# **Feature Papers of Water Resources Management, Policy and Governance**

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*Article* **Remote Sensing of Coastal Vegetation Phenology in a Cold Temperate Intertidal System: Implications for Classification of Coastal Habitats**

**Brigitte Légaré 1,\*,†, Simon Bélanger 1,†, Rakesh Kumar Singh 1, Pascal Bernatchez 1 and Mathieu Cusson 2**

**Abstract:** Intertidal vegetation provides important ecological functions, such as food and shelter for wildlife and ecological services with increased coastline protection from erosion. In cold temperate and subarctic environments, the short growing season has a significant impact on the phenological response of the different vegetation types, which must be considered for their mapping using satellite remote sensing technologies. This study focuses on the effect of the phenology of vegetation in the intertidal ecosystems on remote sensing outputs. The studied sites were dominated by eelgrass (*Zostera marina* L.), saltmarsh cordgrass (*Spartina alterniflora*), creeping saltbush (*Atriplex prostrata*), macroalgae (*Ascophyllum nodosum*, and *Fucus vesiculosus*) attached to scattered boulders. In situ data were collected on ten occasions from May through October 2019 and included biophysical properties (e.g., leaf area index) and hyperspectral reflectance spectra (*Rrs*(*λ*)). The results indicate that even when substantial vegetation growth is observed, the variation in *Rrs*(*λ*) is not significant at the beginning of the growing season, limiting the spectral separability using multispectral imagery. The spectral separability between vegetation types was maximum at the beginning of the season (early June) when the vegetation had not reached its maximum growth. Seasonal time series of the normalized difference vegetation index (NDVI) values were derived from multispectral sensors (Sentinel-2 multispectral instrument (MSI) and PlanetScope) and were validated using in situ-derived NDVI. The results indicate that the phenology of intertidal vegetation can be monitored by satellite if the number of observations obtained at a low tide is sufficient, which helps to discriminate plant species and, therefore, the mapping of vegetation. The optimal period for vegetation mapping was September for the study area.

**Keywords:** vegetation phenology; spectral signature; intertidal coastal ecosystem; remote sensing; eelgrass (*Zostera marina* L.); saltmarsh; classification

#### **1. Introduction**

Intertidal ecosystems are productive and dynamic environments located between low and high tide levels. These environments play various essential ecological and biogeochemical roles that benefit both terrestrial and marine ecosystems by sequestering carbon and nitrogen and regulating biogeochemical cycles [1,2]. With the increase in population, industrial development, and over-exploitation of resources over the past decades, coastal and littoral environments are among the most vulnerable ecosystems in the world [1,3–6]. The anthropogenic pressures associated with coastal ecosystems and the increase in sea levels linked to climate change contribute to the loss of 20 to 70% of these ecosystems [7,8]. In addition, global warming causes a rise in the number and intensity of winter storms

**Citation:** Légaré, B.; Bélanger, S.; Singh, R.K.; Bernatchez, P.; Cusson, M. Remote Sensing of Coastal Vegetation Phenology in a Cold Temperate Intertidal System: Implications for Classification of Coastal Habitats. *Remote Sens.* **2022**, *14*, 3000. https://doi.org/10.3390/ rs14133000

Academic Editors: Matteo Convertino and Jie Li

Received: 30 April 2022 Accepted: 19 June 2022 Published: 23 June 2022

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**Copyright:** © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

and reduces the coastal ice cover in cold temperate regions and higher latitudes, leading to rapid changes in coastal environment functions and structures [8]. Management activity relies on the provision of spatial and explicit information on coastal vegetation distribution, making it more important than ever [9].

Satellite remote sensing technology is increasingly used to map vegetation cover of habitats, varying from forests to coasts and their temporal evolution [10,11]. However, more in situ observations are needed to obtain accurate mapping and to orient the development of satellite-based classification algorithms [12,13]. Optical remote sensing images provide essential information on vegetation cover, such as the spatial extent presence and the dominant vegetation type, the biomass estimate, the percentage cover, and the leaf area index (LAI), [14–16]. Recent advances in satellite sensors and algorithms now provide the ability to monitor coastal vegetation at relatively high spatial (<10 m pixel size) and temporal (weekly) scales [17]. Spaceborne sensors commonly used to map coastal vegetation ecosystems or habitats include Landsat-8 [18], Sentinel-2 [17,19], RapidEye [19], and PlanetScope [20].

Mapping coastal vegetation using satellite remote sensing imagery relies on the assumption that the dominant vegetation type presents unique spectral signatures to distinguish from others [9,21]. However, reflectance spectra of coastal vegetation frequently overlap, change rapidly over the season, and are not always distinguishable by using multispectral sensors alone due to the low number of broad spectral bands. Understanding vegetation spectral reflectance variability is essential and can be used to map different vegetation species using remote sensing images [22,23]. In addition, understanding the seasonal evolution, i.e., the phenology [24], of the reflectance spectra of key vegetation types can provide additional clues for distinguishing them from space [25,26]. It can help, for example, to identify the season when the difference between the band is at its greatest.

The first objective of this study was to document with in situ measurements the seasonal evolution of dominant vegetation reflectance spectra, along with biophysical properties, in a cold temperate intertidal system. Analysis of spectral measurements is crucial to determine appropriate spectral resolutions and a classification scheme. The four prevalent vegetation types included eelgrass (*Zostera Marina*), macroalgae (*Ascophyllum nodosum*, *Fucus vesiculosus*), saltmarsh cordgrass (*Spartina alterniflora*), and creeping saltbush (*Atriplex prostrata*). The second objective was to assess the potential of combining multispectral sensors onboard satellite constellations offering high spatial and temporal resolution (i.e., Sentinel-2 Multispectral Instrument (MSI), Landsat-8 operational land imager (OLI), RapidEye (RE), and PlanetScope (PS)) to quantify the phenological change of intertidal vegetation. Finally, we identified the best seasonal window to classify and map coastal ecosystems during the relatively short growing season (<6 months) in the studied system.

#### **2. Materials and Methods**

#### *2.1. Study Area*

The study area is an intertidal saltmarsh and seagrass meadow near the Baie de l'Isle-Verte National Wildlife Area located along the south shore of the St. Lawrence Estuary, Québec, Canada (Figure 1). The Baie de l'Isle-Verte (BIV), located east of the sampling site, is a protected area of 322 hectares; it was created in 1980 by Environment Canada to protect the intertidal cordgrass marsh of l'Isle-Verte and the adjacent coastal habitats, which are used by waterfowl and numerous other fauna species.

**Figure 1.** True-color image of l'Isle-Verte from PlanetScope captured on 3 September 2019. The outer red box delimits the subset used for the study area, and the black dots identify the 13 harvest sites. White dots on the upper panel are the locations selected for the classification validation.

The sampling site is protected from wave action by the Isle-Verte island (municipality of Notre-Dame-des-Sept-Douleurs) (69°27 00W; 47°58 30N). This area is home to one of the largest eelgrass meadows of the St. Lawrence Estuary, a rich and productive environment that has been monitored by the Department of Fisheries and Oceans since the 1980s [27,28]. The climate of the study area is cold (mean annual temperature of 3.5 °C), humid, and highly influenced by estuarine and marine conditions. In the winter, temperatures are well below the freezing point and most of the bay is covered by landfast ice and ice formed along and attached to the shore, also known as ice foot [29] with a mean winter temperature of −10.8 °C. In the summer, the temperatures on the shore remain colder than inland due to the marine influence. The tides are semi-diurnal, with an average tidal range of 3.5 m [30]. The spring tides can reach 4.7 m and are only 1.5 m during neap tides. The estuarine waters are brackish (about 20–25 PSU) and relatively turbid in the study area, limiting the detection of submerged vegetation by remote sensing [30–32].

#### *2.2. In Situ Measurement*

The sampling area was divided into four zones based on the frequency of immersion, which is a function of elevation, the ice in the winter, the water temperature, and salinity (Figure 2). The zones are: (1) the eelgrass bed of *Zostera marina* (EG); (2) the mud flat with microphytobenthos (SD: sediment) and the macroalgae zone composed of Fucus and Ascophyllum, mainly attached to scattered boulders (MA); (3) the low marsh cordgrass zone dominated by *Spartina alterniflora* (SC); and (4) the high marsh zone mainly dominated by *Atriplex prostrata* (CS, creeping saltbush) [30,31,33]. During the winter, ice scouring creates ice-made tidal pools, which increase the spatial heterogeneity within the shore habitats [34–36].

**Figure 2.** Drone image collected on 1 September 2019 presenting the delimitation of the four zones of the study site and the transect of 13 harvest points.

A 600 m transect perpendicular to the shoreline was set up to cover the four zones identified above (Figure 2). Thirteen stations, or plots, were placed along the transect, covering each zone of the coast, in relatively homogeneous patches of vegetation (>100 m2), except for SD and MA where scattered boulders create high spatial heterogeneity from a remote sensing perspective. A complete species composition list, including the percentage cover estimates, was established for every plot in 50 × 50 cm (2500 cm2) quadrats (Table 1).

**Table 1.** Zone type, percentage coverage at the beginning and the end of the season, and the vegetation biomass harvested at the end of the season in g/m2.

Note: only one station was sampled for CS due to time constraints (i.e., low tide sampling) and difficulty in identifying CS at the beginning of the season.

Each station was geolocated using a GPS, marked with a wooden post, and visited up to 10 times from 17 May–25 October 2019 (Table 2). All stations were sampled during the low tide, approximately every two weeks during the maximum growth period (defined as mid-May to early August for this study) and then every three to four weeks for the rest of the season until late October due to a decrease of change in the vegetation in the summer, or for practical reasons (instrument availability and other academic activities).

**Table 2.** Dates, sky, tidal levels and number of stations of the in situ data collection.

Plant allometry was determined for each station along with radiometric measurements and vertical photographs for the vegetation percent cover (every time). More specifically, plant allometry included the length and width of leaves, and it was determined for eelgrass (EG), the creeping saltbush (CS), and the saltmarsh cordgrass (SC) for every sampling date. For each harvested site, the number of plants (or shoots) were calculated inside the quadrat of ∼2500 cm2 Furthermore, the number of leaves by plant and their lengths and widths for EG and SC were measured on five plants chosen randomly inside the station. For the CS, the lengths of the stems were measured using five plants, chosen randomly. The lengths of the leaves and stems were measured using tape directly on the field. Solely at the end of the season, the vegetation inside the quadrat was harvested for biomass determination. The leaf area index (LAI) was calculated using a similar method by [37] and applied for the EG and SC. Three shoots were collected in the field and photographed with their leaves (flattened out on a white board next to a ruler). The leaf surface area (*S*Leaf) was determined using the wand tool of ImageJ software [38]. *S*Leaf was measured twice for the photosynthetic leaf surface (using only the green parts of the leaves) and for the total leaf surface (including the necrotic tissue). The LAI was then calculated based on the following, by Watson [37]:

$$LAI = \frac{S\_{\text{Leaf}} \times D\_{\text{shotot}}}{1000} \tag{1}$$

where *S*Leaf is the mean surface area (cm2) measured for the three shoots of a given quadrat and shoot density (*D*shoot) is the density (N shoots m−2) for the original value for the same quadrat.

