Volume 1, N°1 , pp : 26 - 36 (2018) ISSN : 2605-6208

Ecotoxicological diagnostic and marine pollution of Marchica lagoon (Nador, Morocco): aerea as bio-indicator species of water quality Asmae Aknaf1*, Mustapha Akodad1, Mourad Baghour1 and Brahim Oudra2 1Observatoire de la lagune de Marchica de Nador et Région Limitrophes (Labo. OLMAN-RL), Faculté Pluridisciplinaire de Nador, Université Mohamed Premier, BP 300, 62700, Selouane, Nador, Maroc, 2Laboratoire de Biologie et Biotechnologie des Microorganismes (LBBM), Département de Biologie, Faculté des Sciences-Semlalia .BP 2390.Marrakech *Email of corresponding author:[email protected]

Received : 11November 2017 Accepted : 15 Junuary 2018

Abstract espèce bioindicatrice de la pollution marine, Chaetomorpha aerea(Dillwyn) Kützing, souvent utilisée pour vérifier la qualité (Chlorophycée), is considered as bio- chimique de l’eau. A cet égard, un suivi de indicatrice specie of the marine pollution, Chaetomorpha aereaa été réalisé au niveau usually used for the chemical quality de 2 sites dans la lagune de Nador durant les verification of water. Here, following of 4 saisons du octobre 2014 à juillet 2015. Le Chaetomorpha aerea realized in the two premier site "Kariat-Arekman" est considéré sites of Nador’s lagoon in the following comme hautement polluée en raison de period between October 2014 and july 2015, l’effet de l’écoulement des rejets des eaux covering the four seasons. The first site usées ainsi que c’est une zone confinés. Le "Kariat-Arekman", is considered highest seconde "Beni-Ensar"est considérée polluted by the reason of its location in commesite témoin, moins pollué. Les confined area, and undergoing the effect at paramètres physico-chimiques de l’eau the disposed waste water. The second site (T°C, pH, CE, O2 dissous, NO3 et PO4) et “Beni-Ensar” is considered at the witness les paramètres biochimiques des algues station because its almost free of pollution (Chlorophylles totales, protéines, glucides sources. The physical-chemical parameters totales et la proline), ont été mesurés sur of water (T°C, pH, salinity, Dissolved l’ensemble des échantillons. Les résultats oxygen, NO3 and PO4) and biochemical recueillis montrent les différences parameters of algae (Chaetomorpha aerea) remarquables pour tous ces paramètres were measured in the gathering of samples. physico-chimiques de l’eau et éco- The obtained results showed the noted of the physiologiques de Chaetomorpha aerea. differences for the whole physico-chemical Aussi, il a été constaté une amélioration de parameter of water and ecophysiological of la qualité de l’eau du site de Beni-Ensar, Chaetomorpha aerea. cette amélioration est liée essentiellement au In addition it found a quality of récent aménagement qu’a connu la lagune improvement water of Beni-Ensar site, this Marchica avec l’ouverture de la nouvelle improvement is realized essentially to the passe, et que Chaetomorpha aerea pourrait recent amenagment that was found in être utilisée dans phytoremédiation en raison Marchica’s lagoon with the opening the new de la haute synthèse de proline qui leur pass and that Chaetomorpha aerea could be confère beaucoup résistant aux polluants. used in phytoremediation bythe reason of the high synthesis of the proline, which Mots clés : Chaetomorpha aerea, confer their resistance against the pollutants. Bioindicateur, paramètres physico- chimique, Paramètres biochimiques, Key words: Chaetomorpha aerea, Pollution, Lagune de Nador. Bioindicator, Physico-chemical parameters, Biochemical parameters, Pollution, Nador Introduction lagoon. The lagoons are original ecosystems that belonge to both the marine and the Résumé continental domain, it contains complex Chaetomorpha aerea(Dillwyn) Kützing, spaces and subject to the increasing (Chlorophycée), est considéré comme demographic, the economic and the

