Growth and nutrient uptake rates of duckweed cultivated on anaerobically digested dairy manure

Kevin Kruger, B. Brian He, Lide Chen*

Growth and nutrient uptake rates of duckweed cultivated on anaerobically digested dairy manure

Kevin Kruger1, B. Brian He2, Lide Chen1*

(1.Department of Soil and Water Systems, College of Agricultural and Life Sciences, University of Idaho, ID 83303-1827, USA;2. Department of Biological Engineering, College of Engineering, University of Idaho, ID 83844-2060, USA)

Nutrient cycling from flushed dairy manure systems to croplands is a national research priority for sustainable dairy operations, resource utilization, and environmental protection. Cultivating aquatic plants on dairy wastewaters has been considered an effective approach for wastewater treatment/reuse and nutrient recycling. This study aimed to investigate nutrient uptake and biomass production of duckweed strains on dairy wastewater. Three duckweed strains, namely0128,7589,and9517,were cultivated on anaerobically digested (AD) dairy manure wastewater over a period of 28 days. The highest reduction rate of total nitrogen (TN)was achieved byfrom the AD dairy manure with a dilution ratio of 1∶18 (83.1 mg?L-1TN) at 11.6% (±1.64%)The highest reduction rate of total phosphorus (TP) was achieved byfrom the AD dairy manure with a dilution ratio of 1∶27 (6.7 mg?L-1TP) at 15.4% (±4.4%).The corresponding fresh weight-based growth rate constants ofwere 0.11 g?d-1and 0.17 g?d-1for the dilution ratios of 1∶18 and 1∶27, respectively. It has been shown that, among the three duckweed strains tested in this study,has the greatest potential to be cultivated on the medium of diluted AD dairy manure for best N and P reduction and biomass production.

Flushed dairy manure; Nutrient recovery; Wastewater treatment; Anaerobic digestion; Dotted duckweed (Landoltia punctata); Fat duckweed(Lemna gibba); Least duckweed(Lemna minuta)

As of 2018, Idaho was the fourth-largest producer of milk in the United States with 490 dairy farms and about 600 000 cows producing over 14.6 billion pounds of milk (USDA, 2018). About 59% of the Idaho dairies are in the Magic Valley Region of Southern Idaho (IDA, 2018) which generate large volumes of wastewater stored in lagoon systems (Chen., 2014). The dairy wastewater contains large quantities of nitrogen (N) and phosphorus (P) which risk being transferred into the environment via run-off from over-irrigation and ammonia volatilization (Adhikari., 2015; Zhao., 2014). Concerns of the environmental impacts caused by concentrated animal productions have resulted in reporting requirements, mandatory management plans, and other regulations (Chen., 2014; Leytem., 2013; IDEQ, 2018). Identifying potential nutrient management technologies that utilize N and P contained in flushed dairy manure is essential to the sustainability of the Idaho dairy industry.

Duckweed is a family of tiny, flowering plants which belong to the Lemnaceae family and adapt to a variety of weather environments worldwide. There are five different genera includingandwith 37 different species (Cheng and Stomp, 2009; Ziegler., 2015). Many species grow in various locations throughout the world and form distinct populations called strains. Each duckweed strain has a specific set of nutrient and growth characteristics under a range of environmental conditions. Duckweed has been studied as a means of domestic and agricultural wastewater treatment in the past 30 years (Mohedano., 2012). The interest in duckweed has stemmed from its ability to 1) double its biomass weight in as little as 2 to 3 days under ideal conditions, 2) uptake N and P from nutrient rich sources, and 3) be harvested and stocked without many challenges (Rusoff., 1980; Sooknah., 2004; Adhikari., 2015).

Previous studies have utilized duckweed for the removal of nutrients from swine and cattle wastewaters in large-scale applications such as constructed wetlands, wastewater stabilization lagoons, and storage ponds (Al-Nozaily, 2001; Mohedano., 2012; Adhikari., 2015). These studies have shown that the cultivation of duckweed is a promising technology to recycle nutrients from wastewaters. However, there are few studies on N and P uptaking from anaerobically digested (AD) dairy manure by duckweed cultivation. To address nutrient management challenges, the aim of this study was to investigate the nutrient recovery and biomass production through duckweed cultivation on AD dairy manure for waste management and resource utilization in a value-added manner, resulting in a sustainable dairy industry in Idaho. The specific objectives of this study were to 1) investigate the feasibility of cultivating duckweed on AD Idaho dairy manure, 2) identify the achievable N and P reduction rates by cultivation of the selected duckweed stains, and 3) determine the duckweed biomass growth rate constants for further research of scale-up cultivation.

