JOURNAL OF GEOPHYSICAL RESEARCH: OCEANS, VOL. 118, 1–13, doi:10.1002/jgrc.

20167, 2013

A comparison of methods to determine phytoplankton bloom initiation

Sarah R. Brody,1 M. Susan Lozier,1 and John P. Dunne2
Received 10 January 2013; revised 14 March 2013; accepted 17 March 2013.

[1] Phytoplankton bloom phenology has important consequences for marine ecosystems
and fisheries. Recent studies have used remotely sensed ocean color data to calculate
metrics associated with the phenological cycle, such as the phytoplankton bloom
initiation date, on regional and global scales. These metrics are often linked to physical or
biological forcings. Most studies choose one of several common methods for calculating
bloom initiation, leading to questions about whether bloom initiation dates calculated
with different methods yield comparable results. Here we compare three methods for
finding the date of phytoplankton bloom initiation in the North Atlantic: a biomass-based
threshold method, a rate of change method, and a cumulative biomass-based threshold
method. We use these methods to examine whether the onset of positive
ocean-atmosphere heat fluxes coincides with subpolar bloom initiation. In several
coherent locations, we find differences in the patterns of bloom initiation created by each
method and differences in the synchrony between bloom initiation and positive heat
fluxes, which likely indicate various physical processes at play in the study region. We
also assess the effect of missing data on the chosen methods.
Citation: Brody, S. R., M. S. Lozier, and J. P. Dunne (2013), A comparison of methods to determine phytoplankton bloom
initiation, J. Geophys. Res. Oceans, 118, doi:10.1002/jgrc.20167.

1. Introduction identify the date of bloom initiation in a manner that can

[2] Ocean primary productivity plays a fundamental role
in controlling the structure and health of marine ecosystems.
Phytoplankton bloom phenology is of particular interest
because its coincidence with vulnerable phases of larval fish
[Platt et al., 2003] and zooplankton cycles [Koeller et al.,
2009] may affect survival rates of those species [Quetin
et al., 1996; Koeller et al., 2009]. A recent study has
suggested that climate change may affect the timing of
bloom initiation [Kahru et al., 2011], leading to a pos-
sible decrease in the synchrony between phytoplankton
blooms and upper trophic level life cycles [Edwards and
Richardson, 2004; Mackas et al., 2007]. Such a possibil-
ity emphasizes the importance of examining the drivers of
phytoplankton bloom initiation and their vulnerability to
interannual climate variability and change [Visser and Both,
2005].
[3] Remotely sensed ocean color data provide a valu-
able tool for examining phytoplankton bloom initiation at
the basin scale [Platt et al., 2009a]. However, before using
ocean color-derived chlorophyll a to investigate the con-
trols on phytoplankton bloom initiation, it is important to
1
Division of Earth and Ocean Sciences, Duke University, Durham,
North Carolina, USA.
2
Geophysical Fluid Dynamics Laboratory, Princeton, New Jersey,
USA.
Corresponding author: S. R. Brody, Division of Earth and Ocean
Sciences, Nicholas School of the Environment, Duke University, Box
90227, Durham, NC 27708, USA. (Sarah.Brody@duke.edu)
©2013. American Geophysical Union. All Rights Reserved.
2169-9275/13/10.1002/jgrc.20167
1
be efficiently and accurately applied to spatially extensive
ocean color data sets. Phenology studies currently use sev-
eral methods to estimate the timing of a phytoplankton
bloom. Ji et al. [2010] identify three broad categories of
methods. Threshold methods based on chlorophyll biomass
define bloom initiation as the time at which a chlorophyll a
time series [Siegel et al., 2002; Fleming and Kaitala, 2006;
Henson et al., 2006; Henson et al., 2009; Thomalla et al.,
2011; Racault et al., 2012; Cole et al., 2012] or a func-
tion or model fit to chlorophyll a data [Platt et al., 2009b;
Vargas et al., 2009; Wiltshire et al., 2008; Yamada and
Ishizaka., 2006; Zhai et al., 2011; Sasaoka et al., 2011;
Sapiano et al., 2012] crosses a set threshold. Threshold
methods based on cumulative chlorophyll biomass, which
have mainly been used to investigate zooplankton phenol-
ogy, identify a bloom as the time at which a cumulative
summation of chlorophyll biomass crosses a threshold per-
centile of the total biomass [Greve et al., 2005; Mackas
et al., 2012]. Rate of change methods estimate bloom initi-
ation from the point of most rapid increase on a chlorophyll
time series or function fit to that time series [Sharples et al.,
2006; Rolinski et al., 2007; White et al., 2009].
[4] In the marine environment, biomass-based thresh-
old methods have been most widely used in conjunction
with ocean color data to identify bloom initiation and other
phenological events in the marine environment at basin
and global scales. However, to date, we are aware of no
marine phenology studies critically comparing bloom initi-
ation dates derived from biomass-based threshold methods
with those derived from cumulative biomass-based thresh-
old methods or rate of change methods. Here we compare
 BRODY ET AL.: METHODS TO DETERMINE BLOOM INITIATION
patterns of bloom initiation dates observed from these three
methods, investigate the drivers of discrepancies, and sug-
gest questions in the field of phytoplankton phenology
research for which each method is best suited. We also exam-
ine how the method we use to fill gaps in the chlorophyll
data affects our conclusions.
[5] Additionally, we present an application to the study
of bloom initiation dates by examining a possible driver of
subpolar phytoplankton blooms, as has been done in many
of the previously cited studies [Siegel et al., 2002; Henson
et al., 2006, 2009; Thomalla et al., 2011; Sasaoka et al.,
2011; Kahru et al., 2011; Racault et al., 2012]. For light-
limited (subpolar) regions, the mechanics of phytoplank-
ton phenology are generally thought to be consistent with
the Sverdrup hypothesis [Sverdrup, 1953]. The Sverdrup
hypothesis states that during winter months, deep mixed
layers and low surface irradiance result in phytoplankton
consistently mixed to depths with too little light to sus-
tain growth. A spring bloom can initiate when the winter
mixed layer shoals above a critical depth, where integrated
photosynthesis is equal to integrated respiration.
[6] Recent studies have challenged the idea that season-
ally shoaling mixed layers create the necessary conditions
to promote phytoplankton growth, and have proposed other
mechanisms that may play a role in subpolar bloom ini-
tiation. For example, Taylor and Ferrari [2011] posit that
the cessation of turbulent convection in the upper mixed
layer, caused by a reversal in atmosphere-ocean heat fluxes
at the end of winter, may stabilize the upper mixed layer
and that this stabilization, rather than the seasonal shoal-
ing of the entire mixed layer, can initiate a phytoplankton
bloom. They provide support for this theory in the subpolar
North Atlantic by noting the synchrony between increases in
chlorophyll biomass and the onset of positive atmosphere-
ocean heat fluxes or net warming of the ocean surface.
However, Mahadevan et al. [2012] have challenged these
conclusions by noting that in their detailed study of the North
Atlantic Bloom Experiment, chlorophyll began increasing
while heat fluxes were still negative. Here we assess the rela-
tionship between heat fluxes and phytoplankton blooms by
comparing the time at which heat fluxes become positive
to the date of bloom initiation determined using the three
different methods.
2. Data and Methods
2.1. Study Site and Data
[7] We conduct our study of bloom phenology methods in
the North Atlantic over the spatial domain 30°N–65°N and
80°W–0°W. Chlorophyll in the North Atlantic has a complex
and variable temporal and spatial structure. Convention-
ally, productivity in this region is divided into subtropi-
cal (nutrient-limited) and subpolar (light-limited) regimes
[Follows and Dutkiewicz., 2001; Henson et al., 2006]. The
main bloom in subtropical areas occurs in fall or winter,
when deep mixed layers entrain nutrients into the euphotic
zone, whereas the main bloom in subpolar areas occurs
in spring and summer, by the mechanisms explained in
section 1. The transition zone between these two regimes
can experience blooms due to the lifting of light and/or
nutrient limitation [Henson et al., 2009]. Conditions at tran-
sition zone latitudes may also permit a second, smaller
2
bloom during the year [D’Ortenzio et al., 2012; Martinez
et al., 2006]. In this study, “primary” blooms denote the
high-magnitude blooms caused by the lifting of the major
limiting factor on phytoplankton growth, while “secondary”
blooms denote smaller blooms created by transient effects.
For instance, at some midlatitude locations, after a light-
driven primary bloom in the spring exhausts the surface
nutrient supply, a deepening mixed layer in the fall can pro-
vide a new source of nutrients, leading to a secondary bloom
[Cushing, 1959; Platt et al., 2009b; Sapiano et al., 2012].
[8] For all the methods in our study, we use level 3
SeaWiFS chlorophyll a concentrations for the years
1998–2007 (all full years of SeaWiFS data), obtained from
http://oceancolor.gsfc.nasa.gov/. We downloaded the 9 km,
8 day resolution SeaWiFS data, then spatially averaged the
original data to half-degree resolution. We chose 8 day data
to circumvent the large amount of missing data and noise
inherent in daily chlorophyll data yet still maintain suffi-
cient temporal resolution to make meaningful connections
between the timing of positive ocean-atmosphere heat fluxes
and bloom initiation. We dealt with missing data in the 8 day,
half-degree data set by first filling in the small and ubiq-
uitous data gaps due to cloud cover by averaging the four
nearest-neighbor points. We performed this spatial averag-
ing twice, so that the farthest distance from which a missing
pixel could draw information was 1°. We then filled remain-
ing data gaps, associated with high-latitude, winter low sun
angles, with the annual minimum chlorophyll value for each
pixel’s yearly time series.
[9] We examine the relationship between ocean-
atmosphere heat flux changes and bloom initiation using
daily net surface heat fluxes for the years 1998–2007,
obtained from NCEP/NCAR reanalysis 2 (http://www.esrl.
noaa.gov/psd/). The heat flux data was plotted on a T62
Gaussian grid, which we averaged to half-degree resolution,
then temporally averaged to 8 day resolution. We employed
the same method of filling small data gaps to the regridded
heat fluxes as in the chlorophyll data but did not fill in large
data gaps with the time series minimum.
2.2. Method 1: Rate of Change Method (ROC Method)
[10] We designed a rate of change method for find-
ing bloom start dates (BSDs). We based this method on
HANTS-FFT (Harmonic analysis of time series-fast Fourier
transform) method [Roerink et al., 2000], which performed
well in a terrestrial phenology study [White et al., 2009].
Our method first performs a discrete FFT on the 10 year
SeaWiFS data set to obtain a set of Fourier coefficients
at each location. The first 20 Fourier coefficients, corre-
sponding to the 20 largest sinusoidal periods, are used
to reconstruct the data set (Figure 1). The first frequency
has a period spanning the 10 year time series; the twen-
tieth frequency has a 6 month period. To find the yearly
blooms, we first identify all of the local maxima in the
reconstruction. We select the 10 largest maxima as the pri-
mary bloom peaks, then check to see if any of those 10
maxima occur less than 8 months apart. If so, one of the
10 largest maxima is a large secondary bloom, rather than
a primary bloom, and we substitute the next-largest local
maxima for the secondary bloom peak. After determin-
ing the 10 primary bloom peaks in the reconstruction, we
define the bloom start date for the yearly blooms as the dchl
dt
 BRODY ET AL.: METHODS TO DETERMINE BLOOM INITIATION

