North Atlantic phytoplankton communities are often dominated by blooms of diatoms in the spring and dinoflagellates in the late summer and early fall [1–3]. Diatoms are characterized by their need for silicon for their cell wall, their tendency to form spring blooms in the mid and high latitudes, and are estimated to contribute approximately 40% of total marine primary production and particulate carbon exported to depth [4–6]. Dinoflagellates often bloom later than diatoms, are amongst the most genetically, morphologically, and trophically diverse groups of plankton; and include photosynthetic, mixotrophic and heterotrophic members [7]. Dinoflagellates are typically bi-flagellated with an organic cell wall formed from specialized vesicles (alveolae) that can form carbon-rich plates of various thicknesses [8,9]. Their C-rich walls, and often large genomes [10], can make their biomass higher in C:N and lower in N:P compared to the siliceous-walled diatoms [11,12], influencing their quality as food to higher trophic levels [13]. In coastal waters, toxin production by some diatom and several dinoflagellate species can episodically disrupt fishing, aquaculture, and economic activities [14,15]. Changes in the relative success of diatoms relative to dinoflagellates are expected to have a large impact on pelagic food web dynamics, fisheries, and the biochemical cycling of carbon, nitrogen, and phosphorus.

The Continuous Plankton Recorder (CPR) survey initiated by the Sir Alister Hardy Foundation for Ocean Science has been monitoring the plankton in the surface North Atlantic Ocean since the 1930s with millions of plankton abundance counts [16,17]. A silk mesh captures many larger phytoplankton species, predominantly diatoms and dinoflagellates. The methods used by the CPR survey have changed little since its initiation, providing an ideal dataset for quantifying how changes in physical and chemical conditions have altered plankton community structure and whether climate warming has left a detectable fingerprint on North Atlantic plankton community structure [17,18]. Analyses of the CPR dataset suggest there have been shifts in the abundance of diatoms relative to dinoflagellates over time and with environmental conditions in some regions of the North Atlantic over the past half century, but the direction of change may be regional. For example, Leterme et al. [19] report increases in the CPR phytoplankton colour index (PCI), the abundance of dinoflagellates, and decreases in the abundance of diatoms in the North Atlantic over the period 1958–2002, especially over the Southeast Atlantic since 1988. The annual development and decline of diatom and dinoflagellate blooms in the North Atlantic follow changes in irradiance, nutrient concentrations, temperature, and grazing, with diatoms proceeding dinoflagellates in cooler, more mixed, nutrient rich waters.

Long-term trends in growth conditions may be expected to shift diatom and dinoflagellate communities in similar ways to the interannual cycle, so that warming and increased stratification may favour dinoflagellates at the expense of diatoms. In the central North Atlantic, Zhai et al. [20] reported a decadal increase in the ratio of dinoflagellates and a decrease in the ratio of diatoms, relative to all other phytoplankton, over 1985–2009. In contrast, Hinder et al. [21] reported an increase in the abundance of diatoms relative to dinoflagellates over 1960–2009, but with most of the increase occurring post 1995 in the northeast Atlantic (45–60°N, 15°W-10°E). Most recently, Holland et al. [22] reported increases in diatom abundance in the CPR record (1960–2019) and many additional shorter near-shore time-series across the Greater North Sea but decreases in the Northeast Atlantic. By contrast dinoflagellate abundance showed decreases in the North East Atlantic and a mixture of increases and decreases in the Greater North Sea.

