© 2014 isproms ISSN 1994-5108 Vol.6 :1 Accumulation of heavy metals by macroalgae along atlatic coast of Morocco|| Mouradi et al.
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World Journal of Biological Research 006: 1
World Journal of Biological Research
Revue Mondiale de la Recherche Biologique
published 30 june 2014
Accumulation of heavy metals by macroalgae along the
Atlantic coast of Morocco between El Jadida and
Essaouira
Aziza Mouradi1*, Laila Bennasser1, Vincent Gloaguen2, Ahlam Mouradi1, Hakima Zidane3 &
Thierry Givernaud4
1- LBBM, Laboratoire de Biologie et Biotechnologies Marines, Université Ibn Tofail, BP. 133. 14000-Kenitra, Maroc
2- LCSN, Laboratoire de Chimie des Substances Naturelles. Université de Limoges, France
3- Institut National de la recherche halieutique, 2 rue Tiznit, 20000-Casablanca, Maroc
4- STECOF, 5, Lot. Johara, 14000-Kénitra, Maroc
Abstract
The diversity of anthropic activities generates many effluent containing different pollutants (metals, pesticides) which are
responsible of the hydro system quality degradation. Contrary to organics compounds, the metallic species tend to persist
indefinitely, accumulating in living tissues through the food chains. On the seashore ultimate receptacle of micropollution, the
benthic seaweeds are the ideal target for micro pollution, thanks to their capacity to bind and to accumulate the metallic
cations. The present study relate to:
- The analysis of specific wealth seaweed on the coast between two cities of El Jadida and Essaouira and the impact of
pollution on the seaweed’s diversity.
- The assessment of metallic concentration in seaweed thalli and comparison of their affinities toward some metallic
elements.
- The selection of seaweed species which can accumulate a specific metallic element or more.
The results obtained showed that the micropollution has consequences on the diversity of seaweed; it generates quantitative
and qualitative modification of seaweed flora. The tested seaweed contains high metallic concentrations which vary
according to the element and seaweed specie. These difference affinities of seaweeds can be assigned to nature of the
parietal polysaccharides and their proportion of sulphate and carboxyl groups which are involved in ionic exchange and
metal sequestration. Some seaweed species have a high capacity to accumulate metallic elements in natural environment.
For this reason some species may be used for an effluent treatment process.
Keywords: Pollution, metals, macroalgae, diversity, accumulation, purification.
* Corresponding author:
Phone : +212 6 61 30 21 41
Fax: +212 5 37 32 94 33
E-Mail: mouradi14@gmail.com
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© 2014 isproms ISSN 1994-5108 Vol.6 :1 Accumulation of heavy metals by macroalgae along atlatic coast of Morocco|| Mouradi et al.
Introduction
Despite to the fundamental role of macroalgae in
maintaining the ecological balance of the marine
environment and the economic interest as the basis of a
diverse industry affecting many sectors (Radmer (1996),
Bixler (1996), Carlsson, Beilen, Möller, Clayton (2007)),
for a long time, they have remained absent from the
debate on biodiversity. Benthic macroalgae may indeed
be reliable tools for monitoring biodiversity on the coast
(Northon, Melkonian, Andersen (1996)). Moreover, the
particular structure of their cell walls gives them the
ability to bind and accumulate micropollutants present in
their aquatic environment, reflecting the impact of
anthropogenic disturbance and they can be good
indicators of micropollution (Levine (1984); Vasquez,
Guerra (1996); Sekabira, Oryem Origa, Basamba,
Mutumba, Kakudidi (2011); Gopinath, Muraleedharan,
Chandramohanakumar, Jayalakshmi (2011)). Some
species can be also good candidates for the treatment of
wastewater in controlled environments.
This work is part of a project of macroalgae cartography
on the Moroccan Atlantic coast between the cities of El
Jadida and Essaouira (Givernaud et al. (2005)):
* Study the macroalgal diversity.