a.
0.3

chlorophyll (mg m−3)

0.25
0.2
0.15
0.1
0.05
0
Sept’98 ’99 ’00 ’01 ’02 ’03 ’04 ’05 ’06 ’07
chl 10 coef. reconstruction 20 coef. reconstruction 30 coef. reconstruction
10 coef. BSD 20 coef. BSD 30 coef. BSD 20 coef. max 21−25 coeff. BSDs

b.
0.3
chlorophyll (mg m−3)

0.25
0.2
0.15
0.1
0.05
0
Sept’03 Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug

Figure 1. Chlorophyll time series (36°N, 59°W) (a) for all 9 years and (b) for 2003–2004, showing the
chlorophyll data (blue line) and the reconstruction using 10 (red line), 20 (black line), and 30 (green line)
Fourier coefficients. Diamonds show BSDs calculated for each reconstruction; filled black circles show
the bloom peaks selected using the 20-coefficient reconstruction. At the bottom of Figure 1a, the BSDs
calculated using the 20-coefficient reconstruction (black diamonds) are shown on the x axis, and the BSDs
calculated using the 21–25 coefficient reconstruction (red, green, blue, magenta, and cyan crosses) are
shown above. Dashed lines denote year start dates.

maximum prior to the bloom peak (Figure 1a). Because the
ROC method determines BSDs based on the yearly chloro-
phyll maxima, results using this method have the advantage
of not being sensitive to the time series start date or the
season in which the primary bloom occurs.
[11] Using the first 20 Fourier coefficients, we produce
reconstructions of chlorophyll time series that display both
spring and fall blooms, accurately reproduce the timing
of the chlorophyll peak, and remove variability at sub-
seasonal and lower scales (Figure 1). We show an exam-
ple of the problems associated with using too few or too
many Fourier coefficients in the reconstruction by plot-
ting a chlorophyll time series from 36°N, 59°W, with the
reconstructions and associated BSDs using 10, 20, and 30
coefficients (Figure 1). This time series represents a sub-
tropical regime, in which deepening mixed layers in fall
(September–November) entrain nutrients from below the
mixed layer, creating a primary bloom that extends through
the winter [Follows and Dutkiewicz, 2001]. For most years,
the time series also shows a secondary chlorophyll peak
occurring near the end of the primary bloom, possibly due to
increased spring irradiance prior to mixed layer depth shoal-
ing and consequent nutrient depletion. The primary bloom
still begins in fall for these years, but the peak of the pri-
mary bloom occurs in spring. Reconstructions of the time
series that use fewer than 20 coefficients do not resolve the
secondary peak; therefore, the bloom peak falls in winter
rather than in spring. While Figure 1 shows the results of the
10-coefficient reconstruction, the same problems occur for
any reconstruction using fewer than 20 coefficients. Using
more than 20 coefficients has a less significant impact on
3
the reconstruction (i.e., BSDs calculated using 20 coeffi-
cients and BSDs calculated using 21–25 coefficients are very
similar), but as increasing numbers of coefficients are used,
the reconstruction will tend to over-emphasize secondary
blooms. For example, the reconstruction using 30 coeffi-
cients resolves the secondary spring bloom in this time series
to such a degree that it identifies the BSD as occurring imme-
diately prior to the secondary bloom (Figure 1). Thus, we
conduct the remainder of our investigation with an ROC
method that uses 20 Fourier coefficients to reconstruct the
chlorophyll time series.
2.3. Method 2: Threshold Method (TH)
[12] The threshold bloom initiation method was intro-
duced for marine phenology studies in Siegel et al. [2002].
This method finds the yearly or climatological median of a
chlorophyll time series, then identifies the bloom start date
as the first point at which chlorophyll levels rise a certain
percentage above the median. The BSDs identified by the
threshold method have been found to be relatively insensi-
tive to the percentage used [Siegel et al., 2002]. Here we
used a threshold of 5% above the median to be consis-
tent with previous threshold-based phenology studies [Siegel
et al., 2002; Henson et al., 2006, 2009; Thomalla et al.,
2011; Racault et al., 2012; Sapiano et al., 2012; Cole et al.,
2012]. The threshold is calculated after filling in the missing
data.
[13] The threshold method is often modified to mini-
mize the misidentification of secondary blooms as primary
blooms by shifting the chlorophyll time series to begin
close to an estimated bloom season, for example, by starting
 BRODY ET AL.: METHODS TO DETERMINE BLOOM INITIATION
0.8
chl time series
0.7 threshold
0.6
maximum point
points below
threshold
0.5 1 insensitive as possible to the time period in which the pri-
BSD
0.4
0.3
2
0.2
0.1
0
Sept Oct Nov Dec Jan Feb
Figure 2. Half year of chlorophyll data (42°N, 33°W,
1997) showing the threshold method, using a threshold of
5% above the yearly median chlorophyll. The straight line
denotes the threshold, the open circle shows the chloro-
phyll maximum or start point of the method, closed circles
show the points below the threshold used to determine the
BSD, and the diamond denotes the BSD. Arrows show
the direction in which the TH algorithm searches for the
below-threshold points (arrow 1) and BSD (arrow 2).
the time series in late summer for regions with fall pri-
mary blooms [Siegel et al., 2002; Henson et al., 2006, 2009;
Thomalla et al., 2011]. Our method, illustrated in Figure 2,
calculates the BSD based on the time series maximum, rather
than on an imposed time series start date. This calculation
is generally consistent with recent phenology studies [e.g.,
Racault et al., 2012; Cole et al., 2012]. Our method finds the
maximum point of the time series (open circle in Figure 2),
then works backward from the maximum (arrow 1) to find
where chlorophyll levels go below the threshold for two con-
secutive weeks (closed circles), in order to ensure that the
identified decrease in chlorophyll is robust over the season
rather than a transient effect of data noise. We subsequently
identify the BSD as one point closer to the maximum than
the below-threshold points (arrow 2, diamond).
[14] While some previous studies implementing the
threshold method with remotely sensed chlorophyll data
have first fit a function or model to the data for smoothing
purposes before identifying the BSD [Platt et al., 2009b;
Vargas et al., 2009; Wiltshire et al., 2008; Yamada and
Ishizaka., 2006; Zhai et al., 2011; Sasaoka et al., 2011;
Sapiano et al., 2012], we find that using chlorophyll data
that has already been temporally and spatially averaged and
requiring chlorophyll levels to stay below the threshold for
two consecutive weeks provides sufficient filtering of noisy
data. To confirm this, we calculated TH BSDs using the
Fourier reconstruction of the chlorophyll data described in
section 2.2 and found very little difference between the TH
BSDs calculated with reconstructed chlorophyll data and
original chlorophyll data.
2.4. Method 3: Cumulative Sum Method (CS Method)
[15] Our third method is based on a cumulative biomass
curve of the chlorophyll time series, created after screen-
ing out points in each yearly time series greater than three
4
standard deviations above the yearly median and replacing
these points with the quality-controlled time series max-
imum. The time at which this curve rises above a set
percentage of the total biomass is identified as the BSD. We
designed the CS method (illustrated in Figure 3) to be as
mary bloom occurs by identifying the minimum point of
each yearly time series (cross in Figure 3) then shifting the
time series to put the minimum at the beginning (dashed
line). The rationale for this shift is the expectation that the
lowest chlorophyll level generally occurs prior to the pri-
mary bloom and will create a cumulative biomass curve
(dotted line) that does not significantly increase until the
primary bloom begins.
[16] BSDs identified by the CS method are sensitive to the
threshold used to define them, in contrast to the TH method.
We determined that a threshold of 15% of the total biomass
(cross) best predicted the bloom initiation date for our study
area using two techniques. First, we visually inspected mul-
tiple chlorophyll time series over the entire study area with
BSDs determined using six thresholds (5–30%). From these
time series, we found that thresholds of 10–15% best pre-
dicted the bloom initiation date in subtropical regions, while
threshold of 15–20% best predicted the bloom initiation date
in subpolar regions. We then plotted, for the six thresholds,
the number of occurrences in which chlorophyll levels at
each threshold’s BSD exceeded chlorophyll levels prior to
the BSD but were not larger than the yearly chlorophyll
median plus one standard deviation. We found that the 15%
threshold had the largest number of points with increasing
chlorophyll levels at the BSD, which confirmed the results
of the visual inspection and led to the choice of the 15%
threshold.
Dec Jan Feb Mar Apr May Jun Jul Aug Sept Oct Nov
chl time series
1.2
minimum point
shifted time series
1
cumulative sum
chlorophyll (mg m−3)
threshold crossing
0.8
BSD
0.6
0.4
0.2
0
Sept Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug
Figure 3. Chlorophyll time series (21° W, 55° N, 2001)
showing the CS method. The thick line is the chlorophyll
time series, the cross is the minimum point of the time series,
the dashed line shows the shifted time series, the dotted line
shows the cumulative sum of the chlorophyll time series
(with the maximum value of the cumulative sum normalized
to the maximum value of the time series), the plus shows the
threshold (15% of the total biomass), and the diamond shows
the BSD. The bottom axis represents the original chlorophyll
time series; the top axis represents the shifted chlorophyll
time series and cumulative sum curve.
 BRODY ET AL.: METHODS TO DETERMINE BLOOM INITIATION

ROC TH CS
80°W 40°W 0° 80°W 40°W 0° 80°W 40°W 0°

a. 60°N b. 60°N c. 60°N

50° N 50° N 50° N

40° N 40° N 40° N

Sept Oct Nov Dec Jan Feb Mar Apr May Jun

TH minus ROC TH minus CS CS minus ROC

80°W 40°W 0° 80°W 40°W 0° 80°W 40°W 0°
6 5 60°N 6 5 60°N 6 5 60°N
d. 4 e. 4 f. 4
50° N 50° N 50° N
3 40° N
3 40° N
3 40° N
2 2 2
1 1 1

−20 −15 −10 −5 0 5 10 15 20

Figure 4. Bloom start dates calculated using (a) ROC, (b) TH, and (c) CS methods, and difference plots
of (d) TH minus ROC BSDs, (e) TH minus CS BSDs, and (f) CS minus ROC BSDs. All plots show the
average of the 10 year time series, with BSDs calculated using a time series start date of 1 September.
The scale of the bottom axis is in 8 day periods. Diamonds denote the locations of the time series in
Figures 6,9,11, and12.

