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Aquaculture 306 (2010) 1–6

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Aquaculture j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / a q u a - o n l i n e

Review

Anaerobic digestion of sludge from intensive recirculating aquaculture systems: Review Natella Mirzoyan a, Yossi Tal b, Amit Gross a,⁎ a Department of Environmental Hydrology and Microbiology, Zuckerberg Institute for Water Research, Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben Gurion 84990, Israel b Center of Marine Biotechnology, University of Maryland, Biotechnology Institute, 701 E. Pratt St., Baltimore, MD 21202, USA

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Article history: Received 14 June 2009 Received in revised form 21 May 2010 Accepted 25 May 2010 Keywords: Anaerobic digestion Aquaculture sludge RAS

a b s t r a c t Intensive recirculating aquaculture systems (RAS) produce high volumes of biosolid waste which is a potential source of pollution if not properly treated. A reduction in sludge-mass would therefore minimize the potential environmental hazard and economic burden stemming from its disposal. Recently, anaerobic digestion was suggested as an alternative to aquaculture sludge digestion and stabilization in RAS. This practice results not only in sludge-mass reduction, but also in water and energy savings, as well as in biogas production in certain practices, which can serve as an alternative energy source and partially cover the RAS's energy demands. In the current review, we summarize the reports on anaerobic digestion of sludge produced in RAS and compare the efficiencies of various methods. © 2010 Elsevier B.V. All rights reserved.

Contents 1. Aquaculture systems and waste production . . . . . . . . 2. Anaerobic digestion . . . . . . . . . . . . . . . . . . . 3. Anaerobic digestion of sludge from recirculating aquaculture 4. Summary . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgements . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . systems . . . . . . . . . . . . . . . .

1. Aquaculture systems and waste production Aquaculture is the most feasible solution to providing sufficient aquatic/sea food to satisfy the increasing market demand combined with a shrinking supply of natural products (e.g. in oceans and lakes). Traditionally, several culture methods are practiced in aquaculture. Earthen ponds are low labour, easily managed systems but can sustain fairly low stocking densities (Boyd and Tucker, 1998). This practice demands extensive use of land and is less efficient in terms of water use. Moreover, pond aquaculture does not provide for the removal and/or concentration of the solids that accumulate on the bottom of the pond, and these must be removed every few years when loads are high (Boyd and Tucker, 1998). Raceway aquaculture, also known as flow-through systems, is an inland operation, where water moves

⁎ Corresponding author. Tel.: + 972 86596896; fax: + 972 86596909. E-mail address: [email protected] (A. Gross). 0044-8486/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.aquaculture.2010.05.028

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through the aquaculture structure in order to maintain the required level of water quality. The effluent water in raceways might appear relatively clear and clean, but in reality it is simply due to dilution. The effluent is generally discharged into a receiving stream with little or no wastewater treatment (Gross, 2001). Net-pen aquaculture is an offshore practice in which species are grown in movable buoyant enclosures (net pens). While this practice provides better conditions for intensification, the waste is discharged directly into the water body and poses a potential threat of environmental pollution (e.g. Atkinson et al., 2004; Bristow et al., 2008). Economical and environmental constraints, as well as the dependence on large volumes of water, were the driving forces for the development of the recirculating aquaculture system (RAS). In RAS (Fig. 1), water typically flows from a fish tank(s) through a series of treatment processes, then back to the same tank (van Rijn, 1996). RAS are typically used when there is a specific need to minimize water replacement, to control over most water quality constituents, or to compensate for an insufficient water supply (Barak et al., 2003; Shnel

