Diatom-based indications of an environmental regime shift and droughts associated with seasonal monsoons during the Holocene in Biển Hồ maar lake,the Central Highlands,Vietnam

Abstract

The interactions of the different monsoon systems across Southeast Asia create extreme climate phenomena. Central Vietnam, located near the centre of this transitional region, has encountered numerous effects. As a result, its sediments from lakes or speleothems are valuable archives for interpreting past climate variability. However, there is still a lack of high-resolution paleoenvironmental and palaeoclimatic reconstructions during the Holocene in Vietnam. Our study presents a paleoenvironmental diatom-based record of sediment cores collected from Biển Hồ maar lake (14°03′N, 108°00′E) in the Central Highlands of Vietnam covering nearly the entire Holocene. Based on changes in diatom assemblages in the sediment sequence, we identified two periods of the Early Holocene (~11,700–7800 cal BP) and the Mid- to Late-Holocene (~7800–360 cal BP), which mark a remarkable shift in the environment around Biển Hồ. Alternations of key diatom species during the Early Holocene indicate intensity variations between water-mixing and thermal stratification mechanisms in meso-eutrophic conditions. During the Mid- to Late-Holocene, the complete dominance of Aulacoseira granulata var. granulata implies year-round destratification and intense mixing of the lake water column in a permanently eutrophic environment. Its morphological variability reveals intervals of dry environmental conditions driven by pronounced droughts across the Asian continent.

Keywords

Central Highlands diatoms drought Holocene maar lake paleoenvironmental reconstruction seasonal monsoon Southeast Asia

Introduction

Numerous studies on climate patterns in the Southeast Asian region, particularly in Vietnam, have highlighted the complexity that arises when multiple monsoon subsystems operate concurrently within a specific geographical area (Buckley et al., 2014; Kaboth-Bahr et al., 2021; Wang and Lin, 2002; Wolf et al., 2023). The Central Highlands of Vietnam lies at the convergence point of three summer monsoon subsystems: the Indian Summer Monsoon (ISM), the East Asian Summer Monsoon (EASM), and the Northwest Pacific Summer Monsoon (NPSM) (Buckley et al., 2014; Wang and Lin, 2002). Additionally, the Northeast Winter Monsoon (NWM) serves as a counterpart to the ISM in this region and develops from the cold and dry East Asian Winter Monsoon (EAWM) commonly known as northwesterly winds across East Asia (Wolf et al., 2023). The NWM and EAWM originate from the Siberian High, a high-pressure system situated over the Siberian-Mongolia region and a low-pressure area over the Maritime Continent during winters (Chang et al., 2011; Chan and Li, 2004). The NWM, after traversing the South China Sea, is a substantial moisture source for Vietnam (Wolf et al., 2023). The evolution of the summer and winter monsoon subsystems has grown progressively complex and diverse due to ongoing climate change since the Late Pleistocene and anthropogenic global warming (Li et al., 2014; Kaboth-Bahr et al., 2021; Wolf, 2022). These mechanisms have given rise to extreme climatic events, including droughts in the Central Highlands already in the past (Nguyễn-Đình et al., 2022), and also leading to significant agricultural losses with profound socio-economic repercussions on local communities in modern times (Asia-CRCiS, 2016).

Located in the Central Highlands of Vietnam, Biển Hồ maar lake (14°03′N, 108°00′E) originated from the amalgamation of three volcanic craters (Ta-Hoa et al., 2015). Before its connection with an artificial reservoir in 1984 CE, the lake maintained a simple hydrological setup with no inflow or outflow, and its sediment accumulation primarily resulted from weathered materials eroded from the surrounding crater slopes was driven by the intensity of the summer monsoon subsystems (Nguyễn-Văn et al., 2022). Along with terrigenous material, aquatic organic matter, including diatoms, are the primary sources of the Biển Hồ lake sediments. Environmental changes during the most recent 70 years of lake history, reflected in the uppermost sedimentary and diatom records, have been published earlier (Nguyễn-Văn et al., 2022).

Diatoms and their morphology show sensitivity to various ecological variables. Due to the resistance to dissolution and breakage of their opaline silica frustules, diatoms have emerged as reliable bioindicators in contemporary environmental investigations and paleoenvironmental reconstructions, particularly focusing on lacustrine sediments (Mohanty et al., 2022; Wang et al., 2009, 2012; Winsborough, 2016). Especially, Aulacoseira granulata (Ehrenberg) Simonsen, a globally distributed species within its genus, displays adaptability and tolerance to a broad spectrum of environmental conditions (Wang et al., 2015). Blooms of A. granulata are typically associated with eutrophication (Gomes, 2000; Kamenir et al., 2004; Lepistö et al., 2006), increased turbidity and nutrient availability (Simiyu and Kurmayer, 2022). The morphological variability of this taxon has also been analysed to investigate its relationship with freshwater environmental features, such as the species valve diameter and mantle height positively correlating with more than one nutrient component (Gómez et al., 1995; Mohanty et al., 2022; O'Farrell et al., 2001; Poulickova, 2003; Turkia and Lepistö, 1999; Wang et al., 2015), or mantle height/valve diameter (H/D) and surface area/volume (SA/V) ratios negatively related to lake water- level and mixing (O'Farrell et al., 2001; Wang et al., 2009, 2015). However, palaeoclimatic records based on lake sediments and studies on modern diatoms in Vietnamese lakes remain notably scarce. Two studies analysed diatom assemblages and geochemical proxies from Ba Bể lake (Weide, 2012) and Ao Tiên (Fairy Pond) (Stevens et al., 2018) to point out monsoonal characteristics in the karst region of Northern Vietnam over the last 500 and 650 years, respectively. In the Central Highlands, two recent studies from Ea Tyn lake (Nguyễn-Đình et al., 2022) and Biển Hồ lake (Nguyễn-Văn et al., 2022) covering the past 1250 and 70 years, respectively, have revealed substantial responses in sedimentary, geochemical, geophysical and microfossil proxies that are attributed to both anthropogenic influences and the impact of monsoon subsystems on the lake ecosystems.

Our study here presents a paleoenvironmental diatom-based record from Biển Hồ lake, covering nearly the whole Holocene (Figure 1). Firstly, we define and describe diatom assemblages, explore their relationships with other diatom and sedimentation rate indices within the sediment sequence. Secondly, we measure the morphological parameters of Aulacoseira granulata var. granulata, including the valve diameter, mantle height, surface area, volume, H/D and SA/V ratios, then interpret their fluxes because of the dominance of this single taxon in the upper half of the sequence but with wide morphological variety.

Figure 1.

Location of Biển Hồ maar lake in Asia and Vietnam, along with the coring site in 2021. The bathymetric map is based on data from Nguyễn-Văn et al. (2022).

Materials and methods

Materials and sample preparation

From the deepest part of Biển Hồ lake (Figure 1), several sediment cores have been retrieved between 2017 and 2021 (Nguyễn-Văn et al., 2023). During the latest coring expedition in April 2021, two parallel and overlapping piston cores (BHM-21 A and B) were retrieved, yielding a sediment sequence of 25 m in length, which reveals a continuous sedimentation from at least ~55,000 calibrated years before present (cal BP) (Ojala et al., 2023) and offers a comprehensive and uninterrupted archive of the lake’s depositional evolution during Late Pleistocene and Holocene times. We here focus only on the Holocene part of the core, that is the depth interval of 58–575 cm corresponding to the ages of ~12,370–360 cal BP. The cross-correlation of all core segments from Biển Hồ lake was based on whole core logging profiles, sedimentary facies description, core photographs, loss-on-ignition, and magnetic susceptibility (Nguyễn-Văn et al., 2023; Ojala et al., 2023). A detailed description of the age-depth model BHM21-5 for the 25-m-long sediment sequence based on ¹³⁷Cs, ¹⁴C and paleomagnetic measurements has already been published by Ojala et al. (2023). The same age-depth model is also applied here and was used to determine the strategy for our diatom analysis and guide environmental interpretations in this study. The sequence shows a homogenous sediment composition with a high water content (~80 wt. %) and varying organic matter content (10–30 wt. %). We identified two main lithofacies, including (1) dark olive silty clay and (2) olive-grey diatom-rich silty clay.

Diatom method

For diatom analysis, we sampled the 58–575 cm section of the BHM-21 cores in 8 cm intervals, corresponding to timesteps of approx. 180 years on average. Sixty-seven samples were processed for the next steps. Diatom slide preparation followed standard procedures with dilution factors recorded during cleaning processes using H₂O₂ (Renberg, 1990) and distilled water from an initial 1 cm³ of each raw sample. A total of 400 diatom valves were counted and identified as species per sample. Diatom valve concentration was estimated by a semi-quantitative analysis via counting valves within a known area on a 22 mm × 22 mm square slide prepared from a 0.5 mL aliquot from a 10 mL suspension of 1 cm³ raw sediments. The analysis was carried out according to an assumption of the random diatom distribution in the samples (Wolfe, 1997). The identification and nomenclature of diatoms were based on a variety of sources, including taxonomic, nomenclatural, and distributional databases and studies (Guiry and Guiry, 2023; Jardim Botânico do Rio de Janeiro, 2023; Jüttner et al., 2023; Kociolek et al., 2023; Potapova et al., 2023; Spaulding et al., 2022; Tremarin et al., 2014).