Changes in diatom and dinoflagellate community abundance over the last 60 years in the North Atlantic have been attributed to changes in temperature, water column stratification and nutrient supply, and wind-driven mixing [19,21,23]. Due to differences in scope and methods, it is difficult to determine if contrasting conclusions about diatom and dinoflagellate abundances across studies should be attributed to differences in the physical regimes across the regions, the time periods analyzed, or differences in how the data were analyzed [22]. Analyses across studies differ in the spatial and temporal subdivision of the North Atlantic examined and the taxa included in the analyses, potentially impacting conclusions. For example, Leterme et al. [19] included species with a frequency of occurrence >1%, Hinder et al. [21] examined the integrated abundance of diatoms and dinoflagellates present in > 4% of samples and with persistent abundance across their timeframe of analyses, while Zhai et al. [20] examined the total diatom and dinoflagellates abundance relative to all phytoplankton taxa identified. A major challenge in plankton time-series analysis is the large number of zero abundance data which is often overcome by focussing on dominant taxa and transforming data, both of which can induce biases [24]. Furthermore, interpretation of changes in abundance and the relative abundance of diatoms and dinoflagellates is complicated by large differences in the cell size and carbon content of the different diatoms and dinoflagellates making up the phytoplankton communities.

Collections of species with similar ecological or biogeochemical roles are commonly aggregated in models or data analyses into functional groups. We develop our analysis at the functional group level, i.e., aggregate biomass of diatoms and dinoflagellates, rather than genera or species, to greatly reduce the number of zeros in our dataset, because many species within these groups have similar niches leading to approximately neutral fluctuations in abundance of species within functional groups [25] and because aggregations of species are inherently more predictable. Diatoms are generally more prevalent in colder, nutrient-rich and well-mixed waters, while dinoflagellates are found in warmer, lower nutrient concentration, and stratified waters. To more robustly assess if there have been temporal changes in diatom and dinoflagellates since 1960 across the North Atlantic, and if there are substantive differences in temporal trends across regions, we quantify the temporal trend in diatom and dinoflagellate biomass and a diatom index (= diatom/ (diatom + dinoflagellate) biomass) using a carbon content estimate of the species identified and a statistical model for the seasonal cycle, decadal-scale fluctuations, de-trended and de-seasoned temperature, latitude, and the long-term trend (linear change over years) in five biogeographic provinces in the North Atlantic.

Our results revealed an increasing long-term trend in the diatom index (diatom biomass divided by total (diatom + dinoflagellate) biomass) in four of the five North Atlantic biogeographic provinces under consideration (NADR, NECS, NWCS, and SARC), with yearly average increases of 0.7–2.5% in NADR, NWCS, SARC, and NECS. By contrast, the long-term trend in the proportion of total biomass due to diatoms is negative in the ARCT province with a yearly average decrease of 0.9% (Fig 2, S4 Table). There was a long-term decrease in diatom biomass of 0.7–0.9% in ARCT and SARC, the two northernmost provinces and a long-term increase of 1.8–2.2% per year in NWCS and NECS. For dinoflagellate biomass, the long-term trend is decreasing in SARC, NADR and NECS with average rates of decrease 0.2–2.2%, whereas the trend in NWCS is increasing at a yearly rate of 1.2%. The average rate of decrease for total (diatom + dinoflagellate) biomass was 0.2–1.4% in the SARC, NADR, and ARCT with average rates of increase of 0.6–1.1% in NECS and NWCS. An annual increase of 1 or 2% per year compounds to an increase of 80% and 230% over 60 years, and a decrease of 1 or 2% per year compounds to a decrease of 45% and 70% over 60 years.

Fig 2. Average annual rate of change in log biomass (top panel: diatoms, red; dinoflagellates blue) and the logit of the biomass ratio (bottom panel: diatom biomass/ (diatom 

+ dinoflagellate biomass)) in the five biogeographic provinces estimated from a time, space and temperature model. An effect (slope) of 0.01 a^–1 corresponds to approximately a 1% change in biomass or the biomass ratio per year. Vertical dashed lines emphasize no change. Symbols are the median of the posterior distribution and error bars are 95% (thin) and 66% (thick) credible intervals. See S3 Fig. for a comparison between two models.