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et al., 2002). As a result of the super-intensive culture in RAS, a considerable amount of sludge is produced that must be treated before it can be disposed of (Losordo and Timmons, 1994; Shnel et al., 2002; Suzuki et al., 2003; Timmons and Ebeling, 2007; van Rijn, 1996). The solids originating in the RAS are composed mainly of fish excretions and a small percentage of uneaten feed; and its volatile (organic) fraction ranges from 50 to 92% (Gebauer, 2004; Gebauer and Eikebrokk, 2006; Mirzoyan et al., 2008; Piedrahita, 2003). Typically, fish sludge is characterized by its low total solid (TS) content (1.5–3%) compared to other animal production or industrial wastewater (Mirzoyan et al., 2008; Timmons and Ebeling, 2007). Waste characteristics may also vary widely, depending on the fish species (Timmons and Ebeling, 2007). A typical characteristic of RAS is the concentration of solid waste into relatively small flows that can be handled more efficiently. Different methods are used for the removal of different particle sizes (Fig. 2). Probably the most common solid-removal units used for aquaculture are: a) settling basins that are based on separation by gravity (Boyd, 1995; Timmons and Ebeling, 2007); b) hydrocyclones or swirl separators that are based on centrifugal sedimentation which allows for more rapid separation of the particles from the liquid (Tchobanoglous and Burton, 1991); c) microscreen filters that are based on screening particles that are larger than the screen's mesh size (Vinci et al., 2001); and d) granular/porous media filters that are based on the passage of water through a medium on which the solids are deposited/strained (Tchobanoglous and Burton, 1991). These filters are cleaned with backwash and often used in combination with other treatment processes. Generally, the more sophisticated the technology, the more costly it is for the farmers. After their removal, the concentrated solids are usually discharged from the RAS either into receiving water bodies or the local sewer system, or into a decentralized treatment unit, most commonly waste-stabilization ponds (WSPs) (Timmons and Ebeling, 2007). Disposal of aquaculture sludge into wastewater-treatment systems is often prohibited as it usually involves high volumes with high organic matter content and/or salts that might interfere with the treatment of municipal sludge. Even more problematic is the sludge's discharge into water-receiving bodies, as it may pollute local environments. The treatment of aquaculture sludge in WSPs is a preferable alternative. Nevertheless, it is estimated that 17 to 30% of the influent organic carbon entering a WSP is recovered as methane (Green et al., 1995), a greenhouse gas that can affect climate changes. Attempts to collect the methane from large surfaces such as those of WSPs have proven to be either expensive or inefficient (Green et al., 1995). Moreover, in WSPs, effluent is most often used for irrigation and sludge for land spread; however, in the case of brackish/marine water, this might lead to soil and groundwater salinization (Boyd and Tucker, 1998; Primavera, 2006). Even though anaerobic digestion (AD) is commonly used for the stabilization of municipal, industrial and agricultural wastes, it is a

Fig. 1. Schematic example of a recirculating aquaculture system.

Fig. 2. Solid-removal processes and the particle size range (in microns) over which the processes are most effective (after Timmons and Ebeling, 2007).

novel approach for the treatment of sludge produced in RAS, and is the focus of this review.