A ratio exhibiting the abundance of planktonic taxa compared with a total of facultative planktonic and benthic taxa is symbolised as P/FB. The planktonic group refers to epilimnetic species, including Aulacoseira spp. (dominant in increased turbulence and deeper epilimnion environments) and Discostella stelligera (Cleve & Grunow) Houk & Klee (prevalent in shallower epilimnion environments) (Bradbury and Dieterich-Rurup, 1993; Kireta, 2018; Reynolds et al., 2002; Saros et al., 2012). The facultative planktonic and benthic group is mainly represented by fragilarioid Pseudostaurosira brevistriata (Grunow) D.M.Williams & Round, while benthic species only periodically appear with very low percentages in the Biển Hồ sediment sequence. The contrasting development of planktonic taxa and facultative planktonic taxa (Zhang et al., 2014), as well as planktonic taxa and benthic taxa (Hofmann et al., 2020; Liu et al., 2020), has been observed concerning water level variations, but we also discuss other ecological changes such as the lake water physical disturbance and circulation from the P/FB ratio since the abundance of facultative planktonic taxa is driven by various factors (Anderson, 2000; Zhang et al., 2016). Additionally, the switching between benthic species to planktonic species is often used as an indicator of determining the diversity and biomass of diatom communities related to water-mixing and eutrophication (Hall and John, 1999; Lei et al., 2021; Liu et al., 2020; Rühland et al., 2015). Therefore, in this study, we calculated and used the P/FB ratio to complement the diatom assemblages in reflecting fluctuations in the Biển Hồ diatom diversity and water level during the Holocene.

Regarding the morphological variability of A. granulata var. granulata, valve diameter and mantle height parameters were measured in 100 valves per sample. Furthermore, the surface area and volume of the valves were calculated based on the valve diameter and mantle height using geometric equations (Gómez et al., 1995). The ratios of mantle height over valve diameter (H/D) and surface area over volume (SA/V) were also figured.

Statistical methods

The diatom percentage data and zonation were computed and presented employing the CONISS method implemented in TILIA software version 3.0.1. Graph design and Principal Component Analysis (PCA) were conducted using the C2 data analysis programme version 1.8.0 (Juggins, 2007) on the relative abundance dataset of diatom species. Before PCA, the dataset underwent logarithmic transformation and standardisation (Baxter, 1995) due to significant disparities in the relative abundance between a few dominant taxa and most of the remaining ones, which appear sporadically. Species variables were logarithmically transformed, and then, sample scores within the dataset were standardised and plotted on the PCA space to assess similarities and differences between samples based on their distribution patterns (Figure 5). Finally, IBM SPSS Statistics software version 2.6 was used to calculate Pearson Correlations for various variables (Field, 2013).

Results

Diatom assemblage zones

Of the 41 diatom species identified in the Holocene sequence of Biển Hồ lake, the planktonic forms Aulacoseira spp. and D. stelligera are largely dominating. Based on transitions in relative abundances of indicative species within the genus Aulacoseira Thwaites and the two taxa D. stelligera and P. brevistriata, two diatom assemblage zones (containing subzones abbreviated as DAZs) were divided for the Holocene sequence. Zone 1, including three sub-zones DAZ 1A, 1B and 1C, and Zone 2, including four sub-zones DAZ 2A, 2B, 2C and 2D, correspond to the Early and the Mid- to Late-Holocene, respectively (Table 1 and Figure 2). The defined zones were later shifted than the formal Early and Middle Holocene boundary recognised by Walker et al. (2012) at 8200 cal BP. In our study, the diatoms are indicators of the paleoenvironmental conditions, therefore, the divided zones were used to present results.

Table 1.

Relative abundances of the five most dominant species in Biển Hồ lake are considered as a criterion for clustering diatom assemblages.

Diatom assemblage zones		Ages (cal BP)	Dominant diatom percentages (median of counting, %)
Diatom assemblage zones		Ages (cal BP)	Aulacoseira granulata var. granulata	Aulacoseira granulata var. angustissima	Aulacoseira veraluciae	Discostella stelligera	Pseudostaurosira brevistriata
Zone 2 (Mid- to Late- Holocene)	DAZ 2D	~450–360	92.1	0	0	0	4.4
	DAZ 2C	~2600–450	96	0	0	0	1.5
	DAZ 2B	~5500–2600	93.5	0	0	0	4.5
	DAZ 2A	~7800–5500	97.2	0	0	0	1.7
Zone 1 (Early Holocene)	DAZ 1C	~9800–7800	0.5	2.6	75.2	6.1	6.1
	DAZ 1B	~11,500–9800	0.5	6.4	51.7	28	6.2
	DAZ 1A	~11,700–11,500	0	4	75.7	9.2	6.9
Late Pleistocene		~12,370–11,700	0	0.7	35.7	23.5	29.5

Figure 2.

Stratigraphic diagram showing variations in the relative abundances (%) of 17 taxa (most common), the diatom valve concentration (×10⁶ valves.cm⁻³), and the P/FB ratio. Other species observed occasionally with less than 1% are not drawn. The diatom valve concentration and the P/FB ratio indices are smoothed as green and blue lines, respectively. The DAZs are separated based on the CONISS cluster analysis result, which is also confirmed by the PCA analysis (Figure 5).

Late Pleistocene (~12,370–11,700 cal BP)

The diatom assemblage around the end of the Late Pleistocene was characterised by three dominant species, including Aulacoseira veraluciae Tremarin, Torgan & T.Ludwig, P. brevistriata, and D. stelligera with relatively equal proportions of each species. Valves of A. granulata are very few in the pre-Holocene interval (Table 1 & Figure 2).

Zone 1: Early Holocene (~11,700–7800 cal BP)

Zone 1, including three subzones, named DAZ 1A to 1C, was characterised by a major group consisting of A. veraluciae and D. stelligera, alongside a minor group comprising P. brevistriata and Aulacoseira granulata var. angustissima (O.Müller) Simonsen (Table 1 & Figure 2). Especially, the variation patterns of A. veraluciae and D. stelligera were inverse to each other.

- DAZ 1A (~11,700–11,500 cal BP)

At the beginning of the Early Holocene, the inverse relationship of the two most dominant species started with the shares of A. veraluciae around 73–78% and D. stelligera ranging from 9% to 10%. Regarding the minor group, the median percentages of P. brevistriata and A. granulata var. angustissima varied around 7% and 4%, respectively.

- DAZ 1B (~11,500–9800 cal BP)

The relative abundance of A. veraluciae reduced to 35–64%, whereas D. stelligera increased to 21–35%. Minimal fluctuations were observed in quantifying counted valves for both P. brevistriata and A. granulata var. angustissima, as they consistently maintained median values exceeding 6% within the subzone.

- DAZ 1C (~9800–7800 cal BP)

DAZ 1C witnessed a substantial resurgence of A. veraluciae, with its abundance reaching 57–84%. This upward trend starkly contrasted with the significant decline of D. stelligera. The proportion of D. stelligera in DAZ 1C dropped below 10% and even fell below 1% at the end of this subzone. P. brevistriata only fluctuated between 3% and 15%, while A. granulata var. angustissima slightly decreased to less than 5%. Remarkably, the proportion of A. granulata var. granulata increasing from 23% to 32% at ~8000 cal BP coincided with mass declines of all other species.

Zone 2: Mid- to Late-Holocene (~7800–360 cal BP)

Four subzones in Zone 2, labelled as DAZ 2A to 2D, were divided based on inverse variations between a complete dominance of A. granulata var. granulata and a co-occurrence of P. brevistriata (Table 1 & Figure 2).

- DAZ 2A (~7800–5500 cal BP)

The early DAZ 2A marked a drop in A. veraluciae from 57% to below 2%. This species was overshadowed by the complete dominance of A. granulata var. granulata, which accounted for over 90% from the beginning of the subzone (~7700 cal BP). In addition, P. brevistriata valves were found with a small proportion of less than 2%, and D. stelligera was not recorded. A. granulata var. angustissima and other species within the genera Aulacoseira, Encyonema Kützing, Eunotia Ehrenberg, Gomphonema Ehrenberg, Navicula Bory, Nitzschia Hassall were occasionally observed below 1%.

- DAZ 2B (~5500–2600 cal BP)

In DAZ 2B, the proportions of A. granulata var. granulata slightly declined from 94–98% to 89–95%, whereas P. brevistriata increased from below 2% to 3–8%. The other facultative planktonic and benthic species were observed as co-occurrences with less than 1% for each, including Amphora copulata (Kützing) Schoeman & R.E.M.Archibald, Encyonema minuta Hilse, Fragilaria lapponica Grunow, and others identified within the genera Eunotia, Gomphonema, Navicula, Nitzschia.

- DAZ 2C (~2600–450 cal BP)

There was a slight increase in A. granulata var. granulata up to over 95% and a decline in P. brevistriata to lower than 2% in the DAZ 2C. This feature reveals an inverse variation of the two species compared to DAZ 2B.

- DAZ 2D (~450–360 cal BP)

The relationship between A. granulata var. granulata and P. brevistriata once exhibited a slight increase in P. brevistriata returning to a range of 3.75–5%, but A. granulata var. granulata still dominating (91–93%). The slightly proportional exchange of these species indicates a stable diatom community in Zone 2. On a remarkable note, the absence of D. stelligera in DAZ 2A continuously remained until the 1984 CE, when the first dam in the north Biển Hồ lake was constructed (Nguyễn-Văn et al., 2022).

