Nutritional value of some algae from the north-westernMediterranean coast of Egypt

N. G. Shams El Din & Z. M. El-Sherif

Received: 12 April 2011 /Revised and accepted: 19 March 2012 /Published online: 4 May 2012# Springer Science+Business Media B.V. 2012

Abstract Fourteen taxa from Chlorophyta, Rhodophytaand Phaeophyta were collected from seven stations at dif-ferent depths, along the north-western Mediterranean coastof Egypt during winter and summer 2006. Total carbohy-drates (TCH), total protein (TPr), total lipids (TL), chloro-phyll a, β-carotene, minerals and trace metals weredetermined in a total of 50 specimens. The concentrationsof these components varied significantly with respect to thealgal taxa and showed different patterns of distribution inthe three classes. The content of TCH ranged from 5 to20.9%, being much higher for Cystoseira spinosa (20.9%),TPr 3.86 to 27.65% where Gelidium corneum showed themaximum value and TL content displayed wide variation(2.34 to 48.95%), with Sargassum hornschuchii having thehighest values. A minor component was β-carotene in allsamples (1.80−2.50×10−3 mg (100 g)−1) which was muchlower than in vegetables, in contrast to chlorophyll a concen-trations which have attained high values (6.70−94.20 mg (100g)−1) and were lower than in vegetables. Mineral content wasabundant in all samples and was higher than in common foodand vegetables, whereas the measured trace metals allexceeded the permissible doses and were far from the acceptedconcentrations in the regulations of many countries. This limitstheir use in food consumption, except copper which recordedacceptable concentrations in the study. The maximum valuesof phosphorus (3 ,305 mg (100 g−1) , potassium(930 mg (100 g−1) and calcium (3,070 mg (100 g−1) were

recorded in members of Chlorophyceae: Codium bursa,Udotea sp. and Udotea petiolata, whereas the red algaRhodymenia ardissonei had the lowest concentrations in iodine(80 ppm) and sodium (1,450 mg (100 g)−1) and the highestconcentrations in the trace metals copper (3.89 ppm), nickel(13.14 ppm), zinc (38.87 ppm) and a relatively large amount oflead (41.60 ppm).

Keywords Seaweeds . Natural components . Mineralsand trace metals . Food

Introduction

In the last decades, many current and potential uses ofseaweeds have been identified in several categories suchas agriculture, animal aquaculture, cosmetics, pharmacolo-gy, biomedicine, health and food (Apaydin et al. 2010).Seaweeds contain almost all of the important nutritionalcomponents, but also contain them in levels that often farexceed their terrestrial counterparts vegetables (Lee 1975).It is now known that seaweeds contain numerous bioactiveproperties including cholesterol-lowering and free radical-scavenging activities (Brennan 2005). In addition, they canstrengthen kidney function, improve mental concentration,can even promote sexual function, protect against cancerand can be helpful in aiding the elimination of nuclearradiation from the body (Van den Hoek et al. 1996). Theyare virtually fat and calorie free (Ismail and Hong 2002), butfew of them exhibit high concentration of proteins andindigestible carbohydrates (Mamatha et al. 2007). It is easyto see why seaweeds are building a reputation as the new‘super food’ (Hotchkiss and Trius 2007). In theory, mostseaweeds are edible, but whether they are palatable is adifferent matter. As many as 500 species of seaweeds are

N. G. S. El Din (*) : Z. M. El-SherifHydrobiology Lab—Marine Environment Department,National Institute of Oceanography and Fisheries,14 Street Sadikat El Ketab El Mokadass, Assafra, Floor No. 8,Flat No. 22,Alexandria, Egypte-mail: nihalshamseldin@yahoo.com

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harvested or cultured, and every year, millions of tonnes areused to supply the food industry (Hotchkiss and Trius2007). Asian countries—in particular China, Japan andKorea—are the primary users of seaweeds for food(Ratana-arporn and Chirapart 2006; Hotchkiss and Trius2007; Madhusudan et al. 2011). Consumption by humansin these countries is (5%) of green algae, brown algae(66.5%) and red algae (33%, Dawes 1998; Devi et al.2009). In Europe, traditional uses of seaweeds are not ascommon as in Asia, but some species such as Porphyra spp.and Palmaria palmata are found in the coastal towns ofIreland and the UK (Hotchkiss and Trius 2007). France wasa pioneer in establishing a specific regulation concerning theuse of seaweeds for human consumption as a nontraditionalsource of mineral elements, macro elements and trace ele-ments (Mabeau and Fleurence 1993). As one of the mostimportant vegetable sources of calcium (Ca), seaweed con-sumption may be useful for expectant mothers, adolescentsand elderly all exposed to a risk of calcium deficiency(Burtin 2003). In addition, they contain high levels of po-tassium (K), sodium (Na), magnesium and phosphorus (P,Mabeau and Fleurence 1993; Rupérez and Saura-Calixto2001; Rupérez et al. 2002; Nisizawa 2006), and have beenshown to have a positive effect on regulating mineral bal-ances and blood pressure (Ismail and Hong 2002). Iodine (I)is necessary not only for the production of thyroid hormones(Dhanalakshmi et al. 2010), but also it is now recognized asplaying a protective role against fibrocystic breast diseaseand breast cancer (Patrick 2008). A relationship also hasbeen hypothesized between iodine deficiency and a numberof other health issues such as attention deficit hyperactivitydisorder, psychiatric disorders, (NHMRC 2005), and non-specific disease categories such as chronic fatigue and de-pressed immunity (Drum 2008). In addition, seaweeds are asource of trace metals such as copper, zinc and iron(Ensminger et al. 1995). Furthermore, polysaccharides andvitamins derived from a number of seaweeds have beenshown to possess antioxidant properties, associated withthe carotenoid fraction (Moore et al. 1998; Potter 1999;Ismail and Hong 2002).

