Response of the major phytoplankton groups

The six decades used here include periods of consistent ocean cooling (1959–1984) and warming (1984–2008) (Fig. 1a). The mean latitude of three isotherms at 11, 12 and 13 °C are correlated with the sea surface temperature (SST) (Fig. 1b, Supplementary Fig. 3), all three moving south in the period of cooling and then moving north in the period of warming. We found that diatoms and dinoflagellates, major phytoplankton groups, both broadly exhibited evidence for a plastic environmental niche: Fig. 2 illustrates the relationship between the percentage of each group north of each of the three isotherms and the latitude of those isotherms in the twelve 5-year periods 1954–2013. In all cases there was a significant negative correlation (Supplementary Table 1a): as the isotherms moved north the proportion of each group north of each isotherm fell and vice versa.

Figure 1: Sea surface temperatures and isotherm latitudes. (a) Mean of the estimated SST values over the twelve 5-year periods. (b) Mean latitudes of the 11, 12 and 13 °C isotherms for each 5-year period. Full size image

Figure 2: Proportions of diatom and dinoflagellate populations north of three isotherms. Proportions (normalized) of the (a) diatom and (b) dinoflagellate populations north of the three isotherms within the geographic area 45–64° N, 20° W–8° E in the twelve 5-year periods from 1954–1958 to 2009–2013. The isotherms move north as the SST rises; these plots illustrate negative correlations (at P<0.05) between the normalized population percentages north of each isotherm and the mean latitude of the isotherms. A loess smoother was used for locally weighted polynomial regression, the grey area indicating the 95% confidence interval for the line. The P values are listed in Supplementary Table 1a. Full size image

Despite this, both groups exhibited major range changes over recent decades: Fig. 3 maps the two groups in the 5-year periods at the start of the cooling period (1959–1963), the transition from cooling to warming (1984–1988) and the end of the warming period (2004–2008). During the period of cooling the median latitude of the diatoms moved south 84 km before moving north 92 km during the period of warming; the median latitude of the dinoflagellates moved south 111 km then north 135 km in the same periods. These range changes were smaller than the movement of the isotherms, that is, the velocity of climate change (Fig. 1, Table 1b, Supplementary Table 5).

Figure 3: Movement of diatoms and dinoflagellates in cooling and warming periods. (a–f) Maps of the totals of the log-transformed (log(x+1)) cell counts determined by ordinary kriging for all diatom and dinoflagellate taxa. The maps were independently scaled 0.0–1.0 to highlight population movements. The movement of the dinoflagellates south in the period of cooling and then north in the period of warming exceeds the corresponding movement of the diatoms. Full size image

Table 1 Details of each taxon and isotherms at 11, 12 and 13 °C. Full size table

Differences revealed by individual taxa

Although the two groups appear to be exhibiting similar behaviour, analysis of the movements of the 35 individual taxa used here (mostly species) provided compelling evidence that more diatom taxa exhibit niche plasticity than do dinoflagellate taxa. Figure 4 and Supplementary Fig. 2 show the movements of each taxon in the periods of cooling and warming, Table 1a indicates significant negative correlations between proportion north of isotherms and isotherm latitudes for each taxon and Supplementary Figs 4–42 show further details for each taxon and group.

Figure 4: Movement of each taxon and isotherm in the cooling and warming periods. Movements in the cooling period of 1959–1984 are indicated with no colours, movements in the warming period of 1984–2008 are indicated with solid colours. The zero position on the x axis is the starting position of the range median latitude of each taxon at the start of each period. Metridia longa, for example, moved south 492 km in the cooling period then north 680 km in the warming period to move 188 km north overall in the two periods. In contrast Eucampia zodiacus moved north 56 km in the cooling period then south 225 km in the warming period to move 169 km south overall in the two periods. The one, two or three asterisks denote significant negative correlations (P<0.05) between the percentages of the populations north of one, two or three isotherms and the mean latitude of the isotherms in the six decades 1954–2013. A significant negative correlation indicates niche plasticity in relation to thermal change. CEU, Calanus, Euchaeta and Undeuchaeta; DIA, diatoms; DIN, dinoflagellates; ISO, isotherms; MP, Metridia and Pleuromamma. Full size image

Ten of the twelve diatom taxa exhibited strong negative correlations between the percentage north of an isotherm and that isotherm position in periods of both warming and cooling (Table 1a), Ditylum brightwellii and Skeletonema costatum being the two diatom species not exhibiting such evidence of a plastic environmental niche. Only one of the diatom taxa, Rhizosolenia styliformis, exhibited a significant negative correlation between population size and mean SST (two others exhibited positive correlations, Table 1c, Supplementary Table 2a). The general observation is that diatoms appear able to adapt to SST changes and those SST changes do not negatively affect their abundance.

In contrast to the diatoms, only 4 of the 12 dinoflagellate taxa (Ceratium fusus, C. minutum, Dinophysis spp. and Protoperidinium spp.) exhibited environmental niche plasticity at all three isotherms examined (Table 1a). Of the dinoflagellate taxa which exhibited niche plasticity to SST at any isotherm, all exhibited negative correlations between population size and mean SST (Table 1c, Supplementary Table 2a) with the exception of Ceratium minutum which has a very low population size over the six decades examined here (Table 1d), resulting in a major decline in the abundance of dinoflagellates in the NE Atlantic region in the recent warming period, as has been noted previously in a shorter time-series21. The general observation is that dinoflagellates either showed no niche plasticity to SST changes or showed plasticity accompanied by falling populations and/or very low populations.