#### 2.2.1. In Situ Radiometry

Field radiometry was performed using a VIS-NIR analytical spectral device (ASD) spectroradiometer (Handheld2-pro model) recording wavelengths from 325 to 1075 nm. The upwelling radiance (*L*, Wm−2sr−1nm−1) spectra were measured at nadir. To avoid any disturbance of the light field, the radiance measurements were collected witha5m bare optical fiber fitted to the ASD, having a field-of-view (FOV) of 25°. The fiber was attached at the end of a rod fixed to a tripod pointing the surface at nadir from 113 cm above the surface to obtain a ∼2500 cm2 surface area (Figure 3), similar to the quadrat

area. For each spectrum recorded, the ASD collects five spectra and computes the average and standard deviation of the spectra. Before each surface radiance measurement (*L*surf), a calibrated white reference (Spectralon plate, *L*ref) with a known reflectance value was measured (99.57%) at nadir (*R*panel). At least two sets of measurements (replicates) were made at each site. More measurements were performed under changing illumination due to the presence of thin clouds or cloudy conditions.

**Figure 3.** Acquisition of the emerged surface reflectance with the ASD fitted to a tripod (**A**) and typical vegetation target photographed at nadir: CS (**B**), EG (**C**), SC (**D**), and MA (**E**).

The surface reflectance, *R*surf (unit less), was calculated following Equation (2).

$$R\_{\text{surf}} = \frac{L\_{\text{surf}} \times R\_{\text{panel}}}{L\_{\text{ref}}} \tag{2}$$

Because the *R*surf were not collected on the same day and time of the day, under different sky conditions, sun-view geometry, and instrument settings (i.e., integration time) (Table 2), variations in magnitude due to illumination differences were present [39]. Similar issues were noticed in the literature [17], and a correction was then applied to *R*surf following [40]. Briefly, the multiplicative scatter correction method (MSC; [40,41]) minimizes the uncertainty in the reflectance spectra due to different measurement conditions while keeping the main spectral features. MSC applies a simple correction to the raw reflectance value at each wavelength of the sample spectra based on the reference spectra. It uses the offset and the slope values estimated by linear least-squares regression of all the raw spectra collected in the field against a reference spectrum [41]. In MSC, the linear regressions are fit to a local wavelength region using a moving window of a specified length. The reference spectra applied in the MSC to the sample spectra were the mean spectra of each station's spectra collected during the growing season.

The spectral similarity between the *R*surf spectra was estimated using the spectral angle mapper (SAM; rad), used [42] as:

$$SAM = \cos^{-1}\left(\frac{\sum\_{k=1}^{B} \mathbf{x}\_k y\_k}{\sqrt{\sum\_{k=1}^{B} \mathbf{x}\_k^2} \times \sqrt{\sum\_{k=1}^{B} y\_k^2}}\right) \tag{3}$$

where *B* is the number of spectral bands, *k* the *i*th waveband, *x* and *y* are two *R*surf spectra to compare, respectively. The SAM was applied to both raw and MSC-corrected spectra, but only the latter were used for further analysis. The SAM was used to examine the

spectra similarities/differences among different species, and for a given species during the growing season.

#### 2.2.2. Spectral Resampling and Vegetation Indices

For comparison with satellite data, the measured hyperspectral *R*surf were resampled to the multispectral bands of OLI, MSI, RapidEye, and PlanetScope using the sensor spectral response function (SRF) provided by the space agencies. For all sensors, only the visible and the near-infrared bands (400–900 nm) were used for the analysis.

Many different vegetation indices (VIs) have previously been applied to multispectral remote sensing data [43]. In the present study, VIs suitable for the satellite sensors were tested (Table 3) to identify which indices respond best to seasonal variability and vegetation density metrics (i.e., LAI).

**Table 3.** Vegetation indices applied to the reflectance spectra and the satellite images.

Note: where *L* is the magnitude of green vegetation cover.

#### *2.3. Satellite Data*

Cloud-free satellite images from OLI, MSI, RapidEye, and PlanetScope captured between May and October 2019 were downloaded for the data providers (USGS EarthExplorer, earthexplorer.usgs.gov; Copernicus Open Access Hub, scihub.copernicus.eu; and PlanetExplorer planet.com/explorer/ all accessed on 16 June 2022).

A total of 16 images (Sentinel-2 (6), Landsat-8 (2), RapidEye (2), and PlanetScope (6)) were selected based on the date, the state of the tide, and the cloud cover, i.e., a low tide under a clear sky (less than 15% of cloud cover) (Table 4).

Level 1 images (top-of-atmosphere radiance) were atmospherically corrected to retrieve the surface reflectance using ACOLITE (version Python 20190326.0), which was adapted for all sensors. To compute the surface reflectance, the dark spectrum fitting method was adopted using the standard parameters proposed by ACOLITE [48]. Briefly, after cloud masking and gas transmission correction of top-of-atmosphere reflectance, ACOLITE found multiple dark pixels in sub-scenes, to define a "dark spectrum" based on the lowest reflectance values in any spectral bands. The dark spectrum was then used to estimate the atmospheric path reflectance according to the best fitting aerosol model. Sky and sun glint components were also estimated over water surfaces, but not for land surfaces. The images were then projected, and the VIs were calculated. The homogeneous area of each vegetation species and sediment were delimited based on GPS collected on the field and from drone images (collected in September) to compare VIs from the images to the in situ. The VI values were extracted from those areas covering the stations visited in the field. For MA, due to the small patch size, subpixel fractions were calculated based on the sensor's pixel size using a very high spatial resolution drone image. For each area, the mean values of the VIs were calculated.

**Table 4.** List of the images acquired for the study and the water level when the sensor collected the images.

Note: A and B in the MSI column depict the satellite Sentinel-2A and Sentinel-2B, respectively. For PlanetScope— DC and DR correspond to Dove Classic and Dove-R sensors, respectively.

#### *2.4. Classification*

Image classification was performed using a machine learning algorithm named the extreme gradient boosted decision tree algorithm (hereafter referred to as XGBoost) [49]. To classify the vegetation, the XGBoost creates decision trees based on the input features and assigns specific weights to these features based on their significance in identifying a vegetation species, thereby defining the feature importance for the model. To train the XGBoost model, the in situ *R*surf spectra associated with each vegetation type and sediment were used [50]. The in situ dataset was divided into training and testing datasets with a 4:1 ratio to train the model effectively. We first trained the model using the *R*surf of each vegetation type and sediment collected during the growing season. This model was applied to the Sentinel-2 image time series (hereafter referred to as XGBoostnoSeason). Six images were classified from June to October (one per month). To cover all months of the growing season, an image from August 2020 was used as no clear sky images were available in August 2019. This process allowed us to identify the most favorable month to distinguish intertidal vegetation. Furthermore, to identify the best period in the season to classify the intertidal coastal habitats, XGBoost models were trained using the in situ *R*surf collected closest to the date of the satellite image acquisition (hereafter referred to as XGBoostSeason).

The classification accuracy was evaluated using 170 different data points for which the vegetation classes were known based on the information collected from the study area and photo-interpretation of the drone or aerial photographs (white dots on Figure 1). A confusion matrix was generated and the overall accuracy, Kappa coefficient (*κ*), and perclass F1-score were calculated to assess the performance of the classification. The *κ* values ranged between 0 and 1; they are measures of accuracy that account for the random chance of correct classification [51]. The F1-score (ranging between 0–1) is the harmonic average of precision and recall for every class to deal with unbalanced validation data [52].

#### *2.5. Satellite Vegetation Index Validation*

The VI values from the reflectance spectra (in situ) and the multispectral satellite images were statistically analyzed for the different vegetation types. It was then possible to determine whether the VI values between vegetation types differed between in situ and satellite data. The accuracies of the satellite VI retrievals were evaluated using the root mean square error (RMSE), the mean relative difference (Bias), and Pearson's correlation coefficient (*r*), expressed respectively as:

$$RMSE = \sqrt{\frac{\sum\_{i=1}^{N} (y\_i - x\_i)^2}{N}} \tag{4}$$

$$Bias = \frac{1}{N} \sum\_{i=1}^{N} (y\_i - x\_i) \tag{5}$$

$$r = \frac{\sum\_{i=1}^{N} (\mathbf{x}\_i - \overline{\mathbf{x}})(y\_i - \overline{\mathbf{y}})}{\sqrt{\sum\_{i=1}^{N} (\mathbf{x}\_i - \overline{\mathbf{x}})^2} \sqrt{\sum\_{i=1}^{N} (y\_i - \overline{\mathbf{y}})^2}} \tag{6}$$

where *N* is the number of samples in the data set, *xi* the in situ value, and *yi* the satellite estimated value of the parameter of interest; *x* and *y* are the corresponding mean values of the samples. We used a significance level of *α* = 0.05 for all statistical analyses.

#### **3. Results**

*3.1. Field Observations*

3.1.1. Biophysical Parameters

Over the season, the number of leaves per shoot, the leaves, and the stem maximum length for *Zostera marina* (EG), *Spartina alterniflora* (SC), and *Atriplex prostrata* (CS) were measured (Figure 4A). For the SC and the CS, the maximum length increased from May to August, with lengths reaching about 35 cm (except for station S9 that remained shorter than 20 cm), which was 30 times longer than at the beginning of the season in mid-May. A sharp decrease in the absolute length of the stem and leaves occurred after the peak reach in August, with leaf length values at ∼10 cm in October. In contrast, the EG leaf length at the beginning of the season was much longer (10 to 25 cm) than the other species. It must be noted that the length of the leaf was inversely proportional to the elevation relative to the sea level, with longer leaves in deeper waters (S1–S3). More than twice shorter leaves were observed at station S4 located at the fringe of the meadow in sightly shallower waters (Figure 2). The maximum lengths of the eelgrass leaves increased until September, reaching lengths >20 cm with a maximum of 80 cm and the absolute lengths decreased at all stations thereafter.

