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The Feasibility of industrial production of Spirulina (Arthrospira) in Southern Spain
´ ´ ´ Carlos Jimenez a,*, Belen R. Cossıo b, Diego Labella b, F. Xavier Niell a
b a ´ ´ Department of Ecology, Faculty of Sciences, University of Malaga, 29071 Malaga, Spain ´ ´ ´ Algas del Estrecho, S.A., Parque Tecnologico de Andalucıa, 29590 Malaga, Spain and Centro Comercial Plaza, ´ ´ Of. 15, 29660 Nueva Andalucıa, Marbella, Malaga, Spain
Received 7 June 2001; received in revised form 5 February 2002; accepted 5 March 2002
Abstract The viability of the industrial production of three strains of Spirulina platensis was tested in Malaga, Southern Spain. In a pre-industrial trial using raceway ponds from laboratory-scale to 450 m2, all three strains displayed satisfactory growth. In a 10-month industrial trial in 450 m2 ponds, production was equivalent to 30 – 32 metric tons of dry powder per hectare per annum. In conclusion, intensive industrial production of Spirulina is viable in certain Mediterranean climates, a region previously thought to be outside its geographic limits. D 2003 Elsevier Science B.V. All rights reserved.
Keywords: Spirulina; Mass culture; Temperate latitude; Commercial production; Microalgae
1. Introduction The microalga Spirulina is produced commercially all over the world, and the dried product is a valuable food supplement (Cifelli, 1983; Belay et al., 1993). It is rich in proteins (60 – 70% by weight), vitamins (especially B12 and h-carotene), and minerals. It contains many essential amino acids and fatty acids, being one of the sources of dietary glinolenic acid (GLA). Pre-clinical and clinical studies suggest it has certain therapeutic effects (see Fox, 1996), such as reduction in blood cholesterol, protection against some cancers, enhancement of the immune system, increase of intestinal lactobacilli, reduction of nephrotoxicity by heavy metals and drugs, radiation protection, reduction of hyper*
Corresponding author. Tel.: +34-95-2134134; fax: +34-95-2132000. ´ E-mail address: jimenezÀc@uma.es (C. Jimenez).
0044-8486/03/$ - see front matter D 2003 Elsevier Science B.V. All rights reserved. PII: S 0 0 4 4 - 8 4 8 6 ( 0 2 ) 0 0 11 8 - 7
Three species now attract major commercial interest. 1987).1. Commercial production of Spirulina is today based almost exclusively on open ponds of the raceway type (Tredici et al. 1987. there is little or no production of cultures in morning hours. Spirulina was probably the most widely used in outdoor cultivation trials and there has been over four decades of intensive ecological and physiological research and development using large-scale production units. Since some of the first studies at the Carnegie Institution of Washington in the 1950s (Burlew. there has been increasing interest in the production of microalgae for commercial use. subsalsa. thus commercial cultivation has been restricted to tropical and subtropical zones. 1997). The objective of these pilot-scale trials was to produce Spirulina in a selected part of the Mediterranean region using traditional open ponds or raceways. the two principal advantages of open culture systems are a small capital investment and the use of free solar energy. although some companies use closed tubular bioreactors (Specktorova et al. In Southern Italy. 4j28VW). It is located in Southern Spain (36j42VN. platensis partially inhibited HIV-1 replication in human T-cell lines. In addition to prolonged periods of natural light. According to Chaumont (1993). as did Fornari et al. namely Chlorella. and obesity (see Belay et al. Jimenez et al.. 1982. could be developed for commercial production in temperate latitudes (Hargraves and Viquez. 1953) many aspects of the biotechnology have been developed which have led to increased efficiency in mass culture (see Richmond. but the technology is capital-intensive even though it may be justified with economies of scale. In some temperate latitudes. Shimada et al. and Langerhans cells. on . several reports have shown that S. where high temperatures are achieved during the day in summer but there are marked falls in the night. (1996) successfully demonstrated the viability of smallscale outdoor cultivation of Arthrospira (Spirulina) platensis during autumn and winter in temperate climates but using tubular bioreactors. 2. Chaumont. (1999) for the production of Spirulina. in Southern Spain. peripheral mononuclear cells. 1997). Consequently. (1998) reported that an aqueous extract of S. The location chosen was ´ Malaga.180 ´ C.. Chini-Zitelli et al. 1986. 1989). 1993).. this microalga requires high temperatures for optimal growth. However. The production site ´ The city of Malaga was selected for the pilot study for production of Spirulina.. Ayehunie et al. Closed photobioreactors allow better control of growth and have higher photosynthetic efficiencies. a estuarine/marine species.. but productivity is far below the theoretical maxima. the overall diurnal temperature range may be a suitable range for growth but the prolonged cold morning temperature is 10– 15 jC below optimum (Richmond. Materials and methods 2. / Aquaculture 217 (2003) 179–190 lipidemia. However. about 100 km east of Gibraltar Strait. 1987. 1993). Spirulina and Dunaliella. Thus. There have been several previous attempts to cultivate Spirulina in Mediterranean climates but most of them have failed (Belay. 1993). Benemann et al. it is simple technology and only practical for certain species in select environments.