Diatom valve concentration and ratio of planktonic versus facultative planktonic and benthic diatoms

The dynamic of the diatom assemblages, supported by the P/FB ratio index, elucidates variations in paleoenvironmental conditions, indicating whether they were favourable for either more planktonic or more benthic habitats. An increase or decrease in the P/FB ratio, respectively, shows a lower or higher diversity of benthic diatom species, which was constrained by the predominance in the quantity of three identified planktonic taxa in Biển Hồ lake. Additionally, the diatom valve concentration represents accumulated and preserved diatom valves within sediments. Therefore, the relationship between these diatom proxies and the sedimentation rate throughout the Holocene has been used to reflect the environmental conditions in each DAZ subzone (Figure 3).

Figure 3.

Fluctuations of the diatom valve concentration and P/FB ratio in Biển Hồ lake during the Holocene. Sedimentation rate was taken from Ojala et al. (2023).

The Early Holocene witnessed a higher average of the diatom valve concentration but a lower average of the P/FB ratio than the subsequent period. The count of diatom valves varied around 20 × 10⁶ valves.cm⁻³ occasionally reaching a large range of 30–35 × 10⁶ valves.cm⁻³ in Zone 1. However, a remarkable 50–80% decrease at the transition from Zone 1 to Zone 2 corresponded to counts below 10 × 10⁶ valves.cm⁻³ in DAZ 2A. In the early DAZ 2B, the number of counted valves strongly increased, peaking around 4800 cal BP. Thereafter, the concentration decreased slightly until the end of DAZ 2C, consistently fluctuating above 15 × 10⁶ valves.cm⁻³ (Figure 3).

In contrast, the P/FB ratio remained stable at a shallow level from DAZ 1A to 1C and then leapt since the end of the first zone, reaching the highest peak around 6200 cal BP (DAZ 2A). A higher abundance of benthic species in DAZ 2B accompanied a drop in the P/FB ratio, but it was still higher than in Zone 1. The proxy P/FB rose again in DAZ 2C, and its inverse relationship with the diatom valve concentration became unclear from the end of the subzone (Figure 3).

Morphological variability of A. granulata var. granulata

According to the high abundance and the morphological variability of A. granulata var. granulata in Biển Hồ lake during the Mid- to Late-Holocene (Zone 2), its valve dimensions mentioning valve diameter, mantle height, surface area and volume were measured. The valve dimensions generally decreased in the first half of Zone 2, from 7690 to 3800 cal BP. They recovered in the later part of DAZ 2B, followed by a slight decrease and relative stability in the early and mid DAZ 2C, respectively. However, from the late DAZ 2C, approximately 1000 cal BP, to DAZ 2D, the valve dimensions exhibited sudden fluctuations with large amplitudes with a peak around 800 cal BP and a trough around 500 cal BP approaching the lowest values as previously recorded at the middle of DAZ 2B, approximately 3800 cal BP. All four dimension parameters then went up in DAZ 2D. Meanwhile, the H/D and SA/V ratios had opposite trends with the valve dimensions during all corresponding time intervals.

The morphological variations of A. granulata var. granulata can be observed as alternating phases, corresponding yellow- and red-shaded intervals. Phases with higher values of the valve dimensions but lower values of the H/D and SA/V ratios are represented by red-shaded intervals, while contrasting phases are indicated by yellow-shaded intervals (Figure 4). Furthermore, the red-shaded intervals coincide with decreasing values of the diatom valve concentration. Conversely, the yellow-shaded intervals correspond to increasing values of the diatom valve concentration compared to the surrounding points.

Figure 4.

Fluctuations of A. granulata var. granulata morphological variables, the diatom valve concentration (abb. = Dia. con.), and the P/FB ratio during the Mid-to Late-Holocene period. Data were smoothed as red lines. Red-shaded intervals indicate phases with higher values of the valve dimensions but lower values of the H/D, SA/V ratios, and the diatom valve concentration, while yellow-shaded intervals represent inverse phases.

The valve dimensions of A. granulata var. granulata positively correlated with the P/FB ratio in the first two subzones of Zone 2. The species exhibited larger valves in DAZ 2A and smaller valves in DAZ 2B, corresponding to higher and lower values of the P/FB ratio, respectively. However, their relationship became ambiguous in DAZ 2C and DAZ 2D.

Principal component analysis

The first two principal components, PC1 and PC2, account for 56% and 35% of the total variance, respectively (Figure 5). The plot of PC1 versus PC2 reveals that all scores in Zone 1 and Zone 2 form two separated coherent clusters with a transition around 8050–7200 cal BP. This confirms that similar environmental conditions prevailed during the respective periods of Zones 1 and 2.

Figure 5.

Plot of Principal Component 1 (PC1) versus PC2 is based on the diatom species only. The ages (in cal BP) of some specific samples are shown as labels next to scores. The gradient-coloured bar is a legend for the ages of samples. Two clusters correspond to Zone 1 (Early Holocene) and Zone 2 (Mid- to Late-Holocene).

Pearson correlations

Relationships among the morphological variables of A. granulata var. granulata, the diatom valve concentration, and the P/FB ratio are reported using Pearson correlations (Table 2). The valve diameter shows strong positive correlations with the surface area (r = 0.98, p < 0.01) and the volume (r = 0.98, p < 0.01), but negative ones with both the H/D (r = −0.89, p < 0.01) and SA/V (r = −0.97, p < 0.01) ratios. Meanwhile, the mantle height exhibits relatively low to moderate correlations (r = −0.22; r = −0.57, p < 0.01; r = 0.56, p < 0.01; r = 0.64, p < 0.01; and r = 0.65, p < 0.01) with the other morphological parameters. It is obvious that the valve diameter of the taxon influences the surface area and volume more than the mantle height. A significantly positive correlation between the H/D and SA/V ratios (r = 0.86, p < 0.01) is also observed. The diatom valve concentration has moderate negative and positive correlations with the valve diameter (r = −0.61, p < 0.01) and the SA/V ratio (r = 0.62, p < 0.01), respectively, but has a relatively low relationship with the mantle height (r = −0.40, p < 0.05). Generally, the valve dimensions of A. granulata var. granulata exhibit an inverse connection with its related ratios and the diatom valve concentration, while they demonstrate a positive association with the P/FB ratio (Table 2), exhibiting concurrent fluctuations of these parameters, as shown in Figure 4. The analysis on this dataset indicates not only the correlations of the diatom morphological parameters but also the nutrient availability.

Table 2.

Correlation matrix of A. granulata var. granulata morphological variables, the diatom valve concentration, and the P/FB ratio are shown in coloured boxes in blue and red, referring to positive and negative relationships, respectively. Progressively darker boxes and bold values indicate strong correlations.

Correlation is significant at the 0.01 level (two-tailed).

Correlation is significant at the 0.05 level (two-tailed).

Note. Please refer to the online version of the article to view this figure in color.

Discussion

Early Holocene – limnology

The predominance of Aulacoseira spp. and P. brevistriata is primarily associated with the lake conditions determined by water-mixing, which is widely employed in paleolimnological reconstructions (Borges et al., 2008; Chen et al., 2013; Lindenschmidt and Chorus, 1998; Pedraza Garzon, 2021; Zalat and Vildary, 2007). Whereas the increase in D. stelligera is driven by extended thermal stratification or shallowing epilimnion, which prevents the water-mixing in lakes (Rühland et al., 2003; Wang et al., 2012; Williamson et al., 2010; Zou et al., 2018). The Biển Hồ environment during the Early Holocene (Zone 1) exhibited the prevalence of the heavily silicified planktonic A. veraluciae and the co-occurrences of the facultative planktonic P. brevistriata and the narrow cylindrical A. granulata var. angustissima suggesting intense water-mixing. Stronger mixing of the lake water often occurs within prolonged rainy seasons accompanied by decreasing air temperatures and intensified winter winds (Wang et al., 2012). In contrast, the relatively significant contribution of the small epilimnetic D. stelligera indicates thermal stratification promoted by rising temperatures and insolation within dry seasons (Wang et al., 2012).

A. veraluciae found in Biển Hồ lake in the Early Holocene is recognised by straight pervalvar rows of areolae, deep and thick ringleiste with three to four rimoportulae above, short and broadly spathulate linking spines with smooth edges, and one spine for every two interstriae, following description of Tremarin et al. (2014). With the H/D ratio of 0.35–2.01 (Tremarin et al., 2014), it can be clearly distinguished from A. granulata (with the H/D ratio of 0.8–5 (Spaulding et al., 2022)) by its relatively lower H/D ratio of the valves and more heavily silicified frustules as optically observed in the Biển Hồ lake samples (LM & SEM photos of four Aulacoseira species from Biển Hồ lake are provided as Supplemental Materials). In the case of Aulacoseira, variations tend to involve increased valve diameter rather than mantle height resulting in morphs associated with lower SA/V ratio (also similar measurement results in Biển Hồ A. granulata var. granulata, as shown in Table 2) and faster sinking velocities (O'Farrell et al., 2001; Wang et al., 2009). Consequently, it can be inferred that A. veraluciae has a typically smaller SA/V ratio, that is, the reduced surface area exposed to the surrounding environment and sinks more rapidly within the water column than A. granulata. Thus, A. veraluciae requires a more vigorous water circulation for its suspension. Moreover, this species has been found in a wide range of environments, from oligotrophic to eutrophic (Nardelli et al., 2021; Nogueira et al., 2006; Pagioro et al., 2005). We suppose that the observed high abundance of A. veraluciae in Biển Hồ lake during the Early Holocene was driven by strong water-mixing primarily occurring during winter seasons along with intense monsoonal winds and rainfalls, which contributed to the influx of silica-rich nutrients into the lake. Importantly, this study is the first report of the occurrence of A. veraluciae outside Brazil where the taxon is very common (Tremarin et al., 2014).