* Measure of the levels of eight metal elements
(Cr, Pb, Cu, Zn, Mn, Fe, Ni and Co) in the thalli
of some species of macroalgae described as
bioaccumulative.
* Comparison of the affinities of different species
for metallic elements.
* Selection of species of macroalgae according
to their retention capacity for one or more
metals for specific use in the treatment of
effluents.
Materials and Methods
1.
Studied Area
It is located on the Atlantic coast of Morocco between the
cities of El Jadida and Essaouira on a part (Figure 1).
The area is characterized by a succession of rocky
shores and sandy beaches.
The main sources of pollution are:
- Urban sewage: Azzemour, El Jadida, Safi and
Essaouira who have no water treatment plant.
- The two phosphate chemical complex (OCP) of
Jorf lasfar (20km south of El Jadida) and Safi
(5km south of Safi)
2.
Sampling sites
36 sites between 31°5 an 33°3 of north latitudes have
been sampled (Figure 1). They were grouped by area.
Area A: from El Jadida to Sidi Bouzid (Site 1 to 12).
Area B: Sidi Bouzid to Jorf Lasfar chemical complex
(Site13 to 23).
Area C: South of Jorf Lasfar to Sidi Moussa (Site 24 to
Site 28).
Area D: Safi to Essaouira (Site 29 to Site 36).
3. Sampling
Samplings were performed between May and September
2004. Seaweeds were collected at low tide in medio
littoral area.
4. Identification of species
Macroalgae are brought to the laboratory where species
are identified using different keys (Gayral (1958); Irvine,
Chamberlain (1994)) and the taxonomy was confirmed
using algaebase website.
5. Assessment of metal concentrations
 Digestion: The Thalli are rinsed quickly with
deionized water, dried and then ground to
powder. The mineralization is achieved
according to Hoenig and Vandrestappen (1978)
by digestion sulfo-nitric-peroxide (1-3-3) ml / g
of algal powder for 12 minutes at 200 ° C.
 Dosage: Eight metal elements namely iron,
copper, Nickel, Lead, Zinc, Chromium, Cobalt
and manganese were determined by atomic
absorption (Varian AA). Atomization is carried
out with flame (air / acetylene).
Results and Discussions
Forty different macro algae species have been identified
on the 36 points sampled. The composition of the
macroflora (Figure 2) showed quite important diversity
with the three taxonomic groups present in different
proportions: the Chlorophyceae representing only 12.5%
with 5 species, the Phaeophyceae represent 25% with 10
species, the red algae represent 62.5% with 25 species.
These proportions are quite similar to those obtained by
Benhissoune, Boudouresque,
Verlaque (2001);
Benhissoune, Boudouresque, Verlaque, (2002a);
Benhissoune, Boudouresque, Bouderesque and
Verlaque (2002b); Benhissoune, Boudouresque,
Bouderesque, Verlaque (2003). However, the frequency
(number of sites where the species are found on the total
number of sites) is highly variable from one species to
another and between species of the same taxonomic
group.
Eighteen species (45% of those identified) are harvested
at least 10 times, 8 species (20% of species) are
harvested more than 2 times in one of the sites, 14
species (35% are harvested 3 to 9 times) (Table 1).
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© 2014 isproms ISSN 1994-5108 Vol.6 :1 Accumulation of heavy metals by macroalgae along atlatic coast of Morocco|| Mouradi et al.
Table I. Inventory and spatial frequency of macroalgal species in the studied area.
