ECOLOGICAL EFFECTS OF METAL IMPACT UPON EXPOSED SOIL PLANT SYSTEM IN AL JUBAIL , EASTERN

BY *Galaledin,

Eglal .M. ; ** Sheikha, S. Alabdulkareem and **Fawzeya, H. Albishr

*Faculty of Science (Girls) , Al-Azhar University, Cairo, Egypt . ** Girls Faculty of Science Ad Dammam , Eastern Province, Saudi Arabia.

ABSTRACT
Heavy metal impact upon seven soil-plant systems (sites: 1-7), have been assessed. Sites (1-3) are located in three islands in the Arabian Gulf, nearby the Saudi Coast; site (4) is an inland sabkha; sites (5-7) are located in the vicinity of the industrial complexes at "Jubail Industrial City". Soil exposure is evident due to the relative topsoil enrichment (RTE) ratios of ~ 1 for the majority of soil profiles in the studied areas; meanwhile, the persistence of bioavailable metals in soil profiles is indicated by total accumulations of the metals: Fe,Pb, Cu, Mn, Zn, Cd , Ni and B. Plants exposure is assessed by both bioaccumulation values of total metals and bioaccumulation values for each metal. The ecological effects, induced by metal exposure, is demonstrated by the recorded ratios of high concentration factors (CFtotal). Moreover, data of CFFe , CFB , CFCu , CFMn , CFZn , CFCd and CFNi , for each plant species represent three Fe-hyperaccumulators, namely: Salsola (CFFe 507.69), Lygos (CFFe 178.72) and Phoenix (CFFe131.10), meanwhile Tamarix is assumed as Zn-hyperaccumulator (CFZn 128.33). On the other hand, six plant species are assumed as coaccumulators; whereas three other plant species attained lower ratios of (CFtotal). The present paper focuses on metal hyperaccumulator plants and their potential uses in phytoremediation technologies.

Key Words: Soil, plant, heavy metals, exposure, bioconcentration,hyperaccumulation,

hyperaccumulators.

INTRODUCTION
Because of their dramatic increase in the biosphere, heavy metals became serious 'stressors'. Impact of heavy metals upon soil-plant systems have been intensively documented, globally, in the last decades; with major contributions to the heavily industrialized-urbanized cities (Martin & Bullock, l994; Sawidis et al., 1995; Tiller et al., 2000; Opera & Pincovschi, 2003 and Rahman et al., 2007). In this respect, the environmental risk is assessed by characterization of both soils exposure and plants exposure, in combination with ecological effects. Landis and Yu (l995) defined 'exposure ' as a measure of the concentrations or persistence of a stressor within the defined system; whereas 'ecological effects' are broadly defined as any impact upon a level of ecosystem organization. 'Bioaccumulation' is considered as one of the numerous interactions between the stressor and the ecological system. Plants exposed to continuous metals input become growing under severe selection pressure; evolution of tolerance can occur within one generation, as a result of the powerful selective forces of metal toxicity (Bradshaw, l984 and Baker, l987). The multiplicity of mechanisms and syndrome of metal tolerance, as well as the concept of metal hyperaccumulator plants, have been widely developed due to their ability to hyperaccumulate and hypertolerate heavy metals (Brooks, l998; Memon et al., 2001 ; Lasat, 2002 and Tappero et al., 2007). Chaney et al. (2000) indicated that hypertolerance is fundamental to hyperaccumulation since high rates of metals uptake and translocation are observed in hyperaccumulator plants. On the other hand, Baker et al. (2000) supposed that determining metal-tolerants is the first step in the differentiation of plant populations under severe selection pressure; and to select plants to be used in phytoremediation technologies. Phytoremediation, the use of plants for environmental restoration, is an emerging cleanup technology. Therefore, defining metal hyperaccumulator species has been an impetus for phytoremediation research (Lasat, 2002). Exposure indices of metals accumulation and distribution in ecosystem have been developed (Colburn & Thoronton, l978; Camberlain, l983; Ross, l994 ;Krolack, 2001 and McGeer et al., 2003). The present study focuses on two exposure indices; these are the relative topsoil enrichment (RTE), relating topsoil metal concentrations to subsoil metal concentrations; and the concentration factor (CF), relating plant metal concentrations to soil metal concentrations. The Study Areas

