MARINE AND FISHERY SCIENCES 33 (2): 205-225 (2020)
https://doi.org/10.47193/mafis.3322020301105
MARINE IMPACTS IN THE ANTHROPOCENE
The color of EPEA: variability in the in situ bio-optical properties in the
period 2000-2017
M. GUILLERMINA RUIZ
1, 2, *
, VIVIAN A. LUTZ
1, 2
, VALERIA SEGURA
1
, CARLA F. BERGHOFF
1
and RUBÉN M. NEGRI
1
1
Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP), Paseo Victoria Ocampo Nº 1, Escollera Norte, B7602HSA -
Mar del Plata, Argentina.
2
Instituto de Investigaciones Marinas y Costeras (IIMyC), Universidad Nacional de Mar del Plata (UNMdP),
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina
ABSTRACT. The ‘Estación Permanente de Estudios Ambientales’ (EPEA, 38° 28′ S-57° 41′ W,
Argentina) is an ecological time series of in situ observations started in 2000 aiming to assess chan-
ges in the marine environment and plankton communities under a global change scenario. Bio-opti-
cal properties are studied at EPEA since the color of the ocean undergoes temporal fluctuations, both
for natural and anthropogenic causes. Here we assessed whether bio-optical properties at EPEA
have changed during 2000-2017, identifying the occurrence of special events and inter-annual
trends in these properties. An increasing trend in chlorophyll-a concentration, possibly due to an
increase in the smaller fraction of phytoplankton was observed. Although the absorption coefficient
of phytoplankton did not follow a significant trend, it represented the occurrence of special events
of high biomass suggesting that satellite information should be useful for the study site. The specific
absorption coefficient of phytoplankton and the blue to red absorption ratio showed high values in
summer and low in winter, according to the probable dominance of different size cells and their
expected acclimation to the light regime. These results emphasize the relevance of periodic bio-opti-
cal in situ observations in understanding coastal ecosystems in a context of climate change.
Key words: Chlorophyll-a, bio-optical properties, inter-annual variability, EPEA, South Atlantic.
El color de la EPEA: variabilidad en las propiedades bio-ópticas in situ en el período 2000-2017
RESUMEN. La “Estación Permanente de Estudios Ambientales” (EPEA, 38° 28′ S-57° 41′ W,
Argentina) es una serie de tiempo ecológica de observaciones in situ iniciada en 2000 con el objetivo
de evaluar los cambios en el medio marino y las comunidades de plancton en un escenario de cambio
global. Las propiedades bio-ópticas se estudian en la EPEA ya que el color del océano sufre fluctua-
ciones temporales, tanto por causas naturales como antropogénicas. Aquí evaluamos si las propieda-
des bio-ópticas de la EPEA han cambiado durante 2000-2017, identificando la ocurrencia de eventos
especiales y tendencias interanuales en estas propiedades. Se observó una tendencia creciente en la
concentración de clorofila-a, posiblemente debido a un aumento en la fracción más pequeña de fito-
plancton. Aunque el coeficiente de absorción del fitoplancton no siguió una tendencia significativa,
representó la ocurrencia de eventos especiales de alta biomasa, lo cual sugiere que la información
satelital debería ser útil para el sitio de estudio. El coeficiente de absorción específico del fitoplancton
y la relación de absorción de azul a rojo mostraron valores altos en verano y bajos en invierno, de
acuerdo con el probable dominio de las células de diferentes tamaños y su aclimatación esperada al
régimen de luz. Estos resultados enfatizan la relevancia de las observaciones bio-ópticas periódicas
in situ para comprender los ecosistemas costeros en un contexto de cambio climático.
Palabras clave: Clorofila-a, propiedades bio-ópticas, variabilidad interanual, EPEA, Atlántico Sur.
205
Marine and
Fishery Sciences
MAFIS
*Correspondence:
mgruiz@inidep.edu.ar
Received: 13 July 2020
Accepted: 18 August 2020
ISSN 2683-7595 (print)
ISSN 2683-7951 (online)
https://ojs.inidep.edu.ar/ojs/index.php/
mafis/
Journal of the Instituto Nacional de
Investigación y Desarrollo Pesquero
(INIDEP)
This work is licensed under a
Creative Commons Attribution-
NonCommercial-ShareAlike 4.0
International License
INTRODUCTION
The importance of evaluating the role of the
oceans in a global climate change scenario is rec-
ognized worldwide. Ecological time series pro-
vide observations that allow assessing changes
occurring in the marine environment and its biota
in the long run (Ducklow et al. 2009). The
‘Estación Permanente de Estudios Ambientales’
(EPEA, 38° 28′ S-57° 41′ W, Argentina) was ini-
tiated in 2000 with the aim of understanding the
functioning of planktonic communities and try to
distinguish the possible effects of climate change.
Besides several physical, chemical, oceanograph-
ic and biological variables, bio-optical properties
are also studied at EPEA since the color of the
waters is one of the ocean characteristics that
undergoes temporal fluctuations, both as part of
natural cycles and due to the impact of anthro-
pogenic global change. Hence, the study of the
bio-optical properties has become an invaluable
tool to monitor changes in marine ecosystems.
Bio-optical properties are crucial in marine
ecological studies because light is an essential
factor governing the heat content in the ocean
and affecting its physical conditions. Light avail-
able in the water triggers biological processes,
providing the energy required in the photosyn-
thesis and hence determining in great part the
amount of primary production fueling the marine
food web, regulating ontogeny in different
organisms (i.e., larval stages), trophic migrations
(e.g., diel vertical movements), and facilitating
or avoiding predation (by affecting the visual
field). Furthermore, given the anthropogenic
impact on the climate, with near 28% of the
anthropogenic carbon dioxide released to the
atmosphere captured by the ocean (IPCC 2019),
there is a need to understand changes in phyto-
plankton bio-optical properties since on a global
scale phytoplankton contributes with about half
of the earth primary production (Longhurst
1995). Dutkiewicz et al. (2019), using a complex
biogeochemical model estimated that by the year
2100 changes in phytoplankton community com-
position would cause a 63% change on the
reflectance in the blue region of the electromag-
netic spectrum (an essential bio-optical property
of the oceans). Therefore, long-term records of
bio-optical properties in different places of the
ocean would provide ground-truth data to ana-
lyze in detail these possible changes.