**Figure 4.** Seasonal evolution of (**A**) the leaves and stem maximal length and (**B**) the leaf area index (LAI) of the EG and SC, and the steam length of the CS from 23 May–25 October 2019.

The leaf area index (LAI), a commonly used proxy to quantify the density of vegetation canopy, allows the estimation of the plant canopy surface area per m2 of the substrate (Figure 4B). For the EG, the LAI was somewhat more stable throughout the season and lower than the SC in the middle of the summer. The seasonal evolution of EG LAI is explained with tissue growth until August, and thereafter—a decrease (due to the appearance of necrosis on the leaves, which reduced the LAI based on the green part of the leaves). As for the SC, the LAI increased from May to July (S11 ad S12) or August (S9 and S10) reaching values > 1 m2 m−2 (maximum close to 3 m2 m−2), and then decreased to values of 0.5 to 1 m2 m−2 in October due to the pigment degradation in the tissue caused by the temperature change.

#### 3.1.2. Spectral Signatures of Vegetation Types and Sediments

Figure 5 presents the average and standard deviation (shaded area) of each vegetation type calculated on all available raw and MSC-corrected *R*surf, respectively. As expected, much larger variability was observed in raw spectra compared to the MSC-corrected, which was due to the seasonal evolution of the spectra, but also, to some extent, due to the illumination conditions that varied from date-to-date (e.g., a clear sky versus cloudy or partly cloudy; (Table 2). Despite a marked seasonality in terms of leaf length and LAI (Figure 4), the standard deviation of raw *R*surf was much lower for *Spartina alterniflora* (SC) compared to the other vegetation species. The largest variability was observed in the NIR for creeping saltbush, followed by macroalgae and eelgrass. A homogeneous spectral variability was also observed for bare sediments, except a notable trough around 676 nm corresponding to the red peak of absorption because of chlorophyll-a. The MSC normalization removed most of the variability, including part of the seasonal variability. Interestingly, the spectral shape of the MSC-corrected spectra for MA in the visible bands showed virtually no variability, suggesting a very stable pigment composition across the growing season for this type of vegetation. For comparison, EG and SC showed the largest variability in the visible bands after the application of the MSC, followed by SD.

**Figure 5.** Mean reflectance spectra of four vegetation species and sediments and their standard deviations (shaded area): (**A**) raw *R*surf; (**B**) MSC-corrected *R*surf.

The SAM quantifies the spectral similarity and difference between the vegetation species (Figure 6). Sediment (SD) spectra differed markedly from all vegetation types (SAM > 0.29 rad), with the largest difference with MA. The spectral differences between the EG and MA, EG and CS, and MA and SC showed intermediate values (0.23 < SAM < 0.27 rad). Between the different vegetation types, MA and CS showed the smallest differences (0.1 rad), followed by SC versus CS (0.17 rad).

**Figure 6.** SAM analyses were applied to the MSC-corrected *R*surf of four vegetation species and sediments.

#### 3.1.3. Spectral Phenology

In general, the spectral shape of vegetation species remained almost the same throughout the season. However, there can be spectral crossovers between species due to changes in the absorption strengths and pigment concentrations. Therefore, it is necessary to consider intra- and inter-species spectral variability throughout the season.

In the visible spectrum, the reflectance peak of the healthy EG was stable over the season and was located between 555 and 564 nm (Figure 7C). The EG showed a very low reflectance peak at the beginning of the season (early May) before jumping up to the highest reflectance for this season at the end of May. Afterward, the spectra remained, with mid- to low peaks and values observed in the middle and at the end of the season. Two major absorption bands were visible and located in the blue (489–496 nm) and red (671–677 nm), respectively. Those absorption bands are typical of the absorption features of chlorophyll and carotenoids. Note that the spectrum observed on 23 May differed from the other. The exact reason for this anomaly could not be confirmed due to the unavailability of supporting data. At any other moment through the season, the EG spectra stayed similar without a clear seasonal evolution.

**Figure 7.** MSC-corrected reflectance spectra collected through the summer for four vegetation species and sediments collected from 17 May to 25 October 2019 for CS (**A**), SC (**B**), EG (**C**), MA (**D**), and SD (**E**).

The macroalgae spectra remained stable over the season (Figure 7D), with almost no change in the visible range compared to the NIR. The location of the green reflectance peak was regular, around 568 to 574 nm. Still, two absorption bands could be located, one in the green (504–520 nm) and the other in the red (671–678 nm). Secondary reflectance peaks are found in the red near 650 and 670 nm, respectively (c.f. Figure 7).

The peaks of reflectance of CS and SC were shifted to the longer wavelengths in the beginning (May to end of June) and at the end (mid-September to November) of the season (Figure 7A,B), but were almost the same as the EG in the middle of the summer (July to the middle of September). For the SC, the peak reflectance location shifted from 556 to 648 nm from the summer to the fall (Figure 7B). As for CS, the reflectance peak was located between 554 nm in the summer and shifted to 648 nm in October (Figure 7A). Both species presented similar absorption bands in blue (488–499 nm) and in red (672–680 nm) portions of the visible. The later corresponds to the red absorption peak of chlorophyll-a. The seasonal shift in the reflectance peak can be explained by the composition of the dominant pigment changing at the beginning and end of the season.

SAM was used to assess the seasonal variation in the spectral reflectance for each vegetation type and bare sediment (Figure 8). For MA and SC, the spectra did not change over the season with SAM values constantly below 0.18 and 0.14 rad, respectively (Figure 8B,D). Even though the SAM values were low for SC, we observed a difference in the spectral shape between the beginning/end and the middle of the season, but the differences remained small in terms of SAM. For example, the August spectrum was clearly different relative to the spectra measured in May, June, and the end of October (0.11 < SAM < 0.14 rad; c.f. Figure 8B). Among the four vegetation types, the CS showed the clearest seasonal evolution in terms of reflectance (Figure 8A). The values obtained by the SAM ranged from 0.02 to 0.27 rad. Spectra at the beginning (May and June) and at the end (September and October) of the season were similar, and different from those from the middle of the season (July to August). As for EG, the SAM values ranged from 0.04 to 0.38 rad (Figure 8C), with an anomalous value for the spectra collected on 23 May. The high SAM values for those spectra may be attributed to a particular moment corresponding to a high EG growth rate, or to the unstable sky conditions while collecting in situ radiometric data. As mentioned previously, the exact reason for this anomaly could not be confirmed due to the unavailability of supporting data. At any moment, the EG spectra stayed remarkably similar without a clear seasonal evolution.

**Figure 8.** SAM analyses were applied to the reflectance spectra of four vegetation species and sediments collected from 17 May to 25 October 2019 for CS (**A**), SC (**B**), EG (**C**), MA (**D**), and SD (**E**).

Figure 9 shows the SAM calculated for a vegetation type using the spectra at a given date, against another date. This analysis helps to understand the variations of spectral changes of a species relative to another during the summer season. The most significant difference between all vegetation species spectra occurred at the beginning (May and June) and the season's end (September and October). For example, Figure 9A compares creeping saltbush (CS) with the other vegetation types (EG, MA, SC) and sediments (SD). The largest difference between CS and the other was in May, except for SC, where the SAM remained stable during the growing season (0.2 rad). In June and July, CS and MA were very similar and difficult to distinguish spectrally (SAM < 0.1 rad) Figure 9A,D. A similar remark can be made for EG, where the lowest SAM were generally found in July. It also suggests that EG differs more from the other vegetation types in the spring (end of May) and in early October. Saltmarsh cordgrass (SC) is more easily distinguished from EG and MA at the beginning and end of the season (Figure 9B), but more different from sediment in July. The sediment spectra are different from all ofthe vegetation spectra (Figure 9E). Overall, this analysis indicates that it can be difficult to distinguish many vegetation species based on a single date in the middle of the growing season (June to August).

**Figure 9.** SAM analyses applied to the reflectance spectra according to the vegetation species and sediment over time, collected from May to the end of October for CS (**A**), SC (**B**), EG (**C**), MA (**D**), and SD (**E**).

#### *3.2. Classification of Vegetation Type*

To examine the implication of spectral and seasonal variability of the vegetation type for mapping the coastal intertidal zone using multispectral imagery, a classification algorithm was applied to the Sentinel-2 MSI time-series covering the growing season (Table 4). This sensor was selected because (i) it provides the best response to seasonal variability and availability over the critical dates for the vegetation phenology; and (ii) it has 13 spectral bands, including key bands in the red-edge portion of the spectrum that is suitable for vegetation mapping.

The XGBoost algorithm was first applied to the image using the in situ spectra associated with the date closest to the acquired image (XGBoostSeason, Figure 10). By changing

the input spectra, the algorithm demonstrated a successful identification of the vegetation species, which confirmed the occurrences and spatial distributions by each species (Table 5). For the first and last images (May and October), most of the classification mistakes were due to confusion between saltmarsh cordgrass (*Spartina alterniflora*, SC) and the sediment (not shown) due to their similar spectral signatures at this time of the year (Figure 9B,E). On every image, the algorithm seems to have a problem identifying the macroalgae (MA). This might have been caused by the spatial resolutions of the images and the sizes of the MA patches attached to the boulders that were generally smaller than the pixel sizes. Note that none of the classified images present MA on the rocky shores of the island (west tip and north east coast of the island). Based on the classification evaluation metrics (overall accuracy and *κ* indices; (Table 5), early June and the end of September images were best suited for the coastal vegetation cover mapping. In other dates, the overall accuracy reached about 70% with the worst performance obtained in October (accuracy of 65% and *κ* of 0.56).

**Table 5.** Model validation statistics (overall accuracy (*κ*), and mean F1-score) of XGBoostSeason.

**Figure 10.** Classification of coastal and intertidal vegetation using XGBoostSeason applied to the Sentinel-2 time series.

