Recent Trends in the Mass Cultivation of Algae in Raceway Ponds

Renewable and Sustainable Energy Reviews 51 (2015) 875–885

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Renewable and Sustainable Energy Reviews

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Recent trends in the mass cultivation of algae in raceway ponds

Kanhaiya Kumar a,n, Sanjiv K. Mishra a, Anupama Shrivastav a, Min S. Park a, Ji-Won Yang a,b,nn a Advanced Biomass R&D Center, KAIST, 291 Daehak-ro, Yuseong-gu, Daejeon 305-701, Republic of Korea b Department of Chemical and Biomolecular Engineering, KAIST, 291 Daehak-ro, Yuseong-gu, Daejeon 305-701, Republic of Korea article info abstract

Article history: Algal technology has potential to combat the global energy crisis, malnutrition, and production of several Received 2 February 2015 value added products useful for the mankind. The cost effective cultivation system is the basis to realize Received in revised form this goal. Microalgal production in raceway ponds seems to be most promising, especially in the large 11 May 2015 scale. Several environmental (location of the cultivation system, rainfall, solar radiation, etc.), engineer- Accepted 29 June 2015 ing (pond depth, CO delivery system, methods of mixing, power consumption, etc.), and biological Available online 21 July 2015 2 (light, pH, oxygen accumulation, salinity, Algal predators etc.) parameters affect the biomass productivity Keywords: in the open pond system. Vertical mixing is an important criteria inﬂuencing the algal growth compared Mixing to axial mixing as it determines the frequency by which cell will travel from bottom (dark zone) to CO delivery 2 surface (light zone) of the open pond. Therefore, different research works on the various designs of Raceway pond design raceway ponds were mostly focused towards enhancing the vertical mixing (e.g. Design of bend and

surface geometry, engineering ﬂow ﬁeld, etc.) and CO2 residence time (e.g. Closed, sump, airlift driven raceway ponds etc.). The present study summarizes the current state of knowledge for the biomass production in raceway ponds. & 2015 Published by Elsevier Ltd.

Contents

1. Introduction...... 876 2. Raceway ponds ...... 877 2.1. General factors affecting the raceway pond productivity ...... 877 2.1.1. Choice of location ...... 877 2.1.2. Pond depth...... 878 2.1.3. Power consumption...... 878 2.1.4. Mixing ...... 878

2.1.5. CO2 delivery into the raceway pond ...... 878 2.1.6. Light...... 879 2.1.7. Oxygen accumulation ...... 879 2.1.8. Salinity ...... 879 2.1.9. Algal predators...... 879 2.2. Raceway pond design ...... 880 2.2.1. The raceway pond with manual mixing ...... 881 2.2.2. Paddle-wheel driven raceway ponds ...... 881 2.2.3. Design of bend and ﬂoor surface geometries of raceway ponds ...... 881 2.2.4. Sump assisted raceway ponds...... 882 2.2.5. Split sump with a central bafﬂe/airlift driven raceway ponds...... 882 2.2.6. External carbonation column ...... 883 2.2.7. Closed raceway ponds ...... 883

n Corresponding author. Tel.: þ82 10 6464 8310; fax: þ82 42 350 3910. nn Corresponding author at: Department of Chemical and Biomolecular Engineering, KAIST, 291 Daehak-ro, Yuseong-gu, Daejeon 305-701, Republic of Korea. Tel.: þ82 42 350 3924; fax: þ82 42 350 8858. E-mail addresses: [email protected] (K. Kumar), [email protected] (J.-W. Yang). http://dx.doi.org/10.1016/j.rser.2015.06.033 1364-0321/& 2015 Published by Elsevier Ltd. 876 K. Kumar et al. / Renewable and Sustainable Energy Reviews 51 (2015) 875–885

2.2.8. Engineering ﬂow ﬁeld...... 883 2.2.9. Hybrid raceway ponds...... 883 3. Commercial open ponds ...... 883 4. Conclusions ...... 883 Acknowledgments...... 884 References...... 884