Study areas lie in the north of AL-Jubail Governorate, in the eastern province of Saudi Arabia; at the western coast of the Arabian Gulf. Seven sampling sites, separated by ecological barriers, were selected. The locations of sampling sites are illustrated in Plate l (A & B). Site (1) is a salt marsh located in Jazirat Abu Ali at (27 21' 0.34'' N & 49 31' 14.3" E) . Site (2) is a salt marsh located in Jazirat Al-Huwaylat at (27 06' 17.9" & 49 35' 03.8"E).Site (3) is a mangrove swamp located in Jazirat Al-Gurmah at (27 07' 21.1" N & 49' 45.6"E). These sites are located in three islands which are directorated by the "National Commission for Wildlife Conservation and Development". Whilst site (4) is a reed swamp, namely "Sabkhat AL-Fasl". It is a man-made wetland created mainly by excess irrigation water rich in nutrients ( Plate2). Another three sites are located inside "Jubail Industrial City" (JIC), one of the largest industrial complexes constructed in l978; and directorated by the "Royal Commission for Jubail and Yanbu". Sites: (5) , (6) and (7) are located in the vicinity of industrial complexes at the roadsides of :"Road 100", "Road 272" and "Road 121", respectively(Plate2). The study areas are subjected to many routes of metal exposure. The principal aerial routes are represented by the industrial emissions.Whereas soil surface routes are represented by industrial and domestic wastes. In addition, subsoil routes are represented by minewastes, as well as, a commercial port and an industrial port which is an oil and petrochemical exporting complex; operated since l984. Obviously, the study areas are exposed to both point source and diffuse sources of metal pollution. Moreover, the environmental effects of the l991 Gulf War on ecosystems in the Saudi Arabian Gulf coast should be considered.

MATERIALS AND METHODS

Field samplings of plants and associated soils took place during field trips that were conducted during October, 2001 (dry season) and March, 2002 (wet season).

Plant Materials :
Thirteen plant species were selected from the study areas. Plant nomenclature followed Al-Zoghet (l989) and Mandaville (l990). Nomenclature of cultivated trees followed the list : "Type of Plants in Community Area" reported by HIS (2002). The above-ground tissues were collected from ten individuals for each plant species of the followings:-

Leptadenia pyrotechnica (Forssk.) Decne, from site (1). Haloxylon ammodendron (C. A.Meyer) Bge and Zygophyllum coccineum auct. non L.; from site (2). Avicennia marina (Forssk.) Decne; from site (3). Phragmites australis (Cav) Trin. Ex Steud; from site (4). Phoenix dactylifera L., Ficus nilotica, Tamarix aphylla (L) Karst, Acacia ehrenbergiana Hayne, and Heliotropium ramosissimum (Lehm) DC.; from site (5). Salsola baryosoma (Roem et schult) Dandy; from site (6). Albizzia lebbek and Lygos raetam (Forssk.) Heywood; from site (7).

Soil Materials
Composite soil samples were collected from soil profiles associated with the collected plant species; at
successive depths .Variables were taken into account during field samplings. Soil profiles are named after the associated plant species.

Methods:
Preparation of aqueous soil extracts (l:5 W/V) and acid plant digests followed Reeve & Barnes (l994). The methods of AOAC (l990) were followed to analyze the heavy metals: cadmium (Cd), zinc (Zn), copper (Cu), B (boron), iron (Fe), lead (Pb) , manganese (Mn) and nickel (Ni) in both soil extracts and plant digests; using an atomic absorption spectrophotometer unit for metal analysis in the Royal Commission Environmental & Public Health Laboratory. Metal concentrations are expressed as meq / 100g.dry weight (meq %) . The obtained data are expressed as averages of wet and dry seasons to overcome the seasonal fluctuations of metal concentrations in soils and plant tissues. The results were statistically evaluated by T-test in SPSS 13.0 (SPSS Inc., Chicago, USA) and Microsoft Excel software . Ross(1994) proposed that long-term studies,by necessity,tend to measure metal budgets annually .

Exposure Indices:
Relative Topsoil Enrichment (RTE) and Concentration Factor (CF) were calculated according to Ross (l994) . (RTE) values were calculated as: total metal in 0 - 5 cm zone of soil RTE metal = total metal in 5 - 25 cm zone of soil Accordingly, RTECd, RTEZn, RTECu, RTEB, RTEFe, RTEMn , RTENi are calculated. RTEtotal is calculated for the average of all metals; in all soil profiles. The concentration factor (CF) is calculated as: CFmetal = metal concentrat ion in plant Accordingly, metal concentrat ion in soil

CF is calculated for each investigated heavy metal in each plant species (CFCd, CFZn, CF Cu, CFB, CFFe, CFMn

and CFNi). CFtotal is calculated, relating the average concentrations of all investigated heavy metals; in a plant species to the average concentrations of those metals in the deepest soil profile of the associated soil.

