Ecological Indicators 104 (2019) 172–183

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Ecological Indicators

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Original Articles Assessing risk of collapse of Lake Burullus Ramsar site in using IUCN Red List of Ecosystems T ⁎ Somaya Magdy M. Ghoraba3, Marwa Waseem A. Halmy1,3, , Boshra B. Salem, Nadia Badr E. Badr2

Department of Environmental Sciences, Faculty of Science, Alexandria University, Alexandria, Egypt

ARTICLE INFO ABSTRACT

Keywords: The IUCN Red List of Ecosystems (RLE) assessment is a new powerful scheme that identifies ecosystems that are Ecosystem assessment at risk of collapse due to global environmental changes, which can help any mitigation actions aimed at con- coastal lakes serving and rescuing these natural ecosystems. The current study applied RLE assessment protocol on Lake Wetlands Burullus ecosystem, a highly productive wetland ecosystem, Ramsar site and International Bird Area (IBA) of Ecological services Egypt. A conceptual model of the key ecosystem processes for Burullus wetland was constructed. The application Anthropogenic impacts of RLE followed the standard protocol for the first four criteria; (A) declines in distribution, (B) restricted dis- tribution, (C) degradation of the abiotic components, and (D) regarding the assessment of the disruption of biotic processes and interactions. However, data were insufficient for assessing Criterion (E) that entails conducting quantitative estimates of the risk of collapse. Multi-date satellite images were obtained and processed to estimate the changes in the spatial distribution under criteria (A) and (B) of the study area. For evaluating Criteria (C) and (D), long-term data were collected from literature and previous works to cover the time frame of the assessment as much as possible. The results from the RLE assessment revealed that the status of the ecosystem is Critically Endangered (CR), which was attributed to various types of threats that caused degradation of the natural quality and integrity of the ecosystem. Although the RLE assessment provides a coherent approach for identifying ecosystems vulnerable to human-induced changes; data insufficiency can be an impediment for the efficient application of the RLE assessment. Remotely-sensed data can help in derivation of suitable spectral indicators of the status of the ecosystems structure and functioning that might overcome some of the challenges of data adequacy and relevance to the RLE assessment especially for the understudied and data-deficient ecosystems.

1. Introduction The RLE protocol rely on the evaluation of the status of the ecological processes and native biota using standard criteria for assessing risks of Humans are fully dependent on Earth’s ecosystems and ecological ecosystems collapse (Mahoney and Bishop, 2017; Rodriguez et al., services they provide for their well-being as these services participate in 2012; Marshall et al., 2018). The state of ecosystem collapse is defined the economic activities and processes (MA, 2005). However, human according to the RLE as the endpoint of ecosystem decline, which oc- activities have altered natural ecosystems and disturb biological life all curs when the ecosystems lose their characteristic biotic and abiotic over the world (Rodriguez et al., 2015). Therefore, controllable actions features in a way that irreparably changed their identity (Rodriguez to manage ecosystems sustainably are a priority to prevent reaching to et al., 2015; Bland et al., 2016; Marshall et al., 2018). The RLE out- high levels of degradation or state of collapse (MA, 2005). The IUCN comes indicate whether ecosystems have reached the final stage of Red List of Ecosystems (RLE) assessment protocol was formulated as a degradation, i.e. state of collapse, or they can be considered as Critically tool to support conservationist and natural resources managers to Endangered, Endangered, Vulnerable levels, or Least Concern. An identify and characterize ecosystems at high risk of degradation and ecosystem can be considered as Least Concern, if it doesn't face any deterioration (Bland et al., 2017; Keith et al., 2015; Keith et al., 2013a). prevailing significant risks (Keith et al., 2013a).

⁎ Corresponding author at: Department of Environmental Sciences, Faculty of Science, Moharm Bek P.O. Box: 21511, Alexandria, Egypt. E-mail address: [email protected] (M.W.A. Halmy). 1 ORCID ID: https://orcid.org/0000-0002-4183-973X. 2 ORCID ID https://orcid.org/0000-0002-4434-7538. 3 These authors contributed equally to the development of this manuscript. https://doi.org/10.1016/j.ecolind.2019.04.075 Received 11 October 2018; Received in revised form 19 April 2019; Accepted 25 April 2019 1470-160X/ © 2019 Elsevier Ltd. All rights reserved. S.M.M. Ghoraba, et al. Ecological Indicators 104 (2019) 172–183

Fig. 1. True colour composite subset of Landsat 8 scene acquired in 2016, showing location of Burullus Wetland ecosystem at the northern Mediterranean coast of Egypt.