Nutritional value of seaweeds in the Egyptian MediterraneanSea, especially on Alexandria beaches and the eastern coast, hasbeen investigated in a limited number of articles (El-Tawil andKhalil 1983; El-Sarraf and El-Shaarawy 1994; Wassef et al.2001, 2005; Abdallah 2007, 2008; Shams El Din et al. 2007).There are also very few studies on the western EgyptianMediterranean Sea (Masoud et al. 2006).

This present study is the first conducted along the north-western Mediterranean coast to analyse the chemical com-position and evaluate nutritional value of some seaweeds fortheir use as potential food ingredient. The toxicologicalaspects associated with some of these components must betaken into account, in addition to find out the spatial andinterspecific differences.

Materials and methods

Two cruises were carried out during winter (31 January to 5February) and summer (3–10 September) 2006 along thenorth-western Mediterranean coast using the Egyptian r/v“El-Salsabil” and covering seven stations with differentdepths, namely El Salloum (St. I), Sidi Barani (St. II),Zawyet El Shamass (El Shalia; St. III), Alam El Roum (St.IV), El Dabaa (St. V), Sidi Abdel Rahman (St. VI) and ElHammam (St. VII; Fig. 1). All these stations except ElDabaa (a restricted site) are subjected to tourism activitiesand irregular agriculture activities, resulting sometimes inseepage water discharging into the sea. In addition, the ElHammam station is located near El Hamra Harbor whichexports petroleum products. On the other hand, the studyarea is influenced by prevailing wind and current regime(Sharaf El-Din et al. 2006). All samples were collectedduring summer except El Salloum (St. V), which was sam-pled during winter. The physico-chemical parameters of theseven stations of the study area are shown in Table 1.

Algae samples were collected by dredging, washed withseawater at the sampling site to remove the adhered sedi-ments, impurities and epiphytes, separated in polyethylenebags and stored at 4°C. Quick rinsing of the algae with tap

25 25.5 26 26.5 27 27.5 28 28.5 29 29.5

Longitude (°E)

31.0

31.5

32.0

32.5

Lat

itud

e (o N

)

Mediterranean Sea

El-

Sallo

um

Egypt

Fig. 1 The study area andsampling stations during 2006

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Table 2 The distribution and frequency of the different algal species at the sampling sites during 2006

Algal group El Salloum SidiBarrani

Zawyet ElShamass

Alam ElRoum

El Dabaa Sidi AbdelRahman

El Hammam No. of samples/species

Class: Chlorophyceae

Order: Bryopsidales

Family: Caulerpaceae

C. prolifera + + − + + − + 5

C. racemosa + + − − + − − 3

Family: Codiaceae

C. bursa + − − + + + − 4

Family: Udoteaceae

H. tuna + − − − − − − 1

U. petiolata − − − + − − − 1

Udotea sp. + − + − − + − 3

Class: Rhodophyceae

Order: Gelidiales

Family: Gelidiaceae

G. corneum + + + + + − + 6

Order: Gigartinales

Family: Gracilariaceae

G. verrucosa + + + + + − + 6

Order: Rhodymeniales

Family: Rhodymeniaceae

R. ardissonei + − − − − − − 1

Class: Phaeophyceae

Order: Dictyotales

Family: Dictyotaceae

D. dichotoma − + − − + − − 2

Order: Fucales

Family: Cystoseiraceae

C. spinosa + + + + + + + 7

Family: Sargassaceae

S. acinarium − + − − + + − 3

S. hornschuchii − + − − + − − 2

S. vulgare + + + + + + − 6

No. of samples=50 10 9 5 7 10 5 4

Note: plus sign, the species is present; minus sign, the species is absent

Table 1 The physico-chemical characteristics of the study area during 2006 [dissolved oxygen and nutrients after Hemaida et al. (2008)temperature and salinity personal communication; Maiyza]

Stations Depth (m) Temp. (°C) Salinity (‰) pH D.O. (mL L−1) NH4 (μM) NO2 (μM) NO3 (μM) PO4 (μM) SiO4 (μM)

El Salloum (St. I) 85 17.1 38.9 8.4 5.05 4.06 0.08 2.41 0.06 1.69

Sidi Barani (II) 73 16.9 38.6 8.3 5.48 2.82 0.37 5.20 0.26 4.04

Zawyet El Shamass (III) 52 16.9 38.4 8.3 5.46 1.9 0.46 7.35 0.56 4.60

Alam El Roum (IV) 50 17.5 38.5 8.3 5.28 1.63 0.28 4.83 0.20 5.74

El Dabaa (V) 50 17.5 38.5 8.2 5.55 1.51 0.33 6.25 0.23 4.73

Sidi Abdel Rahman (VI) 60 18.5 38.6 – – – – – – –

El Hammam (VII) 51 17.6 38.6 8.6 5.45 1.83 0.82 3.01 0.37 5.34

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water was carried out in the laboratory on the same day toget rid of the remaining impurities and epiphytes.Herbarium sheets with a preliminary identification of sepa-rated species were prepared, and/or the algae were preservedin 4% formalin. Microscopic identification was carried outaccording to Riedel (1970) and Aleem (1993). Each algaesample was divided into three subsamples: the first to carryout the measurements for natural products, the second forpigments and iodine, and the third for the minerals and tracemetals. The total average and the standard deviation for eachconstituent of each species were calculated.

Total protein, total carbohydrates and total lipids weremeasured as follows Algal subsamples were dried at roomtemperature (25°C) to a constant weight and then ground tofine powder. For each component, 1 g dry weight (d.w.) wastaken. Total protein (TPr) content was estimated spectropho-tometrically at 650 nm by the method described by Lowry etal. (1951), using a salt-free bovine serum albumin as astandard. Total carbohydrate (TCH) content was estimatedaccording to Dubois et al. (1959). Total lipids (TL) wereestimated according to Bligh and Dyer (1959).

For pigment analysis another algal subsample was dried at25°C to a constant weight for pigment analysis, and 0.5 gm ofseaweeds powder was used for extraction of β-caroteneaccording to the method of Evans (1988). Another 0.5 g ofthe dried seaweed powder was used for extraction of chloro-phyll a (Chl.a) according to Jeffrey and Humphrey (1975).

