JournalofBiology ISSN: 2084-3577 TMKARPIŃSKI PUBLISHER andEarthSciences

BIOLOGY ORIGINAL ARTICLE

Aspects ofvegetation andsoilrelationships aroundathalassohaline lakesofW a d i El-Natrun, Western Desert, Egypt

MonierAbd ElGhani, Rim Hamdy*,Azza Hamed

The Herbarium, Faculty of Science, Cairo University, Giza 12613, Egypt

ABSTRACT The relationship between soil parameters andvegetation aroundthe inland salinelakesofW a d i El- Natruninthe Western D esert ofEgyptwas studied. Twenty-five species in22standsconstituted the floristic composition included one tree, 3 annuals and 21 perennial herbs. The saline f e a t u r e of this habitat enabled somesalttolerant species to growandf l o u r i s h . Fourspecies ( acutus L., J. rigidus Desf.,Cyperus laevigatus L. var. laevigatus andPhragmites australis (Cav.)T r i n . exSteud. subsp. australis) were constantly recorded aroundthe 7 studied lakeswhich exhibited wide ecological andsociological ra n g e s , while 8 species were confined to onlyonelake(narrowest sociological ra n g e ) . Basedontheir frequency values, classification ofthe recorded resulted in5 vegetation groups.Eachof these groupswas linkedto oneormoreofthe soilf a c t o r s which determines itsdistribution. Application

ofRedundancy Analysis (RDA) indicated that CaCO3, Ca+2, SO4-2, NO3-, K+ and Cl- were the most importantsoil variables affected the vegetation around the studied lakes.Itisrecommended that conservation measures shouldbetaken to protectthe remaining populations of Typha elephantina throughout W a d i El-Natrunwhich represents itstype locality f r o m extinction.

Key words: Egypt;halophytes; Inland saltmarshes; Redundancy analysis; Salinelakes;Salinity; Soil- environment re l a t i o n s . J BiolEarthSci2014;4(1):B21-B35

* Corresponding author: Rim Hamdy E-mail:[email protected]

Original Submission: 11November 2013; Revised Submission: 1 0 January 2014; Accepted: 1 4 January 2014

Copyright © 2014 Author(s). Journalof Biology and EarthSciences © 2014 T o m a s z M.Karpiński. This isan open-access article distributed under the terms ofthe CreativeCommons Attribution License, which permitsunrestricted use,distribution, andreproduction inany medium, provided the original work isproperly cited.

http://www.journals.tmkarpinski.com/index.php/jbes or http://jbes.strefa.pl e-mail:[email protected]

JournalofBiology andEarthSciences, 2014,V o l 4,Issue 1 , B21-B35 B21 ElGhanietal. Vegetation and soil relationships around athalassohaline lakes of Wadi El-Natrun, Egypt

INTRODUCTION which is being close to the ground [1 2]. The vege- tation around these lakes has a patchy structure: Athalassohaline lakes are inland saline aquatic different patches contain different species (or so- environments with ionic proportions quite different metimes one species) and even different growth from the dissolved salts in seawater. They are tem- forms [1 3]. porary bodies of water with salinities >3gl-1 and lac- Wadi El-Natrun is characterized by small di- king any connection to the marine environment [1]. sconnected lakes in its bottom, aligned with its ge- Salt lakes are confined to dry regions of the world neral axis in the north-west direction except Lake where evaporation exceeds precipitation and where Al-Gaar [1 4]. These lakes receive a limited supply they are often more abundant than fresh waters. of groundwater which seeps into the depression. Saline lands are widely distributed globally and Since the evaporation rate is high and the lakes lie make up about 1 0% of the Earth’s terrestrial surface in closed basins without outlet, the water in the la- [2]. Inland saline lakes have received increased at- kes has a high salt concentration and are suscepti- tention in recent years due to their sensitivity to cli- ble to marked fluctuations in level and salinity. matic change. Climatic conditions must reach a Although different colourations due to microbial po- certain degree of aridity effectively to remove water pulations are indicated by some of the lakes names by evaporation or freeze drying and so produce (Hamra = red, Khadra = green, Bida = white), the progressively concentrated brine. Geochemical and colouration of the lakes is not constant, but is sub- hydrological features are largely responsible for ject to seasonal changes. There is a discrepancy controlling the concentration and composition of the regarding the number of lakes in Wadi El-Natrun, resulting brine [3, 4]. Changes in evaporation and which ranged between two to sixteen [1 5]. Yet, Za- precipitation can affect the physical and chemical hran and Willis [1 4] reported the presence of 8 prin- conditions in such lakes [5-9]. cipal lakes for a distance of about 30 km; perma- In Egypt, certain areas are lower than the sea nent water in all or some of their parts; from south level and constitute depressions in the desert west to north: Fasida, Um Risha, Al-Razoniya, Abu-Gu- of Nile Delta. They include some water bodies cha- bara, Hamra, El-Zugm, Al-Bida, Khadra and Al- racterized by high salinity and considered as a va- Gaar, noting that Abu Gubara and Hamra form one luable economic resource that can be developed for lake in the summer. The Natrun occurs in solution in better exploitation. One of these depressions is the lakes, forms a crust around the edges of the la- Wadi El-Natrun (23 m below sea level) which consi- kes and in deposits on their bottom. Natrun deposits dered among the important depressions in the We- have long been known and were used by the an- stern Desert for land reclamation and utilization. cient Egyptians in the manufacture of glass, rem- The presence of irrigation water as underground nants of which are still found in the southern part of water of suitable quality, the existence of natural the depression. fresh water springs and the availability of some mo- Compared to studies of coastal marshes, little isture contained in the sandy layers above the shal- attention has been paid to inland saline landscapes low water table southwest of the depression are the [1 6, 1 7]. The earliest account of the vegetation of main reasons for the importance of Wadi El-Natrun the salines in Wadi El-Natrun was that of Stocker region [10]. [1 8]. The growth was studied around some re- The inland saltmarshes of the Western Desert of presentative lakes, providing the actual distribution Egypt are found in the form of Sabkhas around the of around the lakes using aerial photos of two lakes, springs and wells of the oases, e.g. Siwa, lakes [1 9]. The phytosociology of the wetland vege- Dakhla, Kurkur, Dungul, etc. and the depressions, tation revealed the presence of three distinct com- e.g. Qattara, Wadi El-Natrun, El-Fayum, etc. Being munities in addition to two species of common lower in level than the surrounding territories, the occurrence with no sociological affiliation (Cyperus inland saltmarshes are characterized by a shallow laevigatus and ) [20]. Some studies underground water table. In certain instances, the were undertaken; focused on the vegetation around underground water is exposed forming lakes of the inland saline lakes of Wadi El-Natrun [21 , 22] brackish or saline water [11 ]. The formation of this Typha elephantina Roxb. and Cyperus papyrus at saline is due to the uncontrolled spilling of water the shore of Um Risha Lake associated with some and flooding of the plains, or to the water table water loving plants has been reported [23, 24]. The

