Management of Ulva lactuca as a biofilter of mariculture effluents in IMTA system

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Management of Ulva lactuca as a biofilter of mariculture effluents in IMTA system Article in Aquaculture · October 2014 DOI: 10.1016/j.aquaculture.2014.08.034

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Aquaculture 434 (2014) 493–498

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Aquaculture journal homepage: www.elsevier.com/locate/aqua-online

Management of Ulva lactuca as a biofilter of mariculture effluents in IMTA system T. Ben-Ari ⁎, A. Neori, D. Ben-Ezra, L. Shauli, V. Odintsov, M. Shpigel Israel Oceanographic and Limnological Research, National Center for Mariculture, P.O. Box 1212, Eilat 88112, Israel

a r t i c l e

i n f o

Article history: Received 17 June 2014 Received in revised form 21 August 2014 Accepted 21 August 2014 Available online 11 September 2014 Keywords: Seaweed IMTA biofilter Ulva lactuca Aeration Economics

a b s t r a c t A strong aeration evens out light exposure, facilitates solute diffusion and increases yield in macroalgae cultivation. It is also responsible however, for up to 85% of the operating cost in the treatment of fish pond effluents. Optimizing and reducing excess aeration can therefore diminish the overall operation cost in monoculture and in Integrated Multi Trophic Aquaculture (IMTA). Biofiltration efficiency and crude biochemical composition of Ulva lactuca ponds were compared at two aeration regimes (continuous and 15 s min-1 intermittent aeration) in algal culture ponds fed with effluent water from an intensive, semi-closed commercial fish farm. Protein content of the algal yields was similar in both treatments at about 35% in DW. Nitrogen uptake was only 6% lower with the intermittent aeration compared to the continuous aeration, even though the algal yield with continuous aeration was significantly higher. It is suggested that denitrification in the pond with intermittent aeration contributed to the nitrogen uptake efficiency. A significant reduction in aeration led to a shortage in algal yield, but it was coupled with only a relatively small drop in nitrogen uptake. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Sea lettuce (Ulva lactuca) has been identified as an ideal candidate for biofiltering fish pond effluents. The cosmopolitan distribution of the genus in many climate and ecological conditions and its opportunistic growth make it a suitable species for cultivation practically everywhere (Del Rio et al., 1996; Mata et al., 2003; Msuya and Neori, 2002; Neori et al., 2000). The rapid growth of U. lactuca is attributed to its high photosynthetic rates and high ability to uptake dissolved nitrogen (Magnusson et al., 1996; Naldi and Wheeler, 2002; Sand-jensen, 1988). In addition, macroalgae (seaweeds) have been proposed as a biomass source for the production of food, animal feed, bioactive ingredients, pharmaceuticals, and cosmetics (Bobin-Dubigeon et al., 1997; Cumashi et al., 2007). U. lactuca in particular may be an important source of dietary fibers, mainly soluble (Fleury and Lahaye, 1991; Lahaye and Axelos, 1993). In mariculture, U. lactuca can be a valuable feed for macroalgivores such as abalone (Neori and Shpigel, 1999), and sea urchins (Naidoo et al., 2006; Neori et al., 2004; Shpigel and Neori, 1996). The total ammonia-nitrogen (TAN) uptake, yield, and protein content of U. lactuca grown in fishpond effluents were also determined (Cohen and Neori, 1991; Israel et al., 1995; Neori et al., 1996; Vandermeulen and Gordin, 1990) The rate (in g m−2 d−1) and efficiency (as fraction of the inlet) of sustained ammonia uptake by U. lactuca were related to the load of the supplied ammonia (Cohen and Neori, 1991). As the ammonia load increased, the efficiency of removal dropped. ⁎ Corresponding author. E-mail address: [email protected] (T. Ben-Ari).

http://dx.doi.org/10.1016/j.aquaculture.2014.08.034 0044-8486/© 2014 Elsevier B.V. All rights reserved.