3. Results 3.2. Comparison of Heat Flux Changes and BSDs

3.1. Comparison of Bloom Phenology Patterns
[17] We begin our comparison by noting the similarities
and differences in the patterns of bloom initiation dates
calculated using the three methods (Figures 4a–4c). All
methods show the same major pattern in BSDs: a sharp tran-
sition between subtropical latitudes, where blooms occur in
the fall and winter, and subpolar latitudes, where blooms
occur in the spring and summer, indicating that this feature
of North Atlantic bloom phenology is robust to the method
used to identify blooms. However, in several areas, bloom
phenology patterns differ between the methods, with dif-
ferences that can exceed 2 months. We have highlighted
these areas by plotting the difference between BSDs calcu-
lated using each method (Figures 4d–4f). First, ROC BSDs
show a band of early blooms centered at approximately
36°N–39°N, which TH and CS BSDs do not show. Sec-
ond, CS BSDs shift the transition between subtropical and
subpolar regimes northward, especially in the central and
eastern North Atlantic. Third, in the eastern North Atlantic,
between approximately 55°N and 60°N, the TH method
calculates late blooms relative to the rest of the subpolar
study area, while the ROC and CS methods show blooms
in this area occurring at the same time as, or slightly ear-
lier than, the rest of the subpolar North Atlantic. Finally,
all three methods show an area of earlier blooms west of
Greenland, but this feature is exaggerated in ROC blooms.
In sections 3.3–3.6, we will explore the reason for these
differences using time series located at the diamonds in
Figures 4d–4f.
5
[18] We expand upon the idea introduced in Taylor and
Ferrari [2011] by subtracting the 8 day period on which
heat fluxes become positive (the “zero-crossing” or ZC)
from the BSDs calculated using each method (Figure 5).
The difference plots are shown with a discretized colorbar
and a highlighted zero-contour to facilitate the comparison.
In the subtropics, blooms occur well before the heat flux
ZC, as expected, since phytoplankton growth in these areas
is not light-limited. The largest difference between BSDs
and ZCs in the subtropics occurs at the Gulf Stream, where
consistently warm sea surface temperatures delay the zero-
crossing. Over most of the subpolar region, ROC and CS
BSDs (Figures 5a and 5c) are approximately synchronous
with ZCs, occurring within four 8 day periods of each other.
Both of these methods show patchiness in whether the BSD
occurs before or after the zero-crossing. Almost all subpo-
lar TH BSDs (Figure 5b) occur after the zero-crossing, with
some areas occurring over four 8 day periods, or 32 days,
after the zero-crossing. We use the same time series as in
Figures 4d–4f (locations plotted in Figures 5a–5c as purple
diamonds) to examine the relationship between the heat flux
ZC and increases in chlorophyll.
3.3. Time Series 1 and 2
[19] We use time series 1 and 2 (Figure 4), both located
in the nutrient-limited subtropics, to determine why the
ROC method shows early blooms in a band centered at
36°N–39°N (time series 2), compared with the rest of the
subtropical region (time series 1). Figure 6 shows the time
 BRODY ET AL.: METHODS TO DETERMINE BLOOM INITIATION

ROC minus ZC difference between the two BSDs (TH minus ROC) is –2.7
80° W 40° W 0° periods. In contrast, at 36°N (time series 2), TH BSDs often
a. 60° N 12 occur when the bloom is well underway, with an average
°
50 N
difference between the two BSDs of 8.5 periods.
[20] Time series 1 and 2 also show that at 36°N, the yearly
40° N 8 median threshold is elevated relative to the time series, lead-
ing to later TH blooms than at 32°N. The elevated median
4
appears to be caused by the longer duration of the blooms
TH minus ZC at 36°N, as compared with 32°N. Indeed, an overlay of the
80° W 40° W 0° Fourier reconstructions of the two time series (Figure 7)
0 shows that at 36°N the bloom both begins earlier and lasts
b. 60° N
longer than at 32°N. The earlier blooms are likely not iden-
50° N tified by the TH method because the longer bloom duration
−4 elevates the median threshold relative to the chlorophyll time
40° N
series.
−8
[21] We generalize this observation for the entire band of
early ROC BSDs at 36°N–39°N (Figure 4a) by defining a
CS minus ZC metric called the relative median position:
80° W 40° W 0° −12
c. 60° N
chlmax – chlmin
50° N . (1)
−16 chlmax – chlmedian
40° N

−20
Figure 5. (a) ROC, (b) TH, and (c) CS BSDs minus the
8 day period during which heat fluxes become positive
(zero-crossing or ZC). The zero-contour is shown in black.
Monthly heat flux data was downloaded from http://www.
esrl.noaa.gov/psd/data/gridded/data.godas.html and linearly
interpolated to match the 8 day SeaWiFS data.
series plotted for the nine full years of data. At both time
series, ROC BSDs occur as chlorophyll levels are beginning
to increase. At 32°N (time series 1), TH BSDs occur at the
same time as or slightly earlier than ROC BSDs. The average
As seen in the schematic (Figure 8a), long-duration blooms
(solid curve) tend to have higher relative median positions
than short-duration blooms (dashed curve). Plotting relative
median positions for the study area (Figure 8b) shows that
the band of ROC-calculated early blooms at 36°N–39°N
corresponds with high relative median positions. Thus, our
conclusion from time series 1 and 2 that high relative median
positions create earlier blooms likely holds for the entire
band of early blooms.
[22] CS BSDs generally show slightly earlier blooms than
either ROC or TH BSDs for the subtropical regions in the
domain but, like TH BSDs, do not show a band of espe-
cially early blooms at 36°N–39°N for similar reasons: the

Time Series 1
chlorophyll (mg m−3)

0.3
0.25
0.2
0.15
0.1
0.05
Sept’98 ’99 ’00 ’01 ’02 ’03 ’04 ’05 ’06 ’07

Time Series 2
chlorophyll (mg m−3)

0.3
0.25
0.2
0.15
0.1
0.05
Sept’98 ’99 ’00 ’01 ’02 ’03 ’04 ’05 ’06 ’07

Figure 6. Time series with BSDs calculated using all three methods at 32°N and 36°N. The values of
the CS threshold have been normalized to the values of the chlorophyll time series. Dashed lines indicate
September of each year.
6
 BRODY ET AL.: METHODS TO DETERMINE BLOOM INITIATION

° °
0.25 32 N 36 N

chlorophyll (mg m−3)

0.2

0.15

0.1

0.05

Sept’98 ’99 ’00 ’01 ’02 ’03 ’04 ’05 ’06 ’07

Figure 7. Fourier reconstructions of both time series in Figure 6.

longer bloom duration, which increases the total cumula- well with the band of early CS BSDs, supporting the
tive biomass, raises the cumulative sum threshold compared explanation that where CS BSDs occur much earlier than TH
with other subtropical latitudes. The band of early blooms at and ROC BSDs, they identify the start of secondary blooms.
36°N–39°N coincides approximately with the Gulf Stream,
which creates increased eddy kinetic energy and mixing in 3.5. Time Series 4 and 5
this area [Richardson, 1983; Fratantoni, 2001]. Therefore, [25] Time series 4 and 5 (Figure 11) are both located in a
increased mixing, and the consequent increase in entrained relatively large area within the light-limited, subpolar North
nutrients, likely create the conditions necessary to support a Atlantic, from approximately 55°N to 60°N, where TH
longer phytoplankton bloom period. BSDs occur later than either CS or ROC BSDs (Figure 4).
Examining these time series shows that blooms in this area
3.4. Time Series 3
[23] Time series 3 (Figure 9) represents an area in which
the CS method shows fall and winter BSDs, consistent with a.
subtropical areas, while TH and ROC BSDs show spring
BSDs, consistent with subpolar regions. Figures 4e and 4f maximum
show the degree to which the location of the subtropical-
subpolar transition differs between CS BSDs versus TH
and ROC BSDs. The shape of the chlorophyll data and its
Fourier reconstruction in time series 3 indicate that in most maximum
years this area experiences a primary bloom in the spring and
a secondary bloom in the fall, likely due to the mechanisms
described in section 2.1 and consistent with the findings of median
Martinez et al. [2011] and D’Ortenzio et al. [2012]. The tim-
ing of the heat flux ZC just prior to or coincident with the median
primary bloom provides further evidence for a light-limited
spring bloom and a nutrient-limited fall bloom in this region.
Further, the minimum chlorophyll levels occur between the 80° W 40° W 0°
blooms during the highly stratified, nutrient-depleted sum-
b.
mer months. These two observations explain the early CS 60° N
BSDs: for the time series used in the CS method, which is
shifted to start at the minimum chlorophyll point, the sec-
ondary bloom occurs before the primary bloom, and the 50° N
chlorophyll increase during the secondary bloom is large
enough to raise the cumulative chlorophyll sum above the
prescribed threshold. The other two methods, which search 40° N

