Ocean climate and hydrodynamics drive decadal shifts in Northeast Atlantic dinoflagellates.

The abundance of large marine dinoflagellates has declined in the North Sea since 1958. Although hypotheses have been proposed to explain this diminution (increasing temperature and wind), the mechanisms behind this pattern have thus far remained elusive. In this article, we study the long-term changes in dinoflagellate biomass and biodiversity in relation to hydro-climatic conditions and circulation within the North Atlantic. Our results show that the decline in biomass has paralleled an increase in biodiversity caused by a temperature-induced northward movement of subtropical taxa along the European shelf-edge, and facilitated by changes in oceanic circulation (subpolar gyre contraction). However, major changes in North Atlantic hydrodynamics in the 2010s (subpolar gyre expansion and low-salinity anomaly) stopped this movement, which triggered a biodiversity collapse in the North Sea. Further, North Sea dinoflagellate biomass remained low because of warming. Our results, therefore, reveal that regional climate warming and changes in oceanic circulation strongly influenced shifts in dinoflagellate biomass and biodiversity.

Phytoplankton life strategies, phenological shifts and climate change in the North Atlantic Ocean from 1850 to 2100.

Significant phenological shifts induced by climate change are projected within the phytoplankton community. However, projections from current Earth System Models (ESMs) understandably rely on simplified community responses that do not consider evolutionary strategies manifested as various phenotypes and trait groups. Here, we use a species-based modelling approach, combined with large-scale plankton observations, to investigate past, contemporary and future phenological shifts in diatoms (grouped by their morphological traits) and dinoflagellates in three key areas of the North Atlantic Ocean (North Sea, North-East Atlantic and Labrador Sea) from 1850 to 2100. Our study reveals that the three phytoplanktonic groups exhibit coherent and different shifts in phenology and abundance throughout the North Atlantic Ocean. The seasonal duration of large flattened (i.e. oblate) diatoms is predicted to shrink and their abundance to decline, whereas the phenology of slow-sinking elongated (i.e. prolate) diatoms and of dinoflagellates is expected to expand and their abundance to rise, which may alter carbon export in this important sink region. The increase in prolates and dinoflagellates, two groups currently not considered in ESMs, may alleviate the negative influence of global climate change on oblates, which are responsible of massive peaks of biomass and carbon export in spring. We suggest that including prolates and dinoflagellates in models may improve our understanding of the influence of global climate change on the biological carbon cycle in the oceans.

Stepping stones towards Antarctica: Switch to southern spawning grounds explains an abrupt range shift in krill.

Poleward range shifts are a global-scale response to warming, but these vary greatly among taxa and are hard to predict for individual species, localized regions or over shorter (years to decadal) timescales. Moving poleward might be easier in the Arctic than in the Southern Ocean, where evidence for range shifts is sparse and contradictory. Here, we compiled a database of larval Antarctic krill, Euphausia superba and, together with an adult database, it showed how their range shift is out of step with the pace of warming. During a 70-year period of rapid warming (1920s-1990s), distribution centres of both larvae and adults in the SW Atlantic sector remained fixed, despite warming by 0.5-1.0°C and losing sea ice. This was followed by a hiatus in surface warming and ice loss, yet during this period the distributions of krill life stages shifted greatly, by ~1000 km, to the south-west. Understanding the mechanism of such step changes is essential, since they herald system reorganizations that are hard to predict with current modelling approaches. We propose that the abrupt shift was driven by climatic controls acting on localized recruitment hotspots, superimposed on thermal niche conservatism. During the warming hiatus, the Southern Annular Mode index continued to become increasingly positive and, likely through reduced feeding success for larvae, this led to a precipitous decline in recruitment from the main reproduction hotspot along the southern Scotia Arc. This cut replenishment to the northern portion of the krill stock, as evidenced by declining density and swarm frequency. Concomitantly, a new, southern reproduction area developed after the 1990s, reinforcing the range shift despite the lack of surface warming. New spawning hotspots may provide the stepping stones needed for range shifts into polar regions, so planning of climate-ready marine protected areas should include these key areas of future habitat.

How do plankton species coexist in an apparently unstructured environment?