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Aknaf et al. ISSN : 2605-6208 ecological growing more and more, by the sector), of mountains and of course an reason of their role as shelters and their expanding urban environment (the city of strong fishery resources [1]. These pressures Nador, Beni-Ensar and Kariat- threaten seriously the natural resources. Arekman).Due to its biological and Various human’s activities (industry, ecological importance Nador’s lagoon is agriculture, urbanization, tourism…) classified as site of biological and ecological contribute to the contamination of water and interest [17] and since 2005 it has been sediments in these areas and the living declared a Ramsar site [18]. organisms is the area [2]. After release into The first objective sated by this work, to the aquatic environment, organic and evaluate it eutrophication status, by inorganic pollutants may remain in water in selecting two study stations, placed at both dissolved form or be removed from the extremities of the lagoon. By studying the water column by sedimentation and physicochemical parameters of water during absorbed to the organic matter present in the the four seasons..And then, in a second step, sediment [3]. These pollutants are absorbed an estimate of the contamination status of by the algae and bio-assimilated by the the site will be monitored through the different species of benthic macrofauna [4], evaluation and study the biochemical and which can be contributed to the origin of physiological parameters of Chaetomorpha aquatic organisms [5] and can be at the area bioindicator algae. origin of the disappearance of certain species, degrade water quality and threaten Materials and methods aquatic life [6], thus causing malfunctioning Measurement and sampling campaigns of the trophic network [7]. Measurement and sampling campaigns were However, algae have played an important conducted quarterly from October 2014 to role in maintaining aquatic environments: as July 2015, whether 4 measurement primary producers in the food chain, an campaigns in the two station (Fig.1), the important source of O2 in water and a first station that of Kariat-Arekman bioindicator of pollution. Consequently, (N35'06.4,96 /W002 '45 .0,28) is located to several red algae (Alsidium spSargassum the south-east of the Marchica lagoon and fluitans) [8,9], green (Ulva rigida, the second sampling station (N35 ° 14 '951 / , Caulerpa prolifera, W002 ° 55,404) to the north-west of the Enteromorpha intestinalis, Chaetomorpha Marchica lagoon (Figure 1). Each station Linium, Ulva fasciata and Ulva lactuca) position were fixed by GPS. In each station, [10–13] and brun (Ascophyllum nodosum, using a polyethylene bottle, the water Fucus vesiculosus) [14-16] are basically samples were taken at about 20cm of the top used to examine the state of an ecosystem of the water. The samples, kept at low heat given by certain metals (Pb, Zn, Fe and Cd, (T°< 4°C), and in the darkness (cooler), Mg, Zn, Cr). They are the ability to bio- were analyzed in the laboratory.Thus, accumulate metals. collections of Chaetomorpha aereawere Nador’s lagoon is located in the northeast of made as seasonal in the lagoon during the Morocco, is the largest Moroccan lagoon same period, due to the abundance of this and the second largest lagoon in North species throughout the harvest period. The Africa. It is part of the Moroccan biomass of Chaetomorpha was collected be Mediterranean wet complex with an area of dipping, the seaweeds have been cleared of 115 km2, its maximum depth of the order is their epiphytes and rinsed on station be the 8 meters at the center and which decreases water of the lagoon, then placed in plastic towards the shore; it’s width about 7,5Km. bags. At the laboratory, they are washed It’s separated from the sea by a dune cordon with distilled water, by the goal to analyze 25 km long, elongated parallel to the coast total chlorophyll in the same sampling day. in the direction north-west direction (Beni- For the other analyzes, the algae is stored in Ensar) South-East (Kariat-Arekman). It’s the refrigerator at -20°C until analyzed. connected to the sea by a recently built pass (2010) of 300m wide and 6 m deep, allowing by the play of the tides and the renewals of the intra-lagoon waters. It’s made up of long sandy beaches, of bird reserves, of agricultural plains (Bou-Areg