For mineral and trace metal analysis, algal subsampleswere dried at 60°C to a constant weight, homogenized bycrushing each sample in a porcelain pestle and mortar andkept away from metallic materials and dusty conditions toavoid contamination. One gram dry weight of each samplewas acid digested in 5 mL concentrated HNO3 in a Teflon-lined vessel in a microwave oven in pressure-controlledconditions. Digested samples were filtered through anacid-washed filter (Whatman GF/C) and diluted to 25 mLwith double distilled water (Haritonidis et al. 1983;Mohamed and Khaled 2005). Copper (Cu), nickel (Ni), lead(Pb) and zinc (Zn) were measured using a Shimazu atomicabsorption spectrophotometer AA-6800. The reportedresults are means of triplicate determinations and exposedas micrograms per gram dry weight. All glasswares, plasticand Teflon devices were thoroughly acid washed.

The measurement of phosphorus was based on the reac-tion of phosphate with molybdate in strong acidic mediumto form a complex (Gamst and Try 1980). Sodium determi-nation was based on modifications of the method of Trinder(1951) and Maruna (1958) where sodium is precipitated asthe triple salt sodium magnesium uranyl acetate with theexcess uranium which will react with ferrocyanide, produc-ing a chromophore whose absorbance varies inversely as theconcentration of sodium in the sample. Potassium was

determined using the method of Terri and Sesin (1958).Total calcium was measured by the method of Stem andLewis (1957). For iodine measurement algal subsampleswere dried at room temperature (25°C) to a constant weightand then ground to fine powder and 1 g used for analysis.The method of iodine measurement depends upon alkalifusion and ashing of dry seaweed powder using sodiumcarbonate, sodium hydroxide and diluted nitric acid(Hamdy 1982). The diluted solution was measured spectro-photometrically at 540 nm according to Rogina andDubravcic (1953).

Results

A total of 50 algal samples were collected from seven sitesat different depths, representing three algal classes (Table 2).Chlorophyceae was represented by Caulerpa prolifera(Forsskal) Lamouroux and Caulerpa racemosa (Forsskal)J. Ag., forming the frequency of 71 and 43%, respectively,Codium bursa (Linnaeus) C. Agardh (57%), Halimeda tuna(Ellis et Solander) Lamouroux and Udotea petiolata havingboth frequency of 14% and Udotea sp. (43%). The classRhodophyceae was represented by Gelidium corneumGreville (86%), Gracilaria verrucosa (Hudson) Papenfuss(86%) and Rhodymenia ardissonei J. Feldman (14%). Thethird class Phaeophyceae was represented by Dichtyotadichotoma (Hudson) Lamouroux (29%), Cystoseira spinosaSauvageau (100%), Sargassum acinarium Linneaus (43%),Sargassum hornschuchii C. Agardh (29%) and Sargassumvulgare C. Agardh (86%).

The TCH, TPr and TL varied greatly between species(Table 3). The carbohydrate content ranged from 5.00% (R.ardissonei) to 20.91% (C. spinosa). The protein contentranged from (38.60±45.86 mg g−1) in C. prolifera to276.50±264.41 mg g−1 in G. corneum. TL displayed widevariations from the lowest value 23.45±8.49 mg g−1 in C.bursa to 489.50±3.5 mg g−1 in S. hornschuchii. The valuesof TCH and TPr were within the values reported by otherauthors, whereas TL content was much higher. The range ofTCH and TPr content in the present study was more or lessequivalent to many higher plants and whole food, whereasthe range of TL was much higher (Table 4).

Like TCH, TPr and TL, the quantities of the two pig-ments Chl.a and β-carotene also displayed considerableindividual differences (Table 3). The lowest values ofChl.a and β-carotene were in Udotea sp. (6.70±4.60 and1.80±0.10×10−3 mg (100 g)−1, respectively). On the otherhand, the highest value of Chl.a (94.20±24.80 mg (100 g)−1)was found in D. dichotoma, and the highest β-carotene con-centration (2.50×10−3 mg (100 g)−1) was determined in U.petiolata. Thus, the concentration of Chl.a in the three classeswas as follows: Chlorophyceae > Phaeophyceae >

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Rhodophyceae, while the concentration of β-carotene wasalmost equal in the three classes. The values of Chl.a and β-carotene were different than in the previous studies and invegetables (Table 4).

The concentration of minerals I, P, K, Na and Ca alsoshowed great interspecific and among group variation(Table 5). The red alga R. ardissonei had the lowest concen-trations of iodine (80 ppm), sodium (1,450 mg (100 g)−1) andcalcium (520 mg (100 g)−1), whereas Udotea sp. and H. tunacontained the lowest amount of phosphorus (173±94.80 mg (100 g)−1) and potassium (110mg (100 g)−1), respec-tively. Furthermore, S. hornschuchii and S. vulgare containedthe highest amount of iodine (300 ppm) and sodium(3,058.30±1,319.20 mg (100 g)−1), respectively, where-as the green algae C. bursa, Udotea sp. and U. petiolatarecorded the maximum concentration of phosphorus(3,305 ± 3,758.20 mg (100 g)−1), potassium (930±510.20 mg (100 g)−1) and calcium (3,070 mg (100 g)−1), re-spectively. Like the other components, the mineral concen-trations showed different distribution patterns in the threeclasses (Table 5) and varied concentrations with respect toother localities (Table 6).

The red alga R. ardissonei recorded the highest concentra-tions of Cu (3.89 μg g−1), Ni (13.14 μg g−1) and Zn(38.87 μg g−1), whereas the brown alga S. acinarium containedthe highest amount of Pb (45.267±29.98 μg g−1). On the other

hand, Cu was below the detection limit in H. tuna, while C.bursa, U. petiolata and S. acinarium recorded the lowest con-centrations of Ni, Pb and Zn (Table 7). Chlorophyceae showedthe lowest concentrations in Ni and Pb. The order of metalabundance in these seaweeds was generally Cu < Ni < Zn < Pb(Table 7). In comparison with the previous studies, the concen-tration of copper in this study was lower, whereas the otherelements showed varied concentrations (Table 8).