Journal of Biology and Earth Sciences, 201 4, Vol 4, Issue 1 , B21 -B35 B22 ElGhanietal. Vegetation and soil relationships around athalassohaline lakes of Wadi El-Natrun, Egypt human impact revealed that Wadi El-Natrun repre- stream, because of its proximity and low level. A sents a raw grazing ecosystem and ecologically series of isolated saline lakes occupy the axis of the fragile with unique features and resources [10]. In depression. The water level in the lakes fluctuates addition some studies recorded natural and cultiva- seasonally along the year rising up in winter and ted land cover types in the area between 1 997 and falling down in summer but never get dry, and ran- 2000, as well environmental indices from DEM, cli- ges from 1 6 m in Zagig Lake to 23 m in Al-Gaar and mate atlas data, land-use observation and soil Fasida Lakes (Figure 1 ). Wadi El-Natrun area is re- sampling were recorded [25, 26]. garded as an extremely arid region where mean In a previous work [27], the spatial distribution of annual rainfall, evaporation, and temperature are the flora of Wadi El-Natrun within its various habi- 41.4 mm, 114.3 mm, and 21°C, respectively (Egyp- tats, and its changes throughout the last 7 decades tian Meteorological Authority, 2006). was investigated. This study aims to recognize and The water enters the lakes in two ways, as analyze the floristic diversity and variations in the springs in some of the lakes and as very small stre- vegetation around the inland saline lakes of Wadi ams or trickles found on the sloping edges of the El-Natrun, and to assess the environmental factors lakes which find their way directly to the lakes. The that affect their species distribution. origin of the water entering the depression has been discussed [28-31 ]. The study area Also the geology of Wadi El Natrun has been Wadi El-Natrun is a narrow depression located in studied by many authors [29, 32, 33]. In general, the west of the Nile Delta, approximately 11 0 km the area is covered by Quaternary lake deposits northwest of Cairo between longitudes 30° 80' 20" and old alluvial deposits of sand and gravel laid and 30° 82' 90"E and latitudes 30° 81 ' 60" and 30° when the sea encroach the area and the Nile flowed 83' 20"N (Figure 1 ). The total area of Wadi El-Na- through it. The lake deposits and alluvium are un- trun is approximately 281 .7 km2, extending in a derlain by limestone of Miocene, Oligocene and NW–SE direction. The origin of the underground Pliocene ages. water in Wadi El-Natrun is seepage from the Nile The dominating land-use practice is grazing and

Fig. 1. Schematic map of Wadi El-Natrun, showing the position of the studied lakes.

Journal of Biology and Earth Sciences, 201 4, Vol 4, Issue 1 , B21 -B35 B23 ElGhanietal. Vegetation and soil relationships around athalassohaline lakes of Wadi El-Natrun, Egypt cutting. Wadi El-Natrun is a good source of forage, using the electric conductivity. Sulphates were de- based on the palatable salt marsh vegetation cover termined gravimetrically and the soluble sulfates (77%), and these resources are currently used su- precipitated as barium sulphate. Sodium and po- stainable by the local inhabitants. However, areas of tassium ions were determined using a flame photo- natural forage that serve as rangelands are subjec- meter. Calcium and magnesium ions were deter- ted to several types of degradation, overgrazing, mined by titration with EDTA. The estimation of removal for agriculture and fragmentation by roads chlorides in the soil extract was carried out by titra- network and urban sprawl [1 0]. The wadi can be tion methods against silver nitrate (AgNO3) using best described as a raw grazing ecosystem for ra- potassium chromate (K2Cr2O7) as an indicator. So- ising livestock (such as: goats, sheep, cows and luble nitrogen including ammonia and nitrate in soil camels) noting that each type of livestock has a was determined using Kjeldahl method. grazing behaviour different from the other. Expan- ding human demand and economic activities are Data analysis putting constantly increasing pressure on land and A floristic data matrix (25 species × 22 stands) other particular natural resources in the area cre- was subjected to classification by cluster analysis of ating suboptimal use and even destruction. the computer program CAP (Community Analysis Package) version 1.2 [40] using the minimum va- MATERIALS AND METHODS riance as an algorithm, and a dendrogram had been presented. The vegetation groups produced from Data collection cluster analysis was then subjected to ANOVA Between 2008 and 2011 , 22 randomly chosen (One-Way Analysis of Variance) based on soil va- stands, with certain degree of homogeneity, were riables to find out significant variations among gro- permanently visited to study the vegetation and flo- ups. The default option of the computer program ristic composition around the studied 7 lakes (Figu- CANOCO software version 4.5 for window was re 1). The number of studied stands around each used for all ordinations [41 ]. lake varies and depends on the vegetation hetero- Indirect gradient analysis was performed using geneity and species dominance. Due to inaccessi- Principal Components Analysis (PCA), and the di- bility to Lake Fasida, 2 stands were available. rect gradient analysis by Redundancy Analysis Within each stand, species present were recorded, (RDA). Seventeen environmental variables were in- and its frequency (F%) was calculated. Taxonomic cluded in RDA: pH, electric conductivity (EC), nitra- - nomenclature follows Täckholm and updated by tes (NO3 ), calcium carbonate (CaCO3), sodium Boulos [34-38]. (Na+), potassium (K+), calcium (Ca+2), magnesium +2 - -2 Soil samples were collected from each stand at (Mg ) , chloride (Cl ), sulphates (SO4 ), ammonium + - three depths: 0-10, 10-25 and 25-50 cm. The sam- (NH4 ), bicarbonates (HCO3 ), organic matter (OM), ples were pooled together forming one composite fine sand, coarse sand, silt and clay. Due to high in- sample, spread over sheets of paper and left to dry flation factors, electric conductivity, fine sand, silt in the air. Dried soils were passed through 2 mm and clay were excluded from the analysis. All data sieve to remove gravel and debris, and then packed variables were assessed for normality (SPSS for in paper bags for physical and chemical analysis. windows version 17.0) prior to the RDA analysis, Soil textural analysis was determined by the hydro- and appropriate transformations were performed meter analysis method, and the results were used when necessary to improve normality according to to calculate the percentages of sand, silt and clay). Zar [42]. The relationships between vegetation gra- Organic matter was determined by drying and igni- dients and the studied environmental variables can tion at 600°C for 3 hours, and CaCO3 content was be indicated on the ordination diagram produced by determined volumetrically using Collin's calcimeter RDA biplot. The exploratory RDA was evaluated apparatus. Soluble bicarbonates were determined using interest correlations and RDA axes were eva- [39]. Soil extracts were prepared and then used in luated statistically by means of a Monte Carlo per- order to determine chemical analysis. Soil reaction mutation test (499 permutations) [43]. (pH) was measured in soil water extract (1 :2.5) Mapping the vegetation changes around some using a Beckman pH meter. The electrical conducti- selected saline lakes (wet pastures) were based on vity (EC) was measured in soil water extract (1 :5) the estimation of distances between different belts