Once the incident solar radiation passes
through the ocean surface it is attenuated due to
the scattering and absorption processes as a con-
sequence of its interaction with the seawater
(SW) and the active optical components (OACs)
present in it. OACs are the phytoplankton (Phy),
the non-algal particles (NAP) and the chro-
mophoric dissolved organic matter (CDOM).
Hence, the amount of light available for the pho-
tosynthesis depends on the types and proportions
in which the different OACs are present in a cer-
tain time and place. The degree of light attenua-
tion can be measured by the inherent bio-optical
properties, mainly the absorption and the disper-
sion coefficient (a(λ ) and b( λ ) respectively,
m
-1
), which are quantities that have spectral
dependence and are governed by a strict additivi-
ty (Prieur and Sathyendaranath 1981). This
means that the total a( λ ) is equivalent to the sum
of the a
SW
( λ ), a
Phy
( λ ), a
NAP
( λ ) and a
CDOM
( λ ).
In turn, theoretically, the a( λ ) of each OAC can
be expressed as the product between a specific
coefficient and its concentration, that is, a vector
that represents the spectral signature of the com-
ponent and a scalar associated with the amount of
that component present.
The spectral absorption characteristics of phy-
toplankton depend on the species, their size and
specific ensemble of pigments, as well as to their
physiological status (Sathyendranath et al. 1987;
Johnsen and Sakshaug 1996; Lutz et al. 2001;
Lutz et al. 2003). It has been observed that larger
cells have a relatively flatter absorption spectrum,
measurable by a lower value of the specific
206
MARINE AND FISHERY SCIENCES 33 (2): 205-225 (2020)
absorption coefficient of phytoplankton at 443
nm (absorption per concentration unit of chloro-
phyll-a, a
B
Phy
(443)), and a lower ratio of absorp-
tion between the blue and red bands
[a
Phy
(443)/a
Phy
(676)], than smaller cells. At the
same time, any given species can photoacclimate
to the intensity of light to which it is exposed by
adjusting the proportion of its different pigments,
increasing those with a light-harvesting (photo-
protective) function at low (high) irradiances,
which results in spectral changes of the absorp-
tion spectrum (i.e., a lower value of a
B
Phy
(443),
and [a
Phy
(443)/a
Phy
(676)] at low irradiances, and
vice versa). These effects, which respond to the
principle of ‘packaging effect’ (Duyens 1956;
Sathyendranath et al. 1987; Bricaud et al. 1995),
have been reported for different places of the
world ocean (Ciotti et al. 2002; Babin et al. 2003;
Lutz et al. 2003) and the Argentine Sea (Ferreira
et al. 2009; Segura et al. 2013; Williams et al.
2018; Delgado et al. 2019).
Coastal waters as the case of EPEA have a
complex mixture of OACs, which vary their con-
centrations with time. The inherent optical prop-
erties (a
Phy
( λ ), a
NAP
( λ ), a
CDOM
( λ )), the concen-
tration of chlorophyll-a as a proxy of phyto-
plankton biomass (both, the total fraction, Chl
T
,
and that contributed by the phytoplankton frac-
tion less than 5 µm in diameter, Chl
<5
) and the
irradiance integrated in the range of ‘photosyn-
thetically available radiation’ (PA R , 400-700 nm)
incident on the surface, E
0
(PAR) and the down-
welling on the water column, E
d
(PAR), have been
systematically determined as part of the meas-
urements performed at EPEA. A first analysis of
bio-optical characteristics for the 2000-2001
annual cycle at EPEA (Lutz et al. 2006) evi-
denced that CDOM was the main contributor to
absorption, and that lower values of a
B
Phy
(443)
were found in winter (especially during a bloom
of a large diatom) and higher in summer when
small cells (especially of the Genus Synechococ-
cus) predominated. This last result was con-
firmed in a study of ultra-phytoplankton in the
summer 2001-2002 (Silva et al. 2009). More
recently, an analysis of validation of satellite
chlorophyll-a for 18 years of the time series
(Ruiz 2018) reported that CDOM was the main
OAC throughout the year, and hence affecting
the remote sensing signal of ocean-color at
EPEA, overestimating Chl
T
mainly in summer.
To assess whether bio-optical properties at
EPEA have experienced a change during the 2000-
2017 period, the main objectives of this work
were: a) to provide a general description of varia-
tions in these properties; b) to identify the occur-
rence of special events; c) to analyze the occur-
rence of inter-annual trends in these properties.
MATERIALS AND METHODS
Study area
EPEA is located north of the Argentine conti-
nental shelf (38° 28′ S-57° 41′ W), 13.5 nautical
miles from the coast and close to the 50 m iso-
baths (Figure 1). Its hydrographical regime has
been described as the transition between coastal
waters of high salinity and waters of the middle
shelf (Auad and Martos 2012). Occasionally the
site can receive less salty waters from the North,
leading salinity to be less than 31.0, particularly in
summer when the Río de la Plata reaches its max-
imum southern extension (Carreto et al. 1995). A
marked seasonal cycle typical of temperate
regimes has been observed at the EPEA. Sea sur-
face temperature varies between 10 °C and 21 °C
and salinity values vary from 33.5 to 34.1 (Carreto
et al. 2004; Lutz et al. 2006; Silva 2009; Ruiz
2018). The phytoplankton community reaches its
maximum biomass during winter, dominated
mainly by micro planktonic diatoms (20-200 µm)
(Negri and Silva 2011), while in summer the ultra-
phytoplankton fraction (less than 5 μm in diame-
ter) makes the major contribution to total phyto-
plankton biomass (Silva et al. 2009).