Mean daily irradiance.05 mg m À 3. From 1996 to 2000. Irradiance is also high.5 107 J m À 2 day À 1 in summer and 0. the average annual rainfall was < 400 mm. The average number of sunny days per year is 328. measured by sensors in the range 280– 700 nm. The area is one of the sunniest in Europe. 1. Mean daily temperature (A) and integrated daily irradiance in the waveband 280 – 700 nm (B) at the location of the study.04 – 0. Mean daily temperatures are shown in Fig.4 107 J m À 2 day À 1 in winter. / Aquaculture 217 (2003) 179–190 181 the Mediterranean coast. averaging >1. 1B. . 1A. Fig.´ C.8 Am) in atmosphere in the vicinity of the cultivation area was 0. Average daytime temperatures normally exceeds 30 jC in summer. Jimenez et al. is shown in Fig. with >10 h of sun per day for the whole year. and the average concentration of dust particles (>0. and in winter are above 15 jC.
Each had a single paddle wheel located at one end. while the algal slurry was pumped to a Niro minor spray drier (Niro. 2.4. Jimenez et al. Compere 1968/3786 (strain B) and Laporte 1963/8579 (strain C).182 ´ C. and a spiral width of 44. These morphological differences influenced the harvesting performances. and 62 Am. This required scaling-up the volumes from 10 ml to 20 l.2:1. which were tightly coiled. M. The microorganisms Three strains of S. thus micronutrients could be avoided.2 –0.25 mm long) with low spiralization.5 mm.25 mm). These were Laporte ` M132-1 (strain A). Belgium). Agitation of the cultures was performed either by orbital shaking or by bubbling air (only for culture volumes >5 l). up to a maximum of 450 m2. platensis were provided by Prof. The first phase involved production of large volumes of the inocula in the laboratory. Harvesting and drying Before harvesting the biomass concentration was estimated by sampling and filtering 500 ml of each culture through a 62-Am mesh. Strain C also had very short filaments (0.2 – 0. Denmark) without further washing. 2. The second phase was performed outdoors using a series of raceway ponds of increasing area. Total coliforms were calculated after incubation in brilliant green bile lactose .3. All raceways had a length/width ratio of approximately 4 –4. Harvesting was performed by pumping the cultures into a Sweco LS24S555 vibrating screen (Sweco. and had a spiral width of 38.2. Strain B consisted of very long filaments (1– 5 mm long) with very low spiralization. All three strains were isolated from alkaline lakes in Chad. Strain A had short filaments (0. The filtrate was pumped back into the ponds. In these outdoors cultures Zarrouk’s original growth medium was simplified by replacing the micronutrients with technical grade fertilizers. 2. Inoculation of the raceways followed the scaling-up sequence described by Borowitzka and Borowitzka (1989). and the contents were circulated at a speed of 30 cm s À 1.4 Am.5.4 Am. Each had a different morphology as well as different temperature and irradiance optima. The depth of culture in the pond was 30 cm. The selected growth medium was that prescribed by Zarrouk (1966). Brouers from the culture ` collection of the Department of Botany of the University of Liege. Temperature control was set at 25 jC. Microbiological analysis Mesophylic aerobic microorganisms were evaluated at 31j F 1 jC in nutrient agar (Oxoid). and a spiral width of 18 Am. and weighed. and filtered through two membranes of 1. / Aquaculture 217 (2003) 179–190 2. The filter was dried at 105 jC for 24 h. Experimental design The work was developed in several phases. and light was provided continuously by fluorescent lamps. to remove insects and other undesirable material.
