Regional Studies in Marine Science 45 (2021) 101844

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Regional Studies in Marine Science

journal homepage: www.elsevier.com/locate/rsma

Application of IUCN Red List of Ecosystems to assess the ecological

status of marine bar ecosystems of Burullus wetland: A Ramsar site
∗
Somaya Magdy M. Ghoraba, Marwa Waseem A. Halmy , Boshra B. Salem,
Nadia Badr E. Badr
Department of Environmental Sciences, Faculty of Science, Alexandria University, Alexandria, Egypt

article info a b s t r a c t

Article history: The IUCN Red List of Ecosystems has been employed to assess the status of ecosystems and evaluate
Received 4 March 2021 the risk of their collapse. The RLE assessment was conducted on the main ecosystems of the marine
Received in revised form 12 May 2021 bar of Burullus wetland; sand plain and salt marshes ecosystems of the marine bar which separates the
Accepted 13 May 2021
lake from the Mediterranean Sea. Four criteria were used for conducting the assessment; (A) reduction
Available online 15 May 2021
in distribution, (B) constricted distribution, (C) abiotic components degradation, and (D) disruption of
Keywords: biotic processes and interactions. The integration of remotely-sensed data allowed the application of
Salt marshes RLE to study the changes in ecosystems distribution for Criteria A and B. Criterion A showed the same
Sand plain result for sand plain and salt marshes as Critically Endangered (CR). This indicates the distribution
Sand dunes of the marine bar is extremely affected by the urban and human activities in the region. It is also
Ecosystem collapse expected to be affected by any slight changes in the sea-level and costal erosions in the future in
Ecosystem assessment terms of disruption in biotic processes and interactions. Criteria D was applied using floristic quality
assessment for current floristic composition and the available historic data. The results show that
sand plain and salt marshes are Near Threatened (NT). However, the application of Criteria C was Data
Deficient DD due to lack of long term data about the abiotic variables responsible for environmental
degradation. The identical results of RLE assessment of sand plain and salt marshes reflect that both
ecosystems are equally affected by the ongoing activities in the region, particularly over the last few
years. The results indicate that the marine bar ecosystems were disturbed by anthropogenic events
such as urban development, grazing and farming. Also natural events such as climate change and its
consequences are expected to have severe impacts on the marine bar in the future. Therefore, further
studies should focus on the study of the main interactions and processes in the marine bar ecosystems.
© 2021 Elsevier B.V. All rights reserved.

1. Introduction then utilized in assessing the state of various ecosystems across

Alterations to natural ecosystems are mostly irreversible caus-
ing changes to the diversity of species on Earth, and finally lead to
loss of biodiversity. These changes were more obvious and rapid
in the past fifty years (MA, 2005a). Projections and prediction sce-
narios indicate that these rates will accelerate and exacerbate in
the future (MA, 2005b). Therefore, proactive actions and plans to
maintain sustainable ecosystems are urgently required to prevent
further degradation of ecosystem’s goods and services or reaching
a state of collapse (MA, 2005a). Launching and developing a
protocol for assessing the status of ecosystems recognized as the
Red List of Ecosystems (RLE) was a major step by the International
Union for Conservation of Nature (IUCN) (Keith et al., 2015;
Bland et al., 2017; Ghoraba et al., 2019). The RLE protocol was
∗ Correspondence to: Department of Environmental Sciences, Faculty of
Science, Moharm Bek P.O. Box: 21511, Alexandria, Egypt.
E-mail address: marwa.w.halmy@alexu.edu.eg (M.W.A. Halmy).
the world. To date it has been used for assessing over 2800
ecosystems in more than 100 countries (Bland et al., 2019). It
implies the application of five standard criteria to estimate the
changes in spatial symptoms (Criteria A and B) and functional
symptoms (Criteria C and D) of ecosystem change. The application
of these criteria enables the estimation of the risk category based
on the calculation of relative severity for each criterion. Finally,
the overall risk category can be inferred (Rodriguez et al., 2002;
Marshall et al., 2018; Bland et al., 2016; Ghoraba et al., 2019).
The levels of risk are categorized into Critically Endangered, En-
dangered, Vulnerable levels, or Least Concern. An ecosystem can
be considered as Least Concern. However, if the ecosystem has
lost its defining biotic and abiotic features, hence, it is defined as
collapsed (Keith et al., 2013a).
Burullus Protected Area (BPA) lies near to the Mediterranean
Sea on the fringe of the Nile Delta of Egypt. It was declared as
a national protected area in 1998 (Khalil, 2013). The protected
area encompasses Burullus wetland area along with many islets