https://doi.org/10.1371/journal.pone.0323675.g002

In all biogeographic provinces, the intra-annual variation in the relative biomass of diatoms vs. dinoflagellates was characterized by strong seasonal cycles with a peak between March and May, and minimum value in August (Fig 3, bottom). In all five provinces, the intra-annual cycles in diatom biomass displayed a peak between April and June coinciding with the spring bloom. Following this peak, the diatom biomass declined as the dinoflagellate biomass increased toward its climax occurring in July (Fig 3, top). In NWCS, the dinoflagellate biomass exhibited the lowest intra-annual variability, remaining relatively high and continually high throughout the year, consistent with reports of relatively high dinoflagellate biomass in the NWCS, particularly in the Winter [39]. The annual mean biomass is higher for dinoflagellates compared to diatoms in all provinces except the ARCT (horizontal lines, Fig 3, S5 Table). Dinoflagellate relative to diatom biomass was highest in NWCS. Dinoflagellate biomass was lower than diatom biomass, on average, only in the Arctic (ARCT and BPLR), consistent with this province currently being a less favourable habitat for dinoflagellates and greater potential for environmental change to shift the Arctic community towards dinoflagellates due to long-term changes in stratification and warming. Total diatom + dinoflagellate biomass was highest in NECS and lowest in the ARCT.

Fig 3. Mean monthly log biomass (top panels: diatoms, red; dinoflagellates, blue) and logit of biomass ratios (bottom panels: diatom biomass/ (diatom 

+ dinoflagellate biomass)) for five biogeographic provinces estimated from a time, space and temperature model. Horizontal lines denote annual mean log biomass (top) or logit of the diatom index (bottom). Symbols are the median of the posterior distribution and error bars are 95% credible intervals. See S4 Fig. for a comparison between two models.

https://doi.org/10.1371/journal.pone.0323675.g003

We computed an SST anomaly from the Hadley SST data product and a model of SST that accounted for variation by month, over years, across provinces, and with latitude within each province. The SST anomaly was used as a predictor for the diatom index and phytoplankton biomasses. In all provinces, the SST anomaly correlated negatively with the diatom index (Fig 4, bottom right), indicating anomalously warmer SST favored higher dinoflagellate relative to diatom biomass. The SST anomaly correlated positively with the biomasses of both functional groups, indicating enhanced net phytoplankton biomass at warmer SST, but the dinoflagellate response was relatively larger (Fig 4, top right). The effect of SST anomaly on diatom and dinoflagellate biomass in the NWCS province was nearly equal, resulting in almost no effect on the diatom index. The biomass and diatom index trends with latitude were mixed (Fig 4, left side). In the SARC and NADR provinces, diatoms were relatively more dominant in the north, while in the NWCS the community shifted towards dinoflagellates towards the north.

Fig 4. Mean effect of latitude (left panels) and temperature anomaly (right panels) for log biomass (top panels: diatoms, red; dinoflagellates, blue) and logit of biomass ratios (bottom panels: diatom biomass/ (diatom 

+ dinoflagellate biomass)) for five biogeographic provinces estimated from a time, space and temperature model. An effect (slope) of 0.1 corresponds to approximately a 10% change in biomass or the biomass ratio per °latitude or °C. Symbols are the median of the posterior distribution and error bars are 95% (thin) and 66% (thick) credible intervals. Vertical dashed lines emphasize 0 change. See S5 Fig. for a comparison between two models.

https://doi.org/10.1371/journal.pone.0323675.g004

The posterior means for the effects of month, year, province, and latitude from our main model (Time-Space-Temperature) were essentially identical to the results of the Time-Space models. The Time-Space models lacked the SST anomaly predictor and contained a decadal effect omitted in the Time-Space-Temperature model. The SST anomaly had predictive power and reduced uncertainty in these estimated parameters (S3-S5 Figs). Since the SST anomaly was constructed to be independent of the other predictors (month, year, province, latitude), it did not affect the median values of the corresponding parameters. The uncertainty (95% credible interval) in the posterior means was generally smaller for the Time-Space-Temperature model, most notably for the estimates of the inter-annual trends on biomass and biomass ratio (S2 Fig.). The posterior distributions of the decadal effects from the Time-Space models were clustered around zero and the 95% credible intervals generally included 0 (S6 Fig.), implying that the nonlinear temporal changes in the diatom index and phytoplankton biomasses were negligible. Some of the effects were large (±0.5, corresponding to a change of 40–60% relative to the mean) but with a correspondingly large uncertainty. These results support the use of a linear trend over years, since the data did not reveal a non-linear trend on the decade scale.