1. Introduction (http://www.algatech.com/technology.asp). This company grows Haematococcus pluvialis for the production of astaxanthin. The Currently, the world is facing many challenges: global warming, company claims stable climatic condition with high sunlight malnutrition, increasing energy demand are some of them. Algal intensity make them ideally positioned for the algal cultivation. technology is an emerging field, which has potential to combat The mass production of microalgae was started in the early these problems. Microalgae transform gaseous CO2 into their 1950s using Chlorella sp. in Japan. Oswald coined the term high cellular components such as carbohydrates, lipids, and proteins rate algal ponds (HRAPs) for the open and shallow raceway design in a process called photosynthesis. In this way, microalgae help in having a large scale recirculating system [13]. Since then, raceway mitigating the effect of global warming by capturing the CO2 from ponds are being utilized mostly for algal cultivation and waste- the earth's atmosphere [1,2]. Microalgal biomass is rich in protein, water treatment [14]. Generally the four major open systems can and many value-added products having nutraceutical, cosmetic be used for the algal cultivation: shallow big ponds, tanks, circular and pharmaceutical importance [3–5]. These are the sources of ponds, and raceway ponds (RWPs). Each of them has its own Bioenergy such as biohydrogen, biodiesel, bioethanol, biogas etc. characteristic features. The choice of the open cultivation system [1,3–5]. In microalgae, energy condenses in the form of either depends upon types of algal species, local climatic conditions, and starch or triacyglycerides (TAGs) as lipid droplet. Lipids of micro- the cost of lands and water [15]. Open ponds preference is due to algae can be further converted into biodiesel by transesterification. their small capital investment, free solar energy, and the low Microalgae is superior in terms of biomass and biodiesel energy required for mixing, which may be order of as low as yield compared to terrestrial energy crops. Biomass productivity 4Wm3 [3,16]. of energy crops such as soybeans, corn, switch grass is Today, most of the large scale algal biomass production facility 3Mtha1 year1, 9Mtha1 year1, and 10– is based on RWPs and this accounts for nearly 95% of the total 13 Mt ha1 year1, respectively [6]. Therefore, cultivation of worldwide algal production [3]. For example, high value products energy crops is less attractive compared to biomass producti- such as astaxanthin has been produced in raceway ponds of vity of microalgae: 50–70 Mt ha1 year1 in open ponds and 20,000 L capacity [17]. In fact, RWPs use the simplest form of algal 150 Mt ha 1 year1 in photobioreactors [6]. Algal lipid produc- cultivation [18]. Raceway pond was found better compared to tion rates per unit area are several orders of magnitude higher circular pond [19]. On the basis of the cost of production, average than the conventional biofuels feedstocks [7]. For example, poten- lipid production cost in open ponds (12.73 USD per gallon) is tial oil production from the rapeseed grown in U.K is 1.5 t ha 1, significantly lower compared to that of photobioreactor (31.61 USD which is much lower than the microalgae-derived biodiesel of per gallon) [20]. This indicates the financial feasibility of lipid magnitude 40 t ha1 in a large scale open pond [6]. In addition, production in open ponds. Further, Stephenson et al. conducted algal biofuel has a higher heating value of 41 K J Kg1 [8]. the life cycle assessment (LCA) and concluded that the global Algal cultivation is one of the technological thrust areas, which warming potential (GWP) for algal based biodiesel obtained from has a huge market potential for biodiesel as well as other valuable RWPs is nearly 80% lower than the fossil-derived diesel [21]. biochemicals. An estimation by Chisti calculates that energy Contrary to this, GWP was significantly higher for the biodiesel consumed during algal cultivation is nearly 28% of the total obtained from an airlift photobioreactor compared to fossil- biodiesel production cost from microalgae [9]. Open ponds and derived diesel [6]. A comparative evaluation of the performance closed photobioreactors (PBRs) are used for the algal biomass of open pond and photobioreactor has been shown in Table 1. production. Both of them have their own advantages and dis- Raceway ponds are intended to cultivate selected microalgae advantages. Photobioreactors have merits of having significantly growing only in selected environments [18]. Some of the micro- higher volumetric algal productivities (0.2–3.8 g L1 d1) com- algae and cyanobacteria generally cultivated in RWPs are Nanno- pared to those of raceway ponds (0.12–0.48 g L1 d1) [10,11]. chloropsis sp., Chlorella sp., Tetraselmis sp., Arthrospira platensis, Closed PBRs prolong the gas retention time and improve the mass Dunaliella salina, Scenedesmus sp., Haematococcus pluvialis, Ana- transfer efficiency. For example, airlift reactors have advantages baena sp., Phaeodactylum tricornotum, Micractinium sp., Actinas- such as high volumetric mass transfer rate of CO2,efficient mixing, trum sp. etc [3,16,22]. Some of them can make large settleable light/dark cycle, light utilization etc. In addition, closed PBRs offer colonies and bio-floccs helpful in harvesting by gravity sedimenta- greater control over process parameters. tion [22]. Land cost in Australia is cheaper than the USA and Israel. Closed PBRs also have several disadvantages, which limit their Therefore, an Australian company, Betatene Ltd. produces D. salina use for commercial scale. The gas exchange requirement limits PBR in very large ponds (up to 250 ha) having no facility for mixing scale-up to 100 m2 compared to 10,000 m2 in case of open ponds [15]. However, USA and Israel based companies generally use well [12]. The operation and cleaning of thousands of individual PBRs mixed RWPs for the cultivation of microalgae such as Dunaliella sp. are laborious, costly, and time consuming. The cost of commercial CO2 addition in RWPs is necessary to achieve high cell density. PBR is 100 times higher than open ponds. The water and energy However, maintaining high alkaline condition in open ponds is consumption, total actual area occupied by the PBR, and the sufficient for the cultivation of Spirulina sp. In Trebon, Czech problem of long term resistance to contamination are other Republic, algal cell density as high as 10 g L1 is also reported in disadvantages of PBR [12]. Algatechologies, Israel is the probably open air system, but having less than 1 cm culture depth [15]. only commercially successful company, operating modular array of The commercial scale biodiesel production by microalgae is tubular PBR of 300 km long, and occupying 10 acres of desert land possible by minimizing the cultivation cost near to $0.25 per kg of K. Kumar et al. / Renewable and Sustainable Energy Reviews 51 (2015) 875–885 877

Table 1 Comparativea study of the performance of open pond and photobioreator.

Items Open pond Photobioreactor References

Photoconversion efﬁciency 1.5% 5% [8] Biomass concentration 0.5–1Kgm3 2–9Kgm3 [8] Speciﬁc energy demand for cultivation 0.5–4Wm3 2.5–15 W m 3b [8] Maximum possible energy yield (biodiesel and biogas) 81 MJ m2 year1 269MJ m2 year1 [8] Energy (power and heat) demand 57 MJ m 2 year1 207MJ m2 year1 [8] Cost of algal biomass 2.66 $ Kg1 7.32 $ Kg1 [24] Average lipid production cost 12.73 $ per gallon 31.61 $ per gallon [20] Volumetric algal productivities 0.12–0.48 g L1 d1 0.2–3.8 g L1 d1 [10,11] Scale-up capacity 10,000 m2 100 m2 [12,24] Worldwide large scale production facility 95% 5% [3] Global warming potential (GWP) Lower than the fossil-derived Higher than the fossil-derived [6,21] diesel diesel Algal species used in cultivation Selective All [18] Operation, maintenance and cleaning Easy Laborious, costly, time [12] consuming Investment and construction cost Small 100 times higher [12] Land requirement High Depends [24] Light energy requirement Free Costly [3,16] Energy requirement for mixing Low Depends [3,16] Harvesting cost High Medium [24] Surface to volume ratio High Very high [24]