https://doi.org/10.1016/j.rsma.2021.101844
2352-4855/© 2021 Elsevier B.V. All rights reserved.
S.M.M. Ghoraba, M.W.A. Halmy, B.B. Salem et al.
within Burullus Lake and the flat sand bar at the north. The
sand bar has different geomorphologic features forming different
ecosystems including sand flats, sand dunes, sand hillocks and
salt marshes. The wetland also bears a community of reedbeds.
The wetland was also declared as an International Important Bird
Area (IBA) and Ramsar site since 1988 (Khalil, 2018). The risk
category of Burullus wetland was assessed using IUCN RLE in a
study conducted by Ghoraba et al. (2019). The study revealed
that Burullus Wetland was categorized as Endangered (EN). Such
result revealed that the area of Burullus wetland was at very
high risk of collapse due to unwise activities that are going on
within the region. This is expected to affect the whole ecosystems
surrounding the wetland. The marine bar is the extended sand bar
that separates the wetland from the Mediterranean Sea (Fig. 1).
The sand bar has different geomorphologic features forming dif-
ferent ecosystems including sand plain and salt marshes. The
marine bar takes an oblong outline with an area of approximately
165 km2 extending for about 47 km along with a coastline of
about 65 Km. Its width is not constant from east to west; it
varies between 5 and 11 km (Shaltout and Khalil, 2005; Khalil,
2013, 2018). This study attempts to apply the IUCN RLE criteria
and categories to evaluate the status of the main ecosystems of
the marine bar of Burullus Wetland including sand plain and salt
marshes. The study identifies the main threats within the study
area and estimates how these threats affected the habitats of
sand plain and salt marshes in terms of their spatial distribu-
tions and biotic processes and interactions. The application of
IUCN RLE entails the compilation of the necessary datasets and
information for conducting the assessment, which then can be of
great help in supporting proper conservation and management
of natural ecosystems. The assessment requires assembling long-
term datasets about the key processes and interactions; and the
abiotic and biotic components of the ecosystems. The application
of the RLE provides guidelines for data acquisition for data defi-
cient categories that need to be fulfilled. Through applying the
standard criteria of the RLE, evaluation of the current state of
the ecosystems and identification of ecosystems that are mostly
at risk of collapse on the national level will be obtained. The
outcomes will provide insights to the decision makers to help
prioritize conservation actions to the most threatened ecosystems
and will help in managing land use planning and development
actions that mostly affect the ecological status of the marine bar
ecosystems. It is worth mentioning that lack of long-term data is
one of the main obstacles to the proper application of the IUCN
RLE assessment to the marine bar ecosystems.
2. Ecosystem description
The ecosystem description of the study area was compiled
from literature and available data to follow the standard elements
of IUCN RLE. The collected data was used to identify the main
ecosystem components and define the threats within the study
area.
2.1. Sand plain ecosystem
2.1.1. Classification
The sand plain ecosystem is classified nationally, internation-
ally and to the IUCN habitat classification as follows:
National classification: national protected area.
International classification Ramsar site and International Bird
Area (IBA)
IUCN habitat classification (Version 3.0): 13. Marine/
13.3.coastal sand dunes
2
Regional Studies in Marine Science 45 (2021) 101844
2.1.2. Abiotic environment
The sand plain ecosystem at Burullus wetland represents the
principal geomorphologic feature affected by the sedimentation
processes and is well-known by its distinguished sand dunes.
There is a close relation between the locations of the sand dunes
and the ancient Nile Deltaic branches. The coastal sand dune are
sand formations which were predominantly formed by the action
of the western winds through mixing the deposits of the ancient
Nile Deltaic branches and the marine deposits transported by
the marine currents (Bayomi, 1999). A belt of coastal dunes
extends to the south along the coast between the Baltium and
Burg El-Burullus village, where it is now encircled by a recently
established international highway (El Banna, 2004).
2.1.3. Distinctive native biota
About 45 plant species were recorded in sand plain ecosystem
by Shaltout and Khalil (2005) 60% of them are perennials and the
rest are annuals. The most distinctive species include Cistanche
phelypaea, Convolvulus lanatus, Cornulaca monacantha, Cyperus
capitata, Elymus farctus, Heliotropium curassavicum, Orobanche cer-
nua, Panicum turgidum, Silene succulenta, Bromus catharticus, Cak-
ile maritima and Fagonia arabica.
2.1.4. Processes and interactions
Sand is drifted along the coast by waves, wind, and current
action. High energy waves usually erode sand from the beach to
be deposited offshore as submerged sand bars. While, the low
energy waves take sand from seaward sources and deposit it on
the seashore to form the beach bar in the form of low sand dunes
aligned parallel to the coastline. By the time plants and other
material on the bar entrap windblown sand from the seashore
leading to expansion in the bar width and increase in its height
to form higher coastal dunes (O’Keefe, 1978; El Banna, 2004).
Offshore, consecutive seashore berms might be formed, develop
overtime to create a sequence of dunes aligned parallel to the
shoreline. The seawards side of the forefront dunes is reduced
by the action of storm waves and currents. At period of calm
weather, currents develop-up a new bar that will be parallel to
the original forefront dunes. Sand fixing plant species colonize the
new berm and accumulate windblown sand, and a new series of
fore dunes is built up (Bird, 1972; El Banna, 2004).
2.1.5. Threats
The undisturbed system of dunes acts as a flexible coastal
barrier against sea erosion. However, the system is disturbed
during wave attack that sand is lost to form off-shore bars. It
may build up through calm weather as the plants on the beach
entraps windblown sand that has been deposited by current
actions (El Banna, 2004). The coastal dune areas are threatened
by urban expansion and construction of the international coastal
highway, land reclamation projects and establishment of fish
farms (El-Asmar and Al-Olayan, 2013). Coastal dunes of Burullus
wetland could also be vulnerable to the impacts of the expected
sea level rise (El Banna, 2008). That was noticed in the remnant
fore dunes which are subjected to severe erosion by seawater
floods. The coastline east of Burg El Burullus village and Baltium
resorts are receding quickly due to seawater over-overflowing
leading to continuous to cutting back of the dunes (Fanos et al.,
1995; El Banna, 2004). Table 1 illustrates the main threats in the
area of the marine bar.
S.M.M. Ghoraba, M.W.A. Halmy, B.B. Salem et al. Regional Studies in Marine Science 45 (2021) 101844

Fig. 1. Location of Burullus wetland and the marine bar.

