D'Ortenzio and Ribera d'Alcalà (2009, DR09 hereafter) divided the Mediterranean Sea into “bioregions” based on the climatological seasonality (phenology) of phytoplankton. Here we investigate the interannual variability of this bioregionalization. Using 16 years of available ocean color observations (i.e., SeaWiFS and MODIS), we analyzed the spatial distribution of the DR09 trophic regimes on an annual basis. Additionally, we identified new trophic regimes, exhibiting seasonal cycles of phytoplankton biomass different from the DR09 climatological description and named “Anomalous”. Overall, the classification of the Mediterranean phytoplankton phenology proposed by DR09 (i.e., “No Bloom”, “Intermittently”, “Bloom” and “Coastal”), is confirmed to be representative of most of the Mediterranean phytoplankton phenologies. The mean spatial distribution of these trophic regimes (i.e., bioregions) over the 16 years studied is also similar to the one proposed by DR09, although some annual variations were observed at regional scale. Discrepancies with the DR09 study were related to interannual variability in the sub-basin forcing: winter deep convection events, frontal instabilities, inflow of Atlantic or Black Sea Waters and river run-off. The large assortment of phytoplankton phenologies identified in the Mediterranean Sea is thus verified at the interannual scale, further supporting the “sentinel” role of this basin for detecting the impact of climate changes on the pelagic environment.
The Mediterranean Sea is one of the oceanic regions most impacted by climate change (Giorgi, 2006; Giorgi and Lionello, 2008). These important environmental modifications are supposed to strongly modify the dynamics of the Mediterranean marine ecosystems (The Mermex Group, 2011), by modifying the food web structure (Coll et al., 2008), triggering regime shifts (Conversi et al., 2010) or unexpected events (e.g., jellyfish blooms, Purcell, 2005), which should have strong consequences on human activities. In the context of climate change, phytoplankton plays a key role, because any perturbations on its dynamics would affect the rest of the marine food web (Edwards and Richarson, 2004). In a relatively small semi-enclosed sea, such as the Mediterranean, those kinds of processes should be particularly accelerated. A modification of the phytoplankton communities could impact the whole ecosystems much more rapidly than in other oceanic regions (Siokou-Frangou et al., 2010).
In the Mediterranean, as in many of the oceanic regions, the phytoplankton
dynamics are characterized by a strong spatio-temporal variability (Estrada,
1996; Mann and Lazier, 2006), determined by the concomitant influence of
several biotic and abiotic factors (Williams and Follows, 2003; Mann and
Lazier, 2006). The link between abiotic factors and phytoplankton
variability, in the Mediterranean Sea, has been mainly inferred by using
satellite ocean color data (Antoine et al., 1995; Bosc et al., 2004;
Mélin et al., 2011; Volpe et al., 2012). Based on band-ratio algorithms
that infer surface chlorophyll
However, despite the ecological relevance of phytoplankton seasonality (or
phenology), which provides a powerful tool to identify the factors affecting
ecosystem functioning (Edwards and Richarson, 2004), phenology has received
less consideration in the Mediterranean. Phytoplankton phenology was
generally hard to evaluate, as observations were either not available at the
required temporal and/or spatial resolution (see review of Ji et al., 2010),
or were restricted to coastal areas. Satellite observations provide
high-frequency temporal and spatial observations and represent the only
available data set to estimate the seasonal dynamics of phytoplankton at
basin-scale with a proper spatio-temporal resolution (Ji et al., 2010).
Using satellite observations, a first attempt to characterize the
Mediterranean phytoplankton phenology was recently proposed (D'Ortenzio and
Ribera d'Alcalà, 2009, DR09 thereafter). Although limited to the sea
surface, DR09 identified in the available SeaWiFS ocean color data set, seven
recurrent patterns in seasonal cycles of phytoplankton in the Mediterranean.