Increase in O2 concentration Low Very high [1,24] Weather dependence (Fluctuation in light, and temperature), evaporative water loss, High Low [1,24] contamination

a Numerical values are for comparison purpose only. Several researchers have obtained different numerical values as well. b Assuming power input and volume to surface ratio of photobioreactor is in the range of 50–150 W m 3 and 0.05–0.1 m, respectively [8]. dried algal biomass having high lipid content (Z40% w/w). In nutraceutical food market or biofuel sector. Raceway ponds are a addition, there should be provision of nutrient recycling, adequate broadly used technology for algal cultivation. Raceway ponds have and feasible supply of CO2, and energy recovery from the spent shallow configuration. This is necessary to prevent light limitation biomass [23,24]. However, the lower areal productivity of RWPs is inside the culture. However, this limits the areal productivity of one of the challenges. Brennan and Owende reported that theore- the reactor and scale up of the raceway ponds can only be done by tically areal productivity of RWPs can be no more than increasing the footprint. The lower depth of RWPs reduces the 40 g m2 d1 equivalent to 146 t ha1 year1 [11]. However, in efficiency of the sparger due to less gas–liquid contact time. This general areal productivities are much lower. Biomass productivity combines with poor CO2 mass transfer efficiency leading to in open ponds has been reported in the range of 20– process inefficiency and loosing most of gas in the atmosphere. 1 1 110 t ha year . Chisti opined a maximum annual average algal This loss may be as high as 80–90% of the bubbled CO2 [31,32]. 1 1 biomass productivity of 86.7 t ha year in the open pond Similarly, some reports suggest CO2 fixation efficiency ranged from located at more suitable climatic conditions [23]. In terms of 10% to 30% in the open ponds [4]. average annual productivity, RWPs have been observed to produce between 16 and 19 g m2 d1 algal dry cell weight [25]. Similarly, maximum biomass productivity of 21 g m2 d1 and 2.1. General factors affecting the raceway pond productivity 13.2 g m2 d1 were obtained in case of Spirulina [26] and Chlorella [27], respectively. Handler et al. tabulated algal growth 2.1.1. Choice of location rate based on different reports and it was found to vary in the The first thing is to consider the choice of location of RWPs as range of 5–45 g m2 d1 on the basis of foot print [7]. In terms of many local environmental and logistic factors influence the overall power consumption, biomass productivity was reported in the feasibility of the process. These factors are rainfall, solar radiation, range of 0.1–0.69 g W1 d1 [28]. local temperature, land slope, potential nutrient sources, cost of Previously, several modifications in RWPs were carried out such as the water and land, etc. For example, the location having rainfall use of airlift pumps, mixing boards, Archimedes screws, and mechan- not more than 1 m per year was considered desirable for con- ical pumps, etc. Installations of flow deflectors, rectifiers, gilded vans, structing open ponds [33]. This is important as too much rainfall modifying the islands or bend design are some of the other increases the chances of culture dilution. Moreover, location approaches adopted to improve the mixing pattern in RWPs [29]. should not be at flood affected area. An increase in the dilution However, they have higher operating costs and inflexibility during enhances the harvesting cost and decreases the salinity undesir- operation despite having a relatively good efficiency [30]. able for the marine microalgae. It is desirable to construct RWPs The present study summarizes the detail study of the present state near the seashore because of the availability of the plenty of saline of art in RWPs. The focus has been given to discuss the various factors water for the cultivation of marine microalgae such as Tetraselmis affecting the algal growth in general open ponds, and the different sp. Minimum solar power radiation of 4.65 kW h m2 d1 was designs studied to improve the performance of the RWP. found necessary for establishing open ponds for algal cultivation [33]. In many countries, the operation of raceway ponds is not possible throughout the year. This is because in the winter season, 2. Raceway ponds solar radiation and temperature drop to an unacceptable level for the growth of microalgae. Land having slope not more than 5% was The recent scenario in the area of algal research is heading considered desirable to avoid significant earth moving costs towards the demonstration scale of cultivation, either it is during pond construction [33]. 878 K. Kumar et al. / Renewable and Sustainable Energy Reviews 51 (2015) 875–885