2. Anaerobic digestion Anaerobic digestion is the biological degradation of organic matter by microbes under anaerobic conditions. This is a natural process, carried out by facultative and obligatory anaerobic bacteria (Appels et al., 2008; Mshandete et al., 2005; Novak et al., 2003). Commonly, the digestion is practiced at one of three temperature regimes: thermophilic (45–65 °C), mesophilic (25–45 °C) and psychrophilic (10–25 °C) (Marchaim, 1992). AD has long been used for the stabilization and reduction of wastewater (although not aquaculture) sludge, mainly because of the simplicity of the operation, reduced sludge generation, production of biogas and possible high loading rates (Appels et al., 2008; Cakir and Stenstrom, 2005; Krzystek et al., 2001; Marchaim, 1992). Organic sludge undergoes considerable changes in its physical, chemical and biological properties during AD (Appels et al., 2008; Novak et al., 2003). Under ideal conditions, the ultimate products of this process are biogas composed of methane and carbon dioxide with small levels of hydrogen sulfide and ammonia (Ahring, 2003; Appels et al., 2008). Factors such as sludge pH, salinity, mineral composition, temperature, loading rate, hydraulic retention time (HRT), carbon-tonitrogen ratio and volatile fatty acid content influence the digestibility of the sludge and the biogas production (Krzystek et al., 2001; Novak et al., 2003; Sanchez et al., 2006). There are four main stages in the AD process: hydrolysis, fermentation, acetogenesis and methanogenesis (Sowers, 2000; Sowers and Ferry, 2002) (Fig. 3). Different reactor types are used for the AD of sludge produced in RAS and four of the more common ones, which are discussed in this review, are presented in Fig. 4 and briefly described below. In the continuously stirred tank reactor (CSTR) (Fig. 4A), sludge is introduced into a tank reactor equipped with an impeller, which stirs the liquor to ensure proper mixing. This reactor is very efficient in treating different types of organic-rich wastewater, but operational costs are high and it is labour-intensive (Marchaim, 1992). The outflow from the CSTR is often attached to a settler that separates the treated liquid from the solids (biomass), and the solids are then returned to the CSTR. The upflow anaerobic sludge blanket (UASB) reactor (Fig. 4B) uses an anaerobic process while forming a blanket of granular sludge which is suspended in the tank. Wastewater flows upward through the blanket and is processed (degraded) by the anaerobic microorganisms. The main advantages of the system are its low operational costs and simplicity of operation while providing high solid-removal efficiency for wastes with low (3–4%) TS content (Marchaim, 1992).

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Fig. 3. Stages of anaerobic digestion (from http://water.me.vccs.edu/courses/ENV149/ changes/Feat11_picII-1.jpg).

The membrane bioreactor (MBR) combines the activated sludge process of a conventional activated sludge system with a membrane (mainly hollow fibre or flat sheet membranes) submerged in the process water capable of filtering particulate waste constituents from the mixed liquor solution (Sharrer et al., 2007) (Fig. 4C). The main advantages of the MBR over conventional processes include high effluent quality, small footprint and easy retrofit and upgrade of old wastewater-treatment plants (Judd, 2006), while high operational costs and biofouling are the major disadvantages (Cui et al., 2003). 3. Anaerobic digestion of sludge from recirculating aquaculture systems AD of aquaculture sludge is a fairly new concept because in the traditional methods of aquaculture–in ponds, flow-through systems or net pens–sludge is not collected. Consequently, information about aquaculture sludge management in general is scarce, and even less is

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known about saline aquaculture sludge from RAS. To the best of our knowledge, anaerobic sludge digestion from freshwater RAS was first reported in the 1990s (e.g. Kugelman and van Gorder, 1991; Lanari and Franci, 1998). Initially, success was limited. For example: Kugelman and van Gorder (1991) treated freshwater aquaculture sludge with a TS content of 4 to 6% in a batch-type cylindrical digester under mesophilic conditions (35 °C) with the aim of producing methane at HRTs of 10 to 30 days (Table 1). The free ammonia levels were found to be inhibitory to AD (Table 2) and mixing the sludge with tap water enhanced digester performance. Unfortunately, no data were provided on sludge-stabilization efficiency for this study. Based on that study, the authors suggested a CSTR system operating under mesophilic conditions with diluted wastewater (to overcome the inhibition by free ammonia) for aquaculture sludge digestion. In another study, Lanari and Franci (1998) used an upflow cylindrical digester packed with polyurethane cubes to digest freshwater aquaculture sludge which originated from a RAS. The sludge, generated under different feeding regimes (average TS of 1.4 to 2.4%), was digested anaerobically at a temperature of about 25 °C with a 22- to 38-day HRT (Table 1). The feeding rate and HRT in this range did not affect solid removal and resulted in over 90% digestion of TS, total suspended solids (TSS) and volatile solids (VS) (Table 2). In addition to high digestion efficiencies, high quantities of biogas with over 80% methane concentration were produced in this reactor. The addition of a zeolite column to the treatment system enabled the removal of nitrogen from the effluent, which in turn resulted in suitable water quality for potential reuse in the RAS. The first reports dealing with brackish aquaculture sludge (BAS) digestion were published by Gebauer (2004) and Gebauer and Eikebrokk (2006), who successfully used a CSTR-type system, as suggested by Kugelman and van Gorder (1991), for the digestion of saline sludge from a salmon farm and smolt hatchery (8.2–10.2% and 6.3–12.3% TS, respectively) under mesophilic conditions (Table 1). In the first study, the HRT averaged 30 days and in the second study, 55 to 60days (Table 1). The digestion rates were high in both studies, demonstrating VS digestions ranging from 47 to 62% for the salmon farm sludge and 74 to 79% for the hatchery sludge, and up to 53% chemical oxygen demand (COD) removal for the hatchery sludge and 60% for the farm sludge (Table 2). Similar to Kugelman and van Gorder (1991), sludge digestion from the salmon smolt hatchery was inhibited by free