We anticipated the possibility of a non-linear change in the diatom index and biomasses with time, which we modelled as step-wise changes for each decade. While we found some evidence for non-linear changes on the decade scale, the effects were highly variable from decade to decade and our estimates were very uncertain (S6 Fig). We found that the temperature in a patch of water relative to the mean temperature as predicted by location, month, and year (the temperature anomaly) had a notable effect on biomass and the diatom index (Fig 4) and reduced the posterior uncertainty of the effects of month and year as well (S2-S3 Figs).

While temperature change over time (year and month) was not a primary focus in this work, we quantified and removed this variation to compute a temperature anomaly and so we report the results of that analysis. The SST data exhibited the expected seasonal cycles (S7 Fig) with similar results at the CPR sampling locations (blue) and province-wide results (black). In the NWCS, the CPR sampling locations were generally cooler by 2–3°C than the province as a whole and in the other provinces there were notable differences in the temperature at CPR sampling locations and throughout the province in the winter months (except for the ARCT province for which this comparison was not made.) The latitudinal trend in temperature was negative as expected (cooler in the north of each province) and similar whether the CPR sampling locations or whole province was studied (S8 Fig., left). Sea-surface temperatures exhibited an increasing trend of about 0.01–0.02°C a^–1 across the provinces, except at the CPR sampling locations for SARC and NADR which showed no increase in temperature and a decrease in temperature over the study period, respectively (S8 Fig., right). The Hadley SST data show a statistically significant linear increasing trend of similar magnitude when studied at 1° x 1° spatial resolution throughout almost the entire study region (S9 Fig.).

Variable importance for the Time-Space-Temperature model assessed from the changes in the Bayesian R² by omitting the predictors month, latitude, and temperature anomaly one at a time showed that month accounted for most of the variance followed by temperature anomaly. Latitude had only a minor explanatory effect (1–2% of total variance, S6 Table). The total variance explained by the Time-Space-Temperature model ranged from 32–64%. Model checking showed that the posterior distribution of the means and variances of the diatom index and diatom and dinoflagellate biomass from the Time-Space-Temperature models well approximated the data (S10-S11 Figs).

There is accumulating evidence that climate warming over the last century is altering ocean conditions, primary production, chlorophyll concentration, and the biogeography of the key phytoplankton taxa [40–43]. Diatoms and dinoflagellates are two of the major phytoplankton functional groups in the North Atlantic and changes in their relative biomass may impact export production [6]. It has been hypothesized that climate warming will shift plankton communities towards dinoflagellates and away from diatoms, altering food web composition with potentially significant consequences for fisheries [19,44]. The CPR data have been used to investigate trends in the biomass of phytoplankton, diatom and dinoflagellate functional groups, and the relative abundances of diatoms and dinoflagellates on many occasions, but a lack of standardization in how the plankton community has been assessed across regions (e.g., subset of species examined, geographical boundaries, statistical framework, using sums of abundances vs. biomass) and temporal range analyzed makes rigorous North Atlantic regional-temporal comparisons challenging. Here we synthesize nearly 60 years of data (1960–2017) from the Continuous Plankton Recorder project spanning much of the northern North Atlantic divided into 5 provincial regions (Fig 1) to identify if there has been a long-term trend in diatom and dinoflagellate biomass and the proportion of their biomass contributed by diatoms (diatom index) and whether these changes vary regionally. Since the CPR samples the ocean at 7 m depth with a coarse mesh, our analysis was restricted to changes in the biomass of relatively large diatoms and dinoflagellates in the upper-mixed layer of the ocean. In contrast to expectations, we find there has been temporal increase in the diatom index over much of the North Atlantic, except the Arctic region, and the sum of the total biomass of the diatoms and dinoflagellates increases in the shelf regions but decreases in the central and sub-Arctic regions.