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Figure1: Morphometry of the Marchica lagoon (Nador) and location of prospecting station (Sampling of alga and water)

Physico-chimical analysis of water The temperature (T°C) and the salinity of water are measured using a typical conductivity meter 197, the Oxygen dissolved by an Oxymeter DO6+ and the turbidimeter to identify the turbidity of the Figure2: Filamentous Chaetomorpha water are measured in Situ. pictures a): in Situ view at the bottom of the The nutrient salts were analyzed by lagoon. b) Microscopic observation of the algal automated colorimetric methods nitrate filamentous thallus (x100) concentrations were determined by colorimetric analyzes after reduction of Several authors [20, 21], considered the Cadmium to nitrite. The phosphates were Chaetomorpha aereais synonymous with C. analyzed by reaction with ammonium linum (O. F. Müller) Kützing, are probably molybdate in medium acid followed by the forms of growth of the same taxon reduction with ascorbic acid, the [22].But the others are the opposite [23-27]. concentration is then determined at 885 nm The difference between the two taxons, C. wavelength; According to the method linium is a free wild living whereas C. area described by [19]. grows the substratum on a basal disc [28].Chaetomorpha aerea is reported by Biochemical analyzes of Chaetomorpha several studies in Africa, Africa [26]; South area: Africa [29]; Namibia [28]: Egypt [30], Chaetomorpha aerea (Dillwyn) Kützing, Tunis [31], Sud african [32], Libya [33] and alga is formed of unbranched filaments of a Morocco [34-36]. bright green and shiny, of variable length (up to 30 cm long) and 0.3 to 1 mm in Photosynthetic pigments content diameter. These filaments are made up of evaluation barrel-shaped articles visible to the naked The total chlorophyll content was estimated eye (or more easily with a magnifying by the method of Lichtenthaler et al. [37]. glass). The rigid aspect and the tangling of The fresh tissue mere placed in the test tubes the filaments give this alga the appearance with 100% methanol. Using a of tangled nylon threads, each filament spectrophotometer, the optical density of the consisting of a single queue of long pigment solution was recorded at 666nm cylindrical cells. By the naked eye, we can and 653nm to determine total chlorophyll distinguish the partitions segmenting the content. filament. Under the microscope, the transverse partitions separating them are clearly visible (Figure 2).

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Proline and glucose content Ensar. The low values were recorded at the Proline and glucose contents were Beni-Ensar station, which can be explained determined by spectrophotometer according by the circulation of intralagunal water at to the method described in Irigoyen and al. this station, contrary to the Kariat-Arekman [38]. 0,5 g of algal samples were station. homogenized in ethanol (95%) grind everything carefully, then washed twice Salinity with 5ml of ethanol (70%). The salinity of the surface waters shows The mixture was centrifuged at 550 rpm for maximum levels of 39.5g / l during the 10min at 4°C. The supernatant was used to summer season at the Kariat-Arekman measure sugars and proline [38]. station (Tab1). The same results were found One milliliter of the alcoholic extract was by El Madani [40], Zerrouqui et al. [41], diluted with 10ml of distilled water, then Ruiz et al [42], Bloundi [43] and Abouhala 5ml was added to each of ninhydrin acid and et al. [44]. However, this area is glacial acetic. The samples were heated to characterized by the shallowest depth, and a 100°C. zero water turnover rate (after 30 days when in the water bath for 45 minutes and then the the windis low) [45], and under the effect of mixture was cooled. After 5 ml of benzene the high temperature and the low was added and allowed to stand for 15 hydrodynamics of water, which explains the minutes. And then the optical density of the installation of vast marsh at this site [46], upper phase was quantified by but at the Beni-Ensar station level, the spectrophotometer at 515nm using a Sp- decrease in salinity content compared with 200UV spectrophotometer previous studies [47]. Thus, the salinity For the determination of glucose decreases from 42.2 g / l before the opening concentration, we mixed 1 ml of extracted of the new passage [48, 49] to 40 g / l after alcohol mixed with 3ml anthrone (150mg the opening of the new pass [50], it varies anthrone, 100ml sulfuric acid 72%, w / v). from 36.67 to 39.5 g /l, almost similar to the The samples were placed in a boiling water salinity of seawater (36-38g / l). bath for 10min.The absorbance is read at the wave length of 625nm [38]. Dissolved oxygen In our present work, the seasonal evolution Results and Discussion of dissolved oxygen between the two Water heat is an ecological factor that seasons (winter and summer) shows higher causes significant ecological repercussions concentrations during the wet than during [39].It proceeds on the density, the the dry season. In fact , the grades recorded viscosity, the solubility of the gases in the (Table 1) vary between 2.5 mg / l in summer water. The dissociation of dissolved salts, as at the station of kariat-Arekman caused by well as on chemical and biochemical the decomposition of soluble organic matter reactions, development and growth of living becomes very slow, thus showing that the organisms in water.In our present study, the medium is reducing due to the increasing temperature range from a minimum value heat which caused the dissolved O2 content reached in january (15.8 °C) to a maximum to drop [51] and by the low rate of water value in july (30.6 ° C) at Kariat-Arekman turnover.For there more, dead algae’s station. decomposition in dues oxygen consumption: The spatial distribution (Tab.1) shows a while a maximum of 12,3 mg/l. mg/l in growing gradient at the site of Kariat- winter at Beni-Ensar’s interpreted by a Arekman compared to the site of Beni- better circulation of water at this site.

