Asynchronous responses of aquatic ecosystems to hydroclimatic forcing on the Tibetan Plateau

Concentrations and sources of organic compounds

Mid- and long-chain n-alkanes

Throughout most sections, the biomarker composition of the Hala Hu record is dominated by long-chain n-alkanes (Fig. 2a). In most samples, concentrations were highest for nC₃₁ (ca 5–35 µg/g d.w.) and decreasing with chain-length (Supplementary Fig. S3–1). Generally, the concentrations were low in the glacial period, and increased between ca. 10 and 8 ka cal BP, while gradually decreasing after ca. 5 ka cal BP. These alkanes can be attributed to vascular higher plants from the lake catchment²⁷, which is characterized by alpine meadows. Mid-chain nC₂₃ and nC₂₅-alkanes are frequently attributed to aquatic macrophytes²⁸. However, n-alkane patterns of aquatic and terrestrial plants overlap. Moreover, we consider the contribution from macrophyte to the sedimentary n-alkane pool at the coring location to be minor, because of the specific n-alkane pattern of the samples, the overall low concentrations of mid-chain n-alkanes, and the deep water depth of the core site. An exception is a section in the core dated to ca. 15–14 ka cal BP, that has concentrations from ca. 20 up to 50 µg/g d.w. for individual mid-chain n-alkanes (Fig. 2a). This can be explained by enhanced contribution from submerged aquatic plants²⁹ when the lake level was much lower than present^9,23. Alternatively, a contribution from other mid-chain producers, such as Sphagnum species^30,31, is possible during phases of lake regression and the potential formation of peatlands around the lake shore.

Algal biomarkers

Aside from n-alkanes, a range of compounds of mostly aquatic origin can be identified in the aliphatic and ketone fraction of the sediment extracts. Unsaturated mid-chain alkenes nC_21:1, nC_23:1, nC_25:1, and nC_27:1 were abundant in traces in large parts of the core, but exhibit very high concentrations (>100 µg/g d.w.) in the glacial period in a single sample at 17.5 ka cal BP and between 15 and 14 ka cal BP. Relatively high concentrations up to 25 µg/d.w. were also observed in the mid-Holocene sequence from ca. 9 to 5 ka cal BP (Fig. 2b). The origin of those compounds is not fully resolved and so far n-alkenes have not been detected in samples from aquatic and terrestrial vascular plants on the TP. However, algae such as eustigmatophytes and chlorophytes have been suggested as possible precursors in the open freshwater Lake Lugu, southeastern TP³², and in Lake Challa, eastern Africa^33,34. Therefore, we consider phytoplankton as the most likely source of those compounds in Hala Hu.

It is notable that different n-alkene distribution patterns are visible throughout the core, with a predominance of nC_27:1 and nC_25:1 in the mid-Holocene section and nC_23:1 and nC_25:1 in other core sections (Supplementary Fig. S3–1). This indicates either different source organisms for at least nC_23:1 compared to nC_27:1 (supported by more depleted δD-values, see below and Supplementary Fig. S3–3) or a change towards the synthesis of longer chain-lengths by the same source organisms, triggered by changing environmental conditions.

The C₂₀-highly branched isoprenoid (HBI) compound is another observed phytoplankton biomarker, which is widely absent in the glacial sequences but shows traces throughout the Holocene with peak abundances (up to 30 µg/g d.w) in the mid-Holocene (8−5 ka cal BP; Fig. 2b). As often been found in cyanobacterial and algal mats (e.g.,^35,36,37), it has recently been assigned as a trophic indicator derived from diatoms in lake systems³⁸.

Other observed biomarkers of algal origin are alkenones, which are primarily produced by haptophytes, even though a variety of species are possible precursors^39,40 The summed concentrations of C₃₇-, C₃₈-, and C₃₉-compounds were low (<50 ng/g d.w.) in most samples from the glacial sections of the core, but increasing after ca. 12 ka cal BP and reaching peak abundances in the mid-Holocene (>300 ng/g d.w.; ca. 7.8–6.3 ka cal BP) (Fig. 2b). Here, the di- and tri-unsaturated homologues of all chain lengths appear to elute as peaks undisturbed by contamination, while the tetra-unsaturated alkenones show co-elution with a fatty acid ethyl ester (FAEE) at least for the C₃₇-compound.

Pentamethylicosane (PMI) is a compound that was detected in most samples in minor concentrations (<100 ng/g d.w.), but shows enhanced concentrations (>400 ng/g d.w.) during an episode in the glacial period (ca 16.6−14 ka cal BP) and during the late Holocene (4.5 ka cal BP to present). This compound has been assigned to microorganisms, i.e bacteria and archaea, often related to the methane cycle^41,42,43,44.