Our analysis confirms that there are stark regional differences in how diatom and dinoflagellate biomass has changed in the North Atlantic since the 1960s (Fig 2). There were large increases in diatom biomass in the eastern and western shelf regions (NWCS, NECS), diatom biomass was essentially unchanged in the central North Atlantic (NADR), and decreased in the polar regions (SARC, ARCT). Dinoflagellate biomass increased in the NWCS, was unchanged in the ARCT, and decreased in the other three provinces. The decline in diatoms in the NADR, sub-Arctic and Arctic are broadly consistent with a global model of ocean biogeochemistry coupled to a climate model [45]. There is relatively little comparable observational data from the Arctic and North Atlantic Drift province, but Zhai et al. [20] found a decrease in diatom relative to diatom + dinoflagellate abundance in the ARCT and NADR over 1991–2009, consistent with our longer-term trend. While Zhai et al. [20] link these changes in community structure to the NAO, sea surface temperature and stratification, Hátún et al. [23] hypothesize decreases in dissolved silicate may be responsible. Also consistent with our observations: Osman et al. [46] found primary productivity and diatom and dinoflagellate abundance has been in decline in the sub-Arctic, Head and Sameoto [47] reported increases in both diatom and dinoflagellate abundance between 1962–1971 versus 2001–2003 on the Newfoundland shelf, eastern Scotian shelf and central/western Scotian shelf, and Johns et al. [39] found that dinoflagellate abundance has been increasing in the Grand Banks region in winter. There is a wealth of studies from the Northeast Coastal Shelf, particularly in the North Sea, but reported results are not unambiguous. For example, Leterme et al. [19] found a decline in diatom abundance in the NE and SE Atlantic especially since the late 1960s/early 1970s, Hinder et al. [21] found an increase in diatom relative to dinoflagellate abundance using a subset of diatoms species related to sea surface temperature and windy conditions, while Edwards et al. [48] found a north-south contrast, with an increase in diatom abundance with warming in the more northerly versus more southerly part of the region. It is difficult to compare the results across these studies and establish the extent of regional differences across the North Atlantic without a consistent analysis of the entire dataset.

Our analysis identified distinct regional differences in the long-term temporal trend in diatom and dinoflagellate biomass by accounting for intra-annual, interannual, and spatial variability in the diatom index and diatom and dinoflagellate biomass. Our analysis captured the strong interannual trend, including expected differences in timing of peak biomass of both functional groups (diatoms before dinoflagellates), and delay in blooms further north (Fig 3). We evaluated two mechanisms to account for a non-linear trend in biomass and the biomass index with time: decadal variation and alternatively a temperature anomaly, finding that the temperature anomaly approach produced the most explanatory power and reduced uncertainty in the parameter estimates (S3-S5 Figs). Spatial variation was incorporated using the standardized Longhurst provinces and latitude to allow for variation within provinces, while still permitting the spatial aggregation necessary to observe a strong signal. The regular CPR routes have sometimes shifted northward or southward over time, leading to additional variation within provinces that can be partially attributed to the latitude of the observation (see Edwards et al. [48] for a recent detailed description of the CPR dataset).

Regional differences in the response of diatom and dinoflagellate abundance have been correlated to climate indices such as the NAO and associated differences in hydroclimatic conditions such as wind, mixed layer depth and upper water column stratification, that in turn affect nutrients and conditions such as sea surface temperature and light, e.g., [19,21,48]. Interactions between environmental conditions and trophic transfer to zooplankton and fish may also be altering the timing and abundance of diatoms and dinoflagellate populations, through differential effects of temperature on phytoplankton versus zooplankton or trophic cascades [49–51]. Given there has been warming throughout most of the North Atlantic over the past 6 decades [52–54](S9 Fig) and a diversity of responses in diatom and dinoflagellate biomass across regions, there is clearly no universal link between the NAO or increases in sea surface temperature and the temporal trajectory of diatom or dinoflagellate biomass.