Response of the copepods

Of the copepods, five species from the Calanus, Euchaeta and Undeuchaeta genera exhibited no evidence of niche plasticity (Table 1a, E. acuta in Figs 5 and 6, top row). The warm-water species C. helgolandicus exhibited population growth in response to warming while the cold-water species C. finmarchicus exhibited the opposite response (Table 1c). Of the six Metridia and Pleuromamma species four exhibited evidence of niche plasticity (M. lucens, P. abdominalis, P. gracilis and P. robusta) (Table 1a, M. lucens in Figs 5 and 6, bottom row) while two (M. longa and P. borealis), showed no such evidence. The two species in this group with the highest abundances, M. lucens and P. robusta, exhibited a negative correlation between population size and SST in the warming period despite exhibiting niche plasticity to SST (Table 1a,c). The general observation is that no Calanus, Euchaeta or Undeuchaeta genera exhibited niche plasticity and the Metridia and Pleuromamma species showing evidence of plasticity had very low and/or declining abundance.

Figure 5: The proportions (normalized) of two individual copepod taxa north of three isotherms and their abundances in the twelve 5-year periods. Euchaeta acuta on the top row did not exhibit evidence of niche plasticity in relation to thermal change; Metridia lucens on the bottom row did exhibit evidence of niche plasticity. (a,c) Proportions (normalized) of the populations of the two species north of isotherms at 11, 12 and 13 °C in the twelve 5-year periods from 1954–1958 to 2009–2013. The isotherms move north as the SST rises; Euchaeta acuta exhibits no correlation (at P<0.05) between the normalized population percentages north of each isotherm and the mean latitude of the isotherms; Metridia lucens exhibits a significant negative correlation. A loess smoother was used for locally weighted polynomial regression, the grey area indicating the 95% confidence interval for the line. The P values are listed in Supplementary Table 1b. (b,d) Abundance: the mean of the values derived by kriging at each (longitude, latitude) for each 5-year period. Full size image

Figure 6: Movement of two individual copepod taxa in cooling and warming periods. (a–f) Maps of the totals of the log-transformed (log(x+1)) abundance determined by ordinary kriging. The maps were independently scaled 0.0–1.0 to highlight population movements. In the periods of cooling then warming the E. acuta median latitude moved south 5 km then north 182 km while the M. lucens median latitude moved south 87 km then continued south 38 km. Full size image

The complexity of the response of these taxa is illustrated by Figs 5 and 6, which plot and map the responses of two copepod taxa, E. acuta and M. lucens. The former does not display niche plasticity: there was no correlation between proportion north of the isotherms and the latitude of the isotherm (Fig. 5a, Table 1a), meaning that the geographic range of the species moves with the isotherm (Fig. 6a–c): the species moved south 5 km in the period of cooling and then north 181 km in the period of warming (Table 1b). The species displays no correlation between abundance and SST (Fig. 5b, Table 1c).

In contrast, M. lucens displays niche plasticity: significant negative correlations between the proportion north of the isotherms and the latitude of the isotherm (Fig. 5c, Table 1a) were observed and the species unusually moved south in both the periods of cooling and warming, 87 and 38 km, respectively (Fig. 6d–f and Table 1b). The abundance of the species, however, fell in the period of cooling and has not recovered in the period of warming (Fig. 5d).

Range movements in the warming period

The taxa examined here exhibiting niche conservatism (from all groups) showed a mean northward range shift in the warming period of 99 km per decade, contrasting with a 7 km per decade shift for those taxa exhibiting niche plasticity at all three isotherms (derived from Table 1a,b). The mean poleward movement in the warming period for all taxa analysed here was 54 km per decade while the mean latitude shifts for the isotherms at 11, 12 and 13 °C in the same period were 151, 126 and 104 km per decade, respectively. In the period of warming in the geographic area used here we found differences of up to 900 km in the movement of the median range latitude of individual taxa: the diatom Eucampia zodiacus exhibited a southerly movement of >220 km contrasting with the northerly movement of >680 km of the copepod Metridia longa (Fig. 4, Table 1b). While these two species exhibited the largest southerly and northerly range shifts of the taxa investigated here they are not extreme outliers: three taxa exhibited southerly movement of more than 100 km and 18 taxa exhibited a northerly movement of greater than 100 km in that period (Fig. 4, Table 1b).

Analysis of two potential confounding factors

Two of the possible explanations for the lack of range shifts found here among some taxa, particularly the diatoms, are (i) phenological changes, whereby taxa adjust their seasonal timing of maximum abundance so that they continue to experience the same thermal regime even when sea temperatures are warming or cooling, and (ii) the relative positions of the taxon ranges and the latitudes of the isotherms used, whereby the extent of range movement depends on whether the range centre or range limits for a taxon are considered. To consider these possible explanations, we examined phenological shifts and the positions of the taxon ranges with respect to the isotherm latitudes over the period of warming and the six decades respectively. During the recent warming (1984–2008), there was no link between the extent of range movement for individual taxa and their shift in phenology (Fig. 7), that is, taxa that showed a limited northerly range shift in the recent warming era did not have a stronger tendency to shift their phenological timing of abundance to earlier in the year. Note however that generally across taxa, regardless of their range change, there was a tendency for a phenological shift to earlier in the year. The extent of range movement across taxa seemed unrelated to whether isotherms were examined at the range centre or range limits. First, for example, we found similar patterns of range movement with respect to different isotherms that occurred in different parts of the range of each taxon. Second, the extent of range movement seemed unrelated to whether taxa occurred largely to the south of the isotherms considered (for example, the copepod Undeuchaeta plumosa), to the north (for example, the copepod Calanus finmarchicus and the diatom Skeletonema costatum) or straddled the isotherms (the majority of taxa) (Supplementary Figs 4a–42a).