Even though XGBoostSeason can classify the intertidal zone with significantly good accuracy, it is not practical to train separate models for every month of the growing season. Therefore, we trained a single XGBoost model (XGBoostnoSeason) (Table 6) using the same set of in situ spectra, without accounting for the seasonality. The goal was to evaluate the sensitivity of the classification to seasonal variability in the vegetation spectra. XGBoostnoSeason yielded marked differences in vegetation mapping (Figure 11) throughout the season when spectral evolution was not taken into account. More sediment was identified in May, reflecting the early stage in the vegetation development and/or the low LAI. Macroalgae occupied a relatively large surface area, which was not consistent with the field observations. As expected, the classified image from May has the lowest accuracy and *κ* index (57% and 0.44, respectively). Between May and June, we see an expansion of the EG and SC surface areas. The images from July and August have a problem identifying other vegetation types than EG. In the summertime, the vegetation spectra from all types were too similar and could not be distinguished by the model trained without accounting for the seasonality in *Rsur f* . The best performance of XGBoostnoSeason was obtained in September, with accuracy and *κ* values of 87% and 0.85, respectively. At this time, the vegetation was fully grown and the senescence had just started, yielding spectrally distinguishable surfaces. The October image yielded the second-best classification metric despite some senescence within the vegetation. It is interesting to note that the October image did not perform as well with the in situ spectra associated with the same date. Although the results of the two classifications for the October image are quite different, the validation results are almost similar. This can be explained by confusion from the algorithms between different species. For example, in the XGBoostSeason, the majority of the confusion is with the SD and the MA, while in the XGBoostnoSeason, the confusion is between SC and SD, resulting in similar validation statistics.

**Table 6.** Model validation statistics (overall accuracy (*κ*), and mean F1-score) of XGBoostnoSeason.

**Figure 11.** Classification of coastal and intertidal vegetation using XGBoostnoSeason applied to the Sentinel-2 time series.

Overall, only the eelgrass meadows were well classified (>85% accuracy) in all images, although they were over-represented in the middle of the summer. In contrast, confusion between MA and EG was observed for most images, as observed on the rocky coast of the island at the western tip and along the northeast coast.

#### *3.3. Remote Sensing of Coastal Vegetation Phenology*

We further assessed the potential of recent satellite constellations to monitor the phenology of intertidal vegetation found in the study area. The VI time series were computed on both in situ and satellite-derived *R*surf from OLI, MSI, RapidEye, and PlanetScope. We first evaluated the robustness of each VI in terms of its capacity to predict the leaf area index (Section 3.3.1), a classical proxy for vegetation biomass, as well as its response to the seasonal variability in the vegetation. It turns out that the NDVI provided the highest correlation with LAI, which was selected for further analysis. After a comparison of in situ NDVI (NDVIin situ) with satellite-derived NDVI (NDVIsat) (Section 3.3.2), we examined the potential of this spectral index to monitor coastal vegetation phenology in our study area (Section 3.3.3).

#### 3.3.1. Vegetation Indices as Predictor of LAI

Among the VIs listed in Table 3, the NDVI presented the best predictor of the LAI (highest *r* and RMSE). Figure 12 shows the linear relationship between LAI and the NDVI for EG and SC, separately. For both species, we found an important variability in terms of LAI at some stations at a given NDVI value. This is particularly evident at stations S1 and S2, where a dense EG cover (100% coverage throughout the growing season) produced almost constant NDVI value, while the LAI varied by a factor of 2. At other stations where the initial % coverage was lower (Table 1), seasonal variability was more evident, especially for the SC. Note that the MSC correction of *R*surf tends to reduce the variability in NDVI, but increases the Pearson correlation with the LAI (Table 7), confirming the relevance for that correction.

**Table 7.** Pearson's correlation coefficient (*r*) of the LAI versus VI relationships obtained for EG and SC. The highest (**bold**) and lowest (*italic*) values are highlighted.

#### 3.3.2. Satellite-Derived NDVI Validation

Within a given time frame of two days, 15 match-ups, i.e., co-incident in situ and satellite observations, were obtained considering the four satellite sensors evaluated (Figure 13). The relatively strong linear relationship (*r* = 0.76) between the MSC-corrected NDVIin situ and NDVIsat, and the low bias (−0.054) and RMSD (0.16) indicate good agreement between the in situ and satellite NDVI. The NDVIin situ values followed were clustered by vegetation type showing that the MA had the lowest values, followed by SC, EG, and CS. For all sensors, a much larger range of NDVIsat (−0.24 to 0.95) was obtained compared to NDVIin situ (0.13 to 0.75). This was also true for individual vegetation types (e.g., MA and EG), where the NDVIin situ varied in a narrow range compared to the satellite retrievals. One explanation for the low range in NDVIin situ was due to the MSC normalization of the in situ spectra (see below). Sentinel-2 MSI and Landsat-8 OLI presented the best relations between the

NDVIin situ and satellite values. The RapidEye and PlanetScope sensor provided generally good results for most of the vegetation species, except for the MA. These sensors had lower spectral resolutions (i.e., broad spectral bands), yielding outliers, as shown in Figure 13.

**Figure 12.** Linear relationship between the in situ MSC-corrected NDVI and LAI for (**A**) EG and (**B**) SC. Grey data points represent outliers.

#### 3.3.3. NDVI-Based Phenology

Figure 14 shows the seasonal evolution of NDVI for each vegetation type calculated from the in situ MSC-corrected (solid lines) and raw (dashed lines) reflectance spectra. Interestingly, there is not much crossover with the NDVI value among species; each has its specific range (as in Figure 13). The shape and range is similar for both normalized and raw spectra for SD and MA, but the normalization reduces the range for CS, SC, and EG. As expected, bare sediment (SD) or mud had the lowest NDVI values (<0.15), followed by SC, EG, CS, and finally MA. For SD and MA, the NDVI was relatively constant over the season with values of 0.04 ± 0.11 and 0.82 ± 0.07, respectively. Note that MA NDVI was for "pure" spectra while satellite-derived MA NDVI values considered the subpixel coverage (sediment mixed with MA). We can see a clear seasonal evolution for the CS with NDVI as obtained from MSC-corrected reflectance ranging between 0.44 and 0.76. For SC, the NDVI peaked in August at 0.49 and was minimum in May with a value of 0.33. For these two vegetation types, in particular, the MSC-correction substantially

reduced the range of variability Figure 14. EG NDVI constantly increased from May to early October when computed on MSC-corrected spectra but showed two peaks in early July and early September when computed on raw spectra. Note that the decrease in NDVI in mid-summer (July–August) was likely due to the presence of necroses in the leaves. EG seasonal evolution also varied among stations with more marked evolution at S3 and S4 where the initial coverages were 50% and 20%, respectively (Table 1; Figure 4).

**Figure 14.** Temporal evolution of the NDVI values from the in situ spectra collected from May to the end of October of four vegetation species and sediments. Dashed lines are NDVI calculated on raw reflectance spectra.

Since only two images were available for Landsat-8 OLI and RapidEye sensors, respectively,we assessed the space-based phenology using Sentinel-2 and PlanetScope constellations. Six images were available for the Sentinel-2A and 2B MSI sensor from May until the end of October 2019, covering most of the critical moments for the coastal and saltmarsh growing season (Figure 15), but with a more than 2-month gap between 4 July and 12 September.

Eight images from mid-May to early October 2019 were available for the PlanetScope sensor (Figure 16). PS images filled the gap of MSI images, but no images beyond October 3 were available for the senescence period.

**Figure 15.** Time series of NDVI from the Sentinel-2 MSI acquisition obtained at a low tide. Homogeneous regions of interest (ROIs) for the four vegetation types and sediments where the NDVI values were extracted are also shown.

**Figure 16.** Time series of NDVI from the PlanetScope sensor acquisition obtained at a low tide and zoomed in on the region of interest. Homogeneous regions of interest (ROIs) for the four vegetation types and sediments where the NDVI values were extracted are also shown.

Figure 17 depicts the phenology of NDVI by combining the two satellite sensors for the pixels extracted from five homogeneous regions of interest (ROI) located in the sampling area (Figure 16). Steady growth in NDVI for all vegetation types was identifiable from May to August, while the sediment stayed relatively constant. The agreement between MSI and PS was very good for CS and SC throughout the season, except in September/October for SC. The phenology of these two vegetation types agree well with in situ observations (Figure 14) with peaks in August reaching 0.75 and 0.55 for CS and SC, respectively.

**Figure 17.** Satellite-based phenology of coastal vegetation from MSI and PS sensors for the four vegetation types and sediments. NDVI pixels values were extracted from homogeneous surfaces depicted in Figure 16. The LOESS fit was applied for each vegetation type to better visualize the phenology.

A more noisy signal was obtained for EG, which showed higher NDVI relative to other vegetation types. This result contrasts with in situ observations (Figure 14), but not with Figures 15 and 16 where dense EG stations (S1 and S2) constantly showed higher NDVIsat compared to NDVIin situ. EG mapping was more sensitive to tidal differences among satellite acquisitions as it stood in deeper water (e.g., <0.2 m above sea level) relative to CS and SC. The phenology of this vegetation type was more evident from space than for field observations probably due to the percentage coverage of our selected stations.

Macroalgae phenology extracted from satellite images was more pronounced than expected from the in situ observations. Again, the large difference in MA phenology between in situ and the satellite was due to the spectral resolution versus the size of the vegetation patches. The lack of a continuous cover of MA limited our interpretation for this type of vegetation. The SD showed the lowest values and remained relatively constant throughout the season for a given sensor, although a small peak was observed in the late summer. A relatively important discrepancy was obtained between MSI and PS. The later yielded NDVI within the range of the in situ data with non-seasonal variability. In contrast, MSI values for the sediments were relatively high (0.25 to 0.4).

In summary, the images from PS and MSI sensors, allowed us to detect the seasonal evolution of the vegetation. By combining the time series of the two sensors, we can better see the complementary data, offering a better understanding and monitoring of the phenology of the vegetation.

#### **4. Discussion**

In this study, we showed that spectral seasonal evolution in coastal and intertidal vegetation types can be detected by in situ and spaceborne sensors. This evolution is related to the biophysical metric of the vegetation, such as the LAI, but it depends on the vegetation type and the pigment composition. A better understanding of the vegetation phenology provides key insights for the coastal mapping based on spectral classification, with strengths and limitations discussed in the following sections.

We observed an important evolution of the vegetation biophysical metrics, with a growth phase from May to September, which was particularly evident for saltmarsh cordgrass (*Spartina alterniflora*) and creeping saltbush. This observation was consistent with other studies [53–55]. For eelgrass, the growth continued until the beginning of October, while the LAI showed an increase between May and June, remained constant until September, and was followed by a small decrease at the end of the season. Similar results were shown in other studies [56–58].

Our vegetation *R*surf spectra measurement is consistent with other studies [17,59–61]. The in situ spectra analyses suggest that the general shapes of *R*surf are similar for all vegetation types (EG, MA, SC, and CS), but markedly different from the SD. Even if the shape is similar, they are different from each other and evolve over the season, as demonstrated using the SAM and the NDVI. This seasonal evolution is crucial for ecosystem remote sensing and is rarely mentioned and documented in other studies [62]. The spectra from mid-June to the beginning of September often overlapped. At that time of the growing season, the distinction among vegetation types was less obvious. Furthermore, the evaluation of the pure vegetation spectra revealed that MA and EG were stable throughout the season under 100% cover. In contrast, CS and SC presented more variability during the growing season with similar spectra at the start (May and June) and at the end (September and October), but different in the middle of the season (July to August).