for the BSD in relation to the yearly maximum of the

chlorophyll time series, identify the BSD very close to the
heat flux ZC.
[24] The conclusions drawn from time series 3 can be
extended to the entire area of early CS BSDs by plotting 1 1.2 1.4 1.6 1.8 2
the magnitude of the 20th Fourier coefficient, which corre-
sponds to the bi-yearly bloom period, divided by the sum of Figure 8. (a) Schematic diagram illustrating the relative
the magnitudes of all the Fourier coefficients, over the study median position metric (vertical solid line divided by vertical
domain (Figure 10). Areas on the map where the bi-yearly dashed line). The solid curve is an example of a low relative
bloom period is large compared with the other periods can be median position; the dashed curve is an example of a high
used to estimate areas where there are prominent spring and relative median position. (b) Relative median positions,
fall blooms. The band of spring and fall blooms corresponds averaged over the 9 year time series.
7
 BRODY ET AL.: METHODS TO DETERMINE BLOOM INITIATION

Time Series 3

chlorophyll (mg m−3)

0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
Sept’98 ’99 ’00 ’01 ’02 ’03 ’04 ’05 ’06 ’07

Figure 9. Time series with BSDs calculated using all three methods shown for 31°W, 43°N. The values
of the CS threshold have been normalized to the values of the chlorophyll time series. Dashed lines
indicate September of each year.

begin with several small increases in chlorophyll prior to the
chlorophyll maximum. The difference in average TH ver-
sus CS and ROC BSDs is driven by large differences in
BSDs for a few years out of each time series (shaded years
in Figure 11) rather than systemic differences in BSDs. For
the years that do contain late-occurring TH BSDs, the dif-
ference is due to an especially large decrease (two or more
weeks below the threshold) in chlorophyll levels between
the small chlorophyll spikes and the chlorophyll maximum,
which the TH algorithm identifies as the seasonal minimum
prior to the bloom. This effect is likely accentuated by high
relative median positions in this region of the North Atlantic,
as compared to the western North Atlantic at the same lati-
tudes (Figure 8). By contrast, the Fourier reconstruction used
to identify ROC BSDs smooths the multiple chlorophyll
increases into one continuous bloom, and, in most years, the
low-magnitude chlorophyll increases are still large enough
to raise the cumulative chlorophyll sum used to calculate CS
BSDs above the 15% threshold.
[26] There are several possible explanations for the
observed low-magnitude increases in chlorophyll prior to
the main bloom. This pattern could be driven by biology,
where each chlorophyll spike represents a successive phy-
toplankton species that gets quickly grazed down until a
larger phytoplankton species establishes a long-duration,
high-magnitude bloom [Sommer, 1985; Taylor et al., 1993].
Alternatively, this pattern could be driven by physical pro-
cesses. The mechanism for bloom initiation described in
Taylor and Ferrari [2011] and in section 1 could allow for
more transient chlorophyll increases due to mixed layer sta-
bilization before the onset of seasonal stratification. This
explanation finds support in our results: for all years in which
TH blooms are delayed relative to ROC blooms, the heat flux
ZC occurs at roughly the same time as the small chlorophyll
increases identified by the ROC method as the BSD.
study, the heat flux ZC also occurs at the beginning of the
phytoplankton bloom, indicating that stabilization due to
net ocean surface warming may also play a role in driv-
ing blooms here. However, BSDs calculated with the ROC
method are earlier than blooms calculated using TH and CS
methods. Figure 12 shows that the chlorophyll time series
in this area is composed of long periods of very low chloro-
phyll punctuated by brief, high-magnitude blooms. The low
chlorophyll levels throughout the fall, winter, and spring
months are likely due to a combination of low irradiance and
the large amount of missing data in this region, which is then
filled with the yearly time series minimum (see section 3.7).
Comparing the Fourier reconstruction of the data to the
chlorophyll time series shows that the 20 coefficients chosen
to create the reconstruction cannot replicate the extremely
short duration of blooms at this latitude. While the timing
of the chlorophyll maxima in the reconstruction is consistent
with the timing of the maxima in the time series, the recon-
structed blooms are much longer and thus start earlier than
the blooms in the time series, leading to ROC BSDs that
occur during the late winter.
3.7. Effect of Filling Missing Data
[28] While remotely sensed ocean color data provides a
valuable resource for examining phytoplankton bloom phe-
nology, gaps in the data, especially at high latitudes, can
affect the quality of phenology estimates. Cole et al. [2012]

3.6. Time Series 6

[27] Time series 6 (Figure 12) is located west of
Greenland, also a light-limited area for phytoplankton
growth. In this area, all three methods show earlier BSDs
than at the same latitude in other locations (Figure 4). This
pattern is also seen in the phenology study by Henson et al.
[2009] and is attributable to early stratification induced by Figure 10. Magnitude of the 20th Fourier coefficient (cor-
westward advection of relatively light freshwater melt from responding to a 6 month or bi-yearly bloom period) divided
Greenland [Frajka-Williams et al., 2009]. In the present by the sum of the magnitudes of all coefficients.
8
 BRODY ET AL.: METHODS TO DETERMINE BLOOM INITIATION

Time Series 4

chlorophyll (mg m−3)

1.5

0.5

0
Sept’98 ’99 ’00 ’01 ’02 ’03 ’04 ’05 ’06 ’07

Time Series 5
1.2
chlorophyll (mg m−3)

0.8
0.6

0.4

0.2

Sept’98 ’99 ’00 ’01 ’02 ’03 ’04 ’05 ’06 ’07

Figure 11. Time series with BSDs calculated using all three methods shown for 21°W, 55°N and 38°W,
59°N. The values of the CS threshold have been normalized to the values of the chlorophyll time series.
Shading indicates years in which TH BSDs occur later than ROC and CS BSDs. Dashed lines indicate
September of each year.

provided a comprehensive study of the effect of missing
data on the TH method of estimating BSDs by comparing
BSDs and bloom peak dates derived from a SeaWiFS data
set containing missing data with those derived from a SeaW-
iFS data-assimilating biogeochemical model. Similar studies
conducted for other methods of determining BSDs would be
a useful addition to phenology research. However, in this
study, our aims in examining missing data are twofold: one,
to ensure that our method of filling the missing data does not
strongly affect our comparisons between the methods; and
two, to briefly comment upon the effect of filling data gaps
with the time series minimum on the BSDs we observe for
the TH and CS methods.
[29] To address our first aim, we calculated BSDs using
the TH and CS methods applied to a data set with no data
filling. We could not conduct this calculation for the ROC
method, because performing a Fourier reconstruction on the
chlorophyll data requires a gap-free data set. We also calcu-
lated BSDs using the TH and CS methods for a data set that
had been filled using only the spatial averaging described in
section 2.1. However, the BSDs calculated using a data set
with only spatial filling were virtually identical to those cal-
culated using a data set where no filling was applied, leading
to the conclusion that the filling of large data gaps with the
time series minimum has the largest effect on BSDs. When
we created the same difference plots as in Figures 4d–4f
using unfilled data (Figure 13), very similar general pat-
terns appear, although the magnitudes of those patterns
differ (compare Figure 4d with 13a, Figure 4f with 13b,
and Figure 4e with 4c and 4d). In fact, when comparing
BSDs using the unfilled data, the correspondence between
areas with early CS BSDs (Figures 13b and 13d) and areas
with prominent secondary blooms strengthens. We therefore
conclude that our findings regarding the reason for the dif-
ferences in BSDs in sections 3.3 through 3.6 are independent
of the amount of missing data in each time series and the
method of filling missing data.
[30] We address our second aim by examining the differ-
ences between TH and CS BSDs using filled and unfilled
data. Figure 14a shows the average percentage of missing