The observed seasonal patterns (referred by DR09 as “trophic regimes”)
were then regrouped in four main classes on the basis of their shape
characteristics: a “temperate seas-like” dynamic (referred by DR09 as
“Bloom”, characterized by a spring peak), a “tropical seas-like” dynamic
(referred by DR09 as “No bloom”, to indicate the absence of a marked
peak), an “intermittently” dynamic (considered as an intermediate regime
between “Bloom” and “No Bloom” trophic regimes, and interpreted as an
artifactual regime produced by averaging) and a “Coastal” dynamic
(frequently observed in coastal regions, see later). Moreover, the
geographical distribution of the DR09 trophic regimes followed well-defined
spatial patterns, and was thus interpreted as a bioregionalization of the
basin based on the phenological traits of the surface chlorophyll
The DR09 results have already been used to investigate the role of the mixed layer depth (MLD) and the nitrate distribution on the Mediterranean phytoplankton phenology (Lavigne et al., 2013), while modeling studies have used the DR09 bioregionalization based on the seasonal dynamics of phytoplankton to ameliorate the primary production estimates from space (Uitz et al., 2012). Combining temporal (i.e., the trophic regimes) and spatial (i.e., the bioregions) analysis, the DR09 results thus provided a robust framework to identify the role of abiotic and biotic factors on the Mediterranean phytoplankton phenology.
Two main issues are, however, still unresolved. Firstly, the DR09 results
were obtained under a strict climatological approach, providing the most
relevant spatio-temporal patterns, though smoothing any interannual
variability. Secondly, and as a consequence of the climatogical scale, the
DR09 trophic regimes and bioregions could be an artifactual result of the
climatological average, which, by flattening the seasonal cycle of surface
chlorophyll
In this paper, we reappraised the DR09 approach with the specific aim to
account for the interannual variability of the Mediterranean surface
chlorophyll
Schematic representation of the different steps of the method used in this study (see Sect. 2.2 for details).
Surface chlorophyll
The method proposed here initially uses the trophic regimes identified by DR09 to classify pixels on an annual basis. The method consists in identifying, for each “annual” time series of each pixel, the DR09 trophic regime with the most similar time series. After this first classification, a number of time series remain unclassified (i.e., “non assigned”). These “non assigned” time series are then clustered to identify new trophic regimes, which were somehow hidden in the DR09 approach.
In practice (see Fig. 1):
For each year and for each Mediterranean pixel, the “annual” time series
of The similarity between the “annual” time series and each of DR09 trophic
regimes is evaluated using the Chebyshev distance (e.g., Han et al., 2011),
with only the 8-day averages of To be definitively assigned to the selected DR09 trophic regime, the
“annual” time series must be contained in the confidence interval of that
DR09 trophic regime. The confidence interval is defined as the mean
Chebyshev distance between the DR09 trophic regime and all the weekly
climatological time series of If the “annual” time series falls within the confidence interval, then the
“annual” time series and its pixel are assigned to the DR09 trophic regime
initially selected (Fig. 1, step 4). Otherwise, the “annual” time
series (and its associated pixel) is temporarily added to a table with all
“non-assigned” time series. At this stage, 16 annual maps (not shown) were
obtained, indicating if the times series of each pixel were still “non
assigned”, or otherwise the membership of the pixels as one of the DR09
trophic regimes. All of the “non-assigned” time series (from all the 16 years combined)
were clustered by using a K-means clustering (Hartigan and Wong, 1979; Fig. 1, step 5). The number of clusters is decided using the
Calinski and Harabasz index (this index compared the within and between
cluster variance, Calinski and Harabasz, 1974; Milligan and Cooper, 1985).
Then, the stability of the resulting clusters was assessed by comparing them
(using the Jaccard coefficient) with clustering results obtained after a
modification (i.e., adding an artificial noise), or a subset of the data set
(Hennig, 2007, see also DR09). Only clusters with a Jaccard coefficient
greater than 0.75 are considered stable. These new clusters include all the
“annual” time series that are statistically different from the DR09
climatological time series. In some sense, they represent anomalies compared
to the DR09 climatological analysis and, for this reason, they are referred
in the following as “Anomalous” trophic regimes.
Four “Anomalous” trophic regimes are obtained, and all are stable (i.e.,
presenting Jaccard coefficients > 89 %). Overall, 77.2 % of
the “annual” time series is classified as one of the DR09 trophic
regimes, and 12.8 % as one of the “Anomalous” trophic regimes.
Index on the trophic regimes' mean time series (Fig. 2). Summer is
defined from June to August, and the date of the maximal and/or minimal
rate of change as the date of the highest and/or lowest first derivative of the
mean time series of
Mean time series of the seven DR09 trophic regimes (“No Bloom #1”, “No Bloom #2”, “No Bloom #3”, “Intermittently #4”, “Bloom #5”, “Coastal #6” and “Coastal #7”) and of the four “Anomalous” trophic regimes (“Anomalous” #1, #2, #3 and #4) obtained from our method. Standard deviations are indicated as black lines.