Sentinel-2 images were chosen to classify the intertidal and coastal vegetation types in the study area. Using the identical spectra for all images, the XGBoost algorithm (XGBoostnoSeason) was not able to distinguish the vegetation types in July and August. Nevertheless, good results were obtained in June and at the end of the growing season (September and October). The highest accuracy (*κ* of 0.85) was obtained with the September 30th image at the onset of the senescence phase, suggesting that fully-grown vegetation is spectrally distinguishable from each other. We also demonstrate that accounting for vegetation phenology in the classification training dataset (XGBoostSeason) improved the classification accuracy by about 15%.

The NDVI was the most suitable proxy for the LAI among different VIs, and it was selected to evaluate the phenology from remote sensing using in situ spectra and multispectral images from four sensors (Landsat-8 OLI, Sentinel-2 MSI, PlanetScope, and RapidEye). The NDVI has been widely demonstrated to be a good descriptor of vegetation dynamics for many types of ecosystems, including wetlands [17,63–66]. It is also widely used in satellite-based phenology monitoring, as it could be applied to almost any multispectral sensors on a wide range of platforms (in situ, drone, plane, satellite) [67,68]. Based on in situ NDVI measurements, SC and CS clearly showed a seasonal evolution, while MA, EG, and SD were more stable throughout the season. Frequent observations are needed to quantify the seasonal variability and evolution of the vegetation in a cold temperate environment due to a relatively short growing season (<6 months). Changes in coastal vegetation, such as growth, flowering, senescence, and shedding of leaves, take weeks and even months [68–70]. For this reason, we recommend visiting the field as soon as the ice starts to melt (i.e., late March or beginning of April) [69,71]. In our study, we started the fieldwork in mid-May when the EG was already growing, with some stations showing 100% areal coverage.

By combining MSI and PS images, we could also track the vegetation phenology with a clearer signal for EG compared to the in situ. In general, satellite-derived phenology was consistent with the in situ NDVI values shown in this study and as presented by [17,60,72,73]. For example, Zoffoli et al. [17] also used MSI images to document the phenology of intertidal seagrass (*Zostera noltii*) in France. For comparison, these authors obtained 22 MSI images obtained at a low tide under cloud-free conditions for a ten-month period (March to December). With only six MSI images in our region, the combination with the PlanetScope constellation was necessary to fully capture the growing seasons and

the following senescence. However, if our result demonstrates the feasibility, differences in spectral and spatial resolutions between sensors may complicate the combination of multisensor data for phenology monitoring.

As for Landsat-8 and Sentinel-2—both EO missions are dedicated to land cover monitoring and are widely used for phenology assessment. They both acquire images at lower temporal and spatial resolutions compared to PlanetScope. Even if the images are not available at a rapid rate due to tidal height and cloud cover restrictions, we can expect monthly images for the Sentinel-2 sensor, but much less for Landsat (one or two per year). Sentinel-2 images are easily usable and provide much better spectral resolution compared to the very-frequency acquisition of PlanetScope. Therefore, Sentinel-2 images allow further mapping capability by applying a classification algorithm using a high number of bands ( 10 bands). Still, Landsat is a very useful sensor, offering long-term time series for detecting and relatively good spectral capability for coastal mapping [74–76]. In addition, the temporal resolution will improve with the recent launch of Landsat-9 in September 2021, opening the door for data fusion from MSI and OLI [73,77,78]. The fusion of Landsat and Sentinel-2 images has tremendous potential to improve the ability to detect vegetation change and to cover all key periods of the vegetation phenology. However, in our case, combining the data was not necessary because the Sentinel-2 time series was already covering all of the vegetation phenology.

The PlanetScope sensor constellation is relatively new and offers many advantages, including high temporal resolution obtained at high spatial resolution compared to Landsat and Sentinel-2. Those images appear to be promising for extracting natural resources information, including intertidal ecosystem estimates and potentially even vegetation diversity estimates [20,79,80]. As seen in our results, the sensor provides many images covering most of the vegetation key. The spatial resolution of PlanetScope images provides many details, but it is not without issues. Indeed, the variable radiometric quality, inconsistent radiometric calibration across multiple platforms, and low spectral resolution are central challenges for marine and coastal applications, such as vegetation classification and ecosystem monitoring [20,81–83]. The low spectral resolution of the first Dove generation limits its use for the vegetation type classification. Furthermore, the noise level is high, and the radiometric quality and inconsistency are low on clusters of pixels, especially in homogeneous pixels. This indicates the low signal-to-noise ratio of PlanetScope images [20,84]. This issue was encountered during the atmospheric correction, and even after the correction, noise can still be detected in the NDVI images. The next generation of PlanetScope sensors launched in January 2022 with a greater number of bands (eight bands) and a radiometric signal that may have helped resolve most of the limitations of the early sensor fleets.

The presence of water overlying the vegetation at the time of in situ data acquisition or in the images highly affected the spectral reflectance due to its high absorption in the red and the infrared. With high water levels within the vegetation, the species identification can be difficult, and further processes will be needed to use the images and spectra [85–88]. For this reason, the state of the tidal level could significantly influence the spatiotemporal distribution of remotely-sensed parameters, such as vegetation NDVI, which uses red and infrared wavelengths. For example, the bathymetric map combined with water level measurements during the data acquisition could be used to correct the water column interference to retrieve the bottom reflectance [88]. However, estuarine water masses of the St. Lawrence are characterized by high concentrations of colored dissolved organic matter (CDOM) and suspended sediments that severely limit the light penetration, even in the visible bands [89], and impair water column correction. Due to the loss of spectral information in the NIR, submerged vegetation indices need to be based on visible bands only [40,88], or located in the red-edge portion of the spectra [59]. In conclusion, we recommend selecting images at the lowest tides possible to maximize the area to be mapped and to minimize the effect of water on the vegetation. The maximum tidal height that allows the vegetation to be mapped using multispectral data requires prior knowledge of

the area. Furthermore, the mapped area will mainly depend on the area characteristics, such as the bathymetry/elevation and location of the vegetation.

Many atmospheric correction (AC) algorithms can be applied to multispectral images; this is a crucial step in the processing of remote sensing data for aquatic and coastal applications. Ideally, AC aims to separate the top-of-atmosphere observation by the satellite sensor into the signal from the atmosphere and the signal from the surface to retrieve surface reflectance [90]. By using PlanetScope and RapidEye sensors, we are limited by the atmospheric correction algorithm due to a lack of spectral bands (as, for example, in the SWIR). Even though we can apply different atmospheric corrections, the algorithm applied to the image needs to be the same to compare the sensors together. Here, we adopted ACOLITE, as it allows the application of the dark spectrum fitting (DSF) atmospheric correction method to all imagery evaluated in this study. Furthermore, ACOLITE has been developed for the coastal environment and is currently widely used for aquaticbased applications, such as coastal water monitoring [91–94]. The sensitivity of satellitederived NDVI phenology to AC could have been quantified, which was out of the scope of this study.

The area covered by our sampling sites was minimal (472,800 m2) as we focused our effort on one EG meadow and intertidal vegetation section to maximize our frequent visits to the sites. This area was selected for its diversity of vegetation cover and easy access but was nevertheless quite representative of the entire coast of the region. The small size of the studied area helped us to develop excellent knowledge of the vegetation dynamics and the ecosystem structure. However, the sites were not optimal for the detection of small macroalgae patches (e.g., <1–2 m2) with the limited satellite spatial resolution.

#### **5. Conclusions**

In this work, we assessed the seasonal dynamics of four typical intertidal vegetation types encountered in cold temperate coastal littoral, including macroalgae (*Ascophyllum nodosum* and *Fucus vesiculosus*), eelgrass (*Z. marina*), saltmarsh cordgrass (*S. alterniflora*), and creeping saltbush (*A. prostrata*). The seasonal evolution was determined based on biophysical characteristics (leaf area index), in situ reflectance spectra, vegetation indices, and classification of multispectral images. We identified a significant seasonal change in phenology of saltmarsh cordgrass and creeping saltbush. Even though some seasonal change could be observed for some vegetation types, no significant changes were observed in the in situ reflectance spectra for eelgrass and macroalgae. Moreover, we evaluated the potential of the NDVI to quantify the vegetation phenology from space. We demonstrated that the NDVI was the best vegetation index proxy to track the phenology that could be applied to multispectral cameras (including drones). Satellite-based NDVI, which strongly correlates with in situ values for saltmarsh cordgrass and creeping saltbush, were used to assess the potential of multispectral instruments to assess the phenology. By combining Sentinel-2 and planet imagery, we showed that the seasonal evolution of eelgrass NDVI was more evident than with in situ measures, likely because of the initial coverage of the quadrats (2500 cm2). The extreme gradient boosted decision tree (XGBoost) algorithm was applied to a monthly time series of Sentinel-2 using in situ spectra as input spectral classes. The results indicate September as the best month of the year to classify coastal vegetation in our cold temperate environment, i.e., when the vegetation is fully grown and spectrally distinguishable.

Further work is required to monitor the vegetation species from this complex ecosystem located in a cold temperate climate with a relatively short growing season. We intend to extend the vegetation species mapping, especially for marshes that have a high plant diversity (*Salicornia maritima*, *Spartina pectinata*, *Spartina patens*, etc.). Satellite remote sensing provides access to spatial scales, enabling the environment to be documented over vast areas. Widening the study area to cover all the coasts of the St. Lawrence maritime estuary and Gulf system would be interesting to know their conditions and interannual evolution. In addition, it will extend our knowledge of vegetated coastal ecosystems and their overall

importance to the environment. Furthermore, it would be interesting to evaluate the carbon stock sequestration rates in coastal habitats (seagrass and marshes). Remote sensing tools are nowadays developed to quantify the extent of seagrasses and marshes, the species composition of these environments, and the above-ground biomass. In addition, some authors have demonstrated the possibility of estimating carbon stocks using empirical algorithms [95–97]. With these types of data, it will be possible to document and monitor changes in carbon stocks and estimate emissions as functions of ecosystem degradation, conservation, and restoration. Finally, historical data could be used to assess the history of carbon stocks and emissions and the spatial distribution and changes of vegetation species.

