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Example for gains and losses calculation This example shows the calculation of the gains and losses values for Sample A (site V32-8; 0.12 m depth). For the gains and losses calculation, all samples in a time series are always compared to the oldest sample in that time series (here Sample B; site V32-8; 0.88 m depth). Sample A contains 20 species with 4 (G. crassaformis, G. hirsuta, G. menardii and G. rubescens) not being present in Sample B, whereas Sample B (18 species) contains 2 species (N. pachyderma and T. quinqueloba) not present in sample A. Both samples share 16 species. Gains are calculated as the proportion of the number of species present in Sample A but not in Sample B relative to the total number of species in both samples pooled together (22 species: 16 shared plus 6 unique species) resulting in a gain value of 0.1818. Losses are calculated as the number of species not present in Sample A but present in Sample B relative to the total number of species in both samples resulting in a loss value of 0.0909. Sample A and B are also highlighted in Extended Data Fig. 4c.
Source publication
Biodiversity is expected to change in response to future global warming. However, it is difficult to predict how species will track the ongoing climate change. Here we use the fossil record of planktonic foraminifera to assess how biodiversity responded to climate change with a magnitude comparable to future anthropogenic warming. We compiled time...
Citations
... The group has an exceptional fossil record that stretches back to the Jurassic 7,8 . Because the species composition of planktonic foraminifera assemblages is sensitive to temperature 9,10 , fossil assemblages not only offer a chance to study ecosystem and biogeography changes [11][12][13][14] , but also provide a basis for quantitative reconstructions of seawater temperature by means of a range of (multivariate) approaches that relate species composition to seawater temperature 15,16 . In fact, one of the first global compilations of fossil planktonic foraminifera assemblages was conducted for this purpose 17 . ...
... That means that we use the same temporal definition of the LGM: 19,000-23,000 years BP 29 and follow their system of ranking of chronological confidence 30 . In practice, this means that samples with at least two calibrated 14 C dates within the LGM interval are assigned chronozone level 1. Chronozone level 2 indicates samples that are bracketed by at least two radiometric dates within the 12-30 ka BP interval, or have age control based on correlation to time series with level 1 age control using for instance benthic foraminifera oxygen isotope ratios. Level 3 is similar to the hypothesis-based age control as specified for level 2, but with correlations targets that themselves have chronozone level 2. Level 4 is used to indicate sites without chronozone assignment and does not indicate sites with low chronological confidence. ...
Species assemblage composition of marine microfossils offers the possibility to investigate ecological and climatological change on time scales inaccessible using conventional observations. Planktonic foraminifera - calcareous zooplankton - have an excellent fossil record and are used extensively in palaeoecology and palaeoceanography. During the Last Glacial Maximum (LGM; 19,000 – 23,000 years ago), the climate was in a radically different state. This period is therefore a key target to investigate climate and biodiversity under different conditions than today. Studying LGM climate and ecosystems indeed has a long history, yet the most recent global synthesis of planktonic foraminifera assemblage composition is now nearly two decades old. Here we present the ForCenS-LGM dataset with 2,365 species assemblage samples collected using standardised methods and with harmonised taxonomy. The data originate from marine sediments from 664 sites and present a more than 50% increase in coverage compared to previous work. The taxonomy is compatible with the most recent global core top dataset, enabling direct investigation of temporal changes in foraminifera biogeography and facilitating seawater temperature reconstructions.
... An emerging picture from paleobiology is that rapid climatic warming negatively affects biodiversity, especially in the tropics (4)(5)(6)(7)(8)(9). In today's ocean, biodiversity steadily rises from the poles to the tropics but exhibits a "dip" in species richness nearest the equator and at the highest temperatures (6,10). ...
... Recently, Strack et al. (2022) used the fossil record of planktonic foraminifera to study their relationship to climate change during the past 24 thousand years (kyr) on a basin-wide scale (North Atlantic Ocean). During this period, the world transitioned from the Last Glacial Maximum (LGM) to the current warm period (i.e. the Holocene). ...
... Planktonic foraminifera assemblages started to change with the onset of global warming, but their shift continued during the current warm period, when climate change was less pronounced (Strack et al., 2022). One explanation for this prolonged assemblage change into the established warm period is a shift in the drivers of species assembly from more abiotic causes during the last deglaciation (i.e. ...
