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Energetic valorization of Nador lagoon algae and proposal to use it as a means of elimination of the eutrophication in this lagoon
Ecological Engineering 103 (2017) 236–243
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Research Paper
Energetic valorization of Nador lagoon algae and proposal to use it as a means of elimination of the eutrophication in this lagoon Ouahid El Asri a,∗ , Mohamed Ramdani b , Lahbib Latrach c , Benyounes Haloui b , Ramdani Mohamed d , Mohamed elamin Afilal a a
Biochemistry and Biotechnology Laboratory, Mohamed First University, Oujda, Morocco Ecology, Water and Environment Laboratory, Mohamed First University, Oujda, Morocco c Department of Biology, Faculty of Sciences Semlalia, Cadi Ayyad University, Marrakesh, Morocco d Applied Analytical Chemistry, Materials and Environment Laboratory, Mohamed First University, Oujda, Morocco b
a r t i c l e
i n f o
Article history: Received 12 September 2016 Received in revised form 13 March 2017 Accepted 2 April 2017 Keywords: Alsidium corallinum Anaerobic digestion Biogas Cystoseira barbata Chaetomorpha linum
a b s t r a c t The Nador lagoon is one of the best lagoons in the Mediterranean, it currently suffers from eutrophication caused by algae proliferation. In this study, we valorised the three important algae that are responsible for pollution of the lagoon. We determine their potential of biogas production and green energy capacities and we studied their effects on anaerobic bacteria proliferation in digester. After 40 days of incubation in batch mode we observed the red alga (Alsidium corallinum) produced the most biogas with 85.23 ml/gVS, which is equivalent to 511 kWh/tVS of green energy, whereas the brown alga (Cystoseira barbata) ranked second place with 76.45 ml/gVS of biogas product, the equivalent to 458 kWh/tVS of green energy. But, the green alga (Chaetomorpha linum) produced the least biogas do not exceed 22.23 ml/g VS, so these algae produces the lowest amount of energy green 133 kWh/tVS. Thus, this red alga (Alsidium corallinum) were considered excellent substrate for anaerobic digestion. These results correlated with the anaerobic bacterial proliferation of the inoculum, where the two algae (Alsidium corallinum and Cystoseira barbata) led to a large proliferation of anaerobic bacteria, from 1.8 × 105 CFU/g to 61 × 105 CFU/g, followed by the green alga. Therefore, we consider these three algae (Alsidium corallinum, Cystoseira barbata, and Chaetomorpha linum) as an exploitable energy reservoir in Nador lagoon. Finally, we propose that a new system which will halt eutrophication of this lagoon, it comprising anaerobic digestion of these algae, be installed to produce green energy for a lagoon aerator to dissolve the atmospheric oxygen inside the lagoon. © 2017 Elsevier B.V. All rights reserved.
1. Introduction The Nador Lagoon is the only lagoon ecosystem in the Moroccan coast facing the Mediterranean Sea, also called Marchica lagoon. It covers an area of 115 km2 with water depths from 3 to 8 m. (ElAlami et al., 1998; Erimesco, 1961); located in the Rif region of northeast Morocco between Cape Three Forks and the Cape Water (Ramdani et al., 2015); It holds a major interest in present-day Moroccan socioeconomic and ecological (Giuliani et al., 2015; Orbi et al., 2008). This environment is exposed to a number of potential polluting sources (Maanan et al., 2015). The daily discharges of domestic, agricultural, and industrial waste into the lagoon stimulate the proliferation of algae call “harmful algal blooms” (Lapointe et al., 2015; Ruiz et al., 2006). This increases oxygen consumption
∗ Corresponding author. E-mail address: [email protected] (O. El Asri). http://dx.doi.org/10.1016/j.ecoleng.2017.04.016 0925-8574/© 2017 Elsevier B.V. All rights reserved.
due to the degradation of algae produced there causing an imbalance of this ecosystem, which leads to eutrophication (Lapointe et al., 1994; Rybarczyk et al., 1996). Several authors have examined algae proliferation as a means to evaluate the health of the lagoon. They monitored algae as bioindicators of the lagoon’s water quality (Benchekroun et al., 2013; Dokulil, 2003; Hédouin et al., 2008). However, no research has been done to determine an effective means of lagoon depollution and valorisation of these indigenous algae. Faced with the environmental challenge to protect and valorise this natural wonder, it is necessary to develop a technology that combines the management, valorisation, and production of green energy from algae for the depollution of this lagoon. Among current technologies, anaerobic digestion, which is gaining more importance in Morocco and around the world, was chosen for this study. Anaerobic digestion is based on the degradation of various organic wastes, which are partially converted by microorganisms into biogas including methane, in hermetically sealed bioreactors
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Fig. 1. Algae harvesting sites in the Nador lagoon.
Fig. 2. The three macroalgae studied, (a) Chaetomorpha linum; (b) Cystoseira barbata; (c) Alsidium corallinum.
(Angelidaki et al., 2003; Elasri and Afilal, 2016). Algae are again receiving attention as a substrate for anaerobic digestion by several researchers (Ghadiryanfar et al., 2016; Zhao and Ruan, 2013) mainly in Asia and Australia caused by their significant prolifera-
tion in the Pacific region causing more environmental problems but these studies are insufficient front of the big number of species that proliferates every day (Hughes et al., 2012).
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2.2. Total and volatile solids of the algae Total solids (TS) and volatile solids (VS) are considered as the most important qualitative and quantitative criteria for a substrate distended to anaerobic digestion. TS was performed according to the standard protocol which consists of drying the fresh matter (FM) at 105 ◦ C to a constant weight and volatile solids (VS) which is a gravimetric method based on the mass loss of the dry sample (sample from the determination of TS) in a muffle furnace at 550 ◦ C for 6 h (ApHA, 2005). 2.3. Laboratory experiments
Fig. 3. biogas production for the three studied algae.