The correlation coefficient between the physico-chemicalparameters and THC, TPr, TL, pigment content, minerals andtrace element content revealed that iodine, nickel, zinc and β-carotene content were correlated with physico-chemical param-eters; TCH was positively correlated with water temperature(Table 9). Cluster analysis of spatial variations of the compo-nents in the algal species showed three subclusters: the firstincludes stations IV, VI and VII, the second includes stations I,II and III, whereas the third cluster includes only station V(Fig. 2). Cluster analysis of the different algal species alsoshowed clear associations between different species based onthe contents of these species (Fig. 3).

Discussion

Previous studies of the Egyptian Mediterranean coastshowed that the TCH content in seaweeds was relatively

Table 3 The average concentrations and standard deviation (SD) ofnatural components (TCH, TPr, and TL; in mg g−1) and pigmentscontents (Chl.a and β-carotene; mg (100 g)−1) in algal groups

(Chlorophyceae, Rhodophyceae and Phaeophyceae) along the westerncoast of Alexandria, Egypt, 2006

TCH (avg.±SD) TPr (avg.±SD) TL (avg.±SD) Chl.a (avg.±SD) β-Carotene (×10−3) (avg.±SD)

Chlorophyceae

C. prolifera 90.00±54.66 38.60±45.86 137.00±101.48 53.30±29.60 2.40±0.30

C. racemosa 69.33±12.26 82.33±62.49 23.93±5.06 48.70±5.00 2.30±0.20

C. bursa 74.25±9.60 53.50±37.26 23.45±8.49 28.80±18.40 2.10±0.30

H. tuna 74.00 118.00 33.30 11.90 2.30

U. petiolata 86.00 115.00 118.00 46.90 2.50

Udotea sp. 80.00±11.43 145.00±24.86 49.67±24.14 6.70±4.60 1.80±0.10

Total average 79.71±32.78 77.76±59.32 67.70±77.42 35.68±26.61 2.20±0.30

Rhodophyceae

G. corneum 120.33±24.59 276.50±264.41 370.50±235.76 14.30±9.50 2.20±0.20

G. verrucosa 157.67±55.73 70.83±54.54 232.83±201.78 11.90±10.90 2.10±0.40

R. ardissonei 50.00 45.00 120.00 24.00 2.40

Total average 132.15±53.04 163.77±219.75 287.69±235.43 13.93±10.76 2.10±0.40

Phaeophyceae

C. spinosa 209.14±68.30 70.14±35.79 139.43±66.70 19.10±23.40 2.30±0.30

D. dichotoma 86.00±2.00 81.50±57.50 93.00±34.00 94.20±24.80 2.40±0.10

S. acinarium 136.67±24.57 39.00±23.37 301.67±180.59 16.00±7.80 2.30±0.30

S. hornschuchii 165.00±29.00 60.50±36.50 489.50±3.50 9.30±6.80 2.30±0.40

S. vulgare 143.00±65.44 61.50±23.80 182.00±119.35 20.60±12.50 2.10±0.30

Total average 161.70±69.99 63.05±37.05 206.90±156.44 25.63±29.87 2.20±0.30

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low (2.88−10.20%; Abdallah 2007, 2008; Shams El Din etal. 2007; with the exception of El-Tawil and Khalil 1983). Inthe present study, TCH is consistent with the recorded lowvalues. However, these species are edible vegetables inseveral countries and they demonstrated acceptable concen-trations in the present study compared with the previousstudies and with higher plants. The order of concentrationof TCH content in the three classes (Phaeophyceae >Rhodophyceae > Chlorophyceae) agrees with Khalil andEl-Tawil (1982) El-Tawil and Khalil (1983) and Heiba etal. (1990), whereas Shams El Din et al. (2007) found theinverse pattern.

Edible macroalgae are rich in resistant protein and dietaryfibre (Mamatha et al. 2007) compared with fruits and veg-etables (Gómez-Ordóñez et al. 2010). Protein content differsaccording to species being generally low in brown seaweeds(3% d.w.) compared with green or red algae (10% d.w.,

Fleurence 1999; Dere et al. 2003; Marinho-Soriano et al.2006). Our results correspond with these findings, since thelowest protein content was recorded in the brown alga S.acinarium (3.9%) and generally with lower TPr content inPhaeophyceae with respect to Chlorophyceae andRhodophyceae. El-Sarraf and El-Shaarawy (1994) reportedcomparable protein content in algae from eastern EgyptianMediterranean Sea. Marinho-Soriano et al. (2006), Plaza etal. (2008), Manivannan et al. (2009) and Patarra et al. (2011)also recorded comparable level of proteins to the presentstudy. In contrast, Dhanalakshmi et al. (2010) recorded avery low value of TPr content.

The fat content of seaweeds is primarily composed ofunsaturated fatty acids, which makes them a healthy foodchoice. In addition, many seaweeds contain a functionalbalance of the omega-3 and omega-6 essential fatty acids(Ismail and Hong 2002). The lipid content in this study was

Table 4 The concentrations of natural components (%) and pigments (mg/100 g) in the present study, previous studies and in higher plants

Natural components Present study Previous studies Higher plants

Carbohydrate content 5–20% 31–50% (Solimabi et al. 1980) Cabbage (4.10%, McCance et al. 1993)

38–79.74% (El-Tawil and Khalil 1983) Broccoli (5.2%, Dubuc and Lahaie 1998)

0.65–6.3% (Dere et al. 2003) Carrots (7.90%)

5.3–10.2% (Shams El Din et al. 2007) Apples (11.80%)

2.88–8.16% (Abdallah 2007, 2008) Prunes (19.70%, Norziah and Ching 2000)

35.7% (MacArtain et al. 2007) Potato (19.00%, Hanif et al. 2006)

14.34–30.58% (Chakrabortyand Santra 2008)

Red chilli (8.8%, USDA 2010)

67.90% (Plaza et al. 2008)

14.73–17.49% (Manivannan et al. 2009)

2.1–10% (Dhanalakshmi et al. 2010)