The RLE assessment is conducted according to five standard criteria. 2. Methodology The assessment of each of the five RLE criteria depends on assuming a threshold of collapse. The first two criteria A and B assess spatial or A crucial step prior to conducting the assessment is to define and distributional symptoms of collapse; where Criterion A assess the rate of describe the study area (unit of assessment) that will be evaluated. change in geographic distribution, which may influence the ecosystems’ Moreover, a conceptual model that depicts the key ecosystem processes, carrying capacity for the dependent biotic components; and Criterion B interactions and threats need to be formulated (Bland et al., 2017). assess the status of the restricted distribution, which make the eco- system susceptible to spatially specific threats. The threshold of collapse 2.1. Ecosystem description defined for spatial extent criteria (A & B), is generally set as the level at which the ecosystem distribution declines to zero. However, it is worth The ecosystem description of Lake Burullus was compiled from mentioning that some ecosystems may collapse before their mapped published data and literature to fulfil the standard elements of the as- distribution declines to zero. Therefore, threshold of collapse will de- sessment. The information and data collected were used to identify the pend on maps and variables used for the assessment. Both criteria C and key ecosystem components and important threats, and were employed D assess functional symptoms of ecosystem collapse of abiotic compo- in constructing conceptual model (Fig. 2) for the ecosystem. Lake nents and disturbance of biotic processes respectively (Bland et al., Burullus is the main component of Burullus Protected Area (BPA) which 2017; Keith et al., 2013a). The last Criterion E provides quantitative is located on the Mediterranean coast of the northern Delta of Egypt, in estimates of the risk of ecosystem collapse using simulation model that a central position between the two branches of the River Nile (Khalil, rely on multiple mechanisms of interactions between two or more of the 2013). The Lake covers an area of about 410 km2 with a maximum previously mentioned criteria (Bland et al., 2017). length of about 47 km and an average width of 14 km (Tharwat and The current study attempted to assess the status of Lake Burullus Hamied, 2000; Khalil, 2013). According to the IUCN (2012) habitats (Fig. 1) at north of the Nile Delta of Egypt. The wetland is one of five classification scheme (Version 3.1) the site is classified as (13. Marine/ coastal lakes in Egypt that was included among the internationally 13.4 coastal brackish/ saline lagoons, marine lakes). important wetlands of the world in accordance with the Ramsar Con- vention in 1988. The entire area of the lake and most of its surrounding 2.1.1. Abiotic environment wetland area has been declared as a protected area in 1998 (Galal, Lake Burullus is a shallow basin, its depth varies between 40 cm ’ et al., 2012). Burullus is also considered as one of the world s Important near the shores and 200 cm near the Sea outlet and the depth increases Bird Area (IBA) in 1999 (Khalil, 2013). in east–west direction. The lake belongs to the arid region which is ’ The current study sought to consider the applicability of the IUCN s characterized by warm temperatures in summer ranging from 20 to RLE risk assessment protocol criteria to Burullus wetland. The study 30 °C and mild temperatures in winter ranging from 10 to 20 °C examined the common causes of decline in the ecosystem of Lake (Shaltout and Khalil, 2005). There is variation in sources of water that Burullus and tested a set of proposed indicators to be used as predictors enter the lake. The western section receives freshwater from the Nile of the state of the ecosystem by natural resources managers and con- through Brimbal Canal that branches directly from branch of servationists. The application of RLE protocol to evaluate the state of the Nile; however, the eastern side receives saline water directly from Lake Burullus will aid in prioritizing conservation measures and sus- the Mediterranean Sea through El-Boughaz opening (Younis and Nafea, tainable management of the region. 2012)(Fig. 1). This variation resulted in salinity gradient pattern from

173 S.M.M. Ghoraba, et al. Ecological Indicators 104 (2019) 172–183

Fig. 2. Cause-effect conceptual model of the main ecological processes relevant to Lake Burullus ecosystem risk assessment. east to west (El-Reefy et al., 2006; Emara et al., 2016). Average salinity Keddy, 2005). Rotifers are the dominant group followed by copepods, levels of Lake Burullus decreased dramatically from 14‰ in 1966 to while cladocerans are the least abundant group and dominated mostly 3‰ in 2015 due to discharge of agricultural drainage into the lake by freshwater species (Shaltout and Khalil, 2005). The changes in the (Khalil, 2016; Negm et al., 2019). Currently, Lake Burullus receives lake’s salinity towards being more fresh water due to discharge of drainage waters from neighbouring areas through nine main drains (Ali agriculture waste in the lake over the last two decades have changed and Khairy, 2012). The main drains discharging at the lake are dis- the zooplankton species composition and richness (Saad et al., 2006). tributed along the southern and eastern sides of the lake. Through these The secondary consumers level and the tertiary consumers include drains a mix of agriculture wastewater, fish farm discharge and mixed groups of different fish species that comprise a blend of marine and upstream sewage effluent is discharged into the Lake (Dumont and El freshwater species. Other consumer groups can be found on the ter- Shabrawy, 2007; Kennish and Paerl, 2010). The lake receives up to 4 restrial part of the wetland including invertebrates (127 species), rep- billion m3 of agricultural drainage annually which represents about tiles (22 species), amphibians, birds (112 species) and 15 mammal 97% of water inflow into the lake (Negm et al., 2019). Consequently, species (El-Shabrawy 2004; Shaltout and Khalil, 2005). Saprotrophs the Lake is turned into highly eutrophic system with high concentration trophic level is composed of bacteria and fungi (Shaltout, 2010). of nutrients inputs (Shaltout and Khalil, 2005). The fish community of Lake Burullus is usually composed of a mixture of both fresh water species (mainly tilapia sp.) with presence of some species of marine origin. However, increasing discharge of was- 2.1.2. Characteristic native biota tewater during the last two decades has negatively influenced the The structural and functional diversity within Lake Burullus provide abundance, composition and distribution of fish populations in the lake a home to rich assemblages’ biota representing the three trophic levels (Al Sayes et al., 2007). The eastern and southern shores of the lake (producers, consumers and saprotrophs). The producers comprise beside the outlets of the drains are characterized by extensive growth of phytoplankton and epiphytic algae (Shaltout and Khalil, 2005), in ad- hydrophytes (Khalil, 2013). Floating plants such as; Eichhornia crassipes, dition to vascular plants of which 3 endemic species namely Sonchus Lemna gibba and Spirodela polyrhiza appeared near the outlets of the macrocarpus; Sinapis arvensis ssp. allionii, and Zygophyllum album var. drains, where their growth was enhanced by the flowing of fresh water. album (Shaltout & Al-Sodany, 2008). Phytoplankton community of Lake The dominant submerged plant is Fennel Pondweed (Potamogeton pec- Burullus is mainly composed of fresh or brackish species with few saline tinatus), while the dominant emerged plant is the common reed water species, and represented by diatoms, chlorophyta, cyanophyta (Phragmites australis) and southern cattail (Typha domingensis)(Samaan and dinoflagellates groups (Khairy et al., 2015). The most dominant et al., 1988; Shaltout and Al-Sodany, 2008). genera are Cyclotella, Nitzschia, and Scemendus. Three consumers’ trophic sub-levels can be recognized at Burullus lake; the primary consumers level include zooplankton which is represented by three 2.1.3. Processes and interactions groups of zooplanktons: rotifera, cladocera and copepoda (Fraser and Lake Burullus has become very different from what it used to be

