Regional Studies in Marine Science: R.L. Boufeniza, M.M. Alsahli, N.I. Bachari, F. Houma Bachari
Regional Studies in Marine Science: R.L. Boufeniza, M.M. Alsahli, N.I. Bachari, F. Houma Bachari
Regional Studies in Marine Science: R.L. Boufeniza, M.M. Alsahli, N.I. Bachari, F. Houma Bachari
article info a b s t r a c t
Article history: Quantifying phytoplankton and its changes in coastal waters is an important aspect of marine ecosys-
Received 25 March 2019 tems. Synoptic observations of phytoplankton communities became possible with remote sensing
Received in revised form 11 April 2020 technologies and spatial analysis methods. Using these advancements would assist the scientific
Accepted 8 May 2020
community to gain better understanding of marine ecosystem dynamics and consequently contribute
Available online 12 May 2020
in sustaining and maintaining these valuable ecosystems. Thus, this study aimed to evaluate the
Keywords: water quality and aquatic ecosystem status of Algiers Bay, Algeria, through the quantification of
Remote sensing diatoms and dinoflagellates species using in-situ measurements and Landsat images. We developed
GIS empirical models to assess phytoplankton abundance by comparing in-situ measurements of diatoms
Algae bloom and dinoflagellates with various spectral bands and band ratioing products derived from Landsat-8
Marine biogeography OLI images acquired in 4 April 2017 and 9 May 2018. The results showed a wide variation between
Mediterranean sea coastal and offshore stations. The number of diatoms was less than that of dinoflagellates. These two
Aquatic ecosystem
algae communities illustrated a different spectral behavior. Diatoms showed a significant relationship
with one of the ratioing products (i.e., log B7/log B2), whereas dinoflagellates exhibited an insignificant
relationship with the remotely sensed dataset. Also, we learned that the southeastern area of the bay
can be influenced by harmful algae blooms developed offshore because of hydrodynamic forces that
push these blooms toward this area of the bay.
© 2020 Elsevier B.V. All rights reserved.
https://doi.org/10.1016/j.rsma.2020.101311
2352-4855/© 2020 Elsevier B.V. All rights reserved.
2 R.L. Boufeniza, M.M. Alsahli, N.I. Bachari et al. / Regional Studies in Marine Science 36 (2020) 101311
The most common approach to observe diatoms and dinoflag- wastewater is still a significant issue due to the lack of effective
ellates is mainly through field sampling at defined locations treatment strategies and management of wastewater discharge
and subsequent laboratory analysis (Giardino et al., 2001). The at different flows (Seridi et al., 2007). These point and nonpoint
quantification of these species at larger geographical scales is sources of water pollution are disturbing Algiers Bay ecosystems
logistically difficult (Gobler et al., 2017; Ogashawara et al., 2014; and are believed to have a potential role in fluctuating phyto-
Shin et al., 2018). An alternative approach to overcome this issue plankton biomass (Morán et al., 2001; Raimbault et al., 1993;
is to use remote sensing imagery that can significantly estimate Taupier-Letage et al., 2003).
variations in density, size and pigment composition of species’ Phytoplankton biomass and communities within Algerian
cells from a synoptic perspective. Phytoplankton communities coastal waters were not significantly investigated (Illoul et al.,
influence the apparent optical properties (AOP) of seawaters that 2008). In the Algiers Bay, the most common species as reported
can be modeled using remote sensing imagery (Hoepffner and by Illoul et al. (2008) were diatoms and dinoflagellates, with a
Sathyendranath, 1993; Roesler et al., 1989; Ulloa et al., 1994). total of 14 toxic species, and 18 bloom-forming species identified.
Most of phytoplankton models were developed using Advanced Some phytoplankton species discovered in Algerian coastal wa-
Very-High-Resolution Radiometer (AVHRR), Sea-viewing Wide
ters, such as Alexandrium minutum, Dinophysis sacculus (Dinoflag-
Field-of-View Sensor (SeaWiFS), Moderate Resolution Imaging
ellates) and Pseudo-nitschia calliantha (Diatom) are considered as
Spectroradiometer (MODIS) and Geostationary Ocean Color Im-
toxin producers, whereas Lepidodinium chlorophorum (Dinoflag-
ager (GOCI). These sensors have spatial resolutions that range
ellate), Cyclotella meneghiniana (Diatom) and Holococcolithophora
from 250 to 1000 m. This coarse spatial resolution limits the use
sphaeroidea are bloom-forming species.