1 Materials and methods

1.1 Pre-culturing duckweed strains

Three duckweed strains, i.e.,0128 (),7589 (),and9517 (), were obtained from the Rutgers Duckweed Stock Cooperative and aseptically pre-cultured in 114 mm × 86 mm × 102 mm cultivation containers on 200 mg?L-1of Hoagland’s No. 2 Basal Salt Mixture for seven days (Zhao., 2014). The Hoagland’s No. 2 Basal Salt Mixture (hereafter named as Hoagland E-Medium) contains 115.03 mg?L-1of ammonium phosphate monobasic (NH4H2PO4), 2.86 mg?L-1of boric acid (H3BO3), 656.40 mg?L-1of calcium nitrate tetrahydrate [Ca(NO3)2?4H2O], 0.08 mg?L-1of cupric sulfate pentahydrate (CuSO4?5H2O), 5.32 mg?L-1of ferric tartrate (C12Fe2H12O8), 240.76 mg?L-1of magnesium sulfate anhydrous (MgSO4), 1.81 mg?L-1of manganese chloride tetrahydrate (MnCl2?4H2O), 0.02 mg?L-1molybdenum trioxide (MoO3), 606.6 mg?L-1of potassium nitrate (KNO3), and 0.22 mg?L-1of zinc nitrate hexahydrate [Zn(NO3)2?6H2O]. Once a double-layer of duckweed growth was observed, the duckweed strains were transferred to larger rectangular PET cultivation containers (0.267 m2) for 30 days to allow for further growth as inoculum samples for testing.

1.2 Batch testing

1.2.1 Nutrient analysis

AD dairy manure was collected from an anaerobic digester operated on a local dairy in Southern Idaho. Chemical oxygen demand (COD), total nitrogen (TN), total Kjeldahl nitrogen (TKN), nitrates and nitrites (NO3-N+NO2-N), ammonia nitrogen (NH3-N), ortho-phosphate-phosphorus (o-PO4-P), total phosphorus (TP), and suspended solids (SS) of the collected AD manure were analyzed using a spectrophotometer (DR5000, Hach, USA) based on Method 8000, Method 10242, Method 10031, Method 10214, Method 10127, and Method 8006, respectively (Hatch Company, 2005). Total and volatile solids of the collected AD manure were analyzed by the standard methods of APHA (2015). Analyses of pH, dissolved oxygen (DO) and electric conductivity (EC) were conducted using the Sper Scientific 850049 water meter kit (Scottsdale, AZ). Table 1 summarizes the nutrient characteristics of the AD dairy manure used in this study.

1.2.2 Growth media preparation

Growth media were prepared to establish the desired nutrient concentrations by mixing AD dairy manure and deionized water. These corresponded to TN concentrations of 114, 84 and 57 mg?L-1, respectively, and the initial pH values of the media were 8.11±0.03, 8.12±0.04, and 8.19±0.02, respectively, for the media with the dilution ratios of 1∶13, 1∶18 and 1∶27.

Table 1 Characteristics of anaerobically digested dairy manure tested

The pH of the media was then adjusted to 6.7 every 2 days with 5% (/) acetic acid to keep an ideal growth environment and reduce the loss of ammonia nitrogen (NH3-N) from the cultivation containers. After the pH of the media was adjusted to 6.7±0.01, the initial EC, DO and temperature of the media were measured at 1 660±12 μS?cm-1, 4.7±0.1 mg?L-1, and 21.4±0.1 ℃ at the dilution ratio of 1∶13, 1 331±16 μS?cm-1, 3.8±0.2 mg?L-1, and 23.4±0.1 ℃ at the dilution ratio of 1∶18, and 1 066±10 μS?cm-1, 4.5±0.1 mg?L-1, and 23.6±0.1 ℃ at the dilution ratio of 1∶27, respectively. The media were then transferred to cultivation containers with transparent lids to prevent evapotranspiration. The cultivation containers have dimensions of 114 mm × 86 mm × 102 mm, a surface area of 0.011 6 m2, and a total volume of 300 mL. An average of 0.46, 0.57 and 0.61 g of,,andwere added to the cultivation containers to cover 25% of the surface area of each container.

1.2.3 Experimental setup

Batch tests were conducted inside an environmental chamber (Environmental Growth Chambers, Chagrin Falls, Ohio) at an average light intensity of 10 000 lux and a photoperiod of 16∶8 (light∶dark). The experiments consisted of a total 36 cultivation containers having a working volume of 200 mL in each container. Of the 36 cultivation containers, the three duckweed strains, i.e.,,,and, were applied in triplicates to 27 cultivation containers containing the media as described above. Nine control cultivation containers (without duckweed inoculation) consisted of the same media with three dilution ratios (1∶13, 1∶18 and 1∶27) in triplicates.