Fig. 4. Commonly used anaerobic digestion systems for sludge produced by recirculating aquaculture systems: (A) continuously stirred tank reactor (CSTR); (B) upflow anaerobic sludge blanket (UASB) reactor; and (C) membrane bioreactor (MBR).

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Table 1 Operational conditions of anaerobic digestion systems treating sludge originated from recirculating aquaculture systems. Authors

Fish culture

Water salinity

Digester type

Digestion temperature (°C)

HRT (days)

Feed TS (%)

Kugelman and van Gorder (1991) Lanari and Franci (1998) Gebauer (2004) Gebauer and Eikebrokk (2006) Mirzoyan et al. (2008) Mirzoyan (2009) Tal et al. (2009) Sharrer et al. (2007)

Atlantic salmon Rainbow trout Salmon Salmon smolt Prawn Striped bass Seabream Rainbow trout

Fresh Fresh Brackish Brackish Brackish Brackish Marine Fresh, brackish, marine

Batch fill and draw reactors Packed upflow cylindrical digester CSTR CSTR UASB UASB UASB MBR

35 24–25 35 35 25a Ambient-30 – –

10–30 22–38 30a 55–60 15 6–8 – 40.8b

4–6 1.4–2.4 8.2–10.2 6.3–12.3 1.5 0.4 – 0.07–0.17c

HRT — hydraulic retention time; TSS — total suspended solids; TS — total solids; CSTR — continuous stirred tank reactor; UASB — upflow anaerobic sludge blanket; MBR — membrane bioreactor. a Average number. b Given in hours. c As TSS.

ammonia concentrations (Table 2) (Gebauer and Eikebrokk, 2006). The authors also suggested that a high concentration of long-chain fatty acids originating from the fish feed was another factor contributing to inhibition of sludge digestion. Dilution of the sludge with fresh water helped overcome these problems. The dilution with fresh water also reduced the sodium concentration (and probably those of other salt ions), which was also reported to be inhibitory to BAS digestion (Gebauer, 2004) (Table 2). Even though the inhibition was observed in both studies, still high amounts of biogas and a reduction of organic load was achieved. In addition to the high digestion efficiencies, high methane concentrations of up to 61% were found in both studies (Gebauer, 2004; Gebauer and Eikebrokk, 2006) (Table 2). The biogas produced from the salmon smolt hatchery was enough to cover 2 to 4% of the system's energy demands. The digestion of BAS was also addressed by Mirzoyan et al. (2008), using a UASB reactor. Sludge which originated from prawn culture in a RAS (Singer et al., 2008) was anaerobically digested in three laboratoryscale UASB reactors for over 4 months in a temperature-controlled greenhouse with an average temperature of 25 °C and ≤ 15 days HRT. The total organic carbon (TOC) and biochemical oxygen demand (BOD5) in the UASB-treated sludge decreased significantly, by 40 and over 99%, respectively (Mirzoyan et al., 2008). In a similar setup, the influence of different conditions (carbon-to-nitrogen ratio, temperature, and HRT) on saline sludge digestion and biogas production from a striped bass RAS