of these sensors in small coastal areas (Shin et al., 2018; Vincent
et al., 2004). Landsat-8 with high spatial and spectral resolutions
can be an alternative for these sensors in such areas. Landsat-8 3. Methodology
images have been efficiently applied in various aquatic studies
including phytoplankton monitoring (Bresciani et al., 2018; Wei Investigating phytoplankton biomass within Algiers Bay went
et al., 2019; Yadav et al., 2019). through seven stages (Fig. 2): in-situ data collection, laboratory
A comprehensive monitoring of phytoplankton communities analysis, geospatial data acquisition, image pre-processing, im-
in Algiers Bay using in-situ and remotely sensed data have not age processing, in-situ-satellite data matching up and statistical
been established yet. Thus, Landsat-8 images and in-situ data modeling. Phytoplankton algae samples were collected in the
were used in this study to understand the spatial and temporal Algiers Bay within ±2 h of Landsat-8 overpass. These samples
distributions of diatoms and dinoflagellates in Algiers Bay. The were analyzed in laboratory to quantify diatoms and dinoflag-
study objectives were to evaluate the water quality and aquatic
ellates cells using an inversed microscope. Geospatial data (GIS
ecosystem status through: (1) the quantification and identifica-
layers and Landsat-8 images) were used to model and map
tion of diatoms and dinoflagellates; and (2) estimation of tempo-
diatoms and dinoflagellates spatial and temporal patterns within
ral and spatial distributions by developing empirical models that
Algiers Bay. A shapefile of Algiers Bay boundary was downloaded
integrate in-situ measurements of diatoms and dinoflagellates
from the national map of National Institute for Cartography and
algae with various spectral bands and band combinations derived
Remote Sensing (NICRS) (http://www.inct.mdn.dz), whereas the
from the Landsat-8 OLI images in spring of 2017 and 2018.
bay’s bathymetry dataset was obtained from the Houma et al.
2. Study area (2006) study. Cloud-free Landsat-8 images of the study area
were downloaded from the US Geological Survey (USGS) website
Algeria faces the Mediterranean Sea with a coast extending to (https://www.usgs.gov). These images were radiometrically and
about 1300 km. Algiers Bay is semi-circular shape with an average atmospherically corrected during the pre-processing stage. Cor-
depth of 38 m located in the middle of this coast at coordinates rected images with near-concurrent in-situ data were matched
of 36.82◦ North and 03.19◦ East. The bay has an area of 180 km2 to investigate the relationship between water surface reflectance
extending 18 km from East to West and 7 km from North to from different spectral regions and the phytoplankton cell density
South. The bay is surrounded by the Mitidja plain in the South, (i.e., diatoms and dinoflagellate algae). The following subsections
tip of the Pescade (Raïs Hamidou) in the West and Cape Matifou described the methodology in detail.
(El Marsa) in the East (Fig. 1).
Algiers Bay has a significant value to the local and national 3.1. In-situ measurement
socio-economic developments. It is highly populated coast that
hosts more than 3 million people (10% of the Algerian popula-
Phytoplankton algae samples were collected in the Algiers Bay
tion). The bay experiences various anthropogenic activities that
on 4 April 2017 and 9 May 2018 within ±2 h of the satellite
contribute in degrading the bay’s ecosystems through point and
overpass. Such a narrow time window between in-situ data col-
nonpoint sources of water pollution. The coastal zone of Algiers
Bay hosts about one fourth of national companies and Algiers lection and satellite overpass is essential to minimize the effect
Port, one of the most important ports in the country. The bay of environmental condition changes over the time (Butt and
receives industrial water from Wadi El-Hamiz, Wadi El-Harrach Nazeer, 2015; Mouw et al., 2015). The phytoplankton samples
and El Hamma seawater desalination plants (Illoul et al., 2008). were taken from the surface water (1 m) using Niskin bottle of 5 L
Also, the coastal zones experienced over the last decades many at 14 sites in the first voyage and 16 sites in the second voyage
coastal management projects that have contributed significantly (Fig. 1). The water samples were filled in 250 ml opaque and clean
in increasing the amount of nutrients and suspended sediments polypropylene bottles using a tube to protect the planktonic cells
(Woodcock et al., 2008). from deterioration and to take a representative sample. Water
Wastewater is another significant factor that contributes in samples were fixed with acidic Lugol’s solution that changed the
degrading the bay’s water quality by increasing concentrations water color to light brown. The samples were stored at 4 ◦ C in
of organic matter, suspended solids, and chemical and biologi- coolers, and then taken to the laboratory for analysis. The voyages
cal pollutants. Although the Algerian government spent consid- were conducted in favorable weather conditions with clear skies
erable efforts to protect the environments of this region, the and calm seas.