The goal of this study is to propose a new approach and effective design for the remediation and recovery of these native algae in the lagoon. The objectives of this study are: 1) We sought to compare the biogas production by the three major algae that pollute the Nador lagoon (Alsidium corallinum, Cystoseira barbata, and Chaetomorpha linum); 2) We study their effects on anaerobic bacterial growth of inoculum; and 3) We estimated the potential energy produced by these algae to propose an innovative solution for treatment of the Nador lagoon. Finally, This study is the first attempt to treat the algae of this lagoon by anaerobic digestion. 2. Materials and methods 2.1. Study area, harvest and preparation of macroalgae The harvest of the three algae was performed on the same day (25 Mai 2015) from a zodiac inflatable boat by a diver equipped with algae grubbing material. The diver harvested all species in a 1 m2 frame in the Nador lagoon. The sampling sites were located ® by GPS (Garmin GPSMAP 60CSx) (Fig. 1 and Table 1). The three algae used in this work were Alsidium corallinum, Cystoseira barbata, and Chaetomorpha linum. They are Macroalgae, eukaryotic, photosynthetic marine organisms (Vandendriessche et al., 2006). We adapted the simplest classification for algae (green, red, and brown), which is based on the type of chlorophyll pigments they contain (Flores-Moya et al., 1995) (Fig. 2): – Cystoseira barbata is a brown alga that belongs to the class of Pheophyceae, the order of Fucales, and the family of Fucaceae (Pellegrini et al., 1997) . – Chaetomorpha linum is a green alga (Chlorophyta) that belongs to the class of Ulvophyceae, the order of Cladophorales, and the family of Caldophoraceae (Riadi et al., 2000). – Alsidium corallinum is a red alga (Rhodophyta), which belongs to the class of Florideophyceae, the order of Ceramiales, and the family of Rhodomelaceae (Agardh, 1827). The three algae studied, they underwent two pretreatments: thermally pretreated at 105 ◦ C for 24 h to avoid combustion (ApHA, 1999) and grinding by grinder (IKA A11 Basic) and sieving with an inox sieve (diameter 0.04 mm) so the organic material of the algae was accessible to the anaerobic bacteria of the inoculum (Bjerre et al., 2000; Mendez et al., 2015).
Anaerobic digestion test of these algae followed three steps: First step is the activation of inoculum. The inoculum used in this work was removed from the interior of a pilot digester in our laboratory and was produced from the anaerobic digestion of broiler chicken droppings. We maintained it under anaerobic conditions at 35 ◦ C in a 5 l reactor, which was closed with a silicon stopper perforated at the top by a biogas exhaust pipe. It was incubated for 10 days so that all organic material residuals were exhausted and the range of bacteria present in the inoculum was activated. Second step is the construction of digesters. We conducted four digesters tests: 3 experimental (inoculum with one of the three species of algae) and negative control consisting of water in the place of sample in order to determine the biogas produced by the inoculum alone. Each test was performed in a batch-type digester with 1 g TS of algae and 12.5 g of inoculum with a concentration of 8% TS. So, that each digester had a concentration of 9% TS. We selected this concentration because it is considered optimal concentration (Budiyono et al., 2010a; Kreith and Tchobanoglous, 2002). The digesters were filled while on a balance to allow mass balance by grams, and we assumed an inoculum density of 1 (Perimenis et al., 2015). Each digesters headspace was flushed for 2 min with a constant flow of nitrogen gas in order to ensure the absence of oxygen in the digesters prior to stabilize the anaerobic atmosphere, and then proceeds to a sealed closure of the digesters (Wobiwo et al., 2016). All the digesters were incubated in a water bath at 35 ± 1 ◦ C for 40 days. Every day, we followed the biogas production by moving an acidic and saline solution in an inverted burette connected to the digester (Elasri et al., 2015). The volumes of biogas produced were adjusted to the standard conditions of pressure and temperature. 2.4. Monitoring of evolution of pH We measured the pH of the inoculum in digesters with a pH meter (Consort type), which was calibrated by both pH 4 and pH 7 standards. The pH was determined at two time: the start of manipulation (pHi ) to verify the beginning of anaerobic digestion and at the end of incubation (pHf ) i.e. after 40 days of anaerobic digestion. 2.5. Monitoring of proliferation of anaerobic bacteria in digester After 40 days of anaerobic digestion, we counted the anaerobic bacteria in all digesters on Plate Count Agar (PCA) in the middle of an anaerobic jar (Ilmvac Anavac 104 T) incubated at 37 ◦ C for 48 h. The enumeration of anaerobic bacteria was calculated using the following equation: N = colonies/V(X1 + 0.1X2 )D Where N is the number of colony-forming units (CFU) per gram, colonies is the sum of colonies in boxes that can be interpreted, V is the volume of solution deposited in the box (1 ml), X1 is the number of boxes considered at the first dilution retained, X2 is the
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Table 1 Geospatial coordinates of algae harvesting sites in the Nador lagoon.