was studied (Mirzoyan, 2009). The removal efficiencies of sludge VS in all reactors were over 92%, of COD 99% and of TSS 81%. The COD removal in all reactors, as presented in Table 1, was higher than in previous reports (Gebauer and Eikebrokk, 2006; Kugelman and van Gorder, 1991). Interestingly, however, the methane production was carbonlimited and increased with the addition of cotton wool as an external carbon source. The increase in HRT from 6 to 8 days also positively influenced methane production. The methane production was inversely correlated with temperature stability, suggesting higher production at ambient temperature (11–27 °C in winter, 12–30 °C in spring, 21–30 °C in summer and 17–28 °C in autumn) than at a constant temperature of 30 °C (Mirzoyan, 2009). Overall, the biogas produced in this study under all conditions accounted for 0.04 to 3.55 ml COD g− 1 and was lower than in previous reports (Table 2). This was explained by the low TS of 0.4% in the sludge that resulted from a technical problem with sludge thickening at the farm during the experimental period. Under stable operational conditions sludge TS does not influence the specific biogas/ methane production rate. However, if as a result of low TS high microbial biomass cannot be supported, the high solid removal may not lead to high biogas production, as was observed in the current study. Further batch investigations with a thickened sludge (1.4% TS) showed quantities of methane yield comparable to those reported in Gebauer and Eikebrokk (2006). The supernatant of the UASB-treated sludge was of adequate quality for further recycling into the RAS, taking into account its dilution by the tank water.

Table 2 Sludge digestion efficiency and methane production during digestion of sludge from recirculating aquaculture systems. Authors

a

Digestion Digestion Digestion efficiency Digestion efficiency bMethane (% efficiency (% TS) efficiency (% VS) (% BOD5) biogas) (% COD)

Kugelman and van Gorder – (1991) Lanari and Franci (1998) 92 Gebauer (2004) – Gebauer and Eikebrokk (2006) – Mirzoyan et al. (2008) Mirzoyan (2009) Tal et al. (2009) Sharrer et al. (2007)

– – 80g 99.7–100h

Methane production Inhibition (l COD g− 1 added)





34–47c; 57–71 d

36–71

0.125–0.164e

NH3

93–97 47–62c; 58d 74–79

– –

N 80 49–58

0.198–0.250e 0.114–0.184

No Na



– 37–55c; 60d 45–53

59–61

0.14–0.151

– 92–98 – N99.8i

100 – – –

– 99.6 – –

30–60 4–53 60 –

0.02 0.04–3.6f – –

NH3; long-chain fatty acids No No No No

TS — total solids; VS — volatile solids; BOD5 — biochemical oxygen demand; COD — chemical oxygen demand a Digestion efficiency was calculated as the% removal of a component (e.g. TS and BOD5) during the digestion. b Methane is presented as% of the total produced biogas. c Undiluted sludge. d Diluted sludge. e From Gebauer and Eikebrokk (2006). f Presented as ml COD g− 1 added. g Presented as v/v. h Presented as total suspended solid removal efficiency. i Presented as removal efficiency.