174 S.M.M. Ghoraba, et al. Ecological Indicators 104 (2019) 172–183 several decades ago due to the discharge of massive quantities of Table 1 agricultural drainage water with massive loads of nutrients into the lake The threats impacting Burullus wetland and their hierarchical categories ac- (Khalil, 2013). Seasons and the hydrologic gradient between drainage cording the IUCN threats classification scheme (version 3.2). water and sea water determine the spatial distribution of water chem- 1. Residential and commercial development istry and water quality in the lake (Kennish and Paerl, 2010). The main ecological processes and interactions taking place in the lake are sum- 1.1 Housing and urban areas marized in the conceptual presented in (Fig. 2). Phytoplankton com- Ex: Land reclamation on the western side Ex: Building residential areas prises the base of the food chain in the aquatic environment and the main source of food for fish production (Abdel-Moniem and Konswa, 2. Agriculture and aquaculture 2.1 Annual/ perennial crops 2001; Radwan, 2005; Khairy et al., 2015), followed by zooplankton as 2.1.4. Scale unknown/unrecorded food for juvenile and adult fishes (Shaltout and Khalil, 2005). Lake 2.3. Livestock and farming Burullus used to harbour a variety of invertebrates and fish species 2.3.2. Small holder grazing ranching or farming during seventies and early eighties (Khalil, 2013). However, release of 2.4. Marine and freshwater aquaculture 2.4.1. Subsistence/artisanal aquaculture nutrients from different sources has decreased water salinity levels and Ex species: Tilapia and mullets encouraged eutrophication conditions that changed species composi- tion and diversity of zooplankton in the Burullus (Saad et al., 2006). 4. Transportation and service corridors fi 4.1. Roads and railways Consequently, diversity of shes in Lake Burullus was declined from 32 Ex: Highways species to 25 species (Khalil and El-Dawy, 2002; El-Adawy et al., 2013). 5. Biological resource use Eutrophication also encourages fast growth of dominant species such as 5.1. Hunting and collecting terrestrial animals algae, which promotes algal blooms that increase water turbidity and 5.1.1. Intentional use disrupt the balance of food web in Lake Burullus ecosystem (White Ex: Hunting of waterfowl et al., 2006). 5.4. Fishing and harvesting aquatic resources 5.4.1. Intentional use Ex: Catching of fish fry 2.1.4. Threats Ex: Illegal fishing gears with small mesh size The construction of the new international highway along the 6. Human intrusion and disturbances northern shore of the Lake on the sand bar has disturbed the avifauna at 6.1. Recreational activities the north Nile Delta particularly species residing in Burullus wetland Ex: Bird watching

(Galal et al., 2012). In addition, the discharge of untreated wastewater 9. Pollution from the neighbouring villages directly into the Lake has led to the 9.1. Domestic and urban wastewater rapid eutrophication of parts of the lake and further promoted growth 9.1.1 Sewage of extensive reed sheets that clog waterways. Also, uncontrolled illegal Ex: Untreated wastewater from seven drains 9.3 Agriculture and forestry effluents fishing practices disturbed the biological life in the lake (Sadek, 2010; 9.3.1. Nutrients load Soliman and Yacout, 2016). Table 1 provides information about threats Ex: Fertilizer runoff from agriculture to Lake Burullus according to hierarchical categories in the IUCN. Ex: From aquaculture

2.2. Collapse state were selected as indicators for disruption in biotic processes. Chlor- For assessment of Criteria (A) and (B), Lake Burullus ecosystem is ophyll-a concentration is considered as an indicator of phytoplankton assumed to collapse when its mapped distribution declines to zero. biomass which is affected by increasing productivity due to excess Reductions in mapped distribution occur when the lake ecosystem is phosphorous. A threshold of collapse for the chlorophyll-a measures of replaced by agriculture, fish farms (aquaculture) or any other activities being above 75 µg/l of chlorophyll-a is shown to represent hypereu- that cause decline in lake area. For assessment of Criterion (C) both trophic status according to the Organization for Economic Co-Operation reactive phosphorous and salinity levels were used as indicators for and Development (OECD) (El-Serehy et al., 2018; Ryding and Rast, environmental degradation. As the area of Lake Burullus is surrounded 1994). Regarding species richness of zooplankton, collapse is assumed by agricultural lands, agricultural effluents are discharged into the lake to occur when number of species for each of the main three classes with massive loads of phosphorous. Increased phosphorous in water (rotifers, copepods and cladoceras) fell between 0 and 1 species in each systems is responsible for eutrophication associated with low water group. The summary of the selected indicator variables for the assess- clarity, anoxic conditions, algal blooms and fish kill (Bennett and ment of each criteria are summarized in Table 2. Schipanski, 2013). Eutrophication conditions are present in Lake Bur- ullus (Radwan, 2005; Saad et al., 2006; El-Amier et al., 2016). There- 2.3. Data for the assessment fore, phosphorous is used as used as an indicator for environmental degradation. Threshold of reactive phosphorous is driven from the 2.3.1. Criteria A&B standard levels set by EPA, which recommends that total phosphates The remotely-sensed data used in the current assessment were ac- should not be higher than 50 µg/l (as phosphorous) in a ditch at a point quired from from the U.S. Geological Survey (USGS) EarthExplorer where it gets in a lake or reservoir (Muller and Helsel, 1996). Lake database (EarthExplorer, 2017). The image processing was carried out Burullus used to be a brackish lagoon (Shaltout and Khalil, 2005), within the framework of ERDAS-IMAGINE 14.0 software© (Hexagon however due to recent activities salinity has decreased over time Geospatial, 2014) and ArcGIS 10.0 software© ESRI (ESRI, 2011). Be- (Soliman et al., 2013). This drop in salinity level has changed the fore image processing the area of interest was extracted from each species composition of several species in the Lake (Saad et al., 2006; image using a shapefile of Burullus Protected Area obtained from The Khalil, 2013). Therefore, average annual salinity has been also de- World Database on Protected Areas (UNEP-WCMC and IUCN, 2017). monstrated as predictor of likely future ecological degradation in Lake The pre-processing techniques of geo-registration and radiometric Burullus. Threshold of salinity is set when salinity level decreases below correction were essential, because remotely-sensed data used in the the level of brackish water at 5 ppt (Remane and Schlieper, 1971; Moss, analysis represented satellite images that have different spatial resolu- 1994). Collapse was defined as failing to meet environmental water tions and were acquired at different dates. The main characteristics of requirements in all years included in the assessment. For assessment of the satellite imagery used in the analysis are presented in Table 3. For criterion D, both chlorophyll-a and number of species of zooplanktons the geo-registration, 2016 image was used as a reference image, for