Site 1 Site 2 Site 3 Site 4 Site 5 Site 6 Site 7 Site 8
Alsidium corallinum
Cystoseira barbata
Chaetomorpha linum
35◦ 13 54,52 ’/2◦ 55 19,02 ’ 35◦ 11 58,40 ’/2◦ 54 3,94 ’ 35◦ 08 58,15 ’/2◦ 53 54,36 ’ 35◦ 08 52,79 ’/2◦ 50 31,48 ’ 35◦ 08 4,72 ’/2◦ 52 50,45 ’ 35◦ 0 730,60 ’/2◦ 50 11,25 ’ 35◦ 07 12,57 ’/2◦ 45 57,74 ’ 35◦ 09 2,20 ’/2◦ 48 13,13 ’
35◦ 13 52,85 ’/2◦ 55 18,95 ’ 35◦ 12 45,21 ’/2◦ 53 52,08 ’ 35◦ 12 08 ’/2◦ 51 43 ’ 35◦ 10 33,19 ’/2◦ 51 18 ’ 35◦ 8 8 ’/2◦ 52 49 ’ 35◦ 7 57,3 ’/2◦ 50 21,85 ’ 35◦ 7 6,92 ’/2◦ 47 9,10 ’ 35◦ 8 50 ’/2◦ 47 30 ’
35◦ 14 25,39 ’/2◦ 54 26,98 ’ 35◦ 09 7,72 ’/2◦ 53 46,44 ’ 35◦ 08 43,55 ’/2◦ 52 46,12 ’ 35◦ 07 26,69 ’/2◦ 51 5,58 ’ 35◦ 07 14,39 ’/2◦ 50 29,83 ’ 35◦ 06 34,95 ’/2◦ 48 51,23 ’ 35◦ 06 20,05 ’/2◦ 45 13,88 ’ -
Table 2 Comparison of physicochemical characteristics and electricity production for the three studied algae.
TS (g/100 g FM) VS (g/100 g TS) Biogas production (m3 /t VS) Green electricity (KWh)
Alsidium corallinum
Cystoseira barbata
Chaetomorpha linum
79.2 ± 0.4 75.23 ± 0.8 85.23 ± 0.32 170.46 ± 0.32
81.7 ± 0.6 17.19 ± 1.1 76.45 ± 0.1 152.9 ± 0.1
81.2 ± 0.6 75.23 ± 0.8 22.23 ± 0.19 44.46 ± 0.19
number of boxes considered at the second dilution retained, and D is the factor of the first retaining dilution.
3. Results 3.1. Potential and kinetics of biogas production We noticed that all algae produced biogas but in different potential according to species. Alsidium corallinum produced the most biogas (86.35 ± 0.31 ml/g VS), followed by Cystoseira barbata (74.68 ± 0.15 ml/g VS), and Chaetomorpha linum producing the least biogas (24.53 ± 0.16 ml/g VS) (Fig. 3). Therefore, red alga produce more biogas than other algae. The biogas kinetics for the three examined algae showed biogas production from the first day of incubation, i.e. no latency time (Fig. 4). We noted that biogas production increased rapidly with increased time, up to 30 days, after which it was stable in all digesters, due to the depletion of the convertible biodegradable organic material as it turned into biogas (Budiyono et al., 2010b). The three algae showed biphasic production (two production peaks): The first phase from the first day to the 25th day for the red and brown algae but to the 32nd day for the green alga, this phase corresponding to the transformation of the readily biodegradable fraction. The second phase is after 25th and 32nd day of incubation corresponding to the fraction that was difficult to biodegrade (Fig. 4). These results were also observed by (Zhao and Ruan, 2013) for Taihu algae.
3.2. Behaviour of anaerobic bacteria in the inoculum of anaerobic digestion we noted that the anaerobic digestion of these three algae led to an increase in anaerobic bacteria but in different ways. The degradation of red alga (Alsidium corallinum) led to an explosion in the proliferation of inoculum anaerobic bacteria, which multiply more than 33 times the initial quantity (1.8 × 105 CFU/g to 61 × 105 CFU/g) (Fig. 5). The brown alga (Cystoseira barbata) was second best in the proliferation of anaerobic bacteria, which multiply 22 times the initial quantity (1.8 × 105 CFU/g to 41 × 105 CFU/g), followed by the green alga (Chaetomorpha linum), who showed the lowest proliferation (18.5 × 105 CFU/g). These results correlated with the content of biogas produced by each type of algae. Therefore, more the anaerobic bacterial proliferation is important more there is a large biogas production.
3.3. Evolution of pH during the anaerobic digestion of these algae pH is an excellent parameter of evolution of anaerobic digestion (Amani et al., 2011) when measuring the pH before and after incubation. We find that red alga has the largest decrease of pH 7.42–6.72 followed by the brown alga then green alga (Fig. 6). These results are in exact correlation with the production of biogas by these algae. 3.4. Estimation of green energy produced by the three algae Some authors have suggested that the biogas produced by algae is, on average, 60% methane but the conversion of biogas to electricity by an electrical generator produces only 2 kWh, the rest of the energy is dissipated in the form of heat (Hughes et al., 2012; Vergarafernandez et al., 2008). We can calculate the green energy content in the form of lower heating value (LHV) of the biogas produced by these algae by multiplying the biogas production by 2 kWh/m3 . The red alga was most energetic (170 kWh), followed by the brown alga (152 kWh), and finally the green alga had the lowest energy production (44 kWh) (Table 2). If we combine the three Nador algae in a digester, we can obtain a large amount of energy, 367 kWh. 4. Discussion 4.1. Potential and kinetics of biogas production The red alga Alsidium corallinum was more energetic than the other algae studied. When we compared the elemental composition of these algae, we find that this red alga is rich in nutrients such as carbon (22.13%), nitrogen (1.85%) and phosphorus (0.07%) (Lenzi et al., 2012), which are essential nutrients for anaerobic microorganisms compared to other algae (Table 3). This result is almost similar to the production of biogas by Gracilaria bursapastoris (86.35 ml/g VS). As well as some researchers confirms that the high carbohydrate and agar content in red algae promotes the production of biogas (Renaud and Luong-Van, 2006). The brown algae have lower levels of carbon (21.08%), nitrogen (1.71%) and phosphorus (0.06%) than red algae, where its production of biogas is second place (Lenzi et al., 2012). On the other hand the green algae present the lowest content of three elements and the global chemical composition of Chaetomorpha linum shows the presence of a large quantity of the fiber at 27 ± 1.8% containing 21 ± 1.2% cellulose (Schultz-Jensen et al., 2013). Consequently, this quantity of cellulose requires the addition of an enzymatic treatment before
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Fig. 4. Kinetics of biogas production for the three studied algae.