2 Sampling and analysis

Liquid medium samples were extracted from each of the cultivation containers with the duckweed treatments and the control for nutrient analysis on day 0, 4, 8, 12, 16, 20, 24, and 28, and measured for temperature, TN, TKN, NO3-N+NO2-N, NH3-N TP, o-PO4-P, pH, DO, and EC based on the methods mentioned previously. The duckweed samples were carefully filtered from the cultivation containers and separated from the medium using course tulle. Residual liquid on duckweed surfaces was blotted with absorbent paper and fresh weight of duckweed was measured with an analytical balance (Mettler AE 260 Delta Range). After weighting, the duckweed biomass samples were carefully re-inoculated back to their containers immediately.

The rate constant of the fresh weight-based growth (hereafter named growth rate constant, g?d-1) and its standard deviation were established using a linear regression equation (Eq.1) (Cheng., 2009; Xu.,2010).

C = k·t + Co(1)

whereois the initial duckweed fresh weight (g),C(g) is the duckweed fresh weight (g) at time(days), andis the duckweed growth rate constant (g?d-1).

The initial and final nutrient concentrations of the media were used to find the percent TN and TP reduction rates (Sooknah., 2004; Adhikari., 2015). The differences in TN and TP reduction rates between the media with the duckweed (treatments) and without the duckweed (control) were used to calculate the percentages of TN and TP uptake rates by the duckweed strains.

The fresh weights of duckweed biomass samples and the nutrient concentrations in the media were analyzed statistically using a two-way analysis of variance (ANOVA) to determine the validity of the experimental results between the treatments and controls by the statistical software of SPSS (SPSS Inc., Chicago, IL, USA). Tukey simultaneous tests were conducted to determine the statistical differences between treatments.

3 Results and discussion

3.1 Nitrogen and phosphorus uptake by duckweed

Total nitrogen (TN) and total phosphorus (TP) concentrations within the media for the 28-day cultivation period are shown in Figure 1. The growth media was modelled to maintain conditions that would apply to the cultivation environment of a dairy lagoon where bacteria, algae, and duckweed would thrive symbiotically among the batch samples. The three duckweed strains grew well on the cultivation media from diluted AD dairy manure with the dilution ratios of 1∶18 (84 mg?L-1of TN) and 1∶27 (57 mg?L-1of TN). However, the three duckweed strains perished after 4 days of cultivation on the dilution ratio of 1∶13 (114 mg?L-1of TN) which indicated that the nutrient concentration in the medium with the dilution ratio of 1∶13 was too high for the duckweed strains. In the media with dilution ratios of1∶18 and 1∶27 AD dairy manure, TN and TP were removed quickly in the first 12 days of cultivation, and the concentrations of TN and TP slowly decreased in the next 16 days of cultivation. This is in some disagreement with the study by Xu(2010) in which the greatest ammonium nitrogen (NH4-N) recovery occurred in the first 20 days of cultivation. Therefore, it is important to identify the period of fast nutrient reduction rates which in turn helps determine the timing and types of nutrients that need to be replenished to keep a healthy duckweed production system.

Fig. 1 Total nitrogen (TN) and total phosphorus (TP) concentrations in diluted anaerobically digested dairy manure with the dilution ratios of 1∶18 and 1∶27 treated with L. punctata, L. gibba and L. minuta

The changes of nutrient concentrations along with the reduction rates of TN and TP in the cultivation media are shown in Table 2. The highest TN reduction rate of 92.5%±0.3% was observed from the media with the dilution ratio of 1∶18 treated byGenerally, TP reductions of 66.0%±0.6% to 85.6%±4.4% were achieved, and the highest TP reduction rate of 85.6%±4.4% came from the media with the dilution ratio of 1∶27 treated by, which are in agreement with the previously reported N and P reduction ranges of 60%-98% from pretreated livestock wastewaters (Adhikari., 2015; Mohedano, 2012; Xu2010). In addition to the uptake by duckweed, reduction in N and P in the batch experiments could occur due to other means such as ammonia volatilization, nitrification/denitrification, bacterial transformation, sedimentation and algal uptake (Mohedano, 2012; Xu, 2010). The controls in this study were used to explore the possibility of N and P reduction via these alternative pathways to determine the uptake by the duckweed strains.