P. brevistriata and A. granulata var. angustissima, represented by small proportions in the lake sediment, also suggest enhanced water-mixing during this period. P. brevistriata (syn. = Fragilaria brevistriata Grunow) has been reported to thrive in cold waters (Mackay et al., 2003; Schmidt et al., 2004) and favour enhanced turbulence in lakes (Anderson, 2000; Zhang et al., 2016). The decline in P. brevistriata indicates increasing temperatures, rising water levels, and more acidic features (Chen et al., 2014; Van Dam et al., 1994). In the Biển Hồ sediment sequence, a decreasing population of P. brevistriata found around the Pleistocene-Holocene boundary, ~11,700 cal BP (Table 1), marks an environmental transition between two epochs. The observed var. angustissima, a morphologically narrower form of A. granulata, relies on water turbulence to remain within the euphotic zone due to its high specific gravity (Lund, 1954; Nakano et al., 1996; Petrova, 1986). This form exhibits a significantly higher SA/V ratio compared to the nominal variety granulata, which enhances its nutrient and CO₂ absorption efficiency and results in its slower sinking velocity (Gómez et al., 1995; Talling and Rzoska, 1967; Titman and Kilham, 1976). The occurrence of A. granulata var. angustissima during the Early Holocene provides additional evidence of water-mixing but in less intense phases and possibly reduced water temperatures (Wang et al., 2009, 2015).

On the other hand, the presence of D. stelligera in Zone 1 indicates thermal stratification, a contrasting mechanism to the water-mixing. Small-cell Discostella spp. are characterised by minimal silica and nutrient requirements for their growth, very low sinking velocities, and thriving in water column thermally stratified during summer seasons with high light, temperature regimes, and weak winds (Rühland et al., 2003; Wang et al., 2012; Williamson et al., 2010; Zou et al., 2018). Studies of living diatoms in freshwater reservoirs have revealed that D. stelligera prefers oligo- to mesotrophic environments (Gusev and Kulikovskiy, 2014; Moos et al., 2005; Tibby et al., 2012; Wang et al., 2008). A direct relationship between D. stelligera and nitrogen concentration has also been suggested by a positive response to additional nitrogen inputs into its living environment when phosphorus levels remain relatively limited (Rühland et al., 2015; Saros and Anderson, 2015). However, because the high diversity of the diatom community and the frequent occurrence of Aulacoseira taxa imply a high level of trophic state (Nardelli et al., 2021), the phosphorus levels in the Biển Hồ water were probably unlimited during this time. Hence, we suppose that during the Early Holocene, the lake experienced summer seasons with prolonged insolation and reduced rainfall, supplying less silica and nutrients into the lake and promoting thermal stratification.

The inverse correlation between A. veraluciae and D. stelligera reflects variations in water dynamics through Zone 1. The higher predominance of A. veraluciae in DAZ 1A (~11,700–11,500 cal BP) and 1C (~9800–7800 cal BP) suggests that the water-mixing was stronger promoted by intensified winter monsoon increasing winter rainfalls and reducing temperatures. The winter monsoon may extend into the spring season and is strong enough to prevent thermal stratification, thus, heavily silicified diatoms, such as Aulacoseira, cannot remain suspended (Wang et al., 2012). In contrast, the decrease in A. veraluciae by approximately 22% in DAZ 1B (~11,500–9800 cal BP), corresponding to the increase in D. stelligera, suggests the enhancement of the thermal stratification during this subzone due to extended dry summers accompanied by reduced rainfalls, less silica and nutrient inputs into the lake (Wang et al., 2012). The relative abundance of Aulacoseira spp. to D. stelligera can also be employed as an indicator of mixing depth, where the ratio decreases as D. stelligera becomes more dominant, indicating reduced water-mixing intensity (Fowler et al., 2022).

The alternations of water-mixing strength within the subzones of the Early Holocene are also evidenced by the sedimentation rate. In particular, the average value of the sedimentation rate in DAZ 1B was higher than in the other DAZs within Zone 1 (Figure 3) (Ojala et al., 2023). The sedimentation rate can be negatively influenced by water dynamic factors (e.g. turbidity, waves, currents, or other mechanical disturbances), potentially leading to the resuspension of particles back into the water column (Boyd and Tucker, 2012; Stow and Smillie, 2020). In contrast to the effects of water turbulence, thermal stratification results in the creation of distinct water layers with different temperatures, effectively preventing sediment resuspension and redeposition in lakes (Allaby, 2010; Apolinarska et al., 2020; Costa and de Morais, 2014; Park and Allaby, 2007). Therefore, during prolonged dry summer seasons in DAZ 1B (~11,500–9800 cal BP), the thermal stratification and lower water levels facilitated more efficient settling of suspended sediments, including diatom cells, and increasing the sedimentation rate in Biển Hồ lake. Conversely, intensified water-mixing activities decreased sedimentation during extended winter seasons with increased precipitation in DAZ 1A and 1C, corresponding to ~11,700–11,500 and ~9800–7800 cal BP, respectively.

Early Holocene – interaction of monsoon systems

Palaeoclimatic records across the broader monsoon region in Southeast Asia reveal two distinct weak phases of the summer monsoon in the Early Holocene (Kaboth-Bahr et al., 2021; Smittenberg et al., 2022). The first phase extended from 11,700 to 11,000 cal BP, corresponding from DAZ 1A to the beginning of DAZ 1B, while the second phase occurred at ~9000 cal BP, corresponding to DAZ 1C. During these phases, a reduction in temperature and precipitation was probably associated with the most substantial weakening of the Atlantic Meridional Overturning Circulation (AMOC) (Kaboth-Bahr et al., 2021; Smittenberg et al., 2022). However, in an interval of 11,000–9500 cal BP, corresponding from DAZ 1B to the early DAZ 1C, an increasing trend of temperature and humidity was related to the intensification of the ISM and EASM (Kaboth-Bahr et al., 2021; Smittenberg et al., 2022). Relatively dry climatic conditions with a gradual increase in humidity were observed in the Central Highlands of Vietnam across the Early Holocene (equivalent to Zone 1) based on biomarker records in a short sediment sequence from Ia M’He lake (Doiron, 2020). In Biển Hồ lake, the thermal stratification lasted longer during the summer seasons, primarily due to the reduced water-mixing, which was influenced by decreased annual rainfalls in DAZ 1B (~11,500–9800 cal BP), while in DAZ 1A and 1C (~11,700–11,500 cal BP and ~9800–7800 cal BP, respectively), we observed a shorter duration of the thermal stratification, as a result of the increased water-mixing. This phenomenon was probably related to only temperature variations corresponding to the cycles of the ISM and EASM. During winters, the NWM, closely associated with the EAWM, prevailed not only in the lake area but also in Central Vietnam and positively affected the annual precipitation (Buckley et al., 2014; Wolf et al., 2023). Evolution of the EAWM is described by a significant weakening phase from 11,500 to 9800 cal BP (corresponding to DAZ 1B), interspersed between two intensification phases from 11,700 to 11,500 cal BP and from 9800 to 8000 cal BP (corresponding to DAZ 1A and 1C, respectively) (Wang et al., 2012). This suggests that the EAWM had a significantly positive correlation with the local winter monsoon influencing the water-mixing intensity in Biển Hồ lake during the Early Holocene (Zone 1). It further explains the strong connection between the climate of the Central Highlands and the timing and amount of winter precipitation (Doiron, 2020).

The environmental regime shift (7800 cal BP)

At the transition between Zone 1 and Zone 2, there was a significant alteration in the major diatom assemblages with a dominance of A. granulata var. granulata replacing the previously prevalent species of A. veraluciae and D. stelligera (Table 1). This suggests a regime shift in the lake stratification and trophic state, specifically, the epilimnion, which plays an important role in the production of epilimnetic diatoms, including Discostella and Aulacoseira.

A. granulata is commonly used as an indicator species for planktonic habitats in turbid, riverine, and river-influenced environments found in both tropical and subtropical regions (Nguyen-Thi-Thuy et al., 2019; O'Farrell et al., 2001). It predominantly thrives under eutrophic conditions (Ehrlich, 1973; Kilham et al., 1986; Stoermer, 1974; Stoermer et al., 1981) and needs significant water-mixing for its living in the upper layer of lake water (Abdel Karim and Saeed, 1978; Hötzel and Croome, 1996). This alkaliphilous species is frequently observed in freshwaters characterised by high silica, phosphorus and temperature levels (Ehrlich, 1973; Kilham et al., 1986; Stoermer, 1974; Stoermer et al., 1981). Moreover, the growth rate of A. granulata is positively controlled by factors such as dissolved oxygen levels, lake depth, and chlorophyll-a (Mohanty et al., 2022). Since the end of Zone 1, ~7800 cal BP, the dominance of A. granulata var. granulata representing over 90% of the diatom community and the disappearance of D. stelligera indicate a regime shift in the lake structure and trophic state. They explain a transition from the seasonal alternation between the two mechanisms of water-mixing and thermal stratification in the meso-eutrophic conditions in Zone 1 to year-round continuous destratification and mixing of the water in a sustainable eutrophic environment in Zone 2. The term ‘destratification’ is used with meaning to emphasise the phenomenon of a water-mixing mechanism that reduces or eliminates separate layers in the lake (Park and Allaby, 2013). As discussed in the previous sections, the water-mixing mechanism was primarily supported by monsoon rainfalls, which inhibited thermal stratification and the shallowing of the epilimnion in the water column, thereby favouring the blooms of the turbulence-requiring planktonic A. granulata (Wang et al., 2012). We propose that a significant increase in summer rainfalls, besides remaining winter monsoon activities since the end of the Early Holocene (Zone 1), not only continuously promoted water turbulence but also delivered more nutrients into the lake, sustaining the eutrophic state. This hypothesis gains further support from the minor decrease in P. brevistriata, suggesting elevated water levels and temperatures in Zone 2, the Mid- to Late-Holocene (Chen et al., 2014; Van Dam et al., 1994). Additionally, the intense water circulation might lead to the resuspension of sediments, including diatoms, in the water column (Boyd and Tucker, 2012; Stow and Smillie, 2020), causing a remarkable decline in both the sedimentation rate (Ojala et al., 2023) and diatom valve concentration in DAZ 2A, ~7800–5500 cal BP (Figures 3 and 6).