Journal of Biology and Earth Sciences, 201 4, Vol 4, Issue 1 , B21 -B35 B24 El Ghani et al. Vegetation and soil relationships around athalassohaline lakes of Wadi El-Natrun, Egypt

(zones) by using a meter tape and walking. rigidus, Cyperus laevigatus var. laevigatus and Phragmites australis subsp. australis) were con- RESULTS stantly recorded around the 7 lakes which exhibited wide ecological and sociological ranges. On the Floristic variations other hand, 8 species were confined to only one Table 1 demonstrated the floristic analysis of the lake (narrowest sociological range) where Panicum 25 species of vascular plants from 22 stands asso- turgidum and Centropodia forskaolii were confined ciated with the studied seven lakes in the study to Al-Gaar Lake, Samolus valerandi and Berula area, and distributed as follows: one tree, 3 annuals erecta to Hamra Lake, Sporobolus spicatus and Di­ and 21 perennial herbs. The latter included Juncus gitaria sanguinalis (L.) Scop. to Um Risha Lake, acutus, J. rigidus and Cyperus laevigatus var. laevi­ Solanum elaeagnifolium to El-zagig Lake, and the gatus as the common species. It is obvious that the water-loving plant Zannichellia palustris to Al-Bida desert outskirt surrounding the lakes favor the Lake (Table 1 ). growth of some perennials such as Phragmites au­ stralis, Imperata cylindrica (L.) Rauesch., Alhagi Classification of the vegetation and soil charac- graecorum Boiss. and Desmostachya bipinnata (L.) teristics around studied lakes Stapf. Furthermore, the saline feature of this habitat Based on their frequency values, classification of enabled some salt tolerant species to grow and flo- the recorded 25 species from 22 stands around the urish such as Typha domingensis (Pers.) Poier. ex 7 lakes resulted in 5 vegetation groups (A-E), and Steud., Typha elephantina and Spergularia marina named after the dominant and highly frequent spe- (L.) Bessler. Among the less common species Son­ cies. Based on the cluster analysis outcome, the chus maritimus, Panicum turgidum Forssk. and Cy­ dendrogram in Figure 2 was elaborated, and the nodon dactylon L. were noticed. Six species were characteristic species of each group was displayed occasionally recorded (recorded in one stand) in Table 2. Clearly, pH (p = 0.006), percentages of and/or very modestly represented. These included coarse sand (p = 0.020), and silt (p = 0.045), sho- xerophytic species such as Sporobolus spicatus wed significant differences between the identified (Vahl) Kunth and Centropodia forskaolii (Vahl) Cope vegetation groups (Table 3). and water loving species such as Zannichellia palu­ stris L., Berula erecta (Koch ex Rchb.) Rchb.f. and Group A: Juncus rigidus­Desmostachya bipinnata­ Samolus valerandi L. Typha elephantina­Arundo donax L. group The performance of species within the different It is characterized by the dominance of Juncus lakes revealed that four species (Juncus acutus, J. rigidus and Desmostachya bipinnata together with

Fig. 2. Cluster analysis of the 22 stands around the studied 7 lakes of Wadi El-Natrun. (A – E) are the 5 separated vegetation groups.

Journal of Biology and Earth Sciences, 201 4, Vol 4, Issue 1 , B21 -B35 B25 El Ghani et al. Vegetation and soil relationships around athalassohaline lakes of Wadi El-Natrun, Egypt

Table 1. Floristic composition of the selected 22 stands of the lakes habitat; + = presence; - = absence.

Journal of Biology and Earth Sciences, 201 4, Vol 4, Issue 1 , B21 -B35 B26 El Ghani et al. Vegetation and soil relationships around athalassohaline lakes of Wadi El-Natrun, Egypt

Table 2. Overall composition and distribution of the associated species within the five vegetation groups in Lakes habitat of Wadi El-Natrun. Figures in bold are the leading dominant species with higher presence percentages (P%).