Time Series 6
10
chlorophyll (mg m−3)

0
Sept’98 ’99 ’00 ’01 ’02 ’03 ’04 ’05 ’06 ’07

Figure 12. Time series with BSDs calculated using all three methods shown for 53°W, 62°N. The values
of the CS threshold have been normalized to the values of the chlorophyll time series. Dashed lines
indicate September of each year.
9
 BRODY ET AL.: METHODS TO DETERMINE BLOOM INITIATION

unfilled TH minus ROC unfilled CS minus ROC

80° W 40° W 0° 80° W 40° W 0°
rather than the late summer, and thus the bloom will occur
later (farther from 1 September). This explains why the
a.a. 60° N b.
b. 60° N
unfilled CS BSDs have an even higher propensity than the
50° N 50° N filled BSDs to identify secondary, fall blooms as primary
40° N 40° N blooms. North of 50°N, the large amount of missing data
that has been given a value in the filled data set, rather than
unfilled TH minus CS TH minus unfilled CS
treated as a missing, zero value in the unfilled data set,
80° W 40° W 0° 80° W 40° W 0° causes the filled cumulative sum curve to start increasing
c.c. 60° N d. 60° N
during the period of missing data, and thus rise above the
d.
50° N 50° N
threshold earlier than in the unfilled case.
40° N 40° N

−20 −10 0 10
Figure 13. Difference between BSDs calculated with the
three methods, with either (a and c) the TH BSDs or (b and
d) the CS BSDs calculated using unfilled chlorophyll data.
The scale of the colorbar axis is 8 day periods.
data per pixel for the study area, which, as expected,
increases at higher latitudes. Comparing filled and unfilled
TH-calculated BSDs (Figure 14b) shows that south of
approximately 45°N, filled TH BSDs are slightly later than
4. Discussion
[32] Our examination of the differences between the
20 ROC, TH, and CS methods for calculating BSDs has
revealed areas with interesting chlorophyll seasonal cycles
and raised several questions about the biological and phys-
ical underpinnings of those cycles. We find that the TH
method, as we are implementing it, is likely to identify BSDs
as occurring during or immediately after the largest increases
in chlorophyll concentrations, especially when the relative
median position of the chlorophyll time series is large (loca-
missing data 1
80° W 40° W 0°