Table 1 2.2.2. Abiotic environment

The main threats to the marine bar ecosystems according to IUCN threats Coastal salt marshes are defined as lowlands near the coasts,
classification Scheme version 3.2 (2015).
covered with water during the tide and with high salinity particu-
1. Residential and commercial development
larly with the increase of evaporation rate. The clay deposits vary
1.1 Housing and urban areas
between 60 and 80%, which may indicate that the origin of these
Ex: Land reclamation on the western side
Ex: building residential areas marshes were associated with the primary stages of the initiation
of the whole region (Shaltout and Khalil, 2005).
2. Agriculture and aquaculture
2.1 Annual/ perennial crops
2.1.4. scale unknown/unrecorded
2.2.3. Distinctive native biota
2.3. livestock and farming Natural vegetation plays a key role in the creation and exten-
2.3.2. small holder grazing ranching or farming sion of salt marshes. The presence of natural vegetation acceler-
4. Transportation and service corridors ates evaporation rate and increases salinity (Shaltout and Khalil,
4.1. roads and railways Ex: highway 2005). Moreover, the heavy growth of salt tolerant plants traps
the deposits and help in leveling up the beds of the marshes.
5. Biological resource use
About 51 species inhabit salt marshes around Lake Burullus
5.1. Hunting and collecting terrestrial animals
5.1.1. intentional use
and provide key habitats for two important bird subspecies en-
Ex: hunting of waterfowl demic to Egypt which are the Lesser Short-Toed Lark (Calandrella
6. Human intrusion and disturbances
rufescens nicolli) that only known from north Nile Delta, and
Egyptian wagtail (Motacilla flava pygmaea) only known from the
6.1. Recreational activities
Ex: bird watching Nile Delta and Valley (Shaltout and Al-Sodany, 2008).
11. Climate change and severe weather
2.2.4. Processes and interactions
11.1. Habitat shifting alteration
Ex: Sea level rise
Salt marshes are formed due to geomorphologic processes
such as change in sea level rise. Tidal action is among the main
factors that cause the formation and development of salt marshes
along the marine bar of Lake Burullus. With the extension of
2.2. Salt marshes ecosystem water during tide and retreating during ebb-tide, and with the
gentle sloping of the shore, tidal waters extend to cover vast areas
that increase with the happening of storm waves (Shaltout and
Khalil, 2005). Fig. 2 summarizes the main ecological processes in
2.2.1. Classification
the marine bar ecosystems. The main threats to the ecosystem
National classification: national protected area are climate change and urban development which affect the
International classification: Ramsar site and International Bird geographic distribution of the marine bar ecosystems as well as
Area (IBA) the biotic and abiotic factors in the ecosystems. Climate change
has an impact on the environment through two abiotic processes;
IUCN habitat classification (Version 3.0): 12.Marine intertidal/
the sea level rise and erosion. On the other hand, urban develop-
12.5. Salt marshes (IUCN Habitat Classification Scheme version ment promotes the intrusion of new species including invasive
3.1, 2015) species which changes the species composition and lead to loss
3
S.M.M. Ghoraba, M.W.A. Halmy, B.B. Salem et al.
of characteristic biota in the ecosystem including the classes of
micro-fauna, plants, invertebrates, vertebrates and birds which all
interact and functioning together in the food chain.
2.2.5. Threats
Salt marshes ecosystem is exposed to human impact (Table 1)
including continued land reclamation (Shaltout and Al-Sodany,
2008). Moreover, climatic conditions can influence the edaphic
characteristics of salt marshes. The prevailing of dry weather
raises evaporation rate leading to boost in levels of salts in soil
(EEAA, 2009). Salt marshes are also vulnerable to rising sea level
because they are generally within a few centimeters above the
sea level (IPCC, 2007; Soliman and Ushijima, 2013).
3. Ecosystem collapse
The collapse state occurs when the ecosystem transformed
into different state other than its original state that it cannot sus-
tain its defining features (Bland et al., 2019). For the marine bar
ecosystems, the collapse state is assumed when the mapped dis-
tribution of the ecosystem diminishes to zero for both Criteria A
and B. Such reduction takes place when these ecosystems deteri-
orated and replaced due to land reclamation, urban development,
grazing and any other activities that reduce the boundaries of
the ecosystems. Such decline in the distribution will affect the
key process and interactions of the ecosystems, consequently
loss in biodiversity occurs. Assessing functional criteria of the
ecosystem was challenging due to the lack of regular monitoring
data of biotic and abiotic variables. It has been indicated that the
Nile Delta region where the marine bar ecosystem of Burullus
is stretched is one of the most seriously vulnerable regions to
the prospective impacts of sea level rise (El Raey et al., 1999). It
could be inferred that relative sea-level rise is possible indicator
for ecosystem collapse (El Banna, 2008; Soliman and Ushijima,
2013). Erosion is one of the main effects of sea level rise, which
is projected to be intensified leading to loss of considerable areas
of lands and properties (El Banna, 2008). The full understanding
of how biological and physical processes interact in response to
the sea level rise is still lacking (Alongi, 2008; Gilman et al., 2008;
Krauss et al., 2008; Marshall et al., 2018). Therefore, it was dif-
ficult to collect long-term data and set thresholds of collapse for
any of the possible variables for Criterion C. Assessing the changes
in the floristic quality based on the floristic quality indices can
provide a useful approach for evaluating ecosystem degradation
due to disruption of biotic processes and interactions (Criterion
D). The threshold of collapse for Criterion D was assumed when
the value of the floristic quality index measure is lower than
50%. When threshold of collapse is below 50%, the ecosystem
is expected to reflect severe deteriorations of floristic quality
due to replacement of native species as due to environmental
deterioration.
4. Methodology
The methodology followed the protocol of IUCN RLE to apply
the criteria based on data availability for sand plain and salt
marshes ecosystems.
4.1. Data compilation
4.1.1. Data for Criteria A and B
Remotely-sensed data were acquired to extract the changes in
the distribution of sand plain and salt marshes ecosystems over
time which is required for the estimation of Criteria A and B.
Satellite images were available for 1973, 1978, 2003, 2014, 2015
and 2016. The pre-processing and processing of satellite images
4
Regional Studies in Marine Science 45 (2021) 101844
was conducted using ERDAS-IMAGINE 14.0 software⃝ c (Hexagon
Geospatial, 2014) and ArcGIS 10.0 software⃝ c ESRI (ESRI, 2011).
The pre-processing techniques included geo-registration and ra-
diometric correction. Therefore, pre-processing is required to cor-
rect defects and remove of flaws (Mather and Koch, 2011). For
geo-registration, 2016 image was used to rectify the other images
using first order polynomial equation for coordinate’s transforma-
tion. Radiometric correction is essential to remove or reduce the
inconvenience of the recorded values by sensors and the spectral