Typha elephantina and Arundo donax in stands 11 5 Group B: Typha domingensis group and 11 6 which located in Al-Gaar and Al-Bida La- This group (1 2 species) characterized the three kes. Among the associated species; Tamarix niloti­ stands (111 , 11 8 and 1 20) from Um Risha, El–Ra- ca, Alhagi graecorum, Panicum turgidum, Cyperus zoniya and El-Zagig Lakes with high soil contents of +2 +2 + + - laevigatus var. laevigatus and Imperata cylindrica sulphates, Ca , Mg , Na , K and Cl ions. Typha can be enumerated. Centropodia forskaolii showed domingensis was the characteristic species, while a certain degree of fidelity to this group. Organic the common associated species included Alhagi matter, fine sand, coarse sand, pH and bicarbonate graecorum, Juncus rigidus, Juncus acutus, Cyperus attained their highest values in this group (Table 3). laevigatus var. laevigatus, Phragmites australis

Journal of Biology and Earth Sciences, 201 4, Vol 4, Issue 1 , B21 -B35 B27 El Ghani et al. Vegetation and soil relationships around athalassohaline lakes of Wadi El-Natrun, Egypt

Table 3. Mean values, standard deviations (±SD) and ANOVA F values of the soil variables, species richness (SR) and Shannon's index (H’) in the stands representing the five vegetation groups obtained by cluster analysis in the lakes (* = P ≤ 0.05 and **= P ≤ 0.01 ). CS = Coarse Sand; EC = Electric Conductivity; FS = Fine Sand; OM = Organic Matter.

subsp. australis, Desmostachya bipinnata, Arundo (Gouan) Parl. were recorded. The complete absen- donax and Cynodon dactylon were recorded. Digi­ ce of Typha elephantina, Arundo donax, Panicum taria sanguinalis and Senecio glaucus L. subsp. co­ turgidum, Imperata cylindrica, Centropodia forska­ ronopifolius (Maire) C. Alexander were confined to olii, Cynodon dactylon, Senecio glaucus subsp. co­ this group. It is interested to note the complete ab- ronopifolius and Digitaria sanguinalis can also be sence of Typha elephantina. noticed.

Group C: Juncus acutus­Cyperus laevigatus var. Group D: Juncus acutus­Imperata cylindrica group laevigatus group This is the most diversified (1 5 species) among This group characterized by Juncus acutus and the recognized groups. It is characterized by the Cyperus laevigatus var. laevigatus in 7 stands from dominance of Juncus acutus and Imperata cylindri­ five lakes (Al-Bida, El–Razoniya, Al-Gaar, Fasida ca in 4 stands (1 03, 11 7, 11 0 and 1 22) on soil rich in + - and Um Risha) with soil rich in NH4 and clay con- NO3 content (49.73 ± 3.08). The dominant species tents (Table 3). Juncus rigidus and Alhagi graeco­ showed their highest abundance in this group, to- rum were the co-dominant species of this group gether with Cyperus laevigatus var. laevigatus and (F=85.7% and 71 .4%, respectively). Among the as- Phragmites australis subsp. australis. Sporadic sociated species; Tamarix nilotica, Phragmites au­ species were Typha domingensis, Desmostachya stralis subsp. australis and Aeluropus littoralis bipinnata, Sonchus maritimus and Cynodon dacty­

Journal of Biology and Earth Sciences, 201 4, Vol 4, Issue 1 , B21 -B35 B28 El Ghani et al. Vegetation and soil relationships around athalassohaline lakes of Wadi El-Natrun, Egypt

first 2 axes (Figure 3). Stands of group (A) occupied the highest position in the ordination plan. This gro- up was dominated with Juncus rigidus, Desmosta­ chya bipinnata, Typha elephantina and Arundo donax. Stands of the vegetation groups (D) and (E) which dominated with Juncus acutus, J. rigidus and Imperata cylindrica occupied the positive side of axis 1 , while stands of the vegetation groups (B) and (C) that dominated with Typha domingensis, Juncus acutus and Cyperus laevigatus var. laeviga­ tus occupied the other negative end.

Soil-vegetation relationships The relationships between the results of vegeta- tion and soil analyses using Redundancy Analysis (RDA) with the 5 vegetation groups (A-E) were shown in Figure 4. During this analysis, five varia- bles showed high inflation values (Ec, Na+, fine sand, silt and clay), so they are discarded from the analysis. It can be noted that stands of group C were affected by ammonia; stands of groups D and Principal Component Analysis (PCA) scatter plot E were correlated with pH and CaCO while those Fig. 3. 3 for the 22 stands around the lakes habitat in Wadi El- -2 +2 of group B were affected by SO4 and Ca . Two Natrun along the first two axes, with the vegetation stands of group A exhibited high correlation to or- groups (A-E) superimposed. ganic matter and coarse sand. In addition to other stands of groups C and E were correlated with - HCO3 . lon. Five species showed a degree of consistency to The successive decrease of eigenvalues of the this group: Zannichellia palustris, Sporobolus spica­ tus, Samolus valerandi, Berula erecta and Solanum eleagnifolium Cav.

Group E: Juncus rigidus­Juncus acutus group This group comprised 1 3 species from 6 stands inhabiting soil rich in CaCO3 and silt content (Table 3), where Juncus rigidus and J. acutus were the do- minant species (Table 2). Typha domingensis was the most common species. Associated species inc- luded Imperata cylindrica and Typha elephantina. Occasionally recorded species (present in only one stand; P=1 6.6%) was Aeluropus littoralis. Notably, Arundo donax, Centropodia forskaolii, Desmosta­ chya bipinnata, Tamarix nilotica (Ehrenb.) Bunge, Alhagi graecorum, Cynodon dactylon, Senecio glau­ cus subsp. coronopifolius, Digitaria sanguinalis, Zannichellia palustris, Sporobolus spicatus, Samolus valerandi, Berula erecta and Solanum eleagnifolium.

Ordination of stands Principal Components Analysis (PCA) scatter plot Fig. 4. The RDA ordination biplot of the first 2 axes showing the distribution of 22 stands around the lakes, showed the segregation of the 5 groups along the with the examined soil variables.