Fire markers

Another analyzed biomarker group, anhydrous sugars levoglucosan (L), galactosan (G), and mannosan (M) are generated by combustion and pyrolysis of cellulose and hemicellulose, thus, are often referenced as “pyromarkers” or “firemarkers”^45,46,47. They occur in low concentrations (<40 µg/g d.w.) during the early Holocene, but above average concentrations during the mid-Holocene (ca 8–5 ka cal BP), reaching peak values up to 170 µg/g d.w. The concentrations rapidly decrease and then gradually increase to intermediate abundances (ca 80 µg/g d.w.) during the late Holocene (Fig. 2c).

Slightly different trends and lower concentration values of M and G compared to L (Supplementary Fig. S3–1) can be attributed to their different thermal stabilities and consequently much easier degradations of M and G, which derive from hemicellulose^48,49. The mechanisms behind source to sink dynamics of pyromarkers are not fully understood yet but transport via both aerosols and fluvial organic matter seems important⁴⁷. For an in-depth interpretation of the pyromarker data, other related proxies such as polycyclic aromatic hydrocarbons (PAHs), black carbon, and pollen are required, together with the fire records from other surrounding lacustrine systems. Nevertheless, the rapid mid-Holocene increase of firemarker concentrations at Hala Hu is likely not only caused by the increase of supraregional wildfires triggered by high temperatures, but also due to enhanced fluvial influx to the lake due to strengthened glacial melt during this period.

Ecological inferences

The overall succession, i.e., appearances and disappearances of different biomarker groups indicate the expansion and regression of terrestrial vegetation and aquatic organisms throughout the studied 24 ka. The pronounced regime shifts within the lake ecosystem are remarkable, first during a ca. 1000 year episode in the glacial period (ca. 15−14 ka cal BP), which shows a strong expansion of aquatic organisms and eventually influence of Sphagnum species. Further succession of phytoplankton markers started with a first phase of alkenones, appearing from ca. 13–10 ka cal BP, with peak concentration at around 11 ka cal BP. The Holocene is characterized by variable concentrations of all aquatic biomarker groups, that show a clear maximum, starting right above a ca. 15 cm thick mass flow disturbance layer (ca. 8.4−8.0 ka cal BP; Fig. 2) and terminating at ca 5 ka cal BP. Synchronously, some biomarker groups show changes in relative abundances of single compounds (e.g., C_23:1 vs. C_27:1-alkenes, %C_37:4-alkenones and ΣC₃₇/ΣC₃₈ alkenones; Fig. 2b, Supplementary Fig. S3–1), which suggests shifts in communities of precursor organisms. These data give evidence of an ecological optimum between 8 and 5 ka cal BP. This episode was characterized by an overall higher and more diverse aquatic productivity compared to present-day condition, by the expansion of terrestrial vegetation, and by the increased influx of firemarkers.

Hydroclimatic trends throughout the past 24 ka

Catchment hydrology

As the source of terrestrial long-chain n-alkanes is limited to alpine grasses, their δD values represent mainly a growing season (i.e., summer) moisture signal. An influence of meltwater (snow, glaciers, and thawing permafrost) is debated as an additional water source, possibly incorporating a more negative isotope signal during leaf wax synthesis, especially at locations with a short growing season^21,50,51. The δD data since 24 ka cal BP demonstrate more negative values between ca 11 and 5 ka cal BP (minimum from ca. 9–7 ka cal BP) and further indicate a positive shift at around 11 ka cal BP. The latter is -within the margin of age-model uncertainties- probably associated with the Younger Dryas (YD).

In general, the data resembles the isotopic trends observed in other locations in the Asian monsoon realm and adjacent areas, derived from multiple archives and proxies such as speleothem δ¹⁸O and sedimentary leaf wax δD (Fig. 3). While age-model uncertainties often prevent the interpretation of short-term events and local effects and influence the amplitude of the recorded signal, the overall shift of δD values from high (Late Glacial) to low (Holocene) is observable in most sedimentary leaf wax records from the TP⁵², the Indian Monsoonal Realm/Bay of Bengal⁵³, and in Central Asia⁵⁰ (Fig. 3d, f). The available leaf wax δD records next to Hala Hu are from Lake Hurleg and Lake Qinghai, both less than 300 km south and southeast to Hala Hu, respectively (Fig. 1a). Lake Hurleg shows the most negative δD_nC31 values of the record between ca. 9 and 8 ka cal BP⁵⁴ (Fig. 3e). Data from Lake Qinghai show depletion of δD values of C₂₈-fatty acids earlier, i.e., already during the Late Glacial^55,56. Speleothem records show slight differences in detail, but in general reveal the most negative δ¹⁸O values at around 8 ka cal BP^57,58,59 (Fig. 3c, d).