Real Time Computer. 2. positive tubes were confirmed by means of selenite – cystine broth. Climatic measurements Solar irradiance and temperature were measured on a permanent basis using a dosimeter (Eldonet. 2. positive tubes were incubated in Levine agar for the estimation of Escherichia coli. molds and yeasts were estimated through the Sabouraud dextrose agar method. The data were continuously stored on the computer. Jimenez et al. platensis tested during the laboratory phase of this study. / Aquaculture 217 (2003) 179–190 183 broth (BGBL). 315 –400 nm. for Clostridium perfringens sulfite polymixine sulfadiazine agar (SPS) was used. 280– 315 nm. Results 3. Mohrendorf. 2. For solar irradiance ¨ the instrument took readings in three wavelength bands (UV-B. 400– 700 nm) at intervals of 1 s. UV-A.1.6. Intrinsic growth rate (rmax) was calculated for the Fig. Germany). Evolution of the optical density at 680 nm of the three strains of S. and PAR. Finally. Details of the culture conditions may be found in the text. . Laboratory trials During the laboratory phase. strain B (Compere 1963/ 8579) grew faster than the other two.´ C. Presence of Staphylococcus aureus was evaluated by using the Giolitti – Cantoni broth. 3. The dosimeter also had temperature sensors and the data were also collected and stored. the growth of each of the three strains was monitored by ` measuring the optical density at 680 nm. Estimation of Salmonella was performed using Rappaport – Vassiliadis soya peptone (RVS) broth. As shown in Fig.
500 l) and 450 m2 (135. Strain B did not support the same level of production as the other two and there was a continuous decrease of biomass concentration in those particular ponds. All three strains were inoculated in the open raceway ponds of 1. 3. which gave figures of 0.5 m2 (1350 l). the growth rate averaged 0. 0. This was valid for an estimation of biomass through variation of the O. 6.350 l of capacity in August 1997. due to the absorption of phycobilins and chlorophyll a. and 0.2. and productivity was 9.D. platensis in 1350-l open raceway ponds. 45 m2 (13. at 565 and 680 nm.4.26 doublings day À 1 for strains A. First. During this period. and 0. as culture density increased cells acclimated to reducing irradiance by increasing their pigment content. First outdoor trial The open raceway ponds had increasing surface areas of 4. Strain C suffered an initial decrease of biomass concentration when harvesting first took place but it Fig. the high ` light absorption at 680 nm by strain Compere 1963/8579 did not correlate with a high biomass content. Biomass concentration of S.3. and 6.15 doublings day À 1 for strains A. variation of the optical density of the cultures was not a good estimation of the biomass for two reasons. B. operated at a depth of 30 cm from August 1997. B and C. In particular. respectively. and C. respectively. However. 3) and continued until October.28. Second. Harvesting commenced after 12 –15 days (Fig.36.184 ´ C. 3. due to the different morphology of the strains some showed higher light absorption even if the biomass content was low.6 g DW m À 2 day À 1.000 l). respectively. 0. . / Aquaculture 217 (2003) 179–190 exponential phase of growth.09. Jimenez et al.18.
3. Jimenez et al.500 l).17 doublings day À 1 for strain C.13 doublings day À 1. Growth rate for the first 13 days after inoculation was 0.03 2. were also inoculated with strains A and C in August.3 Strain C 10.3.7 All cultures were operated at a depth of 30 cm (13.500-l capacity. / Aquaculture 217 (2003) 179–190 185 Fig. and yield.81 Strain B 7. subsequently stabilized with values around 130 g m À 2 for the rest of the harvesting season. harvesting performance. Two of the larger raceway ponds. strain A was selected for extended cultivation in this pond.500-l open raceway ponds operated at a depth of 30 cm. . Based on the previous data.´ C.6 7. 4. Growth and biomass concentration of S.19 doublings day À 1 for strain A and 0. 1997 and the pond was in continuous operation until July 29. and daily harvesting comTable 1 Biomass yield of the Spirulina strains in the 45 m2 open raceway ponds Month September October November December Strain A 10. During this period the biomass concentration in the pond ranged from 85 g DW m À 2 in winter to 140 g DW m À 2 in summer. Second outdoor trials The second trial used a single open raceway pond of 450 m2. Both ponds were harvested daily and the results showed productivities of 10. Inoculation took place on September 23.7 9. 4. platensis in 13. Table 1 shows the results of the biomass yields during the different months of operation. Details of biomass yield are shown in Table 1. and their biomass concentrations are shown in Fig. Both displayed satisfactory growth.7 g m À 2 day À 1 for both strains in September. of 13. with an intrinsic growth rate of 0. 1998.