Journal of Biology and Earth Sciences, 201 4, Vol 4, Issue 1 , B21 -B35 B29 El Ghani et al. Vegetation and soil relationships around athalassohaline lakes of Wadi El-Natrun, Egypt

Table 4. Redundancy analysis results showing the inter-set correlations of the soil variables, together with eigenvalues and species-environment correlation of the studied lakes. For abbreviations and units, see Table 2. *= P ≤ 0.05.

four RDA axes (0.1 40, 0.11 5, 0.090 and 0.077 for axes 1 , 2, 3 and 4, respectively) that illustrated in Table 4 suggesting a well structured data set. The species-environment correlations were high for the four axes, explaining 67.5% of the cumulative va- riance. These results suggested an association be- tween vegetation and the measured soil variables presented in the biplot. The inter-set correlations resulted from RDA of the examined soil variables were shown in Table 4. Axis 1 was positively corre- lated with CaCO3, while negatively correlated with +2 -2 - Ca , SO4 and NO3 . The RDA axis 1 can be inter- - Vegetation mapping around El-Hamara Lake preted as CaCO3-NO3 gradient. Axis 2 was positi- Fig. 5. vely correlated with coarse sand, and negatively showing the distribution of the dominant species. +2 + - -2 correlated with CaCO3, Ca , K , Cl , SO4 , and - NO3 . The RDA axis 2 can be interpreted as coarse sand-Cl- gradient. A test for significance with an unrestricted Monte Carlo permutation test found the F-ratio for the eigenvalue of RDA axis 1 and the trace statistics to be significant (p=0.03), indicating that the observed patterns did not arise by chance. The ordination biplot diagram (Figure 4) was similar to the pattern of ordination obtained from the flori- stic PCA (Figure 3), with most of the sites remaining in their respective cluster group.

Mapping of vegetation around lakes Figures 5 and 6 are sketch drawings exemplify Fig. 6. Vegetation mapping around El-Hamara Lake zonation of vegetation around two saline lakes (wet showing the distribution of the dominant species.

Journal of Biology and Earth Sciences, 201 4, Vol 4, Issue 1 , B21 -B35 B30 El Ghani et al. Vegetation and soil relationships around athalassohaline lakes of Wadi El-Natrun, Egypt pastures); El-Hamra for the former and Um Risha ties. This difference may be related to the method of for the latter. These are the most common among vegetation analysis that followed in each study. The the lakes of Wadi El-Natrun. significant role of abiotic factors that controlling the distribution of halophytes in saline habitats was stu- El­Hamra Lake died [47-49]. Redundancy analysis (RDA) of the A wide bare zone of barren soil devoid of vege- present data set demonstrated the effect of edaphic tation surrounds the southern shore of this lake. factors on the spatial distribution of plant communi- Thickets of var. cover ties around the lakes. CaCO , Ca+2, K+, SO -2, NO - Cyperus laevigatus laevigatus 3 4 3 the ground of the distant zone far away from the and coarse sand were of significant variations shore. The latter zone was always wet, and the (p<0.05) among the 5 vegetation groups (communi- - plants were browed by goats and animals. A narrow ties). RDA axis 1 can be inferred as CaCO3-NO3 belt of Juncus acutus surrounds the outer limits of gradient, while RDA axis 2 showed a gradient of this zone. Along the eastern side, a pure zone of coarse sand and Cl- gradient. These results were in Juncus acutus vertically traverses these two zones. consistent with those of El-Sawaf and Emad El- Deen [20]. On the contrary, around the inland sali- Um Risha Lake ne lakes in Dakhla and Siwa Oases of the western Apparently, the grass Desmostachya bipinnata Desert [50], 1 2 halophytic plant communities linked largely contributes to the vegetation zones around to two main habitats (wet-moist and dry-mesic) this lake, with the absence of the sedge Cyperus were identified, with few communities were in com- laevigatus var. laevigatus. Along the western side of mon with Wadi El-Natrun salines. Alhagi graecorum, the shore, Juncus actus zone was represented, Tamarix nilotica, Cressa cretica, Juncus rigidus and otherwise Alhagi graecorum zone were recognized. Phragmites australis were the most common in the A zone of barren soil separates the outer zone of two oases. Whereas communities of Cyperus laevi­ Juncus acutus from the inner Desmostachya bipin­ gatus, Suaeda aegyptiaca, Suaeda vermiculata, nata zone. Typha domingensis and Aeluropus lagopoides were recorded from Dakhla Oasis, Cladium mariscus and DISCUSSION Arthrocnemum macrostachyum communities were recorded from Siwa Oasis. The most important In total, 25 species were recorded, and repre- edaphic variables affecting the distribution and sented the species composition around the inland structure of the plant communities were: salinity, saline lakes in this study. The fewer number of spe- moisture content and fine fractions, yet CaCO3 con- cies (mostly salt-tolerant) may be attributed to the tent seem to be more effective in the Dakhla Oasis. high soil salinity around the lakes. Such salinity When studying the saltmarsh communities of the stress on floristic diversity in the study area and re- western Mediterranean coastal desert [51 ], they lated areas was documented [44-46]. Application of pointed out that salinity; concentration of different multivariate analysis techniques (classification and ions and the periodical variation in the water table ordination) to the floristic composition and soil fe- determine the distribution of species and the diffe- atures around the lakes yielded five vegetation gro- rences between communities. They also conclude ups (communities): that the saltmarsh vegetation in this part of the co- (A) Juncus rigidus­Desmostachya bipinnata­Typha untry represents a transition from the western com- elephantina­Arundo donax, munities in North Africa and those characteristic of (B) Typha domingensis, the Eastern Mediterranean region. (C) Juncus acutus­Cyperus laevigatus var. laeviga­ From a phytosociological point of view, the pure tus, community of Typha elephantina existed under the (D) Juncus acutus­Imperata cylindrica, and conditions of deep fresh water (total soluble salts c. (E) Juncus rigidus­Juncus acutus. 2000 ppm) around Al-Gaar Lake. Typha domingen­ None of the obtained vegetation groups has sis replaced T. elephantina when the total soluble analogues in other former studies. Despite the dif- salts reached 4000 ppm coupled with basin eleva- ference in their dominating species, these commu- tion. More accumulation of sand on the bank enco- nities are undoubtedly having the same floristic uraged Phragmites australis to grow [21 ]. Simpson composition of the previously recorded communi- stated that Typha domingensis is more sensitive to