The pattern with lower δD-values during the early and mid-Holocene has frequently been explained by intensified monsoon (e.g.,^55,60, and refs. in Fig. 3). While this is plausible, the extent to which enhanced precipitation amounts, temperature effects, or change of vapour sources contribute to local isotopic signals in sediments and speleothems is still under debate^20,58. Modern seasonal data from the Qilian Mountains suggest a pattern of temperature control and no amount effect on precipitation isotopes, i.e., relatively high modern isotopic values during the summer season⁶¹. On longer time-scales, expected temperature effects run opposite to the observed lower/higher δD values during the mid-Holocene/YD, respectively. An increase of precipitation amounts could possibly contribute to a more negative isotopic signal in summers. Indeed, the episode of most negative δD values corresponds to lake level highstands in more eastern locations, such as Lake Baijian⁶². More likely, we hypothesize that the isotope signal is driven by changes of vapour sources, induced by the movement and tilt of the jet-stream during the Holocene⁶³, or by coupling processes to upstream regions such as the tropical monsoon realms^58,64 In any case, shifts of the boundaries between monsoonal and westerly air masses are the most likely explanation for the observed trend of long-chain n-alkane δD-values in the Hala Hu sediments.

Lake isotope hydrology

To infer hydrological states of lakes, the hydrogen isotopic compositions of aquatic organisms have frequently been used. Biomarkers derived from aquatic macrophytes, such as nC₂₃, appear to be good recorders of lake water δD⁶⁵. However, in Hala Hu they were abundant only in low concentrations and therefore most likely mixed with terrestrial alkanes. Exceptional is the period ca. 15–14 ka cal BP. Here, the highly concentrated nC₂₃ exhibited highly variable δD values, averaging ca. 70‰ higher compared to the terrestrial compounds (Supplementary Fig. S3–3). This possibly indicates a mixed origin of compounds from macrophytes and Sphagnum sources, both of which have grown under uptake of lake and wetland water that has undergone evaporative D-enrichment. The drivers behind δD values of algal markers have been relatively well-investigated for alkenones but comparably little data exist for mid-chain n-alkenes and HBIs. A recent transect study has shown that C₂₀-HBIs potentially track lake water δD⁶⁶. Alkenones appear to record the δD values of the ambient water, but with strong potential effects of salinity and species associations^{67,68,69,70,71,72,73}.

In Hala Hu, δD values of all three analyzed biomarker groups (alkenones, alkenes, and HBIs) show tendencies towards higher values from the early to the mid and late Holocene, mostly reflecting the trend as derived from terrestrial compounds (Fig. 2b and Supplementary Fig. S3–3). Here, C₂₀-HBIs are slightly D-enriched compared to C₃₇-alkenones, and n-alkenes show further 50–60‰ higher values than those two compounds. The termination of the mid-Holocene is characterized by strong and opposing shifts in δD values of alkenones and n-alkenes. Given the succession of climatic, ecological, and hydrological changes, which include cooling and community shifts, these factors are plausible triggers for a ca. 40‰ positive shift in δD values of alkenones after 5 ka cal BP and the general trend towards higher δD values during the late Holocene (Fig. 2b; Supplementary Fig. S3–3). An opposite (i.e., negative) 60‰ shift in δD values of alkenes at ca. 6−5 ka cal BP (Fig. 2b) is more difficult to explain. Similar to alkenones, a change in community compositions of alkene producers can be a relevant factor, since this shift is mostly visible in nC_23:1 and nC_25:1, less in nC_27:1 (Supplementary Fig. S3–3), in agreement with varying nC_23:1 to nC_27:1 ratios (Supplementary Fig. S3–1). Considering the present day algal zone at 25–32 m depth²³, migration to different depths as a consequence of the hydrological changes and a related change of source water δD is another possible explanation.

In general, both the alkenone and n-alkene δD-data pinpoint to a range of ecological and hydrological changes around 6–5 ka cal BP. Further, the alkenones mirror the YD-isotopic signal at around 11 ka cal BP, as observed in the terrestrial long-chain n-alkanes (Fig. 2a). The results show the impact of climatic changes on lake ecology and hydrology during these episodes. They further highlight the potential of the applied proxy parameters to integrate and track aquatic community responses.