RESULTS AND DISCUSSION

Soil Exposure :
Table (1) indicates that the accumulations of bioavailable B and Fe, in soils, codominate in all sampling sites; ranging between (0.123 0.86 meq%) for B and (0.006 1.100 meq%) for Fe. On the other hand, the low accumulation levels of both Cd (0.006 0.071 meq%) and Zn (0.006 0.017 meq%), in soils (Table l), may indicate the rapid mobilization and redistribution of both metals in soil (Martin & Bullock, l994). Though Mn attained relatively low accumulation levels in soil (0.006-0.092 meq%), Mn may become detrimental because of the relatively increase in levels of available Cu in soils (0.006 0.321 meq%); Dufus (l983) recorded similar observations. The highest total average of metals accumulation (2.45 meq. %) was recorded in the soil of the reed swamp at site (4). This highlights the immobilization of metals in this constructed wetlands as well as, the high
heavy metal retention capacities of such wetlands. May and Edwards (2001) reported that heavy metal retention by constructed and natural wetlands has been effectively used in mining regions of the U.S.

and Europe to reduce levels of Cu, Zn, Ni, Pb and other metals in runoff and drainage. Meanwhile, Tanner (l996) explained that the wetland is a self-maintaining system through the annual production of organic matter that will renew binding sites for metals and maintain redox conditions for sediment chemistry to continue.The potential uses of constructed wetlands in phytoremediation technologies have been, recently reported (Weiss et al., 2006).The calculated RTEtotal values exceed one ; suggesting that metal deposition is an important contributor to metals input into soils at all sampling sites. RTEtotal values may be arranged in a descending order: Site l Leptadenia 2.120 Site 7 Albizzia 1.781 Site 2 Haloxylon 1.448 Site 3 Avicennia 1.400

Site 7 Lygos 1.260

Site 5 T rees 1.229

Site 5 Heliotropi um 1.137

Site 2 Site 6 Zygophyllu m Salsola 1.061 1.031 Moreover, the highest RTE total values in the sites l,2 and 3 which are outside JIC indicate that the areas under study lie within the deposition zones of the industrial sources of emissions. Kanchenco and Singh (2004) suggested that a major pathway of soil contamination is through atmospheric deposition of heavy

metals from point sources such as: metalliferous mining, smelting and industrial activities, and from non point sources such as: fertilizers and organic manures. Moreover, HIS (2002) reported high monthly averages of soil temperatures (30.4C 37.4C) that coincide with high air temperatures (means maxima of 43.8C & means minima of 20.8C) ; during the sampling period. Tiller et al. (2000) related the increase in metal bioavailability in soil to the increase in soil temperature. Hence, the persistence of heavy metals in soil at all sampling sites is evident; implying the exposure of soil to the heavy metals impact. Soils exposure, in turn, represents a principal route for plants exposure in the soil-plant system (Wang et al., 2003 and Kumar et al., 2007).

Plant Exposure :
Generally, plants tend to bioaccumulate metals in their above-ground tissues following the order : Fe > Mn > B > Zn > Cu > Ni > Cd Undetectable values for Pb, in all investigated plants may be due to the high levels of Fe in associated soils. Chaney et al. (2000) recorded that soils rich in Fe may transform soil Pb into forms with lower bioavailability and / or phytoavailability. Most investigated plants seem to be Fe indicators since they tend to accumulate Fe with relatively higher levels than the other metals (Figure1a&b). Memon et al. (2001) considered plants that can accumulate metals in their above-ground tissues, with levels that reflect metal level in the soil, as metal indicators. Total averages of metal bioaccumulations (meq.%) varied among plants species following the order: Salsola 32.367 Albizzia 9.304 Avicennia 9.487 Zygophyllum 7.097 Heliotropium 9.333 Phoenix 6.523

Ficus 5.968

Haloxylon 5.775

Acacia 5.712

Lygos 5.46

`Leptadenia 5.171

Tamarix 5.003

Phragmites 3.432

These levels of metal bioaccumulations in the above-ground tissues of plants, the primary producer trophic level, indicate their bioaccumulative properties which may pose health risks at higher trophic levels of ecosystem. Metal bioaccumulations have been considered as one of the parameters useful in the bioindication of metal impact (Ross, l994 and Mulgrew & Williams, 2000). Meanwhile, Memon et al. (2001) assumed metal accumulation in plants as a plant response to metal stress.