Although there is no coherent response of diatom or dinoflagellate biomass with increasing sea surface temperatures in the North Atlantic since the 1960s, anomalous temperature increases, after accounting for province, latitude, month, and year, result in a lower diatom index (shift towards dinoflagellates) in all provinces except the NWCS (Fig 4). We speculate that since the NWCS community is already relatively enriched in dinoflagellates with low interannual variation, there is limited potential for further shifts towards dinoflagellates (Fig 3). This almost universal response may be a direct effect of increasing temperature on growth rates, leading to increased biomass. Indirect effects of temperature can be positive or negative through correlated increases in stratification and windiness, affecting turbulence and the availability of light and nutrients. Differential effects of temperature on grazers and their prey may alter food web structure, diatom and dinoflagellate biomass and the diatom index. Increases in the temperature anomaly shifts the community towards dinoflagellates, while the long-term trend with time (and increasing temperature) shifts the community towards diatoms in most regions. We hypothesize that these short-term variations in temperature are too rapid for diatoms and dinoflagellates to adapt and therefore reflect eco-physiological responses to the associated hydroclimatic changes. Independent analyses in other parts of the ocean and experimental evolution studies in the lab show that phytoplankton can adapt to changes in temperature over several tens to hundreds of generations [55–58]. Our inference is that plankton adapt evolutionarily to temperature change over decadal scales and to predict or interpret the effects of decades of temperature change requires a consideration of evolutionary as well as eco-physiological responses to environmental variables.

Here we document a long-term shift towards diatoms and away from dinoflagellates, on a biomass basis, throughout the temperate and sub-polar North Atlantic. This shift towards diatoms was the result of both increasing and decreasing trends in diatom and dinoflagellate biomass, depending on the biogeographic province. This analysis reveals a signature of a large-scale restructuring of the North Atlantic phytoplankton community not typically anticipated as the consequences of climate change. To document this trend required decades of investment in consistent sampling. Data from the CPR plankton survey are as valuable as they are rare. Continued investment in these surveys is essential for developing an understanding of the ocean-climate system. Although we reported results for the Arctic province, we recognize a severe under-sampling of the spatial extent of this province and caution our results are only representative of the southernmost extent of the Arctic and Boreal province in the North Atlantic. In the other four provinces, we see good agreement in the rate of warming at CPR sampling sites and the whole province in the NWCS and NECS, but note that the average temperature at the sites sampled by the CPR in the SARC and NADR decreased over 6 decades, despite the average temperature in these provinces increasing (S8, S9 Figs). As a result, we caution that CPR sampling in SARC and NADR may not be representative of the provinces as a whole, so there is some risk in extrapolating observed changes at sampling sites to the whole province in these provinces. The hallmark of our analysis is that the trends are highly variable across provinces, reflecting the consequences of regional changes in climate (e.g., increased windiness in NECS) and differences in the baseline community composition across provinces. Notably, dinoflagellate biomass was much lower in the Arctic resulting in a higher diatom index and dinoflagellate biomass was only weakly seasonal in the NWCS (Fig 3), so it seems reasonable to anticipate distinctive responses to climate change in these provinces.

Assuming the underlying mechanisms do not change, the next few decades could bring further decreases in diatom and dinoflagellate biomass, with a shift towards diatoms in much of the North Atlantic and a shift towards dinoflagellates in the Arctic. These changes have likely had notable consequences for carbon export and the amount of biomass transferred up the food web. Future climate change might have similar effects, although non-linear or unanticipated changes are certainly possible. Extrapolating the long-term effects of climate change from this analysis is challenging because of the opposing factors documented by the long-term change (Fig 2) and the temperature anomaly (Fig 4). The effect of a 1°C temperature anomaly on diatom and dinoflagellate biomass and the diatom index is approximately equal, but opposite, to several decades of long-term climatic change (Figs 2, 4). Changes to future carbon export and trophic transfer will depend on the relative importance of long-term trends and short-term variation arising from temperature change, sea-ice melt, changes in freshwater inputs, wind-driven mixing and circulation.