/ Aquaculture 217 (2003) 179–190 Fig. and during the winter months the concentration fell to around 85– 90 g DW m À 2. For 10 months. menced. . Monthly average productivity of S. In the spring and summer months it reverted back to about 120 g DW m À 2. platensis Laporte M132-1 in a 450 m2 open raceway pond. 5. Harvesting the biomass was only stopped for 17 days in February when there was a period of local heavy rains. In October and November. Daily biomass yield (in g DW m À 2 day À 1) of S. platensis Laporte M132-1 in a 450 m2 pond during the feasibility study. the biomass concentration averaged ca.186 ´ C. Fig. 6. the pond was never emptied or renewed. Jimenez et al. Temperatures of the culture ranged from a minimum of 12 jC in winter to a maximum of 28 jC in summer. 120 g DW m À 2.
1997).8 g kg À 1. ca.9 1.4.1 Standards 140 6. averaging 2 g DW m À 2 day À 1. They could be considered as negative. Sweden and Spain). France.S. All values < 3 were below the detection limit of the MPN method. estimated through the standard plate count at 31 jC (Table 2).9 55 – 70 4–7 6 – 13 9 <3 <3 <3 <3 <3 40 <3 7.1 – 10 3. For other Table 2 Results of the analysis of the dry powder of Spirulina Strain A Composition Phycocyanin (g kg À 1) Chlorophyll (g kg À 1) Carotenoids (g kg À 1) h-Carotene (g kg À 1) Proteins (%) Moisture (%) Ash (%) Microbiology Mesophylic microorganisms SPC ( Â 103/g) Total coliforms MPN/g Escherichia coli MPN/g Staphylococcus aureus MPN/g Clostridium perfringens MPN/g Salmonella MPN/g Mold (#/g) Yeast (#/g) 60.9 g kg À 1. averaging only 47% on a dry weight basis. The results are given in Table 2.´ C. The total carotenoid and chlorophyll a concentrations averaged 6 and 7. 1996. averaging only 58.0 2. Microbiological analysis gave low concentration of mesophylic bacteria (7. 5 summarizes daily biomass harvesting from a pond 450 m2 in surface area. Jimenez et al. with values over 15 g DW m À 2 day À 1. 6 shows the average productivity of the pond in the 10-month trial period. < 100 – < 1000 SPC—standard plate count. respectively.2 g DW m À 2 day À 1 in a 365-day cycle. Extrapolating the data from the successful operation of a 450 m2 pond. Phycocyanin concentration was below the standards.000 l) and average production of 8. Japan.0 6.7 6. MPN—most probable number.9 21. Neg. . Microbiological standards resume the regulations of several countries (e. 3.. U.6 5..5 – 1. Peak productivity occurred in July.A.9 47. The moisture accounted for 6– 7% and the ash content was high. Fig. The protein content was low. Composition standards have been taken from several sources (Fox. Belay. / Aquaculture 217 (2003) 179–190 187 Fig. Neg.2 6.4 6.5 <3 <3 <3 <3 <3 30 <3 50 < 10 Neg.9 9. with an operational depth of 30 cm (135.5 Strain C 56.0 19. Analysis of the algal powder Several samples of the dry biomass of Spirulina harvested during the period of operation of the 450 m2 pond were analysed for cell composition and for microbiological standards. The lowest productivity occurred in January and February.1 47.5 – 9 103 bacteria g À 1).7 1. Neg. 20%. the annual productivity would be 30 metric tons of dry weight product per hectare of surface area.g.
Outdoors the minimal temperature that permits growth is around 18 jC and the culture deteriorates quickly when maximum daytime temperatures are lower than 12 jC (Richmond. in this case. At 15 jC. different strains of Spirulina differ in their optimal growth temperature. according to Vonshak and Tomaselli (2000). typical values 60– 65%). This process normally reduces the ash content. Winter temperature of the cultures in fact averaged 12 jC. / Aquaculture 217 (2003) 179–190 analyses. 4. when estimating humidity. platensis was successfully cultured at temperatures as low as 9 jC. gives an average humidity content of the dry powder of 4 –5%. leading to a wide range of values. 1997). the algal slurry obtained from the filtering unit was introduced directly into the spray drier without acid washing. and ca. ´ The results of these trials at Malaga indicate that outdoor cultivation of Spirulina is satisfactory at temperature above 15 jC. and the cultures did not deteriorate at ambient winter temperatures. This work describes the results of a pilot study for commercial production of Spirulina in open raceways in Southern Spain. However. In these trials S. and 110 jC for 2 h. Belay. acid washing is necessary to eliminate them. . which is high (typical values are 5– 7%). Richmond (1986) concluded that minimal temperatures for production of Spirulina was 18 jC. However. which. several temperatures are used. Temperature in the outdoor cultivation ponds never exceeded 28 jC at midday. ash content was around 20%. who presented data on several Spirulina isolates with optimal growth temperatures ranging from 24 to 42 jC. etc. The calculation of the protein content as ashfree dry weight would give values of 60%. which had concentrations of 40 colonies g À 1 for strain A and 30 colonies g À 1 for strain C. Discussion Spirulina is a thermophilic microorganism with an optimal growth temperature of 35– 37 jC. However. Belay (1997) reported two unsuccessful attempts in Israel and another in Southern Spain. which supported a biomass yield of 2 g DW m À 2 day À 1. at a latitude of 36jN. Several previous attempts have been made to cultivate Spirulina in Mediterranean climates in open raceways but without success.. 