The optimal density for the culture of U. lactuca was determined to be 1 kg m−2 (DeBusk et al., 1986; Neori et al., 1991). The yield of the algae and its protein content were also correlated with the load of ammonia (Msuya and Neori, 2008). The biomass of U. lactuca produced in a fish pond effluent contained 2–4 times more protein (up to 40% in dry weight) than U. lactuca from the wild (Neori and Shpigel, 1999). Ulva sp. culture is based on the bottom-aeration method (Lapointe and Tenore, 1981; Neori et al., 1991). Aeration stimulates growth by breaking down diffusive boundary layers at the surface of the thalli which would otherwise hinder the uptake of nutrients and inorganic carbon (Debusk and Ryther, 1984). Aeration also stirs the algae vertically in tanks and evens the exposure of all the thalli to light even in relatively deep tanks with high alga density. It is doubtful whether aeration supplies enough carbon to the cultures (via CO2 from air) to stimulate growth (DeBusk et al., 1986). Different systems to grow algae replace air agitation by water movement or water exchange. Under laboratory conditions, often no significant differences were observed in biomass yield and growth rates by reduced air agitation especially in high-nutrient water (Msuya and Neori, 2008; Vandermeulen and Gordin, 1990). A positive relation between photosynthetic rates to water velocity was found by Gonen et al. (1993) and Madsen et al. (2001). A low-cost low-tech system developed in Tanzania using gravity generated flow was suggested by Msuya et al. (2006). However, for commercial biomass production these systems require a substantial amount of water and at the same time need aeration to keep an even distribution of the macroalgae thalli close to the surface. The bottom aeration method is energy-intensive (Caines et al., 2014), and in previous experiments of

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ours, constituted about 85% of total algal culture cost (Shpigel, unpublished). Improving aeration regimes therefore seems necessary for increasing the overall profitability of land-based Integrated MultiTrophic Aquaculture (IMTA) systems. It was considered that the cost benefit of reduced aeration regimes could possibly be offset by reduced performance and inferior biochemistry of the macroalgae. However, several studies have reported a satisfactory performance of the algae with reduced aeration (Cohen and Neori, 1991; DeBusk et al., 1986; Msuya and Neori, 2008; Vandermeulen and Gordin, 1990). These experiments were made in small tanks, high water exchange rates and often with fertilizers, rather than fish ponds effluents. However, in fish pond effluent, the sinking of the algae to the bottom of the tank with no overnight aeration (instead of intermittent aeration) and low water exchange rates leads to anaerobiosis and can damage the algae (Shpigel, personal observation). The aim of the present work was to evaluate the impact of a reduced aeration regime activated in frequent pulses on growth, yield, biochemical composition and nitrogen metabolism in Ulva lactuca ponds. 2. Material and methods The experimental system consisted of two semi-commercial concave PVC ponds, each one stocked with 16 kg (0.8 kg m−2, according to DeBusk et al., 1986; Cohen and Neori, 1991) U. lactuca fronds, under a 150 m2 greenhouse. The surface area of each pond was 22.5 m2 (18 m length, 1.3 m width and 0.50 m average depth; Fig. 1). Effluent water originating from a commercial super-intensive fish farm (ARDAG Ltd., Eilat, Israel) stocked with gilthead sea bream (Sparus aurata) drained into one side of each pond and drained out from the opposite end. A vertical screen-covered overflow standpipe maintained the water depth at 50 cm. Effluent drained into the pond at an average flow rate of 0.64 m3 h−1, and HRT (Hydraulic Retention Time, volume/ flow rate*24) was 0.78 d for each of the two algal ponds. The concentration range of TAN in the inflow water during the diel cycle was lower than NOx (nitrate + nitrite, Table 1). The algae were grown unattached and kept suspended in the water column by air diffusers situated at the bottom of the tanks as in Neori et al. (1991). The aeration time was controlled by a 2 inch pneumatic air valve that provided continuous aeration in one pond, and 15 s min− 1 (25% of the time) aeration in the other. Three experimental trials took place, each lasting 48 h, with 10-day acclimation interval between runs, from May to June 2012, with

Table 1 Effluent water composition (N-NH4 and N-NOx levels) from Ardag fish farm throughout 24-hour observations, % is calculated from the total TIN (NH4-N + NOx-N. N = 6). Time

NH4-N (mg L−1)

NOx-N (mg L−1)

09:00

1.12 ± 3.72 (39.2%) 2.24 ± 0.07 (26.7%) 2.58 ± 0.16 (27.4%) 2.45 ± 0.17 (25.8%)

5.79±0.74 (60.8%) 6.18 ± 0.26 (73.3%) 6.84 ± 0.43 (72.6%) 7.05 ± 0.20 (74.2%)

