) Holocene history of the Baltic Sea as a background for assessing records of human impact in the sediments of the Gotland basin. Holocene 10: 687–702.

Andrén

van Wirdum

Norbäck Ivarsson

, et al. (2020) Medieval versus recent environmental conditions in the Baltic proper, what was different a thousand years ago? Palaeogeography Palaeoclimatology Palaeoecology 555: 109878.

Barker

Fontes

Gasse

, et al. (1994) Experimental dissolution of diatom silica in concentrated salt solutions and implications for paleoenvironmental reconstruction. Limnology and Oceanography 39: 99–110.

Borzenkova

Zorita

Borisova

, et al. (2015) Climate change during the Holocene (past 12,000 years). In: The Bacc Ii Author Team (ed.) Second Assessment of Climate Change for the Baltic Sea Basin. Regional Climate Studies. Cham: Springer, pp.25–49.

Brumsack

H-J

(2006) The trace metal content of recent organic carbon-rich sediments: Implications for Cretaceous black shale formation. Palaeogeography Palaeoclimatology Palaeoecology 232: 344–361.

Casford

JSL

Rohling

Abu-Zied

, et al. (2003) A dynamic concept for eastern Mediterranean circulation and oxygenation during sapropel formation. Palaeogeography Palaeoclimatology Palaeoecology 190: 103–119.

de Bar

Stolwijk

McManus

, et al. (2018) A Late Quaternary climate record based on long-chain diol proxies from the Chilean margin. Climate of the Past 14: 1783–1803.

Dellwig

Schnetger

Meyer

, et al. (2018) Impact of the major Baltic inflow in 2014 on manganese cycling in the Gotland Deep (Baltic Sea). Frontiers in Marine Science 5: 248.

Dellwig

Wegwerth

Arz

(2021) Anatomy of the major Baltic inflow in 2014: Impact of manganese and iron shuttling on phosphorus and trace metals in the Gotland Basin, Baltic Sea. Continental Shelf Research 223: 104449.

10.

Fonselius

Valderrama

(2003) One hundred years of hydrographic measurements in the Baltic Sea. Journal of Sea Research 49: 229–241.

11.

Goldman

McGillicuddy

DJJ

(2003) Effect of large marine diatoms growing at low light on episodic new production. Limnology and Oceanography 48: 1176–1182.

12.

Gustafsson

Westman

(2002) On the causes for salinity variations in the Baltic Sea during the last 8500 years. Paleoceanography 17: 1–14.

13.

Häusler

Moros

Wacker

, et al. (2017) Mid- to late Holocene environmental separation of the northern and central Baltic Sea basins in response to differential land uplift. Boreas 46: 111–128.

14.

Holm

Kiørboe

Brun

, et al. (2018) Resting eggs in free living marine and estuarine copepods. Journal of Plankton Research 40: 2–15.

15.

Jilbert

Conley

Gustafsson

, et al. (2015) Glacio-isostatic control on hypoxia in a high-latitude shelf basin. Geology 43: 427–430.

16.

Kaiser

Belt

Tomczak

, et al. (2016) C₂₅ highly branched isoprenoid alkenes in the Baltic Sea produced by the marine planktonic diatom Pseudosolenia calcar-avis. Organic Geochemistry 93: 51–58.

17.

Karpinsky

(2010) Pseudosolenia calcar-avis (Bacillariophyta, Centrophyceae) in the Caspian Sea. Russian Journal of Biological Invasions 1: 81–86.

18.

Kemp

AES

Pearce

Koizumi

, et al. (1999) The role of mat-forming diatoms in the formation of Mediterranean sapropels. Nature 398: 57–61.

19.

Kemp

AES

Pike

Pearce

, et al. (2000) The “Fall dump” — a new perspective on the role of a “shade flora” in the annual cycle of diatom production and export flux. Deep Sea Research Part I:I Topical Studies in Oceanography 47: 2129–2154.

20.

Koizumi

Masamichi

(2006) Diatoms in the eastern Mediterranean sapropels. Nova Hedwigia 130: 185–200.

21.

Lange

Hasle

Syvertsen

(1992) Seasonal cycle of diatoms in the Skagerrak, North Atlantic, with emphasis on the period 1980–1990. Sarsia 77: 173–187.

22.

Martin-Puertas

Matthes

Brauer

, et al. (2012) Regional atmospheric circulation shifts induced by a grand solar minimum. Nature Geoscience 5: 397–401.

23.

Pilskaln

Villareal

Dennett

, et al. (2005) High concentrations of marine snow and diatom algal mats in the North Pacific subtropical gyre: Implications for carbon and nitrogen cycles in the oligotrophic ocean. Deep-Sea Research Part I: Oceanographic Research Papers 52: 2315–2332.

24.

Reinholdsson

Snowball

Zillén

, et al. (2013) Magnetic enhancement of Baltic Sea sapropels by greigite magnetofossils. Earth and Planetary Science Letters 366: 137–150.

25.

Rohling

Marino

Grant

(2015) Mediterranean climate and oceanography, and the periodic development of anoxic events (sapropels). Earth-Science Reviews 143: 62–97.

26.

Schrader

Matherne

(1981) Sapropel formation in the eastern Mediterranean Sea: Evidence from preserved opal assemblages. Micropaleontology 27: 191–203.

27.

Snoeijs-Leijonmalm

Andrén

(2017) Why is the Baltic Sea so special to live in? In: Snoeijs-Leijonmalm

Schubert

Radziejewska

(eds) Biological Oceanography of the Baltic Sea. Dordrecht: Springer, pp.23–84.

28.

Snoeijs

Kasperovičienė

(1996) Intercalibration and Distribution of Diatom Species in the Baltic Sea 4. Uppsala: The Baltic marine Biologists Publication 16d, Opulus Press.

29.

Sohlenius

Westman

(1998) Salinity and redox alternations in the northwestern Baltic proper during the late-Holocene. Boreas 27: 101–114.

30.

Stel’makh

Babich

Tugrul

, et al. (2009) Phytoplankton growth rate and zooplankton grazing in the western part of the Black Sea in the autumn period. Oceanology 49: 83–92.

31.

van Wirdum

Andrén

Wienholz

, et al. (2019) Middle to late Holocene variations in salinity and primary productivity in the central Baltic Sea: A multiproxy study from the Landsort Deep. Frontiers in Marine Science 6: 51.

32.

Wanner

Solomina

Grosjean

, et al. (2011) Structure and origin of Holocene cold events. Quaternary Science Reviews 30: 3109–3123.

33.

Warnock

Bauersachs

Kotthoff

, et al. (2018) Holocene environmental history of the Ångermanälven estuary, northern Baltic Sea. Boreas 47: 593–608.

34.

Wegwerth

Eckert

Dellwig

, et al. (2018) Redox evolution during Eemian and Holocene sapropel formation in the Black Sea. Palaeogeography Palaeoclimatology Palaeoecology 489: 249–260.

35.

Widerlund

Andersson

(2011) Late holocene freshening of the Baltic Sea derived from high-resolution strontium isotope analyses of mollusk shells. Geology 39: 187–190.

36.

Willmott

Rampen

Domack

, et al. (2010) Holocene changes in Proboscia diatom productivity in shelf waters of the north-western Antarctic Peninsula. Antarctic Science 22: 3–10.

37.

Zillén

Conley

Andrén

, et al. (2008) Past occurrences of hypoxia in the Baltic Sea and the role of climate variability, environmental change and human impact. Earth-Science Reviews 91: 77–92.