Journal of Biology and Earth Sciences, 201 4, Vol 4, Issue 1 , B21 -B35 B31 El Ghani et al. Vegetation and soil relationships around athalassohaline lakes of Wadi El-Natrun, Egypt salt than Phragmites australis as the latter forms spicatus. forms one of the main well into Lake Mariut while Typha is present only scrubland types along the northern part of the Red where the Lake receives fresh water from Mahmu- Sea littoral of Egypt, and is also common in the wa- diya canal [52]. El-Sawaf and Emad El-Deen reco- dis of the limestone desert east of the Nile. Nitraria gnized the disappearance of Typha species from retusa was recorded in some of the principal wadis Hamra Lake where Phragmites australis was scat- to the west of Hamra Lake and on terraces east of tered among the Juncus acutus plants as well as El-Khadra and Al-Gaar lakes [58]. Boulos [21 ] re- higher elevations, near the road [20]. They also re- ported that Nitraria retusa dominated with increased cognized 3 distinct communities around the lakes: salinity on the surface soil layer, where the under- (A) Juncus rigidus­Tamarix nilotica community, in- ground water table was deep. In this study, it is a habited soil with relatively high contents of Cl-, Na+, point of importance to recognize the disappearance SO -2, pH and EC with high silt content and low of and around 4 Zygophyllum album Nitraria retusa sand, related to the fairly saline habitats. the studied lakes. (B) Phragmites australis­Typha elephantina com- The zonation of saltmarsh vegetation is a uni- munity inhabiting swampy lands (border of the la- versal phenomenon [1 7, 59, 60]. Concentric zona- kes) where there is a rich and continuous feed of tion of halophytic communities around small lakes fresh brackish water. Soils showed low content of and saltmarshes of the Egyptian oases and the - + -2 Cl , Na , SO4 , relatively high organic matter and ring-shaped vegetation formations in NW-Egypt re- silt and low values of EC and sand. sulting from different habitat gradients were descri- (C) Nitraria retusa­Sporobolus spicatus community, bed [61 , 62]. The vegetation and flora of Qara Oasis - + -2 inhabited soil with low content of Cl , Na , SO4 , re- demonstrated four concentric zones of plant com- latively high organic matter and silt and low values munities bounding the oasis [63]. The zonation pat- of EC and sand. terns of the littoral salt marsh vegetation are mainly Boulos et al [21 ] reported that Juncus acutus influenced by the tidal phenomena, seven salt communities were scattered among Cyperus laevi­ marsh zones of plant communities around middle gatus were they distributed as contour lines parallel lakes (Hamra, Zugm, Zagig, Al-Bida and El-Khadra) to the lake bank, and both species decreased in of Wadi El-Natrun were observed [54, 57]: Swamps number and vigour by increasing the ground surfa- of Typha elephantina and Phragmites australis, Cy­ ce until they disappeared. In the present study, Ty­ perus laevigatus and Juncus acutus complex (wet pha elephantina was represented in vegetation salt marsh), Sporobolus spicatus community, De­ group (A), with fewer individuals. It is recommended smostachya bipinnata community, Zygophyllum al­ that conservation measures should be taken to pro- bum community, Nitraria retusa community and a tect and secure the remaining populations thro- community of Tamarix sp., where the last five com- ughout Wadi El-Natrun which represents its type munity revealed as the dry salt marsh. He also re- locality from extinction [53]. cognized the mosaic pattern of the vegetation which Two species; Zygophyllum album and Nitraria means that the plant life is affected by several inte- retusa deserve special comments. In Egypt, Zygo- racting factors with no single dominant factor. In phyllum album is a species of wide ecological am- Wadi El-Natrun, the lakes occupy the central part of plitude. It was recognized by several habitats of the this depression, and bordered by saline which may country, such as in the littoral salt marshs [54], in harbour different plant communities [1 9]. While the the inland desert, in the wadis of the limestone ha- conditions though different, yet vegetation zonation bitat [55], in the sand dunes of the oases of the is controlled by seasonal fluctuations of water level Western Desert of Egypt [56]. Zygophyllum album in the lakes and hence that of water table: shallow community abounds in the sand formations west of in wet season and deeper in dry season. Under the the lakes (e.g. Hamra and El-Rhazonia Lakes) fur- prevalent arid climate, evaporation causes the ac- ther than area occupied by Sporobolus spicatus cumulation of salts at the ground surface forming community and in water runnels lined with sand de- crusts. The other important factor is relief [64]. The posits and dissecting the gravel deposits where the soil physical and chemical characteristics are appa- salinity is lower [57]. El-Sawaf and Emad El-Deen rently one of the main factors influencing the plant [20] recorded Zygophyllum album just as associated cover, distribution and also the zonal pattern of the species to community of Nitraria retusa­Sporobolus vegetation types [65].

Journal of Biology and Earth Sciences, 201 4, Vol 4, Issue 1 , B21 -B35 B32 El Ghani et al. Vegetation and soil relationships around athalassohaline lakes of Wadi El-Natrun, Egypt