15:00 21:00 03:00

daylight lasting 13:44 h in run 1, 14:10 h in run 2 and 14:15 h in run 3. Water temperature, dissolved oxygen (DO, OxyGuard®) pH (Checker-Hanna Instruments), salinity (CyberScan CON 410, Eutech Instruments) and light intensity (TES-1336A Datalogging Light Meter) were recorded daily. Water flow rate was monitored with electromagnetic flow meters (Arad Dalia, Israel). Water samples for dissolved total ammonia nitrogen (TAN), nitrite and nitrate were taken at the inlet and the outlet of the alga ponds at 6 h intervals (at 09:00, 15:00, 21:00, and 03:00 h) during each 48-h trial, using 250 ml acid-rinsed plastic jars, and filtered through GF/C Whatman® glass microfiber filters. Nutrient concentration analyses were made in duplicates with a Skalar Autoanalyzer (mod. SA1100, The Netherlands). At the end of each run, the algal biomass was harvested and air dried for 2 h to remove excess water, and weighed. Biomass subsamples of 250 g were taken for the determination of biochemical composition. Fresh macroalgae were then restocked for the next trial at the original stocking density of 0.8 kg m− 2. Proximate biochemical composition (protein, carbohydrate, lipid and phosphate levels) of U. lactuca was measured at the end of each trial. Kjeldahl nitrogen levels were determined (AOAC International, 1980), and multiplied by 6.25 as an estimate of protein content (Jones, 1931). Carbohydrate content was measured using the phenol-sulfuric acid method (Dubois et al., 1956). Lipid content was measured using the extraction method suggested by Folch et al. (1957). For the determination of total phosphorus, the algal samples were ashed in a muffle furnace, and processed by the vanado–molybdate analysis method (AOAC International, 1980).

Fig. 1. U. lactuca ponds, in the background, ARDAG intensive sea bream farm.

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Table 2 Min and max temperature, oxygen and pH in inlet and outlet water of the ponds exposed to continuous and 15 s min−1 aeration regimes (May to Jun, 2012). 100% Aeration

Intermittent Aeration

In Temp C°

Oxygen (%)

pH

Out

In

Out

Date

Mini

Max

Mini

Max

Mini

Max

Mini

Max

20−22.5.12 9−11.6.12 24−26.6.12 20−22.5.12 9−11.6.12 24−26.6.12 20−22.5.12 9−11.6.12 24−26.6.12

23.2 25.0 25.5 15 12 18 7.2 7.2 7.1

25.8 29.2 28.9 27 26 51 7.6 7.9 7.6

22.6 24.4 24.8 62 68 67 7.4 7.7 8.0

28.5 31.6 34 130 136 137 10.0 10.0 9.9

23.2 24.9 25.9 15 11 17 7.2 7.2 7.2

25.7 28.5 29.2 26 26 47 7.6 7.9 7.5

22.7 24.5 25.4 66 71 75 7.5 7.6 7.5

28.3 32.2 33.5 127 136 138 9.8 9.8 9.8

The specific growth rate (SGR) was calculated as: SGRð% growth=dÞ ¼ 100  ½ ln ðWt =W0 Þ=t

3.2. Yield, biochemical composition and nitrogen assimilation ð1Þ

where W0 is the initial biomass; Wt is the final biomass and t expressed as culture days of the experimental trial. Fresh yield (WW) was calculated as the difference between initial and final weights and expressed in units of g m−2 d−1. Nutrient flux was calculated as the product of water flow and nutrient concentration (g m−2 d−1). The removal rate (RR) of nutrients by all processes was calculated as: −2

RR ¼ ðCi−CoÞ gr N m

−1

time

:

Fresh yield of U. lactuca was 318 ± 40 and 178 ± 71 g m−2 d−1 for the continuous and the intermittent aeration regimes respectively (Fig. 2). SGR in the continuous aeration regime was 13.3 ± 0.95% d−1, i.e. significantly higher (P b 0.05) than in the intermittent aeration regime (8.1 ± 3.11% d−1). Total yield per trial was similarly significantly higher (P b 0.05) in the continuous than in the intermittent aeration regime (78.8 ± 9.9 and 44.2 ± 17.7 kg WW), respectively. The biochemical composition of the algae (contents of protein, ash, lipids, carbohydrate and phosphorus) was statistically similar between the two aeration treatments (Table 3), while nitrogen assimilation in the continuous aeration regime was twice as high as in the intermittent aeration regime (Table 5).