Fig. 5. Comparison of the proliferation of anaerobic bacteria in the inoculum during the anaerobic digestion of three algae.
introducing it to the digester for improve biogas production (Ben Yahmed et al., 2016), thus its low production of biogas. Therefore,
more seaweed contains these components (C, N, P) in its biomass it more produces biogas.
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Fig. 6. Comparison of evolution of pH in the three tests.
Fig. 7. Biogas plant proposal for the protection of Nador Lagoon. 1: Algae harvesting; 2: Cutters; 3: Digester; 4: Gasometer; 5: Agitator motor; 6: Cogeneration motor; 7: Aerator; 8: Aeration channels; 9: Air bubbles.
Table 3 Carbon, nitrogen and phorphorus content in tissue of Alsidium corallinum, Chaetomorpha linum (Lenzi et al., 2012) and Cystoseira sp. (Delgado et al., 1994).
Carbon content (g/100 g TS) Nitrogen content (g/100 g TS) Phorphorus content (g/100 g TS)
Alsidium corallinum
Chaetomorpha linum
Cystoseira sp.
22.13 ± 7.44 1.85 ± 0.88 0.07 ± 0.01
18.23 ± 5.32 1.65 ± 1.18 0.05 ± 0.03
21.08 ± 5.22 1.71 ± 0.01 0.06 ± 0.01
The biogas kinetics showed an absence of latency time. Therefore, the transformation of algae organic matter to biogas occurred quickly and without bacterial adaptation to the anaerobic conditions, which is due to the pretreatment (drying, crushing, and sieving) of the algae before they were introduced into the digester (Montingelli et al., 2016). This mechanical pretreatment (drying, crushing, and sieving) of the algae allowed for a reduction in particle size, crystallinity, and degree of polymerization of cellulose for making the manipulation of organic charge easier; and for an increase in the surface/volume ratio, which shortened the cycle and improved digestion (Rodriguez et al., 2015).
4.2. Behaviour of the inoculum bacteria during the anaerobic digestion of algae Three algae led to an increase in anaerobic bacteria because the release of algal organic matter can enhance survival and even growth of these bacteria mainly the algal degradation provides the carbon and energy sources for the bacteria (Bouteleux et al., 2005). Some authors have confirmed that the proliferation of bacteria such as E. coli is influenced by type of chlorophyll pigment. Ansa et al., 2011; declares that the chlorophyll a has led to removal E.coli. So, the low proliferation of anaerobic bacteria by the green
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algae (Chaetomorpha linum) is due to the large amount of chlorophyll a in this specie compared to the other two algae. Pierre et al., 2011; has described antibacterial activity of a this green alga by production of sulfated galactan which inhibited the development of the anaerobic bacteria, so, the low production of biogas. At the end of incubation, we noticed that red algae (Alsidium corallinum) leads to an increase in the number of anaerobic bacteria. These big proliferation is due to the presence of agar and carbohydrates in this specie which allowed the bacterial proliferation to accelerate (Polifrone et al., 2006) and the presence of a significant amount of carbon, nitrogen and phosphorus, which are essential nutrients for growth of anaerobic microorganisms. These results correlated with the content of biogas produced by each type of algae. 4.3. Evolution of pH during the anaerobic digestion of these algae The significant decrease in pH during the anaerobic digestion of the red algae is due to an important degradation of its organic matter in volatile fatty acids (VFAs) and CO2 which led to a slight acidity of digester (Angelidaki et al., 2003). On the other hand, green algae have a low production of biogas which confirms a low production of VFAs that will be converted to biogas, resulting in a small decrease in pH. 4.4. Estimation of green energy produced by the three algae We can consider the three algae provocative of eutrophication in the Nador lagoon that are non-exploitable energy deposit (367 kWh), instead of viewing them as a potential source of pollution. These results are in agreement with several studies which demonstrated that the macroalgae are potentially a good source for bioenergy production. For this, we propose to install anaerobic algae digesters around the lagoon, mainly in algae proliferation areas (Schultz-Jensen et al., 2013). The algae will be harvested and added to the digesters to produce energy by cogeneration that will then fuel an aerator that will dissolve atmospheric oxygen inside the lagoon (Fig. 7). By employing this process, eutrophication will be inhibited and hopefully disappear. The energy produced using this method generally will be more expensive than that from fossil fuels, but it can be profitable and compete with other energy sources if rules are adopted to limit emissions, including carbon taxes and subsidies for biomass energy (Chynoweth et al., 2001). 5. Conclusion We conclude that the red alga Alsidium corallinum and brown alga Cystoseira barbata are two excellent substrates for methanation through their biogas production and the increase in anaerobic bacterial proliferation that optimized anaerobic digestion. The green alga Chaetomorpha linum produced much less biogas. These results show that these three lagoon-polluting algae (Alsidium corallinum, Cystoseira barbata, Chaetomorpha linum) are green energy producers. We combine the three Marchica algae in a digester, we can obtain a large amount of energy (367 kWh). Hence, there is a need to install an innovative plant, which includes an algae digester, for energy production and a lagoon aerator for atmospheric oxygen dissolution inside the lagoon to destroy the favourable conditions for eutrophication, thus protecting the lagoon. This pilot plant will be the topic of a future publication. Acknowledgment We deeply thank, Mr Hicham Elasri, Shokri Mahmoudi for his technical support to produce this work.