Similarly, the choice between an indoor or outdoor cultivation during the night and even in winter season to minimize the is also important. An indoor environment has several advantages operational cost [30]. over an outdoor environment for running RWPs. For example, it Mixing in RWPs was found to occur mainly near the sump, prevents decrease in salinity and dilution of biomass due to rain paddlewheels and bends with maximum dispersion coefficient of fall and precipitation and increase in the salinity due to evapora- 0.07 m2 s1 [3]. Culture velocity is generally kept between 5 and tion of water during the summer time. Further, in the winter 30 cm s1 depending upon the size of RWPs with larger ponds season, indoor RWPs enjoy relatively higher culture temperature requiring higher velocities. Mixing is conventionally measured by (nearly 4 1C) than the outside environment [34]. Indoor RWPs the Reynolds number (Re), where high Re number indicates better have the disadvantage of receiving nearly 20% less transmission of mixing of the culture. The high Re number means turbulent flow, light. However, overall indoor RWPs have been found to have which in turn also causes vertical mixing. However, good level of higher productivity due to partial control over salinity and turbulence determined by Re may not necessarily have sufficient temperature [34]. mixing in the vertical direction [37]. Even liquid having high turbulent flow can have poor vertical mixing and low levels of 2.1.2. Pond depth horizontal turbulence can have better vertical mixing [37]. Vertical Pond depth of RWPs greatly influences the environmental and mixing is an more important criteria compared to axial mixing in engineering parameters such as temperature, light utilization RWPs. At this culture velocity, axial mixing in RWPs is comparable efficiency, mixing, and power consumption by the paddle wheel. to photobioreactor. Vertical mixing in RWPs is very poor compared fi Ponds depth determines the amount of light and frequency of algal to closed photobioreactor. It is de ned as cyclical movements of cell exposed to optimal light [35]. Generally areal productivity the liquid between the bottom (dark zone) and the surface (light increases with an increase in the pond depth. For example, areal zone) of the open pond [5]. Long straight region of RWPs is the productivity increased nearly 134–200% in algal ponds at a depth poorest zone in terms of vertical mixing. Whereas, at the bend fl of 40 cm compared to 20 cm depth ponds [35]. Further, microalgae vertical mixing is maximized due to vortex generated by the ow fl in the deep HRAP was found more efficient in ammonia uptake separation [5]. Baf es in RWPs increase the vertical mixing usually and photosynthesis efficiency [35]. Ponds depth also regulates the at the cost of energy dissipated in the axial direction [3]. temperature gradient inside the algal culture. For example, temperature variation in 10 cm ponds is nearly two times higher 2.1.5. CO2 delivery into the raceway pond compared to 50 cm ponds. This was one of the reasons for higher Cost of the carbon source in the algal medium ranges from 8– annual areal productivity in 50 cm depth RWPs at Algeria com- 27% of the daily production cost [4]. Similarly, in another report pared to 10 cm pond depth. However, the same effect was less cost of supply and transfer of CO2 accounts for nearly one third of significant in RWPs located in the Netherlands compared to the total algal cultivation cost [28].CO2 concentration of at least Algeria [36]. 65 μmol L1 at a pH of 8.5 was found optimal for the high Contrary to above findings, in some reports increasing the pond productivity of some microalgae [32]. Contrary to this, studies of 1 depth was not found significantly improving the areal biomass Li et al. reveals that CO2 concentration greater than 73 μmol L at productivity. For example, areal biomass productivity for Tetra- a pH of 8 is required for the normal growth of microalgae [4]. The selmis suecica F&M-M33 and Nannochloropsis sp. F&M-M24 were differences in the estimated values may be due to use of two 8.37 g m2 d1, and 14.1 g m2 d1 in 15 cm depth RWPs, which different types of microalgae in the study. Surface aeration is the 2 1 2 1 were comparable with 8.9 g m d and 10.44 g m d in primitive way by which CO2 diffuses into the algal culture. This has 5 cm depth RWPs, respectively [37]. In fact, low depth RWPs were the disadvantage of poor residence time to the gas bubbles leading considered more energy efficient with better biomass productivity to the poor CO2 utilization efficiency of the algae. Additional CO2 per unit energy consumption. delivery is required even in the open ponds running using wastewater. This is because C:N ratio in the algal cells ranges from 6 C:N 2.1.3. Power consumption to 8 C:N [38], which is much higher compared to general C:N ratio Specific power consumption depends upon the depth of RWPs, of the wastewater (3 C:N). Therefore, it is imperative to provide presence of baffles and paddlewheel speeds. This was found in the CO2 additionally into the culture [11].CO2 delivery in the open range of 1.5–8.4 W m3 [3]. Specific power consumption was pond depends upon culture pH, mixing, volumetric mass transfer fi – minimized when the RWP was operated at the depth of 20 cm. coef cients, liquid velocity, gas liquid contact time, type of the The reduction in water head was found to conserve the energy sparger etc. losses [37]. Introduction of baffles generally increases the specific power consumption [3]. Therefore, it is important to understand 2.1.5.1. Effect of culture pH. Rate of absorption of CO2 in the that too many baffles can decrease the overall performance of medium is accelerated by increasing the pH of the medium. At

RWPs [3]. alkaline pH, CO2 is absorbed because of the reactions taking place between hydroxyl ions and CO2 to produce bicarbonate. However, – 2.1.4. Mixing the optimal pH of most of the algae is in the range of 7 8 [39]. Provision of having adequate mixing is the major concern in Therefore, CO2 delivery in the raceway pond by a chemical RWPs. Mixing accounts for the nearly 69% of the total utilities cost reaction is limited as the bicarbonate formation dominates at pH fi [29]. Optimal mixing in RWPs can enhance the algal productivity values above 10. de Godos et al. reported a suf cient mass transfer by nearly 10 fold [29]. Mixing serves several purposes such as rate for the actively growing algal cells at pH 8 [14]. Spirulina sp. fi periodic exposure of cells to sunlight, keeping cells into suspen- are generally grown in RWPs as they ef ciently grow at pH greater sion, availability of the nutrient to algal cells, removal of photo- than 10 thus minimizing the chances of contamination. In some synthetically generated oxygen etc [5]. Mixing is important to cases, CO2 in the form of carbonate is used as the carbon source. avoid photolimitation and photoinhibition and enhances the light utilization efficiency [37]. However, unnecessarily mixing should 2.1.5.2. Geometry of diffusors. Membrane tube diffusers, plate be avoided. For example, biomass losses have been experienced in diffuser, and porous tubing diffuser are commonly used for the the absence of light [30]. This may be up to 25% during the night. introduction of CO2 into RWPs. Each of the diffuser has its own Therefore, it was recommended to reduce the mixing velocity merits and demerits. For example, membrane tube diffuser K. Kumar et al. / Renewable and Sustainable Energy Reviews 51 (2015) 875–885 879

generates small bubble size but high pressure drop, plate diffuser photosynthesis by respiration. High partial pressure of CO2 and O2 gives the smaller bubble size with low pressure drop, and porous activates carboxylase and oxygenase activity of RuBisCO, respectively. tubing diffuser generates medium size bubbles with low pressure Therefore, under high partial pressure of oxygen, RuBisCO enzyme drop. Small size bubbles helps in high volumetric mass transfer (participating in Calvin cycle) shifts towards catalyzing the oxygenase coefficient irrespective of pressure drop [3]. Similarly, Merriman reaction.ThisisbecauseRuBisCOaffinity constant for oxygen (Km)is et al. compared the bubbling of CO2 through open tube, through nearly 700 times lower than its Km for CO2 [1].Theoxygenasereaction porous diffuser, and through the hollow fiber membrane (HFM) produces undesired Glycolate 2-phosphate as the end product, which manifold and found HFM as a far superior method of CO2 is formed at the cost of consuming significant amounts of cellular introduction especially at the shallow depth [40]. It enhances the energy. The catabolism of Glycolate 2-phosphate releases glycine, surface area over which mass transfer can occur. HFM has a high which on condensation with another glycine molecule produces surface to volume ratio and produces small bubbles. In addition, it serine, resulting in the loss of CO2 [44]. The release of previously generates low pressure drop and unused gas can be recirculated fixed CO2 has been estimated up to 50% of the algal biomass [1,45]. thus minimizing the production cost [40]. The performance of the The regeneration of ribulose-1,5-bisphosphate, the starting compound hydrophobic membrane used in HFM was found superior of the Calvin cycle is compromised due to loss of fixed carbon. compared to the hydrophilic [41]. In RWPs, maximum dissolved oxygen concentration was found An increase in the liquid velocity is another method by which in the range of 25 mg L1–30 mg L1 in summer, when the solar

