For ∼35% of the areas analyzed, cluster membership did not change from 1979 to 1983 to 1998–2002 (dark gray areas in Figure 5). In the remaining ∼65% of the pixels, the most conspicuous phenological changes were the emergence of the Transitional Bloom regime (blue and green areas, Figure 5) and the disappearance of the Transitional Tropical regime (purple and pink areas, Figure 5). More precisely, 13.5% of the 1979–1983 pixels changed their membership in Transitional Bloom, and 19% of the 1979–1983 changed their membership from Transitional Tropical to another regime. To further explore these changes of cluster membership, we looked to characterizations of upper-ocean stratification, reports of widespread decadal-scale ecosystem-related change (e.g., Chl concentrations), and changes in large-scale climate indices and their oceanic signatures. To map mixed-layer behavior specifically, changes in the average annual maximum mixed layer depth (MLD;Figure 6a) and the timing of the annual maximum (Figure 6b), we relied on Simple Ocean Data Assimilation (SODA) model output [Carton and Giese, 2008]. The MLD is determined using a temperature criterion, as being the depth where the temperature is 0.2°C different from the temperature at 10 m [de Boyer Montégut et al., 2004].
4.2.1. Emergence of the Transitional Bloom Regime
 Emergence of the Transitional Bloom regime during the 1998–2002 SeaWiFS years is observed in the 20°–40°N latitudinal belt of both the Atlantic and Pacific Oceans (green and blue regions in Figure 5). This “new” regime replaces much of the Bloom and Subtropical North regimes of the 1979–1983 CZCS years: nearly a third of each of these original regimes had converted to Transitional Bloom (Table 2). We have also shown that this replacement is even more important if the whole SeaWiFS series (1998–2010) is considered, but also that it is dominant during La Niña years.
Table 2. Changes in Regime Assignments Between the Periods 1979–1983 (CZCS) and 1998–2002 (SeaWiFS)a
|Regimes and Seasonal Cycles||Total Number of Pixels for the CZCS Period||Bloom||Tropical||Subtropical North||Subtropical South||Transitional Bloom|
|Transitional Tropical North Hemisphere||274||7%||42%||22%||20%||9%|
|Transitional Tropical South Hemisphere||221||5%||28%||5%||60%||3%|
 One area that changed from Bloom to Transitional Bloom (green regions in Figure 5) is the western subtropical North Atlantic. Phenologically (Figures 1a and 1f), this change can be seen in both the seasonality (i.e., difference between annual maximum and minimum) of the normalized surface Chl and the timing of the peak. Seasonality during the 1998–2002 period (Figure 1f) is relatively muted, and the time of peak normalized Chl is shifted earlier by two months (from May to March). SODA mixed layer depths show a general shoaling of the annual maximum depth over that same time period (Figure 6a); no change in the timing of the maximum was observed (Figure 6b). Chlorophyll concentrations in this region generally diminished between the 1979–1983 years and the 1998–2002 years [Antoine et al., 2005; Martinez et al., 2009]. Both these lines of evidence (decreased mixing and generally lower Chl concentrations), as well as the shift to a more muted seasonality, are consistent with a presumed reduction in nutrient flux to the upper layer, related to enhanced upper-ocean stratification [as proposed byBehrenfeld et al., 2006; Follows and Dutkiewicz, 2001].
 For subpolar North Atlantic regions, the timing of the chlorophyll peak, variability of mixed layer depth [Henson et al., 2009], and abundance of zooplankton [Beaugrand et al., 2000] have all been correlated with the North Atlantic Ocean (NAO) index [Hurrell, 1995]. Such NAO correlations are less evident, however, for the subtropical areas (25°N–40°N) [Carton et al., 2008; Henson et al., 2009] where we observed the change from Bloom to Transitional Bloom. A more relevant index for this region is the Atlantic Multidecadal Oscillation (AMO) index, which tracks the long-term detrended mean of North Atlantic Ocean sea surface temperature (SST), revealing cycles of about 65–80 years duration [Enfield et al., 2001]. This index has been found to correlate with chlorophyll–SST long-term variability in the North Atlantic [Martinez et al., 2009]. The AMO index shifted from negative (cool phase) during the 1979–1983 CZCS years to positive (warm phase) during 1998–2002 SeaWiFS years. This overall increase of North Atlantic SST and likely consequent increase in upper-layer stratification is also consistent with the results of our mixed-layer and phenological analyses in the Western sub tropical Atlantic—i.e., generally shoaling mixed layer annual maximum depths (red regions inFigure 6) and generally muted normalized-Chl seasonality (green pixels inFigure 5).