ð2Þ 3.3. Nitrogen dynamics in the U. lactuca ponds (48-hour observation)

The removal efficiency (RE) of nutrients by all processes was calculated as: RE ¼ ðCi−CoÞ=Ci  100

ð3Þ

where: Ci = concentration of inflow water; Co = concentration of effluent water. The proportion of the nitrogen that was taken up by the Ulva from the total RR was calculated using the Kjeldahl protein values and the Ulva yield. The results were standardized by dividing these parameters by the surface area so as to define the values obtained per square meter. 2.1. Statistics Data were analyzed using the JMP® version 9 (SAS Institute Inc., Cary, NC). One-Way ANOVA was employed to compare mean values (t test, α = 0.05). Averages of the abiotic parameters were compared using non-parametric matched pairs. Parameters in figures and text are presented as average values ± SEM.

3.3.1. Ammonia Ammonia-N levels in the pond inlets were stable throughout the day and had similar values in both treatments (Fig. 3). The high levels measured at 09:00 h seem to be due to the routine wash system of the bacterial biofilters in the fish farm at 08:00 h, and were not considered in the following analyses. Ammonia levels in the pond outlets were consistently and significantly lower than those measured at the inlets throughout the day (p b 0.01, Fig. 3), and reflect ammonia-N removal rates of 1.8 and 1.44 g m−2 d−1 in the continuous and intermittent aeration, respectively (Table 4). Outlet ammonia levels rose in both ponds during the night. The rise was higher in the intermittent treatment, where at 03:00 h inlet and outlet levels became similar (Fig. 3). 3.3.2. NOX NOx in the pond inlets were stable throughout the day and had similar values in both treatments (Fig. 4). The lower levels at 09:00 h seem to be due to routine wash system of the bacterial biofilters in the fish farm at 08:00 h, and were not considered in the following analyses. NOx in the ponds outlets were slightly and consistently lower than in

3. Results 3.1. Abiotic parameters Salinity levels remained at 41.1 ± 0.1 ppt throughout the experiments. The maximum and minimum values of temperature, pH and oxygen remained similar in both treatments during the three experimental trials (Table 2). Particulate organic matter (POM) accumulated at the bottom of the intermittent aeration pond.

Fig. 2. Growth (wet weight) of Ulva lactuca at continuous and intermittent (15 s min−1) aeration regimes (n = 3). Significant different (t-test, P b 0.05) was measured between aeration treatments.

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Table 3 Biochemical composition (% in DW) of Ulva lactuca exposed to continuous and 15 s min−1 aeration regimes. Protein

Lipid

Carbohydrate Phosphorus

Initial 20.8 ± 2.4 2.1 ± 1.7 54.4 ± 3.7 100% aeration 34.7 ± 4.0 2.4 ± 0.9 43.8 ± 3.2 Intermittent 35 ± 4.0 1.7 ± 0.07 43.5 ± 1.8 aeration

Ash

0.5 ± 0.07 22.1 ± 2.4 0.9 ± 0.1 16.9 ± 2.3 0.83 ± 0.07 16.9 ± 1

the inlets (p b 0.01), and reflect NOx-N removal rates of 0.36 and 0.45 g m−2 d−1 (the difference, p b 0.7, is statistically insignificant) in the continuous and intermittent aeration, respectively (Table 4).

3.4. Nitrogen assimilation Uptake rates of TAN and total inorganic nitrogen (TIN) were significantly higher (p b 0.01) in the continuous aeration treatment while uptake of NOX did not differ between treatments (Table 4). TIN uptake efficiency was higher in the continuous aeration regime than in the intermittent aeration regime (Table 4). In the continuous aeration regime the algae assimilated 88.2% of the nitrogen, compared to 67.0% that was taken up in the intermittent aeration regime (Table 4).