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Ecological Engineering journal homepage: www.elsevier.com/locate/ecoleng
Research Paper
Energetic valorization of Nador lagoon algae and proposal to use it as a means of elimination of the eutrophication in this lagoon Ouahid El Asri a,∗ , Mohamed Ramdani b , Lahbib Latrach c , Benyounes Haloui b , Ramdani Mohamed d , Mohamed elamin Afilal a a
Biochemistry and Biotechnology Laboratory, Mohamed First University, Oujda, Morocco Ecology, Water and Environment Laboratory, Mohamed First University, Oujda, Morocco c Department of Biology, Faculty of Sciences Semlalia, Cadi Ayyad University, Marrakesh, Morocco d Applied Analytical Chemistry, Materials and Environment Laboratory, Mohamed First University, Oujda, Morocco b
a r t i c l e
i n f o
Article history: Received 12 September 2016 Received in revised form 13 March 2017 Accepted 2 April 2017 Keywords: Alsidium corallinum Anaerobic digestion Biogas Cystoseira barbata Chaetomorpha linum
a b s t r a c t The Nador lagoon is one of the best lagoons in the Mediterranean, it currently suffers from eutrophication caused by algae proliferation. In this study, we valorised the three important algae that are responsible for pollution of the lagoon. We determine their potential of biogas production and green energy capacities and we studied their effects on anaerobic bacteria proliferation in digester. After 40 days of incubation in batch mode we observed the red alga (Alsidium corallinum) produced the most biogas with 85.23 ml/gVS, which is equivalent to 511 kWh/tVS of green energy, whereas the brown alga (Cystoseira barbata) ranked second place with 76.45 ml/gVS of biogas product, the equivalent to 458 kWh/tVS of green energy. But, the green alga (Chaetomorpha linum) produced the least biogas do not exceed 22.23 ml/g VS, so these algae produces the lowest amount of energy green 133 kWh/tVS. Thus, this red alga (Alsidium corallinum) were considered excellent substrate for anaerobic digestion. These results correlated with the anaerobic bacterial proliferation of the inoculum, where the two algae (Alsidium corallinum and Cystoseira barbata) led to a large proliferation of anaerobic bacteria, from 1.8 × 105 CFU/g to 61 × 105 CFU/g, followed by the green alga. Therefore, we consider these three algae (Alsidium corallinum, Cystoseira barbata, and Chaetomorpha linum) as an exploitable energy reservoir in Nador lagoon. Finally, we propose that a new system which will halt eutrophication of this lagoon, it comprising anaerobic digestion of these algae, be installed to produce green energy for a lagoon aerator to dissolve the atmospheric oxygen inside the lagoon. © 2017 Elsevier B.V. All rights reserved.
1. Introduction The Nador Lagoon is the only lagoon ecosystem in the Moroccan coast facing the Mediterranean Sea, also called Marchica lagoon. It covers an area of 115 km2 with water depths from 3 to 8 m. (ElAlami et al., 1998; Erimesco, 1961); located in the Rif region of northeast Morocco between Cape Three Forks and the Cape Water (Ramdani et al., 2015); It holds a major interest in present-day Moroccan socioeconomic and ecological (Giuliani et al., 2015; Orbi et al., 2008). This environment is exposed to a number of potential polluting sources (Maanan et al., 2015). The daily discharges of domestic, agricultural, and industrial waste into the lagoon stimulate the proliferation of algae call “harmful algal blooms” (Lapointe et al., 2015; Ruiz et al., 2006). This increases oxygen consumption
∗ Corresponding author. E-mail address: [email protected] (O. El Asri). http://dx.doi.org/10.1016/j.ecoleng.2017.04.016 0925-8574/© 2017 Elsevier B.V. All rights reserved.
due to the degradation of algae produced there causing an imbalance of this ecosystem, which leads to eutrophication (Lapointe et al., 1994; Rybarczyk et al., 1996). Several authors have examined algae proliferation as a means to evaluate the health of the lagoon. They monitored algae as bioindicators of the lagoon’s water quality (Benchekroun et al., 2013; Dokulil, 2003; Hédouin et al., 2008). However, no research has been done to determine an effective means of lagoon depollution and valorisation of these indigenous algae. Faced with the environmental challenge to protect and valorise this natural wonder, it is necessary to develop a technology that combines the management, valorisation, and production of green energy from algae for the depollution of this lagoon. Among current technologies, anaerobic digestion, which is gaining more importance in Morocco and around the world, was chosen for this study. Anaerobic digestion is based on the degradation of various organic wastes, which are partially converted by microorganisms into biogas including methane, in hermetically sealed bioreactors
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Fig. 1. Algae harvesting sites in the Nador lagoon.
Fig. 2. The three macroalgae studied, (a) Chaetomorpha linum; (b) Cystoseira barbata; (c) Alsidium corallinum.
(Angelidaki et al., 2003; Elasri and Afilal, 2016). Algae are again receiving attention as a substrate for anaerobic digestion by several researchers (Ghadiryanfar et al., 2016; Zhao and Ruan, 2013) mainly in Asia and Australia caused by their significant prolifera-
tion in the Pacific region causing more environmental problems but these studies are insufficient front of the big number of species that proliferates every day (Hughes et al., 2012).
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2.2. Total and volatile solids of the algae Total solids (TS) and volatile solids (VS) are considered as the most important qualitative and quantitative criteria for a substrate distended to anaerobic digestion. TS was performed according to the standard protocol which consists of drying the fresh matter (FM) at 105 ◦ C to a constant weight and volatile solids (VS) which is a gravimetric method based on the mass loss of the dry sample (sample from the determination of TS) in a muffle furnace at 550 ◦ C for 6 h (ApHA, 2005). 2.3. Laboratory experiments
Fig. 3. biogas production for the three studied algae.