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Table 2 Summary of indicator variables and collapse thresholds defined and used in the assessment of Lake Burullus.

Criteria Indicator variable(s) Collapse threshold Data used

Criterion A -Change in geographic extent of lake Burullus -Extent declines to 0 -Landsat images of 1973, 1978, 2003, 2014, 2015 Reduction in geographic and 2016 used for production of LULC maps distribution -Changes in the geographic extent and distribution of -Extent declines to 0 -Landsat images of 1973, 1978, 2003, 2014, 2015 reed bed and reed vegetation in Burullus wetland and 2016 used for production of LULC maps Criterion B -Restricted geographic distribution -EOO and AOO are 0 -Landsat 2016 image Restricted geographic distribution

Criterion C -Change in PO4-P concentration -More than 50 µg/l -long-term data collected from literature Environmental degradation -Change in salinity -Less than 5 ppt -long-term data collected from literature Criterion D -Change in chlorophyll-a concentration -More than 75 µg/l -long-term data collected from literature Disruption of biotic processes and -Change in richness of rotifers -Existence of only one to -long-term data collected from literature interactions no species -Change in richness of copepods -Existence of only one to -long-term data collected from literature no species -Change in richness of cladoceras -Existence of only one to -long-term data collected from literature no species Criterion E NA NA NA Quantitative risk analysis which all other images acquired in 2015, 2014, 2003, 1999, 1978 and et al., 2017). However, there are no available records of the selected 1973 were geo-registered. The first order polynomial equation for co- variables that dated back 50 years ago. Generally, the research on the ordinate’s transformation was applied for geo-registration. Egyptian coastal lakes has started in the seventeenth and most of these Radiometric correction was conducted to remove or reduce the in- studies weren't carried out on regular basis. Therefore, long-term data consistency between the values recorded by the different sensors and were collected from literature as much as available. The assessment of the spectral reference and radiance of the earth-surface features (Li environmental degradation Criterion (C) implied the assessment of two et al., 2008). The radiometric correction differs according to the type of variables; reactive phosphorous and salinity. The time frame of the sensor by which the satellite image was captured. The digital numbers assessment for the variables used in criterion C was 39 years for Phos- of the satellite images from 1973 to 2003 were converted to top-of- phorous and 44 years for salinity. (Table 4). Their data were available atmosphere reflectance values using the standard equations and scaling as follows; i) reactive phosphorous represented by 17 readings from factors applied to Landsat data as outlined by Chander et al. (2009), 1978 to 2017 and ii) salinity levels represented by 14 readings from while for those acquired using Landsat 8, the correction was conducted 1973 to 2017. These measures were used to calculate relative severity according to Landsat 8 Data User Handbook (USGS, 2016). of the assessment. The disruption of biotic interactions and processes For classifying the satellite imagery, the supervised classification was assessed using two variables; chlorophyll-a and species richness of approach was applied using maximum likelihood algorithm within the zooplanktons. The time frame of the assessment was 30 years for framework of the ERDAS imagine 14.0 image processing package. The chlorophyll-a and 41 years for species richness of zooplanktons as fol- identification of the classes is based on the spectral response pattern of lows; i) chlorophyll-a represented by 12 readings 1987 to 2017 the pre-selected training sites, in addition to recent or previous litera- (Table 4), and ii) species richness of zooplankton represented by 10 ture work. The scheme used for classification followed Anderson et al., readings from 1978 to 2016 (Table 5). All data used in the assessment (1976) system of LULC classification his implies the selection of training are provided in supplementary material (S1.1, S1.2. and S1.3). sites representing the land use/land cover (LULC) categories from known locations on the ground. To ensure the homogeneity of the se- lected training areas, class separability using Euclidean distance mea- 2.4. RLE assessment sure between means of signatures was estimated (Bhatta, 2008). The produced LULC maps should be evaluated against uncertainty (Giri, 2.4.1. Criteria A&B 2012). Therefore, the most commonly used accuracy assessment mea- The assessment of Criterion (A) implies estimate of changes in the sures (Lu et al., 2004), including overall accuracy, user's accuracy, geographic extent of Lake Burullus using outcomes from supervised fi ff producer's accuracy and Kappa coefficient were estimated for all the classi cation of satellite images of di erent dates. Three independent produced LULC maps. After the supervised classification is carried out, temporal analyses of the distribution of Lake Burullus have been carried fi a shape file of sea layer was drawn and its area was subtracted from the out; the rst was a comparison of outputs from maps of 1973 and 2014, whole area of water class to obtain the area of the lake only. the second was for data from maps of 1978 and 2015, and the third analysis was for the lake ecosystem produced from 2003 and 2016. Absolute and proportional rate of declines (ARD) and (PRD) for 50 year- 2.3.2. Criteria C&D period were calculated according to Bland et al. (2017) using Eqs. (1) The standard time frame of RLE assessment is 50 year-period (Bland and (2) respectively as follows:

Table 3 The main characteristics of Landsat satellite imagery scenes used in the analysis.