CO2 mass transfer can be enhanced. An increase in the turbulence radiation was at peak during noon time [18]. In Spain during reduces the liquid layer and thus decreases the mass transfer winter time when the solar radiation was low, the maximum O2 resistance and increases the mass transfer coefficient. concentration was 10 mg L1 [18]. This was found to increase to as high as 500% in larger ponds [26]. It has been observed that the increase in oxygen concentration greater than 25 mg L1 had a 2.1.5.3. Volumetric mass transfer coefficients (Kla). Mendoza et al. negative impact on the biomass productivity [18]. Therefore compared the KlaofCO2 at different sections of the raceway pond and at two different modes of mixing: paddle wheel, and sump mixing may be necessary to drive out produced oxygen even assisted RWPs [3]. Mass transfer coefficients at a fixed gas flow when CO2 is not required in the algal culture. rate of 6 m3 h1 for paddle wheel, sump, and straight and curved channel sections were found as 164.50, 63.66, 0.87 and 0.94 h1, 2.1.8. Salinity 1 respectively. In the channel where mixing is poor, Kla was 0.7 h Fluctuation in the salinity concentration is the common problem in [3]. It was clear that paddle-driven RWPs had higher Kla. However, open ponds and it can affect the growth and cell composition of considering the power requirement for driving paddle-wheel, microalgae. Every microalgal strain has its own requirement of sump assisted RWPs was believed more appropriate for the algal optimum salinity in the medium, but some strains of microalgae have cultivation. The authors further speculated scope of improvement selective advantages of salinity. For example, D. salina, Tetraselmis sp. by increasing the volume of the sump, improving the performance have ability to grow low to high salinity [15]. But other oleaginous of the sparger, and increasing the gas flow to the sparger [3]. strain behaviors to salinity is strange during cultivation. The salinity of the medium keeps changing due to evaporation, rain, and precipita- 2.1.6. Light tion [46]. Changes in the salt concentration may affect algae in three Light is one of the major constraints for the algal biomass ways: osmotic stress, ion (salt) stress, and changes of the cellular ionic productivity. Pigmentation of algal culture causes exponential decrease ratios due to the membrane selective ion permeability [47].Thisaffects in the light intensity [42]. Light received by each of the algal cells the biomass productivity of marine microalgae. However, some depends upon a pond depth, biomass concentration, and turbulence marine microalgae have an adaptable mechanism to cope with regime [35]. Among them, pond depth and biomass concentration changing salinity concentration. For example, Tetraselmis sp. has a fi þ determine the degree of light attenuation, whereas the turbulent highly ef cient Na pump and a highly adaptable osmoregulatory regime determines the frequency at which a cell travels into and out of mechanism to cope with rapid and gradual changes in the salinity – the favorable light regime [35]. Therefore, maintaining RWPs shal- over a wide range (5.5 12% w/v, NaCl) [47]. The simplest way to get rid lower helps in exposing the algal cells to the maximum possible of the problem of salinity is using extra freshwater or salt added as amount of light [35]. However, a decrease in the depth of the RWP necessary [47]. compromises with the areal algal productivity. Raceway pond depth reported in the literature is as high as 50 cm [11].Mendozaetal. 2.1.9. Algal predators recommended depth of 20 cm for the raceway pond considering the Open ponds are of risk of several algal predators such as birds, overall hydraulic performance in terms of power consumption [3].Ina frogs, aquatic insects, etc. A range of microorganisms also feed study of light penetration in the algal culture, it was found that microalgae causing contamination of culture, and loss of biomass. pigmentation of algal cells does not block the light significantly up to These microorganisms can be fungus, bacteria, virus, rotifers, biomass concentration up to 0.66 g L1 [42,43].Ontheflip side, Cladocerans (e.g. Daphnia), Amoebae, Cyclopoid copepods, Ciliates, keeping the low biomass concentration in the open ponds is not Chironomid midges, Yesteryears etc. Most of the microalgal desirable as it enhances the harvesting cost and decreases the total cultivator is looking for smart strains that can produce valuable biomass productivity of microalgae. Therefore, targeting high biomass products and biodiesel along with resistance to predators. In concentration by ensuring sufficient mixing and suitable light/dark addition, thrust area of research is to engineer genetically mod- cycle is the economically viable option for the algal cultivation. ified microalgae (GMOs type), which always has challenges of fitness [48]. This is the reason of moving towards the extremophile 2.1.7. Oxygen accumulation nature of microalgae, which always have less chances of having Oxygen is produced in the process of photosynthesis and evolved predators during outdoor mass cultivation in RWPs. from the algal culture as the byproduct. An increase in the growth rate is generally proportional to the oxygen generation. The stoichiometric 2.1.9.1. Bacterial contamination. Nowdays, cultivation of microalgae in analysis reveals generation of 1.9 g oxygen per gram of the algal raceway pond is largely dependent on wastewater. Wastewater is used biomass synthesis [38].Ahighconcentrationofoxygenseverely as a solution to provide water and nutrients required in mass- damages the algal cells by photo oxidation and inhibits the cultivation of microalgae as a feedstock for biodiesel or biofertilizer. 880 K. Kumar et al. / Renewable and Sustainable Energy Reviews 51 (2015) 875–885

Table 2 Comparative study of the mass cultivation of microalgae in open ponds.