Maps of the spatial distribution of the trophic regimes (i.e.,
bioregions),
The method described in Sect. 2.2 provides 11 time series (i.e., the seven
DR09 trophic regimes and the four “Anomalous”) obtained by averaging all
the “annual” time series of
The main traits of the trophic regime time series is sketched in the next paragraphs (for the seven DR09 and the four “Anomalous”), whereas their associated geographical distributions is analyzed afterwards.
The
The “Coastal” DR09 trophic regimes show different seasonal characteristics
from the rest of the DR09 trophic regimes (Table 1). The maximum
value of the “Coastal #6” time series is lower (0.72
All of the “Anomalous” trophic regimes (#1, #2, #3 and #4)
show minimum values of
All the above suggests that the “Anomalous” trophic regimes could be
considered as modified versions of the DR09 trophic regimes. The “Bloom
#5” and the “Anomalous #1” trophic regimes have a similar shape,
showing both a spring peak (for both the date of the maximal value in
April). Although they differ slightly for the dates of the maximal and
minimal rate of change (early March and late April for “Bloom #5”, and
late March and mid-April for the “Anomalous #1”), the “Anomalous
#1” trophic regime appears as a more peaked version of the “Bloom
#5” trophic regime, with a higher amplitude in [Chl]
Similarly, the “No Bloom #2” and the “Anomalous #2” trophic
regimes could be associated. They both display weak amplitudes of
Finally, the “No Bloom #3” and the “Anomalous #3” and “#4”
trophic regimes have similar shapes and spatial repartition (see the next
section). However, the “Anomalous #3” trophic regime displays
differences in the timing of the maximal rate of change and of the maximal
value (in November and December for the “Anomalous #3”, and in December
and February for the “No Bloom #3”), and the “Anomalous #4”
trophic regime presents a higher maximal value of [Chl]
The association of the “Anomalous” trophic regimes with the DR09 trophic regimes confirms the general partitions proposed by DR09 into “Bloom” and “No Bloom” trophic regimes. The low occurrence of the “Anomalous” trophic regimes indicates also that their importance in the basin behavior is low. They possibly signify an accentuation or a diminishing of the factors influencing the phytoplankton phenology, although they should be likely considered as temporary perturbations of the general “Bloom”/”No Bloom” regimes. We will discuss this later.
The 16 annual maps, showing the spatial distribution of the 11 trophic regimes (Fig. 3), represent a first attempt to evaluate the interannual spatial variability of the bioregions (defined, in the sense of DR09, as regions having similar phytoplankton phenology or, more precisely, having the same trophic regime). In the next, the results are presented following the four main DR09 groups of trophic regimes (i.e., “No Bloom”, “Bloom”, “Intermittently” and “Coastal”). The “Anomalous” trophic regimes are discussed separately. The last paragraph will be dedicated to a wider analysis on the interannual spatio-temporal variability of the bioregions.
Over the studied 16 years, “No Bloom” bioregions cover most of the Mediterranean Sea (67.2 % on average, Fig. 4). The “No Bloom #1” is the most occurring “No Bloom” bioregion (Fig. 4). Exceptions are observed in 1999, 2001, 2004, 2012 (dominance of the “No Bloom #3”) and in 2000, 2007 (dominance of the “No Bloom #2”). The “No Bloom #1” bioregion is permanently observed in the Levantine basin, and often in the Ionian Sea (Fig. 3). Episodically, it is also observed in the western basin, in particular over the Tyrrhenian Sea. During the 1999 to 2007 period, the “No Bloom #1” bioregion on average covered 25.6 % of the Mediterranean Sea, while from 2008 to 2014, its mean percentage increases to 33.5 %.
The second most occurring bioregion is the “No Bloom #3”, with a mean value of 21.5 % of covered surface over the 16 years (Fig. 4). It is associated with the Algerian basin (except in 2013 and 2014), although its northern and eastern boundaries are more variable (Fig. 3). It is also observed in the Northwestern Mediterranean (NWM), in the Tyrrhenian, and sometimes in a large portion of the eastern basin (i.e., 2004 and 2012). No clear trends are observed over its interannual evolution, except in 1999, 2001, 2004 and 2012, when it was the most widespread bioregion.