... The analyses are based on a previous compilation of 25 planktonic foraminifera assemblage time series (Strack et al., 2022) that, after an exhaustive search, has been expanded with 6 organic-walled dinoflagellate cyst (dinocyst) and 6 coccolithophore assemblage time series to compare patterns across groups (see Supporting Information Table S1 for full list of time series). Throughout this study, the terms 'assemblage' and 'community' are used as defined by Fauth et al. (1996), where 'community' refers to all species that occur in the same place at the same time, and 'assemblage' refers to all taxa of phylogenetically related groups within a community. ...
Aim
We are using the fossil record of different marine plankton groups to determine how their biodiversity has changed during past climate warming comparable to projected future warming.
Location
North Atlantic Ocean and adjacent seas. Time series cover a latitudinal range from 75° N to 6° S.
Time period
Past 24,000 years, from the Last Glacial Maximum (LGM) to the current warm period covering the last deglaciation.
Major taxa studied
Planktonic foraminifera, dinoflagellates and coccolithophores.
Methods
We analyse time series of fossil plankton communities using principal component analysis and generalized additive models to estimate the overall trend of temporal compositional change in each plankton group and to identify periods of significant change. We further analyse local biodiversity change by analysing species richness, species gains and losses, and the effective number of species in each sample, and compare alpha diversity to the LGM mean.
Results
All plankton groups show remarkably similar trends in the rates and spatio‐temporal dynamics of local biodiversity change and a pronounced non‐linearity with climate change in the current warm period. Assemblages of planktonic foraminifera and dinoflagellates started to change significantly with the onset of global warming around 15,500 to 17,000 years ago and continued to change at the same rate during the current warm period until at least 5000 years ago, while coccolithophore assemblages changed at a constant rate throughout the past 24,000 years, seemingly irrespective of the prevailing temperature change.
Main conclusions
Climate change during the transition from the LGM to the current warm period led to a long‐lasting reshuffling of zoo‐ and phytoplankton assemblages, likely associated with the emergence of new ecological interactions and possibly a shift in the dominant drivers of plankton assemblage change from more abiotic‐dominated causes during the last deglaciation to more biotic‐dominated causes with the onset of the Holocene.
... The speed at which the biosphere will respond to global warming remains a major uncertainty (Beaugrand et al., 2009;Strack et al., 2022). Some studies have shown that the marine environment tends to respond more rapidly than terrestrial systems due to the short life-span of the phytoplanktonic base of the marine, pelagic food-web (e.g. ...
The North Sea region boasted one of the world’s most important fisheries for many centuries. Climate directly and indirectly influences the development and survival of many important pelagic fish in the North Sea ecosystem. One indirect influence is the food availability in the form of phyto- and zooplankton abundance, which is strongly controlled by environmental factors. One of these environmental factors is local sea surface temperatures. A negative correlation between zooplankton abundance and sea surface temperature is well established for the epeiric sea on the European continental shelf. Continuous temporal observations of North Sea zooplankton production only exist since 1958. Therefore we developed a Historical Plankton Index (HPI) from 800 CE onwards to extend our record of temperature-driven zooplankton abundance in the North Sea over a multi-centennial time scale. For this we used the North Atlantic temperature reconstructions and associations between zooplankton abundance and contemporary sea surface temperatures established applying a General Additive Modelling (GAM) approach. We then examined the association between the HPI and historical landings from the Dutch commercial herring fishery in the 17th century to test the utility of our HPI. We examine the potential influence of food availability (in terms of zooplankton abundance) on the fishery, the evolution of which is often only considered in terms of human influences such as conflict, fishing gear and demand for fish as a commodity. We find that under certain conditions the HPI can explain 20% of the variability in Dutch herring landings. This highlights the importance of developing long-term and large-scale indices of natural marine ecosystem dynamics to understand the historical fortunes of the commercial fishing industry. The results are directly relevant to the United Nations’ sustainable development goal 14 – life below water.