unfilled BSDs, especially off the coast of Cape Cod, where

60° N
the percentage of missing data per pixel is somewhat higher a.
than the surrounding areas. North of 50°N, filled TH BSDs 50° N 0.5
are generally earlier than unfilled TH BSDs. Time series
from these areas (not shown) reveal that south of 45°N, data 40° N
filling tends to occur in winter, when chlorophyll levels are
high. While the gaps at these latitudes are small enough that
data filling does not noticeably affect the median thresh- 0
old, the gaps can occur as chlorophyll levels are increasing
prior to a bloom. If the gaps are two weeks or longer, filling TH minus TH unfilled
the gaps with the minimum chlorophyll value can delay the 80° W 40° W 0°
filled BSDs until after the gap, even if the chlorophyll time 20
series has increased above the threshold prior to the gap. 60° N
North of 50°N, where the amount of missing data per pixel b.
is higher, filled TH BSDs occur earlier than unfilled BSDs 50° N
because filling large data gaps with the time series minimum
10
lowers the median threshold for filled data as compared to 40° N
unfilled data. The tendency of filled data to produce earlier
blooms than unfilled data at subpolar latitudes is consistent
with Cole et al. [2012], while the tendency of filled data to
produce later blooms than unfilled data at subtropical lati- 0
tudes differs from Cole et al. [2012]. In that study, the filled CS minus CS unfilled
data set, which came from a data-assimilating biogeochemi- 80° W 40° W 0°
cal model, did not replace gaps in the chlorophyll data with
60° N
the yearly minimum chlorophyll value. c. −10
[31] Filled versus unfilled CS-calculated BSDs
50° N
(Figure 14c) show the same general patterns as TH BSDs.
In this case, filled CS BSDs occur later than unfilled BSDs 40° N
south of 50°N because filling the data set with the time
−20
series minimum can change the position of the first occur-
rence of the chlorophyll minimum after 1 September, which
has been set as day 1 of the year for all methods. Since the Figure 14. (a) Percentage of 8 day periods with missing
chlorophyll time series minimum generally occurs in the data per year, averaged for the 10 year time series. (b and
late summer or early fall in these regions and data gaps c) Comparison of TH BSDs minus TH BSDs calculated
occur in the winter, using filled data will cause the time using the unfilled data set (b) and CS BSDs minus CS BSDs
series used to calculate the CS BSD to start in the winter calculated using the unfilled data set (c).
10
 BRODY ET AL.: METHODS TO DETERMINE BLOOM INITIATION
tions 1 and 2, Figure 6) or the start of the bloom consists
of successive, low-magnitude chlorophyll increases (loca-
tions 4 and 5, Figure 11). Based on these findings, the TH
method might be especially appropriate for investigating
the match or mismatch between phytoplankton and upper
trophic levels [e.g., Edwards and Richardson, 2004; Mackas
et al., 2007; Koeller et al., 2009], because the match-
mismatch hypothesis is based on the timing of the high
phytoplankton biomass period [Cushing, 1959]. The way in
which we chose to implement the TH method contributed
somewhat to these conclusions, especially at locations 4 and
5 and in areas where data gaps filled with the time series
minimum occurred near the beginning of the bloom, by
potentially increasing the likelihood that the identified BSD
would occur during a period of high chlorophyll growth.
It would be possible to modify the method we used by
increasing the number of 8 day periods below the thresh-
old required to find a bloom, although this heightens the
risk of identifying isolated chlorophyll spikes as the main
bloom. Starting the search for points above the threshold
from the beginning of the time series is a more commonly
used TH method and might also provide somewhat differ-
ent results with chlorophyll time series similar to those at
locations 4 and 5. Implementing the threshold method in this
manner increases its sensitivity to the time series start date
and, depending on the start date chosen, could also be used
to identify the timing of secondary blooms. Finally, the dis-
crepancies in our comparison of TH BSDs from filled and
unfilled data with the findings of Cole et al. [2012] indi-
cate that temporal interpolation of missing data may be a
more appropriate method of filling data gaps in subtropical
areas, where data gaps often occur as chlorophyll levels are
increasing prior to the bloom.
[33] The ROC method identifies blooms as starting when
chlorophyll is increasing rapidly from the pre-bloom min-
imum, but biomass levels may still remain low. The ROC
method, therefore, could be useful in examining the sea-
sonal physical or biological mechanisms that create condi-
tions in which a bloom can occur [e.g., Behrenfeld, 2010].
The Fourier reconstruction method we used to smooth the
chlorophyll data to implement the ROC method negatively
impacted the ROC BSDs at location 6 (Figure 12) and may
have had similar impacts at other high-latitude locations.
Alternative methods of reconstructing the chlorophyll data,
such as the Gamma Generalized Linear Model method in
Vargas et al. [2009] and Sapiano et al. [2012] or the method
of filtering coefficients using a Lanczos filter [Duchon,
1979] could be tested in the future to determine whether
they produce different ROC BSD,s and which smoothing
technique best reconstructs the chlorophyll time series.
[34] While the CS method, like the TH method, depends
on a biomass-based threshold, the sensitivity of the CS BSDs
to the particular threshold creates flexibility in the feature
of the chlorophyll time series that the CS method identifies
as a bloom. The 15% of the cumulative biomass thresh-
old we used produced BSDs more closely aligned with the
first increases in chlorophyll biomass, while a 30% threshold
would produce BSDs associated with the largest increases
in biomass. Thus, the CS method could be used for either
of the purposes we identified for the TH and ROC methods.
However, this feature of the CS method also necessitates
a careful choice of the threshold to ensure that it identifies
11
the relevant feature of the chlorophyll times series. The CS
method is also very sensitive to the date used for the start of
the time series and thus cannot be implemented at the basin
scale using a fixed start date. Our method of shifting each
time series to start at its minimum chlorophyll level, based
on the assumption that the yearly chlorophyll minimum