Algal species Raceway pond Raceway Culture velocity Experimental Average areal biomass Average volumetric References volume (m3) pond depth (m s1) conditions productivity biomass productivity (m) (g m2 d1) (g L1 d1)

Scenedesmus sp. 20 0.2 0.22 Sump assisted 17 – [14] raceway ponds Tetraselmis MUR 233 25 0.2 0.2 Recycling of water, 29.6 (max. – 37.5) Ash – [46] salinity tolerance free biomass testing Scenedesmus sp. 0.023 – 0.1 Airlift-driven 1% – 0.085 in batch [10] a 1 1 CO2; 0.6 g W d 80 μmol m2 s1 Scenedesmus sp. 0.023 – 0.1 Airlift-driven 1% – 0.19 in continuous; [10] a 1 1 CO2; 0.69 g W d 110 μmol m2 s1 Scenedesmus sp. 0.020 – 0.08 Airlift-driven – 0.16 [28] 4,000 lx Spirulina platensis 135 0.3 0.3 Paddle wheels 8.2 (max. – 13.95) 0.027 [18] Haematococcus pluvialis 20 0.2 0.15–1.2 Circular pond – 0.107 (15 days batch) [17] WZ Haematococcus pluvialis 26 100 0.2 0.15–1.2 Circular pond – 0.122 (15 days batch) [17] Tetraselmis suecica F&M- 20 0.15–0.20 0.15–0.25 – 8.37 (6 days batch) – [37] M33 Nannochloropsis sp. F&M- 20 0.15–0.20 0.15–0.25 – 14.1 (6 days batch) – [37] M24 Scenedesmus sp. 20 0.2 0.22 Sump assisted – 0.33 (5 days batch) [60] raceway pond Chlorella vulgaris 0.012 0.04 0.03 Covered raceway – 0.35 (5 days batch) [4] pond Chlorella vulgaris 58.89 m3 0.12 0.3 (in raceway Hybrid system – 1.67 g L1 [6] airliftþ392 m3 pond); 0.5 (in raceway pond airlift) Dictyosphaerium sp. 8 0.3 0.15 – 5.8 – [53] (dominated) over Pediastrun boryanum Pediastrun boryanum 8 0.3 0.15 Algal recycling 9.2 – [53] (dominated) over Dictyosphaerium sp. Botryococcus bruanii Kutz. 20.15– Manual mixing at – 0.114 g L1 based on [2] AP103 every 30 min batch Botryococcus braunii LB- 0.080 0.3 – Manual mixing twice – 0.1 (18 days batch) [19] 572 a day

a Based on power consumption.

Fig. 1. Schematic diagram of paddle-wheel driven raceway ponds.

The reduction and reuse of wastewater are the key parts of the it is under continuous exposer to the environment. However, the environmental and economic sustainability in the production of condition that is selective towards desired microorganisms can be microalgal biofuels. For example, recycling of medium has been ensured [51]. It is essential to prevent an increase in the bacterial load reported to reduce the cost of nutrient requirement by 16%, and with each harvest cycle. This can be done by monitoring the bacterial watersavingby63%[24]. The addition of bacterial population in contamination in microalgae within the recycled water from a raceway ponds during recycling may have other positive effects. harvesting system [51]. Viruses have been reported to infect mainly Bacteria make symbiosis with microalgae and the former have fresh water microalgae species such as Chlorella. However, this is less ability to secrete B12, an essential vitamin for microalgae [48–51]. common with marine microalgae [53]. However, water recycling can increase the inhibitory substances and dissolved organic matters from previous batch causing a decrease in 2.2. Raceway pond design the algal productivity [24,51]. In addition, the enhanced bacterial growth can introduce the competition for nutrients and loss of During the last few years, several modifications in raceway ponds nitrogen through denitrification processes [51–52].Itisimpractical have been proposed and demonstrated to enhance the biomass to maintain axenic culture of microalgae in a large scale open pond as productivity of the algal ponds. Most of the design focused on the K. Kumar et al. / Renewable and Sustainable Energy Reviews 51 (2015) 875–885 881 enhancing the mixing efficiency, gas/liquid mass transfer, residence the same flow rate. At the similar speed of paddle wheels, both the time of the gas bubbles and light penetration into RWPs [3,54,55]. configurations were found to sweep same amount of liquid and These modifications can be summarized in the following categories. A therefore had similar liquid flow. Dispersion coefficient was comparative study of biomass productivity of different microalgae in significantly higher in the aligned blades than the non-aligned open ponds have been shown in Table 2. blade configuration. However, non-aligned blade was found to reduce pulsation on the drive train and in the water flow. Aligned blade configuration causes non-smooth flow generation condi- 2.2.1. The raceway pond with manual mixing tions as all paddles advance simultaneously sweeping large Large scale biomass production in several raceway ponds relies amount of water at once. This may be the main reason for upon manual mixing. CO2 availability to algal cells depends upon enhancing the mixing in the reactor due to micro (turbulence) the natural diffusion of CO2 from the atmosphere. For example: and macro (convection) mixing of the liquid [29]. Antenna Nutritech Foundation (a non-profit organization), Paddlewheel efficiency depends upon the factors such as Madurai, India produces Spirulina in large scale for nutraceutical number of blades, rotational speed, the ratio between hydraulic purposes, where agitation is carried out by manual mixing. The head and radius of a paddle wheel, clearance between blades, cheap labor available for the manual mixing near the location of pond wall and pond surface [37]. Paddlewheel efficiency generally organization makes it viable process. Spirulina sp. are generally increases with the increase in the diameter of the paddle wheel. grown in this way as they efficiently grow at pH greater than 10 However, it increases the construction and production cost. and hence having less chances of contamination. In some cases, Propeller, centrifugal pump, microchannel paddle wheels are some CO2 in the form of carbonate is used as the carbon source. of the other substitute of the traditional paddle-wheel, which have been tested to induce vertical mixing and reduce power consump- 2.2.2. Paddle-wheel driven raceway ponds tion [37]. For example, fully axial flow propeller generally reduces The paddle-wheel driven RWPs are traditionally used for the the energy cost by nearly 50% compared to the traditional paddle- fi microalgal cultivation (Fig. 1). The rst use of paddle wheel for mixing wheel driven RWPs [37]. Reduction in the water head enhances in a RWP for wastewater treatment was reported by Benemann et al. the utilization efficiency. However, it increases the head loss and [56]. The paddle-wheel helps in the creation of eddies, which help in paddle wheel efficiency is greatly reduced at low water head [37]. moving the algae from the bottom to the upper layer. Vertical mixing The fully axial propeller can compensate the disadvantage of the is more pronounced near the paddlewheel due to blade passage and paddle wheel based design at low water head. near the bends due to secondary flows [29]. Raceway ponds incorpo- rate low energy consuming paddle wheels for gas–liquid mixing and circulation. Even after the bend, a wide recirculation area can be 2.2.3. Design of bend and floor surface geometries of raceway ponds visualized indicating the presence of the flow field at several meters Liffman et al. worked on the design of lower energy consump- away from the bend [37].Mixingbypaddle-wheeldrivenRWPshas tion bend geometries in the RWP [58]. Sharp bends in the RWP many advantages. They can be used to pump at high flow rate with cause a huge amount of energy losses. Water was directed at the low head devices. Paddle wheels are mechanically simple and require outer edge of the curvature by increasing the radius of curvature little maintenance. These generate gentle mixing useful, especially to by keeping the channel width same and varying the depth, flocculated and fragile microalgae. Small clearance zone (distance shallow at the center and deep at the periphery using some between the blade tip and the bottom floor) prevents the possible function such as linear, quadratic, square root profile (Fig. 2a). backflow of the liquid and thus paddle-wheel acts as a positive Another strategy was adopted to keep the cross sectional area of displacement pump. For example, the minimum clearance distance the curvature perpendicular to the culture flow. In this approach, of 19 cm was recommended by Hreiz et al. [29]. Temperature control channel width was kept narrow and the channel depth was in the cold season is an issue with the paddle-wheel driven RWPs. increased, maintaining the uniformity (box like design). Among Better mixing improves the algal productivity. However, it is always the various geometries tested at the bends in the RWP, box like desirable to minimize the energy consumption to drive the flow and shape was found to minimize the energy losses, and improve the mixing [57]. mixing of the RWP by removing the low speed and stagnation Dead zone develops near the middle wall downstream of bends region of the flow [58]. Previously, some other designs were also which increases the energy dissipation and reduces the pond tested at the bends of the raceway ponds. Multi-vane flow capacity [29]. The authors compared the differences between rectifiers have been used at the bends to minimize the flow aligned, and nonaligned blades (angular offset of nearly 22.5o) separations and energy losses [59]. Installation of an eccentric on the mixing [29]. Aligned bladed had better mixing performance curved wall with baffles at the bends was another approach taken with a comparatively little increase in the power consumption at into consideration [60].