reference and radiance of the objects (Li et al., 2008). The DN
values of the scenes representing the period between 1973 and
2003 were transformed to top-atmosphere reflectance values by
utilizing the standard equations and scaling factors employed to
Landsat data following Chander et al. (2009). The other acquired
satellite images from 2014 to 2016 were corrected according to
Landsat 8 Data User Handbook (USGS, 2016).
The maximum likelihood was the algorithm applied for su-
pervised classification of satellite images within ERDAS imagines
14.0 image processing package. The identification of the resulted
classes is based on the spectral response pattern of the pre-
selected training sites, in addition to ground trothing points. The
classification followed Anderson et al. (1976) system of LULC
classification which implies the selection of training sites rep-
resenting the land use/land cover (LULC) categories from known
locations on the ground. To deal with uncertainty of classification
of remotely-sensed data, the error or confusion matrix was used
(Card, 1982; Giri, 2012). It implies the measure of overall accu-
racy, Kappa coefficient, user’s accuracy and producer’s accuracy
and (Lu et al., 2004).
4.1.2. Data for Criterion D
The marine bar ecosystems are unique ecosystems represent-
ing the only remaining natural fragments of the Nile Delta (Galal
and Fawzy, 2007). The changes in the floristic quality can provide
an insight about the disturbances occurred to the ecosystem due
to anthropogenic activities and changes of land use over time. The
floristic quality assessment was conducted on the data obtained
through the field surveys and investigations made during the
current study and also to historic data assembled from available
literature.
Floristic quality indices are plant-based metrics which are
used to evaluate the ecological conditions according to the quality
of the habitat, in addition to providing a tool for monitoring
and assessing natural areas (DeBerry and Perry, 2015; Halmy,
2019). The assessment is applied by employing and integrating
metrics of richness with other measures of species tolerances
to disturbance and stressors (Miller and Wardrop, 2006; Halmy,
2019). The assessment is based on scoring the recorded plant
species for what is known as the coefficient of conservatism (C-
values). It assigns a value to each species from 0 to 10 depending
on the species fidelity to their habitat (Miller and Wardrop, 2006).
These values are assigned according to (Table 2) based on data
and information from the available literature. Two floristic qual-
ity indices were assessed, the floristic quality assessment index
(FQAI) and the adjusted floristic quality assessment index (ad-
justed FQAI) according to Lopez and Fennessy (2002), Rodriguez
et al. (2002) and Miller and Wardrop (2006). Data on the number
of the recorded non-native species were used to calculate the
adjusted FQAI values, which showed strong correlation with the
coefficient of conservatism (C-value) (Miller and Wardrop, 2006;
Halmy, 2019). The increase in the number of non-native species
can obviously impact the existence of native species because of
competition on the available resources, thus in turn result in
reduction in the quality of the natural ecosystems (Miller and
Wardrop, 2006).
Field surveys were carried out during March/April 2019. In
each field visit, the following data were recorded: species list,
S.M.M. Ghoraba, M.W.A. Halmy, B.B. Salem et al.
Fig. 2. Cause–effect model for the main ecological processes and interactions in the marine bar ecosystems of Burullus wetland. It shows the various components
of the ecosystem; the threats are illustrated in the red rectangles, the biotic components are shown in green polygons, the biotic processes are shown in green
oval-shaped polygons, the abiotic processes are shown in blue oval-shaped polygons and the compartment in the dotted box represents ecosystem components
functioning and interacting together.. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
geographic coordinates, habitat type, type of disturbance and
visual estimate of the distribution of each species. Identification
and nomenclature of species were done according to Boulos
(2009). Data were used to calculate both the FQAI and the Ad-
justed FQAI for the current state of the habitats on the marine
bar. To conduct the RLE, historic data about plant species were
compiled from previous work and literature and used to calculate
the FQAI and Adjusted FQAI for the historic states. Collection of
data was a challenge as the available historic data were very
restricted and insufficient to rely on for providing accurate and
reliable overview about the disturbance within the ecosystems.
However, it can be used as an indicator for the degree of threats
facing the ecosystem. Non-native species were determined fol-
lowing El-Kady (1993), Boulos and El-Hadidi (1994), El-Hadidi
(2000), Kassas (2002), Boulos (2009), Zahran and Willis (2009)
and Shaltout et al. (2016).
Regarding the sand plain habitat, literature data were available
from Zahran et al. (1990), Shaltout et al. (1995), Galal and Fawzy
(2007) and Shaltout and Al-Sodany (2008). For salt marshes,
the floristic quality assessment was conducted using data from
Zahran et al. (1990), Shaltout et al. (1995) and Shaltout and
Al-Sodany (2008).
4.2. RLE assessment
4.2.1. Criteria A and B
For Criterion A, the pace of decrease in an ecosystem distri-
bution might signify its path in the direction of collapse, with
ecosystem collapse habitually taking place when no spatial occur-
rences of the ecosystem type remaining (i.e. extent of distribution
collapses to zero) (Bland et al., 2017). Criterion A is estimated
according to four sub-criteria each at a different time frames;
(A1) over past 50 years; (A2a) over next 50 years; (A2b) over
any 50 year period including past, present and future; and (A3)
over historical period (since 1750) (Keith et al., 2013a). In the
current study, Criterion A is estimated under sub-criteria A2b by
using data from the analyzed satellite images over the periods
5
Regional Studies in Marine Science 45 (2021) 101844
1973–2014, 1978–2015 and 2003–2016. Assuming a constant
rate of change over each time frame, extrapolation of the col-
lected data was conducted to project changes for each time frame
over 50 years period by calculating the Absolute Rate of Decline
(ARD) and Proportional Rate of Decline (PRD) according to Bland
et al. (2017) using Eqs. (1) and (2) respectively as follows:
areat2 − areat1
ARD = (1)
yeart2 − yeart1
LN(areat2 /areat1 )
PRD = (2)
yeart2 − yeart1
where,
area t2 : area at the end time of assessment
area t1 : area at the initial time of assessment
year t2 : end time of assessment
year t1 : initial time of assessment
The outcomes were used to estimate percent of decline (%
decline) for 50 years period following Bland et al. (2017) equation
(3) to estimate the state of the ecosystem.
areat2
% of decline = (1 − ) × 100 (3)
areat1
For Criterion B, two standardized metrics are used to estimate the
state of the ecosystem; the first one is the Extent of Occurrence
(EOO) (sub-criterion B1). This metric measures the dispersion
of risk over particular area that include all incidences of an
ecosystem through using the area of a minimum convex polygon
that encompass the ecosystem. The second metric is the Area of
Occurrence (AOO) (sub-criterion B2) that measures the dispersion