In a paper entitled The paradox of the plankton, Hutchinson asked 'how it is possible for a number of species to coexist in a relatively isotropic or unstructured environment all competing for the same sorts of materials' (Hutchinson 1961 Am. Nat. 95, 137-145 (doi:10.1086/282171)). Particularly relevant for phytoplankton, this paradox was based on two implicit, and perhaps naive, postulates, i.e. (i) that all plankton species have similar requirements and (ii) that the marine environment is relatively homogeneous in space and time. A number of hypotheses, based on purely theoretical or experimental studies, have been proposed to solve this conundrum, ranging from spatio-temporal environmental heterogeneity to biotic chaotic variability. Here, we characterize the ecological niche of 117 plankton species belonging to three different taxonomic groups and show that all species have a niche sufficiently distinct to ensure coexistence in a structured marine environment. We also provide evidence that pelagic habitats are, unsurprisingly, more diverse in space and time than Hutchinson imagined, the marine environment being neither unstructured nor stable in space and time. We, therefore, conclude that the niche theory, and its corollary the principle of competitive exclusion, apply as much for the plankton as for other forms of life, be they terrestrial or marine.

Global impacts of the 1980s regime shift.

Despite evidence from a number of Earth systems that abrupt temporal changes known as regime shifts are important, their nature, scale and mechanisms remain poorly documented and understood. Applying principal component analysis, change-point analysis and a sequential t-test analysis of regime shifts to 72 time series, we confirm that the 1980s regime shift represented a major change in the Earth's biophysical systems from the upper atmosphere to the depths of the ocean and from the Arctic to the Antarctic, and occurred at slightly different times around the world. Using historical climate model simulations from the Coupled Model Intercomparison Project Phase 5 (CMIP5) and statistical modelling of historical temperatures, we then demonstrate that this event was triggered by rapid global warming from anthropogenic plus natural forcing, the latter associated with the recovery from the El Chichón volcanic eruption. The shift in temperature that occurred at this time is hypothesized as the main forcing for a cascade of abrupt environmental changes. Within the context of the last century or more, the 1980s event was unique in terms of its global scope and scale; our observed consequences imply that if unavoidable natural events such as major volcanic eruptions interact with anthropogenic warming unforeseen multiplier effects may occur.

Marine biological shifts and climate.

Phenological, biogeographic and community shifts are among the reported responses of marine ecosystems and their species to climate change. However, despite both the profound consequences for ecosystem functioning and services, our understanding of the root causes underlying these biological changes remains rudimentary. Here, we show that a significant proportion of the responses of species and communities to climate change are deterministic at some emergent spatio-temporal scales, enabling testable predictions and more accurate projections of future changes. We propose a theory based on the concept of the ecological niche to connect phenological, biogeographic and long-term community shifts. The theory explains approximately 70% of the phenological and biogeographic shifts of a key zooplankton Calanus finmarchicus in the North Atlantic and approximately 56% of the long-term shifts in copepods observed in the North Sea during the period 1958-2009.

A niche-based theory of island biogeography.

The equilibrium theory of island biogeography (ETIB) is a widely applied dynamic theory proposed in the 1960s to explain why islands have coherent differences in species richness. The development of the ETIB was temporarily challenged in the 1970s by the alternative static theory of ecological impoverishment (TEI). The TEI suggests that the number of species on an island is determined by its number of habitats or niches but, with no clear evidence relating species richness to the number of niches however, the TEI has been almost dismissed as a theory in favour of the original ETIB. Here, we show that the number of climatic niches on islands is an important predictor of the species richness of plants, herpetofauna and land birds. We therefore propose a model called the niche-based theory of island biogeography (NTIB), based on the MacroEcological Theory on the Arrangement of Life (METAL), which successfully integrates the number of niches sensu Hutchinson into ETIB. To account for greater species turnover at the beginning of colonisation, we include higher initial extinction rates. When we test our NTIB for resident land birds in the Krakatau Islands, it reveals a good correspondence with observed species richness, immigration and extinction rates. Provided the environmental regime remains unchanged, we estimate that the current species richness at equilibrium is ~45 species (range between 38.39 and 61.51). Our NTIB provides better prediction because it counts for changes in species richness with latitude, which is not considered in any theory of island biogeography.

Marine biodiversity, ecosystem functioning, and carbon cycles.

Although recent studies suggest that climate change may substantially accelerate the rate of species loss in the biosphere, only a few studies have focused on the potential consequences of a spatial reorganization of biodiversity with global warming. Here, we show a pronounced latitudinal increase in phytoplanktonic and zooplanktonic biodiversity in the extratropical North Atlantic Ocean in recent decades. We also show that this rise in biodiversity paralleled a decrease in the mean size of zooplanktonic copepods and that the reorganization of the planktonic ecosystem toward dominance by smaller organisms may influence the networks in which carbon flows, with negative effects on the downward biological carbon pump and demersal Atlantic cod (Gadus morhua). Our study suggests that, contrary to the usual interpretation of increasing biodiversity being a positive emergent property promoting the stability/resilience of ecosystems, the parallel decrease in sizes of planktonic organisms could be viewed in the North Atlantic as reducing some of the services provided by marine ecosystems to humans.