Finally, the “No Bloom #2” bioregion covers 16.7 % of the Mediterranean Sea on average (Fig. 4), and it is permanently observed in the Aegean and Adriatic Seas (Fig. 3). Peaks of occurrence are observed in 2000 and 2007, when its distribution extended over the North Ionian (in 2000) and most of the eastern Basin (in 2007). Similarly to the “No Bloom #1” bioregion, two periods could be identified in its interannual trend. Before 2008, the occurrence of the “No Bloom #2” bioregion is erratic, ranging from 11.5 to 31.7 %. After 2008, the surface cover is low (i.e., 10.4 % on average) and constant.
The “Bloom #5” bioregion covers 4 % of the Mediterranean Sea on average (Fig. 4), and it is observed quite exclusively in the NWM (Fig. 3). Notable exceptions are the years 1999 and 2006, when it is observed in the Southern Adriatic, and in 2003, in the Rhodes gyre area. The interannual variability of its extent (Fig. 4) ranges from very low values (i.e., in 2001, 2007 and 2014) up to 9 % of the total Mediterranean surface (i.e., in 2005, which is, however, a special year due to a high number of missing values). When the “Bloom #5” bioregion is weakly observed, it is generally replaced either by “Intermittently #4” (i.e., as in 2001 or in the 2007) or by the “Anomalous #1” bioregion (Fig. 3). In the first case, the “Intermittently #4” bioregion extends all over the NWM with an almost total disappearance of the “Bloom #5” bioregion. In the second case, the “Bloom #5” bioregion is still present, but located in the border area of the NWM. Instead, the central area is occupied by the “Anomalous #1” bioregion (especially in 2005, 2006, 2008, 2010, 2013 and 2014).
On average, the “Intermittently #4” bioregion occupies 12.2 % of the Mediterranean Sea (Fig. 4). However, this percentage shows strong interannual variations, ranging from 7.2 to almost 24.5 % of the total surface. It is permanently observed in the NWM, in the frontal area south of the large cyclonic gyre of the Ligurian Sea (Fig. 3). Its interannual variability is expressed by the high values of occurrence in 2003, 2006, 2007 and 2013, for the most part in the western basin. In the eastern basin, it is recurrently observed in the Rhodes Gyres (2000, 2003, 2005, 2006, 2007, 2008, 2009 and 2012), in the North Ionian (1999, 2000, 2006, 2008 and 2012) and in the Southern Adriatic (1999, 2002, 2007, 2008, 2012 and 2014).
The “Coastal” bioregions cover 3.5 % of the Mediterranean Sea on average
(Fig. 4), with a weak interannual variability (
The “Coastal #7” bioregion, being rarely present, (less than 0.25 % of the Mediterranean Sea), will be neglected in the rest of the present study.
The “Anomalous” bioregions occupy 12.8 % of the surface basin on average (Fig. 4), although they are primarily concentrated in coastal zones: the “Anomalous #2” bioregion along the Adriatic and Aegean coasts, the “Anomalous #3” bioregion along the southeastern basin coasts and the “Anomalous #4” bioregion along the Algerian coast (Fig. 3). Apart from coastal zones, the “Anomalous #1” bioregion is episodically observed in the NWM, where it occupies a region usually classified as “Bloom #5” (see Sect. 3.3.2).
Although interannual variability in the geographical distribution of the bioregions is high, some general patterns emerge. To demonstrate this, a dominance map was calculated by evaluating, for each pixel, the most recurrent bioregion (i.e., the dominant regime), over the 16-year period (Fig. 5a). Most of the Mediterranean basin is assigned to one of the DR09 bioregions (96 % of the map) and only 4 % to an “Anomalous” bioregion. A second map showing the degree of membership (defined as the percent of years in which each pixel belongs to its most recurrent bioregion, Fig. 5b) was generated. The mean degree of membership over the whole Mediterranean area is 46 % (Fig. 5b), quantifying the large interannual variability of the basin. Spatial differences are, however, visible: coastal zones are generally characterized by a low degree of memberships, while open-ocean regions display higher values, showing less interannual variability.
To better highlight these geographical patterns, only areas with a degree of membership greater than 50 % were plotted (Fig. 5c). The colored areas in Fig. 5c indicate where the bioregions are the most temporally recurrent, reflecting then the regions characterized by a weak interannual variability in the phenological traits. All the coastal areas (except in the Gulf of Gabes), as well as the regions at the frontier between bioregions, disappear. Most of the “Intermittently #4” bioregion also disappear (maintained only in a limited region of the NWM), as well as all the “Anomalous” bioregions (except the “Anomalous #1” bioregion in the NWM) and most of the region of the Alboran Sea.