Figure 6.

Temporal correlation between the Biển Hồ diatom data and regional palaeoclimatic events. [a] (Ojala et al., 2023), [b] (Wang et al., 2012), [c] (Moy et al., 2002); [1,2,3] (Dykoski et al., 2005; Marcott et al., 2013); [2,3,5] (Smittenberg et al., 2022); [3,4] (Kaboth-Bahr et al., 2021); [4,6] (Wolf, 2022); [6,9] (Griffiths et al., 2020); [6] (Kajita et al., 2018; Pausata et al., 2017; Wolf et al., 2023); [7] (Nguyễn-Đình et al., 2022); [8] (Buckley et al., 2010, 2014).

The P/FB ratio displayed a difference before and after the regime shift between Zone 1 and Zone 2. The P/FB ratio in Zone 1 was negatively influenced by the abundance of P. brevistriata and the relatively frequent, though not statistically significant, co-occurrences of benthic species within genera of Encyonema, Gomphonema, Navicula, and Nitzschia. These species, along with the major contribution of D. stelligera, indicated a calm water condition, with typical features of shallow-water phases, thermal stratification, and low nutrient availability favouring littoral and benthic habitats (Wolin and Jeffery, 2010). As a result, this environmental condition occurring during dry summer seasons in Zone 1 raised the diversity of the diatom community. However, the weaker stratification in the lake caused a change in diatom assemblages from small-cell cyclotelloid and elongate pennate species to small benthic fragilarioid and heavily-silicified tychoplanktonic taxa (Hofmann et al., 2020; Rühland et al., 2015). The significant increase in the P/FB ratio from the late Zone 1 (~8200 cal BP) to DAZ 2A (~7800–5500 cal BP) was associated with not only the decline of facultative planktonic and benthic species but also the replacement of D. stelligera by A. granulata var. granulata, indicate a notable rise in the lake water level, trophic state, frequency, and intensity of disturbance in the lake environment in summer seasons (Wolin and Jeffery, 2010). During winter seasons, A. granulata var. granulata also completely replaced A. veraluciae, which potentially requires stronger mixing for resuspension due to faster sinking velocities than A. granulata, as explained above. The mixing depth also probably decreased simultaneously with the occurrence of the regime shift that was influenced by the winter monsoon, sufficient to maintain A. granulata var. granulata in the euphotic zone (Lund, 1954; Nakano et al., 1996; Petrova, 1986) rather than A. veraluciae. Moreover, multiproxy hydroclimate records in Vietnam and Laos, which show synchronised enhanced summer and winter monsoon precipitation between 8000 and 6000 cal BP (Kaboth-Bahr et al., 2021; Wolf, 2022), potentially encouraged the summer destratification in Biển Hồ. Further, a relatively weak phase of EAWM in Southern China recorded near the end of the Early Holocene and during an interval of from 8000 to 7000 cal BP (Figure 6) (Wang et al., 2012), was possibly related to the limitation of the intensity of water-mixing in the euphotic zone in Biển Hồ lake during winter seasons, leading to the persistence of A. granulata var. granulata over A. veraluciae. Therefore, the year-round mixing mechanism reduced the diatom diversity with the absolute dominance of A. granulata var. granulata in Zone 2.

Mid- to Late-Holocene – drought events

The heavily-silicified diatoms, that is, A. granulata var. granulata, typically require sufficient silica and nutrient levels for their quantitative and dimensional development (Litchman et al., 2007; Nascimento et al., 2021; O'Farrell et al., 2001; Round et al., 1990). Their size and shape are susceptible to various lacustrine parameters such as water level, water-mixing, water transparency, silica concentration, nutrient content, and temperature (Davey, 1986; Genkal and Trifonova, 2020; Gómez et al., 1995; Mohanty et al., 2022; O'Farrell et al., 2001; Turkia and Lepistö, 1999). In Biển Hồ lake, an optimal environment related to the water-mixing and nutrient-rich conditions favoured the absolute prevalence of A. granulata var. granulata in Zone 2. Noticeable trends in morphological variations of this taxon correspond relatively well with the other diatom proxies and the sedimentation rate over time that reflect changes in nutrient availability and water levels of the lake (Figure 6).

Parameters of the valve dimensions of A. granulata var. granulata reached the highest average values in DAZ 2A, ~7800–6000 cal BP, while the H/D and SA/V ratios had their lowest values. In the lacustrine environment, the valve diameter and mantle height positively correlate with the dissolved inorganic nitrogen and the total dissolved reactive phosphorus, respectively (Gómez et al., 1995). Additionally, the mantle height has a significant positive relationship with concentrations of total nitrogen, total phosphate, and silicate (Mohanty et al., 2022). As discussed in the previous paragraph, DAZ 2A was marked by the dropped sedimentation rate (Ojala et al., 2023) and diatom valve concentration, and the dramatically increased P/FB ratio (Figures 3 and 6), then was interpreted with the synchronous activities of both the summer and winter monsoons activating the regime shift and contributing to the elevated nutrient content, high water levels and year-round deep water-mixing in Biển Hồ lake. Thus, such conditions in this subzone promoted the size development of A. granulata var. granulata, especially the valve diameter, but the reduction in their H/D and SA/V ratios (Gómez et al., 1995; O'Farrell et al., 2001; Wang et al., 2009).

Subsequently, the size and shape of A. granulata var. granulata varied significantly from the end of DAZ 2A (~7800–5500 cal BP) to DAZ 2B (~5500–2600 cal BP), with a drastic decline in the valve dimensions, consistent with a raise in the H/D and SA/V ratios. Hence, Biển Hồ lake in DAZ 2B probably experienced a simultaneous decrease in water levels and mixing due to reduced monsoon precipitation and wind intensity. This resulted in increased water transparency and decreased nutrient content. From 6000 to 4000 cal BP, a general downtrend of monsoon precipitation was recorded in the Asian and African regions represented by the lack of vegetation in Africa (Griffiths et al., 2020; Pausata et al., 2017) combined with decreasing summer insolation that led to an increase in atmospheric dust loading (Kröpelin et al., 2008; McGee and DeMenocal, 2017). The phenomena consequently resulted in reduced sea surface temperatures in the Indo-Pacific Warm Pool (Abram et al., 2009; Kuhnert et al., 2014) that was believed to be associated with an eastward movement in the Pacific Walker Circulation (Wolf et al., 2023). This movement is like the current El Niño, where the upwelling and uplift of air masses in the western Pacific Ocean are replaced by drier air moving downward, which resulted in reduced summer monsoon precipitation in Laos during this time interval (Griffiths et al., 2020). Moreover, sea surface temperatures in the East China Sea region declined to extremely low values during an interval of 5000–4000 cal BP (Kajita et al., 2018), contributing to the decreased NWM rainfalls that caused dry conditions in Central Vietnam during winter seasons (Wolf et al., 2023). However, warm and humid conditions temporarily occurred around 4500 cal BP, although the EASM was weakening (Smittenberg et al., 2022). This could potentially explain a slight increase in the water level of Biển Hồ lake, which was observed during an interval of approximately 4700–4200 cal BP in DAZ 2B.

In the middle of DAZ 2B, between 4000 and 3300 cal BP, the valve dimensions of A. granulata var. granulata varied to the smallest (Figure 4), explained by a severe deficiency of necessary nutrients for their size development. In addition, the proliferation of P. brevistriata along with other benthic taxa, as evidenced by the reduced P/FB ratio, and an enhancement of the sedimentation rate (Ojala et al., 2023) (Figure 6), suggested a limitation in the Biển Hồ water level and mixing. These characteristics point towards a potential dry condition. Significant weakening phases of the EASM and EAWM found around 4000 cal BP were associated with the 4.2 ka event and were believed to be linked to the pronounced decline in the AMOC (Lippold et al., 2019). The intensification of El Niño at the same time led to reduced local rainfalls in the South China Sea, as the Asian monsoon onset is typically delayed due to an equatorward contraction of the ITCZ (Figure 6) (Berry and Reeder, 2014; Griffiths et al., 2020). Furthermore, arid conditions and megadroughts were witnessed from 5000 to 3000 cal BP in certain regions of Africa and Asia (Griffiths et al., 2020; Kathayat et al., 2018) and particularly in Central Vietnam associated with the simultaneously weakened ISM and NWM (Wolf et al., 2023). Similar conditions at Biển Hồ lake, although with weaker signals, were also recorded in several intervals within DAZ 2C (from 2300 to 2200 cal BP; from 1200 to 1100 cal BP; and from 700 to 450 cal BP) (Figure 4). Conversely, during the time spans in DAZ 2B (from 4700 to 4200 cal BP, and from 3200 to 2700 cal BP), in DAZ 2C (from 900 to 750 cal BP), and in DAZ 2D (from 450 to 360 cal BP), Biển Hồ lake was characterised by raised water levels, alike to those observed in DAZ 2A which were promoted by enhanced monsoon precipitation.