Ecological Effects:
Investigated plants varied widely in their capabilities to bioconcentrate heavy metals in their above - ground tissues ,as indicated by the recorded values of CFtotal for each plant (Table2). Accordingly , plants followed the descending order: Salsola > Heliotropium > Albizzia > Phoenix > Haloxylon > Zygophyllum > Lygos > Leptadenia > Avicennia > Acacia > Tamarix > Ficus >Phragmites. Such variation suggests that plants are ecologically affected, differently, by metal exposure. Hence, an attempt to categorize them may represent three categories. The first, includes three Fe-hyperaccumulators that are capable of bioconcentrating Fe to exceptionally high levels, in their above-ground tissues. These are: Salsola (CFFe 507.69) , Lygos (CF Fe 178.72) and Phoenix (CF Fe 131.10) . This metal hyperaccumulation is considered as an ecological effect of exposure that implies the evolution of metal tolerance in these exposed plants. From another point of view, such metal hyperaccumulation points to high affinities for metals uptake from soils, and for metals translocation from roots to shoots; hence, the above mentioned species are efficient to be used in phytoextraction technology. In addition, Tamarix is assumed to be Zn hyperaccumulator (CF zn128.33); though this species failed to bioconcentrate metals with high levels (CF total 3.00) . This may be explained by the fact that Tamarix is, ecologically, classified as an excluder (Ahmed & Girgis, l979) . Hence, Tamarix trees can prevent, effectively, metals from entering their aerial parts over a broad range of metals concentration in the soil. However, they still contain large amount of metals in their roots (Memon et al.,2001 and Prasad, 2006).Such plants can be efficient for phytostabilization technology (Lasat 2002 and Pauwels et al., 2008). The second category includes six coaccumulators which are capable of bioconcentrating, usually , high levels of more than one metal in their above-ground tissues. Moreover, they recorded high levels of CFtotal (Table2) . The cultivated trees of both Albizzia and Avicennia bioconcentrate high levels of both Fe (CF Fe62.06 and CFFe 44.73, respectively ) and Zn (CF zn24.07 and CF zn 37.67 , respectively). Though, Albizzia bioconcentrates total metals (CF total) with higher levels. Whereas, the wild shrubs Leptadenia and Heliotropium bioconcentrate high levels of both Zn (CF zn51.50 and CFzn75.00 , respectively) and Mn(CFMn34.19 and CFMn 30.53, respectively). Though, Heliotropium was able to bioconcentrate total metals (CF total) with higher levels. On the other hand, the succulent shrubs: Haloxylon and Zygophyllum bioconcentrate total metals (CFtotal) with similar levels , as well as, remarkable high levels of Fe (CFFe74.83 and CFFe77.88, respectively). Coaccumulation and cotolerance is well established among species (Baker et al., 2000); though, coaccumulators do not follow definite mechanism in metal tolerance (Memon et al., 2001) . Hence,

coaccumulation may be regarded as defensive mechanism adopted by the exposed plants towards metals impact. Edward et al. (2006) suggested that metal concentrations at or below the accumulator range may be defensively effected. The third category includes three non-accumulators; these are: the common reed Phragmites and the cultivated trees of Ficus and Acacia . The three species bioconcnetrated the lowest levels of metals (CFtotal) among the other investigated plants (Table2). Though, Phragmites and Acacia bioconcentrate high levels of Zn, CF zn43.71 and CF zn52.33; respectively. Whilst, Ficus was unique in bioconcentrating high level of Mn (CF Mn 56.28). The survival of these non-accumulators in such exposed areas may point to the development of stress- tolerant plantmycorrhizal associations. Schutzendubel and Polle (2002) proposed that mycorrhization protects plant roots from metal-induced injury. Whilst, Shutes (2004) recorded that Phragmites australis has been commonly used for its metal tolerance uptake and filtration ability. Boer (l994) reported that salt-marshes and mangroves of the Saudi Aabian Gulf coast were identified as the most severely affected habitats following the l991 Gulf War oil spill . Hence, significant ecological effect is expected due to the exposure of soil-plant systems to combinations of metals and oil spill. Edward et al. (2006) suggested that effects of such combinations are additive rather than synergistic or antagonistic.

Acknowledgement The authors gratefully acknowledge financial support form the Health Service Department, Directorate General for Jubail Project; and from the National Commission for Wildlife conservation and Development, Jubail Marine Wildlife Sanctuary .

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