precedes the primary bloom, accounts for that sensitivity.
However, location 3 (Figure 9) shows an area where the
yearly chlorophyll minimum precedes the secondary bloom,
causing the CS method to misidentify secondary fall blooms
as primary blooms and thus falsely extend the subtropical
region of the North Atlantic. Shifting the time series in this
manner, combined with our method of data filling, also cre-
ated differences in filled and unfilled CS BSDs. However,
when examining phytoplankton blooms using basin-scale,
remotely sensed chlorophyll data, the need to efficiently
process large data sets necessitates the use of simplifying
assumptions such as the one we made. Future use of the CS
method in remotely sensed phytoplankton phenology stud-
ies should be accompanied by a careful treatment of the time
series start date, and it may be found that the CS method
works better as a way of identifying the first bloom in a
time series regardless of whether that bloom is a primary or
secondary bloom.
[35] The discussion of positive heat fluxes as a possible
driver of subpolar phytoplankton blooms in section 3.2 illus-
trates the importance of carefully considering which method
to use for an investigation into phytoplankton bloom phe-
nology, since comparing the heat flux zero-crossing to the
ROC-, TH-, and CS-calculated BSDs (Figure 5) produced
different results. Comparing subpolar ROC or CS BSDs to
the zero-crossing (Figures 5b and 5c) leads to the conclu-
sion that blooms begin very near the time that heat fluxes
become positive, consistent with the theory and results of
Taylor and Ferrari [2011]. Additionally, because in some
areas BSDs can occur before heat fluxes become positive,
ROC and CS BSDs support the findings of [Mahadevan
et al., 2012]. In contrast, comparing subpolar TH BSDs to
the zero-crossing (Figure 5d) leads to the conclusion that,
because BSDs occur well after the zero-crossing, positive
heat fluxes alone are not sufficient to initiate a bloom. These
two conclusions can be reconciled by the patterns seen in
time series 4 and 5 (Figure 11): during years with sev-
eral low-magnitude chlorophyll increases prior to the main
chlorophyll increase, the TH method identifies BSDs as
occurring after the low-magnitude increases, while the ROC
and CS methods identify BSDs as occurring at the beginning
of the low-magnitude chlorophyll increases. It is possible
that the low-magnitude chlorophyll increases identified by
the ROC and TH methods could be caused by a decrease in
turbulent convection driven by heat fluxes becoming posi-
tive, while the high-magnitude chlorophyll increase identi-
fied by the TH method could be caused by the seasonally
shoaling mixed layer, consistent with the Sverdrup hypothe-
sis. However, while the results of our investigation support
the theory advanced by Taylor and Ferrari [2011], these
results do not provide definitive evidence for the onset of
positive ocean-atmosphere heat fluxes as opposed to sea-
sonal mixed layer shoaling as a driver of subpolar bloom
initiation. First, the onset of positive ocean-atmosphere heat
fluxes may coincide with seasonal mixed layer shoaling. If
this is the case, it would not be clear whether one factor was
 BRODY ET AL.: METHODS TO DETERMINE BLOOM INITIATION
primarily responsible for phytoplankton bloom initiation.
Second, net warming of the ocean surface is not the only
factor that could stratify the upper mixed layer of the ocean.
For example, the mechanism for bloom initiation described
in Mahadevan et al. [2012] relies on eddy-induced stratifi-
cation of the mixed layer. Factors such as wind-generated
mixing and freshwater fluxes from seasonal sea ice melt,
as we briefly discussed in section 3.6, may also play a role
in upper mixed layer stratification. While a more detailed
investigation of the potential mechanisms that create and
break down chlorophyll increases prior to the main bloom
would need to address these questions, the heat flux study
we present here is an example of why comparisons of mul-
tiple BSD methods can be useful and why the selection of
a definition for the onset of a phytoplankton bloom appro-
priate to the question being asked is important to consider
when selecting a method for determining the date of bloom
initiation.
[36] Acknowledgments. SeaWiFS chlorophyll a data were obtained
using the NASA ocean color database. Heat flux data were obtained from
the ESRL/PSD database. This work was funded by a NASA Earth and
Space Science Fellowship and by a NOAA MPOWIR fellowship. We would
like to thank R. Asch, who provided helpful suggestions and comments dur-
ing the development of this work. We would also like to acknowledge three
anonymous reviewers, whose helpful suggestions and comments greatly
improved this paper.
References
Behrenfeld, M. (2010), Abandoning Sverdrup’s Critical Depth Hypothesis
on phytoplankton blooms, Ecology, 91, 977–989, doi:10.1890/09-1207.1.
Cole, H., S. Henson, A. Martin, and A. Yool (2012), Mind the gap: The
impact of missing data on the calculation of phytoplankton phenology
metrics, J. Geophys. Res., 117, C08030, doi:10.1029/2012JC008249.
Cushing, D. (1959), The seasonal variation in oceanic production as a
problem in phytoplankton dynamics, Journ. Conseil., 24, 455–464.
D’Ortenzio, F., D. Antoine, E. Martinez, and M. R. d’Alcalá (2012), Phe-
nological changes of oceanic phytoplankton in the 1980s and 2000s
as revealed by remotely sensed ocean-color observations, Global Bio-
geochem. Cycles, 26, GB4003, doi:10.1029/2011GB004269.
Duchon, C. (1979), Lanczos filtering in one and two dimensions, J. Appl.
Meteorol., 18, 1016–1023.
Edwards, M., and J. Richardson (2004), Impact of climate change on marine
pelagic phenology and trophic mismatch, Nature, 430, 881–884, doi:
10.1038/nature02808.
Fleming, V., and S. Kaitala (2006), Phytoplankton spring bloom inten-
sity index for the Baltic Sea estimated for the years 1992 to 2004,
Hydrobiologia, 554, doi:10.1007/s10750-005-1006-7.
Follows, M., and S. Dutkiewicz (2001), Meteorological modulation of the
North Atlantic spring bloom, Deep Sea Res. Part II, 49, 321–344, doi:
10.1016/S0967-0645(01)00105-9.
Frajka-Williams, E., P. Rhines, and C. Eriksen (2009), Physical controls
and mesoscale variability in the Labrador Sea spring phytoplankton
bloom observed by Seaglider, Deep Sea Res. Part I, 56, 2144–2161, doi:
10.1016/j.dsr.2009.07.008.
Fratantoni, D. (2001), North Atlantic surface circulation during the 1990’s