The goal of this study is to propose a new approach and effective design for the remediation and recovery of these native algae in the lagoon. The objectives of this study are: 1) We sought to compare the biogas production by the three major algae that pollute the Nador lagoon (Alsidium corallinum, Cystoseira barbata, and Chaetomorpha linum); 2) We study their effects on anaerobic bacterial growth of inoculum; and 3) We estimated the potential energy produced by these algae to propose an innovative solution for treatment of the Nador lagoon. Finally, This study is the first attempt to treat the algae of this lagoon by anaerobic digestion. 2. Materials and methods 2.1. Study area, harvest and preparation of macroalgae The harvest of the three algae was performed on the same day (25 Mai 2015) from a zodiac inflatable boat by a diver equipped with algae grubbing material. The diver harvested all species in a 1 m2 frame in the Nador lagoon. The sampling sites were located ® by GPS (Garmin GPSMAP 60CSx) (Fig. 1 and Table 1). The three algae used in this work were Alsidium corallinum, Cystoseira barbata, and Chaetomorpha linum. They are Macroalgae, eukaryotic, photosynthetic marine organisms (Vandendriessche et al., 2006). We adapted the simplest classification for algae (green, red, and brown), which is based on the type of chlorophyll pigments they contain (Flores-Moya et al., 1995) (Fig. 2): – Cystoseira barbata is a brown alga that belongs to the class of Pheophyceae, the order of Fucales, and the family of Fucaceae (Pellegrini et al., 1997) . – Chaetomorpha linum is a green alga (Chlorophyta) that belongs to the class of Ulvophyceae, the order of Cladophorales, and the family of Caldophoraceae (Riadi et al., 2000). – Alsidium corallinum is a red alga (Rhodophyta), which belongs to the class of Florideophyceae, the order of Ceramiales, and the family of Rhodomelaceae (Agardh, 1827). The three algae studied, they underwent two pretreatments: thermally pretreated at 105 ◦ C for 24 h to avoid combustion (ApHA, 1999) and grinding by grinder (IKA A11 Basic) and sieving with an inox sieve (diameter 0.04 mm) so the organic material of the algae was accessible to the anaerobic bacteria of the inoculum (Bjerre et al., 2000; Mendez et al., 2015).
Anaerobic digestion test of these algae followed three steps: First step is the activation of inoculum. The inoculum used in this work was removed from the interior of a pilot digester in our laboratory and was produced from the anaerobic digestion of broiler chicken droppings. We maintained it under anaerobic conditions at 35 ◦ C in a 5 l reactor, which was closed with a silicon stopper perforated at the top by a biogas exhaust pipe. It was incubated for 10 days so that all organic material residuals were exhausted and the range of bacteria present in the inoculum was activated. Second step is the construction of digesters. We conducted four digesters tests: 3 experimental (inoculum with one of the three species of algae) and negative control consisting of water in the place of sample in order to determine the biogas produced by the inoculum alone. Each test was performed in a batch-type digester with 1 g TS of algae and 12.5 g of inoculum with a concentration of 8% TS. So, that each digester had a concentration of 9% TS. We selected this concentration because it is considered optimal concentration (Budiyono et al., 2010a; Kreith and Tchobanoglous, 2002). The digesters were filled while on a balance to allow mass balance by grams, and we assumed an inoculum density of 1 (Perimenis et al., 2015). Each digesters headspace was flushed for 2 min with a constant flow of nitrogen gas in order to ensure the absence of oxygen in the digesters prior to stabilize the anaerobic atmosphere, and then proceeds to a sealed closure of the digesters (Wobiwo et al., 2016). All the digesters were incubated in a water bath at 35 ± 1 ◦ C for 40 days. Every day, we followed the biogas production by moving an acidic and saline solution in an inverted burette connected to the digester (Elasri et al., 2015). The volumes of biogas produced were adjusted to the standard conditions of pressure and temperature. 2.4. Monitoring of evolution of pH We measured the pH of the inoculum in digesters with a pH meter (Consort type), which was calibrated by both pH 4 and pH 7 standards. The pH was determined at two time: the start of manipulation (pHi ) to verify the beginning of anaerobic digestion and at the end of incubation (pHf ) i.e. after 40 days of anaerobic digestion. 2.5. Monitoring of proliferation of anaerobic bacteria in digester After 40 days of anaerobic digestion, we counted the anaerobic bacteria in all digesters on Plate Count Agar (PCA) in the middle of an anaerobic jar (Ilmvac Anavac 104 T) incubated at 37 ◦ C for 48 h. The enumeration of anaerobic bacteria was calculated using the following equation: N = colonies/V(X1 + 0.1X2 )D Where N is the number of colony-forming units (CFU) per gram, colonies is the sum of colonies in boxes that can be interpreted, V is the volume of solution deposited in the box (1 ml), X1 is the number of boxes considered at the first dilution retained, X2 is the
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Table 1 Geospatial coordinates of algae harvesting sites in the Nador lagoon.