 In other areas of the subtropical North Atlantic, we observe shifts from Bloom to Subtropical North (red regions in Figure 5) and, to a lesser extent, from Subtropical North to Transitional Bloom (blue regions in Figure 5). Overall, these changes describe a general dampening of the differences between seasonal minima and maxima and a spreading of the ‘growth’ season over one or two additional months (Figure 1). Other analyses document a decrease in upper-ocean chlorophyll content in these regions, as observed comparing the trends for two disconnected climatologies of the 1979–1983 and 1998–2002 years [Antoine et al., 2005; Martinez et al., 2009] but also more continuously over the period 1998–2006 [Behrenfeld et al., 2006]. The phenological change of the whole subtropical North Atlantic Ocean could be linked to enhanced stratification, which may in turn be related to the SST variability indicated by the AMO index (i.e., enhanced stratification during AMO warm, positive-index phases).
 Transitional Bloom emergence is also observed in the Kuroshio area, replacing earlier Bloom conditions (western North Pacific; green pixels in Figure 5). Here, chlorophyll concentrations decreased between 1979–1983 and 1998–2002 [Martinez et al., 2009] and mixed layer depth annual maxima shoaled (Figure 6a), similar to the pattern observed in the North Atlantic. No change was observed in the timing of peak normalized chlorophyll (Figures 1a and 1f) or annual maximum depth of mixing (Figure 6b).
 Widespread emergence of the Transitional Bloom regime occurred in the North Pacific along the longitudinal belt of 20°–30°N, replacing the Subtropical North regime observed in the period 1979–1983 CZCS (blue regions in Figure 5). This change implies a delay of about one month in the phytoplankton annual maximum (from February to March) and a smoothed seasonality (Figures 1c and 1f). SODA MLDs (Figure 6) indicate a shoaling of the maximum mixed layer depth and no change in the timing of the maximum. A general decrease of surface chlorophyll concentrations was observed over this time period [Antoine et al., 2005; Martinez et al., 2009].
 The region of this major phenological change is located approximately along the Pacific Transition Zone Chlorophyll Front (TZCF) [Polovina et al., 2001], a dynamic, seasonally migrating, basin-wide front that divides the high-chlorophyll subarctic gyre from the low-chlorophyll subtropical gyre. Strong chlorophyll seasonality is observed to the north of the front and weak seasonality to the south [Longhurst, 1995]. During El Niño winters, the front migrates especially far southward, to move northward during La Niña periods [Bograd et al., 2004]. During the 1979–1983 CZCS years (which included a strong El Niño event), the TZCF exhibited its greatest observed range of migration and southward extent [Bograd et al., 2004]. This frontal behavior is consistent with the phenological conditions we detected–i.e., the presence of the Subtropical North regime (moderate seasonality) in the longitudinal belt of 20°–30°N. The subsequent emergence of the Transitional Bloom regime (relatively muted seasonality) is similarly consistent with the observed shrinkage and more northerly position of the TZCF during the 1998–2002 SeaWiFS years, which comprises at least three La Niña events [Radenac et al., 2012]. This effect of the El Niño/La Niña on the TZCF, and, in turn, on the phytoplankton phenology of the subtropical North Pacific, is confirmed by the separate analysis of the El Niño and La Niña years on the 1998–2010 data set (Figure 7).
Figure 7. Cluster-derived maps of phenological regimes for (a) La Niña and (b) for El Niño years over the 1998–2010 SeaWiFS time period.