**Author Contributions:** B.L. contributed to the data collection and processing and wrote the original draft of this manuscript. S.B. supervised the work, came up with the original idea, contributed to the revision, wrote the manuscript versions, and provided funding. R.K.S. contributed to the atmospheric correction of satellite imagery, data processing (XGBoost classification), and revised the manuscript. P.B. co-supervised B.L., contributed to the fieldwork planning, and revised the manuscript. M.C. led the R.Q.M. project (see below) and provided funding. He contributed to the fieldwork planning and revised the latter version of the manuscript. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research was mainly funded by the program Odyssée Saint-Laurent from the Réseau Québec Maritime (grant number 2018-38-04) attributed to MC (PI), PB, and SB (co-PIs). SB was provided funding from an NSERC discovery grant (RGPIN-2019-06070) and from the WISE-Man Project funded by the Canadian Space Agency through the FAST program (FARIMA18).

**Data Availability Statement:** The data that support the findings of this study are available from the author upon reasonable request.

**Acknowledgments:** The authors acknowledge Véronique Thériault and Colin Surprenant for sharing the drone images. The students who contributed to the field work are also acknowledged: Loïc Théberge-Dallaire, Jimmy Mayrand, François Pierre Danhiez, Soham Mukherjee, Romy Léger-Daigle, and Christel Blot. Furthermore, the authors are thankful to the three reviewers for their comments and suggestions, which improved the quality and readability of the article.

**Conflicts of Interest:** The authors declare no conflict of interest.

#### **Abbreviations**

The following abbreviations are used in this manuscript:

#### **References**


**2. Capabilities of smart systems in rotor blades**

Smart-blades can greatly enhance the performances of modern helicopters. Local modifications of the aerodynamic characteristics of a blade profile provide an optimised performance across the full blade revolution. The control of such systems conditions its capabilities and usage. In the introduction, focus was made on the lift characteristics of the retreating side. Most concepts improve directly the lift of the profile at fixed angle of attack. Other systems increase the efficiency of the helicopter improving the stall behavior of the profile or by reducting the vibration on the rotor. Vibrations decrease an helicopter blade efficiency, influence the dynamic stall and generate noise. The latter is a great concern for helicopter operating in a urban environment.

## **2.1. Flaps**

Flaps on helicopter blades are not designed as a primary control surface like in airplanes. They act as a secondary control to improve the efficiency of the rotorblade by modifying the lift of the profile and by reducing vibrations on the rotor.

### *2.1.1. Active trailing edge flaps*

Active trailing edge flaps are flaps situated at the trailing edge that actively modify the rotorblade performance. A schematic of a trailing edge flap for a helicopter blade taken from Koratkar [28] is shown in Figure 4. Although research has been conducted to study the possibility to use them for control in a swashplateless configuration [49], most of the studies focus on their ability to reduce the vibrations of helicopter blades [1, 15, 18, 27, 28, 35, 62]. The angle of the flap directly relates to a change of the bending of the blade during rotation

**Figure 4.** Schematic of a trailing-edge flap and its actuation system (adapted from Koratkar paper [28]

[18, 28]. The position of the flaps along the rotor has a great influence on the final performances of the mechanism. Although the optimum positioning of the flap depends on the application objective, studies show that multiple flaps achieve a better vibration reduction that a single flap [18, 27, 62]. These flaps only need a few degrees of deflection to affect the system dynamics [15, 28]. Loads on the helicopter rotor are function of the rotational frequency of the blade. The largest loads happens at 1, 2, 3 and 4 times the rotational frequency of the blade [6]. Therefore the flaps need to be actuated at similar frequencies to cancel undesired vibrations. With multiple flaps, the phase between the flaps is another key element. Under a suitable control authority, literature shows that the vibratory loads on the rotor can be reduced up to 80% [15, 18].

The amount of noise generated by helicopters is another important issue, especially because many helicopter missions involve flying over dense populated area. Noise generated by the helicopter blade comes mainly from the interaction between one blade and the vortexes generated by the previous blade [69]. This phenomenon is called blade-vortex interaction (BVI). Decreasing the effects of blade-vortex interaction can not only lead to a reduction in the noise emitted but also to a decrease in the power requirement. Active trailing edge flaps are actively studied to limit this effect by an individual control on each blade [1, 18, 69]. Controlling the trailing edge flap at 2 cycles per revolution (hereafter indicated as 2/rev) shows potential for consequent noise reduction [1].

#### *2.1.2. The Gurney flap*

4 Will-be-set-by-IN-TECH

Smart-blades can greatly enhance the performances of modern helicopters. Local modifications of the aerodynamic characteristics of a blade profile provide an optimised performance across the full blade revolution. The control of such systems conditions its capabilities and usage. In the introduction, focus was made on the lift characteristics of the retreating side. Most concepts improve directly the lift of the profile at fixed angle of attack. Other systems increase the efficiency of the helicopter improving the stall behavior of the profile or by reducting the vibration on the rotor. Vibrations decrease an helicopter blade efficiency, influence the dynamic stall and generate noise. The latter is a great concern for

Flaps on helicopter blades are not designed as a primary control surface like in airplanes. They act as a secondary control to improve the efficiency of the rotorblade by modifying the lift of

Active trailing edge flaps are flaps situated at the trailing edge that actively modify the rotorblade performance. A schematic of a trailing edge flap for a helicopter blade taken from Koratkar [28] is shown in Figure 4. Although research has been conducted to study the possibility to use them for control in a swashplateless configuration [49], most of the studies focus on their ability to reduce the vibrations of helicopter blades [1, 15, 18, 27, 28, 35, 62]. The angle of the flap directly relates to a change of the bending of the blade during rotation

Helicopter motion

Wing speed relative to air

Reverse flow region

**Figure 3.** Helicopter in forward flight.

helicopter operating in a urban environment.

the profile and by reducing vibrations on the rotor.

**2.1. Flaps**

*2.1.1. Active trailing edge flaps*

**2. Capabilities of smart systems in rotor blades**

The Gurney flap is a small flap deployed at 90 degrees at the edge of the trailing edge of the rotorblade, as shown in Figure 5. Typically its length is 2% of the chord length of the blade profile. The Gurney flap modifies the flow at the blade trailing edge and induces a low pressure zone which brings the separation point closer to the trailing edge [53]. The result is an increase of the lift over a large range of angles of attack with a small drag penalty [38, 53, 59,

**Figure 5.** Sketch of a Naca 23012 profile with a 2% Gurney flap.

68]. Although the Gurney flap induces pitching moment, it provides a beneficial improvement of the efficiency of the rotorblade profile for the hovering situation [68]. In forward flight, the Gurney flap provides the blade with additional lift on the retreating side to balance the lift distribution [59]. For large forward velocity, the Gurney flap improves the airfoil behaviour in light stall conditions, which increases directly the flight envelope of a helicopter [68]. The behaviour of the Gurney flap is related to its length and placement. Studies about the length of the Gurney flap show an increase in drag and pitching moments with increasing lengths [38, 53, 63, 68]. Depending on the application, the Gurney flap length is limited to the point where these disadvantages outweigh its benefits in lift and stall characteristics.

Furthermore, the Gurney flap can have a positive effect on blade-vortex interaction. Similarly to a trailing edge flap, the Gurney flap acts on the blade mechanical behaviour [68]. Actuating the Gurney flap at 2/rev with suitable control would lead to a decrease in vibration and noise in a similar way than active trailing edge flaps [69].


**4.7 Flow properties**

Flow property of material can be affected by a number of factors including frictional forces, surface tension forces, electric forces, and van der Waals forces.

Efficient flow of drug substance powder is needed for effective tablet formulation. The main reason behind inclusion of this parameter in preformulation is its linkage with other physical parameters like hygroscopicity and particle size and shape. Importance of flow property is even more when dose loading is more.

**Table 6** gives outline on correlation of flow properties of a material with moisture uptake at different humidity levels.

Normally, flow property of solid drug substance can be measured by Hausner ratio, Carr's index, and angle of repose, and in case of liquids or semisolid, rheology and thixotropy. Carr's compressibility index can be represented by the following formula.

$$\text{xotropy. Carr's compressibility index can be represented by the following formula}$$

$$\text{Carr's compressibility index} = \frac{\text{Tapped density - Bulk density}}{\text{Tapped density}} \times 100.\tag{3}$$

Hausner's ratio can be represented by the following equation:

$$\text{Hausner's ratio can be } \texttt{Teprecium} \text{ and by the following equation:}$$

$$\texttt{Hausner's ratio} = \frac{\texttt{Tapped density}}{\texttt{Bulk density}}.\tag{4}$$

**Table 7** provides the correlation between Carr's index, Hausner's ratio, and flowability.

Another way of measuring flow property is angle of repose, which provides the idea resistance to the movement of particle. It can be represented by the following formula:

$$
\tan \Theta = \mathcal{Z}h/D \tag{5}
$$

**17**

*Preformulation Studies: An Integral Part of Formulation Design*

It is the maximum angle that can be obtained between height of pile and a horizontal plane. It gives a brief idea about internal cohesive and frictional levels. There

Excipients are added along with the active pharmaceutical ingredient in formulations. Most excipients possess biological activity but having role in administration, mediating the release of the active component, and providing stability against degradation. However, inappropriate excipients can also give rise to inadvertent and/or unintended effects, which can affect the chemical nature, the stability, and the bioavailability of the API, and consequently, their therapeutic efficacy and safety. So study about interaction between active ingredient and inactive ingredient can provide idea about type of incompatibility and the justification behind the

are basically two types of methods that are available, which are as follows:

*DOI: http://dx.doi.org/10.5772/intechopen.82868*

Static angle of repose

1.Fixed funnel method

2.Fixed cone method

2.Tilting box method

Dynamic angle of repose

1.Rotating cylinder method

**5. Drug excipient compatibility**

inactive ingredient selection [14].

**5.1 Physical incompatibility**

• Change in organoleptic properties of formulation.

• Decreased potency of active ingredient.

• Generation of toxic degradation product.

• Changes in in vivo performance of formulation, that is, dissolution.

• Change in physical appearance of formulation, that is, color, phase conversion.

In general, one can say that drug-excipient incompatibility may result in change in

In such an instance, active pharmaceutical ingredient and excipients interact without undergoing changes involving like breaking or formation of new bonds. The resulting drug product retains its original chemical properties but may involve changes such as alteration in physical properties. Such interaction results in changes like change in color, odor, flow properties, and sedimentation rate. Such an example of physical incompatibility is between tetracycline and calcium carbonate. It results in formation of insoluble complex with calcium carbonate, leading to slower dis-

physical, chemical, microbiological, or therapeutic properties of formulation.

solution and decreased absorption in the gastrointestinal tract [15].