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Table1: Results of the seasonal variation of the physicochemical parameters of the waters at both stations of Beni-Ensar and Kariat-Arekman.1:Beni-Ensar’s station and 2:Kariat-Arekman’s station,T: Temperature; DO: Dissolved Oxygen; Sal: Salinity; Turb: Turbidity Parameter’s T (°C) DO (mg/l) Sal (g/l) pH Turb (NTU) Sites 1 2 1 2 1 2 1 2 1 2 October 15,9 16,8 9,24 9,74 38,73 38,53 8,1 8,3 0,25 2,28 January 15,9 15,8 12,3 6,49 38,6 38,52 8,2 8 2,65 1,6 April 22,7 23,7 8,68 9,83 37,91 38,25 8,3 8,5 0,04 0,82 July 30 30,6 7,16 2,5 38,9 39,5 8,4 7,8 4,56 6,95

Table 2: The results of seasonal variation of Nitrate nutrient salts in both stations of Beni-Ensar The nitrate concentration varied between and Kariat-Arekman. 1: Beni-Ensar station 0,02 mg/l in the autumn at the Beni-Ensar’s and 2: Kariat-Arekman station and 0.11 mg / l in summer by the stage of Parameter’s NO3 (mg/g) PO4 (mg/g) Kariat-Arekman’s station (Table 2), this Sites 1 2 1 2 high nitrate content in water may come from October 0,02 0,052 0 0,14 indirect sources, namely the decomposition of dead algae, which also induces oxygen’s January 0,116 0,021 0 0,004 consumption (2.5 mg / l), resulted in an April 0,024 0,021 0,008 0,006 accumulation of nitrate compounds .The July 0,081 0,1 0,007 0,008 following obtained values in our studied stations are probably related to the inputs of Table 3: Thresholds of some physical and effluents arriving at the lagoon. Indeed, chemical elements of water, relative to the Oued-Afelion’s effluents in Kariat- French standards adapted to the context of Arekman’s site are marked by the the Mediterranean lagoons, established by anthropogenic inputs arriving at the lagoon the IFRMR [52] and are witnessing the water degradation Seuil Good Medium Poor Bad quality. Nitrate (mg/l) 0,43 0,62 1,24 1,86