Similarly, a dominance map generated by considering the four “Anomalous” bioregions only (Fig. 6a), shows their patchy distribution and irregular occurrences. However, some spatial patterns exist, and are highlighted when only the pixels having at least two occurrences of the same “Anomalous” bioregion over the 16-year period were shown (Fig. 6b). The Anomalous #2, #3 and #4 bioregions are recurrently observed, but only along coasts. As always highlighted, the only open-ocean region exhibiting a coherent and recurrent “Anomalous” pattern is the NWM (classified as “Anomalous #1”).
The new method proposed here is intrinsically different from the one of DR09, although it similarly provides trophic regimes and their spatial distributions (interpreted here as bioregions). A comparison between the two approaches is therefore required before discussing the results.
To do so, we verified that the algorithms used in the new method provide the
same results as the DR09 methodology (i.e., generation of a weekly
climatological database and then application of a K-means clustering) when
the results are presented in a climatological point of view (i.e., on average
over the 16 years). Then, all the “annual” time series of
Furthermore, the spatial distribution of trophic regimes obtained with the DR09 methodology (Fig. 8) applied on the new 16-year database, is close to the dominance map of Fig. 5a (74 % of similarity, defined as the percentage of pixels in Fig. 5a belonging to the same DR09 trophic regime in Fig. 8). However, some differences with the DR09 10-year map (see Fig. 4 of DR09) exist, mainly the disappearance of the “Intermittently #4” bioregion in the North Ionian. The differences observed when using the new method could be ascribed more to the natural interannual variability, rather than to biases introduced through the novel methodology. Note also that the observed differences with the DR09 10-year map could additionally be ascribed to the 7-year extension of the database. In conclusion, the new method proposed here broadly supports the results of DR09 obtained at the climatological timescale, but there are some key differences generated by the larger extension of the database, or by the intrinsic natural interannual variability of the Mediterranean. We will address this last point in the next section.
Fig. 5c clearly indicates that the interannual variability is mostly part concentrated at the boundaries between bioregions. In addition, the four “Anomalous” trophic regimes, although statistically significant (i.e., Jaccard coefficient > 89 %), have recurrent patterns in open-ocean only in the NWM (Fig. 6b). In the rest of the basin, they appear more as episodic fluctuations or noise than as real patterns. Although not surprising given the approach used (i.e., first finding occurrence of the DR09 trophic regimes and only second searching for anomalies), this point is not trivial. From the methodological point of view, the capability of the method to detect four anomalies demonstrates its potential application in long-term studies. However, at a more in-depth analysis and in view of an oceanographic interpretation, these anomalies are not particularly relevant, as occurring only episodically and rarely indicating coherent, recurring patterns. Thus, the main climatological bioregions identified by DR09 (i.e., “No Bloom”, “Bloom”, “Intermittently” and “Coastal”) are sufficiently comprehensive to summarize the surface phytoplankton phenology in the Mediterranean Sea, even at interannual level. A notable exception in this global picture is the NWM area, with the recurrent occurrence of the “Anomalous #1” trophic regime.
Mean time series of the DR09 trophic regimes (in color) and their standard deviations (vertical bars) obtained from our analysis. The standard deviations from the DR09 methodology (in shade area) are obtained by applying the DR09 methodology (i.e., a K-means) on a weekly climatology done with the 16-year database.
Finally, it is important to note that, as suggested by DR09, each bioregion
(even the “Anomalous” bioregions) is directly related to a specific range
of [Chl]
The unimodal pattern of “No Bloom” regimes, with a higher biomass in
fall-winter and lower biomass in spring–summer, were explained in DR09 by a
combined mechanism involving both the vertical redistribution of biomass in
fall–winter (i.e., at the deepening of MLD) and the seasonality in the ratio
consumers vs. primary producers. More recently, Lavigne et al. (2013)
demonstrated the absence of light limitation in the “No Bloom” areas,
confirming that the winter increase of [Chl]
Spatial distribution of the climatological trophic regimes obtained from the DR09 methodology (i.e., a K-means) applied on a weekly climatology calculated from the 16-year database.