Fig. 2. Schematic diagram of different design of bend and floor surface geometries. All cross-sections had the same area and drawn from the start of the turn towards the straight section of the raceway pond. (a) Standard, (b) square root profile, (c) linear profile, (d) quadratic profile, (e) wide box, (f) medium box, and (g) narrow box. The figure is redrawn from Liffman et al. and permission has been taken from the publisher for its reuse [58]. 882 K. Kumar et al. / Renewable and Sustainable Energy Reviews 51 (2015) 875–885

In one innovative way, ﬂoor surface has slope in both sides of by the paddle wheel and gravitational energy help in the move- the channel of the raceway pond. Paddle-wheel was placed on one ment of the water back and forth along the lower slope of the side of the RWP having greater depth. Slope of the RWP was RWP. Thus, culture in these RWPs experiences gradient of the decreasing gradually, ultimately ending with long zero depth ﬂoor sunlight. However, bottleneck of this type of RWPs is the require- surface at the other side of the paddle-wheel. The energy provided ment of large land footprint. Based on this design, eight RWPs, each having a capacity of 200 m3, are under operation at High Tech Algae Center, Hadong, South Korea.

2.2.4. Sump assisted raceway ponds Sump assisted RWPs are the easiest way to construct as it does

not require external energy supply and easy to fabricate [61].CO2 is injected in the counter-current direction to increase the liquid/ gas contact time. Gas is introduced at the bottom of the sump having greater depth. This allows an increased contact time of gas

phase and liquid phase. This enhances the CO2 utilization efﬁ- ciency and minimizes the CO2 loss into the atmosphere [62].de Godos et al. found the areal productivity of 17 g m2 d1 in the

sump assisted RWPs [14]. This was corresponding to CO2 capture of 66% of the inlet carbon in the biomass when the carbon transfer rate was 10 g C min1. Interestingly, most of the carbon was found

to lose as dissolved inorganic carbon in the harvest stream. CO2 lost in the form of gaseous CO2 was estimated at only 6%. Lowering the liquid velocity in the sump decreased the CO2 removal efﬁciency probably due to decrease in the driving force. An

increase in the gas ﬂow was found to reduce the CO2 removal efﬁciency. CO2 volumetric mass transfer by bubbling gas through the liquid phase was found in the range of 0.4–350 h1 in raceway ponds [41]. Operating at high liquid/gas ratio was considered a

good way for improving the CO2 removal efﬁciency [14].

2.2.5. Split sump with a central baffle/airlift driven raceway ponds This is the modification of the sump assisted RWPs. The advantage of this type of configuration is to improve the gas/ liquid contact and provide sufficient culture velocity to the culture suspension. An increase in the turbulence reduces the thickness of liquid layer and thus decreases the mass transfer resistance and increases the mass transfer coefficient. In this configuration, one side of the baffle acts as a downcomer where culture is forced to flow downward whereas the other side of the baffle acts as a riser

Fig. 3. Schematic diagram showing split sump/airlift driven raceway pond. The (Fig. 3). Airlift system of sump is generally fabricated using ﬁgure is redrawn from Ketheesan and Nirmalakhandan, and permission has been plexiglass. An inner partition in the tube (sump) gives the shape taken from the publisher for its reuse [28]. of the U tube [14].CO2 enriched air is introduced into the RWP