... However, the degree to which marine species keep pace with current rates of climate change via dispersal remains uncertain (García Molinos et al., 2016;Munday, Warner, Monro, Pandolfi, & Marshall, 2013). Although individual species of marine ectotherms are projected to closely track their thermal limits (Sunday, Bates, & Dulvy, 2012), assemblages are unlikely to respond cohesively to climate change (García Molinos et al., 2016;Graham et al., 1996;Walther et al., 2002), which can be attributed to the differential needs and tolerances of individual species across multiple abiotic parameters (Strack, Jonkers, C Rillo, Hillebrand, & Kucera, 2022). The individualistic responses of species to climate change may make certain regions or populations within assemblages more vulnerable to extirpation and global extinction (Reddin, Aberhan, Raja, & Kocsis, 2022;Stuart-Smith, Edgar, Barrett, Kininmonth, & Bates, 2015). ...
... Our findings suggest that assemblages of planktonic foraminifera track temperature changes, which is congruent with existing literature on marine microfossils on global (Strack et al., 2022;Yasuhara, Hunt, Dowsett, Robinson, & Stoll, 2012;Yasuhara, Tittensor, Hillebrand, & Worm, 2017) and local (Bond et al., 1997;Field, Baumgartner, Charles, Ferreira-Bartrina, & Ohman, 2006;Hüls & Zahn, 2000) spatial scales. However, assemblages tolerate modest temperature changes (< 0.3°C) with only little change in composition. ...
... /2024 responded to warming or cooling through substantial abundance changes within an assemblage. Novel plankton communities, such as those described since the last ice age (Strack et al., 2022), could therefore result from both habitat tracking and in situ abundance changes, and both mechanisms need to be incorporated when assessing the biotic response to temperature change. ...
Aim
To determine the degree to which assemblages of planktonic foraminifera track thermal conditions.
Location
The world’s oceans.
Time period
The last 700,000 years of glacial-interglacial cycles.
Major taxa studied
Planktonic foraminifera.
Methods
We investigate assemblage dynamics in planktonic foraminifera in response to temperature changes using a global dataset of Quaternary planktonic foraminifera, together with a coupled Atmosphere–Ocean General Circulation Model (AOGCM) at 8,000-year resolution. We use ‘thermal deviance’ to assess assemblage responses to climate change, defined as the difference between the temperature at a given location and the bio-indicated temperature (i.e., the abundance-weighted average of estimated temperature optima for the species present).
Results
Assemblages generally tracked annual mean temperature changes through compositional turnover, but large thermal deviances are evident under certain conditions. The coldest-adapted species persisted in polar regions during warming but were not joined by additional immigrants, resulting in decreased assemblage turnover with warming. The warmest-adapted species persisted in equatorial regions during cooling. Assemblages at mid latitudes closely tracked temperature cooling and showed a modest increase in thermal deviance with warming.
Main conclusions
Planktonic foraminiferal assemblages were generally able to track or endure temperature changes: as climate warmed or cooled, bio-indicated temperature also became warmer or cooler, although to a variable degree. At polar sites under warming and at equatorial sites under cooling, the change in temperature predicted from assemblage composition was less than, or even opposite to, expectations based on estimated environmental change. Nevertheless, all species survived the accumulation of thermal deviance—a result that highlights the resilience and inertia of planktonic foraminifera on an assemblage level to the last 700,000 years of climate change, which might be facilitated by broad thermal tolerances or depth shifts.
... The pattern has been studied intensively in planktonic foraminifera thanks to the global coverage of census counts in surface sediment data (Rillo, Woolley & Hillebrand, 2022). The study of the fossil record of planktonic foraminifera showed that this gradient started to emerge in the last 15 million years , and the tropical dip in diversity emerged during Planktonic foraminifera global diversity the transition from the last glacial maximum to the Holocene from 19 to 11.5 thousand years ago (Yasuhara et al., 2020;Strack et al., 2022). Our collection also reveals the latitudinal diversity gradient, with a broad maximum in diversity spanning from 45 S to 45 N latitude (Fig. 7A). ...