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RUIZ ET AL.: THE COLOR OF EPEA
Sampling and determinations at EPEA station
The study period considered in this work was
January 2000-December 2017 with a monthly
sampling frequency (with gaps), covering 119
visits to EPEA, performed in different scientific
research vessels from the Instituto Nacional de
Investigación y Desarrollo Pesquero (INIDEP),
the Navy and the Naval Prefecture of Argentina.
Not all variables were obtained in all cruises. For
this work we used data from samples collected at
5 m depth.
Chlorophyll-a total concentration (Chl
T
)
Water samples were collected at 5 m depth
using a Niskin bottle. A total of 119 water sam-
ples for Chl
T
determination were collected in dark
bottles and immediately filtered after collection
on glass microfiber filters, Grade GF/F 0.7 μm,
under dim light and low pressure (< 35 kPa). Fil-
ters were kept in liquid nitrogen (-195.8 °C) and
in an ultrafreezer (-86 °C) until analysis. For the
determination Chl
<5
, water samples were pre-fil-
tered through a 5 µm pore Nuclepore membrane
filters and then the same procedure as for the Chl
T
was applied to the filtrate. In the laboratory, Chl
T
and Chl
<5
were determined using a spectrofluo-
rometer (Perkin Elmer LS3) following the Holm-
Hansen et al. (1965) method for samples collect-
ed between 2000-2005 and a modified version
according to Lutz et al. (2010) since 2006.
Particulate absorption
Samples for determination of absorption spec-
tra of total particulate material were collected, fil-
tered and preserved following the same procedure
described for Chl
T
. A total of 110 samples were
analyzed during 2000-2017 using a spectropho-
tometer (Shimadzu UV-210-A), placing filters
close to the photomultiplier for samples collected
until 2006, and on a spectrophotometer (Shi-
madzu UV-2450) with an integrating sphere from
2006 onwards, following the quantitative filter
technique (Mitchell 1990), and using the amplifi-
208
MARINE AND FISHERY SCIENCES 33 (2): 205-225 (2020)
Figure 1. ‘Estación Permanente de Estudios Ambientales’ (EPEA), 38° 28′ S-57° 41′ W.
42°
41°
40°
39°
38°
37°
36°
35°
S
EPEA
W 61° 59° 57° 55° 53°
Mar del Plata
Atlantic Ocean
Río de la Plata
50 m
100 m
200 m
Study
area
N
cation factors of Hoepffner and Sathyendranath
(1992). Then, the method of Kishino et al. (1985)
was used to determine the a
NAP
( λ ) spectrum and
a
Phy
( λ ) was estimated by subtracting a
NAP
( λ )
from a
p
( λ ). More details can be found elsewhere
(Lutz et al. 2006; Ruiz 2018). The specific
absorption coefficient of phytoplankton in the
blue, which is a
Phy
(443) normalized by Chl
T
(a
B
Phy
(443), m
2
mg
-1
), and the ratio of the absorp-
tion in the blue to the red ([a
Phy
(443)/a
Phy
(676)])
were derived from a
Phy
( λ ) spectra.
Chromophoric dissolved organic matter (CDOM)
For the determination of CDOM absorption
spectra, a total of 78 seawater samples were col-
lected directly from the Niskin bottle into acid-
washed transparent borosilicate bottles with
teflon lids, and kept in the dark at 4 °C until
scanned at the laboratory (usually within 1 to 3
days after each cruise). Samples were filtered
through pre-combusted glass microfiber filters
Grade GF/F 0.7 μm at 450 °C during 3.5 h, and
the a
CDOM
( λ ) of the filtrate determined in a UV-
VIS spectrophotometer (Shimadzu UV-210-A)
for samples collected until 2006 using 4 cm opti-
cal path quartz cuvettes (Lutz et al. 2006), and in
a UV-VIS spectrophotometer using 10 cm optical
path quartz cuvettes since 2006 until present
(Mitchell 1990; Ruiz et al. 2017).
Vertical profiles of conductivity-temperature-
depth (CTD)
CTD profiles in the water column were record-
ed at each cruise using a Seabird SBE19 or SBE
911 CTD, according to availability of the equip-
ment. Quality controlled temperature data
(processed by the Physical Oceanography Cabi-
net of INIDEP) was used to estimate the depth of
the thermocline (Z
dTdZ,
m), defined as the depth at
which the maximum value of the first derivative
of the temperature respect to depth, dTdZ, was
found. Note that this parameter is indicative of
the stratification-mixing state of the water col-
umn. The depth Z = 42 m was used as a fixed
limit, when the water column was completely
mixed, in order to avoid variability regarding the
deepest depth reached by the CTD.
In situ photosynthetically available radiation
(PAR)
A submersible radiometer (PUV-500/510B,
Biospherical Instrument) was deployed manually
by releasing a conductor cable to record the
downwelling irradiance integrated between 400-
700 nm (E
d
(PAR), μmol quanta m
-2
s
-1
) as a func-
tion of depth. The euphotic depth (Z
eu
, m) was
determined as the depth at which the closest value
to the 1% of the recorded E
0
(PAR) occurred.
When the water column was completely illumi-
nated and the 1% of E
0
(PAR) was not reached, Z
eu
was assumed to be 40 m.
Satellite photosynthetically available radiation
(PAR)
Monthly averages of incident solar radiation
were estimated using the standard photo-synthet-
ically available radiation (PAR) satellite product.
PAR product was retrieved from monthly com-
posite images collected by the Aqua Moderate
Resolution Imaging Spectroradiometer (MODIS)
at spatial resolution of 4 km, at Level 3 Standard
Mapped Image (Version R2014.0, Ocean Color
Website http://oceancolor.gsfc.nasa.gov). PAR
data was provided by the Remote Sensing Cabi-
net of INIDEP.