Alkenone indices

To elucidate the proxy potential of alkenones in the Hala Hu record, we computed multiple common ratios for comparison (Supplement S1–1). The temperature dependency of the degree of unsaturation of alkenones³⁹ have led to extensive calibration attempts in order to reconstruct water temperatures⁷⁴. While established in the marine realm, numerous indices and calibration-equations have been proposed for lacustrine systems in different regions⁷⁵ including China^{24,76,77,78,79,80,81,82,83,84}. All of these studies suggest that the influencing factors on alkenone biosynthesis are complex. Alongside temperature they include the effects of variable salinities and other water chemistry-related parameters, changes in the seasonality of biosynthesis, community shifts and phylogeny of alkenone producers, and their potential relocation and depth migration within lakes.

For this study, we calculated the classic U^k and U^k´ indices for either C₃₇– or C₃₈-compounds^85,86, hybrid indices based on both the C₃₇ and C₃₈-group^80,87, as well as the percentages of C₃₇– and C₃₈– compounds and the ratio ΣC₃₇/ΣC₃₈ (plotted for comparison in Supplementary Fig. S3–2).

The data show comparable trends of all indices which exclude the tetra unsaturated C_37:4 alkenone, i.e., U^k′₃₇; U^k₃₈, U^k′₃₈, and U^k′₃₇₃₈ (Supplementary Fig. S3–2). The different behaviour of C_37:4 has been observed previously and was explained by complex influences of salinity and species contribution^67,79,88. Notable in the Hala Hu record is a negative correlation between %C_37:4 and concentrations of terrestrial n-alkanes during the Holocene (Fig. 2a and Supplementary Fig. S3–2), which suggests that control mechanisms on C_37:4 abundances other than temperature are likely. Finally, the calculated C_37:4 concentrations may be biased by partial co-elution of this compound with FAEE. For this reason, we focus on the indices which exclude C_37:4 and therefore chose the integrative hybrid index U^k′₃₇₃₈⁸⁷ (Fig. 2b) for further data interpretation.

In general, U^k′₃₇₃₈ shows relatively low values during the glacial period and the YD, indicating low temperatures. Increasing U^k′₃₇₃₈ values between ca. 11 and 9 ka cal BP could then be related to warming conditions at the Late Glacial—early Holocene transition.

A reversal to lower values from ca. 9 to 5 ka cal BP would then indicate cooler water temperatures at the location of alkenone synthesis. Those could be explained by glacial freshwater pulses and related cooling of the lake water above the thermocline, as a mid-Holocene lake transgression was inferred from biological and sedimentary proxies²³. However, most algae within the modern lake are found far below the thermocline, where water temperatures are relatively stable, diminishing the potential influence of water temperature on alkenone parameters.

The integrated results from aquatic biomarkers illustrate the profound effects of rising lake levels and related change in lake water chemistry on phytoplankton communities during the mid-Holocene. It is therefore likely that shifts in alkenone producers rather than temperature changes are the primary cause of the lower U^k′₃₇₃₈ values between 9 and 5 ka cal BP.

Hydroclimatic inferences

δD values of long-chain n-alkanes reflect regional isotope hydrology and hence are considered as a proxy for shifts within the atmospheric circulation system. We, therefore, interpret the most negative δD values of the records, from ca. 9 to 7 ka cal BP, to be associated with changes in moisture source, synchronous with an intensified ASM over Asia. It needs to be highlighted that this inference is independent from the exact origin of vapour transported to the study area during ASM, which possibly includes westerly moisture sources and local convection²⁰. Further, the actual increase of precipitation and/or effective moisture in the Hala Hu catchment during this episode were most likely minor.

A YD signal is observable in both terrestrial and aquatic δD values (Fig. 2), indicating an impact of this event on both the catchment and lake hydrology in the Hala Hu region. While an early Holocene warming is probably recorded by the U^k′₃₇₃₈, there is evidence of strong effects of community shifts during the mid-Holocene (8−ca. 5 ka cal BP). The termination of the mid-Holocene is characterized by multiple hydrological and ecological changes, visible in decreasing aquatic and terrestrial biomarker concentrations and shifts in δD values of aquatic compounds.

Ecological responses to hydroclimatic forcing

The current trophic status of Hala Hu has not been determined by water chemical parameters, but the extensive oxygen supersaturated algal zone above an oxygen zone support mesotrophic conditions. These conditions are reflected by low to average concentrations of phytoplankton biomarkers from the late Holocene to the present (Fig. 2b).

In principle, lakes often achieve alternate steady states, that are ecosystem states where either macrophyte or phytoplankton dominates⁸⁹. This concept was initially proposed for shallow lakes but has been shown to be applicable also for some deeper lakes, in which especially submerged macrophytes have a stabilizing function on ecosystem composition^90,91. Many lakes on the TP are saline, oligotrophic, and relatively shallow¹². Due to high insolation and clear water, strong submerged macrophyte growth, often down to significant depths, is very common in Tibetan lakes²⁹.