R.L. Boufeniza, M.M. Alsahli, N.I. Bachari et al. / Regional Studies in Marine Science 36 (2020) 101311 3
3.1.1. Phytoplankton quantification Mcmanus and Katz, 2009; Palmer and Maloney, 1954). Among
Several techniques can be used to quantify and identify phy- these techniques, we followed the standard guide for phytoplank-
toplankton cell densities (Downing and Rigler, 1984; Hasle, 1978; ton counting by inverse microscopy (SGPCIM) - Standard NF EN
Havens et al., 1996; Hötzel and Croome, 1999; Lund et al., 1958; 15204, 2006 (AFNOR, 2006). The guide is based on the Utermöhl
4 R.L. Boufeniza, M.M. Alsahli, N.I. Bachari et al. / Regional Studies in Marine Science 36 (2020) 101311
method (Utermöhl, 1958) and adopted by many marine and noise. Pixels over shallow waters (<8 m in depth) were removed
coastal monitoring programs worldwide (Downing and Rigler, from the analysis to minimize the bottom reflectance (Lodhi,
1984; Havens et al., 1996). We counted and identified planktonic 2002). Excluding these invalid pixels reduced the uncertainty of
cells (diatoms and dinoflagellates) through systematic identifi- modeling phytoplankton cell density.
cation procedures using an inversed (optical) microscope. Cell
counting was performed with horizontal scanning in a prepared 3.3. Comparison of in-situ and satellite data
sedimentation tank (2.5 to 10 ml after a settling period of 48
h). The results were expressed in cells density per volume (Cell In-situ measurements taken within two hours or less from
l−1 ) (Barton et al., 2013; Druart and Rimet, 2008; Throndsen, the satellite overpass were matched with the processed Landsat
1995). The process of counting and identification took 20 days images by extracting the pixel values of 3-by-3 window centered
from the date of the sampling voyage, following the work of at each in-situ point. The mean of each extracted window was
Laplace-Treyture et al. (2009) work. computed using a filtering approach described by Bailey and
Werdell (2006). The filtered mean is mathematically expressed
3.2. Remote sensing data by the following equation:
.5 ∗ σ − X ) < Xi < (1.5 ∗ σ + X )
∑
3.2.1. Landsat-8 satellite imagery i (1
filtered Mean = (1)
Two Landsat-8 images downloaded on 4 April 2017 and 9 May n
2018 were used to model phytoplankton cell density within Al- where X and σ are the mean and the standard deviation of
giers Bay water as Landsat imagery was successfully used in mea- the nine-pixel values from each window. n is the number of
suring phytoplankton abundance (Bresciani et al., 2018; Nazeer pixel values within ± 1.5 ∗ σ from the mean. The filtered mean
et al., 2017; Wei et al., 2019). Landsat-8 operated by USGS was was disregarded whenever n was less than five. This matching
launched on 11 February 2013 (Bonansea et al., 2018; Roy et al., approach was applied to the first seven bands (i.e., from coastal
2014). The satellite carries two sensors: The Operational Land aerosol to SWIR-2 band) of processed Landsat OLI images.
Imager (OLI) and the Thermal Infrared Sensor (TIRS) with a spatial
resolution of 30 m and 100 m, respectively (Olmanson et al., 3.4. Statistical analysis and spatial analyses
2016; Roy et al., 2014). The temporal resolution of Landsat-8 is
16 days, and its images are delivered in 16-bit unsigned integer The in-situ datasets were statistically summarized to explore
format in level 1. The landsat-8 OLI sensor has four visible bands, the phytoplankton species temporal variability. Also, the spatial
four near infrared bands, and one panchromatic band, whereas variability of diatoms was compared to dinoflagellate spatial vari-
TIRS has two thermal infrared bands (Msi et al., 2019; Pahlevan ability at study sites using Chi-square test. The relationship of
and Schott, 2013; Vanhellemont and Ruddick, 2014). Landsat- plankton (i.e., diatoms and dinoflagellate algae) cell density to the
8 images are distributed by USGS through their website (https: seven bands of processed Landsat OLI images was investigated
//www.usgs.gov). using the correlation coefficient and regression analysis. The re-
lationship was investigated by comparing in-situ observation to
3.2.2. Sentinel-2A satellite imagery reflectance values of each band and the products of ratioing
A Sentinel-2A image obtained on 15 May 2018 (6 days after these bands. Data transformations were applied for non-normally
the second voyage) was used for visual interpretation purposes distributed variables to meet linear regression assumptions. The
to track algae blooms. Sentinel-2A operated by European Space accuracy of models was evaluated using root mean squared error
Agency was launched on 23 June 2015 carrying Multispectral (RMSE) and mean absolute percent difference (MAPD). Also, the
Imager (MSI) that records 12 spectral bands from blue to short- spatial interpolation technique was used to estimate the spatial
wave near infrared (SWIR) spectrum with a spatial resolution and temporal distribution of dinoflagellates in spring 2017 and
ranging from 10 m to 60 m (www.sentinel.esa.int). The sensor 2018. All statistical analyses were preformed using IBM SPSS
has a red-edge band with a spatial resolution of 20 m that Statistics 24 (IBM Corp, New York, USA), whereas the spatial
allows detecting chlorophyll-a absorptions in case II waters, such analysis was conducted using QGIS 3.6.