After 3000 cal BP, the ISM weakened, leading to drier conditions, while the NWM intensified, resulting in Central Vietnam receiving an increased amount of winter precipitation (Wolf, 2022). A decrease in the valve dimensions of A. granulata var. granulata during the Late-Holocene indicates a weakening of the summer monsoon (Figure 6). Specifically, the lake water level declined between 700 and 400 cal BP (in DAZ 2C), coincided with severe drought events in mainland Southeast Asia, such as Angkor I & II Droughts (Buckley et al., 2010, 2014; Nguyễn-Đình et al., 2022).

Conclusion

The Holocene limnological shift in Biển Hồ maar lake in the Central Highlands of Vietnam was recorded from meso-eutrophic to eutrophic conditions via diatom analysis of the sediment sequence, especially with a remarkable transition in the diatom assemblages and diatom valve concentration at ~7800 cal BP.

During the Early Holocene (~11,700–7800 cal BP), with the alternating redistribution in the relative abundance of the heavily silicified A. veraluciae and the small-cell D. stelligera, the lake water exhibited switching between two prevailing mechanisms, including water-mixing and thermal stratification that established meso-eutrophic conditions.

During the Mid- to Late-Holocene (~7800–360 cal BP), the complete dominance of A. granulata var. granulata in the lake, replacing the previous dominant taxa including the var. angustissima and the two major species (A. veraluciae and D. stelligera), suggests eutrophication caused by year-round continuous destratification and intense mixing of the water. The variations of the valve dimensions of A. granulata var. granulata and its related ratios, including H/D and SA/V, possibly indicate fluctuations in the lake water level and nutrient concentration, and thus, mark the occurrences of drought intervals, from ~4000 to 3300 cal BP and from ~700 to 450 cal BP in the Central Highlands.

These findings further reveal changes in palaeoclimatic conditions in response to variability in large-scale monsoon systems, including changes in the intensity of the ISM, EASM, and EAWM throughout the epoch, which, in turn, directly correlated with the local summer and winter monsoons. The winter monsoon had a positive impact on extending the duration of water-mixing, while the summer monsoons, in conditions of increased temperatures, prolonged insolation, and reduced precipitation, facilitated thermal stratification remaining in the lake during the Early Holocene. Towards the end of this period, the synchronous activity of these monsoon subsystems, accompanied by significantly increased summer precipitation, triggered the regime shift in Biển Hồ lake around 7800 cal BP. This strengthening phase lasted until ~6000 cal BP when the EASM, ISM, and EAWM simultaneously weakened, resulting in a noticeable decrease in precipitation supply to the lake. The weakest phases of the monsoon subsystems and the driest conditions in the Central Highlands of Vietnam in the Mid- to Late-Holocene coincided with pronounced drought events across Africa and Asia continents.

Supplemental Material

sj-docx-1-hol-10.1177_09596836241236342 – Supplemental material for Diatom-based indications of an environmental regime shift and droughts associated with seasonal monsoons during the Holocene in Biển Hồ maar lake, the Central Highlands, Vietnam

Supplemental material, sj-docx-1-hol-10.1177_09596836241236342 for Diatom-based indications of an environmental regime shift and droughts associated with seasonal monsoons during the Holocene in Biển Hồ maar lake, the Central Highlands, Vietnam by Hoàn Đào-Trung, Yu Fukumoto, Dương Nguyễn-Thùy, Thành Đinh-Xuân, Thái Nguyễn-Đình, Ingmar Unkel and Hướng Nguyễn-Văn in The Holocene

Footnotes

Acknowledgements

We are indebted to VNU faculty and EOS’s international collaborators for practical support and assistance in the field and laboratory.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Hoàn Đào-Trung was funded by the Master, PhD Scholarship Programme of Vingroup Innovation Foundation (VINIF), code VINIF.2022.TS049.

ORCID iDs

Hoàn Đào-Trung

Thái Nguyễn-Đình

Ingmar Unkel

Hướng Nguyễn-Văn

Supplemental material

Supplemental material for this article is available online.

References

Abdel Karim

Saeed

(1978) Studies on the freshwater algae of the Sudan III, vertical distribution of Melosira granulata (Ehren.) Ralfs. in the White Nile, with reference to certain environmental variables. Hydrobiologia 57: 73–79.

Abram

McGregor

Gagan

, et al. (2009) Oscillations in the southern extent of the Indo-Pacific Warm Pool during the mid-Holocene. Quaternary Science Reviews 28(25-26): 2794–2803.

Allaby

(2010) A Dictionary of Ecology. Oxford: Oxford Quick Reference.

Anderson

(2000) Miniview: Diatoms, temperature and climatic change. European Journal of Phycology 35(4): 307–314.

Apolinarska

Pleskot

Pełechata

, et al. (2020) The recent deposition of laminated sediments in highly eutrophic Lake Kierskie, western Poland: 1 year pilot study of limnological monitoring and sediment traps. Journal of Paleolimnology 63(4): 283–304.

Asia-CRCiS (2016) The Drought Crisis in the Central Highlands of Vietnam. Gia Lai, Dak Lak: Kon Tum.

Baxter

(1995) Standardization and transformation in principal component analysis, with applications to archaeometry. Journal of the Royal Statistical Society. Series C, Applied Statistics 44(4): 513–527.

Berry

Reeder

(2014) Objective identification of the intertropical convergence zone: Climatology and trends from the ERA-Interim. Journal of Climate 27(5): 1894–1909.

Borges

PAF

Train

Rodrigues

(2008) Spatial and temporal variation of phytoplankton in two subtropical Brazilian reservoirs. Hydrobiologia 607: 63–74.

10.

Boyd

Tucker

(2012) Pond Aquaculture Water Quality Management. New York, NY: Springer Science & Business Media.

11.

Bradbury

Dieterich-Rurup

(1993) Holocene diatom paleolimnology of Elk Lake, Minnesota. In: Bradbury

Dean

(eds) Elk Lake, Minnesota: Evidence for Rapid Climate Change in the North-Central United States. Boulder, CO: Geological Society of America, Special paper 276, pp.215–238.

12.

Buckley

Anchukaitis

Penny

, et al. (2010) Climate as a contributing factor in the demise of Angkor, Cambodia. Proceedings of the National Academy of Sciences 107(15): 6748–6752.

13.

Buckley

Fletcher

Wang

S-YS

, et al. (2014) Monsoon extremes and society over the past millennium on mainland Southeast Asia. Quaternary Science Reviews 95: 1–19.

14.

Chang

C-P

M-M

Wang

(2011) The East Asian winter monsoon. In: Chang

Wang

Lau

NCG

(eds) The Global Monsoon System: Research and Forecast. Singapore: World Scientific, pp.99–109.

15.

Chan

JCL

(2004) The East Asian Winter Monsoon. In: Chang

(ed.) East Asian Monsoon. Singapore: World Scientific, pp.54–106.

16.

Chen

Metcalfe

, et al. (2014) Diatom response to Asian monsoon variability during the late glacial to Holocene in a small treeline lake, SW China. Holocene 24(10): 1369–1377.

17.

Chen

Yang

Dong

, et al. (2013) Environmental changes in Chaohu Lake (southeast, China) since the mid 20th century: The interactive impacts of nutrients, hydrology and climate. Limnologica 43(1): 10–17.

18.

Costa

JAV

de Morais

(2014) An open pond system for microalgal cultivation. In: Pandey

Lee

Soccol

(eds) Biofuels From Algae. Amsterdam: Elsevier, pp.1–22.

19.

Davey

(1986) The relationship between size, density and sinking velocity through the life cycle of Melosira granulata (Bacillariophyta). Diatom Research 1(1): 1–18.

20.

Doiron

(2020) Paleoclimatic and Paleoenvrionmental Changes Since the Last Glacial Maximum Recorded in Maar Lake Sediments From the Central Highlands of Vietnam. Long Beach, CA: California State University.

21.

Dykoski

Edwards

Cheng

, et al. (2005) A high-resolution, absolute-dated Holocene and deglacial Asian monsoon record from Dongge Cave, China. Earth and Planetary Science Letters 233(1-2): 71–86.

22.

Ehrlich

(1973) Quaternary Diatoms of the Hula Basin (Northern Israel). Geological Survey of Israel Bulletin 58: 1–39.

23.

Field

(2013) Discovering Statistics Using IBM SPSS Statistics. Thousand Oaks, CA: Sage.

24.

Fowler

Warner

Gawley

, et al. (2022) Paleolimnological comparison of algal changes in a clear-versus a brown-water lake over the last two centuries in the northeastern USA. Journal of Paleolimnology 67(3): 289–305.

25.

Genkal

Trifonova

(2020) Morphology and taxonomy of Aulacoseira muzzanensis (Bacillariophyta). Novosti sistematiki nizshikh rastenii 54: 355–369.

26.

Gomes

(2000) Phytoplankton composition, dominance and abundance as indicators of environmental compartmentalization in Jurumirim Reservoir (Paranapanema River), São Paulo, Brazil. Hydrobiologia 431(2-3): 115–128.

