Global change drives modern plankton communities away from the pre-industrial state

The ocean—the Earth’s largest ecosystem—is increasingly affected by anthropogenic climate change1,2. Large and globally consistent shifts have been detected in species phenology, range extension and community composition in marine ecosystems3,4,5. However, despite evidence for ongoing change, it remains unknown whether marine ecosystems have entered an Anthropocene6 state beyond the natural decadal to centennial variability. This is because most observational time series lack a long-term baseline, and the few time series that extend back into the pre-industrial era have limited spatial coverage7,8. Here we use the unique potential of the sedimentary record of planktonic foraminifera—ubiquitous marine zooplankton—to provide a global pre-industrial baseline for the composition of modern species communities. We use a global compilation of 3,774 seafloor-derived planktonic foraminifera communities of pre-industrial age9 and compare these with communities from sediment-trap time series that have sampled plankton flux since ad 1978 (33 sites, 87 observation years). We find that the Anthropocene assemblages differ from their pre-industrial counterparts in proportion to the historical change in temperature. We observe community changes towards warmer or cooler compositions that are consistent with historical changes in temperature in 85% of the cases. These observations not only confirm the existing evidence for changes in marine zooplankton communities in historical times, but also demonstrate that Anthropocene communities of a globally distributed zooplankton group systematically differ from their unperturbed pre-industrial state

Calcification depth of deep-dwelling planktonic foraminifera from the eastern North Atlantic constrained by stable oxygen isotope ratios of shells from stratified plankton tows

Stable oxygen isotopes (delta O-18) of planktonic foraminifera are one of the most used tools to reconstruct environmental conditions of the water column. Since different species live and calcify at different depths in the water column, the delta O-18 of sedimentary foraminifera reflects to a large degree the vertical habitat and interspecies delta O-18 differences and can thus potentially provide information on the vertical structure of the water column. However, to fully unlock the potential of foraminifera as recorders of past surface water properties, it is necessary to understand how and under what conditions the environmental signal is incorporated into the calcite shells of individual species. Deep-dwelling species play a particularly important role in this context since their calcification depth reaches below the surface mixed layer. Here we report delta O-18 measurements made on four deep-dwelling Globorotalia species collected with stratified plankton tows in the eastern North Atlantic. Size and crust effects on the delta O-18 signal were evaluated showing that a larger size increases the delta O-18 of G. inflata and G. hirsuta, and a crust effect is reflected in a higher delta O-18 signal in G. truncatulinoides. The great majority of the delta O-18 values can be explained without invoking disequilibrium calcification. When interpreted in this way the data imply depth-integrated calcification with progressive addition of calcite with depth to about 300m for G. inflata and to about 500m for G. hirsuta. In G. scitula, despite a strong subsurface maximum in abundance, the vertical delta O-18 profile is flat and appears dominated by a surface layer signal. In G. truncatulinoides, the delta O-18 profile follows equilibrium for each depth, implying a constant habitat during growth at each depth layer. The delta O-18 values are more consistent with the predictions of the Shackleton (1974) palaeotemperature equation, except in G. scitula which shows values more consistent with the Kim and O'Neil (1997) prediction. In all cases, we observe a difference between the level where most of the specimens were present and the depth where most of their shell appears to calcify.Agência financiadora Portuguese Foundation for Science and Technology (FCT): SFRH/BD/78016/2011; UID/Multi/04326/2019 European Union Seventh Framework Programme (FP7/2007-2013): 228344-EUROFLEETS German Research Foundation (DFG): WA2175/2-1; WA2175/4-1 German Climate Modelling consortium PalMod - German Federal Ministry of Education and Research (BMBF)info:eu-repo/semantics/publishedVersio

Quantifying the effect of seasonal and vertical habitat tracking on planktonic foraminifera proxies