as Algiers Bay (Dörnhöfer et al., 2016). Sentinel-2A images are
distributed through the Copernicus Open Access Hub website 4. Result and discussion
(https://scihub.copernicus.eu/).
The mean diatom and dinoflagellate cell densities in 2017 and
3.2.3. Image preprocessing 2018 were 5084, 1502, 15 589 and 21 655 Cell l−1 , respectively
Landsat-8 level 1 images were radiometrically and atmospher- (Table 1). Dinoflagellate cell densities were higher than diatom
ically corrected using ENVI 5.3. Row values (i.e., digital numbers) cell densities in all stations in 2017 and 2018. In general, phy-
of the images were converted to surface reflectance values. Then, toplankton cell densities in the northwestern side of the bay is
the dark object subtraction (DOS) method was used to atmo- lower than densities in the eastern side of the bay. The max-
spherically corrected images. This method is largely used due to imum diatom cell density was observed at station 16 in 2017,
its simplicity. The DOS-based approach assumes that the mini- whereas the maximum dinoflagellate cell density was observed
mum value of each band is zero (Nazeer et al., 2014; Norjamaki at station 16 in 2018 (Fig. 3). The spatial distributions of diatoms
and Tokola, 2007), and minimum values above zero occur due and dinoflagellates at the study sites exhibited a distinct pattern
to scattering. The scattering effects are minimized by subtracting that divided the bay into two zones as revealed by the Chi-
the minimum value from each pixel value in a corresponding square test: One in the northwestern area of the bay (zone1)
band (Chavez, 1989). This approach is very practical with the characterized by spatial dependency of the two species; and the
absence of atmospheric measurements and can provide accurate other in the southeastern area of the bay (zone 2) where the
results comparable to those provided by complicated atmospheric observed dinoflagellates density was higher than what was ex-
algorithms (Jensen, 2015). pected (Fig. 4). This can be explained by the hydrodynamic factors
Three types of pixels were excluded from the analysis during in Algiers Bay, such as drift current and swell that disperses
the image preprocessing stage: mixed pixels (inland-water pix- the seawater masses to the southeastern zone. Also, effluents
els), shallow-water pixels and incorrect pixels induced by sensors of the wastewater discharging from Wadi El Harrach (near to
R.L. Boufeniza, M.M. Alsahli, N.I. Bachari et al. / Regional Studies in Marine Science 36 (2020) 101311 5
Fig. 4. The distribution of chi-square for (log10 ) diatoms and dinoflagellates cell densities 2017 and 2018.
Table 3
Linear regression models between Operational Land Imager reflectance values and for all
phytoplankton cell densities in all stations.
Variable Equation RMSE MAPD r2 n
0.2592(LogB6/LogB3) + 0.4355 3.25 3.81 0.23
0.1345∗(LogB6/LogB4) + 0.7075 3.19 3.80 0.11
Log (phytoplankton) 0.2185∗(LogB7/LogB2) + 0.6903 3.04 3.76 0.17 30
0.3194∗Log(B2/B6) − 0.5264 4.34 4.09 0.13
0.2186∗Log(B4/B7) − 0.3825 4.33 4.09 0.17
In this study, we demonstrated the efficiency of using Landsat- their pigment concentrations, especially chlorophyll-a that signif-
8 images to model phytoplankton cell density. Landsat-8 OLI icantly contributes in changing AOP of water.
bands successfully captured the diatom cell density variations, The methodology used in this study to model phytoplankton
whereas dinoflagellate cell density exhibited insignificant rela-
tionship with OLI bands. The reason for this insignificant re- density can be applied in future investigations to include more
lationship was probably because almost half of dinoflagellate in-situ data. The proposed model can be improved by using more
species are heterotrophs whose abundance does not covary with in-situ observations well distributed over the year. Including a
R.L. Boufeniza, M.M. Alsahli, N.I. Bachari et al. / Regional Studies in Marine Science 36 (2020) 101311 7
Fig. 5. The relationship between diatoms and the band ratio (REF logB7/REF logB2).