Site 1 Site 2 Site 3 Site 4 Site 5 Site 6 Site 7 Site 8
Alsidium corallinum
Cystoseira barbata
Chaetomorpha linum
35◦ 13 54,52 ’/2◦ 55 19,02 ’ 35◦ 11 58,40 ’/2◦ 54 3,94 ’ 35◦ 08 58,15 ’/2◦ 53 54,36 ’ 35◦ 08 52,79 ’/2◦ 50 31,48 ’ 35◦ 08 4,72 ’/2◦ 52 50,45 ’ 35◦ 0 730,60 ’/2◦ 50 11,25 ’ 35◦ 07 12,57 ’/2◦ 45 57,74 ’ 35◦ 09 2,20 ’/2◦ 48 13,13 ’
35◦ 13 52,85 ’/2◦ 55 18,95 ’ 35◦ 12 45,21 ’/2◦ 53 52,08 ’ 35◦ 12 08 ’/2◦ 51 43 ’ 35◦ 10 33,19 ’/2◦ 51 18 ’ 35◦ 8 8 ’/2◦ 52 49 ’ 35◦ 7 57,3 ’/2◦ 50 21,85 ’ 35◦ 7 6,92 ’/2◦ 47 9,10 ’ 35◦ 8 50 ’/2◦ 47 30 ’
35◦ 14 25,39 ’/2◦ 54 26,98 ’ 35◦ 09 7,72 ’/2◦ 53 46,44 ’ 35◦ 08 43,55 ’/2◦ 52 46,12 ’ 35◦ 07 26,69 ’/2◦ 51 5,58 ’ 35◦ 07 14,39 ’/2◦ 50 29,83 ’ 35◦ 06 34,95 ’/2◦ 48 51,23 ’ 35◦ 06 20,05 ’/2◦ 45 13,88 ’ -
Table 2 Comparison of physicochemical characteristics and electricity production for the three studied algae.
TS (g/100 g FM) VS (g/100 g TS) Biogas production (m3 /t VS) Green electricity (KWh)
Alsidium corallinum
Cystoseira barbata
Chaetomorpha linum
79.2 ± 0.4 75.23 ± 0.8 85.23 ± 0.32 170.46 ± 0.32
81.7 ± 0.6 17.19 ± 1.1 76.45 ± 0.1 152.9 ± 0.1
81.2 ± 0.6 75.23 ± 0.8 22.23 ± 0.19 44.46 ± 0.19
number of boxes considered at the second dilution retained, and D is the factor of the first retaining dilution.
3. Results 3.1. Potential and kinetics of biogas production We noticed that all algae produced biogas but in different potential according to species. Alsidium corallinum produced the most biogas (86.35 ± 0.31 ml/g VS), followed by Cystoseira barbata (74.68 ± 0.15 ml/g VS), and Chaetomorpha linum producing the least biogas (24.53 ± 0.16 ml/g VS) (Fig. 3). Therefore, red alga produce more biogas than other algae. The biogas kinetics for the three examined algae showed biogas production from the first day of incubation, i.e. no latency time (Fig. 4). We noted that biogas production increased rapidly with increased time, up to 30 days, after which it was stable in all digesters, due to the depletion of the convertible biodegradable organic material as it turned into biogas (Budiyono et al., 2010b). The three algae showed biphasic production (two production peaks): The first phase from the first day to the 25th day for the red and brown algae but to the 32nd day for the green alga, this phase corresponding to the transformation of the readily biodegradable fraction. The second phase is after 25th and 32nd day of incubation corresponding to the fraction that was difficult to biodegrade (Fig. 4). These results were also observed by (Zhao and Ruan, 2013) for Taihu algae.
3.2. Behaviour of anaerobic bacteria in the inoculum of anaerobic digestion we noted that the anaerobic digestion of these three algae led to an increase in anaerobic bacteria but in different ways. The degradation of red alga (Alsidium corallinum) led to an explosion in the proliferation of inoculum anaerobic bacteria, which multiply more than 33 times the initial quantity (1.8 × 105 CFU/g to 61 × 105 CFU/g) (Fig. 5). The brown alga (Cystoseira barbata) was second best in the proliferation of anaerobic bacteria, which multiply 22 times the initial quantity (1.8 × 105 CFU/g to 41 × 105 CFU/g), followed by the green alga (Chaetomorpha linum), who showed the lowest proliferation (18.5 × 105 CFU/g). These results correlated with the content of biogas produced by each type of algae. Therefore, more the anaerobic bacterial proliferation is important more there is a large biogas production.
3.3. Evolution of pH during the anaerobic digestion of these algae pH is an excellent parameter of evolution of anaerobic digestion (Amani et al., 2011) when measuring the pH before and after incubation. We find that red alga has the largest decrease of pH 7.42–6.72 followed by the brown alga then green alga (Fig. 6). These results are in exact correlation with the production of biogas by these algae. 3.4. Estimation of green energy produced by the three algae Some authors have suggested that the biogas produced by algae is, on average, 60% methane but the conversion of biogas to electricity by an electrical generator produces only 2 kWh, the rest of the energy is dissipated in the form of heat (Hughes et al., 2012; Vergarafernandez et al., 2008). We can calculate the green energy content in the form of lower heating value (LHV) of the biogas produced by these algae by multiplying the biogas production by 2 kWh/m3 . The red alga was most energetic (170 kWh), followed by the brown alga (152 kWh), and finally the green alga had the lowest energy production (44 kWh) (Table 2). If we combine the three Nador algae in a digester, we can obtain a large amount of energy, 367 kWh. 4. Discussion 4.1. Potential and kinetics of biogas production The red alga Alsidium corallinum was more energetic than the other algae studied. When we compared the elemental composition of these algae, we find that this red alga is rich in nutrients such as carbon (22.13%), nitrogen (1.85%) and phosphorus (0.07%) (Lenzi et al., 2012), which are essential nutrients for anaerobic microorganisms compared to other algae (Table 3). This result is almost similar to the production of biogas by Gracilaria bursapastoris (86.35 ml/g VS). As well as some researchers confirms that the high carbohydrate and agar content in red algae promotes the production of biogas (Renaud and Luong-Van, 2006). The brown algae have lower levels of carbon (21.08%), nitrogen (1.71%) and phosphorus (0.06%) than red algae, where its production of biogas is second place (Lenzi et al., 2012). On the other hand the green algae present the lowest content of three elements and the global chemical composition of Chaetomorpha linum shows the presence of a large quantity of the fiber at 27 ± 1.8% containing 21 ± 1.2% cellulose (Schultz-Jensen et al., 2013). Consequently, this quantity of cellulose requires the addition of an enzymatic treatment before
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Fig. 4. Kinetics of biogas production for the three studied algae.