of risk amongst occupied patches by counting up occupied grid
cells (Bland et al., 2017). Both metrics have been proven to be
useful indicators for forecasting the risk of ecosystem collapse
in landscapes facing many threats (Murray et al., 2017). The
application of Criterion B implied the use of the most recent
image of 2016 to estimate the EOO and AOO metrics.
S.M.M. Ghoraba, M.W.A. Halmy, B.B. Salem et al.
Table 2
Criteria used to assign the coefficient of conservatism (C-value) to species
identified in the marine bar of Burullus wetland.
Source: Halmy (2019).
C-Values Description
0 Weedy invasive species non-native to Egypt.
1 weeds native to Egypt, but non-native to the study area
2 Weed native to Egypt and the region, found in cultivated and
disturbed lands and many habitats, widespread and are not an
indicator of a particular community type.
3 Weed native to Egypt and the region, restricted to cultivated
lands, not an indicator of a particular community type.
4 Species native to the region, tolerate moderate disturbance,
found in almost all habitats, and show early phase of
succession of native community.
5 Species native to the region, tolerate moderate disturbance,
found in few (more than three) different habitats, and show
advanced phase of succession of native Community.
6 Species native to the region, tolerate moderate disturbance,
found in (≤3) habitats, and show advanced phase of
succession of native community
7 Species native to the region, found in almost natural habitats
with some disturbance, not restricted to one habitat, and show
more advanced phase of succession of native community.
8 Species native to the region, found in almost natural habitats
with little disturbance, not restricted to one habitat, and show
more advanced phase of succession of native community.
9 Species native to the region, with narrow ecological tolerance,
found in natural habitats with little or no disturbance. The
species has tolerance to a narrow range of ecological
parameters.
10 Rare native species confined to one habitat with little or no
disturbance including endemic species and species with
tolerance to ecological parameters.
4.2.2. Criterion D
Relative severity for Criterion D was calculated using the fre-
quency equation (4) following Keith et al. (2013b):
mo
Relative severity of degradation = ∗ 100 (4)
mt
Where, mt refer to the total number of cases, mo refer to number
of cases outside the collapse limit. This estimation was used to
evaluate the disruption in biological processes and interactions
in terms of reduction in floristic quality of species.
5. Results
5.1. Criteria A and B
In general the measures of accuracy revealed high accuracy of
the produced LULC maps for the years 2016, 2015, 2014, 2003,
1999, 1978 and 1973, where the values of the overall accuracy for
the produced LULC maps exceeded 93%. The maximum accuracy
was attained by the year 1978 (96.2%) and the minimum was
attained by 1973 (93.6%). The outcomes from supervised classi-
fication of the satellite images were utilized to get an estimation
of the rate of change in geographical distribution of the marine
bar, sand plain and salt marsh ecosystems.
5.1.1. Sand plain ecosystem
The analysis of the remotely-sensed data revealed that the
sand plain of Burullus wetland has undergone dramatic changes
over time between 1973 and 2016. The changes resulted in an
annual decline rate of 98.45 ha per year, causing the sand plain to
reach 4005 ha in 2016. An estimate of decline in the distribution
of sand plain ecosystem over the three time frames revealed
6
Regional Studies in Marine Science 45 (2021) 101844
that in the first period from 1973 to 2014 the area of sand
plain has increased from 8238.6 ha to 9173.3. This indicated a
state of ecosystem as Least Concern. In the second period from
1978 to 2015 the area of sand plain ecosystem decreased from
10648.2 to 6637.8 with annual decline of 1.26%. Assuming this
rate was constant for 50 year period, extrapolation produced an
estimate of 47.2% decline in the area. This suggests a state of
Vulnerable (VU) Table 3. However, in the third period from 2003
to 2016 the area of sand plain decreased from 8980 to 4005 ha.
This resulted in an annual current decline of 6.02%. Extrapolation
of data for 50 years projected a rate of decline of 95.5%, this
indicated that the state of ecosystem is Critically Endangered
(CR) for this period. According to the outcomes of these analyses
showed that the overall state of the ecosystem can be considered
as Critically Endangered (CR) under sub-criterion A2b.
A minimum convex polygon enclosing all mapped occurrences
of sand plain ecosystem has an area of 278 Km2 (Fig. 3). Conse-
quently, the status of the sand plain ecosystem with regard to
criterion B1 is Critically Endangered (CR). Superimposing a 10×10
km grid over the mapped polygons of sand plain ecosystem
showed that the ecosystem were occupied by seven grid cells, of
these only four grid cells contain more than 1% of the ecosystem.
This indicated that the ecosystem can be evaluated as Endangered
(EN) under criterion B2. The ecosystem of sand plain is facing
threats from human activities and stochastic events that can drive
the ecosystem to be Critically Endangered in the future. Thus, the
state of sand plain ecosystem can be declared as Vulnerable (VU)
under Criterion B3.
5.1.2. Salt marshes
Although the analysis of the remotely-sensed data revealed
that the salt marshes has overall increased between 1973 and
2016 from 2885.7 to 3493.9 ha respectively; different trends
were detected over the three time frames investigated in the
assessment. In both the first period between 1973 and 2014 and
the second period between 1978 and 2015 there was no decline
in the area of salt marshes. However, in the third period between
years 2003–2016, salt marshes have decreased from 6147.1 to
3493.9 ha. Although the time frame of comparison was slightly
shorter, the rate of decline was higher during this period with
rate of decline of 43.1% and estimated annual decay rate of 0.043
ha/yr. Assuming that rate of decline is roughly constant at 4.25%
over 50 year period; extrapolation projected an estimate decline
of 88.6% over next 50 years (Table 4). Therefore, the state of
ecosystem can be considered as Critically Endangered (CR) under
Criterion A2b.
A minimum convex polygon enclosing all mapped occurrences
of salt marshes ecosystem has an area of 243 Km2 . Thus, the
ecosystem under criterion B1 is evaluated as Critically Endan-
gered (CR). Superimposing a 10×10 km grid over the mapped
polygons of salt marshes ecosystem of Burullus indicated that
the ecosystem occupied 9 grid cells (Fig. 4). This, together with
evidence of decline in distribution and function described under
EOO supports Endangered (EN) status under criterion B2. Fig. 4
showed the results of map of spatial extent of EOO and AOO. The
salt marshes of Burullus is currently subjected to human activities
such as land use changes in addition to other human-induced
threats, which supports the idea that ecosystem may become,
or may already be Critically Endangered. Consequently, the salt
marshes ecosystems can be considered as Vulnerable (VU) under
Criterion B3.
5.2. Criterion D
5.2.1. Sand plain ecosystem
The field investigation of the sand plain habitat resulted in
the identification of 59 plant species. This number is lower than
S.M.M. Ghoraba, M.W.A. Halmy, B.B. Salem et al. Regional Studies in Marine Science 45 (2021) 101844