Statistical analysis
Descriptive statistics was performed on the
bio-optical properties and thermal stratification
parameters. Spearman correlations were used to
explore the relationship between the different
variables under study. Then, monthly averages
were plotted against the months to evidence sea-
sonal cycles. Values deviating > 2 standard devi-
ations (SD) from the mean were considered
‘extreme values’ or extreme events (Davies and
Gather 1993). Long term variability was assessed
209
RUIZ ET AL.: THE COLOR OF EPEA
by the Seasonal Mann Kendall Trend Test (SMK
test, Hirsch and Slack 1984), a non-parametric
test for seasonal data. For that, a FORTRAN rou-
tine implemented by Hernández and Mendiolar
(2018) was used. Values higher than mean > 2 SD
were excluded of the trend calculation for each
variable.
RESULTS
Bio-optical properties and thermal stratifica-
tion parameters
The thermal classification criterion proposed
by Baldoni (2010) was applied to identify season-
al differences in each bio-optical property. It can
be observed that all properties showed a broad
range in their values, mainly attributed to season-
al variations, but also to the occurrence of special
events (Table 1). Phytoplankton absorption coef-
ficient presented a high standard deviation rela-
tive to the mean value. On average, the contribu-
tion of the small fraction of phytoplankton (quan-
tified as %Chl
<5
) to the total concentration of
chlorophyll was not negligible.
Annual cycle of bio-optical properties and
thermal stratification parameters
Incident PAR (estimated by the satellite prod-
uct) at EPEA reaches a maximum average value
in December and a minimum in June (Figure 2),
denoting a sinusoidal cycle expected for a middle
latitude site in the Southern hemisphere. Variabil-
ity during winter months was notoriously smaller
than during the rest of the year. Correspondingly,
light penetration is maximum in the warm period
(Z
eu
= 31.70 ± 8.02), reaching depths close to the
bottom of the water column in January, and is
minimum in the cold period (Z
eu
= 24.78 ± 5.01;
Figure 2). Since light penetration is attenuated by
OACs present in the water column, Z
eu
shows an
opposite sinusoidal pattern distorted respect to
the observed in incident PAR cycle. On the other
hand, the water column is homogeneous in win-
ter, and a thermocline starts to develop in spring
reaching its shallowest depths in summer (aver-
age for December Z
dTdZ
= 27 ± 8 m; Figure 3).
Variability of Z
dTdZ
is notoriously higher during
the cold to warm and warm periods than during
the warm to cold and cold periods.
EPEA is characterized by optically complex
waters during the whole annual cycle, with
CDOM as the main OAC contributing to total
absorption (Figure 4). Phytoplankton biomass at
EPEA, here estimated by Chl
T
, had an annual
mean of 1.162 ± 1.019 mg m
-3
, with higher values
during the cold period (Chl
T
= 1.49 ± 1.14), and
lower during the warm period (Chl
T
= 0.89 ±
0.89), although dispersion is high (Figure 5).
Chl
<5
contributed on average 45% to Chl
T
and
mean monthly values were relatively similar
throughout the annual cycle (Table 1; Figure 6).
Specific absorption coefficient of phytoplankton
(a
B
Phy
(443)) and the ratio of absorption in the
blue over the red [a
Phy
(443)/a
Phy
(676)] carry
information regarding the packaging effect.
Although both parameters followed the same pat-
terns, the latter showed a clearest feature of
increase towards summer (Figure 7), when small
cells are predominant and they are photo-accli-
mated to high incident light (Silva et al. 2009).
Relationships between bio-optical and physi-
cal properties
Spearman rank correlations (rho) were com-
puted in order to explore the relationship between
bio-optical and physical properties at EPEA
(Table 2). Temperature was positively correlated
with Z
eu
and negatively correlated with Z
dTdZ
.
These relationships showed that as the spring pro-
gresses, the increasing incident irradiance and
hence the increase in air temperature, induced the
warming of the upper sea layer and, consequent-
ly, the thermal stratification (also denoted by the
210
MARINE AND FISHERY SCIENCES 33 (2): 205-225 (2020)
211
RUIZ ET AL.: THE COLOR OF EPEA
Table 1. Descriptive statistics of bio-optical properties and thermal stratification parameters estimated at EPEA during 2000-2017. For Z
dTdZ
and Z
eu
threshold
maximum depths were set at 42 and 40 m respectively. Temperature corresponds to sampling depth Z = 5 m. Numbers between brackets indicate the
months included in each thermal period according to Baldoni (2010). Temp.: temperature, RBR: [a
Phy
(443)/a
Phy
(676)].
Warm period (12-1-2-3) Warm-cold transition (4-5) Cold period (6-7-8) Cold-warm transition (9-10-11)
Mean ± SD Range N Mean ± SD Range N Mean ± SD Range N Mean ± SD Range N
Temp. 19.48 ± 1.81 14.29-23.07 45 16.99 ± 1.25 15.11-18.79 14 12.09 ± 1.46 10-16 26 11.95 ± 1.65 9.68-15.71 33
Chl
T
0.89 ± 0.89 0.11-5.38 45 1.18 ± 0.61 0.21-2.42 15 1.49 ± 1.14 0.58-6.42 26 1.27 ± 1.17 0.32-6.13 33
Chl
<5
0.41 ± 0.52 0.03-2.63 35 0.51 ± 0.49 0.08-1.94 15 0.50 ± 0.29 0.08-1.18 21 0.57 ± 0.48 0.06-1.93 28
% Chl
<5
48.23 ± 23.02 19-100 35 40.27 ± 22.71 14-100 15 41.04 ± 22.34 6-74 21 47.54 ± 25.36 10-93 28
a
Phy
(443) 0.04 ± 0.04 0.01-0.27 41 0.04 ± 0.01 0.02-0.06 14 0.04 ± 0.01 0.02-0.06 23 0.08 ± 0.17 0.01-0.81 30
a
NAP
(443) 0.02 ± 0.02 0-0.07 41 0.03 ± 0.01 0.01-0.05 14 0.03 ± 0.02 0.01-0.10 23 0.02 ± 0.01 0-0.07 30
a
CDOM
(443) 0.07 ± 0.03 0.02-0.16 28 0.06 ± 0.03 0.02-0.13 13 0.06 ± 0.03 0.01-0.14 14 0.06 ± 0.02 0.02-0.1 21
a
B
Phy
(443) 0.07 ± 0.05 0.01-0.24 41 0.04 ± 0.03 0.02-0.14 14 0.03 ± 0.02 0.01-0.07 23 0.04 ± 0.03 0.01-0.13 30
RBR 2.78 ± 0.57 1.86-5.17 41 1.97 ± 0.25 1.48-2.27 14 2.08 ± 0.36 1.57-3.05 23 2.35 ± 0.36 1.65-3.09 30
Z
dTdZ
31.42 ± 7.75 9-42 45 39.93 ± 3.35 33-42 15 41.5 ± 1.3 36-43 26 35.88 ± 10.09 5-42 33
dT/dZ -1.21 ± 0.94 -3.94-0 45 -0.12 ± 0.39 -1.49-0 15 0 ± 0 -0.01-0.0 26 -0.17 ± 0.32 -1.32-0 33
Z
eu
31.70 ± 8.02 11.1-40 34 25.98 ± 5.63 20.1-38.9 14 24.78 ± 5.01 14.0-33.8 18 29.31 ± 6.71 15.5-39.6 25
positive correlation between Z
eu
and dTdZ). In
turn, Z
eu
showed a significant negative correla-
tion with Z
dTdZ
, that is, the more mixed the water
column, the weaker the stratification and the shal-
lower the light penetration.