27.

Gómez

Riera

Sabater

(1995) Ecology and morphological variability of Aulacoseira granulata (Bacillariophyceae) in Spanish reservoirs. Journal of Plankton Research 17(1): 1–16.

28.

Griffiths

Johnson

Pausata

FSR

, et al. (2020) End of Green Sahara amplified mid- to late Holocene megadroughts in mainland Southeast Asia. Nature Communications 11(1): 4204.

29.

Guiry

(2023) AlgaeBase. Available at: https://www.algaebase.org (accessed 22 September 2023).

30.

Gusev

Kulikovskiy

(2014) Centric diatoms from Vietnam reservoirs with description of one new Urosolenia species. Nova Hedwigia. Beiheft 143: 111–126.

31.

Hall

RIS

John

(1999) Diatoms as indicators of lake eutrophication. In: Smol

(ed.) The Diatoms: Applications for the Environmental and Earth Sciences. Cambridge: Cambridge University Press, pp.128–168.

32.

Hofmann

Geist

Nowotny

, et al. (2020) Depth-distribution of lake benthic diatom assemblages in relation to light availability and substrate: Implications for paleolimnological studies. Journal of Paleolimnology 64: 315–334.

33.

Hötzel

Croome

(1996) Population dynamics of Aulacoseira granulata (EHR.) SIMONSON (Bacillariophyceae, Centrales), the dominant alga in the Murray River, Australia. Archiv fur Hydrobiologie 136: 191–215.

34.

Jardim Botânico do Rio de Janeiro (2023) Flora e Funga do Brasil. Available at: http://floradobrasil.jbrj.gov.br/.

35.

Juggins

(2007) C2: Software for Ecological and Palaeoecological Data Analysis and Visualisation (User Guide Version 1.5). Newcastle upon Tyne: Newcastle University 77: 680.

36.

Jüttner

Carter

Chudaev

, et al. (2023) Freshwater Diatom Flora of Britain and Ireland. Amgueddfa Cymru - National Museum Wales.

37.

Kaboth-Bahr

Bahr

Zeeden

, et al. (2021) A tale of shifting relations: East Asian summer and winter monsoon variability during the Holocene. Scientific Reports 11(1): 1–10.

38.

Kajita

Kawahata

Wang

, et al. (2018) Extraordinary cold episodes during the mid-Holocene in the Yangtze delta: Interruption of the earliest rice cultivating civilization. Quaternary Science Reviews 201: 418–428.

39.

Kamenir

Dubinsky

Zohary

(2004) Phytoplankton size structure stability in a meso-eutrophic subtropical lake. Hydrobiologia 520: 89–104.

40.

Kathayat

Cheng

Sinha

, et al. (2018) Evaluating the timing and structure of the 4.2 ka event in the Indian summer monsoon domain from an annually resolved speleothem record from Northeast India. Climate of the Past 14: 1869–1879.

41.

Kilham

Hecky

(1986) Hypothesized resource relationships among African planktonic diatoms. Limnology and Oceanography 31(6): 1169–1181.

42.

Kireta

(2018) Deciphering Climate-Driven Changes in Planktonic Diatom Communities in Lake Superior. Maine: The University of Maine.

43.

Kociolek

Blanco

Coste

, et al. (2023) DiatomBase. Available at: https://www.diatombase.org.

44.

Kröpelin

Verschuren

Lézine

A-M

, et al. (2008) Climate-driven ecosystem succession in the Sahara: The past 6,000 years. Science 320(5877): 765–768.

45.

Kuhnert

Kuhlmann

Mohtadi

, et al. (2014) Holocene tropical western Indian Ocean sea surface temperatures in covariation with climatic changes in the Indonesian region. Paleoceanography 29(5): 423–437.

46.

Lei

Wang

Qin

, et al. (2021) Diatom assemblage shift driven by nutrient dynamics in a large, subtropical reservoir in southern China. Journal of Cleaner Production 317: 1–13.

47.

Lepistö

Kauppila

Rapala

, et al. (2006) Estimation of reference conditions for phytoplankton in a naturally eutrophic shallow lake. Hydrobiologia 568: 55–66.

48.

Lindenschmidt

K-E

Chorus

(1998) The effect of water column mixing on phytoplankton succession, diversity and similarity. Journal of Plankton Research 20(10): 1927–1951.

49.

Lippold

Pöppelmeier

Süfke

, et al. (2019) Constraining the variability of the Atlantic meridional overturning circulation during the Holocene. Geophysical Research Letters 46(20): 11338–11346.

50.

Litchman

Klausmeier

Schofield

, et al. (2007) The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. Ecology Letters 10(12): 1170–1181.

51.

Liu

Chen

Liu

, et al. (2020) Changes in the ratio of benthic to planktonic diatoms to eutrophication status of Muskegon Lake through time: Implications for a valuable indicator on water quality. Ecological Indicators 114: 1–8.

52.

Wang

Zhou

, et al. (2014) Synchronous or asynchronous Holocene Indian and East Asian summer monsoon evolution: A synthesis on Holocene Asian summer monsoon simulations, records and modern monsoon indices. Global and Planetary Change 116: 30–40.

53.

Lund

JWG

(1954) The seasonal cycle of the plankton diatom, Melosira italica (Ehr.) Kutz. subsp. subarctica O. Mull. Journal of Ecology 42: 151–179.

54.

Mackay

Jones

Battarbee

(2003) Approaches to Holocene climate reconstruction using diatoms. In: Mackay AW, Battarbee R, Birks J and Oldfield F (eds) Global Change in the Holocene. London: A Hodder Arnold Publication, Chapter 20: 294–309.

55.

Marcott

Shakun

Clark

, et al. (2013) A reconstruction of regional and global temperature for the past 11,300 years. Science 339(6124): 1198–1201.

56.

McGee

DeMenocal

(2017) Climatic changes and cultural responses during the African humid period recorded in multi-proxy data. In: Storch HV (Ed) Oxford Research Encyclopedia of Climate Science. Oxford: Oxford University Press 2024, pp.1–47.

57.

Mohanty

Tiwari

Kumari

, et al. (2022) Variation of Aulacoseira granulata as an eco-pollution indicator in subtropical large river Ganga in India: A multivariate analytical approach. Environmental Science and Pollution Research 29(25): 37498–37512.

58.

Moos

Laird

Cumming

(2005) Diatom assemblages and water depth in Lake 239 (Experimental Lakes area, Ontario): Implications for paleoclimatic studies. Journal of Paleolimnology 34: 217–227.

59.

Moy

Seltzer

Rodbell

, et al. (2002) Variability of El Niño/Southern Oscillation activity at millennial timescales during the Holocene epoch. Nature 420(6912): 162–165.

60.

Nakano

S-I

Seike

Sekino

, et al. (1996) A rapid growth of Aulacoseira granulata (Bacillariophyceae) during the typhoon season in the south basin of Lake Biwa. Japanese Journal of Limnology 57(4-2): 493–500.

61.

Nardelli

Bicudo

Sampaio

, et al. (2021) Structure and species composition of diatom community during the wet season in three floodplain lakes of Brazilian Pantanal. PLoS One 16(5): 1–22.

62.

Nascimento

MDN

Bush

Bicudo

DDC

(2021) Water quality and spatial and seasonal dynamics in the largest water supply reservoir in Brazil and implications for diatom assemblages. Acta Limnologica Brasiliensia 33(7): 1–19.

63.

Nguyen-Thi-Thuy

Nguyen-Hai

Le-Thi-Phuong

, et al. (2019) Transitions in diatom assemblages and pigments through dry and wet season conditions in the Red River, Hanoi (Vietnam). Plant Ecology and Evolution 152(2): 163–177.

64.

Nguyễn-Văn

Schimmelmann

Nguyễn-Thùy

, et al. (2022) Environmental history recorded over the last 70 years in Biển Hồ maar sediment, central highlands of Vietnam. Quaternary International 621: 84–100.

65.

Nguyễn-Văn

Unkel

Nguyễn-Thùy

, et al. (2023) Paleoenvironmental potential of lacustrine sediments in the Central Highlands of Vietnam: A review on the state of research. Vietnam Journal of Earth Sciences 45(2): 164–182.

66.

Nguyễn-Đình

Nguyễn-Thùy

Nguyễn-Văn

, et al. (2022) A high-resolution, 1,250-year long drought record from ea Tyn Lake, Central Highlands of Việt Nam. Holocene 32(10): 1026–1040.

67.

Nogueira

Jorcin

Vianna

, et al. (2006) Reservatórios em cascata e os efeitos na limnologia e organização das comunidades bióticas (fitoplâncton, zooplâncton e zoobentos): um estudo de caso no rio Paranapanema (SP/PR). Ecologia de reservatórios: impactos potenciais, ações de manejo e sistemas em cascata 2: 435–459.

68.

O'Farrell

Tell

Podlejski

(2001) Morphological variability of Aulacoseira granulata (Ehr.) Simonsen (Bacillariophyceae) in the Lower Paraná River (Argentina). Limnology 2: 65–71.

69.

Ojala

AEK

Nguyễn-Văn

Unkel

, et al. (2023) High-resolution∼ ∼55 ka paleomagnetic record of Biển Hồ maar lake sediment from Vietnam in relation to detailed 14C and 137Cs geochronologies. Quaternary Geochronology 76: 1–15.

70.