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A similar UASB system was used by Tal et al. (2009) to investigate sludge digestion and methane production under higher salinities of 15 to 17 g l− 1. The UASB reactor was incorporated into a pilot zerodischarge system growing 1.7 t of seabream (Table 1). The 20-l benchscale UASB reactor was able to reduce 80% of the solids, achieving greater than 60% conversion to methane (Table 2). This accounted for about 5% of the RAS's energy requirements. Based on their data, Tal et al. (2009) calculated that in their suggested full-scale urban RAS (aimed at growing 1 t of seabream), it would be possible to treat the accumulating sludge with a 100-l biogas reactor, for an expected yield of 26 mol methane gas for every 1000 kg fish produced. It was also noted that the system enhances recirculation and minimizes the use of saltwater. The use of a MBR was suggested by Sharrer et al. (2007) for solid and nutrient removal from a saline RAS. The RAS effluent treated in this reactor was generated during clarifier backwash and contained 0.07 to 0.17% TSS (Table 1). The role of the membrane is to separate the solids from the treated liquor, ensuring reliable and stable water quality. In this study, the MBR system was operated under the following salinities: 0, 8, 16 and 32 g l− 1 at a HRT of 40.8 h (Table 1) and a solid retention time of 64 ± 8 days. High TSS and VS removal efficiencies (over 99.7% and 99.9%, respectively) were demonstrated at all salinities (Table 2). Moreover, high efficiency of nitrogen and phosphorus removal was also detected simultaneously in the nitrification/denitrification processes. Ultrasonication was proposed as a pretreatment method to increase aquaculture sludge digestion and methane production (McDermott et al., 2001). It was shown to be not only effective at increasing the sludge COD removal, but also at enhancing biogas production as compared to untreated sludge. 4. Summary AD is an attractive approach for aquaculture sludge management. It allows addressing many of the problems associated with the traditionally used management methods such as WSPs, municipal waste-treatment systems and discharge into receiving water bodies. AD of RAS sludge can significantly reduce its volume, to more than 90%, due to its high digestion efficiencies, consequently lowering sludge transport and external treatment costs, major factors in the feasibility of RAS operation (Black and Veatch Holding Company, 1995; Reed et al., 1995). Moreover, the “polluting strength” of the treated sludge is significantly lower than that of raw sludge. Another advantage of integrating an AD unit into the RAS is its smaller environmental footprint compared to traditional systems, specifically to WSPs that require large areas of land (sometimes with high agricultural value) and to discharge into receiving water bodies that pollutes local environment. Many of the methods of AD of aquaculture sludge result in water whose effluent quality is adequate for reuse in the RAS. In this case, lower feed-water use as a result of lower water-exchange rates can be achieved. This, in turn, results in energy savings (pumping and heating) and further water and salt savings for the farmer. Moreover, the WSP effluent is most often used for irrigation; however, in the case of brackish/marine water, this can lead to soil salinization, which may also be avoided by the recirculation of effluent into the RAS. The observed methane production levels from the digestion of aquaculture sludge are lower than from other origins, such as domestic and industrial sludge, probably due to the sludge's lower TS content (Mirzoyan et al., 2008; Timmons and Ebeling, 2007). However, calculations suggest that 2 to 5% of the RAS's energy demand can be met by the amount of methane produced during the AD of aquaculture sludge (Gebauer and Eikebrokk, 2006; Tal et al., 2009). Production and utilization of methane have been suggested by several authors (e.g. Gebauer, 2004; Gebauer and Eikebrokk, 2006; Mirzoyan et al., 2008; Mirzoyan, 2009; Tal et al., 2009) to not only create an alternative