Groupe
Chlorophyceae
Pheophyceae
Rhodophyceae
Genre
Occurrence
rate
22/36
20/36
10/36
6/36
2/36
12/36
12/36
14/36
15/36
8/36
6/36
9/36
2/36
4/36
1/36
14/36
10/36
16/36
16/36
16/36
18/36
16/36
14/36
18/36
14/36
9/36
9/36
8/36
1/36
2/36
3/36
1/36
8/36
10/36
Espèce
Ulva
Ulva
Cladophora
Codium
Enteromorpha
Laminaria
Bifurcaria
Fucus
Fucus
cystoseira
cystoseira
cystoseira
cystoseira
Saragasum
Colpomenia
Gracilariopsis
Gracilariopsis
Gracilaria
Gracilaria
Gracilaria
Gracilaria
Gracilaria
Gracilaria
Gelidium
Gelidium
Gelidium
Gymnocongrus
Gymnocongrus
Catenella
Plocamium
Pterosiphonia
Pterosiphonia
Gigartina
Gigartina =
Chondracanthus
Rodymenia
Porphyra
Bornetia
Palmaria
Pterocladiella
Hypnea
lactuca
sp
rupestris
elangatum
intestinalis
ochroleuca
bifurcata
spiralis
vesiculosus
humilis
compressa
tamariscifolia
baccta
vulgare
sp
longissima
musciformis
gracilis (rouge)
Gracilis (verte)
conferta
multipartita
vermiculophylla
dura
sesquipedale
spinosum
reptans
patens
griffithsiae
repens
cartilagineum
complanata
pennata
pistillata
acicularis
palmata
umbilicalis
secundiflora
palmata
capillacea
musciformis
2/36
6/36
5/36
2/36
6/36
4/36
Aera
A
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
Aera
B
+
+
+
+
+
+
+
+
+
Aera
C
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
Aera
D
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
Table II. Natural levels of heavy metals in water (ppm) (Wedepohl, 1991)
Metal contents
Cr
Zn
Cu
Pb
Cd
Hg
Sea water
River water
0,2
1,0
0,6
7,0
0,25
2,00
0,003
0,300
0,1
0,02
0,002
0,07
The results of the spatial analysis of macroalgae on this
stretch of coast also show quantitative and qualitative
changes in species richness from one area to another.
The structural elements of biotic ecosystems are often
considered as the most sensitive indicators of
perturbations. Indeed, permanent or chronic low levels of
contaminants often lead to significant effects on animal
communities (Tahiri, Bennasser, Idrissi, Fekhaoui, El
Abidi, Mouradi (2005)) and plants in aquatic
environments (Eisler (1981); Gaudry et al. (2001);
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© 2014 isproms ISSN 1994-5108 Vol.6 :1 Accumulation of heavy metals by macroalgae along atlatic coast of Morocco|| Mouradi et al.
Gaudry et al. (2007); Sanz-L´azaro, Malea, Apostolaki,
Kalantzi. Marin, Karakassis (2012)). All species of
macroalgae did not have the same nutritional and
environmental
requirements
(substrate
type,
temperature, light, hydrodynamic, nutrients) or the same
degree of sensitivity and tolerance to pollutants (metals,
organic residues, pesticides,…). However, the spatial
distribution of algal species is not uniform along this
stretch; it seems to be influenced by several factors,
among others the degree of pollution at the sites,
because species diversity decreases remarkably in
polluted areas (Figure 3); this is how:
* Area B which has the largest number of species (31), is
considered as the least polluted, It’s far from any human
activity.
* Area A, although subject to urban discharges of El
Jadida and the pollution from the Oum Erbia River, 23
species have been identified, with species of Ulva, Fucus
and Gelidium. It should be noted that areas A and B are
known for their high productivity, they are characterized
by the trade winds that maintain water upwelling system
(Roy, 1991). This may be the cause of the abundance of
some
macroalgae.
Figure 1. Geographical location of sampling sites.
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© 2014 isproms ISSN 1994-5108 Vol.6 :1 Accumulation of heavy metals by macroalgae along atlatic coast of Morocco|| Mouradi et al.
* Area C shows a low number of species (13 species)
probably due to the impact of the sewage of Jorf Lasfar
chemical complex that are discharged directly into the
sea and spread along the coast to the south with the
marine currents.
* Area D is subjected to the same effect as Area C, due
to urban discharges from the city of Safi and industrial
waste of the Phosphate chemical industry. However, the
water quality is improving gradually to the south of Safi,
resulting in a significant increase in species richness that
reaches 25 species in north of Essaouira city.