The nature and extent of diversity in the plankton has fascinated scientists for over a century. Initially, the discovery of many new species in the remarkably uniform and unstructured pelagic environment appeared to challenge the concept of ecological niches. Later, it became obvious that only a fraction of plankton diversity had been formally described, because plankton assemblages are dominated by understudied eukaryotic lineages with small size that lack clearly distin-guishable morphological features. The high diversity of the plankton has been confirmed by comprehensive metabarcod-ing surveys, but interpretation of the underlying molecular taxonomies is hindered by insufficient integration of genetic diversity with morphological taxonomy and ecological observations. Here we use planktonic foraminifera as a study model and reveal the full extent of their genetic diversity and investigate geographical and ecological patterns in their distribution. To this end, we assembled a global data set of 7600 ribosomal DNA sequences obtained from morphologically characterised individual foraminifera, established a robust molecular taxonomic framework for the observed diversity , and used it to query a global metabarcoding data set covering 1700 samples with 2.48 billion reads. This allowed us to extract and assign 1 million reads, enabling characterisation of the structure of the genetic diversity of the group across 1100 oceanic stations worldwide. Our sampling revealed the existence of, at most, 94 distinct molecular operational taxonomic units (MOTUs) at a level of divergence indicative of biological species. The genetic diversity only doubles the number of formally described species identified by morphological features. Furthermore, we observed that the allocation of genetic diversity to morphospecies is uneven. Only 16 morphospecies disguise evolutionarily significant genetic diversity, and the proportion of morphospecies that show genetic diversity increases poleward. Finally, we observe that MOTUs have a narrower geographic distribution than morphospecies and that in some cases the MOTUs belonging to the same morphospecies (cryptic species) have different environmental preferences. Overall, our analysis reveals that even in the light of global genetic sampling, planktonic foraminifera diversity is modest and finite. However, the extent and structure of the cryptic diversity reveals that genetic diversification is decoupled from morphological diversification, hinting at different mechanisms acting at different levels of divergence.
... In fact, lipidomics has already been shown to quantify the effects of herbicide exposure, as an experimental stressor, on microalgae [99] and lipid changes in heat-stressed mussels [100]. The lipidomics platform we have established provides the technology required to monitor copepod species-specific lipid adaptations to climate change as well as shifts in their food sources [101]. This is essential for the quantification of long-term multigenerational responses of this oceanic sentinel species to altering climate conditions. ...
... In fact, lipidomics has already been shown to quantify the effects of herbicide exposure, as an experimental stressor, on microalgae [99] and lipid changes in heatstressed mussels [100]. The lipidomics platform we have established provides the technology required to monitor copepod species-specific lipid adaptations to climate change as well as shifts in their food sources [101]. This is essential for the quantification of longterm multigenerational responses of this oceanic sentinel species to altering climate conditions. ...
Maintenance of the health of our oceans is critical for the survival of the oceanic food chain upon which humanity is dependent. Zooplanktonic copepods are among the most numerous multicellular organisms on earth. As the base of the primary consumer food web, they constitute a major biomass in oceans, being an important food source for fish and functioning in the carbon cycle. The potential impact of climate change on copepod populations is an area of intense study. Omics technologies offer the potential to detect early metabolic alterations induced by the stresses of climate change. One such omics approach is lipidomics, which can accurately quantify changes in lipid pools serving structural, signal transduction, and energy roles. We utilized high-resolution mass spectrometry (≤2 ppm mass error) to characterize the lipidome of three different species of copepods in an effort to identify lipid-based biomarkers of copepod health and viability which are more sensitive than observational tools. With the establishment of such a lipid database, we will have an analytical platform useful for prospectively monitoring the lipidome of copepods in a planned long-term five-year ecological study of climate change on this oceanic sentinel species. The copepods examined in this pilot study included a North Atlantic species (Calanus finmarchicus) and two species from the Gulf of Mexico, one a filter feeder (Acartia tonsa) and one a hunter (Labidocerca aestiva). Our findings clearly indicate that the lipidomes of copepod species can vary greatly, supporting the need to obtain a broad snapshot of each unique lipidome in a long-term multigeneration prospective study of climate change. This is critical, since there may well be species-specific responses to the stressors of climate change and co-stressors such as pollution. While lipid nomenclature and biochemistry are extremely complex, it is not essential for all readers interested in climate change to understand all of the various lipid classes presented in this study. The clear message from this research is that we can monitor key copepod lipid families with high accuracy, and therefore potentially monitor lipid families that respond to environmental perturbations evoked by climate change.
... This mirrors a decline in equatorial diversity in the pre-industrial era 23 , and diminished diversity in warmer low-latitude waters affecting PF distribution 24 . This shift is consistent with long-term changes in biological assemblages, as predicted by several modeling studies 18, 25,26 . ...