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energy source, but also reduce the atmospheric pollution that has been demonstrated for WSP (Green et al., 1995). Biogas collection also prevents the production of undesired odors associated with sludge stabilization in open ponds. As the AD of aquaculture sludge is a fairly new concept, information is still lacking and further research is required. Aside from further optimization of the current systems, the research community should be looking at ways to further reduce the sludge mass as well as improve on the “benefits” from the sludge treatment, such as methane production or nitrogen removal. The stabilized sludge's suitability for reuse (e.g. as a fertilizer or soil amendment) is another topic of interest. The stabilized sludge characteristics need to be identified and tested and its potential benefit should be assessed. Issues such as potential accumulation of heavy metals (Gebauer and Eikebrokk, 2006), the presence of chemicals, pathogens and odors (Stickney, 2000), and soil salinization should be addressed, as well as the potential availability of beneficial compounds such as nitrogen and phosphorus (Stickney, 2000). Acknowledgements This study was funded by the US–Israel Binational Agricultural Research and Development fund, the University of Maryland (MB8707-04), the Rozenzweige–Coopersmith Foundation (RCF) and the Rosinger–Barcza Fund. References Ahring, B.K., 2003. Biomethanation I and II. Springer-Verlag, Berlin. Appels, L., Baeyens, J., Degréve, J., Dewil, R., 2008. Principles and potential of the anaerobic digestion of waste-activated sludge. Prog. Energ. Combust. 34, 755–781. Atkinson, M.J., Brik, Y., Rosental, H., 2004. Evaluation of fish cages in the Gulf of Eilat. Report for the Israeli Ministries of Infrastructure, Environment and Agriculture, Israel. Barak, Y., Cytryn, E., Gelfand, I., Krom, M., van Rijn, J., 2003. Phosphorus removal in a marine prototype, recirculating aquaculture system. Aquaculture 220, 313–326. Black, Veatch Holding Company, 1995. Wastewater biosolids and water residuals: reference manual on conditioning, thickening, dewatering, and drying. CEC Report CR-105603: The Electric Power Research Institute, Community Environment Center, Washington University, St. Louis, MO. Boyd, C.E., 1995. Bottom Soils Sediment and Pond Aquaculture. Chapman & Hall, New York. Boyd, C.E., Tucker, C.S., 1998. Pond Aquaculture Water Quality Management. Kluwer Academic Publisher, Boston. Bristow, C.E., Morin, A., Hesslein, R.H., Podemski, C.L., 2008. Phosphorus budget and productivity of an experimental lake during the initial three years of cage aquaculture. Can. J. Fish. Aquat. Sci. 65, 2485–2495. Cakir, F.Y., Stenstrom, M.K., 2005. Greenhouse gas production: a comparison between aerobic and anaerobic wastewater treatment technology. Water Res. 39, 4197–4203. Cui, Z.F., Chang, S., Fane, A.G., 2003. The use of gas bubbling to enhance membrane process. J. Membr. Sci. 2211, 1–35. Gebauer, R., 2004. Mesophilic anaerobic treatment of sludge from saline fish farm effluents with biogas production. Bioresour. Technol. 93, 155–167. Gebauer, R., Eikebrokk, B., 2006. Mesophilic anaerobic treatment of sludge from salmon smolt hatching. Bioresour. Technol. 97, 2389–2401. Green, F.B., Bernstone, L., Lundquist, T.J., Muir, J., Tresan, R.B., Oswald, W.J., 1995. Methane fermentation, submerged gas collection, and the fate of carbon in advanced integrated wastewater pond systems. Water Sci. Technol. 31, 55–65. Gross, A., 2001. The effect of effluents from fish hatcheries on slightly disturbed rivers—a case study. In: Falconer, R.A., Blain, W.R. (Eds.), River Basin Management. Wit Press Publications, Southampton, Boston, pp. 205–217. Judd, S., 2006. Principles and Applications of Membrane Bioreactors in Water and Wastewater Treatment. Elsevier, Oxford. Krzystek, L., Ledakowicz, S., Kahle, H.J., Kaczorek, K., 2001. Degradation of household biowaste in reactors. J. Biotechnol. 92, 103–112. Kugelman, I.J., van Gorder, S., 1991. Water and energy recycling in closed aquaculture systems. Engineering Aspects of Intensive Aquaculture. Proc. Aquaculture Symposium, Cornell University, April 4–6, 1991. : Northeast Regional Agricultural Engineering Service (NRAES)-49. New York, Ithaca, pp. 80–87. Lanari, D., Franci, C., 1998. Biogas production from solid wastes removed from fish farm effluents. Aquat. Living Resour. 11, 289–295. Losordo, T., Timmons, M., 1994. An introduction to water reuse system. In: Timmons, M., Losordo, T. (Eds.), Aquaculture Water Reuse Systems: Engineering Design and Management. Elsevier Science B.V., Amsterdam, pp. 1–6. Marchaim, U., 1992. Biogas Processes for Sustainable Development. FAO, Rome, Italy. McDermott, B.L., Chalmers, A.D., Goodwin, A.S., 2001. Ultrasonication as a pre-treatment for the enhancement of the psychrophilic anaerobic digestion of aquaculture effluents. Environ. Technol. 7, 823–830.

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