4. Discussion As aeration costs are substantial in the operation of a large mass culture facility (Caines et al., 2014; Debusk and Ryther, 1984), optimization of aeration regimes are of great importance. In our experiments we were able to demonstrate that it is possible to reduce aeration time by 75%, and still maintain satisfactory nitrogen assimilation, biomass yield and high protein content. Supplying 24 h\d aeration to a 200 m2 of Ulva pond in Israel is estimated to cost around 30$. Applying a 25% intermittent aeration regime will cut this cost by three quarters. The performance of a seaweed biofiltration pond depends on several parameters, some of which are controllable (e.g., pond design, stocking density, algal strain, nutrient load and hydraulic regime), while others (e.g., climate, weather, pests and light conditions) are not. The type of aquaculture system (recirculation or flow-through) and its management, fish feed chemistry and feeding regimes also determine the performance of the pond (Cripps and Bergheim, 2000). Differences in these factors hamper the comparison in macroalgae pond performance between studies. A number of studies reported nutrient removal efficiency of between 40 and 68% by Ulva sp. (Del Rio et al., 1996; Msuya and Neori, 2008; Neori et al., 2003; Schuenhoff et al., 2003; Troell et al., 2003; Wang et al., 2007). However, nutrient mass balance based on nutrient concentrations alone (e.g. in the inlet and the outlet), without taking into consideration the hydraulics and pond dimensions, is not an effective comparative tool, in particular for photosynthetic organisms. Nutrient removal efficiency can be compared only between studies with similar nutrients loads.

Table 5 TAN uptake rates (g N m−2 d−1) by the pond and assimilation rates by U. lactuca (N = 6). Aeration 15 s min−1

Continuous aeration Uptake by U. lactuca

Uptake by microorganisms

Total uptake

Uptake by U. lactuca

Uptake by microorganisms

Total uptake

1.50 ± 0.27 (83.3%)

0.3 (16.6%)

1.8

0.76 ± 0.05 (52.8%)

0.68 (47.2%)

1.44

An important issue in using macroalgae pond for effluent purification is the surface area that is required to remove the nutrients discharged for 1 kg of fish feed. We have therefore given relevance to the data reporting nutrient areal removal rates (g N or P m− 2 d− 1), for a comparison with our results. It should be considered that in addition to algal uptake, denitrification and other processes take up dissolved nitrogen. Such processes should be considered in the interpretation of algal nutrients uptake rates that are high with respect to algal yield and protein content, as observed by Msuya et al. (2006). 4.1. U. lactuca performance: biochemical composition and growth The general performance parameters of U. lactuca in the present study fall within the values reported in the literature (Table 6). Different aeration regimes influenced biochemistry of Ulva lactuca, particularly protein content, only under very low rate of nitrogen supply (Msuya and Neori, 2008). The similar biochemistry of the algae in the present experiments confirms that both treatments received sufficient nutrients. Protein content was higher than reported elsewhere (DeBusk et al., 1986; Fleurence, 1999) and similar to that measured in Israel in the past (Msuya and Neori, 2008). As it seems, inadequate exposure to light was the main growthlimiting factor in the intermittent aeration regime, considering that algae tended to sink in the turbid water when not aerated. 4.2. Ammonia-N dynamics The elevated Ammonia-N concentrations levels (and reduced NOx levels) that were measured in the inlets in both treatments at 09:00 h were due to routine wash system of the bacterial biofilters in the fish farm at 08:00 h. During daytime, light-dependant rate of ammonia assimilation by Ulva was much higher. Average daily ammonia uptake shows that although the TAN uptake rate was significantly lower in the intermittent aeration treatment, both treatments presented a higher uptake rates than those measured by Msuya and Neori (2008) under similar conditions. In light of our results, three processes lowered the apparent night time TAN uptake rate in the intermittent aeration treatment, measured as higher TAN levels: 1. Inadequate light due to the above mentioned sinking of the algae in the turbid water. 2. Low biomass, as it has been shown to be associated with low night time TAN uptake rate in Ulva (Vandermeulen and Gordin, 1990).

Table 4 Nitrogen load and uptake in the algal ponds (g m−2 d−1; N = 18), NOx data from the 09:00 h measurements were excluded. Continuous Aeration

TAN NOx TIN

Intermittent Aeration

Inlet

Outlet

Uptake and efficiency

Inlet

Outlet

Uptake and efficiency

2.04 ± 0.14 4.33 ± 0.80 6.37

0.24 ± 0.06 3.97 ± 0.80 4.21

1.8 (88.2%) 0.36 (8%) 2.16 (33%)

2.16 ± 0.12 4.80 ± 0.80 6.96

0.72 ± 0.13 4.35 ± 0.78 5.07

1.44 (67%) 0.45 (9.3%) 1.90 (27%)

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decrease in NOx levels between the inlets and outlets of the ponds was unlikely related to algal uptake. Thomas and Harrison (1987), Neori et al. (1996) and Ale et al. (2010) had shown that the presence of ammonia all but inhibits nitrate uptake, which is energetically disadvantageous for the algae uptake compared with the uptake of the reduced ammonia. 4.4. Pond performance

Fig. 3. Ammonia-N levels (μmol L−1), at the inlet and outlet of the Ulva ponds throughout 48 hour measurements (n = 6). The high inflow values in the 09:00 h samples coincided with a routine flashing of the bacterial filters of the fish farm.