Towards an Understanding of Large-Scale Biodiversity Patterns on Land and in the Sea.

This review presents a recent theory named 'macroecological theory on the arrangement of life' (METAL). This theory is based on the concept of the ecological niche and shows that the niche-environment (including climate) interaction is fundamental to explain many phenomena observed in nature from the individual to the community level (e.g., phenology, biogeographical shifts, and community arrangement and reorganisation, gradual or abrupt). The application of the theory in climate change biology as well as individual and species ecology has been presented elsewhere. In this review, I show how METAL explains why there are more species at low than high latitudes, why the peak of biodiversity is located at mid-latitudes in the oceanic domain and at the equator in the terrestrial domain, and finally why there are more terrestrial than marine species, despite the fact that biodiversity has emerged in the oceans. I postulate that the arrangement of planetary biodiversity is mathematically constrained, a constraint we previously called 'the great chessboard of life', which determines the maximum number of species that may colonise a given region or domain. This theory also makes it possible to reconstruct past biodiversity and understand how biodiversity could be reorganised in the context of anthropogenic climate change.

Impact of global climate cooling on Ordovician marine biodiversity.

Global cooling has been proposed as a driver of the Great Ordovician Biodiversification Event, the largest radiation of Phanerozoic marine animal Life. Yet, mechanistic understanding of the underlying pathways is lacking and other possible causes are debated. Here we couple a global climate model with a macroecological model to reconstruct global biodiversity patterns during the Ordovician. In our simulations, an inverted latitudinal biodiversity gradient characterizes the late Cambrian and Early Ordovician when climate was much warmer than today. During the Mid-Late Ordovician, climate cooling simultaneously permits the development of a modern latitudinal biodiversity gradient and an increase in global biodiversity. This increase is a consequence of the ecophysiological limitations to marine Life and is robust to uncertainties in both proxy-derived temperature reconstructions and organism physiology. First-order model-data agreement suggests that the most conspicuous rise in biodiversity over Earth's history - the Great Ordovician Biodiversification Event - was primarily driven by global cooling.

The FORCIS database: A global census of planktonic Foraminifera from ocean waters.

Planktonic Foraminifera are unique paleo-environmental indicators through their excellent fossil record in ocean sediments. Their distribution and diversity are affected by different environmental factors including anthropogenically forced ocean and climate change. Until now, historical changes in their distribution have not been fully assessed at the global scale. Here we present the FORCIS (Foraminifera Response to Climatic Stress) database on foraminiferal species diversity and distribution in the global ocean from 1910 until 2018 including published and unpublished data. The FORCIS database includes data collected using plankton tows, continuous plankton recorder, sediment traps and plankton pump, and contains ~22,000, ~157,000, ~9,000, ~400 subsamples, respectively (one single plankton aliquot collected within a depth range, time interval, size fraction range, at a single location) from each category. Our database provides a perspective of the distribution patterns of planktonic Foraminifera in the global ocean on large spatial (regional to basin scale, and at the vertical scale), and temporal (seasonal to interdecadal) scales over the past century.

The species chromatogram, a new graphical method to represent, characterize, and compare the ecological niches of different species.

The ecological niche sensu Hutchinson is defined as the set of environmental conditions allowing a species to grow, maintain, and reproduce. This conception of the niche, which is assimilated to a p-dimensional hypervolume, with p representing all environmental variables, has been widely applied in ecology. However, displaying the niche hypervolume has proved challenging when more than three environmental dimensions are considered simultaneously. We propose a simple method (implemented in the specieschrom R package) that displays the full multidimensionality of the ecological niche of a species into a two-dimensional space by means of a graphic we call species chromatogram. This method gives a graphical summary of the niche by representing together abundance gradients with respect to all environmental variables. A chromatogram enables niche optimums and breaths to be rapidly quantified, and when several chromatograms are examined (one per species), rapid comparisons can be made. From our chromatograms, we proposed a procedure that quantifies niche optimum and breadth as well as niche overlapping (index D) and the identification of the most discriminant combination of environmental variables. We apply these analyses on eight planktonic species collected by the Continuous Plankton Recorder (CPR) survey in the North Atlantic Ocean using 10 environmental variables. We display their full multidimensional niches and quantify their niche optimums and breadths along each dimension. We also compare our index D with other indices by means of hypervolume and dynRB R packages. By catching the full complexity of the niche, species chromatograms allow many different niche properties to be rapidly assessed and compared among species from niche optimums and breadths to the identification of the most relevant environmental parameters and the degree of niche overlapping among species. Species chromatograms may be seen as species' fingerprint and may also allow a better identification of the mechanisms involved in species assembly.