Satellite Date acquired Sensor Spatial resolution Path row Cloud cover (%) Sun elevation angle Sun azimuth angle No. of bands

Landsat8 11/3/2016 OLI-TIRS 30 m 177 38 0.03 47.8 142.1 11 Landsat8 5/2/2015 OLI-TIRS 30 m 177 38 3.48 36.6 149.1 11 Landsat8 6/3/2014 OLI-TIRS 30 m 177 38 0.07 46.05 143.5 11 Landsat7 11/1/2003 ETM+ 30 m 177 38 8.73 30.6 151.02 8 Landsat7 16/11/1999 ETM+ 30 m 177 38 0 36.1 156.5 8 Landsat3 2/5/1978 MSS 60 m 190 38 0 57 112 4 Landsat1 10/5/1973 MSS 60 m 190 38 0 61 112 4

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Table 4 where the ecosystem is qualified for Vulnerable status if meets two Maximum phosphorous (PO4-P) concentration in µg/l, average salinity level conditions; first, it has a very restricted distribution, generally with (ppt) and maximum chlorophyll-a concentration (µg/l) of Lake Burullus for the fewer than five threat-defined locations; second, it faces severe threats period from 1973 to 2017. The bold numbers represent the values that exceed (human activities or stochastic events) within a very short time period the threshold of collapse (The critical values of collapse are estimated at 50 µg/l in an uncertain future and thus capable of collapse or becoming Criti- for PO -P, 5 ppt for salinity, and 75 µg/l for chlorophyll-a). 4 cally Endangered (CR) within a very short time period (Bland et al.,

Year PO4-P (µg/L) Salinity (ppt) Chlorophyll-a (µg/l) 2017).

2017 1872 3.85 382.9 2016 514 5.83 120.4 2.4.2. Criteria C&D 2015 716.46 3.52 319.43 Relative severity describes the proportional changes observed in an 2014 591.06 5.59 411.46 environmental variable scaled between two values: one describing the 2013 932.6 3.75 138.41 initial state of the system (0%), and the other describing a collapsed 2012 1117.12 2.78 223.65 2011 660.59 2.3 355.97 state (100%). In the simplest case, relative severity may be calculated 2010 375.75 1.88 125.87 by range-standardizing the raw values of the abiotic variable between 2006 270 – 126 its initial value and its collapse value using the Eq. (3) according to 2003 297.3 3.73 127.4 Bland et al., (2017). This equation was applied to estimate relative 2002 – 3.89 – severity of number of zooplankton species under criterion (D). 2001 2.7 –– 2000 3.4 – 13.4 Relative severity (%)=× Observed or predicted decline/Max. decline 100 1997 2.9 4.15 – 1987 2.32 – 6.6 (3) – 1985 1.33 8.9 where, 1979 0.6 –– 1978 1.23 3.29 – Observed or predicted decline =−Initial value present or future value 1973 – 10.1 – Max. decline =− Initial value Collapse value

Table 5 The relative severity under Criterion (C) for reactive phosphorous Number of zooplankton species of three classes (rotifers, copepods and clado- and salinity, and under Criterion (D) for chlorophyll-a was estimated ceras) recorded in Lake Burullus from 1978 to 2016. using Eq. (4), taking in consideration frequency data in relation to a

Year Number of species of Zooplankton Refs. collapse threshold for assessing relative severity as it was adjusted by Keith et al. (2013b) as follows: Rotifers Copepods Cladoceras n Relative severity of degradation =∗o 100 2016 24 10 4 EEAA (2016) nt (4) 2015 17 12 4 EEAA (2015) 2014 20 13 7 EEAA (2014) where, nt represents the total number of instances, norepresents number 2013 23 16 3 EEAA (2013) of instances outside the collapse threshold. 2012 22 9 4 EEAA (2012) 2011 45 27 9 EEAA (2011a,b) 3. Results 2010 28 13 2 EEAA (2010) 2001 34 7 7 Saad et al. (2006) 1987 26 26 7 Aboul Ezz (1995) 3.1. Criteria A&B 1978 34 45 10 Aboul Ezz (1984) The overall accuracy of the LULC maps produced was very high exceeding 90% for all the maps (96.1, 94.81, 95.78, 93.61, 93.51, 96.2 areat2− area t1 ARD = and 93.6 for the LULC maps of 2016, 2015, 2014, 2003, 1999, 1978 and yeart2− year t1 (1) 1973 respectively) (see supplementary material S2.1). The land cover/ land use (LULC) maps produced by applying the supervised classifica- ⎛ ⎛ 1 ⎞⎞ ⎛ areat2 ⎞⎝ ()yeart2− year t1 ⎠ tion included eight LULC categories. However, some of these LULC PRD =×100⎜ 1 − ⎜⎟ ⎟ ⎜ ⎝ areat1 ⎠ ⎟ categories weren't detected in older images due to changes in land use (2) ⎝ ⎠ activities in conjunction with development around the study area. The where, produced LULC maps over the whole assessment period revealed that six LULC classes were common over the different dates. These classes