#### **Table 6.**

*Correlation between relative humidity, moisture uptake, and flowability.*

#### **Table 7.**

*Correlation between Carr's index, Hausner's ration, and flowability.*

*Preformulation Studies: An Integral Part of Formulation Design DOI: http://dx.doi.org/10.5772/intechopen.82868*

It is the maximum angle that can be obtained between height of pile and a horizontal plane. It gives a brief idea about internal cohesive and frictional levels. There are basically two types of methods that are available, which are as follows:

Static angle of repose

*Pharmaceutical Formulation Design - Recent Practices*

uptake at different humidity levels.

property of drug.

flowability.

formula:

**Table 6** gives outline on correlation of flow properties of a material with moisture

• In case of hygroscopic material, flow property of drug tends to deteriorate as

• Irregular particle size and nonuniform shape can also disturb normal flow

Carr's index, and angle of repose, and in case of liquids or semisolid, rheology and thixotropy. Carr's compressibility index can be represented by the following formula. Carr� s compressibility index = Tapped density − Bulk density \_\_\_\_\_\_\_\_\_\_\_\_\_\_\_\_\_\_\_\_\_\_\_ Tapped density × 100. (3)

**Table 7** provides the correlation between Carr's index, Hausner's ratio, and

Another way of measuring flow property is angle of repose, which provides the idea resistance to the movement of particle. It can be represented by the following

tanθ = 2*h*/*D* (5)

40 0.35 Base of powder adheres to the container

**Relative humidity (%) Moisture uptake (%) Flowability** 0.30 Free flowing 0.24 Free flowing 0.27 Less free flowing

80 0.62 Cake formation

**Carr's index Hausner's ratio Flowability** 5–15 1.05–1.18 Excellent 12–16 1.14–1.20 Good 18–21 1.22–1.26 Fair-passable 23–35 1.30–1.54 Poor 33–38 1.50–1.61 Very poor Greater than 40 Greater than 1.67 Very very poor

*Correlation between Carr's index, Hausner's ration, and flowability.*

*Correlation between relative humidity, moisture uptake, and flowability.*

Normally, flow property of solid drug substance can be measured by Hausner ratio,

Bulk density . (4)

the presence of absorbed moisture increases cohesiveness.

Hausner's ratio can be represented by the following equation:

Hausner� s ratio = Tapped density \_\_\_\_\_\_\_\_\_\_\_\_

**16**

**Table 7.**

**Table 6.**

Dynamic angle of repose


**Effect of the Er, Cr: YSGG Laser Parameters on Shear Bond Strength and Microstructure on Human Dentin Surface**

Eun Mi Rhim1, Sungyoon Huh2, Duck Su Kim3, Sun-Young Kim4, Su-Jin Ahn5, Kyung Lhi Kang6 and Sang Hyuk Park4,7 *1The Catholic University of Korea, St. Paul's Hospital, Dept. of Conservative Dentistry, Seoul, 2Shingu University, Dept. of Dental Hygiene, Seongnam, 3Kyung Hee University, Dental Hospital, Dept. of Conservative Dentistry, Seoul 4Kyung Hee University, Dept. of Conservative Dentistry, Seoul, 5Kyung Hee University, Dental Hospital at Gandong, Dept. of Biomaterials & Prosthodontics, 6Kyung Hee University, Dental Hospital at Gandong, Dept. of Periodontology, 7Kyung Hee University Dental Hospital at Gandong, Dept. of Conservative Dentistry Korea*


**Age Moderates the Effect of Injury Severity on Functional Trajectories in Traumatic Brain Injury: A Study Using the NIDILRR Traumatic Brain Injury Model Systems National Dataset**

**Laraine Winter 1,2,\*, Janell L. Mensinger 3, Helene J. Moriarty 1,2, Keith M. Robinson 4, Michelle McKay 2 and Benjamin E. Leiby 5**

**Abstract:** Age is a risk factor for a host of poor outcomes following traumatic brain injury (TBI), with some evidence suggesting that age is also a source of excess disability. We tested the extent to which age moderates the effect of injury severity on functional trajectories over 15 years post injury. Data from 11,442 participants from the 2020 National Institute of Disability and Independent Living Rehabiitation Research (NIDILRR) Traumatic Brain Injury Model Systems (TBIMS) National Dataset were analyzed using linear mixed effects models. Injury severity was operationally defined using a composite of Glasgow Coma Scale scores, structural imaging findings, and the number of days with post-trauma amnesia. Functioning was measured using the Glasgow Outcomes Scale-Extended. Age at injury was the hypothesized moderator. Race, ethnicity, sex, education, and marital status served as covariates. The results showed a significant confounder-adjusted effect of injury severity and age of injury on the linear slope in functioning. The age effect was strongest for those with mild TBI. Thus, the effects of injury severity on functional trajectory were found to be moderated by age. To optimize outcomes, TBI rehabilitation should be developed specifically for older patients. Age should also be a major focus in TBI research.

**Keywords:** brain injury; traumatic; age; functional impairments; recovery trajectory; injury severity


**1. Introduction**

Biodiesel is obtained predominantly by transesterification (chemically or enzymatic) of vegetable oils and animal fats and is known for its energy security awareness. It is composed of free fatty acid alkyl esters and has low toxicity and high biodegradability [1]. Biofuels are a clean energy source, whose combustion emits ≈ 35% fewer greenhouse gases compared with diesel fuel [1,2]. However due to technological limitations, biodiesel's cost is still higher than fossil diesel [1].

The transesterification of a variety of materials that contain fatty acids that include various vegetable and animal fats, vegetable oils, and edible oil processing residues such as soybean [3], sunflower [4], palm [5], rapeseed [6], canola [7], Jatropha, and cottonseed [8–10] generates a large amount of glycerol waste. For instance, for each 10 kg of biodiesel produced, 1 kg of glycerol is generated [11]. The increase of biodiesel production has, as a consequence, an increase of glycerol production. Solutions for this glycerol must be found [12–15] to ensure the economic feasibility of biodiesel. Yet this crude glycerol cannot be used in most of the traditional applications of glycerol such as food [16–19] and pharmaceutical industries [20–23], personal care products [24–26], anti-freezers [27,28], e-cigarette liquids [29–31], explosives [32] and many other processes as an intermediate compound [33–35] due to its poor quality. Additionally, the use of crude glycerol has been gaining ground as a component of heavier fuels and in the processes of obtaining acrylic acid [36]. A much less explored possible use of crude glycerol concerns the development of new solid materials generating high-value products. Coal is traditionally produced from waste, thus adding value to the residue [37,38]. However, the use of glycerol as a precursor in the preparation of carbon materials (carbon and activated carbon, Figure 1) is

**Citation:** Batista, M.; Carvalho, S.; Carvalho, R.; Pinto, M.L.; Pires, J. Waste-Glycerol as a Precursor for Carbon Materials: An Overview. *Compounds* **2022**, *2*, 222–236. https://doi.org/10.3390/ compounds2030018

Academic Editor: Juan C. Mejuto

Received: 23 June 2022 Accepted: 9 September 2022 Published: 16 September 2022

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

33

relatively new and unexplored in comparison with other precursors such as rapeseed [37], potato peel [38,39], sugarcane bagasse [40,41], waste coffee residues [42,43], waste rice husk [44,45], and waste corn [46,47], etc. The glycerol-based carbon materials are obtained in one step by in situ partial carbonization and sulfonation of glycerol with sulfuric acid. In turn, glycerol-based activated carbon materials are prepared in two steps: (i) partial carbonization and sulfonation of glycerol in the presence of sulfuric acid; (ii) chemical or thermal activation of the glycerol-based carbon material. The main advantages of the coal obtained from glycerol are the sulfonic acid groups on the material surface, which give them specific properties for diverse environmental applications such as catalyst, capacitor, and adsorbent materials. This review collected the existing data about the production and use of carbons from glycerol. Despite their potential, most of the research is not contemporary. We intended to show the potential and arouse the interest for this type of material, thus allowing the development of more effective glycerol-based carbons. The synthetic method of the glycerol-based carbons investigated is the same with few variations in the experimental conditions. More in-depth research into the synthesis may lead to carbons with improved properties for the desired applications. The use of these carbons in catalysis is the most explored application. Still, activated carbons have much potential as adsorbents of pollutants and capacitors, yet they are unexplored, and new research is needed, as may be seen in this review. In this work, we intended to call the attention of scientists in the area by showing the potentialities of this by-product in developing advanced carbon materials and promote research in an area with great potential.

**Figure 1.** Synthesis of glycerol-based carbons and their main applications.

#### **2. Synthesis of Glycerol-Based Carbon Materials**

The synthesis of carbons from glycerol is a relatively new area concerning the use of glycerol. It mainly consists of the partial carbonization and sulfonation of glycerol with sulfuric acid. The main differences observed in the literature concerning the synthesis of carbons are variations in experimental conditions such as glycerol: sulfuric acid mass ratio, reaction temperature, and time. The paper of Devi et al. published in 2009 [48] was the first to synthesize carbon from glycerol. It used the one-pot reaction shown in Figure 1. The partial carbonization and sulfonation of glycerol were carried out with concentrated sulfuric acid (1:4 w/w) using soft experimental conditions. First, the glycerol and sulfuric acid mixture was heated to 180 ◦C. The mixture was kept at this temperature until foaming ceased. Then, the product was cooled to room temperature and washed with hot water under agitation until reaching neutral pH value. Two years later, the same authors synthesized other carbon using the same procedure but used pitch glycerol as a carbon source and at a different temperature (250 ◦C) [49]. The reaction yields were 50% and 40%, respectively, and no explanation for why a higher temperature had to be used for this last procedure was presented. The carbons were fully characterized by a great diversity of techniques (elemental analysis, X-ray photoelectron spectroscopy (XPS), X-ray Powder Diffraction (XRD), scanning electron microscopy (SEM), Fourier Transform InfraRed (FTIR), Magic-angle spinning (MAS) NMR 13C, Raman, potentiometric titrations, N2 isotherms, and thermogravimetry/differential thermal analysis (TG/DTA). The obtained carbons had a non-porous nature (<1 m2·g−1), a high density of sulfonic acid groups (–SO3H), and their catalytic capacity in the esterification of palmitic acid, tetrahydropyranylation, and dehydropyranylation was evaluated (See Section 3.1 for more details).

Mantovanic et al. [50] and Gonçalves et al. [51] prepared carbons by hydrothermal carbonization using a mixture of glycerol waste and sulfuric acid (different mass ratio) at 150 ◦C or 180 ◦C and using several reaction times (0.25–24 h). Interestingly, the authors successfully increased the number of sulfonic groups using sulfuric acid in a post-synthesis treatment [51]. The carbons also had a non-porous nature and a high numbers of acidic surface groups and were tested as catalysts in acetalization and etherification reactions (see Section 3.1 for more details).