Fig. 6. Predicted distributions of surface diatoms using the most accurate Landsat model: (A in Apr 04, 2017) and (B in May 09, 2018).
Table 4
Linear regression models between Operational Land Imager reflectance values and for dinoflagellates cell densities
in all stations.
Variable Equation RMSE MAPD r2 n
−1,1845(R5/R3) + 4,2606 0,726 2,700 0,189
Log (dinoflagellates) −2,4036(B3/B4) + 5,8196 0,728 2,701 0,185
0,19*log(B4/B6) + 3,6666 0,804 2,689 0,005
101,09*(B1/B3) + 32,22 80,821 105,339 0,100
Root (dinoflagellates) −82,494*(R5/R3) + 143,15 81,764 105,391 0,080 30
16,985Log(R4/R6) + 100,17 85,132 105,242 0,004
−977,43*(LogB5/LogB7) + 952,2 53,209 72,993 0,169
Root (dinoflagellates) 31,425*Log (B2/B4) + 62,55 57,466 72,827 0,032
4,3577*(B2/B4) + 60,541 57,478 72,826 0,031
8 R.L. Boufeniza, M.M. Alsahli, N.I. Bachari et al. / Regional Studies in Marine Science 36 (2020) 101311
Fig. 7. (A and B): phytoplankton bloom in the surface waters of Algiers Bay (09/05/2018), (C): Noctiluca scintillans algal blooms (small picture) and its color (large
picture) in the Algiers bay coastal water (May 2018) and (D): hydrodynamic of plankton bloom and suspended matter to the southeastern part of the Bay observed
by Sentinel-A2 in 15/5/2018 (R = Band4, G = Band3, B = Band2).
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and coastal monitoring programs. dust and wind on phytoplankton activities in the Arabian Gulf. In: 2012
IEEE International Geoscience and Remote Sensing Symposium. IEEE, pp.
CRediT authorship contribution statement 2571–2574. http://dx.doi.org/10.1109/IGARSS.2012.6350954.
Bailey, S.W., Werdell, P.J., 2006. A multi-sensor approach for the on-orbit
validation of ocean color satellite data products. Remote Sens. Environ. 102,
R.L. Boufeniza: Conceptualization, Software, Validation, For- 12–23. http://dx.doi.org/10.1016/j.rse.2006.01.015.
mal analysis, Writing - original draft. M.M. Alsahli: conceptual- Barton, A.D., Finkel, Z.V., Ward, B.A., Johns, D.G., Follows, M.J., 2013. On the roles
ization, Methodology, Writing - review & editing. N.I. Bachari: In- of cell size and trophic strategy in North Atlantic diatom and dinoflagellate
vestigation, Resources, Data curation. F. Houma Bachari: Project communities. Limnol. Oceanogr. 58, 254–266. http://dx.doi.org/10.4319/lo.
2013.58.1.0254.
administration,Supervision, Formal analysis. Bonansea, M., Ledesma, M., Rodriguez, C., Pinotti, L., 2018. Using new remote
sensing satellites for assessing water quality in a reservoir. Hydrol. Sci. J.
Declaration of competing interest http://dx.doi.org/10.1080/02626667.2018.1552001.
Bresciani, M., Cazzaniga, I., Austoni, M., Sforzi, T., Buzzi, F., Morabito, G.,
Giardino, C., 2018. Mapping phytoplankton blooms in deep subalpine lakes
The authors declare that they have no known competing finan-
from Sentinel-2A and Landsat-8. Hydrobiologia 824, 197–214. http://dx.doi.
cial interests or personal relationships that could have appeared org/10.1007/s10750-017-3462-2.
to influence the work reported in this paper. Butt, M.J., Nazeer, M., 2015. Landsat ETM+ Secchi Disc Transparency (SDT)
retrievals for Rawal Lake. Pak. Adv. Sp. Res. 56, 1428–1440. http://dx.doi.
Acknowledgments org/10.1016/j.asr.2015.06.041.
Chabane, K., Bahbeh, L., Seridi, H., 2018. Ecological Quality Status of the Algiers
coastal waters by using macroalgae assemblages as bioindicators (Algeria,
The authors would like to express their gratitude to Mediterranean Sea). Mediterr. Mar. Sci. 305. http://dx.doi.org/10.12681/mms.
Dr. Amarouche Khalid for his assistance in obtaining in-situ data 15951.
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the Space Oceanography Laboratory for the advice and support. multispectral images. Photogramm. Eng. Remote Sens. 55, 1285–1294.
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