area t2: area at the end time of assessment include lake water, agricultural lands, sand plains, reed vegetation, salt area t1: area at the initial time of assessment marshes and bare soil (Figs. 3 and 4). The built-up/residential class has year t2: end time of assessment grown up exponentially over the recent years of 2014, 2015 and 2016. year t1: initial time of assessment However, fish farms class has not been recognized in 1973 and 1978 images. The most recent LULC map of Burullus wetland produced for year The results from supervised classification were used to obtain an 2016 was used to measure the three sub-criteria of Criterion B. (1) sub- estimate of the rate of change in geographic distribution of the Lake criterion B1 (extent of occurrence (EOO)) was assessed using a ecosystem for three temporal analyses, revealed that the analysis of minimum convex polygon method to provide an estimate of the ex- period from 1973 to 2014 exhibited decline of 32%. The analysis of a pansion of risk over area that encompasses the entire occurrences of the second period from 1978 to 2015 revealed a decline of 28%, while that ecosystem. (2) sub-criterion B2 (the area of occupancy (AOO)) this of the third period from 2003 to 2016 showed a decline of 10% in the indicator provides a measure of the expansion of risk among patches extent of the lake as a whole. Extrapolation of these rates over 50-year occupied by the habitat of interest. It was estimated by overlying a grid period using ARD and PRD scenarios produced remarkably similar network of cells, each with size of 10 × 10 km2, then counting the rates. For the first analysis from 1973 to 2014 an estimated rates of number of cells in which the habitat of interest occupied an area greater 39%, 37% for ARD and PRD were obtained (Table 6), the second than 1 Km2 (Bland et al., 2017; Keith et al., 2013a). (3) sub-criterion B3: analysis from 1978 to 2015 produced rates of 38%, 36% for ARD and

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Fig. 3. Area (in hectares) of LULC categories as produced by supervised classification of Landsat 1 and 3 satellite imagery in 1973&1978 respectively, Landsat 7 ETM+ imagery in 1999 & 2003, and Landsat 8 OLI imagery in 2014, 2015 and 2016.

PRD, and third analysis for the period from 2003 to 2016 produced an zooplanktons classes (rotifers, copepods and cladoceras), assuming that estimate of 39%, 34% for ARD and PRD respectively. threshold of collapse is when number of species is between 0 (lower Therefore, under sub-criterion A2b the state of Lake Burullus is boundary) and 1 species (upper boundary), revealed that rotifers lie Vulnerable (Vu) (≥30% decline over any 50 year period including the between 29% and 30% relative severity. On the other hand, the severity present and future). No data were available to assess the reduction in of decline of copepods richness varied between 78% and 80%, while geographic extent in historic time frame since 1750 and in the past cladoceras exhibited a decline with relative severity between 60% and 50 years, therefore sub-criteria A1 and A3 were assessed as Data 67%. Overall declines in biotic interactions suggest a decline of at least Deficient (DD). For Criterion B (Fig. 5), the EOO of Lake Burullus 29% to 83% of relative severity. Therefore, the status of the ecosystem ecosystem was measured to be 770 Km2. Therefore, the ecosystem is is Endangered (EN) (plausible range Vulnerable – Critically considered as Critically Endangered (CR) under sub-criterion B1a Endangered) (VU - CR) under Criterion D1. No data and projections (≤2000 Km2), and AOO of Lake ecosystem was found within 13 grid were available to assess the disruption in biotic interactions in future cells of size 10 × 10 Km. Of these grid cells only two cells contains < and historic time frames. Therefore, the ecosystem is assessed as Data 1km2 of the ecosystem (i.e., less than 1% of the area of a grid cell). By Deficient (DD) under sub-criteria D2 and D3. excluding these small occurrences, the lake was estimated to occupy eleven grid cells of size 10 × 10 km. Therefore, the state of the eco- 4. Discussion system is considered as Endangered (EN) under sub-criterion B2a. The ecosystem of Burullus Lake occupies a single location and is prone to The Convention on Biological Diversity (CBD, 1992)defines natural various environmental challenges due to human activities, of which the ecosystem as: land reclamation and water pollution are considered as the most series plausible threats. Thus, Lake Burullus may change to be Critically En- ‘a dynamic complex system of plant, animal and micro-organisms dangered in the future. Therefore, Lake Burullus ecosystem is qualified communities and their non-living environment interacting as a for Vulnerable (VU) status under criterion B3. functional unit’. Lake Burullus ecosystem suffers from deteriorated environmental 3.2. Criteria C&D conditions due to poorly-managed activities and practices such as; agricultural activities, land reclamation, aquaculture and pollution The use of frequency data in relation to a collapse threshold for (Galal et al., 2012). Pollution is a series problem that disturbs the assessing relative severity of environmental degradation show that ecological and biological life inside the lake (Khalil, 2013). Thus, the phosphorous and salinity levels are more frequently maintained above ecological integrity of the ecosystem and the quality of the provided threshold levels. Using values for reactive phosphorous and salinity, the goods and services has been diminished. Therefore, there was an es- average extent of environmental degradation across 100% of the eco- sential need for an assessment protocol that is able to systematically system extent is between 58.8% and 71.4% for reactive phosphorous assess the risk to Lake Burullus focusing on all elements that determine and salinity respectively. Therefore, the status of Lake Burullus eco- ecosystem identity. Through the application of IUCN RLE protocol, the system is considered as Endangered (EN) (≥50%) under Criterion C1. current state of Lake Burullus will be assigned which in turn would help No data were available to assess the state of ecosystem in future and in monitoring its future status based on standard criteria and categories. historic time frames. Therefore, sub-criteria C2 and C3 are assigned as Remotely-sensed data have been used increasingly to monitor and Data Deficient (DD). The maximum chlorophyll-a concentration and study changes of surface area and other number of species of zooplanktons are used for the assessment of biotic morphometric characteristics of inland and coastal water bodies and disruption in interactions and processes. The estimate of relative se- wetlands as well at different scales (Moufaddal et al., 2008; Chasmer verity of chlorophyll-a as an indicator of phytoplankton biomass, pro- et al., 2016; Montgomery et al., 2018; Montgomery et al., 2019). Re- duced severity of 83%. While, the relative severity for the richness of mote sensing analysis revealed that area of Lake Burullus has