Among the species recorded, it was noticed also
qualitative changes in species richness of macroalgae
which is characterized by the existence of:
* Species sensitive to pollution, encountered only in
unpolluted areas: Rodymenia, Catenella, Pterosiphonia
and Palmaria.
* Species tolerant to pollution and changes in the quality
of the aquatic environment, they have a wide spatial
distribution and are found in several sites, these belong
to the genera Ulva, Fucus, Gracilaria and Geliduim.
* Species resistant to pollution, which appear and
proliferate in polluted areas; they may be good indicators
of pollution such as genera Gymnogongrus, Gigartina
and Cladophora.
1
2
6
Chlorophyceae
Pheophyceae
Rhodophyceae
Figure 2. Algal composition of macroflora on the Atlantic coast of Morocco.
Number of species
35
30
25
20
15
10
5
0
Area I
Area II
Area III
Area IV
Figure 3. Spatial distribution (number of species).
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© 2014 isproms ISSN 1994-5108 Vol.6 :1 Accumulation of heavy metals by macroalgae along atlatic coast of Morocco|| Mouradi et al.
PPM
200
160
120
80
40
0
Lead
Chromium
Figure 4a. Levels (µg.g-1) chromium, lead, iron and manganese in the different species of macroalgae.
Many researchers were interested in studying the use of
the ability of seaweeds to bind and accumulate metals
(Vasquez, Guerra (1996)), sometimes without their being
metabolized to eliminate pollutants (Kratochvil, Pimentel,
Volesky (1998)). Being Benthic, they can be considered
as good indicators of micropollution in the wild (Weis,
Skurnick, Weis (2004)). They can also be tested in the
treatment of decontamination of metal-rich waters in a
controlled environment as is the case of the
pheophyceae Sargassum sp. on the Brazilian coast
(Cossich, Tavares, Ravagnani Kakuta (2002)).
The second part of the study consists in the evaluation of
metal concentrations in the thalli of 10 species selected
as the most frequent and some of them are already
known for their retention performance for metals. The
results reported in Figures 4a and 4b showed significant
bioaccumulation of metallic elements in all species at
varying rates depending on the species and on the
nature of the metal. Comparison of the value recorded
with those naturally found in surface waters (sea and
river) are reported in Table 2 (Wedepohl, 1991), they can
confirm the accumulation of metals by these organisms in
natural environments. Variability of the affinity is
expressed for a metallic component by the difference of
its content in selected species and for the same species
by the different levels of metal elements studied. These
differences in affinity may be related to variable behavior
of species to metals, involving different mechanisms of
accumulation of these elements. The cell wall
polysaccharides of seaweed are often identified as the
cause of the phenomenon of sorption (Gloaguen, Morvan
(1997); Gaballah, Goy, Allain, Kilbertus, Thauront (1997);
Salehizadeh, Shojaosadati (2003)). However, variations
between species affinity for the same element can be
explained by the diversity of nature and proportions of the
chemical constituents of the cell wall from one species to
another. The carboxyl groups of alginate and the sulfate
groups of agars and carrageenans are responsible for ion
exchange of cell wall polysaccharides and are the main
sites of capture and sequestration of metal components
(Leonardi, Vasquez (1999)). These acid groups, whose
availability depends on the pH, generate negatively
charged polyelectrolytes, leading to ionic or electrostatic
interactions between the surface and the metal elements,
the majority of which are cations (Crist, Martin, Guptill,
Eslinger (1990); Andrade et al. (2010); Conti et al.
(2010)). Other authors (Kloareg, Demarty, Mabeau,
(1987)) showed that sulfate groups rather played a role in
the regulation of ion exchanges between the external
environment and the cell during stress due to salinity and
their presence in seaweed is correlated to their position
on the foreshore. The differences in affinity of the same
species to different metallic elements are probably
related to their physical and chemical properties, their
speciations and competitions between the elements
(Guilizzoni (1991)).