TRANSPARENCY DECLARATION Subarctic lake. Int J Salt Lake Res. 1 992; 1 : 92-1 23. doi: 1 0.1 007/BF02904364 The authors declare no conflicts of interest. 1 0. Salem BB, Heneidy SZ, Awad MA. Mapping rangelands for sustainable utilization in Wadi El- AUTHORS' CONTRIBUTION Natrun area, Egypt. Taeckholmia. 2003; 23(1 ): 23-43. 11 . Zahran MA. On the ecology of Siwa Oasis, Egypt. Egypt J Bot. 1 972; 1 5(2): 223-242. MAEG: Conception and design; MAEG and RH: 1 2. Migahid AM, El-Shafei AM, Abdel Rahman AA, Development of methodology; AH: Acquisition of Hammouda MA. An ecological study of Kharga and data; MAEG, RH and AH: Analysis and interpreta- Dakhla Oases. Bulletin de la Société de Géographie tion of data; RH and AH: Writing, review and/or re- d’Egypte. 1 960; 33: 279-31 0. vision of the manuscript; Administrative, technical, 1 3. El Hadidi MN. 1 993. Natural vegetation. In: The or material support; MAEG and RH: Study supervi- Agriculture of Egypt. Ed. Graig GM. pp. 39-62. sion. All authors are involved in drafting the manu- London, Oxford University press. script, read and approved the final version of the 1 4. Zahran MA, Wills AJ. 2009. The Vegetation of Egypt. manuscript. 2nd ed. In: Plant and vegetation. Vol. 2. Ed. Werger MJA. pp. 1 -437. London, Springer Verlag & Bussiness Media B.V. REFERENCES 1 5. Abu Al-Izz MS. 1 971 . Land forms of Egypt. pp. 281 . Cairo, The American University in Cairo Press. 1 . Bayly IAE. 1 967. The general biological classification 1 6. Adam P. 1 990. Salt marsh ecology. pp. 461 . UK, of aquatic environments with special reference to Cambridge University Press. those in Australia. In: Australian inland waters and 1 7. Krüger HR, Peinemann N. Coastal plain halophytes their fauna: eleven studies. Ed. Weatherley AH. pp. in relation to soil ionic composition. Vegetatio. 1 996; 78-1 04. Canberra, Australian National University 1 22: 1 43-1 50. doi:1 0.1 007/BF00044696 Press. 1 8. Stocker O. 1 927. Das Wadi El-Natrun. In: Vegetations 2. O’Leary JW, Glenn EP. Global distribution and bilder. Eds. Karsten G, Schenck H. pp. 6. 1 8 Reihe, potential for halophytes. In: Halophytes as a resource Heft 1 , Tafel 1 . Jena, Fischer. for livestock and for rehabilitation of degraded lands. 1 9. Hussein AH. 1 980. Ecological studies on plants Eds. Squaries VR, Ayoub AT. Tasks Veget Sci. 1 994; inhabiting various habitats in Wadi El-Natrun. Ph. D. 32: 7-1 5. Thesis, Faculty of Science, Cairo University, Egypt, 3. Eugester HP, Hardie IA. 1 978. Saline lakes. In: pp. 1 88. Lakes: chemistry, geology and physics. Ed. Lerman 20. El-Sawaf N, Emad El-Deen, HM. 2000. Phytosocio- A. pp. 237-293. New York, Springer-Verlag. logical of the wetland vegetation at Wadi El Natrun, 4. Lent RM, Lyons WB. 1 995. Pore water geochemistry Egypt. Proceedings of the 1 st International and recommendation for ground water investigations, Conference of Biological Science (ICBS), Faculty of Wadi El-Natrun, Western desert of Egypt. Egypt, Science, Tanta University 1 : 40-49. General Desert Development Organization. 21 . Boulos ST, De Marco G, Girace M. Ecological studies 5. Williams WD. Inland salt lakes: An introduction. on Lakes area of wadi El-Natrun. I-El Gaar Lake and Hydrobiol. 1 981 ; 81 : 1 -1 4. doi: 1 0.1 007/BF00048701 its vegetation. II-El Fasda and El-Rhazounia Lakes 6. Hammer UT. Saline Lakes. Proceeding of the 2nd and their vegetation. Bulletin de I’Institut du désert International Symposium on Athalassic (inland) saline d’Egypte. 1 974; 24: 255-268. Lakes, Saskatchewan, Canada, June 1 982. Hydrobiol. 22. Taher AG. Inland saline lakes of Wadi El-Natrun 1 983; 1 05(1 ): 1 -263. depression, Egypt. Int J Salt Lake Res. 1 999; 8: 1 49- 7. Melack JM. Saline Lakes. Proceedings of the 3rd 1 69. doi: 1 0.1 007/BF024421 28 International Symposium on Inland Saline Lakes, 23. Boulos L. Typha elephantina Roxb. in Egypt. held at Nairobi, Kenya, August 1 985. Dev Hydrobiol. Candollea. 1 962; 1 8: 1 29-1 35. 1 988; 44: 1 -31 6. doi: 1 0.1 007/978-94-009-3095-7 24. El-Hadidi MN. Distribution of Cyperus papyrus and 8. Comin EA, Northcote TG. Saline lakes. Proceedings Nymphaea lotus in inland water of Egypt. Mittei- of the 4th International Symposium on Athalassic lungen der Botanischen Staatssammlung München. (Inland) saline lakes, held in Banyoles, Spain 1 988. 1 971 ; 1 0: 470-478. Dev Hydrobiol. 1 990; 59: 1 -308. doi: 1 0.1 007/978-94- 25. Awad MA. 2002. Land use planning of Wadi El- 009-0603-7 Natrun depression towards sustainable development: 9. Pienitz R, Walker IR, Zeeb BA, Smol JP, Leavitt PR. pp. 238. Alexandria, Department of Environmental Biomonitoring past salinity changes in an athalassic Sciences, University of Alexandria.

Journal of Biology and Earth Sciences, 201 4, Vol 4, Issue 1 , B21 -B35 B33 El Ghani et al. Vegetation and soil relationships around athalassohaline lakes of Wadi El-Natrun, Egypt