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 The TZCF position is correlated with the strength of the Aleutian Low [Bograd et al., 2004; Peterson and Schwing, 2003], which is in turn related to the Pacific Decadal Oscillation [Mantua and Hare, 2002; Mantua et al., 1997]. The PDO index is widely used to characterize North Pacific atmosphere–ocean–ecosystem variability. Twentieth-century events typically lasted 20 to 30 years [Mantua and Hare, 2002; Mantua et al., 1997] and appear to be driven in equals parts, at decadal scale, by the variability of the Aleutian Low, the ENSO and the zonal advection anomalies of the Kuroshio-Oyashio extension [Schneider and Cornuelle, 2005]. In 1977, the PDO experienced a major polarity shift and entered a positive (“warm”) phase, typically characterized by anomalously warm SSTs along the coasts of North and South America, anomalously cool SSTs in the central North Pacific, enhanced North Pacific counterclockwise wind stress [Mantua and Hare, 2002], and a deepened mixed layer north of 25°N [Carton et al., 2008; Di Lorenzo et al., 2008]. Subsequent years (the CZCS years) saw a stronger Aleutian Low, a southward shift of westerly winds, and the aforementioned southerly TZCF excursion [Bograd et al., 2004; Peterson and Schwing, 2003]. Our detection of the Subtropical North regime (moderate seasonality) in the 20°N–30°N belt could well be an element induced by the PDO positive phase.
 During the 1998–2002 SeaWiFS period, the PDO index was negative, but atmospheric and SST patterns were different from classical cool-phase conditions [Bond et al., 2003]. There are some indications that the North Pacific Gyre Oscillation (NPGO)—i.e., changes in gyre circulation intensity—may better explain large-scale ecosystem variability of 1998–2002 years than does the PDO [Di Lorenzo et al., 2008]. The NPGO index, which was strongly positive during the 1998–2002 SeaWiFS years, has been promoted as a primary indicator of upwelling strength and associated biogeochemical change (e.g., nutrient fluxes and Chl concentrations) off the California coast [Di Lorenzo et al., 2008]. Large-scale effects on ecosystems of the open Pacific basin remain somewhat speculative, and the role of the NPGO in forcing the phenological changes we observed is at present unclear. We can hypothesize that if present suspicions are confirmed (i.e., if the NPGO does turn out to be a strong indicator of large-scale variability), then it may, through its influence on Aleutian Low and TZCF variability, ultimately be found to drive the phenology of the subtropical North Pacific's surface chlorophyll.
 Overall, considering the main features of Transition Bloom regime (i.e., longer and flatter ‘growth’ season, reduced difference between minima and maxima, highstandard deviation), we interpret the widespread emergence of Transitional Bloom during the l998–2002 period (Figures 2b, 3, 4, and 5) as the weakening of a strong latitudinal seasonality gradient observed during the 1979–1983 years. The Transitional Bloom, which replaces geographically the Bloom and Subtropical bioregions, reflects then a much higher zonal variability in the phenological regimes of the Northern Hemisphere. Phytoplankton in affected areas lost synchrony and fragmented the pronounced seasonality characterizing the previous period. This regime shift would be consistent with an overall decrease in the upward flux of nutrients due to stronger upper-ocean stratification (i.e., shallower MLDs;Figure 6a), likely coupled with a larger spatial and interannual variability in the dynamics of the mixed layer. It would also be consistent with changes in other processes, such as a stronger coupling between producers and grazers (more akin to a classical Tropical regime), but data are not available to assess the relative contributions of the many potential contributing factors, particularly those that involve trophic interactions. If we confine our attention to first-order bottom-up controls on phytoplankton phenology, we can say that the appearance of the Transitional Bloom regime during the 1998–2002 period indicates a general smoothing of the normalized-chlorophyll seasonality in the Northern Hemisphere if averaged at large scales, due in large part to a change mixed layer dynamics [Carton et al., 2008] and a consequent increase of variability in the phase of the seasonal cycle. This mechanism to explain the appearance of Transitional Bloom is partially confirmed by our analysis of the El Niño/La Niña years. We observe Transitional Bloom only during La Niña years. During these years, the variability of atmospheric forcing in the Northern Hemisphere increases respect to the mean state [i.e., Li and Lau, 2012], likely inducing the modifications of the mixed layer dynamic, which are supposed to determine the appearance of the Transitional Bloom. It is worth noting, however, that the Radenac et al.  classification we used to group La Niña/El Niño years is different from others [i.e., McPhaden et al., 2011], which makes the explanation of the link La Niña-Transitional Bloom very preliminary and worthy for further analysis.