Phosphate (mg/l) 0,03 0,1 0,14 0,38 Orthophosphats

Orthophosphate concentrations in surface Biochemical analyzes of Chaetomorpha water at the two sites of the lagoon vary area between its absence in Autumn and winter Chaetomorpha aerea (Dillwyn) Kützing et the Beni-Ensar’s station and high level in was extracted from both ends, north-west Autumn by Kariat-Arekman’s station of (Beni-Ensar) and south-east (Kariat- 0.16 mg / l (Table 2) .These analyzed values Arekman) of Marchica’s lagoon, during the reflect a strong anthropization probably four seasons. It is limited in these two related to domestic discharges. Indeed, the stations, the same results were found by domestic urban discharges directly into the Bloundi [43]. Or, an algal tissues analysis water by living population on the inputs of provides a reliable indicator of water quality runoff induce the large variation of this [53, 54]. component according; the domestic Basically algae’s could be used as wastewater would contain many detergents biomarkers in the monitoring of organic which are the main sources of the pollution and inorganic pollution in phosphorus. terrestrial and aquatic ecosystems [55, 56]. Thus, the high nutrient values (Nitrate and phosphates) are the main responsible of the Total chlorophylls macroalgae proliferation especially at the Photosynthetic pigments are vital Kariat-Arekman’s station of Marchica’s components for the production of organic lagoon. Or, this station is a confined foods in algae, and cells viability is environment. associated with photosynthetic activity [57].

The highest concentrations of total

chlorophyll in Chaetomorpha in

respectively .4 mg / 100g in winter and

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153.96 mg / 100g (Figure 2) in summer at mg / 100g) mainly at the Beni-Ensar site, the station of Kariat-Arekman, this increase this decrease is probably caused by a low in chlorophyll levels during these two nitrogen content [65], which can be periods was found by Aguilera et al. [58] in explained by a better circulation of the water the brown algae’s (Laminaria digitata, L. mass caused by the opening of the new pass saccharina, Saccorhiza dermatodea and which contributes to the reduction of Desmarestia aculeata), Red algae pollution at this site. (Deevaleraea ramentacea and Palmaria It can therefore be concluded that the total palmata) and green algae (Monostroma chlorophyll content in Chaetomorpha algae Arcticum).This trend can be seen as a at the Kariat-Arekman level is important consequence of extreme lox light or nutrient because of the high levels of nitrogen 2- deficiency in winter. Nitrogen (NO 3) in the adsorbed by the algae; many researchers waters of both sites, low levels were found, have reached the same conclusion [66]. which explains the absorption of this element by the alga. So, nitrogen was recognized as the most limiting nutrient for 0,08 the proliferation from Chaetomorpha area. 0,06 Beni- Ensar 0,04 400 mg/g Kariat- Beni- 0,02 Arekman 300 Ensar 0 200 Kariat- mg/100g 100 Arekman Month 0

Figure 4: seasonal variation in glucose concentration (mg/g) in the Month collectedChaetomorpha area at the two studied stations between 2014 and 2015 Figure 3: Seasonal variation in chlorophyll pigment content in Chaetomorpha area Glucose between 2014 and 2015 Carbohydrates are the most important components for metabolism because it According to Menédez and al. [59], the high provides the energy needed for respiration levels of total chlorophyll can be considered and other metabolic processes [67], as a consequence of the high nitrate and specifically, glucose they also allow a nitrite content absorbed by algae and that preservation of the membrane’s integrity in the exogenous concentrations of P and N are the dried organs as well as a protection of directly correlated with the total chlorophyll the proteins [68].Seasonal changes in concentration [60]. Therefore, the glucose content in Chaetomorpha areaalgae chlorophyll content is directly related to the were observed during this study (Fig.4).The nitrogen concentration that has been results obtained in this study show that the recognized as the most limiting nutrient for glucose content measured in algae depends Chaetomorpha area proliferation. The same on many environmental and seasonal factors results were found in Ulva Rigida in the [69, 70] and the richness of the nitrogenous Venice Lagoon [61] and in Lake Tunis [62], element medium [71].Among these Ulva lactuca and Chaetomorpha linum in environmental factors identified in this the Roskilde Fjord, Denmark [63]. study, the temperature appears to have more However, Chaetomorpha acts as a impact on glucose content in the biological filter for the phosphate Chaetomorpha area. The strong glucose transported in the effluents of the lagoon synthesis is more important in the alga, [64]. which is responsible for the increase in the While the levels fell during the fall, when temperature of the medium (between 28 and they marked the lowest concentration (41.75 31°C) at the two stations during the summer