178 S.M.M. Ghoraba, et al. Ecological Indicators 104 (2019) 172–183

at very high risk of ecosystem collapse when exposed to spatial cata- strophes due to its restricted geographic distribution. This reflects that the distribution could be currently stable according to results from Criterion (A) in Table 6, however, further decline in distribution could strongly occur due to intensive human activities that explicit threats to lake ecosystem. Therefore, rates of decline should be monitored and managed due to potential pressure from the continual increase of human population with the associated activities in this area. The col- lection of data for assessing environmental degradation of Lake Bur- ullus depicts that there was a gap in the monitoring of the lake's water quality parameters. Some years have no available data for the selected variables and sometimes data are not consistent for the same year, in particular before 2000, however, recent data were more consistent and available. The period of assessment for Criterion C variables was 34 years for and 44 years for Phosphorous. While the period of assess- ment for Criterion D variables was 30 years for chlorophyll-a and 41 years for species richness of zooplanktons. The low salinity com- bined with prevailing of less favourable environmental conditions are considered the main factors influencing the occurrence of aquatic spe- cies and their distribution in Lake Burullus (Soliman et al., 2013; Shaltout and Khalil, 2005). The major reason for these deteriorations is the massive discharge of untreated wastewater that is directly released into the lake (Khalil, 2013). It should be noted that Lake Burullus be- longs to the arid region, therefore the input from precipitation is minimal. Studies on the annual water balance of the lake have indicated that the discharge of water into the lake comes mainly from agriculture drainage that contributes about 97%, while the contribution of rainfall is less than 2% and ground water is less than 1% of the total water recharging the lake (Negm et al., 2019). Currently, Lake Burullus re- ceives drainage waters from neighbouring areas through nine main drains (Ali and Khairy, 2012).The main drains discharging at the lake are distributed along the southern and eastern sides of the lake. Through these drains a mix of agriculture wastewater, fish farm dis- charge and mixed upstream sewage effluent is discharged into the lake (Dumont and El Shabrawy, 2007; Kennish and Paerl, 2010). Due to the high inflow of freshwater to the lake through the drains, the salinity of water in the lake becomes lower than 4.0 g/1. The massive discharges of agriculture drainage is also responsible for the increase in phos- Fig. 4. Land use/Land cover maps of Burullus Wetland produced by supervised phorus concentration (Negm et al., 2019). fi classi cation of Landsat 1 & 3 MSS images in (a) 1973 and (b) 1978 respec- Until the mid-1990 s, discharge of nutrients in Lake Burullus was tively; classification of Landsat 7 ETM + images in (c) 1999 and (d) 2003; rather modest, but had amplified tremendously by the end of the classification of Landsat 8 OLI images in (e) 2014, (f) 2015 and (g) 2016. twentieth century (Dumont and El Shabrawy, 2007). In 1970 the total amount of drainage received by Lake Burullus estimated as dimensioned during the whole time frame of the assessment from 1973 3200 × 106 m3 (Faouzi, 1935; El-Sedfy and Libovarsky, 1974; Dumont to 2016 as a result of anthropogenic activities for development. Be- and El Shabrawy, 2007). In 2001 these discharges increased to an es- tween 1973 and 1978 the decrease in the area of the lake was due to the timate of 4000 × 106 m3 (Dumont and El Shabrawy, 2007). The latest spread of reed vegetation over the open water. In 1999, a dramatic report of EEAA (2017) estimated the discharge of municipal, agri- decline in the lake area has occurred, which was associated with mas- cultural and fish farms in Lake Burullus by 30 × 109 m3/yr. sive increase in reed distribution and the spread in the construction of Currently, three waste water treatment plants (WWTP) exist in Kafr fish farms as a new activity in the region during that time. Later in El Sheikh governorate where the study area is located. These WWTPs 2003, the area of the lake has been restored to some extent which could have limited capacity for full treatment of sewage and wastewaters be attributed to decrease in reed area within the lake; however, fish before discharged into the lake. The Wastewater farms were growing continuously. From 2014 to 2016 the lake area has Expansion (KESWE) project is under implementation for the construc- declined at higher rates than before in this short time, this was asso- tion of two new WWTPs and expansion of the three existing ones. The ciated with massive expansion of fish farms. Estimations Criterion A KESWE project is funded by the European Union’s (EU) Horizon 2020 (rate of change in geographic distribution) of the lake ecosystem was Initiative and aims at reducing the pollution of the Mediterranean Sea carried out on three periods of 41, 37 and 13 years respectively. Results by 2020. This project will be implemented in two phases the last one is show that the lake is in Vulnerable state. It also reveals that the lake has expected to conclude by 2023. faced degradation and can be considered to be at a high risk of collapse. The collected measures revealed that maximum reactive phos- The outcomes from the conducted RLE assessment are summarized in phorous concentration was stable until 2001 with value of 2.7 µg/l, (Table 7). The exhibition of nearly similar rates of decline extrapolated then increased more than one hundred times to reach 297.3 µg/l in for 50 years for each temporal analysis indicated that satellite image 2003. In 2003 loads of phosphorous in the lake were estimated to be processing was compatible for all the images employed in the current 4000 tons (Dumont and El Shabrawy, 2007). This increase was attrib- study representing different dates, but with slight variations. On the uted to Phosphorous enrichment in water bodies causing eutrophication contrary, the status of the lake is Endangered according to criterion B (Saad, 1976; Valoon and Duffy, 2000; El-zeiny and El-Kafrawy, 2017). which is conducted only on 2016 image. This indicates that the lake is Thus, continuous release of phosphorous could shift the lake from a