Chl
T
had a significant negative correlation with
temperature, dTdZ, Z
eu
, a
B
Phy
(443) and [a
Phy
(443)/
a
Phy
(676)], while it was positively correlated with
Z
dTdZ
. These relationships indicated that phyto-
plankton biomass tended to be higher during win-
212
MARINE AND FISHERY SCIENCES 33 (2): 205-225 (2020)
Figure 2. Monthly satellite incident PAR irradiance (black squares) and monthly averages Z
eu
(open circles) at EPEA for 2003-
2017. Purple circles indicate extreme Z
eu
values (> 2 SD), not used in the calculation of the means. Bars indicate SD.
Figure 3. Z
dTdZ
for 2000-2017. Black circles represent monthly averages. Bars indicate SD. Purple circles indicate extreme val-
ues (> 2 SD), not used in the calculation of the means.
60
50
40
30
20
10
0
10
20
30
40
Jan. Feb. Mar. Apr. May Jun. Jul. Aug. Sep. Oct. Nov. Dec.
Z
eu
(m)
E
0
(PAR) (M quanta m d)
-2 -1
Month
0
5
10
15
20
25
30
35
40
45
Jan. Feb.Mar. Apr.May Jun. Jul. Aug.Sep. Oct. Nov.Dec.
Z
dTdZ
(m)
Month
ter, mainly due to the presence of larger cells with
lower light absorption efficiency and greater pack-
aging effect coupled with a mixed water column
and less light penetration. This interpretation is
consistent with the negative correlations found
between a
B
Phy
(443) and [a
Phy
(443)/a
Phy
(676)]
with Z
dTdZ
, and positive correlation with dTdZ and
Z
eu
. Regarding the relationships with the OACs,
Chl
T
was more positively correlated with
a
Phy
(443) than with a
NAP
(443) and non-correlated
213
RUIZ ET AL.: THE COLOR OF EPEA
Figure 4. Contribution to total absorption coefficient at 443 nm of optically active components (phytoplankton, NAP and
CDOM) expressed as percentage in a ternary plot.
Figure 5. In situ Chl
T
for 2000-2017. Black circles represent monthly averages. Bars indicate SD. Purple circles indicate extreme
values (> 2 SD), excluded from the calculation of the means.
20
40
60
80
100
20
40
60
80
100
20
40
60
80
100
PHY
CDOM NAP
7
6
5
4
3
2
1
0
Jan. Feb.Mar. Apr.May Jun. Jul. Aug.Sep. Oct. Nov.Dec.
Chl
T
(m )g m
-3
Month
with a
CDOM
(443), which was expected in part
since a
NAP
(443) increased with mixing also due to
resuspension of bottom material. In turn,
a
CDOM
(443) was not correlated with stratification
parameters, suggesting an independent behavior of
the mixing-stratification cycle at EPEA station.
%Chl
<5
showed only a weak positive signifi-
cant correlation with Z
eu
, dTdZ and [a
Phy
(443)-
/a
Phy
(676)], suggesting that when light penetra-
tion is deeper and stratification stronger at
EPEA, the percentage of smaller cells tended to
increase.
214
MARINE AND FISHERY SCIENCES 33 (2): 205-225 (2020)
Figure 6. Percentage of Chl
<5
over Chl
T
for 2000-2017. Black circles represent monthly averages. Bars indicate SD. Purple cir-
cles indicate extreme values (> 2 SD), excluded from the calculation of the means.
Figure 7. Values of [a
Phy
(443)/a
Phy
(676)] for 2000-2017. Black circles represent monthly averages. Bars indicate SD. Purple cir-
cles indicate extreme values (> 2 SD), excluded from the calculation of the means.
%Chl
<5
100
80
60
40
20
0
Jan. Feb. Mar. Apr.May Jun. Jul. Aug.Sep. Oct. Nov.Dec.
Month
5
4
3
2
1
Jan. Feb. Mar. Apr. May Jun. Jul. Aug. Sep. Oct. Nov.Dec.
a (443)/a (676)
Phy Phy
Month
Inter-annual variations in bio-optical proper-
ties and extreme events
Time series of bio-optical observations
throughout the study period (2000-2017) reflect-
ed the repetition of seasonal cycles as well as the
occurrence of extreme events (Figures 8, 9 and
10) which were associated to specific events
involving an exceptional increase in phytoplank-
ton abundance. An extremely high Chl
T
value of
6.420 mg m
-3
(the highest for the entire time
series) was recorded in June 2001, but unfortu-
215
RUIZ ET AL.: THE COLOR OF EPEA
Table 2. Spearman correlation coefficients between bio-optical and physical properties at EPEA. Spearman coefficient of corre-
lation (rho), probability (p) and data number (n) used are written from top to bottom. Temp.: temperature, RBR:
[a
Phy
(443)/a
Phy
(676)]. Bold values are significant at a α=0.05 confidence level.