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Aknaf et al. ISSN : 2605-6208 period. Similar observations have been stress more strongly that the Beni-Ensar made on others species [72-75]; these high station. leveels are explained by the high rate of photosynthesis [76]. Whereas Khairy et al Conclusion [67] found that the highest glucose content The present study combain physico- was observed in U. lactuca and P. chemical characterization elements of water, capillacea during the spring period [67]. biochemical and physiological parameters of This accumulation of glucose will be vital Chaetomorpha area in the two studied for plant endurance under stressful stations of the Marchica lagoon, and which conditions in the marine ecosystem [77]. got implications on the status health of the both stations. Prooline A remarkable difference was obtained by According to Figure 5, we note that the high the results for water’s physico-chemical proline content was recorded during July at parameters and Chaetomorpha aerea eco- botth stations Beni-Ensar and Kariat- physiological parameters. As well, there has arekmann respectively 1.76 μg/g and 1.17 been an improvement in water’s quality at μg / g while the low grade was recorded in Beni-Ensar station, it’s basically related to January period at Beni-Ensar (0.26 ug/g) . the recent development of Marchica lagoon with the opening of the new pass, also that Chaetomorpha aerea may be used as the 4 best biomonitoring’s indicator of Beeni- 3 Ennsar eutrophication in Marchica lagoon “Nador”

2 Acknowledgements: mg/g We would like to thank Mr Mesfioui 1 Kaariat- Arrekman Abdelhakim, Dr. Layachi Mostafa and the 0 diver from INRH Nador for the logistic support and help to carry out the sampling of algae throughout the seasonal monitoring Month campaigns.

Figure 5: Seasonal variation in proline Referencese concentrations (μg/g) in Chaetomorpha area [1]Maanan M. (2003). Etudes collected at the two studied stations between sédimentologique du remplissage de la 2014 and 2015 lagune de Sidi Moussa (Côte Atlantique Marocaine). Thèse de Doctorat en This study shows that the season factor has Géologie, Université Chouïab Doukkali, an impact on free proline content. The El Jadida, p 164. maximum proline accumulation in [2] Joulami L., Daief Z., El Malki S., El Chaetomorphaareawas recorded during the Hamoumi R. (2013).Variation spatio- summer period under stressful conditions to temporelle des caractéristiques physico- know: high temperature [78], salinity [79, chimiques et la qualité des eaux et des 80]. However, high salinity concentrations sédiments d’une lagune côtière (38,53g/l) have been recorded at the Kariat- marocaine (Sidi Moussa, El Jadida). arekman station (S2), resulting in a high Science en liberté, Editions Mersenne : proline accumulation in this Volume 5, N ° 130702. species.Otherwise, proline can be tending a [3] Oueslati W. (2011). Cycles resistance index to salinity stress, as the case biogéochimiques des métaux lourds dans of Chaetomorpha at stage of Kariat- les sédiments marins de la lagune de Arekman station during the summer period, Ghar El Melh. Thèse de Doctorat. the same results were found by Nazali and Université Tunis El Manar. p 271. al. [81]. [4] Rybak A., Messayaz B., Pikosz M., The results show that the Chaetomorphha of Szendzina L., ŁŁęska B. (2013). Kariat-Arekman’s station synthesized and Accumulation of heavy metals (Co, Cr, acccumulates more proline for cells Cu, Mn, Zn) in the freshwater alga Ulva protection against any osmotic and oxidative type, sediments and water of the

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