179 S.M.M. Ghoraba, et al. Ecological Indicators 104 (2019) 172–183

Fig. 4. (continued) macrophyte-dominated state to one with perennial cyanobacterial 2008). The concentration of chlorophyll-a is considered as an efficient blooms (Dumont and El Shabrawy, 2007). In addition to phosphorous, ecological indicator of phytoplankton biomass (Okbah and Hussein, salinity was also used as an abiotic variable for environmental de- 2006). It is also considered as an important indicator of the status of the gradation. Lake Burullus used to be a brackish lagoon (Shaltout and aquatic ecosystem and changes in the composition of the community Khalil, 2005). may indicate the beginning of environmental changes (Tilman et al., However, as an ecological indicator, it has decreased over time 1982). The correlation between chlorophyll-a and phosphorous con- (Soliman et al., 2013) due to increasing amount of fresh water entering centration measures was 0.6 which indicates phosphorous limitation to the lake from drainage which in turn caused decline or disappearance of phytoplankton growth. In 2003 chlorophyll-a increased one hundred many high-valued marine fish species (Khalil, 2013). Collected mea- times more than previous records and reached 127.4 µg/l. This is far sures of salinity from 1973 to 2017 revealed that salinity highly fluc- beyond the permissible levels by OECD standards for maximum chlor- tuated through years with a value of 11.7 ppt in 1973 and decreased to ophyll-a concentration of hypereutrophic state (ultimate stage of eu- reach 3.85 ppt in 2017. These deteriorations in the abiotic environment trophication process) starts at a level of 75 µg/L of maximum chlor- estimated that Lake ecosystem is Endangered (EN). ophyll-a concentration. Eutrophication has also changed the The availability and level of nutrients are considered to be the main community composition of zooplanktons. Last studies proved the dis- direct factors that control phytoplankton composition and abundance, appearance of all marine copepod species and dominance of rotifers and also influence the composition of biotic communities (Blanco et al., over the other zooplankton classes (Shaltout and Khalil, 2005). The

Table 6 Estimated rate of changes in geographic distribution of Lake Burullus.

Year Area (hectares) Period (yrs.) Observed Decline (%) Annual ARD Annual PRD Extrapolated ARD (%) Extrapolated PRD (%)

1973–2014 41,346 41 31.84 0.77 0.93 38.57 37.1 28268.2 1978–2015 39,870 37 28.25 0.76 0.89 38.17 36.15 28607.9 2003–2016 29352.1 13 10.26 0.78 0.83 39.47 34.06 26340.1

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Fig. 5. A map of the spatial extent of Burullus wetland 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.

Table 7 According to the current study, the overall status of Lake Burullus The IUCN Red List of Ecosystem assessment results for Lake Burullus. ecosystem is Endangered (EN). Estimates of environmental degradation DD = Data Deficient, Vu = Vulnerable, CR = Critically endangered, and biotic components provided useful outcomes about the deteriora- EN = Endangered and NE = Not Evaluated. tions that occurred in the ecosystem over long-term assessment. Criterion A B C D E Overall However, there was a challenge to obtain regular, accurate and long- term datasets for Criteria (C) and (D) that cover the relevant time frame Sub-criterion 1 DD CR DD DD NE EN of RLE assessment. The assessment of Criterion (A) using remote sen- Sub-criterion 2 Vu EN EN EN NE sing data analysis revealed that the area of the Lake Burullus has di- Sub-criterion 3 DD VU DD DD NE minished between 1973 and 2016 due to spread of aquatic vegetation, land reclamation and expansion of fish farms. These changes qualified collected records from 1978 to 2016 show that number of species of the Lake ecosystem as Vulnerable (Vu). The assessment of Criterion (C) main zooplankton classes have considerably changed. Number of spe- depicts the occurrence of dramatic changes to reactive phosphorous and cies of cladoceras and copepods highly decreased over time. On the salinity levels due to the reception of discharges from agricultural other hand, number of species of rotifers increased over this period and drains and drainage from fish farms and other human activities. sometimes the number of species is greater than that recorded at the Therefore, the ecosystem is classified as Endangered (EN) according to initial time of the assessment. High abundance of rotifers and alteration these alterations. The assessment of Criterion (D) shows the con- of species composition indicates that the lake transformed into fresh- sequences of the current environmental deteriorations on phyto- water eutrophic ecosystem (Mageed, 2007). This agrees with the results plankton and zooplankton communities of Lake Burullus. These dis- of the assessment of biotic disruption in interactions and processes ruptions in the biotic components qualified the Lake as Endangered which qualifies the ecosystem as Endangered (EN) and at very high risk (EN). The obtained results revealed that the ecosystem of Lake Burullus of collapse. requires:1-urgent actions against some anthropogenic threats that dis- rupt the ecological processes and interactions. 2- strategic plan to re- verse the current threats on the biotic life in the ecosystem such as; 5. Conclusion discharge of nutrient-enriched effluents, spread of aquatic reeds and establishment of aquaculture ponds. 3- regular monitoring of the de- The IUCN Red List of Ecosystems is a powerful standard scheme to fined key variables. 4- application of risk assessment models in Lake monitor changes and deteriorations in wetlands and enable comparing Burullus. 5- Application of RLE assessment on other wetlands of Egypt of ecosystem states. However, due to their strict distribution and lim- to prevent further degradation of wetlands ecosystems. ited extent, wetlands could provide over-estimated results in case of assessment of restricted geographic distribution Criterion (B). The ap- plication of this assessment requires clear understanding for the pro- Appendix A. Supplementary data cesses and interactions within the ecosystem to select the key variables that dominate the interactions and processes in the ecosystem. Supplementary data to this article can be found online at https://

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