26. Ali RR, El-Baroudy AA. Use of GIS in mapping the 42. Zar JH. 1 984. Biostatistical analysis. 2nd ed. environmental sensitivity to desertification in Wadi El- Englewood Cliffs, NJ Prentice-Hall. Natrun depression, Egypt. Austral J Basic Appl Sci. 43. Ter Braak CJF, Prentice IC. A theory of gradient 2008; 2: 1 57-1 64. analysis. Adv Ecol Res. 1 988; 1 8: 271 -31 7. 27. Abd El-Ghani MM, Hamdy R, Hamed A (in press). 44. Shaltout KH, El-Ghareeb R. Diversity of the salt Spatial and temporal variations in the flora of Wadi marsh plant communities in the western Medi- El-Natrun (Western Desert, Egypt): 73 Years of terranean region of Egypt. J Univ Kuwait (Science). Change. 1 992; 1 9: 75-84. 28. Pavlov MJ. Preliminary report on the geology, 45. Shaltout KH, El-Halawany EF, El-Garawany MM. hydrology, ground water of Wadi El-Natrun and Coastal lowland vegetation of eastern Saudi Arabia. adjacent areas. Cairo, UNESCO, pp. 1 83. Biodivers Conserv. 1 997; 6: 1 027-1 070. 29. Shata A, El-Fayoumi IF. Geomorphological and 46. Omer LS. Small-scale resource heterogeneity among morphological aspects of the region west of the Nile halophytic plant species in an upper salt marsh Delta with special reference to wadi El-Natrun area. community. Aquat Bot. 2004; 78: 337-348. doi: 1 0. Bulletin de I’Institut du désert d’Egypte. 1 967; 1 7(1 ): 1 01 6/j.aquabot.2003.1 2.002 1 -28. 47. Weiqiang Li, Xiao-Jing L, Khan MA, Gul B. Rela- 30. Attia AKM, Hilmy EM, Boulos, SN. Mineralogy of the tionship between soil characteristics and halophytic incrustation deposits of Wadi El Natrun depression, vegetation in coastal region of north China. Pak J Egypt. Bulletin de I’Institut du désert d’Egypte. 1 970; Bot. 2008; 40(3): 1 081 -1 090. doi: 01 /2008;40:1 081 - 20(2): 301 -326. 1 090 31 . El-Fayoumi IF. 1 964. Geology of ground water 48. Ungar IA. Are biotic factors significant in influencing supplies of Wadi El-Natrun area. M.SC. Thesis, the distribution of halophytes in saline habitats? Bot Faculty of Science, Cairo University, Egypt. Rev. 1 998; 64: 1 76-1 99. 32. La Moreaux, PE. Reconnaissance report and re- 49. Sanchez JM, Otero XL, Izco J. Relationship between commendations for ground water investigations, Wadi vegetation and environmental characteristics in a El-Natrun, Western Desert, Egypt. The General salt-marsh system on the coast of Northwest Spain. Desert Development Organization, Cairo. Bulletin de Plant Ecol. 1 998; 1 36: 1 -8. doi: 1 0.1 023/A:1 00971 2 I’Institut du désert d’Egypte. 1 962; 81 : 1 2-25. 629733 33. Marzouk I. 1 970. Rock stratigraphy and oil 50. Isacch JP, Costa CSB, Rodríguez-Gallego L, Conde potentialities of the Oligocene and Miocene in the D, Escapa M, Gagliardini DA, Iribarne OO. Distri- western desert of Egypt. 7th Arab Petrol. Congr. 54: bution of saltmarsh plant communities associated 1 -37, Kuwait. with environmental factors along a latitudinal gradient 34. Täckholm V. 1 974. Students´ flora of Egypt. 2nd ed: on the south-west Atlantic coast. J Biogeogr. 2006; pp. 888. Beirut, Cairo University (Publ.) and Coope- 33: 888-900. doi: 1 0.1111 /j.1 365-2699.2006.01 461 . rative Printing Company. x51 35. Boulos L. 1 995. Flora of Egypt checklist. pp. 287. 51 . Abd El-Ghani MM. Vegetation composition of Cairo, Al Hadara Publishing. Egyptian inland saltmarshes. Bot Bull Acad Sin. 36. Boulos L. 1 999. Flora of Egypt. Vol. 1 : Azollaceae- 2000; 41 : 305-31 4. Oxalidaceae. pp. 41 9. Cairo, Al Hadara Publishing. 52. Ayyad MA, El-Ghareeb R. Salt marsh vegetation of 37. Boulos L. 2000. Flora of Egypt. Vol. 2: Geraniaceae- the western Mediterranean desert of Egypt. Boraginaceae. pp. 352. Cairo, Al Hadara Publishing. Vegetatio. 1 982; 49: 3-1 9. 38. Boulos L. 2002. Flora of Egypt. Vol. 3: Verbenaceae- 53. Simpson ND. 1 932. A report on the weed flora of the Compositae. pp. 373. Cairo, Al Hadara Publishing. irrigation channels in Egypt. Ministry of Public Works, 39. Page AL, Miller RH, Keeny DR. 1 982. Methods of soil Government Press, Cairo, pp. 1 24. analysis. Part 2, Chemical and microbiological 54. Boulos L. 2009. Flora of Egypt checklist. Revised properties. 2nd ed. Agronomy Monograph series 9, annotated edition. pp. 41 0. Cairo, Al Hadara American Society of Agronomy, Soil Science of Publishing. America. Madison, Wisconsin. 55. Kassas M, Zahran MA. On the ecology of the Red 40. Henderson PA, Seaby RMH. 1 999. Community sea littoral salt marsh. Ecol Monogr. 1 967; 37(4): Analysis Package (CAP) version 1 .2. UK. Pisces 297-31 5. Conservation Ltd. IRC House. 56. Kassas M, Girgis WA. Habitat and plant communities 41 . Ter Braak CJF. 2003. CANOCO for windows 4.52 in the Egyptian desert. V. The limestone plateau. J 1 997-2002; Biometric-quantitative methods in the life Ecol. 1 964; 52: 1 07-11 9. and earth sciences. The Nertherlands. Wageningen 57. Zahran MA. 1 962. On the ecology of the Red sea University and Research Center. oases. Unpublished Ph.D. Thesis, Faculty of Science,

Journal of Biology and Earth Sciences, 201 4, Vol 4, Issue 1 , B21 -B35 B34 El Ghani et al. Vegetation and soil relationships around athalassohaline lakes of Wadi El-Natrun, Egypt

Cairo University, Egypt. 58. Zahran MA, Girgis WA. On the ecology of wadi El- Natrun. Bulletin de I’Institut du désert d’Egypte. 1 970; 20(1 ): 229-267. 59. Winter E. Characteristics and distribution of halo- phytes at a Jordanian salt pan. Flora. 1 990; 1 84: 341 - 367. 60. Apaydin Z, Kutbay HG, Ozbucak T, Yalcin E, Bilgin A. Relationships between vegetation zonation and edaphic factors in a salt-marsh community (Black Sea coast). Pol J Ecol. 2009; 5 (1 ): 99-11 2. 61 . Kassas M. The River Nile ecological system: a study towards an international program. Biol Conserv. 1 971 ; 4: 1 9-25. 62. Kehl H, Stahr K, Gauer J. Soil-vegetation relationship of a small catchment area on the Libyan plateau in NW Egypt. Berl Geowiss Abh. 1 984; 50: 303-324. 63. Abd El-Ghani MM. Flora and vegetation of Qara Oasis, Egypt. Phytocoenologia. 1 992; 21 (1 -2): 1 -1 4. 64. Chapman VJ. 1 960. Salt marshes and Salt desert of the world. pp. 392. London, Leonard Hill (Books) Ltd. 65. Zahran MA. 1 977. Africa. A wet formations of the African Red sea coast. In: Wet coastal ecosystems of the world 1 . Ed. Chapman ND. pp. 21 5-231 . Amsterdam, Elsevier.

Journal of Biology and Earth Sciences, 201 4, Vol 4, Issue 1 , B21 -B35 B35