Fig. 4. Schematic diagram showing directed flow field using baffles in the raceway pond. The algal culture flows from the reservoir to the bottom tank by gravity. The pump is used to take the algal culture back into the reservoir. The necessary permission has been taken from the publisher for the reuse of this figure [57]. K. Kumar et al. / Renewable and Sustainable Energy Reviews 51 (2015) 875–885 883 through a sparger located at the bottom of the riser. The gassed Mixing of spill over with the main flow was found to give spirally liquid in the riser has less density compared to liquid in the forwarding flow. This was found helpful in improving the cycle of downcomer. The density difference between the two sides is the algal cells and dissolved gases from bottom to top in the flow driving force to induce the axial movement of the liquid culture. channels. The authors claimed the benefit of this type of RWP is in Growth of Scenedesmus sp. was evaluated in a pilot-scale airlift reducing the heat loss and freezing [57]. Another advantage of this driven raceway pond in laboratories condition and maximum design was the decreased slope per unit area which decreases the volumetric productivity of 0.19 dry g L1 day1 was obtained pump lift per unit area. The distance between the two channels

[10,28]. The maximum CO2 utilization efficiency of 33% has been (W) and the depth of water (D) in the channel were the determin- reported by this design [10]. The authors claim the 80% reduction ing factors influencing the flow mixing. The authors claimed W/D in the energy consumption to maintain typical raceway culture ratio of 5 as a suitable value for the good flow mixing under the velocity of 14 cm/s and keeping algal cells in suspension compared same flow rate [57]. to paddle-wheel driven RWPs [28]. Therefore, airlift-driven RWPs fi were observed more energy ef cient compared to traditional 2.2.9. Hybrid raceway ponds paddle wheel-driven RWPs. Some report suggests it is advanta- In this innovative approach, alga is cultivated in the combined geous to inject CO2 into the culture at the counter-current of the system of photobioreactor and open system. Thus, it has synergis- downcomer section of the sump preferably at half the height of tic effects which harness the advantage and minimizes the the downcomer through the sparger. This further enhances the demerits of both of the system. For example, coupling the airlift – CO2 liquid contact time. photobioreactor and open system reduces the high cost associated In other report, de Godos et al. additionally used paddle wheel with photobioreactor and reduces the contamination in the race- fl in the RWP along with the sump having provision of a baf einit way ponds [6]. Similarly, microalgae can be cultivated up to high [14]. The sump was mainly used for introducing CO2. The partition density in the photobioreactor in nutrient sufficient medium and fl baf e was placed 30 cm above the bottom of the sump to above then a portion can be transferred into the open raceway pond in the water surface [14]. The sump was placed 1.8 m to the down- nutrient deprived medium for the lipid induction [6]. Previously, stream of the raceway pond, which was 1 m deep, 0.65 m wide hybrid system was successfully operated for the cultivation of spanning to the full width of the channel of 1 m [14]. In his study, Haematococcus pluvialis for several years [63]. CO2 removal in the RWP assisted with baffle was only slightly higher compared to without a baffle. However, the power requirement was increased by nearly 6 folds in the baffle assisted RWPs 3. Commercial open ponds compared to without a baffle at the same flow velocity [14]. Therefore, disadvantages of this system is the change in the Several commercial level open ponds are under operation world- hydrodynamic behavior of entire reactor, decrease in the flow wide. For example, Muradel Demonstration Plant, Whyalla, Australia velocity, increase in power consumption, and decrease in the is cultivating microalgae in 4000 m2 paddle wheels mixed open pond degree of mixing [14]. having recycling facility with an average biomass productivity of 20 g m2 d1 (http://www.muradel.com/). The projected biofuel 2.2.6. External carbonation column production by this cultivation facility is nearly 30,000 l annually using Green2BlackTM technology. The company EARTHRISE estab- CO2 transfer stations adjacent to the RWP location is another lished in 1982 is the result of the merger of DIC Corporation (Japan) way to deliver CO2 gas supply into raceway ponds [54]. Putt et al. and Proteus Corporation (USA) (http://www.earthrise.com/). The investigated the CO2 transfer efficiency by combining carbonation column (CC) having internal diameter 0.076 m and height 3.0 m to company claims to be the largest Spirulina farm in the world. It 2 cultivates Spirulina in outdoor open ponds of 37 farms, each having the open pond with a surface area of 1.1 m [55]. The CO2 transfer an area of 5000 m2 in desert areas of California, USA. The open ponds rate by CC (83% CO2 transfer efficiency) was twice compared with direct bubbling. are operated by the recycling of nutrient and water for seven months a year. Another DIC group of company is Hainan-DIC Microalgae Company, China established in 1996. Algae Testbed Public -Private 2.2.7. Closed raceway ponds Partnership (ATP3) in USA rents their commercial level algal cultiva- In this configuration, RWPs were covered with the specially tion facility (open pond and photobioreator) to the entrepreneurs designed transparent cover. Gas bubbles were used to go along the working in the field of algal technology. The company “Algae culture flow and thus remain in contact with liquid for a prolonged systems” in USA conducts wastewater treatment by cultivating algae period of time [4]. This cover directly touches the algal culture, in mass scale in offshore photobioreactor made up of light transmit- causing hindrance to the gas bubbles from escaping into the ting durable plastic bags (http://algaesystems.com/). The CO partial atmosphere. CO fixation efficiency was found to enhance up to 2 2 pressure is maintained in the headspace of these plastic bags. The 95% under intermittent mixing [4]. In addition, this approach has algal cultivation system utilizes the energy of sea wave for mixing. advantages of reducing the water loss due to evaporation and The produced algal biomass is used for the production of biofuel culture dilution due to precipitation and rain. using hydrothermal liquefaction (HTL) process.

2.2.8. Engineering flow field In this approach, water was drained into the deep canal and 4. Conclusions lifted using the propeller pump to the RWP. The ground level of the RWP had low slope and had laterally-laid serpentine channels In the last 60 years, our knowledge has been improved guided by the partly open baffles. The flow rate of water was considerably in the area of environmental, biological, and techno- controlled in such a way that it can flow over the upper lateral logical aspects of algal cultivation. Some of them are the location channel wall naturally due to gravity and mix with the main flow of the cultivation system, rainfall, solar radiation, pond depth, CO2 of water in the next lower lateral channel (Fig. 4). The reservoir delivery system, methods of mixing, power consumption, light, was at the lower end of the RWP. 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