Fig. 4. NOx levels (μmol L−1), at the inlet and outlet of the Ulva ponds throughout 48 hour measurements (n = 6). The low inflow values in the 09:00 h samples coincided.

3. Organic matter accumulated at the bottom of the Ulva pond in the intermittent aeration regime as a layer of most likely decomposed and bacterially ammonified algae, a process that can mask the night time uptake rate of ammonia by algae.

The three abiotic parameters (temperature, oxygen and pH) and their dynamics presented minor differences in the two treatments. It is unlikely that these differences can account for variety in pond performance (DeBusk et al., 1986; Duke et al., 1989). The much higher (almost double) biomass yield and daily growth rate by U. lactuca at the continuous aeration treatment compared to the intermittent aeration treatment was not proportional to the total nitrogen uptake values. These latter were much closer to each other in both treatments. It can be postulated that the nitrogen component in the Ulva composition originated exclusively from ammonia assimilation, since a high TAN load inhibits macroalgal assimilation of nitrate (Ale et al., 2010; Thomas and Harrison, 1987). Taking into account the product of yield and biochemical composition, 83% vs. only 52% of the TAN uptake were harvested in algal yield in the continuous and intermittent aeration, respectively (Table 5). Some of the TAN that was not recovered in Ulva biomass might have been lost in small algal fragments that pass through the screen. Consistent with Crab's et al. (2007) observations, microbial processes, such as nitrogen uptake by bacterial growth and nitrification/denitrification probably accounted for the large fraction of the missing TAN, particularly considering the high organic deposit that was observed at the bottom of the intermittent treatment pond. In a case where biofiltering efficiency is more crucial than algal yield, intermittent aeration can be an effective tool to reduce operation cost in IMTA systems. Acknowledgments

4.3. NOx-N dynamics Nitrate was removed in both ponds (disregarding the data from the morning samples), most likely by denitrification (Dvir et al., 1999). The

This research was supported by US AID foundation (TA- MOU-06M25-053). We wish to thank Dr. Angelo Colorni for his comments and editorial assistance and to Ala Zalmanson for her invaluable assistance in this work.

Table 6 Comparison between the cultivation conditions, biomass yields, biofiltering efficiency, and TAN removal of Ulva spp. cultivated in flow-through integrated systems. Species

Tank volume (liter)

Stocking density (kg WW m−2)

Water exchange (vol. d−1)

Growth Rate (g DW m−2 d−1)

TAN removal (g m−2 d−1)

TIN removal (g m−2 d−1)

References

U. lactuca (cont. aeration) U. lactuca (25% aeration) U. rigida U. rigida U. lactuca U. reticulata U. lactuca U. lactuca U. lactuca (cont. aeration) U. lactuca (non-aerated) U. lactuca U. lactuca U. lactuca

11700 11700 110 1900 600 40 600 600 700 700 600 600 6900−1700

0.8 0.8 1.9 1.9 1 1 2−6 1 1 1 1−8 1.5 1

1.1 1.1 91.2-98.4 14.4 34 2040a 4−16 4−8 10 10 12 2 14−56

31.3 17.8 44−73 48 11.2−37.6 46 55 55 18.8 6.8 12.32 21.3 18.9

1.8 1.4 2.7−5.1 1.3 0.4−7.4 1.9−6.5 1.2−5.6 − − − − − 2.9

2.16 1.9 2.7−3.6 1.45 − − − − − − − 1.72 −

This study This study Mata et al. (2010) Mata et al. (2003) Msuya and Neori (2008) Msuya et al. (2006) Neori et al. (1991) Vandermeulen and Gordin (1990) DeBusk et al. (1986) DeBusk et al. (1986) Bruhn et al., 2011 Neori et al. (2000) Neori et al. (2003)

a

High volume of water movement were used instead of bottom aeration.

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