4.2.2. Disappearance of the Transitional Tropical Regime
 During the 1979–1983 years, the Transitional Tropical regime occupied most of the tropical ocean belt (Figure 2). By the 1998–2002 years, though, this regime had been replaced by others (Table 2). In the Indian Ocean along the east coast of central Africa, Transitional Tropical shifted to Subtropical South (purple pixels in Figure 5), and in the western equatorial Atlantic and the eastern tropical and subtropical Pacific, it shifted to Tropical (Table 2; pink pixels in Figure 5). In other words, conditions had apparently become generally less tropical (i.e., with heightened seasonality) in the Indian Ocean and generally more tropical (more muted seasonality) in the western equatorial Atlantic and eastern and subtropical Pacific.
 In the Indian Ocean, monsoonal dynamics typically induce a first bloom in summer and a secondary weaker bloom in late fall–winter, with little interannual variability [Marra and Barber, 2005; Yoder et al., 1993]. This pattern of a strong summertime bloom is more similar to our Subtropical South regime (observed during the 1998–2002 SeaWiFS years; Figure 2b) than to Transitional Tropical (obtained during the 1979–1983 CZCS period; Figure 2a), which exhibits no summertime bloom. This apparent shift from winter bloom (during 1979–1983) to summer bloom (in the 1998–2002) could perhaps be ascribed to a change in the relative intensity of the summer and fall monsoons which in turn might imply interannual variability of the physical forcing [Longhurst, 1998; Marra and Barber, 2005]. However, SODA-derived mixed layer characteristics (i.e., the magnitude and timing of annual maximum depths) during the two periods are relatively constant (Figure 6), which would seem to exclude significant impacts from changes in mixed layer dynamics. An alternative explanation of the anomalous winter-bloom cluster obtained for the 1979–1983 CZCS period might be artifactual bias due to extensive summertime cloud cover [Banse and McClain, 1986; Brock and McClain, 1992; Brock et al., 1992]. We are unable to attribute the apparent shift in the Indian Ocean to either real phenological change or coverage-related artifact.
 Similarly, in the western equatorial Atlantic the 1979–1983 CZCS Transitional Tropical regime could be considered atypical or perhaps even artifactual. In this region, summertime chlorophyll increase is driven by seasonal intensification of the trade winds [Grodsky et al., 2008; Li and Philander, 1997; Monger et al., 1997] and is modulated by high precipitation and river runoff in the westernmost area [Dessier and Donguy, 1994]. Our observed Tropical patterns of the 1998–2002 SeaWiFS years agree with this scenario [e.g., Pérez et al., 2005]. The Transitional Tropical regime observed in the period 1979–1983, on the other hand, with its larger wintertime biomass (normalized chlorophyll) accumulation (Figure 1e), would be considered unusual for this region. The signal observed in the 1979–1983 CZCS observations was ascribed by Deuser et al.  to river runoff; such runoff could potentially confound the cluster analysis of the reprocessed CZCS signal.
 The third region where we observed disappearance of the Transitional Tropical regime is in the Eastern Tropical Pacific (between 10°N and 10°S and between 90°W and 120°W). Here, the Tropical regime had become prominent during 1998–2002 (Figure 5, pink pixels). Phytoplankton seasonality in this region is characterized by a winter maximum driven primarily by nutrients advected in from the Equatorial upwelling region and the Peru current by the South Equatorial Current and from the equatorial front and the 10°N thermocline ridge by the North Equatorial Counter Current [Pennington et al., 2006]. Overall, the region is strongly influenced by large-scale El Niño and La Niña interannual variability, the strength of which is tracked by the Multivariate ENSO Index (MEI) [Wolter and Timlin, 2011]. Typical event duration is 6–18 months [Wang and Fiedler, 2006]. During El Niño years (MEI positive), a deeper pycnocline in the eastern equatorial Pacific results in a diminished supply of nutrients to surface waters [Pennington et al., 2006]. A general smoothing of the winter phytoplankton maximum has been observed during these positive phases [Feldman et al., 1984; Strutton et al., 2008]. For La Niña years (MEI negative), the sources of variability in phytoplankton seasonality are less well understood. Recent findings [Behrenfeld et al., 2001] indicate that during La Niña years biomass generally increases across the whole equatorial Pacific, though this effect seems less pronounced in the east [Strutton et al., 2008]. It is noteworthy, moreover, that the statistically relevance of the Tropical regime for the 1998–2002 period is low. The observed shift between the Transitional Tropical to Tropical in the Eastern Tropical Pacific could be then an artifact of the clustering method.