Fig. 5. Comparison of the proliferation of anaerobic bacteria in the inoculum during the anaerobic digestion of three algae.
introducing it to the digester for improve biogas production (Ben Yahmed et al., 2016), thus its low production of biogas. Therefore,
more seaweed contains these components (C, N, P) in its biomass it more produces biogas.
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Fig. 6. Comparison of evolution of pH in the three tests.
Fig. 7. Biogas plant proposal for the protection of Nador Lagoon. 1: Algae harvesting; 2: Cutters; 3: Digester; 4: Gasometer; 5: Agitator motor; 6: Cogeneration motor; 7: Aerator; 8: Aeration channels; 9: Air bubbles.
Table 3 Carbon, nitrogen and phorphorus content in tissue of Alsidium corallinum, Chaetomorpha linum (Lenzi et al., 2012) and Cystoseira sp. (Delgado et al., 1994).
Carbon content (g/100 g TS) Nitrogen content (g/100 g TS) Phorphorus content (g/100 g TS)
Alsidium corallinum
Chaetomorpha linum
Cystoseira sp.
22.13 ± 7.44 1.85 ± 0.88 0.07 ± 0.01
18.23 ± 5.32 1.65 ± 1.18 0.05 ± 0.03
21.08 ± 5.22 1.71 ± 0.01 0.06 ± 0.01
The biogas kinetics showed an absence of latency time. Therefore, the transformation of algae organic matter to biogas occurred quickly and without bacterial adaptation to the anaerobic conditions, which is due to the pretreatment (drying, crushing, and sieving) of the algae before they were introduced into the digester (Montingelli et al., 2016). This mechanical pretreatment (drying, crushing, and sieving) of the algae allowed for a reduction in particle size, crystallinity, and degree of polymerization of cellulose for making the manipulation of organic charge easier; and for an increase in the surface/volume ratio, which shortened the cycle and improved digestion (Rodriguez et al., 2015).
4.2. Behaviour of the inoculum bacteria during the anaerobic digestion of algae Three algae led to an increase in anaerobic bacteria because the release of algal organic matter can enhance survival and even growth of these bacteria mainly the algal degradation provides the carbon and energy sources for the bacteria (Bouteleux et al., 2005). Some authors have confirmed that the proliferation of bacteria such as E. coli is influenced by type of chlorophyll pigment. Ansa et al., 2011; declares that the chlorophyll a has led to removal E.coli. So, the low proliferation of anaerobic bacteria by the green
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algae (Chaetomorpha linum) is due to the large amount of chlorophyll a in this specie compared to the other two algae. Pierre et al., 2011; has described antibacterial activity of a this green alga by production of sulfated galactan which inhibited the development of the anaerobic bacteria, so, the low production of biogas. At the end of incubation, we noticed that red algae (Alsidium corallinum) leads to an increase in the number of anaerobic bacteria. These big proliferation is due to the presence of agar and carbohydrates in this specie which allowed the bacterial proliferation to accelerate (Polifrone et al., 2006) and the presence of a significant amount of carbon, nitrogen and phosphorus, which are essential nutrients for growth of anaerobic microorganisms. These results correlated with the content of biogas produced by each type of algae. 4.3. Evolution of pH during the anaerobic digestion of these algae The significant decrease in pH during the anaerobic digestion of the red algae is due to an important degradation of its organic matter in volatile fatty acids (VFAs) and CO2 which led to a slight acidity of digester (Angelidaki et al., 2003). On the other hand, green algae have a low production of biogas which confirms a low production of VFAs that will be converted to biogas, resulting in a small decrease in pH. 4.4. Estimation of green energy produced by the three algae We can consider the three algae provocative of eutrophication in the Nador lagoon that are non-exploitable energy deposit (367 kWh), instead of viewing them as a potential source of pollution. These results are in agreement with several studies which demonstrated that the macroalgae are potentially a good source for bioenergy production. For this, we propose to install anaerobic algae digesters around the lagoon, mainly in algae proliferation areas (Schultz-Jensen et al., 2013). The algae will be harvested and added to the digesters to produce energy by cogeneration that will then fuel an aerator that will dissolve atmospheric oxygen inside the lagoon (Fig. 7). By employing this process, eutrophication will be inhibited and hopefully disappear. The energy produced using this method generally will be more expensive than that from fossil fuels, but it can be profitable and compete with other energy sources if rules are adopted to limit emissions, including carbon taxes and subsidies for biomass energy (Chynoweth et al., 2001). 5. Conclusion We conclude that the red alga Alsidium corallinum and brown alga Cystoseira barbata are two excellent substrates for methanation through their biogas production and the increase in anaerobic bacterial proliferation that optimized anaerobic digestion. The green alga Chaetomorpha linum produced much less biogas. These results show that these three lagoon-polluting algae (Alsidium corallinum, Cystoseira barbata, Chaetomorpha linum) are green energy producers. We combine the three Marchica algae in a digester, we can obtain a large amount of energy (367 kWh). Hence, there is a need to install an innovative plant, which includes an algae digester, for energy production and a lagoon aerator for atmospheric oxygen dissolution inside the lagoon to destroy the favourable conditions for eutrophication, thus protecting the lagoon. This pilot plant will be the topic of a future publication. Acknowledgment We deeply thank, Mr Hicham Elasri, Shokri Mahmoudi for his technical support to produce this work.
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