Addressing the dichotomy of fishing and climate in fishery management with the FishClim model.

The relative influence of fishing and Climate-Induced Environmental Change (CIEC) on long-term fluctuations in exploited fish stocks has been controversial1-3 because separating their contributions is difficult for two reasons. Firstly, there is in general, no estimation of CIEC for a pre-fishing period and secondly, the assessment of the effects of fishing on stocks has taken place at the same time as CIEC4. Here, we describe a new model we have called FishClim that we apply to North Sea cod from 1963 to 2019 to estimate how fishing and CIEC interact and how they both may affect stocks in the future (2020-2100) using CMIP6 scenarios5. The FishClim model shows that both fishing and CIEC are intertwined and can either act synergistically (e.g. the 2000-2007 collapse) or antagonistically (e.g. second phase of the gadoid outburst). Failure to monitor CIEC, so that fisheries management immediately adjusts fishing effort in response to environmentally-driven shifts in stock productivity, will therefore create a deleterious response lag that may cause the stock to collapse. We found that during 1963-2019, although the effect of fishing and CIEC drivers fluctuated annually, the pooled influence of fishing and CIEC on the North Sea cod stock was nearly equal at ~55 and ~45%, respectively. Consequently, the application of FishClim, which quantifies precisely the respective influence of fishing and climate, will help to develop better strategies for sustainable, long-term, fish stock management.

Expected contraction in the distribution ranges of demersal fish of high economic value in the Mediterranean and European Seas.

Fisheries and aquaculture are facing many challenges worldwide, especially adaptation to climate change. Investigating future distributional changes of largely harvested species has become an extensive research topic, aiming at providing realistic ecological scenarios on which to build management measures, to help fisheries and aquaculture adapt to future climate-driven changes. Here, we use an ensemble modelling approach to estimate the contemporary and future distributional range of eight demersal fish species of high economic value in the Mediterranean Sea. We identify a cardinal influence of (i) temperature on fish species distributions, all being shaped by yearly mean and seasonality in sea bottom temperature, and (ii) the primary production. By assessing the effects of changes in future climate conditions under three Representative Concentration Pathway (RCP2.6, RCP4.5 and RCP8.5) scenarios over three periods of the twenty-first century, we project a contraction of the distributional range of the eight species in the Mediterranean Sea, with a general biogeographical displacement towards the North European coasts. This will help anticipating changes in future catch potential in a warmer world, which is expected to have substantial economic consequences for Mediterranean fisheries.

Spawning stock and recruitment in North Sea cod shaped by food and climate.

In order to provide better fisheries management and conservation decisions, there is a need to discern the underlying relationship between the spawning stock and recruitment of marine fishes, a relationship which is influenced by the environmental conditions. Here, we demonstrate how the environmental conditions (temperature and the food availability for fish larvae) influence the stock-recruitment relationship and indeed what kind of stock-recruitment relationship we might see under different environmental conditions. Using unique zooplankton data from the Continuous Plankton Recorder, we find that food availability (i.e. zooplankton) in essence determines which model applies for the once large North Sea cod (Gadus morhua) stock. Further, we show that recruitment is strengthened during cold years and weakened during warm years. Our combined model explained 45 per cent of the total variance in cod recruitment, while the traditional Ricker and Beverton-Holt models only explained about 10 per cent. Specifically, our approach predicts that a full recovery of the North Sea cod stock might not be expected until the environment becomes more favourable.

Marine copepod diversity patterns and the metabolic theory of ecology.

Temperature is a powerful correlate of large-scale terrestrial and marine diversity patterns but the mechanistic links remain unclear. Whilst many explanations have been proposed, quantitative predictions that allow them to be tested statistically are often lacking. As an important exception, the metabolic theory of ecology (MTE) provides a rather robust technique using the relationship between diversity, temperature and metabolic rate in order to elucidate the ultimate underlying mechanisms driving large-scale diversity patterns. We tested if the MTE could explain geographic variations in marine copepod diversity on both ocean-wide and regional scales (East Japan Sea and North East Atlantic). The values of the regression slopes of diversity (ln taxonomic richness) over temperature (1/kT) across all spatial scales were lower than the range predicted by the metabolic scaling law for species richness (i.e. -0.60 to -0.70).We therefore conclude that the MTE in its present form is not suitable for predicting marine copepod diversity patterns. These results further question the applicability of the MTE for explaining diversity patterns and, despite the relative lack of comparable studies in the marine environment, the generality of the MTE across systems.