Chl
T
a
NAP
(443) a
Phy
(443) a
B
Phy
(443) RBR a
CDOM
(443) Z
dTdZ
dTdZ Z
eu
%Chl
<5
Temp. -0.307 -0.117 0.016 0.391 0.500 0.031 -0.505 0.588 0.311 0.104
0.000 0.224 0.869 0.000 0.000 0.785 0.000 0.000 0.003 0.295
118 109 109 109 109 77 118 118 91 102
Chl
T
0.238 0.584 -0.639 -0.365 0.229 0.340 -0.454 -0.647 -0.061
0.012 0.000 0.000 0.000 0.044 0.000 0.000 0.000 0.542
110 110 110 110 78 119 119 92 103
a
NAP
(443) 0.336 0.007 -0.233 0.137 0.193 -0.361 -0.638 -0.404
0.000 0.945 0.014 0.232 0.043 0.000 0.000 0.000
110 110 110 78 110 110 90 99
a
Phy
(443) 0.136 -0.093 0.230 0.150 -0.178 -0.607 -0.031
0.157 0.335 0.043 0.117 0.062 0.000 0.762
110 110 78 110 110 90 99
a
B
Phy
(443) 0.449 -0.075 -0.386 0.475 0.268 -0.061
0.000 0.513 0.000 0.000 0.011 0.551
110 78 110 110 90 99
RBR 0.022 -0.610 0.661 0.468 0.206
0.848 0.000 0.000 0.000 0.040
78 110 110 90 99
a
CDOM
(443) -0.045 0.004 -0.209 0.002
0.693 0.972 0.072 0.987
78 78 75 77
Z
dTdZ
-0.704 -0.392 -0.095
0.000 0.000 0.341
119 92 103
dTdZ 0.536 0.200
0.000 0.043
92 103
Z
eu
0.316
0.002
91
nately no bio-optical data is available for that
sampling. In November 2005 an event character-
ized by values of Chl
T
= 6.130 mg m
-3
, a
Phy
(443)
= 0.811 m
-1
and a
NAP
(443) = 0.0128 m
-1
was
observed. In December 2008 another maximum
of phytoplankton occurred, characterized by high
values of chlorophyll concentration and OACs
absorption (Chl
T
= 5.377 mg m
-3
, a
Phy
(443) =
0.266 m
-1
and a
NAP
(443) = 0.063 m
-1
). The high
absorption by OACs attenuated the light produc-
ing the shallowest Z
eu
registered at EPEA (Z
eu
=
11.1 m). Interestingly, in the following month
(January 2009) stratification intensified reaching
an extreme value of dTdZ = -2.9 and Z
dTdZ
= 24.0
m, while Chl
T
decreased up to 0.353 mg m
-3
and
the ratio [a
Phy
(443)/a
Phy
(676)] increased to 3.66,
a rather high value denoting a change in the phy-
toplankton composition. In turn, a
NAP
(443) and
a
CDOM
(443) continued to be high (0.06 m
-1
and
0.096 m
-1
, respectively), probably as a conse-
quence of the bloom decay. Finally, in November
2016 another extreme increase in phytoplankton
occurred, evidenced by both the high values
of Chl
T
and a
Phy
(443) of 4.163 mg m
-3
and
0.527 m
-1
respectively. Possibly other extreme
events have occurred at EPEA in between our on-
site sampling.
Trends in bio-optical and physical properties
for the period 2000-2017
Chl
T
and Chl
<5
showed significant increasing
216
MARINE AND FISHERY SCIENCES 33 (2): 205-225 (2020)
Figure 8. Inter-annual distribution of coefficients of light absorption at 443 nm by phytoplankton [a
Phy
(443)], non-algal particles
[a
NAP
(443)], and CDOM [a
CDOM
(443)] estimated for 5 m samples at EPEA for the period 2000-2017. Purple circles indi-
cate extreme values (> 2 standard deviations).
0.16
0.14
0.12
0.10
0.08
0.06
0.04
0.02
0.00
0.10
0.08
0.06
0.04
0.02
0.00
0.80
0.60
0.40
0.20
0.09
0.06
0.03
0.00
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
2010
2011
2012
2013
2014
2015
2016
2017
2018
Serial years
a (443)
Phy
[m ]
-1
a (443)
NAP
[m ]
-1
a (443)
CDOM
[m ]
-1
trends (Table 3; Figures 11 and 12). Percentage of
Chl
<5
also showed a significant positive trend
(Figure 13), in agreement with the significant
positive trend in the pico-phytoplankton fraction
observed at EPEA (Silva, pers. comm.). On the
other hand, the Seasonal Mann-Kendal test
(SMK) revealed that the specific absorption coef-
ficient of phytoplankton, a
B
Phy
(443), decreased
significantly during the same period (Figure 14).
This trend appears to be simply governed by the
increasing trend in chlorophyll, since an increase
in pico-phytoplankton is expected to be reflected
in an increase in the efficiency of light absorption
per unit chlorophyll. The rest of properties stud-
ied didn’t show any significant trend of change
during the period analysed (Table 3).
DISCUSSION
Changes in the incident irradiance at EPEA
seem to be the main driver of the seasonal forma-
tion of a warmer less dense upper layer separated
by a thermocline from deep colder waters (Ruiz,
2018; Luz Clara, pers. comm.). Basic description
of phytoplankton growth cycle in temperate seas
explains that blooms occur in spring as the water
column stratifies, allowing cells to remain in the
lit zone at the same time that they have plenty of
nutrients, which were replenished by mixing dur-
ing the previous winter (Riley 1946). Neverthe-
less, at EPEA, except for special events, phyto-
217
RUIZ ET AL.: THE COLOR OF EPEA
Figure 9. Inter-annual distribution of concentration of chlorophyll-a Chl
T
, percentage of Chl
<5
from Chl
T
, and ratio
[a
Phy
(443)/a
Phy
(676)] estimated for 5 m samples at EPEA for the period 2000-2017. Purple circles indicate extreme val-
ues (> 2 standard deviations).