Among the three “No Bloom” trophic regimes, however, and considering their geographical distribution, the “No Bloom #3” bioregion was interpreted by DR09 as driven by the Atlantic Water inflow from Gibraltar. The interannual variability of the Gibraltar water inflow was recently assessed (Boutov et al., 2014; Fenoglio-Marc et al., 2013), by combining in situ observations, modeling experiments and atmospheric estimations. Inflow at Gibraltar over the 1999–2008 period was maximum in 2001 and minimum in 2002, 2005 and 2007, whereas it was constant around its mean value during the other years (Boutov et al., 2014). The occurrence of the “No Bloom #3” bioregion, calculated exclusively over the Western Mediterranean (as in Fig. 4, not shown), follows a similar behavior, with an absolute maximum in 2001 and two relative minima in 2002 and 2007 (the lack of data prevents an evaluation of the “No Bloom #3” bioregion occurrence in 2005). The interannual occurrence of the “No Bloom #3” bioregion appears related to the Gibraltar water inflow. Although speculative, this correlation seems to confirm the predominant role of the Atlantic Water in shaping interannual variability of phytoplankton phenology in this region. Interestingly, the “Anomalous #4” trophic regime, already identified as a slightly modified version of the “No Bloom #3” trophic regime, is observed mainly in the Algerian Basin (see Fig. 6). It could indicate the presence and/or absence of episodic anticyclonic eddies (see Olita et al., 2011), generated by instabilities of the Algerian current (Millot et al., 1990), which could induce slight variations of the annual phenology by locally modifying the surface layers.
The geographical distribution of the other two “No Bloom” trophic regimes (#1 and #2) is rather stable, with a predominance of the #2 in the Adriatic, Aegean and North Ionian and of the #1 in the Tyrrhenian, Levantine and Southern Ionian (Fig. 5a). However, in the Western Adriatic and in the Northern Aegean seas, which are linked to the “No Bloom #2” bioregion, an important interannual variability is observed (Fig. 5c). In the Adriatic, the organic and inorganic matter run-off generated by rivers in the Italian and Balkan peninsulas is characterized by important interannual variability, which is generally related to the timing and the intensity of the run-off. This interannual variability, which controls the injection of river nutrients into oceanic surface waters (Revelante and Gilmartin, 1976; Aubry et al., 2012), could induce the phenological changes observed in the North Adriatic. In the North Aegean Sea, the influence of the rivers and of the Black Sea Water on the phytoplankton productivity has been recently confirmed (Tsiaras et al., 2012, 2014; Petihakis et al., 2014). The load of nutrients in these areas by the river and/or the Black Sea Water in late spring (in May, Balkis, 2009) could also explain the occurrence of the “Anomalous #2” trophic regime, which presents a “plateau” in May, instead of the “No Bloom #2” trophic regime. At an interannual level, however, no trends or correlations have been identified.
The rest of the spatial modifications concerning both the “No Bloom #1” and the “No Bloom #2” bioregions are for the most part induced by the eastward extension of the “No Bloom #3” or by the appearance of the “Bloom #5” and/or “Intermittently #4” bioregions. The first case is likely related to the spreading of Atlantic Water, as already mentioned. The second case, discussed in the next section, could be ascribed to local sub-basin forcing, which enables favorable blooming conditions in specific years.
In the DR09 climatological classification, only one trophic regime exhibited a clear spring peak, and was therefore named “Bloom #5”. Located exclusively in the NWM, the most productive area in the Mediterranean Sea (Morel and André, 1991; Bosc et al., 2004), it was associated with the winter deep convection (MEDOC Group, 1970; Marshall and Schott, 1999; D'Ortenzio et al., 2005; Schott et al., 1997), which induces a large phytoplankton bloom through intense nutrient uptake (Marty et al., 2002). An important interannual variability on the intensity of the winter deep convection has been observed, for the most part related to the variability of atmospheric and hydrodynamic forcing (Mertens and Schott, 1998; L'Hévéder et al., 2013). In response to this oceanic and atmospheric variability, significant interannual differences in the biological response were also reported (Marty et al., 2002; Herrmann et al., 2013; Severin et al., 2014).