Plankton biogeography in the North Atlantic Ocean and its adjacent seas: Species assemblages and environmental signatures.

Plankton biodiversity is a key component of marine pelagic ecosystems. They are at the base of the food web, control the productivity of marine ecosystems, and provide many provisioning and regulating ecological services. It is therefore important to understand how plankton are organized in both space and time. Here, we use data of varying taxonomic resolution, collected by the Continuous Plankton Recorder (CPR) survey, to map phytoplankton and zooplankton biodiversity in the North Atlantic and its adjacent seas. We then decompose biodiversity into 24 species assemblages and investigate their spatial distribution using ecological units and ecoregions recently proposed. Finally, we propose a descriptive method, which we call the environmental chromatogram, to characterize the environmental signature of each plankton assemblage. The method is based on a graphic that identifies where species of an assemblage aggregate along an environmental gradient composed of multiple ecological dimensions. The decomposition of the biodiversity into species assemblages allows us to show (a) that most marine regions of the North Atlantic are composed of coenoclines (i.e., gradients of biocoenoses or communities) and (b) that the overlapping spatial distribution of assemblages is the result of their environmental signatures. It follows that neither the ecoregions nor the ecological units identified in the North Atlantic are characterized by a unique assemblage but instead by a mosaic of assemblages that overlap in many places.

Citizens and scientists collect comparable oceanographic data: measurements of ocean transparency from the Secchi Disk study and science programmes.

Marine phytoplankton accounts for approximately 50% of all photosynthesis on Earth, underpins the marine food chain and plays a central role in the Earth's biogeochemical cycles and climate. In situ measurements of ocean transparency can be used to estimate phytoplankton biomass. The scale and challenging conditions of the ocean make it a difficult environment for in situ studies, however. Here, we show that citizen scientists (seafarers) using a simple white Secchi Disk can collect ocean transparency data to complement formal scientific efforts using similar equipment. Citizen scientist data can therefore help understand current climate-driven changes in phytoplankton biomass at a global scale.

Effects of temperature on the behaviour and metabolism of an intertidal foraminifera and consequences for benthic ecosystem functioning.

Heatwaves have increased in intensity, duration and frequency over the last decades due to climate change. Intertidal species, living in a highly variable environment, are likely to be exposed to such heatwaves since they can be emerged for more than 6 h during a tidal cycle. Little is known, however, on how temperature affects species traits (e.g. locomotion and behaviour) of slow-moving organisms such as benthic foraminifera (single-celled protists), which abound in marine sediments. Here, we examine how temperature influences motion-behaviour and metabolic traits of the dominant temperate foraminifera Haynesina germanica by exposing individuals to usual (6, 12, 18, 24, 30 °C) and extreme (high; i.e. 32, 34, 36 °C) temperature regimes. Our results show that individuals reduced their activity by up to 80% under high temperature regimes whereas they remained active under the temperatures they usually experience in the field. When exposed to a hyper-thermic stress (i.e. 36 °C), all individuals remained burrowed and the photosynthetic activity of their sequestered chloroplasts significantly decreased. Recovery experiments subsequently revealed that individuals initially exposed to a high thermal regime partially recovered when the hyper-thermic stress ceased. H. germanica contribution to surface sediment reworking substantially diminished from 10 mm3 indiv-1 day-1 (usual temperature) to 0 mm3 indiv-1 day-1 when individuals were exposed to high temperature regimes (i.e. above 32 °C). Given their role in sediment reworking and organic matter remineralisation, our results suggest that heatwaves may have profound long-lasting effects on the functioning of intertidal muddy ecosystems and some key biogeochemical cycles.

Truncated bimodal latitudinal diversity gradient in early Paleozoic phytoplankton.

The latitudinal diversity gradient (LDG)-the decline in species richness from the equator to the poles-is classically considered as the most pervasive macroecological pattern on Earth, but the timing of its establishment, its ubiquity in the geological past, and explanatory mechanisms remain uncertain. By combining empirical and modeling approaches, we show that the first representatives of marine phytoplankton exhibited an LDG from the beginning of the Cambrian, when most major phyla appeared. However, this LDG showed a single peak of diversity centered on the Southern Hemisphere, in contrast to the equatorial peak classically observed for most modern taxa. We find that this LDG most likely corresponds to a truncated bimodal gradient, which probably results from an uneven sediment preservation, smaller sampling effort, and/or lower initial diversity in the Northern Hemisphere. Variation of the documented LDG through time resulted primarily from fluctuations in annual sea-surface temperature and long-term climate changes.