5
4
3
2
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
2010
2011
2012
2013
2014
2015
2016
2017
2018
Serial years
100
80
60
40
20
0
7.0
6.0
5.0
4.0
2.7
1.8
0.9
0.0
Chl
T
[]mg m
-3
%Chl
<5
a (443)/a (676)
Phy Phy
218
MARINE AND FISHERY SCIENCES 33 (2): 205-225 (2020)
Figure 10. Inter-annual distribution of euphotic depth, Z
eu
, the depth at which the maximum value of the derivate of temperature
with respect to depth (dT/dZ) occurred, Z
dTdZ
, and the strength of the dT/dZ at EPEA for the period 2000-2017. Purple
circles indicate extreme values (> 2 standard deviations).
0
10
20
30
40
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
2010
2011
2012
2013
2014
2015
2016
2017
2018
Serial years
0
10
20
30
40
0
-1
-2
-3
-4
Z
eu
(m)
Z (m)
dTdT
dT/dT
Table 3. Values of p obtained from the Seasonal Mann-Kendal test (SMK) trend analysis for bio-optical properties and thermal
stratification parameters at EPEA for the period 2000-2017. Values marked in bold are significant at a α=0.05 confi-
dence level.
Property Trend sign p SMK
Chl
T
Positive 0.00013
Chl
<5
Positive < 0.00001
%Chl
<5
Positive < 0.00002
a
Phy
(443) 0.5945
a
NAP
(443) 0.1878
a
CDOM
(443) 0.2167
a
B
Phy
(443) Negative < 0.00003
a
Phy
(443)/a
Phy
(676) 0.5272
Z
dTdZ
0.2659
Z
eu
0.7282
plankton biomass as indicated by Chl
T
does not
follow this dynamic, since Chl
T
tends to be higher
at the end of winter. This could be due to the fact
that bottom depth (~ 48 m) is shallow enough to
allow phytoplankton cells to be brought up by
mixing to the lit layer with a frequency that per-
mits them to grow, even during the darkest
months at EPEA. Incident irradiance starts
increasing in August, being the trigger for a rela-
tive increment in phytoplankton growth, whose
biomass starts to decrease as the stratification
progresses and nutrients are consumed (Negri et
219
RUIZ ET AL.: THE COLOR OF EPEA
Figure 11. Annual mean Chl
T
anomalies for the period 2000-2017.
Figure 12. Annual mean Chl
<5
anomalies for the period 2000-2017.
-0.5
-0.4
-0.3
-0.2
-0.1
0.0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017
Annual mean anomaly
Year
p 1e-05<
2001 2002 2003 2004 2005 2006
2007
2008
2009
2010 2011 2013 2014 2015 2016
2017
Annual mean anomaly
Year
2012
0.60
0.55
0.50
0.45
0.40
0.35
0.30
0.25
0.20
0.15
0.10
0.05
0.00
-0.05
-0.10
-0.15
-0.20
-0.25
-0.30
2000
p 1e-05<
al. 2003; Carreto et al. 2004). Relationships
among properties studied add evidence to this
explanation since Chl
T
was significantly and pos-
itively correlated with Z
dTdZ
and significantly and
negatively correlated with Z
eu
.
It is known that small cells are more efficient
to assimilate nutrients when these are scarce, due
to their higher surface to volume ratio (Richard-
son et al. 1983; Chisholm 1992), and at the same
time of being better suited to cope with high irra-
diances, which may cause photo-inhibition due to
the higher proportion of photo-protective pig-
220
MARINE AND FISHERY SCIENCES 33 (2): 205-225 (2020)
Figure 13. Annual mean %Chl
<5
anomalies for the period 2000-2017.
Figure 14. Annual mean a
B
Phy
(443) anomalies for the period 2000-2017.
-0.020
-0.015
-0.010
-0.005
0.000
0.005
0.010
0.015
0.020
2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017
Annual mean anomaly
Year
p 3e-05<
-20
-15
-10
-5
0
5
10
15
20
25
2000 2002 2004 2005 2006
2007
2008
2009
2010 2011 2012 2013 2014 2015 2016
2017
Annual mean anomaly
Year
p 5e-05<
20032001
ments, such as zeaxanthin in Synechococcus.
Higher blue to red ratios have been attributed to
the dominance of phytoplankton populations with
small cell sizes and photoacclimated to high light
(Sosik and Mitchell 1995; Millán-Núñez et al.
2004). At EPEA station, this photoacclimation
strategy is evidenced in higher values of blue to
red absorption ratio [a
Phy
(443)/a
Phy
(676)] during
summer and also in the correlation with the shal-
lower and stronger stratification and deeper
euphotic depth. A similar but not as conspicuous
pattern was observed for a
B
Phy
(443), a bio-optical
property indicative of absorption efficiency
which is usually negatively correlated with cell
size. Thus, it is possible to discern the link of bio-
optical properties following main seasonal varia-
tions in phytoplankton types and how they pho-
toacclimate, even at this optically complex
coastal site.
Variations in the annual cycle of absorption
coefficients of OACs at EPEA station for the peri-
od 2000-2017 have been previously analyzed
(Lutz et al. 2006; Ruiz 2018). From those studies
it became clear that a
CDOM
(443) is the OAC with
largest values of absorption at all months (with
peaks in fall and summer), followed by a
Phy
(443)
(with almost no variation throughout the year),
and finally a
NAP
(443) which is maximum in win-
ter. The fact that at EPEA a
Phy
(443) did not show
seasonal variability as it was in the case for Chl
T
could be due to the fact that the spectral absorp-
tion coefficient of phytoplankton is a complex
bio-optical property that represents the sum of the
absorption by different pigment-protein complex-
es present in different phytoplankton species that
make up a given sample. However, a
Phy
(443) still
was correlated to Chl
T
, and it showed extreme
values in events when phytoplankton biomass
was high. As mentioned, the blue to red absorp-
tion ratio [a
Phy
(443)/a
Phy
(676)] is a property that
changes both with the phytoplankton community
and with how the cells were photoacclimated,
with the advantage that as being dimensionless it
emphasizes these variations in the absorption
spectral shape rather than in its magnitude (Sosik
and Mitchell 1995). At EPEA, the annual cycle of
[a
Phy
(443)/a
Phy
(676)] showed higher values dur-
ing the warm period; whether this suggests that
phytoplankton populations are mainly composed
of small cells (Negri and Silva 2003) or different
size cells which were photoacclimated to high
irradiances remains to be addressed.