The synthetic procedure described gives rise to non-porous carbons whose main application is in catalysis. For other applications, such as adsorption, the development of a porous structure is crucial. Typically, the synthesis of activated carbons from glycerol requires two steps, carbonization, followed by an activation step [52–54]. Some examples of those activated carbons obtained via chemical activation (KOH, ZnCl2, and H3PO4) [52,53] and thermal activation [55,56] may be found in the literature. Different activation agent ratios and temperatures have been tested to vary the porosity of the obtained materials. For instance, the group of Ribeiro et al. [56], after obtaining the carbon using the already described procedure, carried out further calcination (120 ◦C, 400 ◦C, 600 ◦C—60 min in each temperature, plus 800 ◦C—240 min) under nitrogen flow. The obtained material showed high thermal stability, a basic character due to the decomposition of the sulphonic acid groups, and non-porous nature. This material was then thermally activated under an air atmosphere at different temperatures (150 ◦C, 200 ◦C, 300 ◦C, and 350 ◦C) for 1 h and generated porosity which increased with the temperature as shown in Figure 2. Additionally, the increase in temperature in the surface oxygen groups (lactones, phenols, and quinones) increases its acid character. Although rare, this work used activated carbons in the catalytic wet peroxide oxidation (CWPO) of 2-nitrophenol (See Section 3.1 for more details).

**Figure 2.** Influence of the activation temperature in the generation of porosity and development of microporosity.

Another way of obtaining porous carbons may be using a pore-forming agent. The work of Lee et al. [57] used a pure glycerol and crude waste glycerol as a carbon precursor for mesoporous carbon. It also explored glycerol as a pore-forming agent for mesoporous silica. The mesoporous carbon was obtained by the carbonization of glycerol–silica nanoparticles at high temperatures (600 ◦C) under a nitrogen atmosphere. NaOH solution was used for the removal of the silica–nanoparticle framework. By simply changing the silica particle size in glycerol–silica nanocomposites or changing the silica particle size, it was possible to tailor the pore size and volume, surface area, and pore wall thickness of mesoporous carbon. Due to the presence of other components that may also act as a pore-forming agent in the crude waste glycerol, its use in the synthesis leads to a multimodal pore size distribution of micropores smaller than 2 nm, small mesopores centered at 3.8 nm, and large mesopores above 10 nm.

To the best of our knowledge, the work published in 2016 by Álvarez-Torrellas et al. was the first to study the application of glycerol-based activated carbons as adsorbent materials [55]. The synthesis consisted in the partial carbonization of a glycerol– sulfuric acid mixture, followed by thermal activation. A glycerol and sulfuric acid mixture was heated to 180 ◦C for 20 min. The resulting material was calcinated in a tube furnace under a nitrogen flow (100 cm3·min−1) at different temperatures (120 ◦C, 400 ◦C and 600 ◦C) during 60 min and 800 ◦C during 240 min. Then the calcined material (GBCM) was thermally activated at different temperatures (200 ◦C, 300 ◦C and 350 ◦C, for 60 min) in a tube furnace under oxidative atmosphere (flow of 100 cm3·min−1). The textural properties were studied by N2 adsorption-desorption isotherms. The presence of the oxygenated groups was investigated by zeta potential and FTIR data. All obtained acid activated carbons (GBCM200, GBSM300 and GBCM350—where the subscript represents the activation temperature) presented high surface area and microporous structure developed. Their adsorption capacities were evaluated through flumequine and tetracycline (See Section 3.2 for more details).

Cui et al. [54] investigated glycerol as a liquid precursor for the preparation of activated carbon. The authors concluded that glycerol pyrolysis in the absence of acid generates no carbon material. This was justified by the evaporation of glycerol (boiling point of 290 ◦C) before it was carbonized. The description of different acids' roles and the absence of acid in carbon formation was reported. For this effect, glycerol was mixed with an acid (H2SO4, H3PO4, HCl, or CH3COOH) at volume ratios (10:1, 10:2 and 10:3 v/v). The solutions were added to a quartz boat and heated on the tube furnace in N2 atmosphere to 400 ◦C, 500 ◦C, 600 ◦C, 700 ◦C, or 800 ◦C for 1 h. The glycerol pyrolysis in the presence of HCl or CH3COOH did not produce carbon material. However, with H2SO4 or H3PO4 addition, glycerol pyrolysis generated carbon materials. According to the authors, the glycerol is dehydrated and polymerized when exposed to the presence of acids (H2SO4 or H3PO4) at moderate temperatures (<200 ◦C). Both acids induce dehydration of alcohol groups via protonation of the alcoholic oxygen (Figure 3).

**Figure 3.** General representation of the polymerization reaction.

In the case of HCl, it has a low boiling point (48 ◦C), and in the case of CH3COOH, because it is a weak acid, it cannot initiate the glycerol dehydration. In this context, carbon materials with various functional groups and porosities were prepared via sulfuric or phosphoric acid-mediated polymerization and carbonization followed by steam or CO2 activation. The porosity in the activated carbons reached surface areas up to 2470 m2·g−1 and pore volumes up to 1.44 cm3·g−1. The samples prepared with H3PO4 were consistently more mesoporous than samples prepared with H2SO4. The adsorption capacity of those materials was evaluated for the removal of gas phase volatile organic compounds (VOCs) and aqueous phase chromium Cr(VI) (See Section 3.2 for more details).

Naverkar et al. [58] prepared glycerol-based carbon by partial carbonization of glycerol using concentrated sulfuric acid (molar ratio 1:4) followed by thermal treatment. The sulfuric acid was added dropwise to glycerol (10 g) and stirred for 20 min at 180 ◦C. The carbonized material was further treated at 120 ◦C and 350 ◦C to obtain the samples GBC-120 and GBC-350. The carbon materials were characterized by XRD, FTIR, thermal analysis (TG/DTG/DTA), pHPZC measurements, SEM, and N2 adsorption-desorption at low temperature. The samples GBC-120 and GBC-350 presented BET surface areas of 21 m2·g−1 and 464 m2·g−1, respectively. They were studied for the adsorption of methylene blue (See Section 3.2 for more details).

Gonçalves et al. [53] also prepared glycerol-based activated carbon via two steps (polymerization + chemical activation). Firstly, the glycerol polymer was prepared by glycerol polymerization under reflux in the presence of sulfuric acid. The glycerol polymer was chemically activated with ZnCl2 or H3PO4. The authors also investigated several activated carbon synthesis conditions such as the type of activating agent (ZnCl2 or H3PO4), the impregnation ratio (ZnCl2 (*X*Zn = 0.4 and 0.8) and H3PO4 (*X*P = 0.3 or 0.6) activating agent mass/polymer mass), activation time, and temperature. They were evaluated as supercapacitor electrode and for the adsorption of organic contaminants (See Sections 3.2 and 3.3 for more details).

Glycerol-based magnetic carbon composites were synthesized by Medeiros et al. [59]. The carbon composites were prepared by mixing glycerol waste and iron(III) salt (heating to 380 ◦C, 600 ◦C, or 800 ◦C) for 3 h in a vertical reflux reactor. The textural properties of GFe3-380 (5 m2·g−1), GFe3-600 (140 m2·g−1), and GFe3-800 (136 m2·g−1) composites were evaluated by N2 adsorption–desorption isotherms. The carbon composites presented the following surface area 5 m2·g−1 (GFe3-380), 140 m2·g−1 (GFe3-600) and 136 m2·g−1 (GFe3-800). According to the pore size distribution for composites, the samples GFe3-600 and GFe3-800 contain both micropores and mesopores (essentially). The composites (GFe3-600 and GFe3-800) were tested as adsorbents of dyes (methylene blue and indigo carmine) (See Section 3.2 for more detail).

More recently, Batista et al. [52] prepared a series of glycerin-activated carbons from crude glycerin (82% glycerol) for application in the gas separation by adsorption processes. Glycerin-activated carbons were prepared via a two-step procedure involving carbonization followed by chemical activation with KOH. A mixture of industrial crude glycerin (82% glycerol) and concentrated sulfuric acid was prepared using a volume ratio of 1:0.5 (glycerol:H2SO4). The acid carbonization process was carried out in a Teflon lined Hydrothermal Autoclave at 180 ◦C for 6 h in an oven. The carbonized (glycerin-char) was washed with distilled water until the washing was neutral and dried (100 ◦C); The obtained solid (glycerin-char, crushed to fine powder of dimension < 0.297 mm) was mixed with an activating agent (KOH) in distilled water, been stirring for 2 h (at ambient temperature) and when dried (100 ◦C). It was used two activation temperatures (700 ◦C and 800 ◦C) and weight ratios (1:1, 2:1 and 3:1, KOH:glycerin-char). The mixture (activating agent:glycerin-char) was activated in a horizontal furnace Thermolyne 21100 (under N2 flow 5 cm3·s−1 and 10 ◦C·min−1·h−1). The glycerin-activated carbons were washed with distilled water until the washing was neutral and dried at 100 ◦C. The prepared samples (G@700/1, G@700/2, G@700/3 and G@800/1, G@800/2 and G@800/3—the 700/800 corresponds to the activation temperature and the 1, 2 and 3 to the KOH:glycerin-char ratio) presented high surface areas (1166–2150 m2·g−1) and pore volumes between 0.63 and 1.03 cm3·g−1. These glycerin-activated carbons were evaluated as adsorbents for the adsorption separation of ethane and ethylene (See Section 3.2 for more details).

In another work, Batista et al. [60] modified a glycerin-activated carbon and zeolite type A surfaces with chitosan. The purpose of this work was different from the other works presented here. It was to evaluate the potential of those materials as H2S donors for therapeutic application. The activated carbon (Gta@600) was prepared by a combination of acid carbonization with H2SO4 followed by thermal activation (in a nitrogen flow rate = 5 cm3·min−1 at 600 ◦C for 1 h). The modification of the material surface was obtained by adding chitosan dissolved in acetic acid solution (1 wt%). to a suspension of Gta@600. The chitosan-based carbon (Gta@600Chi) was characterized (FTIR, SEM, XDR, Elemental analysis and N2 adsorption–desorption isotherms). The adsorption capacity of H2S by Gta@600 and Gta@600Chi was performed to evaluate their use as H2S donors (See Section 3.2 for more information).

#### **3. Principal Uses of Carbons from Glycerol**