Anthropogenic activities, in particular rising CO 2 emissions, provoke ocean warming and acidification 1,2 , altering plankton habitats and threatening calcifying species 3,4 such as planktonic Foraminifera (PF). Whether they can cope with these unprecedented rates of environmental change, through lateral migrations and vertical displacements, is unresolved. Here we show, using over a century of data from the FORCIS ⁵ global census counts, that PF display evident poleward migratory behaviours, increasing their diversity at mid to high latitudes, and for some symbiont-barren species descending in the water column. Global PF abundance decreased by 24.24±0.11% over the last decades. Beyond lateral migrations ⁶ , our study uncovers intricate vertical migration patterns among PF species, presenting a nuanced understanding of their adaptive strategies. In projected temperature and carbonate saturation states for 2050 and 2100, low-latitude PF species will face physico-chemical environments that surpass their current tolerance. While these species might replace high-latitude ones through poleward shifts, this would radically alter low-latitude ecosystems. Our insights of PF adaptation during the Anthropocene reveals that 'migration is not enough', and has broader implications for the evolution of marine biodiversity under multiple stressors.
... This has been observed in the Arctic Ocean where subpolar/Atlantic species become increasingly more common in summer, a phenomenon referred to as Atlantification (e.g. Meilland et al., 2020;Ingvaldsen et al., 2021;Strack et al., 2022). If these species also have the ability to remain dormant in unfavourable conditions, this will allow them to populate the higher latitudes faster as the ocean warms (c.f., Ross and Hallock, 2016). ...
The planktic foraminifera Neogloboquadrina pachyderma is a calcifying marine protist and the dominant planktic foraminifera species in the polar oceans, making it a key species in marine polar ecosystems. The calcium carbonate shells of foraminifera are widely used in palaeoclimate studies because their chemical composition reflects the seawater conditions in which they grow. This species provides unique proxy data for past surface ocean hydrography, which can provide valuable insight to future climate scenarios. However, little is known about the response of N. pachyderma to variable and changing environmental conditions.
Here, we present observations from large-scale culturing experiments where temperature, salinity and carbonate chemistry were altered independently. We observed overall low mortality, calcification of new chambers and addition of secondary calcite crust in all our treatments. In-culture asexual reproduction events also allowed us to monitor the variable growth of N. pachyderma’s offspring. Several specimens had extended periods of dormancy or inactivity after which they recovered. These observations suggest that N. pachyderma can tolerate, adapt to and calcify within a wide range of environmental conditions. This has implications for the species-level response to ocean warming and acidification, for future studies aiming to culture N. pachyderma and use in palaeoenvironmental reconstruction.
... Our analyses of modern, ecological time series potentially even underestimate the extent of delay as can be derived from paleoecological responses to abiotic changes. Strack et al. (2022) analyzed how communities of pelagic Foraminifera responded to increasing temperature after the last glacial maximum using time series data across the North Atlantic. They find consistent gradual changes in composition (without any tipping behavior), which, importantly, continued for several thousands of years after the temperature had reached its pre-industrial equilibrium. ...
Thresholds and tipping points are frequently used concepts to address the risks of global change pressures and their mitigation. It is tempting to also consider them to understand biodiversity change and design measures to ensure biotic integrity. Here, we argue that thresholds and tipping points do not work well in the context of biodiversity change for conceptual, ethical, and empirical reasons. Defining a threshold for biodiversity change (a maximum tolerable degree of turnover or loss) neglects that ecosystem multifunctionality often relies on the complete entangled web of species interactions and invokes the ethical issue of declaring some biodiversity dispensable. Alternatively defining a threshold for pressures on biodiversity might seem more straightforward as it addresses the causes of biodiversity change. However, most biodiversity change appears to be gradual and accumulating over time rather than reflecting a disproportionate change when transgressing a pressure threshold. Moreover, biodiversity change is not in synchrony with environmental change, but massively delayed through inertia inflicted by population dynamics and demography. In consequence, formulating environmental management targets as preventing the transgression of thresholds is less useful in the context of biodiversity change, as such thresholds neither capture how biodiversity responds to anthropogenic pressures nor how it links to ecosystem functioning. Instead, addressing biodiversity change requires reflecting the spatiotemporal complexity of altered local community dynamics and temporal turnover in composition leading to shifts in distributional ranges and species interactions.