Our 16-year analysis confirms the recurrent presence of the “Bloom #5”
bioregion in the NWM area, although it also highlights the sporadic
occurrence of the “Anomalous #1” trophic regime, considered as a
modified version of the “Bloom #5” bioregion (more peaked than the
“Bloom #5” regime, see Sect. 3.2). The occurrence of the “Anomalous
#1” regime in the NWM temporally coincides with recorded events of
exceptionally deep winter convection in the area (years 2005, 2006, 2008,
2010 and 2013; Smith et al., 2008; Bernardello et al., 2012; Herrmann et
al., 2010; Houpert et al., 2014). Such temporal coincidence suggests that
deep convection events could impact the phytoplankton phenology of the
region, by inducing a stronger phytoplankton bloom (i.e., a higher amplitude,
0.82 mg m
On the other hand, the recurrent occurrence of the “Bloom #5” regime in
the NWM area suggests that important phytoplankton growth occurs also when
deep convection is relatively weak (as in 2001 and 2007, Houpert et al.,
2014). However recent results from profiling floats measuring the [Chl] and
the particle mass concentration, suggest also that in this region the
photoacclimatation process could contribute to the change in the
[Chl]
Unlike DR09, the “Bloom #5” regime is also observed in the Southern Adriatic, in the Rhodes Gyres area and in the central Tyrrhenian. In the DR09 climatological analysis, these regions were all classified as “Intermittently #4”, and they are discussed in the next section.
The “Intermittently” trophic regime was explained by DR09 as an effect of the interannual alternation of the “Bloom” and “No Bloom” conditions. Therefore, the resulting regime should be an artifact of the climatological approach of DR09. More recently, the interannual switch between the “Bloom” and “No Bloom” regimes over the “Intermittently #4” area was partially confirmed using in situ estimations of the MLD, although the number of observations was too scarce to draw any conclusions at the basin scale (Lavigne et al., 2013). Here, the interannual analysis over the 16-year period indicates that, among the regions classed as “Intermittently #4” by DR09, the Balearic front is permanently classified as “Intermittently #4” (Fig. 5c), while the Rhodes Gyre and the Adriatic and North Ionian seas switch between “Bloom”, “No Bloom” and “Intermittently” bioregions. In other words, the DR09 “Intermittently #4” regime is confirmed to be strongly impacted by the interannual variability. However, its permanent occurrence in the Balearic Sea and its sporadic presence in the rest of the basin suggest that it could be considered a “true” regime more than an artifact of the average. The “Intermittently #4” trophic regime should be considered truly an intermediate regime between “No Bloom” and “Bloom” trophic regimes. Thus the name “Intermittently #4” will be replaced by “Intermediate #4”.
Its occurrence in the Balearic area could be then ascribed to frontal instabilities that are generated all along the Balearic front (Lévy et al., 2008; Taylor and Ferrari, 2011) during the blooming period (Olita et al., 2014). These instabilities (i.e., eddies, gyres or filaments) could also modify the local distribution of surface phytoplankton, by exporting phytoplankton-rich waters in the oligotrophic waters south of the Balearic front and vice versa. The chaotic nature of these instabilities could explain the lack of clear trends in the “Intermediate #4” (before considered as “Intermittently #4”) spatial variability.
For the Southern Adriatic, similar to the NWM, the cyclonic circulation and the atmospheric conditions are generally evoked to explain the bloom onset, as the deep mixing recurrently observed in the area is supposed to inject enough nutrients to sustain phytoplankton growth (Gacic et al., 2002; Civitarese et al., 2010; Shabrang et al., 2016). The interannual variability of the deep mixing could then influence the variability observed in the annual bioregions maps (Fig. 3). Intense deep convection events were reported in 2005, 2006, and 2012 winters (Civitarese et al., 2010; Bensi et al., 2013) when the area is classed as “Bloom #5”. Less intense convection, reported for the winters 2000, 2008, 2009 and 2010 (Gacic et al., 2002; Bensi et al., 2013), seems to be associated with “Intermediate #4” or “No Bloom #5” regimes.
The alternating occurrence of “Bloom #5”, “Intermediate #4” and “No Bloom” regimes in the Rhodes Gyre region cannot be explained on the basis of existing data over the study period. The Rhodes Gyre is known to be the region of formation of the Levantine Intermediate Water (LIW), which is generated under specific atmospheric forcing conditions and in a permanent cyclonic structure (Wüstz, 1961). Phytoplankton blooms are sporadically observed from space (D'Ortenzio et al., 2003; Volpe et al., 2012), although the link between LIW formation events and phytoplankton enhancement was only hypothesized (Lavigne et al., 2013). The link between bioregions and dense water formation events is not clear in the Rhodes gyre region. The episodic occurrence of “Bloom”/“Intermediate” bioregions demonstrates the specificity of this area in the Levantine basin, and it demands further investigation.