Long term trends of change were observed both
for Chl
T
, Chl
<5
and %Chl
<5
. This fact could have
been exacerbated by the change in the extraction
method of the chlorophyll concentration determi-
nation that took place in 2006 at EPEA station
(from acetone 90% to methanol 100%), which is
more efficient in the case of smaller cells (Lutz et
al. 2010). Nevertheless, independent sources of
Chl
T
estimation (satellite) in the region also ren-
dered an increasing trend (Marrari et al. 2017).
However, despite the positive and significant cor-
relation observed between Chl
T
and a
Phy
(443),
long-term changes were not reflected in a signifi-
cant trend of a
Phy
(443). This could have been pos-
sibly related to the wide seasonal variability of
this coefficient and the fact that absorption coeffi-
cients are complex properties encompassing many
factors. In agreement with the positive significant
trend in Chl
<5
, the picoplankton and nanoplankton
size fractions showed significant positive trends
(Silva, pers. Comm.). Contrary to what could be
expected from these observations, we have
observed a significant decreasing trend in the total
a
B
Phy
(443) (which is a lineal combination of Chl
T
,
a
B
Phy
(443) = a
Phy
(443)/Chl
T
) and no trend in
[a
Phy
(443)/a
Phy
(676)].
A few special bloom events were observed at
EPEA, some of them associated with different
extraordinary physical conditions. In 2001, an
almost exclusively blooming of diatoms from the
nano and micro planktonic size fraction was
observed. In November 2005 a bloom of the
Genus Prymnesium sp. was identified, character-
ized by the absence of micro planktonic diatoms.
In December 2008, another maximum of phyto-
plankton occurred, which was associated with an
221
RUIZ ET AL.: THE COLOR OF EPEA
event of cold temperature and characterized by
the presence of atypical phytoplankton species for
the study site and the absence of micro planktonic
diatoms, which could be the reason why a relative
high a
Phy
(443) was observed for the recorded
Chl
T
(Negri et al. 2015). The bloom observed in
November 2016 was particular due to its high
concentration of nano planktonic dinoflagellates.
Whether the frequency of such events has been
increasing at EPEA is a question that we cannot
still assess upon our in situ database, mainly
given the unfortunate gaps in the sampling. Nev-
ertheless, in this work it has been shown that IOPs
did capture these special events, indicating that
satellite information should also be useful to
detect them, even considering the possible inac-
curacies of this data source for the study site
(Ruiz 2018; IOCCG 2020). Long term time series
of observations, either in situ or satellite, are not
exempt from changes in the methodologies or
from gaps in the sampling frequency. These two
factors, together with the autocorrelation and
decadal natural variability of oceanic ecosystems
challenge the unambiguous detection of a trend,
possibly driven by climate change, above the nat-
ural variability. It has been stated that time series
of about 40 years long would be necessary to dis-
tinguish a trend from natural variability, assuming
no gaps on the observational record (Henson et al.
2010). This is a condition that only very few eco-
logical time series are able to meet so far, which
points out the necessity of maintaining time series
to assess changes occurring in the marine envi-
ronment (O’Brien et al. 2017). Long-term in situ
bio-optical data is particularly scarce in the global
ocean. From the beginning of this time series to
the present, the technological capacity imple-
mented (ships, equipment, human resources) has
been improved, and despite the irregular sam-
pling frequency, this work based on the observa-
tions at EPEA emphasize the relevance of in situ
ecological time series to contribute to the under-
standing of coastal ecosystems dynamics in a
context of climate change.
CONCLUSIONS
Our results derived from almost two decades
of in situ observations at this coastal site in the
South Atlantic indicate an increasing trend in
chlorophyll-a concentration, possibly due to an
increase in the smaller fraction of phytoplankton.
Although the absorption coefficient of phyto-
plankton did not follow a significant trend, it did
represent the occurrence of special events of high
biomass, which is an encouraging result for the
use of satellite information at the study site. Two
main parameters of phytoplankton absorption, the
specific absorption coefficient of phytoplankton
a
B
Phy
(443) and the blue to red ratio
[a
Phy
(443)/a
Phy
(676)], follow an annual cycle
with high values in summer and low in winter,
according to the probable dominance of different
size cells and their expected acclimation to the
light regime. Though, a
B
Phy
(443) showed a trend
to decrease throughout the years, which is consis-
tent with the increase in Chl
T
, but how this is con-
nected to the increase in small cells should be fur-
ther investigated. An in depth study of the vari-
ability in the phytoplankton absorption spectral
shapes and its direct link to phytoplankton
species and their photoacclimation status would
be a next step at EPEA. Possible sources of
CDOM should also be explored, since it is a
major component absorbing light and was not
correlated to any of the variables studied.
ACKNOWLEDGEMENTS
This work was supported by INIDEP and
CONICET. The authors thank Daniel Cucchi
Colleoni for his collaboration on board and labo-
ratory analysis since the beginning of the time
series. Special thanks to Daniel Hernández and
Manuela Mendiolar who provided statistical
222
MARINE AND FISHERY SCIENCES 33 (2): 205-225 (2020)
advice, and to Ezequiel Cozzolino who provided
satellite data. The authors are also thankful to the
crew and captains of all the vessels used to
achieve the sampling at EPEA time series and to
the anonymous reviewers. INIDEP contribution
no 2224.
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