Table 3
Estimated declines in distribution (Criterion A) of sand plain ecosystem.
Year Area (ha) Time frame (Yrs) Magnitude Observed change % Annual PRD PRD % Status
1973 8238.6
41 + – – – LC
2014 9173.3

1978 10648.2
37 – 37.6 0.013 47.2 VU
2015 6637.8

2003 8980
13 – 55.4 0.06 95.5 CR
2016 4005

Table 4
Estimated declines in distribution (Criterion A) of salt marshes ecosystem.
Year Area (ha) Time frame (Yrs) Magnitude Observed change % Annual PRD PRD % Status
1973 2885.7
41 + – – – LC
2014 4645.6

1978 3362.2
37 + – – – LC
2015 3944.7

2003 6147.1
13 – 43.1 0.043 88.6 CR
2016 3493.9

Table 5
The results of floristic quality assessment in sand plain ecosystem.
Data reference Total no. species Native species % Non-native species % Mean C-value FQAI Adjusted FQAI
Zahran et al. (1990) 27 100.0 0.0 7.7 40.0 77.03
Shaltout et al. (1995) 79 97.4 2.6 5.7 50.0 56.20
Galal and Fawzy (2007) 69 95.6 4.4 5.2 42.0 51.70
Shaltout and Al-Sodany (2008) 42 97.6 2.4 5.5 35.6 54.90
The current study (2019) 59 91.5 8.5 4.9 36.0 47.10

Fig. 3. A map of the spatial extent of sand plain ecosystem and the assessment under criterion B of the IUCN RLE, the Extent of Occurrence (EOO) and Area of
Occupancy (AOO) are indicated. The blue polygon indicates the EOO of the ecosystem. Pink grid cells represent areas of 10×10 km and indicate the AOO of the
ecosystem; blue grid cells represent areas of 10×10 km with less than 1% occupation.

what was recorded by Shaltout et al. (1995) and Galal and Fawzy
(2007). Five invasive species were documented in the ecosystem,
representing 8.5% of the total species recorded (Table 5). The
recorded invasive species are namely Amaranthus hybridus L.,
Enarthrocarpus hydratus (Forssk) DC., Ricinus communis L., Sper-
atularia rubra (L.) J. and C. presl and Trifolium alexandrinum L.
The recorded number of invasive species in the region is higher
compared to the previous records.
The floristic quality assessment (Table 5), revealed that the
mean coefficient of conservatism C-value of 4.9 obtained from
the current investigations was the lowest compared to the values
assessed for the ecosystems based on the previously recorded
species composition, which ranged from 5.2 to 5.7. A trend
of decline in the floristic quality of the sand plain over time
7
was observed for both floristic quality indices, the FQAI and
Adjusted FQAI. The variation between the FQAI and Adjusted FQAI
is because the FQAI is sensitive to the number of non-native
species recorded in the investigated ecosystems. The current
floristic composition attained the lowest value of the Adjusted
FQAI (Fig. 5), while the highest value (77.03) was obtained by the
floristic composition of the earlier investigation by Zahran et al.
(1990) in which they have no records of non-native species. A
trend of decline in the floristic quality of the ecosystem can be
observed over time as revealed by the values of Adjusted FQAI.
Results of relative severity estimation revealed that the %
severity of adjusted FQAI of sand plain is 20%, which indicates
that the ecosystem can be considered as Near Threatened (NT)
under sub-criterion D1.
S.M.M. Ghoraba, M.W.A. Halmy, B.B. Salem et al. Regional Studies in Marine Science 45 (2021) 101844

Fig. 4. A map of the spatial extent of salt marshes ecosystem and the assessment under criterion B of the IUCN RLE, the Extent of Occurrence (EOO) and Area of
Occupancy (AOO) are indicated. The blue polygon indicates the EOO of the ecosystem. Pink grid cells represent areas of 10×10 km and indicate the AOO of the
ecosystem; blue grid cells represent areas of 10×10 km with less than 1% occupation.. (For interpretation of the references to color in this figure legend, the reader
is referred to the web version of this article.)

Fig. 6. The adjusted FQAI values for the current study and previous studies for
Fig. 5. The adjusted FQAI values for the current study and previous studies for the salt marshes ecosystem.
the sand plain ecosystem.

The overall outcomes of the RLE assessment of the sand plain
ecosystem is summarized in Table 6 which shows the changes in
the state of the sand plain ecosystem under different assessment
criteria and sub-criteria.
5.2.2. Salt marshes ecosystem
The number of species recorded in salt marshes habitat in the
current study was 70 species, which ranked second in number to
the 78 species recorded by Shaltout et al. (1995). However the
current study recorded the highest percentage (7.2%) of invasive
species compared to all of the previous studies investigated (Ta-
ble 7). The recorded non-native species were namely Amaranthus
hybridus L., Ricinus communis L., Sisymbrium irio L., Speratularia
rubra (L.) J. and C. presl and Trifolium alexandrinum L.
The floristic quality assessment of the salt marshes (Table 7),
revealed that the mean coefficient of conservatism (C- value) of
5.01 obtained from the current investigations was the lowest
compared to the values assessed for the ecosystem based on the
previously recorded species composition, which ranged from 9.04
to 5.40. A trend of decline in the floristic quality of the sand plain
8
over time was observed for both floristic quality indices, the FQAI
and Adjusted FQAI. The current floristic composition attained the
lowest value (48.19) of the Adjusted FQAI (Fig. 6), while the
highest value of 90.0 was obtained by the floristic composition
of the earlier investigation conducted by Zahran et al. (1990), in
which they have no records of alien species.
The % severity of the adjusted FQAI of salt marshes is 25%.
Therefore, the ecosystem is considered as Near Threatened (NT)
under sub-criterion D1. The data available were not sufficient
to allow the projection of the status of the ecosystem in future
time frames. Consequently, both sub-criteria D2 and D3 were
designated as Data Deficient (DD). The summary of the outcomes
of the assessment of salt marshes ecosystem is shown in Table 8.
6. Discussion
Naturally, Burullus wetland is separated from the Mediter-
ranean Sea at the north by the existence of a main sand bar. The
surface of the bar was flat and mainly covered by sand dunes
which were formed due to sedimentation process (Bayomi, 1999).
S.M.M. Ghoraba, M.W.A. Halmy, B.B. Salem et al. Regional Studies in Marine Science 45 (2021) 101844