Protein content 3.86–27.65% 6.8–27.7% (El-Sarraf andEl- Shaarawy 1994)

Dry bean (22%)

15.97–23.05% (Marinho-Soriano et al. 2006) Soya bean (36%, Haytowitz and Matthews 1986;Anderson et al. 1991)

1.12–3.05% (Polat and Ozogul 2008) Broccoli (3%, Dubuc and Lahaie 1998)

9.65–31.07% (Manivannan et al. 2009) Red chilli (1.9%, USDA 2010)0.01–0.1% (Dhanalakshmi et al. 2010)

6.81–26.62% (Patarra et al. 2011)

Lipid content 2.34–48.95% 0.8–11.36% (El-Tawil and Khalil 1983) Dry bean (1%)

10.8–14.5% (Shams El Din et al. 2007) Soya bean (19%, Haytowitz and Matthews 1986;Anderson et al. 1991)

5.7–8% (Abdallah 2008) Broccoli (0.3%, Dubuc and Lahaie 1998)

2.61–7.13% (Chakraborty and Santra 2008) Red chilli (0.4%, USDA 2010)0.45% (Plaza et al. 2008)

0.26–3.53% (Manivannan et al. 2009)

Chlorophyll a 6.7–94.2 2.8–23.6 (Amer 1999) Spinach (12–24×102)

11.34–24.32 (Shams El Din et al. 2007) Broccoli (1.03×102, Bhat 2005)37–245 (Chakraborty and Santra 2008)

β-Carotene 0.0018–0.0025 0.08–0.88 (Amer 1999) Spinach (5.63)

0.0021–0.0035 (Shams El Din et al. 2007) Red chilli (0.534)

Broccoli (0.361, USDA 2010)

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much higher than reported in previous studies (2.34−48.95%). In fact, a high lipid content is frequently encoun-tered in some microalgae, reaching 38−40% and can reach90% under certain conditions (Undeland et al. 2009) butrarely in macroalgae. Whereas microalgae have receivedextensive attention regarding lipid content, benthic algaehave received relatively little attention and our knowledgeis still rather poor (Rajasulochana et al. 2010). In general,productivity and lipid content are inversely correlated, andstress conditions such as deprivation of nitrogen or phos-phate (Scott et al. 2010), which limit cell growth, alsoincrease lipid content (Rodolfi et al. 2009). The nature ofthe process by which the increased lipid synthesis is inducedseems to be of considerable interest in basic studies on lipidmetabolism (Richardson et al. 1969). One of the factors thataffect lipid metabolism is excess light energy, which can bepotentially harmful and result in harmful reactive oxygenspecies formation. These accumulate and can cause moredamage than can be reconciled, and the algae may experi-ence photoinhibition and oxidative stress. Hence, with in-creased light, there is an increased susceptibility to photo-oxidative stress (Niyogi 2000), and it has been proposed thatincreased lipid synthesis is perhaps the ‘default pathway’ todefend against photo-oxidative stress that can occur as aresult of too much reducing energy (Hu et al. 2008). Theother factor that may affect lipid content is the relationship

with other organisms in the same communities resulting instress as predation, epiphytism or competition leading toallelopathy (Hay 2009). However, seaweeds show greatspecies-specific variation in the three components (TCH,TPr and TL) as well as different distribution patterns in thethree classes. These may reflect the influence of geographicorigin, environmental factors such as water temperature,salinity, light and nutrients, as well as different samplingmethodologies (Fleurence 1999; Dere et al. 2003; Marinho-Soriano et al. 2006). In the present study, TL and TPrcontent displayed varied correlations with environmentalfactors, and TCH was positively influenced by water tem-perature. Thus, further studies should be undertaken todetermine the role of light and currents, and to focus onseasonal variations.

The present study found higher chlorophyll a concentra-tions and lower β-carotene than those given by Amer (1999)along the Suez Canal and by Shams El Din et al. (2007)along the eastern coast of the Egyptian Mediterranean Sea,while Chakraborty and Santra (2008) reported Chl.a con-centration from 37 to 245 mg (100 g)−1. These differences inthe pigments concentrations may be related to the algalspecies and light intensity (Li and Titlyanov 1978; Dring1981) and other factors such as degree of algal maturity,method of extraction and certain biological and technicalfactors (Rahmani et al. 1991). Recent studies have reported

Table 5 The average concentrations and standard deviation (SD) of minerals [iodine (μg gm−1) and P, Na, K and Ca (mg (100 g)−1 dry weight)] inalgal groups (Chlorophyceae, Rhodophyceae and Phaeophyceae) along the western coast of Alexandria, Egypt, 2006

Iodine (avg.±SD) P (avg.±SD) Na (avg.±SD) K (avg.±SD) Ca (avg.±SD)

Chlorophyceae

C. prolifera 251.00±74.00 311.60±164.00 1,500.00±757.60 342.00±390.40 1,854.00±617.40

C. racemosa 181.00±62.00 356.70±28.70 2,250.00±717.60 833.30±267.10 2,940.00±70.70

C. bursa 213.00±95.00 3,305.00±3,758.20 2,325.00±396.10 307.50±290.70 2,505.00±427.90

H. tuna 88.00 390.00 1,500.00 110.00 1,240.00

U. petiolata 290.00 280.00 1,950.00 170.00 3,070.00

Udotea sp. 206.00±82.00 173.00±94.80 2,216.70±704.00 930.00±510.20 1,993.30±721.50

Total average 214.00±89.00 1,002.20±2,297.60 1,979.40±740.60 500.60±468.80 2,258.80±732.10

Rhodophyceae

G. corneum 249.00±74.00 258.30±66.90 2,091.70±614.00 271.70±52.40 2,690.00±384.40

G. verrucosa 248.00±75.00 212.00±112.30 2,308.30±591.90 268.30±66.20 2,505.00±287.30

R. ardissonei 80.00 850.00 1,450.00 320.00 520.00

Total average 234.00±88.70 282.50±195.30 2,142.30±647.10 273.80±61.30 2,437.70±675.00