To interpret past changes of these conditions from organic geochemical proxy data, transporting mechanisms of biomarkers need to be considered. For example, a survey of surface sediments in Lake Donggi Cona has shown that submerged macrophytes mainly influence the near shore zones, and samples from deeper parts of the lake receive low concentrations of aquatic mid-chain n-alkanes⁹². At present, aquatic macrophytes occur at least in the near-shore zones at Hala Hu²³. The very low concentrations of macrophyte markers (nC₂₃ and nC₂₅) can be explained by the absence of submerged higher plants at the coring location since the early Holocene, but do not allow conclusions about potential abundances at more shallow water depths.

Very different conditions occurred in the glacial period, when a peak of nC₂₃ provides evidence for macrophyte expansion during a phase of much lower lake level than present. An increased influence of wetlands and supply of nC₂₃ derived from Sphagnum sp. is likely and could explain enhanced concentrations of PMI derived from methanogens. Before 15 ka cal BP glaciers extended into the lake, evidenced by the moraine deposits found in the lower part of a core which was obtained near the northwestern shore of Hala Hu²². Sr and S contents were high during this period, salinity was likely greater, which is in line with the appearance of the first alkenone producers²³ (Fig. 2b, d). After 15 ka cal BP other phytoplankton- (n-alkenes), macrophyte- (alkanes), and microbial markers (PMI) increased synchronously. These data point towards a slightly enhanced nutrient supply and a change in lake water chemistry that is supported by the increased elemental values (Fig. 2d). This first short-term expansion phase of both macrophytes and phytoplankton was associated with a temperature increase at 15 ka cal BP, and likely accompanied by receding glaciers, enhanced freshwater influx, and more favourable conditions for growth in general. This episode is synchronous to Northern Hemispheric warming (Bølling interstadial)⁹³, but a definite correlation with this event needs to be considered with care, due to age-model uncertainties.

While the exact progression of glacier retreat at surrounding mountains after the ca. 50 m rise of the lake level between ca 12 and 10 ka cal BP remains unknown, multi-proxy data indicate water level fluctuations with episodes of higher lake levels than present during the mid-Holocene from ca. 8 to 6 ka cal BP^9,23. The combined effects of changes in water chemistry due to glacial meltwater, and higher temperatures probably shifted the lake ecosystem to a more phytoplankton-dominated state. A fertilization effect from either glacial meltwater and/or aerosols is possible and supported by the high firemarker concentrations during the mid-Holocene^47,94. Suspended sediments transported by glacial meltwater is an important influencing factor in high-altitude lake ecosystems, with effects on both light penetration and nutrient supply, in combination often limiting macrophyte growth^94,95,96. Terrestrial biomarkers reached their highest concentrations between ca. 8 and 5 ka cal BP, however their increase and decrease before and after this ecological optimum is more gradual than that of aquatic compounds. We interpret this variability as the result of expansion and regression of grasses in the catchment, driven by the effects of higher temperatures and increase of effective moisture⁹⁷ (Fig. 2). Additionally, increased surface runoff derived from melting glaciers could have contributed to the higher influx from terrestrial leaf waxes to the sediments during the mid-Holocene.

There is a considerable lag in the Hala Hu record between the mid-Holocene ecological optimum (characterized by the maximum expansion of alpine grasses and the highest phytoplankton productivity in the lake), and the initial atmospheric forcing (i.e., change of vapour source synchronous to monsoonal intensification). The controlling mechanisms on Holocene vegetation expansion have been debated recently, though there are hints that temperature and temperature-controlled feedback mechanisms are the dominant force on terrestrial ecosystems on the eastern TP^16,18,97. The Hala Hu data likewise point towards air temperature and the subsequent discharge of glacial meltwater as driving factors of massive ecosystem response in the lake and its catchment.

The termination of a mid-Holocene optimum has been observed in numerous lake sediment, speleothem, and ice core records^{6,9,11,13,20,59,97} (Fig. 3). It has been hypothesized that a cooling episode 5–3 ka cal BP, inferred from an Lake Qinghai alkenone record, delayed the population of the northeastern TP in the late Holocene⁷⁸. We do not see a similar trend in the alkenone indices at Hala Hu, however, we observe regression of grasses, a sharp decrease of aquatic biomarkers concentrations, and shifts in aquatic δD values, all illustrating rapid ecosystem responses to cooler conditions after ca. 5 ka cal BP.

Source: Ecology - nature.com