Pagioro

Velho

Lansac-Tôha

, et al. (2005) Influência do grau de trofia sobre os padrões de abundância de bactérias e protozoários planctônicos em reservatórios do Estado do Paraná. In: Rodrigues L, Thomaz SM, Agostinho AA and Gomes LC (eds) Biocenose em Reservatórios: padrões espaciais e temporais. Sao Paulo: Rima Editora, pp.47–56.

71.

Park

Allaby

(2007) A Dictionary of Environment and Conservation. Agenda 21: 12. Oxford: Oxford University Press.

72.

Park

Allaby

(eds) (2013) A Dictionary of Environment and Conservation, 2nd edn. Oxford: Oxford University Press.

73.

Pausata

FSR

Zhang

Muschitiello

, et al. (2017) Greening of the Sahara suppressed ENSO activity during the mid-Holocene. Nature Communications 8(1): 1–12.

74.

Pedraza Garzon

(2021) Deciphering the Ecology of Aulacoseira Taxa in Alpine Lakes: Implications for Paleoclimate Reconstructions. Orono, ME: The University of Maine.

75.

Petrova

(1986) Seasonality of Melosira-plankton of the great northern lakes. Hydrobiologia 138: 65–73.

76.

Potapova

Veselá

Smith

, et al. (2023) Diatom New Taxon File at the Academy of Natural Sciences (DNTF-ANS). Available at: http://dh.ansp.org/dntf

77.

Poulickova

(2003) Morphological variability of natural populations of Aulacoseira granulata (EHR.) SIMONS (Bacillariophyceae). Czech Phycology, Olomouc 3: 125–140.

78.

Renberg

(1990) A procedure for preparing large sets of diatom slides from sediment cores. Journal of Paleolimnology 4: 87–90.

79.

Reynolds

Huszar

Kruk

, et al. (2002) Towards a functional classification of the freshwater phytoplankton. Journal of Plankton Research 24(5): 417–428.

80.

Round

Crawford

Mann

(1990) Diatoms: Biology and Morphology of the Genera. Cambridge: Cambridge University Press.

81.

Rühland

Priesnitz

Smol

(2003) Paleolimnological evidence from diatoms for recent environmental changes in 50 lakes across Canadian Arctic treeline. Arctic, Antarctic, and Alpine Research 35(1): 110–123.

82.

Rühland

Paterson

Smol

(2015) Lake diatom responses to warming: Reviewing the evidence. Journal of Paleolimnology 54: 1–35.

83.

Saros

Anderson

(2015) The ecology of the planktonic diatom Cyclotella and its implications for global environmental change studies. Biological Reviews 90(2): 522–541.

84.

Saros

Stone

Pederson

, et al. (2012) Climate-induced changes in lake ecosystem structure inferred from coupled neo- and paleoecological approaches. Ecology 93(10): 2155–2164.

85.

Schmidt

Kamenik

Lange-Bertalot

, et al. (2004) Fragilaria and Staurosira (Bacillariophyceae) from sediment surfaces of 40 lakes in the Austrian alps in relation to environmental variables, and their potential for palaeoclimatology. Journal of Limnology 63(2): 171–189.

86.

Simiyu

Kurmayer

(2022) Response of planktonic diatoms to eutrophication in Nyanza Gulf of Lake Victoria, Kenya. Limnologica 93: 1–12.

87.

Smittenberg

Yamoah

Chabangborn

, et al. (2022) A 18,000 yr record of tropical land temperature, convective activity and rainfall seasonality from the maritime continent. EarthArXiv. DOI: 10.31223/X52W4H. In review.

88.

Spaulding

Potapova

Bishop

, et al. (2022) Diatoms.org: Supporting taxonomists, connecting communities. Diatom Research 36(4): 291–304.

89.

Stevens

Buckley

Kim

, et al. (2018) Increased effective moisture in northern Vietnam during the Little Ice Age. Palaeogeography Palaeoclimatology Palaeoecology 511: 449–461.

90.

Stoermer

(1974) Phytoplankton Composition and Abundance in Lake Ontario During IFYGL. Ann Arbor, MI: Great Lakes Research Division, University of Michigan.

91.

Stoermer

Kreis

Sicko-Goad

(1981) A systematic, quantitative, and ecological comparison of Melosira islandica O. Müll. with M. granulata (Ehr.) Ralfs from the Laurentian Great Lakes. Journal of Great Lakes Research 7(4): 345–356.

92.

Stow

Smillie

(2020) Distinguishing between deep-water sediment facies: Turbidites, contourites and hemipelagites. Geosciences 10(2): 68.

93.

Ta-Hoa

Truong-Quang

Dang-Van

(2015) Some natural heritages of outstanding values for tourism development in Central Highland. Science of the Earth 37(2): 182–192.

94.

Talling

Rzoska

(1967) The development of plankton in relation to hydrological regime in the Blue Nile. Journal of Ecology 55: 637–662.

95.

Tibby

Penny

Leahy

, et al. (2012) Vegetation and water quality responses to Holocene climate variability in Lake Purrumbete, western Victoria. Peopled Landscapes: Archaeological biogeographic approaches to landscapes, Terra Australis 34: 359–374.

96.

Titman

Kilham

(1976) Sinking in freshwater phytoplankton: Some ecological implications of cell nutrient status and physical mixing processes1. Limnology and Oceanography 21(3): 409–417.

97.

Tremarin

Ludwig

Torgan

(2014) Aulacoseira veraluciae sp. Nov. (Coscinodiscophyceae, Aulacoseiraceae): A common freshwater diatom from Brazil. Phytotaxa 184(4): 208–222.

98.

Turkia

Lepistö

(1999) Size variations of planktonic Aulacoseira Thwaites (Diatomae) in water and in sediment from Finnish lakes of varying trophic state. Journal of Plankton Research 21(4): 757–770.

99.

Van Dam

Mertens

Sinkeldam

(1994) A coded checklist and ecological indicator values of freshwater diatoms from the Netherlands. Netherlands Journal of Aquatic Ecology 28: 117–133.

100.

Walker

MJC

Berkelhammer

Björck

, et al. (2012) Formal subdivision of the Holocene Series/Epoch: A discussion paper by a Working Group of INTIMATE (Integration of ice-core, marine and terrestrial records) and the Subcommission on Quaternary Stratigraphy (International Commission on Stratigraphy). Journal of Quaternary Science 27(7): 649–659.

101.

Wang

Lin

(2002) Rainy season of the Asian–Pacific Summer Monsoon. Journal of Climate 15(4): 386–398.

102.

Wang

Baehr

Lai

, et al. (2015) Exploring temporal trend of morphological variability of a dominant diatom in response to environmental factors in a large subtropical river. Ecological Informatics 29: 96–106.

103.

Wang

Lai

, et al. (2009) Seasonal variations of Aulacoseira granulata population abundance in the Pearl River Estuary. Estuarine Coastal and Shelf Science 85(4): 585–592.

104.

Wang

, et al. (2012) The East Asian winter monsoon over the last 15,000 years: Its links to high-latitudes and tropical climate systems and complex correlation to the summer monsoon. Quaternary Science Reviews 32: 131–142.

105.

Wang

Liu

, et al. (2008) Diatom-based inference of variations in the strength of Asian winter monsoon winds between 17,500 and 6000 calendar years BP. Journal of Geophysical Research Atmospheres 113(D21): 1–9.

106.

Weide

(2012) Freshwater diatoms as a proxy for Late-Holocene monsoon intensity in Lac Ba Bê in the Karst Region of Northern Viêt Nam. Long Beach, CA: California State University.

107.

Williamson

Salm

Cooke

, et al. (2010) How do UV radiation, temperature, and zooplankton influence the dynamics of alpine phytoplankton communities? Hydrobiologia 648: 73–81.

108.

Winsborough

(2016) Diatom Paleoenvironmental Analysis of Sediments From the Water Canyon Paleoindian Site (LA134764). Albuquerque: The University of New Mexico.

109.

Wolf

(2022) Hydroclimate variability in central Vietnam: past and present. PhD Thesis, University of Northumbria at Newcastle, UK.

110.

Wolf

Ersek

Braun

, et al. (2023) Deciphering local and regional hydroclimate resolves contradicting evidence on the Asian monsoon evolution. Nature Communications 14(1): 5697.

111.

Wolfe

(1997) On diatom concentrations in lake sediments: Results from an inter-laboratory comparison and other tests performed on a uniform sample. Journal of Paleolimnology 18(3): 261–268.

112.

Wolin

Jeffery

(2010) Diatoms as indicators of water-level change in freshwater lakes. In: Smol

(ed.) The Diatoms: Applications for the Environmental and Earth Sciences. Cambridge: Cambridge University Press, pp.174–185.

113.

Zalat

Vildary

(2007) Environmental change in Northern Egyptian delta lakes during the late Holocene, based on diatom analysis. Journal of Paleolimnology 37: 273–299.

114.

Zhang

Reed

Wagner

, et al. (2014) Lateglacial and Holocene climate and environmental change in the northeastern Mediterranean region: Diatom evidence from Lake Dojran (Republic of Macedonia/Greece). Quaternary Science Reviews 103: 51–66.

115.

Zhang

Reed

Lacey

, et al. (2016) Complexity of diatom response to lateglacial and Holocene climate and environmental change in ancient, deep and oligotrophic Lake Ohrid (Macedonia and Albania). Biogeosciences 13(4): 1351–1365.

116.

Zou

Wang

Zhang

, et al. (2018) Seasonal diatom variability of Yunlong Lake, southwest China – AA case study based on sediment trap records. Diatom Research 33(3): 381–396.

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

5.96 MB