To identify the best accumulating species, we have
established for each of the elements studied, the
classification of species of macroalgae (in decreasing
order of affinity):
Copper: Gra > Ulv > Gig > Gym > Cla > Cys > Gel
> Lam > Fuc > Bif
Cobalt: Gra > Fuc > Ulv > Gym > Gel > Lam > Cys
> Cla > Gig > Bif
Zinc: Gig > Ulv > Gra > Gym > Cla > Cys > Fuc >
Bif > Gel > Lam
Nickel: Gra > Gig > Ulv > Gym > Gel > Fuc > Cys >
Cla > Lam > Bif
Lead: Gra > Ulv > Fuc > Gym > Gel > Lam > Gig >
Cla > Cys > Bif
Chrome: Ulv > Gym > Cys > Gra > Cla > Fuc > Gig
> Lam > Bif > Gel
Iron: Gym > Ulv > Gra > Gel > Cla > Gig > Fuc > Bif
> Lam > Cys
Manganese: Gra > Gym > Gel > Ulv > Fuc > Lam >
Cla > Cys > Gig > Bif
NB Gracilaria (Gra.), Ulva (Ulv.), Gigartina (Gig.),
Gymnocongrus (Gym.), Cladiphora (Cla.), Cystiseira
(Cys.), Gelidium (Gel.), Laminaria (Lam.), Fucus (Fuc.),
Bifurcaria (Bif.).
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© 2014 isproms ISSN 1994-5108 Vol.6 :1 Accumulation of heavy metals by macroalgae along atlatic coast of Morocco|| Mouradi et al.
PPM
1000
900
800
700
600
500
400
300
200
100
0
Iron
PPM
Coppe
r
70
60
50
40
30
20
10
0
PPM
100
80
60
40
20
0
Nicke
l
Figure 4b. Levels (mg.g-1) of copper, nickel, zinc and cobalt in the different species of macroalgae.
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© 2014 isproms ISSN 1994-5108 Vol.6 :1 Accumulation of heavy metals by macroalgae along atlatic coast of Morocco|| Mouradi et al.
On the other hand, comparison of total contents of the
eight metal elements accumulated by each species
allowed us to retain in decreasing order of retention
capacity, 5 species of macroalgae:
Gracilaria > Ulva > Gymnogongrus > Gigartina >
Fucus
It should be underlined that after this study, the species
selected as performers in terms of retention of metals are
characterized by parietal polysaccharide substituded by
sulfate or carboxylic acid groups. That is how the genus
Gracilaria, agarophyte (agar: sulfated polysaccharide)
has been able to accumulate higher levels of copper,
nickel, lead, cobalt and manganese, followed by Ulva,
Ulvaceae
(ulvan:
sulfated and
carboxylated
polysaccharide) securing more chromium, followed by
Gymnogongrus, (carrageenan: sulfated polysaccharide)
showing a preference for iron. As for zinc, the most
important levels are observed in the genus Gigartina,
carageenophyte (carrageenan: sulfated polysaccharide).
Fucus (alginate: carboxylated polysaccharide), showed
no preference between the different metals. The nature
and content of polysaccharide sulfate or carboxyl groups
and the type of bond that develops between these groups
and the metal cations appear to be the selection criteria
fixing species of metals.
Conclusion
Performances of certain species of macroalgae are not
limited to the removal of nutrients in the waters of farms,
but also in the retention of metallic elements generated
by human activity. A high accumulation rates and
variable in nature depending on their affinity for metals,
some species such as Gracilaria, Ulva, Fucus
Gymnocongrus Gigartina and have shown great
performance in terms of retention of pollutants. However,
it would be interesting to test in controlled conditions the
maximum accumulation of a given element in each of
these species, so, these macroalgae find their potential
application in the specific treatment of industrial
wastewater rich in metals, and can be a valorisation of
the by products of agar industry.
Acknowledgements
We thank the French cooperation, CNRST, society
Setexam and UNESCO for their collaboration.
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