Table 6
The IUCN Red List of Ecosystem assessment outcomes for the sand plain ecosystem. DD = Data Deficient, NT = Near
Threatened, VU = Vulnerable, CR = Critically Endangered, EN = Endangered and NE = Not Evaluated. Sub-criterion 1 for
criteria A, C and D indicating estimates over past 50 years.
Criteria and Sub-criteria State of ecosystem
A. Reduction in geographic distribution
1. Present: over the past 50 years DD
2. Future: 2a. Over the next 50 years DD
2b. Over any 50 year period including the present and future CR
3. Historic: since 1750 DD
B. Restricted geographic distribution
1. Extent of a minimum convex polygon enclosing all occurrences (Extent of Occurrence) CR
2. The number of 10610 km grid cells occupied (Area of Occupancy) EN
3. A very small number of locations (generally fewer than 5) VU
C. Environmental degradation
1. Over the past 50 years DD
2. Over the next 50 years or any 50 years DD
3. Historic (since 1750) DD
D. Disruption of biotic processes and interactions
1. Over the past 50 years NT
2. Over the next 50 years or any 50 years period DD
3. Historic (since 1750) DD
E. Quantitative analysis NE
Overall status CR

Table 7
The results of floristic quality assessment in salt marshes ecosystem.
Data reference Total no. species Native species % Non-native species % Mean C-value FQAI Adjusted FQAI (El-Kady, 1993)
Zahran et al. (1990) 23 100.0 0.0 9.04 43.0 90.00
Shaltout et al. (1995) 78 98.7 1.3 5.40 48.1 53.00
Shaltout and Al-Sodany (2008) 42 97.6 2.4 5.56 37.7 54.98
The current study (2019) 70 92.8 7.2 5.01 40.3 48.19

Table 8
The IUCN Red List of Ecosystem assessment outcomes for salt marshes ecosystem. DD = Data Deficient, NT = Near Threatened, VU
= Vulnerable, CR = Critically Endangered, EN = Endangered and NE = Not Evaluated.
Criteria and Sub-criteria State of ecosystem
A. Reduction in geographic distribution
1. Present: Over the past 50 years DD
2. Future: 2a. Over the next 50 years DD
2b. Over any 50 year period including the present and future CR
3. Historic: Since 1750 DD
B. Restricted geographic distribution
1. Extent of a minimum convex polygon enclosing all occurrences (Extent of Occurrence) CR
2. The number of 10610 km grid cells occupied (Area of Occupancy) EN
3. A very small number of locations (generally fewer than 5) VU
C. Environmental degradation
1. Over the past 50 years DD
2. Over the next 50 years or any 50 years DD
3. Historic: since 1750 DD
D. Disruption of biotic processes and interactions
1. Over the past 50 years NT
2. Over the next 50 years or any 50 years DD
3. Historic: since 1750 DD
E. Quantitative analysis NE
Overall status CR