Phaeophyceae

C. spinosa 240.00±75.00 305.70±293.90 1,914.30±410.30 184.30±82.80 2,457.10±645.20

D. dichotoma 283.00±8.00 325.00±15.00 2,100.00±150.00 905.00±685.00 2,735.00±175.00

D. dichotoma 243.00±82.00 260.00±92.70 2,033.30±271.80 330.00±14.10 2,163.30±662.40

S. hornschuchii 300.00±0.00 275.00±45.00 2,225.00±375.00 315.00±145.00 1,990.00±30.00

S. vulgare 236.00±79.00 330.00±151.50 3,058.30±1,319.20 620.00±500.50 2,026.70±789.70

Total average 249.00±75.00 305.00±203.30 2,325.00±944.60 422.00±440.00 2,265.00±698.10

J Appl Phycol (2012) 24:613–626 619

that average dietary intake of natural β-carotene is some-where between 2 and 5 mg day−1 and that supplementingwith excessive amounts of synthetic β-carotene in isolation

is of no benefit and may be harmful, especially for smokers(Omenn et al. 1996; Woodall et al. 1996). However, naturalsource of β-carotene is highly recommended as they protect

Table 6 The concentrations of minerals [iodine (μg/g–1) and P, Na, K and Ca (mg/100 gm dry weight)] in the present study, previous studies and inhigher plants and whole food

Minerals Presentstudy

Previous studies Higher plants and whole food Permissible doses

Iodine 80–300 30–90 (El-Tawil and Khalil 1983) Peanuts (200) 150–250 μg day−1 (Madhusudanet al. 2011)220–480 (Shams El Din et al. 2007) Whole milk (150)

Banana (80 ppm)

Spinach (20, McCance et al. 1993)

Phosphorus 173–3,305 15.60–185.40 (Masoud et al. 2006) Broccoli (66) 700 mg day−1 for male and female(Ratana-arporn and Chirapart2006)

100–740×102 (Murata and Nakazoe 2001) Spinach (84)

140–180 (Ratana-arporn and Chirapart2006)

Potato (46, Hanif et al. 2006)

Cabbage (29, Yildirim et al. 2001)

Calcium 520–3,070 4,563–32,537 (Masoud et al. 2006) Broccoli (48) 800 mg day−1 for male and female(Ratana-arporn and Chirapart2006)

710–1,400×102 (Murata and Nakazoe2001)

Spinach (76)

780–1,030 (Ratana-arporn andChirapart 2006)

Potato (8) (Hanif et al. 2006)

280–2,830 (Santoso et al. 2006) Cabbage (49, Yildirim et al. 2001)329.69–3,792.06 (Matanjun et al. 2009)

Na/K ratio 2.7–13.63 <1.5 (Rupérez 2002) Spinach (0.28)0.41–8.03 (Santoso et al. 2006) Cheddar cheese (8.7, McCance

et al. 1993)

1.14–1.42 (Abdallah 2008) Olive (45.63)

0.14–0.16 (Matanjun et al. 2009) Sausages (4.89, Ortega-Calvoet al. 1993)

Table 7 The average concen-trations and standard deviationof the trace metals [Cu, Ni, Pband Zn (μg/g–1) dry weight] inalgal groups (Chlorophyceae,Rhodophyceae and Phaeophy-ceae) along the western coast ofAlexandria, Egypt, 2006

Cu (avg.±SD) Ni (avg.±SD) Pb (avg.±SD) Zn (avg.±SD)

Chlorophyceae

C. prolifera 0.06±0.12 7.62±3.89 20.43±4.33 22.33±20.40

C. racemosa 0.49±0.69 8.96±2.49 18.24±3.62 26.17±13.42

C. bursa 1.05±1.54 4.98±3.05 17.70±2.80 14.97±5.58

H. tuna 0.00 10.60 32.84 33.16

U. petiolata 0.10 7.27 13.14 22.84

Udotea sp. 2.83±2.04 7.11±5.15 14.84±2.75 25.61±17.72

Total average 2.19±5.55 6.88±4.34 18.37±6.02 21.95±16.16

Rhodophyceae

G. corneum 0.52±0.56 7.46±3.15 27.37±14.18 19.64±4.43

G. verrucosa 0.39±0.59 7.60±5.30 21.27±9.29 20.57±16.26

R. ardissonei 3.89 13.14 41.60 38.87

Total average 0.72±6.47 7.96±4.49 25.65±6.44 21.55±13.81

Phaeophyceae

C. spinosa 0.50±0.85 6.56±2.32 21.27±4.09 18.01±8.47

D. dichotoma 1.95±0.05 7.35±1.55 40.90±5.10 19.00±2.70

S. acinarium 1.57±2.22 6.73±2.66 45.27±29.99 9.10±4.86

S. hornschuchii 1.70±0.80 8.05±3.15 27.35±7.65 29.35±1.75

S. vulgare 1.10±1.91 7.30±3.55 32.33±17.14 24.55±15.13

Total average 1.11±5.83 7.04±4.23 30.76±11.92 19.87±10.69

620 J Appl Phycol (2012) 24:613–626

against the development of cancer (Omenn et al. 1996;Woodall et al. 1996).

Iodine is one of the most important elements provided byseaweeds (Drum 2008). Compared to terrestrial plants andanimals that contain only trace amounts of iodine (1 ppm),these marine plants generally have high concentrations of

this nutrient (500–8,000 ppm; IGoNutrition 2008).Furthermore, seaweed concentrations are 100–1,000 timeshigher than in fish (maximum amount 2.5 ppm; Science andTechnology Agency Japan 2001). However, iodine fromfish must be limited because of mercury problems(IgoNutrition 2008). The highest iodine content is found in

Table 8 The concentrations of the trace metals [Cu, Ni, Pb and Zn (in µg g−1 dry wt.)] in the present study, previous studies and in higher plantsand whole food

Trace metals Present study Previous studies Higher plants Permissible doses

Copper 0.00–3.89 2.00–13.90 (El-Sarraf 1995) Spinach (0.00) <12,000 ppm for male

2.35–3.65 (Krentz 2004) Cheddar cheese (0.00) <10,000 ppm for female (Public ServiceSeries of International CopperAssociation 2009)