observed with satellite-tracked drifters, J. Geophys. Res., 106 (C10),
22,067–22,093.
Greve, W., S. Prinage, H. Zidowitz, J. Nast, and F. Reiners (2005), On
the phenology of North Sea ichthyoplankton, ICES J. Mar. Sci., 62,
1216–1223, doi:10.1016/j.icesjms.2005.03.011.
Henson, S., I. Robinson, J. Allen, and J. Waniek (2006), Effect of meteoro-
logical conditions on interannual variability in timing and magnitude of
the spring bloom in the Irminger Basin, North Atlantic, Deep Sea Res.
Part I, 53, 1601–1615, doi:10.1016/j.dsr.2006.07.009.
Henson, S., J. Dunne, and J. Sarmiento (2009), Decadal variability in
North Atlantic phytoplankton blooms, J. Geophys. Res., 114, c04013,
doi:10.1029/2008JC005139.
Ji, R., M. Edwards, D. Mackas, J. Runge, and A. Thomas (2010), Marine
plankton phenology and life history in a changing climate: Current
12
research and future directions, J. Plankton Res., 32(10), 1355–1368, doi:
10.1093/plankt/fbq062.
Kahru, M., V. Brotas, M. Manzano-Sarabiaz, and B. Mitchell (2011), Are
phytoplankton blooms occurring earlier in the Arctic? Global Change
Biol., 17, doi:10.1111/j.1365-2486.2010.02312.X.
Koeller, P., et al. (2009), Basin-scale coherence in phenology of shrimps
and phytoplankton in the North Atlantic ocean, Science, 324 (5928),
791–793, doi:10.1126/science.1170987.
Mackas, D., S. Batten, and M. Trudel (2007), Effects on zooplankton of
a warmer ocean: Recent evidence from the Northeast Pacific, Prog.
Oceanogr., 75, 223–252.
Mackas, D., et al. (2012), Changing zooplankton in a changing ocean:
Comparing time series of zooplankton phenology, Prog. Oceanogr., 97,
31–62, doi:10.1016/j.pocean.2011.11.005.
Mahadevan, A., E. D’Asaro, C. Lee, and M. Perry (2012), Eddy-driven
stratification initiates North Atlantic spring phytoplankton blooms,
Science, 337, 54–58, doi:10.1126/science.1218740.
Martinez, E., D. Antoine, F. D’Ortenzio, and D. de Boyer Montégut (2011),
Phytoplankton spring and fall blooms in the North Atlantic in the 1980s
and 2000s, J. Geophys. Res., 116, C11029, doi:10.1029/2010JC006836.
Platt, T., C. Fuentes-Yaco, and K. Frank (2003), Spring algal bloom and
larval fish survival, Nature, 423, 398–399, doi:10.1038/423398b.
Platt, T., S. Sathyendranath, G. White, C. Fuentes-Yaco, L. Zhai, E. Devred,
and C. Tang (2009a), Diagnostic properties of phytoplankton time series
from remote sensing, Estuaries Coasts, 33, doi:10.1007/s12237-009-
9161-0.
Platt, T., G. White III, L. Zhai, S. Sathyendranath, and S. Roy
(2009b), The phenology of phytoplankton blooms: Ecosystem indi-
cators from remote sensing, Ecol. Model., 220, 3057–3069, doi:
10.1016/j.ecolmodel.2008.11.022.
Quetin, L., R. Ross, T. Frazer, and K. Haberman (1996), Factors affecting
distribution and abundance of zooplankton with an emphasis on Antarctic
krill, Euphausia superba, Antar. Res. S., 70, 357–371.
Racault, M., C. Le Quéré, E. Buitenhuis, S. Sathyendranath, and T. Platt
(2012), Phytoplankton phenology in the global ocean, Ecol. Indic., 14,
152–163.
Richardson, P. (1983), Eddy kinetic energy in the North Atlantic from
surface drifters, J. Geophys. Res., 88(C7), 4355–4367.
Roerink, G., M. Menenti, and W. Verhoef (2000), Reconstructing cloud-free
NDVI composites using Fourier analysis of time series, Int. J. Remote
Sens., 21, 1911–1917.
Rolinski, S., H. Horn, T. Petzoldt, and L. Paul (2007), Identifying cardinal
dates in phytoplankton time series to enable the analysis of long-term
trends, Oecologia, 153, 997–1008, doi:10.1007/s00442-007-0783.
Sapiano, M., C. Brown, U. Schollaert S., and M. Vargas (2012), Establish-
ing a global climatology of marine phytoplankton phenological charac-
teristics, J. Geophys. Res., 117, C08026, doi:10.1029/2012JC007958.
Sasaoka, K., S. Chiba, and T. Saino (2011), Climatic forcing and phyto-
plankton phenology over the subpolar North Pacific from 1998 to 2006,
as observed from ocean color data, Geophys. Res. Lett., 38, L15609, doi:
10.1029/2011GL048299.
Sharples, J., O. Ross, B. Scott, S. Greenstreet, and H. Fraser (2006), Inter-
annual variability in the timing of stratification and the spring bloom
in the North-western North Sea, Cont. Shelf Res., 26, 733–751, doi:
10.1016/j.csr.2006.01.011.
Siegel, D., S. Doney, and J. Yoder (2002), The North Atlantic spring phyto-
plankton bloom and Sverdrup’s Critical Depth Hypothesis, Science, 296
(5568), 730–733, doi:10.1126/science.1069174.
Sommer, U. (1985), Seasonal succession of phytoplankton in Lake
Constance, BioScience, 35(6), 351–357.
Sverdrup, H. (1953), On conditions for the vernal blooming of phytoplank-
ton, Journ. Conseil., 18, 287–295.
Taylor, A., D. Harbour, R. Harris, P. Burkill, and E. Edwards (1993), Sea-
sonal succession in the pelagic ecosystem of the North Atlantic and the
utilization of nitrogen, J. Plankton Res., 15(8), 875–891.
Taylor, J., and R. Ferrari (2011), Shutdown of turbulent convection as a
new criterion for the onset of spring phytoplankton blooms, Limnol.
Oceanogr., 56, 2293–2307, doi:10.4319/lo.2011.56.6.229.
Thomalla, S., N. Fauchereau, S. Swart, and P. Monteiro (2011), Regional
scale characteristics of the seasonal cycle of chlorophyll in the Southern
Ocean, Biogeosciences, 8, 2849–2866, doi:10.5194/bg-8-2849-2011.
Vargas, M., C. Brown, and M. Sapiano (2009), Phenology of marine phy-
toplankton from satellite ocean color measurements, Geophys. Res. Lett.,
36, L01608, doi:10.1029/2008GL036006.
Visser, M., and C. Both (2005), Shifts in phenology due to global climate
change: The need for a yardstick, P. Roy. Soc. B, 272, 2561–2569, doi:
10.1098/rspb.2005.3356.
White, M., et al. (2009), Intercomparison, interpretation, and assessment of
spring phenology in North America estimated from remote sensing for
 BRODY ET AL.: METHODS TO DETERMINE BLOOM INITIATION

1982–2006, Global Change Biol., 15, 2335–2359, doi:10.1111/j.1365-
2486.2009.01910.X.
Wiltshire, K., A. Malzahn, K. Wirtz, W. Greve, S. Janisch, P. Mangelsdorf,
B. F. J. Manly, and M. Boersma (2008), Resilience of North Sea phy-
toplankton spring bloom dynamics: An analysis of long-term data at
Helgoland Roads, Limnol. Oceanogr., 53, 1294–1302.
Yamada, K., and J. Ishizaka (2006), Estimation of interdecadal change of
spring bloom timing, in the case of the Japan Sea, Geophys. Res. Lett.,
33, L02608, doi:10.1029/2005GL024792.
Zhai, L., T. Platt, C. Tang, S. Sathyendranath, and R. Walls (2011), Phy-
toplankton phenology on the Scotian Shelf, ICES J. Mar. Sci., 68,
781–791, doi:10.1093/icesjms/fsq175.

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