The interannual variability of the Mediterranean Sea trophic regimes, retrieved from satellite ocean color data was presented here. Compared to DR09, a method was developed to account for the interannual variability in the spatial distribution of the DR09 trophic regimes (i.e., bioregions), and for the emergence of new trophic regimes (i.e., the “Anomalous”), which could have been hidden by the climatological approach of DR09. The satellite database was also enlarged to encompass here 16 complete years (from 1998 to 2014).
Firstly, the results from the new approach confirmed that over the studied
16 years, the DR09 bioregions (except the “Coastal #7”) were the most
recurrent (77.2 %), and that their mean spatial distribution was similar
to the one proposed by DR09 (i.e., dominance map, Fig. 5a). In fact, the new
interannual approach demonstrates that every year the patterns in the
phytoplankton phenology described by DR09 (except the “Coastal #7”
trophic regimes) were always recovered. Even the “Intermittently #4”
trophic regime, which was interpreted by DR09 as an artifactual regime
produced by their climatological averaging, was recovered, and thus
confirmed to be a real “Intermediate” trophic regime between the “No
Bloom” and “Bloom” trophic regimes. Therefore, the DR09 trophic regimes
are argued to be representative of most of the observed seasonality in the
[Chl]
Secondly, important regional interannual variabilities in bioregions' spatial distribution, and in the emergence of “Anomalous” trophic regimes, were also highlighted and related to environmental factors. Actually, the interannual extension of the “No Bloom #3” bioregion over the Algerian Basin was related to the inflow of Atlantic Water at Gibraltar. Though less clear, a relation was also proposed between the load of nutrients, from river run-off and the Black Sea Water, and the spatial distribution of the “No Bloom #2” and an “Anomalous” bioregion with a weaker seasonal variability (i.e., the “Anomalous #2”). In contrast, a clear link between the dense water formation events in the Southern Adriatic and the occurrence of the “Bloom #5” bioregion was detected. In the NWM, a clear parallel between the dense water formations, from open-ocean deep convection events, and the occurrence of an “Anomalous” bioregion with a stronger phytoplankton spring bloom (i.e., the “Anomalous #1) has been identified. However, in the NWM, the permanent occurrence of the “Bloom #5” trophic regimes suggests that a sufficient replenishment of nutrients for allowing a phytoplankton spring bloom exists every year, even without a deep convection event. On the other hand, the permanent occurrence in the Balearic front of the “Intermediate #4” trophic regime (originally considered to be an artifactual regime) reveals that it is a real trophic regime, supposedly related to frontal instabilities. Finally, in the Eastern Mediterranean basin (i.e., in the Rhodes gyre), the alternating occurrence between the “Intermediate #4”, the “Bloom #5”, and the “No Bloom” regimes was detected but cannot be explained. This highlights the need for further information over the Mediterranean basin, in order to understand the underlying mechanisms of phytoplankton phenology, and to evaluate whether future climatic changes will promote the oligotrophic status (i.e., more occurrences of “No Bloom” bioregions).
All these results demonstrate that a bioregionalization based on the
analysis of phenological patterns, as the one proposed here, provides a
robust framework to identify the evolution of an oceanic area and to
summarize the huge quantity of information that the satellite data offer.
The limits of the approach are mainly related to the inherent errors of the
ocean color data: algorithmic errors, cloud coverage and their restriction
to surface layers of the ocean. These limitations are however partially
attenuated by the normalization applied to the time series of the
[Chl]
The Mediterranean Sea is thus confirmed to be a basin showing a large variety of phenological conditions in a very narrow latitudinal range. It could be then considered as a “sentinel” for rapidly detecting the climate change impacts on the marine biomes (as suggested by Siokou-Frangou et al., 2010), as it provides a place where intense and long-term monitoring, associated with the development of informative tools, are possible. The utilization of the invaluable data set of ocean color observations, combined with the proposed methodology, is a first step towards this direction. The future utilization of networks of biogeochemical dedicated autonomous platforms (as gliders and Bio-Argo floats), in strong combination with remote-sensing data and in the framework of bioregions (as suggested by Claustre et al., 2010 and by The Mermex Group, 2011), are likely to confirm the “sentinel” role of the Mediterranean Sea.
The authors would like to thank the NASA Ocean Biology Processing Group
(OBPG) for the access to SeaWiFS and MODIS data
(