65 jC to constant weight. As the growth medium is highly enriched with bicarbonate.188 ´ C. it is more appropriate to determine humidity at 65 jC to constant weight. Jimenez et al. the small deviations can be explained. The above normal high value of ash content must be considered an artefact. all results were in the detection limit of the most probable number (MPN) method with the exception of the molds. 105 jC for 24 h. In the analysis of the chemical composition of Spirulina dry powder produced in the pilot study. 8 g DW m À 2 day À 1 was produced at 18 jC by one of the three strains tested. Another large unit of 5000 m2 in Southern Spain is also reported to be undergoing some difficulty. and the protein content was low (47%. These practical requirements mean that commercial cultivation is restricted to tropical and subtropical areas around the world. and proper acid washing of the slurry would produce the more typical values of 5 –7%. the yield averaged 6 g DW m À 2 day À 1. several figures differed from those of the standard composition (see Fox. For example. 1986). 1996. According to the methodology adopted by the food industry. Similarly. for example.
H. M. Borowitzka. T. The average 12-month productivity is about 8. Spirulina platensis (Arthrospira): Physiology. in the analysis of the dry powder (Table 2). the high ash content. 1998. J. J.C. A. Phycol. together with the high humidity make the protein content lower than expected.. Inhibition of HIV-1 replication by an aqueous extract of Spirulina platensis (Arthrospira platensis). the only component lower in concentration than expected was phycocyanin (typical values 140 g kg À 1). U.1450 between the ´ Department of Ecology of the University of Malaga and Algas del Estrecho. 593 – 604.1154 and 8. (Ed. Sergio Canete supplied the data on dust particles in the atmosphere. / Aquaculture 217 (2003) 179–190 189 Therefore.). (Ed. 131 – 158. K. Belay. 5. 18.A. Current knowledge on potential health benefits of Spirulina. All microorganisms were below the norms required by the strict regulations for members of the European Union. 5. Phycol. Conclusion From a scientific and technical point of view. project AMB99-1088. 5.. Acquir. Ruprecht. Rees.M. Borowitzka. 294 – 316.. and Japan (Belay. Immmune Defic.. However. Baba. Shimamatsu. 1953. Biotechnology of algal biomass production: a review of systems for outdoor mass culture.´ C. which would yield a production of 30 metric tons Ha À 1 year À 1. pp. 1997). J.. There is no obvious explanation for this lower value but again it is found to vary highly between different strains of Spirulina and more research at a production level may be necessary to help understand variations in phycocyanin content.)...W. Cell-Biology and Biotechnology Taylor & Francis. Algal Culture from Laboratory to Pilot Plant. R. Acknowledgements This work was supported by contracts 8. Most concentrations were in fact below the level of detection of the approved microbiological techniques. pp. 5. Syndr. 235 – 241. Carnegie Institution of Washington.. Jimenez et al. Benemann. Longman.. USA.06/44..C. T. Burlew. UK. 1987.2 g DW m À 2 day À 1. Weissman. Human Retrovirol. mass production of Spirulina in open ponds is viable under the climatic conditions of Southern Spain for a period of 9 months per year. Miyakawa... R. S.. Industrial production: methods and economics. References Ayehunie. J. Tillett.S. Appl. Shah. A. 1993. D.. A. (Eds. Belay.3 g DW m À 2 day À 1.06/44. A. Mass culture of Spirulina outdoors—the Earthrise Farms experience. 1989. In: Creswell. In: Vonhask. Belay.A. and by ˜ the CICYT.R. 7 – 12. 47 – 53. 1993.K. . Algal and Cyanobacterial Biotechnology..). London. J. The potential average productivity for this period is of the order of 10.M. Tibtech... from March to November. L. Chaumont. S. All the analyses carried out gave values averaging 6% by weight (60 g kg À 1). Ota.V.J. Washington DC. N. Dr. Y. 1997. Appl. Microalgae biotechnology.. Microbiological analyses confirmed that the dry powder passed the necessary sanitary control regulations to qualify the product as food for human consumption. J. D..
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