Figure 2 shows the results of TN and TP uptake by the duckweed strains from the cultivation media after a 28-day batch growth. These results were determined by the difference between the N and P reductions from the batch system (Table 2) of the duckweed treatments and the controls. At the dilution ratio of 1∶18, the duckweed achieved TN and TP reduction rates of 11.6%±1.6% and 10.6%±1.1% for,7.9%±1.6% and 9.3%±2.7% for,and 4.1%±1.2% and 3.2%±0.8% forAt the dilution ratio of 1∶27, reduction rates of 7.8%±2.9% of TN and 15.4%±4.4% of TP, 3.3%±0.9% of TN and 12.9%±2.4% of TP,and 1.6%±0.8% of TN and 5.6%±1.7% of TP for,, and,respectively, were observed. In our batch systems, the combined alternative pathways (i.e., ammonia volatilization, nitrification/denitrification, bacterial transformation, sedimentation and algal uptake) contributed to a N reduction in the range of 65.0% to 80.8% in the growth media with the dilution ratio of 1∶18 and 53.8% to 61.6% in the growth media with the dilution ratio 1∶27. The main pathways for P reduction are bacterial transformations, biomass absorption either by duckweed or algae, and sedimentation. Mohedano(2012) reported that P was most strongly reduced in the anaerobic stage of a lagoon system probably due to sedimentation. An anaerobic zone could have formed at the bottom of the cultivation containers where anaerobic bacteria can assimilate P. The P reduction caused by bacterial transformations, algae biomass adsorption, and sedimentation contributed to an average of 64% and 69% among the duckweed treatments in the growth media with the dilution ratio of 1∶18 and 1∶27, respectively.

Table 2 Total nitrogen (TN) and total phosphorus (TP) reductions in diluted anaerobically digested dairy manure with the dilution ratios of 1∶18 and 1∶27 treated with L. punctata, L. gibba and L. minuta at the end of the 28-day test

Data in the table are mean ± S.D. (the standard deviation of triplicate samples).

Fig. 2 Percent recovery of total nitrogen (TN) and total phosphorus (TP) by the duckweed strains from the anaerobically digested dairy manure with (a) the dilution ratio of 1∶18, (b) the dilution ratio of 1∶27. Percent recoveries of TN and TP among the three duckweed strains were statistically significant at P≤0.05.

3.2 Duckweed growth rate

It was observed that the first eight days of cultivation were most productive withandcovering over three quarters of the surface area.did not double its biomass in the first eight days of cultivation and covered less than half of the surface area. Throughout the entire cultivation period of 28-days for both the dilution ratios of 1∶18 and 1∶27,andmaintained a healthy complexion on the surface of the AD dairy manure and the Hoagland E-medium. However, at day 16 the fronds on the first layer ofstarted turning white but maintained buoyancy to float on the surface of the PET containers until day 28 for the dilution ratio of 1∶18. A double layer ofandformed at the surface of the dilution ratio of 1∶27 by the 28th day. Filamentous algae growth was visible on the surface of the controls as well as on the sides of the cultivation containers. Algae growth was not visible on the surface of the duckweed treatments but was visible on the sides of the containers by the end of the cultivation period.

The growth of duckweed biomass was quantitatively analyzed by the growth rate constants which were calculated from the measured fresh weights of duckweed biomass samples cultivated with the dilution ratios of 1∶18 and 1∶27 through a linear model (Tables 3 and 4). As shown in Figure 3, no lag phases were observed due to the pre-culturing of the duckweed strains on the Hoagland E-Medium. The zero-order regressions fit the experimental data well with2values in the range of 0.79 and 0.97. Growth rate constants of the three duckweed strains were higher at the dilution ratio of 1∶27 with the growth rate constants of 0.17±0.02, 0.19±0.06 and 0.04±0.00 g?d-1(10.0, 8.0, 1.6 mg?d-1dry weight) for,, and,respectively. In this study, the differences between the growth rate constants ofandat the dilution ratios of 1∶18 and 1∶27 were significant (≤0.05) different from that of.

In a study conducted by Toyama(2018), the growth rate constants for duckweed strains ofandwere approximately determined as 30 and 4.5 mg?d-1, respectively, when cultivated on AD domestic wastewaterat 30.1 mg?L-1of NH4-N and 3.3 mg?L-1of nitrate nitrogen (NO3-N). It is possible that the higher nitrogen concentrations in this study inhibited growth of the duckweed strains as compared to the values reported by Toyama(2018).

Table 3 Linear equations describing relationships between the duckweed biomass fresh weight and cultivation time. The regression equations were found to significantly fit a linear model (P ≤ 0.05).