4.2.3. Other Regime Shifts and Transitions
 Other changes of more limited spatial extent were also detected in the phenological patterns between the 1979–1983 and the 1998–2002 years. The western tropical North Atlantic shifted from Bloom to Subtropical North (red pixels in Figure 5), consistent with a general shoaling of MLD maxima as previously discussed. The transitions from Tropical or Subtropical North to Bloom (brown pixels in Figure 5) on the western side of the Pacific equatorial belt is likely driven by the two strong La Niña events that occurred near the turn of the century. The 1998–1999 event is documented to have increased seasonality of surface chlorophyll in the region [Radenac et al., 2012], which would be consistent with our observed emergence of the Bloom regime.
 In the 1998–2002 period, clusters typical of the Northern Hemisphere were assigned to a few areas of the Southern Hemisphere poleward of 40°S (e.g., the Tasman Sea and the southern edge of the Algulhas Current; gold pixels in Figure 5). These cycles exhibit a 6-month lag with the seasonal cycle of irradiance–i.e., the normalized-chlorophyll peak is offset from the maximum irradiance by half a year. In these areas, intense mesoscale activity is often observed [Tilburg et al., 2002; Weeks and Shillington, 1994]. Such processes may decouple phytoplankton growth events from the annual illumination cycle.
 The transitional clusters (i.e., Transitional Tropical and Transitional Bloom regimes) represent important phenological states of oceanic phytoplankton. The notion that these clusters represent change from one regime to another is evident when mean seasonal cycles of the 1998–2002 period are calculated for pixels that during the years 1979–1983 were identified as Transitional Tropical (Figure 1e). The resulting cycle (Figure 1g) is clearly different from its predecessor. It appears more similar to the Tropical cycle (Figure 1b), which is a reasonable result for the latitudinal belt in question (Figure 2a, blue pixels; Figure 5, pink pixels). When mean seasonal cycles for the years 1979–1983 are calculated on pixels identified in the 1998–2002 years as Transitional Bloom (Figure 1f), the resulting pattern (Figure 1h) appears very similar to its successor. This similarity (persistence) supports our hypothesis that the Transitional Bloom regime, more than representing an intermediate state between the Bloom and Subtropical North, arises from the coexistence of the two regimes in the same year and from the alternation over the years. The use of multiyear averages merged the two regimes in one unique cluster, which display then a higher variance than the others.
 Properly speaking, Transitional Bloom is not a new regime, but the superposition of two well-identified regimes, modulated by the interannual variability. However, its appearance/disappearance occurs during La Niña/El Niño years (Figure 7), and it strikes the similarity between the cluster spatial distribution for the 1979–1983 CZCS period (Figure 2a) and of the 1998–2010 SeaWiFS El Niño years (Figure 7b). Less evident, though still visible in particular in the Northwestern subtropical Pacific, is the correspondence between the 1998–2002 SeaWiFS period (Figure 1b) and the La Niña years (Figure 7a). Again, we interpret these patterns of the Transitional Bloom as an effect of the multiyear average, as during the CZCS period (1979–1983), a strong El Niño was detected, while during the 1982–2002 SeaWiFS years both El Niño and La Niña events are observed.
 Despite this, the expansion of the Transitional Bloom during 1998–2002 (which further intensifies if the whole 1998–2010 SeaWiFS period is considered) indicates that the change from 1979 to 1983 and 1998–2002 reflects a large scale change in the functioning of a part of the Northern Hemisphere, which could be related to the La Niña/El Niño effects. From a marked and geographically well defined seasonality, chlorophyll distribution changed to a much higher variability in time and space, which produces an overall smoothing of the seasonal patterns. Typical phytoplankton maxima of December–January in the Subtropical North and April–May in the Bloom regimes respectively flattens over a longer time interval (November–March), mostly reflecting a phase shift in space and time. In other words, the change in phenology does not occur coherently all over a given bioregion but with a patchy pattern.
 This change may have also been enhanced by the fact that spatial variability during CZCS might have been minimized by the averaging of a less frequent and spatially coarser coverage. Therefore, it is not possible to state if it reflects a long-term trend or just a variation at decadal scale. Certainly, it prompts for an in depth investigation on the possible link of the evident change in the seasonal cycle of phytoplankton chlorophyll with the functioning of the food web.