The composition of planktonic foraminiferal (PF) calcite is routinely used to reconstruct climate variability. However, PF ecology leaves a large imprint on the proxy signal: seasonal and vertical habitats of PF species vary spatially, causing variable offsets from annual mean surface conditions recorded by sedimentary assemblages. PF seasonality changes with temperature in a way that minimises the environmental change that individual species experience and it is not unlikely that changes in depth habitat also result from such habitat tracking. While this behaviour could lead to an underestimation of spatial or temporal trends as well as of variability in proxy records, most palaeoceanographic studies are (implicitly) based on the assumption of a constant habitat. Up to now, the effect of habitat tracking on foraminifera proxy records has not yet been formally quantified on a global scale. Here we attempt to characterise this effect on the amplitude of environmental change recorded in sedimentary PF using core top δ18O data from six species. We find that the offset from mean annual near-surface δ18O values varies with temperature, with PF δ18O indicating warmer than mean conditions in colder waters (on average by −0.1 ‰ (equivalent to 0.4 °C) per °C), thus providing a first-order quantification of the degree of underestimation due to habitat tracking. We use an empirical model to estimate the contribution of seasonality to the observed difference between PF and annual mean δ18O and use the residual Δδ18O to assess trends in calcification depth. Our analysis indicates that given an observation-based model parametrisation calcification depth increases with temperature in all species and sensitivity analysis suggests that a temperature-related seasonal habitat adjustment is essential to explain the observed isotope signal. Habitat tracking can thus lead to a significant reduction in the amplitude of recorded environmental change. However, we show that this behaviour is predictable. This allows accounting for habitat tracking, enabling more meaningful reconstructions and improved data–model comparison

Global analysis of seasonality in the shell flux of extant planktonic foraminifera

Shell fluxes of planktonic Foraminifera species vary intra-annually in a pattern that appears to follow the seasonal cycle. However, the variation in the timing and prominence of seasonal flux maxima in space and among species remains poorly constrained. Thus, although changing seasonality may result in a flux-weighted temperature offset of more than 5° C within a species, this effect is often ignored in the interpretation of Foraminifera-based paleoceanographic records. To address this issue we present an analysis of the intra-annual pattern of shell flux variability in 37 globally distributed time series. The existence of a seasonal component in flux variability was objectively characterised using periodic regression. This analysis yielded estimates of the number, timing and prominence of seasonal flux maxima. Over 80% of the flux series across all species showed a statistically significant periodic component, indicating that a considerable part of the intra-annual flux variability is predictable. Temperature appears to be a powerful predictor of flux seasonality, but its effect differs among species. Three different modes of seasonality are distinguishable. Tropical and subtropical species (Globigerinoides ruber (white and pink varieties), Neogloboquadrina dutertrei, Globigerinoides sacculifer, Orbulina universa, Globigerinella siphonifera, Pulleniatina obliquiloculata, Globorotalia menardii, Globoturborotalita rubescens, Globoturborotalita tenella and Globigerinoides conglobatus) appear to have a less predictable flux pattern, with random peak timing in warm waters. In colder waters, seasonality is more prevalent: peak fluxes occur shortly after summer temperature maxima and peak prominence increases. This tendency is stronger in species with a narrower temperature range, implying that warm-adapted species find it increasingly difficult to reproduce outside their optimum temperature range and that, with decreasing mean temperature, their flux is progressively more focussed in the warm season. The second group includes the temperate to cold-water species Globigerina bulloides, Globigerinita glutinata, Turborotalita quinqueloba, Neogloboquadrina incompta, Neogloboquadrina pachyderma, Globorotalia scitula, Globigerinella calida, Globigerina falconensis, Globorotalia theyeri and Globigerinita uvula. These species show a highly predictable seasonal pattern, with one to two peaks a year, which occur earlier in warmer waters. Peak prominence in this group is independent of temperature. The earlier-when-warmer pattern in this group is related to the timing of productivity maxima. Finally, the deep-dwelling Globorotalia truncatulinoides and Globorotalia inflata show a regular and pronounced peak in winter and spring. The remarkably low flux outside the main pulse may indicate a long reproductive cycle of these species. Overall, our analysis indicates that the seasonality of planktonic Foraminifera shell flux is predictable and reveals the existence of distinct modes of phenology among species. We evaluate the effect of changing seasonality on paleoceanographic reconstructions and find that, irrespective of the seasonality mode, the actual magnitude of environmental change will be underestimated. The observed constraints on flux seasonality can serve as the basis for predictive modelling of flux pattern. As long as the diversity of species seasonality is accounted for in such models, the results can be used to improve reconstructions of the magnitude of environmental change in paleoceanographic records