Table 4 Growth rate constants of L. punctata, L. gibba, and L. minuta cultivated on the anaerobically digested dairy manure with the dilution ratios of 1∶18 and 1∶27. The growth rate constants of both L. punctate and L. gibba were significantly higher (P ≤0.05) than that of L. minuta for both the dilution ratios of 1∶18 and 1∶27.

Data of growth rate constants in the table are mean ± S.D. (the standard deviation of triplicate samples).

Further research should include the verification of the N and P contents in the duckweed biomass and an analysis of the mechanisms of N and P assimilation by bacteria, algae, and duckweed strains when cultivated on flushed AD dairy manure. These factors will potentially maximize biomass production and nutrient reduction such that the cultivation of duckweed on dairy farms could be utilized as a protein supplement for dairy cattle.

4 Conclusions

The results obtained from this study have shown that,andcould be cultivated on diluted AD dairy manure for nutrient recovery and biomass production. On average, the TN and TP reduction rates were 11.6% and 10.6% for,7.9% and 9.3% for,and 4.1% and 3.2% forfrom the AD dairy manure with the dilution ratio of 1∶18. The TN and TP reduction rates with the dilution ratio of 1∶27 were 7.8% and 15.4% for,3.3% and 12.9% for,and 1.6% and 5.6% for. It is concluded that the duckweed strains recovered approximately the same percentages of TN and TP from the AD dairy manure at the dilution ratio of 1∶18. The duckweed strains had a higher TP recovery than TN recovery when cultivated on the AD dairy manure with the dilution ratio of 1∶27. At the dilution ratios of 1∶18 and 1∶27 the growth rate constants were 0.11 g?d-1and 0.17 g?d-1for, 0.11 g?d-1and 0.19 g?d-1for, and 0.04 g?d-1and 0.03 g?d-1forBothandhad significantly higher growth rate constants when compared toIt has been shown that, among the three duckweed strains tested in this study,has the greatest potential to be cultivated on the medium of diluted AD dairy manure for the best N and P reduction and biomass production.

Fig. 3 Fresh biomass of L. punctata, L. gibba, and L. minuta cultivated on the anaerobically digested dairy manure with the dilution ratios of 1∶18 and 1∶27. The growth rate constants of both L. punctata and L. gibba were significantly higher than that of L. minuta for both the dilution ratios of 1∶18 and 1∶27 (P ≤0.05).

Acknowledgements This research was financially supported in partial by the USDA NIFA, USDA Multi-State Hatch Projects and the Idaho Agricultural Experiment Station.

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厭氧發(fā)酵牛糞對浮萍生長和養(yǎng)分吸收的影響

Kevin Kruger1, B. Brian He2, Lide Chen1*

(1. 愛達荷大學農(nóng)業(yè)和生命科學學院土壤和水分系統(tǒng)系 愛達荷州 83303-1827 美國; 2. 愛達荷大學工程學院生物工程系 愛達荷州 83844-2060 美國)

養(yǎng)分從牛糞到農(nóng)田的循環(huán)利用是養(yǎng)牛場可持續(xù)發(fā)展、資源利用和環(huán)境保護的重點研究內(nèi)容。利用奶牛場廢水種植水生植物被認為是一種有效的廢水處理及養(yǎng)分循環(huán)的方法。本文研究了3種浮萍[少根紫萍0128(0128)、膨脹浮萍7589(7589)和小浮萍9517(9517)]在厭氧發(fā)酵過的奶牛場廢水中種植時的養(yǎng)分吸收和生物質(zhì)變化。在28 d的測試期間, 種植在稀釋比例為1∶18的厭氧發(fā)酵過的牛奶場廢水中的少根紫萍01283獲得最高的總氮吸收率(11.6%±1.6%), 種植在稀釋比例為1∶27厭氧發(fā)酵過的牛奶場廢水中的少根紫萍0128獲得最高的總磷吸收率(15.4%±4.4%);相應地少根紫萍鮮重的增長率分別為0.11 g?d-1和0.17 g?d-1。3種浮萍中, 少根紫萍最具有吸收牛奶場廢水氮、磷并獲得較高生物質(zhì)的潛力。

牛糞; 養(yǎng)分循環(huán); 廢水處理; 厭氧發(fā)酵; 少根紫萍(); 膨脹浮萍();小浮萍()

Chinese Library Classification: X713

Paper Number: 2096-6237(2019)09-1402-07

Open Science Identity:

, E-mail: lchen@uidaho.edu

Apr. 3, 2019;

May 20, 2019

KRUGER K, HE B B, CHEN L D.Growth and nutrient uptake rates of duckweed cultivated on anaerobically digested dairy manure[J]. Chinese Journal of Eco-Agriculture, 2019, 27(9): 1402-1408