4.66–6.14 (Mohamed and Khaled 2005) Peanuts (10, McCanceet al. 1993)4–53 (Masoud et al. 2006)

2–251 (Santoso et al. 2006)

2.10–3.40 (Abdallah 2008)

0.39–1.51 (Devi et al. 2009)

1.70–17.10 (Tuzen et al. 2009)

Zinc 9–38.87 11.30–340.70 (El-Sarraf 1995) Spinach (7) 70 μg day−1 for male

8.30–24.30 (Krentz 2004) Cheddar cheese (23) 130 μg day−1 for female (Ratana-arpornand Chirapart 2006)7.96–74.82 (Mohamed and Khaled 2005) Peanuts (35, McCance

et al. 1993)15–861 (Masoud et al. 2006)

3–227 (Santoso et al. 2006)

17.80–31.90 (Abdallah 2008)

0.74–4.23 (Devi et al. 2009)

3.64–64.8 (Tuzen et al. 2009)

Lead 13.14–45.27 4.31–30.4 (El-Sarraf 1995)9.41–53.31 (Mohamed and Khaled 2005)

Nickel 4.98–13.14 7.23–28.19 (Mohamed and Khaled 2005)8–44 (Masoud et al. 2006)

0.05–0.503 (Devi et al. 2009)

2.60 (Nilka de Oliveira et al. 2009)

Table 9 The correlation coeffi-cient between the physico-chemical parameters and naturalcomponents, pigments content,minerals and trace elementsmeasured in the study areaduring 2006

r is significant if r>0.28. p≤0.05, n045 for all parameters,except for water temperature,salinity and depth (n050)

Depth Temp. S (‰) pH DO NH4 NO2 NO3 PO4 SiO4

TCH −0.14 0.38* −0.07 0.20 0.10 −0.13 0.27 −0.06 0.11 0.13

TPr −0.18 0.05 −0.13 0.37* 0.11 −0.13 0.40* 0.01 0.35* 0.16

TL −0.28 0.08 −0.27 0.04 0.33* −0.30* 0.35* 0.16 0.21 0.30*

Chl.a −0.09 0.04 −0.06 −0.13 0.06 −0.12 −0.02 0.00 −0.13 0.12

β-Carotene −0.36* 0.12 −0.20 0.05 0.34* −0.38* 0.40* 0.03 0.07* 0.31*

Iodine −0.68* −0.02 −0.81* −0.29* 0.78* −0.82* 0.54* 0.68* 0.50* 0.88*

P −0.03 0.01 0.00 −0.16 0.05 −0.04 −0.07 0.04 −0.09 −0.03

Na −0.29* 0.22 −0.29* −0.27 0.22 −0.31* 0.03 0.29* 0.10 0.26

K 0.31* −0.06 0.25 −0.05 −0.16 0.32* −0.24 −0.14 −0.20 −0.33*

Ca −0.16 0.06 −0.18 −0.01 0.18 −0.20 0.17 0.08 0.06 0.25

Cu 0.17 0.48* 0.14 0.03 −0.18 0.33* −0.20 −0.17 −0.18 −0.31*

Ni 0.66* −0.51* 0.56* −0.04 −0.56* 0.64* −0.61* −0.49* −0.65* −0.50*

Pb 0.08 0.13 −0.04 −0.14 0.20 0.05 0.01 0.06 −0.08 0.03

Zn 0.35* −0.10 0.43* −0.08 −0.45* 0.37* −0.47* −0.38* −0.52* −0.38*

J Appl Phycol (2012) 24:613–626 621

brown algae, with dry kelp (Laminaria) ranging from 1,500to 8,000 ppm d.w., Fucus (500–1,000 ppm), Sargassumfusiformis (628 ppm) and Undaria (400 ppm). In mostinstances, red and green algae have lower contents, about100–300 ppm (Madhusudan et al. 2011). However, ourresults showed the same distribution pattern of iodine con-tent in the three phyla but lower than those in commonedible seaweeds, but much higher than terrestrial plants,animals and fish. The World Health Organization (WHO)recommends the daily intake of iodine as 150 μg for ado-lescents/adults and 250 μg for pregnant/lactating women

(Centre for Food Safety, Food and Environmental HygieneDepartment and the Department of Health 2011). Thus,eating 1 g of dried, unrinsed brown algae or 3–5 g of redor green algae will provide the recommended dietary intakeof 100–150 μg day−1 (Drum 2008; Madhusudan et al.2011).

Phosphorus, calcium, sodium and potassium are amongthe minerals which are present in significant amounts inmarine algae (Nisizawa 2006). The highest P content wasrecorded in the green alga C. bursa, whereas the maximumvalue of Ca was in U. petiolata, a calcareous species, which

Sim

ilari

ty

C. burs

a

S. vulga

re

C. spin

osa

G. ver

ruco

sa

G. cor

neum

S. hor

nschuch

ii

D. dich

otom

a

S. acin

ariu

m

U dotea

sp.

U. peti

olata

R. ard

isson

ei

H. tuna

C. rac

emos

a

C. pro

lifer

a

43.97

62.64

81.32

100.00

Dendrogram with Single Linkage and Euclidean DistanceFig. 3 Cluster analysis of algalspecies based on naturalcomponents, pigments,minerals and trace elementscontent during 2006

Sim

ilari

ty

St VSt ISt IIST IIISt IVSt VISt VII

58.20

72.13

86.07

100.00

Dendrogram with Single Linkage and Euclidean DistanceFig. 2 Cluster analysis ofspatial variations of naturalcomponents, pigments content,minerals and trace elements inthe algal species during 2006

622 J Appl Phycol (2012) 24:613–626

concentrates large amounts of CaCO3 within its thallus(Steneck 1986). Chemical composition and nutrient contentvary with seaweed species, habitat, maturity and environ-mental conditions (Ito and Hori 1989) as well as with thevarious phases of algal growth (Devi et al. 2009). As a resultvariable distribution patterns are displayed in the three phy-la. In the present study, physico-chemical parameters werenot correlated with either phosphorus or calcium content.Ratana-arporn and Chirapart (2006) mentioned that dietaryintake of phosphorus is about 700 mg day−1 and calcium800 mg day−1 for both male and females. Compared withedible seaweeds in previous studies, vegetables and somecommon foods, the two elements in this study exceed theconcentrations reported by others, except Murata andNakazoe (2001).