Complex spatio-temporal structure of the Holocene Thermal Maximum

Inconsistencies between Holocene climate reconstructions and numerical model simulations question the robustness of climate models and proxy temperature records. Climate reconstructions suggest an early-middle Holocene Thermal Maximum (HTM) followed by gradual cooling, whereas climate models indicate continuous warming. This discrepancy either implies seasonal biases in proxy-based climate reconstructions, or that the climate model sensitivity to forcings and feedbacks needs to be reevaluated. Here, we analyze a global database of Holocene paleotemperature records to investigate the spatiotemporal structure of the HTM. Continental proxy records at mid and high latitudes of the Northern Hemisphere portray a “classic” HTM (8–4 ka). In contrast, marine proxy records from the same latitudes reveal an earlier HTM (11–7ka), while a clear temperature anomaly is missing in the tropics. The results indicate a heterogeneous response to climate forcing and highlight the lack of globally synchronous HTM

Scale dependence of temporal biodiversity change in modern and fossil marine plankton

Aim Biodiversity dynamics comprise evolutionary and ecological changes on multiple temporal scales from millions of years to decades, but they are often interpreted within a single time frame. Planktonic foraminifera communities offer a unique opportunity for analysing the dynamics of marine biodiversity over different temporal scales. Our study aims to provide a baseline for assessments of biodiversity patterns over multiple time-scales, which is urgently needed to interpret biodiversity responses to increasing anthropogenic pressure. Location Global (26 sites). Time period Five time-scales: multi-million-year (0-7 Myr), million-year (0-0.5 Myr), multi-millennial (0-15 thousand years), millennial (0-1,100 years) and decadal (0-32 years). Major taxa studied Planktonic foraminifera. Methods We analysed community composition of planktonic foraminifera at five time-scales, combining measures of standing diversity (richness and effective number of species, ENS) with measures of temporal community turnover (presence-absence-based, dominance-based). Observed biodiversity patterns were compared with the outcome of a neutral model to separate the effects of sampling resolution (the highest in the shortest time series) from biological responses. Results Richness and ENS decreased from multi-million-year to millennial time-scales, but higher standing diversity was observed on the decadal scale. As predicted by the neutral model, turnover in species identity and dominance was strongest at the multi-million-year time-scale and decreased towards the millennial scale. However, contrary to the model predictions, modern time series show rapid decadal variation in the dominance structure of foraminifera communities, which is of comparable magnitude as over much longer time periods. Community turnover was significantly correlated with global temperature change, but not on the shortest time-scale. Main conclusions Biodiversity patterns can be to some degree predicted from the scaling effects related to different durations of time series, but changes in the dominance structure observed over the last few decades reach higher magnitude, probably forced by anthropogenic effects, than those observed over much longer durations

Chamber formation leads to Mg/Ca banding in the planktonic foraminifer <i>Neogloboquadrina pachyderma</i>

Many species of planktonic foraminifera show distinct banding in the intratest distribution of Mg/Ca. This heterogeneity appears biologically controlled and thus poses a challenge to Mg/Ca paleothermometry. The cause of this banding and its relation with chamber formation are poorly constrained and most of what we know about intratest Mg/Ca variability stems from culture studies of tropical, symbiont-bearing foraminifera. Here we present data on the non-spinose, symbiont-barren Neogloboquadrina pachyderma from the subpolar North Atlantic where wintertime mixing removes vertical gradients in temperature and salinity. This allows investigation of biologically controlled Mg/Ca intratest variability under natural conditions. We find that intratest Mg/Ca varies between <0.1 and 7 mmol/mol, even in winter specimens. High Mg/Ca bands occur at the outer edge of the laminae, indicating reduced Mg removal at the end of chamber formation. Our data thus provide new constraints on the timing of the formation of such bands and indicate that their presence is intrinsic to the chamber formation process. Additionally, all specimens are covered with an outer crust consisting of large euhedral crystals. The composition of the crust is similar to the low Mg/Ca bands in the laminar calcite in winter and summer specimens, indicating a tight biological control on crust formation and composition. Nevertheless, despite high intratest variability, the median Mg/Ca of summertime tests is higher than that of wintertime tests. This provides support for Mg/Ca paleothermometry, but to improve the accuracy of paleotemperature estimates biological effects on Mg incorporation need to be better accounted fo