The sand bar of Burullus wetland and its components have not
been fully studied. Sand is composed of whitish yellow and black
sands as a result of deposits from River Nile silt and clay suspen-
sions. The difference in sand color was due to the difference in
the concentration of dark minerals in sand (Hegazy and Emam,
2011). The sand plain contains the sand dunes which protect the
central part of the Delta shoreline and backshore cultivated land
and acts as a barrier against sea erosion (El Banna, 2004). One of
the reasons of the formation of sand dunes is movement of sand
by wind causing wind drifts to be accumulated in another place.
9
The coastline was an ideal location where dunes can be formed
depending on some factors such as; the geometry of shorelines,
sand supply, wind speed, topography and presence or absence of
vegetation cover in the coastal area determine the size, width and
geometry of sand dunes (El Banna, 2004). The presence of fine
texture sand allows wind to draw sands easily and rapidly pro-
moting the formation of dune, however, coarse texture beaches
takes longer time to allow formation of dunes (EL-Bady, 2014).
Remote sensing and GIS provide a powerful tool to track the
S.M.M. Ghoraba, M.W.A. Halmy, B.B. Salem et al.
changes in different types of geographic features. Thus, it pro-
vided a helpful tool for studying the changes in sand plain ecosys-
tem of Burullus over time.
The analysis of the remotely-sensed data revealed that the
area recognized as sand plain has changed dynamically over time.
The maximum area of sand plain (10648 ha) was detected in
1978, while the minimum area (4005 ha) was detected in 2016.
These variations can be attributed mainly to human activities
including construction of the international coastal highway and
the electric power plant. Also, the local inhabitants of the area
have contributed to the disturbance of the ecosystem through the
grazing activities and cultivation of some crops such as tomato
and other vegetables. From the analysis of satellite imagery, it
was detected that the decrease in the sand plain area in the most
recent dates (2014, 2015 and 2016) was accompanied with an
increase in the built up and residential areas in the region.
The RLE was applied to detect the changes in the distribution
(Criterion A) of sand plain, which revealed that the dynamics
of the change in the ecosystem distribution was not constant
over the whole period of assessment. For the first period of
the assessment (1973–2014), sand plain ecosystem showed Least
Concern (LC) state which means that there was no major threats
to the ecosystem. In the second assessment period (1978–2015)
the ecosystem was evaluated as of a Vulnerable (VU) state. This
means that the ecosystem is at high risk of collapse. Finally, the
last assessment period (2003–2016) showed that the ecosystem
can be rendered as in a Critically Endangered (CR) state. Thus,
the overall status of the ecosystem according to Criterion A is
Critically Endangered (CR) plausible level (LC-CR), which means
that the ecosystem is at extreme risk of collapse.
It can also be concluded that after 2003 major changes have
occurred to sand plain ecosystem due to human activities. This
finding strongly suggests that this ecosystem is going to suffer
higher risks in the future if no proper monitoring of the changes
is maintained and appropriate management of the resources is
not sustained.
The current floristic quality is lower than the historic state of
the ecosystems as indicated by the lowest value of the Adjusted
FQAI compared to the value attained by the floristic composition
of the earlier studies by Zahran et al. (1990). A trend of decline
in the floristic quality of the ecosystem can be observed over
time as revealed by the values of Adjusted FQAI. However, the
values from the studies conducted by Shaltout et al. (1995), Galal
and Fawzy (2007) and Shaltout and Al-Sodany (2008) produced
almost similar levels of the floristic quality index of 56.2, 51.7 and
54.9 respectively. This could be attributed to the fact that these
studies reported quite similar percentage of non-native species
with slight variations in species richness. On the other hand,
the obtained value from the current study revealed a significant
decline in the value of floristic quality that reached (47.1) due to
higher percentage of the recorded non-native species (8.5%).
The decline in the floristic quality indices and the increase in
the percentage of non-native species recently recorded compared
to the previous studies indicated that deteriorations has occurred
to the ecosystem from 1990 to 2019, and particularly acceler-
ated in the last few years. This deterioration can be attributed
to intensive activities in the region such as; the construction
of the international high way which increased the chances for
non-native species transfer through vehicles and transportation
means. Furthermore, some practices of local inhabitants such as
farming and grazing can potentially reduce the niche to native
species and promote the recruitment of more opportunistic inva-
sive species. The outcomes were in accordance with the findings
of the assessment of Criteria A and B. The results from the
estimation of Criterion D reveals that sand plain is designated as
Near Threatened, however, it is likely to become Vulnerable in
the near future.
10
Regional Studies in Marine Science 45 (2021) 101844
Salt marshes, the other major component that distinguishes
the coastal sand bar of Burullus area are mainly formed due
to changes in sea level and coastal erosion (Bayomi, 1999). The
role of natural vegetation is important to the development and
evolution of salt marshes as it can increase evaporation rate,
consequently increase salinity level of soil. Moreover, the heavy
growth of salt tolerant plants traps the deposits and help in
leveling up the beds of the marshes (Shaltout and Khalil, 2005).
Salt marshes of Burullus are mostly located near the main road
and characterized by lower species richness compared to sandy
areas.
The outcomes revealed that the distribution of salt marshes
along the marine bar of Burullus overlaps with the distribution
of sand dunes. The area occupied by salt marshes has slightly
changed over time. The assessment revealed that the estima-
tion of Criterion A of salt marshes ecosystem indicated that this
ecosystem has experienced a Least Concern (LC) state for the
first two periods of the assessment, 1973–2014 and 1978–2015.
However, the state of the ecosystem has changed in the last
period of assessment (2003–2016) to be Critically Endangered
(CR). This was in agreement with the outcomes from the assess-
ment of sand plain ecosystem that after 2003, because of the
tremendous alterations that have occurred to the area, which led
the ecosystem to be evaluated at a state of an extremely high
risk of collapse. Therefore, under Criterion A the evaluation of the
state of the ecosystem is designated as Critically Endangered (CR)
(LC-CR).
The recorded species in salt marshes was 70 species, how-
ever, only few species were unique for the ecosystem including;
Anthemis microsperma Bioss.& Kotschy, Erodium crassifolium L’
Her., Filago desertorum Pomel, Helianthemum kahirikum Delile and
Silene villosa Frossk. The revealed trend of decline in the floristic
quality of the salt marshes over time as indicated by both floristic
quality indices, the FQAI and Adjusted FQAI can be attributed
to the increased percent of recorded non-native species over
time reaching maximum in the current study, 7.2% compared to
zero non-native species in the previous study. This indicates that
the salt marshes ecosystem has been widely disturbed due to
man-made activities that influenced the marine bar of Burullus
wetland which encompass the salt marshes. The estimation of
relative severity of salt marshes under Criterion D indicated that
the ecosystem qualify for Near Threatened (NT) category. The
ecosystem is expected to turn into Vulnerable (VU) state in the
near future due rapid changes triggered by the intensive human
activities in the region as indicated from results of Criteria A and
B.
7. Conclusions
The RLE assessment was conducted on the sand plain and salt
marshes ecosystems of the marine bar which separates the lake
from the Mediterranean Sea. Data integration of remote sensing
images allowed the application of RLE to study the changes in
ecosystems distribution. The rate of geographic distribution Cri-
terion A showed the same result for sand plain and salt marshes
as Critically Endangered (CR). This indicates the distribution of
the marine bar is extremely affected by the urban and human
activities in the region. It is also expected to be affected by
any slight changes in sea-level and costal erosions in the fu-
ture. Floristic quality assessment was selected as an indicator
variable for Criterion D. The results show that sand plain and
salt marshes are Near Threatened (NT) in terms of disruption
in biotic processes and interactions. However, these results are
likely to be changed into higher risk category in the future.
The quite similar results of RLE of sand plain and salt marshes
reflect that both ecosystems are equally affected by the ongoing
S.M.M. Ghoraba, M.W.A. Halmy, B.B. Salem et al.
activities in the region, in particular in the last few years. This also
indicates the compatibility of analysis of remote sensing images
and application of the RLE. The results indicate that the marine
bar ecosystems were disturbed by human activities such as urban
development, grazing and farming. Also natural events such as
climate change and its consequences are expected to have severe
impacts on these ecosystems in the future. The lack of long term
data about the abiotic variables responsible for environmental
degradation did not allow the assessment of Criterion C. Thus,
further studies should be conducted to focus on the study of the
main interactions and processes in the marine bar with estab-
lishing national programs to monitor the highlighted variables as
a prerequisite for protection and sustainable development of the
region.
Declaration of competing interest
The authors declare that they have no known competing finan-
cial interests or personal relationships that could have appeared
to influence the work reported in this paper.
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