On the other hand, intakes of high Na/K ratios have beencorrelated to a higher incidence of hypertension. Seaweedscan therefore help balance high Na/K ratio diets. Rupérez(2002), Santoso et al. (2006), Abdallah (2008) andMatanjun et al. (2009) reported low Na/K ratios. However,in the present study, the ratio is higher than in the previousones, but still in the range of many common foods.

The trace elements Cu and Zn are essential for growth butin very low concentrations (Round 1973), and it has beenreported that Zn is required for the metabolic activity of 300of the body’s enzymes, and is essential for cell division,synthesis of DNA and protein (Bhowmik et al. 2010).Copper is crucial for the normal formation of the brain,nervous system, bone development and for the maintenanceof a healthy immune system (Allen and Klevay 1994). TheCu concentrations in the present study are acceptable withrespect to the common foods and previous studies.According to the estimate of intake of seaweeds in Japan,the daily average consumption is 2–3 g d.w. of brown algaewith a maximum daily average consumption of 12 g(Sakurai et al. 1997; Almela et al. 2006). The PublicService Series of International Copper Association (2009)mentions that dietary intake of copper should not exceed12,000 ppm for males and10,000 ppm for females. If oneassumes a mean consumption of 3 gday−1, seaweeds of thepresent study would contribute Cu up to 11.67 ppm of therecommended daily average allowance, which is a very lowpercentage 0.1% of the total dietary intake (TDI). Theycould contribute Zn between 27 and 116.6 ppm, which is20.7–89.7% of the TDI for males but exceeds that forfemales. Therefore, the high contribution of Zn in someseaweeds must be taken into account regarding seaweedconsumption as food.

In terms of legislation, the concentration of Pb in theseaweeds of the present study far exceeded the values estab-lished in legislation by France (≤5 ppm) and Spain (1 ppm,Real Decreto 1978, 2420/78; Almela et al. 2006), limitingtheir use in food consumption. The seaweeds in the present

study would contribute between 40.20 and 135.80 ppm tothe daily average consumption, which is 16.08 to 54.32% ofthe TDI recommended by the WHO for an adult weighing70 kg (250 μg day−1; WHO 1993). This contribution of Pbthrough consumption of a single product can be consideredvery high (Almela et al. 2006), and in the case of extremeconsumers, it would substantially increase the Pb dietaryintakes recommended by some countries, which vary be-tween 17 and 131% of the TDI (Nasreddine and Parent-Massin 2002) and which vary between 64.32 and 217.30%in this study.

With respect to the previous studies on edible seaweeds,the concentration of Ni is markedly higher and restricts theusage of these seaweeds in food consumption (Devi et al.2009; Nilka de Oliveira et al. 2009). However, manycountries have established specific regulations for toxicelements in edible seaweed (Mabeau and Fleurence 1993;ANZFA 1997), and the Commission Regulation (EC) No.466/2001 for European Communities (Commission of theEuropean Communities 2001) has set maximum levels forcertain contaminants in foodstuffs, although nickel was notincluded. The high levels of some heavy metals in the algareflect firstly the high concentration of the metals in thestudy area and secondly the capacity of the alga to takethem up (Karez et al. 1994). Many factors may influencethe uptake of metals in algae such as the physico-chemicalparameters (Karez et al. 1994), as well as the stage ofdevelopment and variation in growth and chemical compo-sition of the algae, which may influence the pattern of theaccumulation (Ho 1990; Carlson and Erlandsson 1991).

The cluster analysis of spatial variations of natural com-ponents, minerals and trace elements in the algal species inthe present study reflects the ecological conditions at thestations, whereas El Dabaa (St. V) represents an indepen-dent cluster group as it is not subjected to human activities.The other two clusters grouped the stations that were almostsimilar in the ecological conditions. On the other hand, thesimilarity index between the species reflected their conver-gence, based on contents of these components. The highestsimilarity index (S095%) was found between the two greenalgae of similar origin C. prolifera and C. racemosa, fol-lowed by similarity index (S090%) between the calcareousalgae H. tuna, R. ardissonei and U. petiolata, whereas thelowest includes the green alga C. bursa (S043%).

In conclusion, the seaweeds in this study varied betweenspecies and spatially and were shown to have a high mineralcontent as well as being interesting potential sources ofprotein, carbohydrates, lipids and pigments, especiallyChl.a. Specifically, minerals are abundant in seaweeds com-pared to common food and vegetables. However, the mea-sured trace metals exceeded the permissible levels and arefar from the accepted concentrations established in the reg-ulations of many countries. This limits their use in food

J Appl Phycol (2012) 24:613–626 623

consumption, except for Cu which is one micronutrientwhich recorded acceptable concentrations throughout theentire study. In conclusion, this study can be considered asa preliminary investigation of natural products in someEgyptian seaweeds. It should encourage the governmentto select suitable species for cultivation and to focus onthis new trend in our country to eliminate the negativefactors encountered in wild species. As a variablesource of protein and containing a wide variety ofbeneficial nutritional compounds, macroalgae must notbe overlooked. Further studies including other functionalproducts need to be carried out on Egyptian seaweeds,especially as many of them are still underexploited eventhough they are highly diversified.

Acknowledgments We are greatly indebted to Dr. Ibraim AminMaiyza, Marine Environment Department, National Institute of Ocean-ography and Fisheries, Alexandria, Egypt, who helped us and suppliedus with physical parameter data in this work. This study was part of theresearch plan of National Institute of Oceanography and Fisheries,Alexandria entitled “Development of the pelagic and the demersal fishand invertebrates along the Egyptian coast between Alexandria andSalloum in relation to the prevailing environmental conditions”.

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