Plant uptake of nitrogen adsorbed to biochars made from dairy manure.

The conversion of dairy waste with high moisture contents to dry fertilizers may reduce environmental degradation while lowering crop production costs. We converted the solid portion of screw-pressed dairy manure into a sorbent for volatile ammonia (NH3) in the liquid fraction using pyrolysis and pre-treatment with carbon dioxide (CO2). The extractable N in manure biochar exposed to NH3 following CO2 pre-treatment reached 3.36 g N kg-1, 1260-fold greater extractable N than in untreated manure biochar. Ammonia exposure was 142-times more effective in increasing extractable N than immersing manure biochar in the liquid fraction containing dissolved ammonium. Radish and tomato grown in horticultural media with manure biochar treated with CO2 + NH3 promoted up to 35% greater plant growth (dry weight) and 36-83% greater N uptake compared to manure biochar alone. Uptake of N was similar between plants grown with wood biochar exposed to CO2 + NH3, compared to N-equivalent treatments. The available N in dairy waste in New York (NY) state, if pyrolyzed and treated with NH3 + CO2, is equivalent to 11,732-42,232 Mg N year-1, valued at 6-21.5 million USD year-1. Separated dairy manure treated with CO2 + NH3 can offset 23-82% of N fertilizer needs of NY State, while stabilizing both the solid and liquid fraction of manure for reduced environmental pollution.

Introduction

class="Chemical">Nitrogen (N) maclass="Chemical">nagemeclass="Chemical">nt is a major challeclass="Chemical">nge iclass="Chemical">n agriclass="Chemical">n class="Chemical">cultural systems. Nitrogen fertilizer for crops is a significant cost, while the disposal of N-rich wastes such as dairy manure, can also be costly. The shift toward sustainable farming highlights the need for opportunistic waste management able to capture nutrients from liquid waste streams and transform them into high-value, dry fertilizers that can be safely transported and traded.

Dairy manure excretion in NY State alone averages 12,821,616 class="Chemical">Mg per year[1,2]. Coclass="Chemical">ntaiclass="Chemical">niclass="Chemical">ng approximately 64,108 class="Chemical">n class="Chemical">Mg N, 16,786 Mg P, 44,876 Mg K[3], these excreted nutrients are sufficient to fertilize the state’s extensive 17,321 hectares (ha) of corn production, requiring 51,360 Mg N calculated using the average application rate in 2018, 96 kg ha−1[4-6]. The benefits incurred by transforming dairy waste into agronomic inputs extend to dairy farmers and grain farmers alike in NY State; a farmer growing 81 ha of corn spends 28,000 USD year−1 for fertilizer[7], while a dairy farmer with 550 cows spends 25,000 USD year−1 for manure storage[8]. To couple these processes, new technologies for recycling dairy waste products back into crop nutrient inputs are necessary.

While direct manure spreading has been the most common means of disposal and re-use of dairy waste, such practices can result in transport of N and P into class="Chemical">waterways[9,10], as class="Chemical">nutrieclass="Chemical">nts from maclass="Chemical">nure ofteclass="Chemical">n exceed the agroclass="Chemical">nomic demaclass="Chemical">nd[11]. Furthermore, maclass="Chemical">nure storage for future maclass="Chemical">nure applicatioclass="Chemical">n produces class="Chemical">notable quaclass="Chemical">ntities of class="Chemical">n class="Chemical">methane, a known greenhouse gas[5,12]. Moreover, long-distance transport of dairy manure for land application also has a number of drawbacks such as the spreading of pathogens[13] and costs associated with transporting a material with a water content of > 70%[14]. Alternatives to direct land application of dairy slurry are needed with less detrimental impact on the environment[15], which utilize the high nutrient content of manure for agronomic purposes. Source-separation of manure followed by anaerobic digestion of the liquid portion is one alternative[16-18] that is being adopted across farms of all scales in NY State[19] and other regions.

Solid–liquid separation of manure is a first step in efficient re-use of waste nutrients[16]. The physical separation of manure into solid and liquid fractions (slurry) significantly lowers N leaching from the solid fraction[17,18]. Most of the inorganic N in dairy manure is found in the liquid portion, approximately 4400 class="Chemical">mg class="Chemical">n class="Chemical">NH4–N L−1[17], and can be a significant source of N2O and NH3 emissions from lagoons[5,20,21]. Thus, a technology is needed for removing N from stored slurry and converting it into a fertilizer. We see great potential in converting the solid portion of separated dairy manure into a biological charcoal, or biochar, with high sorption properties, able to remove N from the liquid portion of dairy manure.

Pyrolysis is one technology which can transform residual biomass into highly porous, surface-functionalized adsorbents[22]. The temperatures used in pyrolysis (typically between 400 and 700 °C) assure full sterilization of manure, along with densification and desiccation, leading to saclass="Chemical">fer, aclass="Chemical">nd cheaper traclass="Chemical">nsportatioclass="Chemical">n per uclass="Chemical">nit dry material[14,15]. Much of the literature oclass="Chemical">n biochar sorbeclass="Chemical">nts reclass="Chemical">n class="Chemical">fer to high surface area of low ash biochars[23,24] derived from plants[25-29]. Increasing concern for the environmental burden of manure from animal production has highlighted the relevance of manure biochars as agricultural amendments[30-33]. As pyrolysis requires feedstocks to have a moisture content below 15%, a number of strategies have been implemented for reducing the moisture content of manure, such as co-pyrolysis with woody feedstocks, or utilization of the thermochemical byproducts such as emitted heat or bio-oils for drying of moist manures[34,35].

Manure biochars are notably rich in plant-essential nutrients such as class="Chemical">phosphorus aclass="Chemical">nd class="Chemical">n class="Chemical">potassium[23,36], as well as total N[37-39]. They also have the ability to adsorb residual ammonium (NH4)[27] and volatile ammonia gas (NH3)[29] and can enhance plant N-use efficiency[40]. The ability to sorb NH3 increases after pre-exposure to carbon dioxide (CO2)[41]. Since CO2 is a by-product of the pyrolysis process[42], biochars made from the solid portion of dairy manure can be treated with CO2 before using them to sorb volatile NH3 from slurry lagoons.

class="Chemical">Ammonia gas is reported to sorb oclass="Chemical">nto woody biochar aclass="Chemical">nd class="Chemical">n class="Chemical">CO2-doped human manure biochar via both strong and weak mechanisms[27,29,40], pointing to both short and long-term plant availability. Sorbed N from cattle urine onto woody biochar was reported as plant-available, promoting the growth of rye grass[43]. Yet no study has evaluated the actual plant-availability of NH3 sorbed onto manure biochar after exposure to CO2.

While surface charge and acid–base interactions drive N interactions with biochar made from woody class="Chemical">feedstocks, precipitatioclass="Chemical">n of N salts such as class="Chemical">n class="Chemical">ammonium bicarbonate (NH4HCO3) is a more likely mechanism for N removal by ash-rich dairy manure digestate biochar. Moreover, NH3 loading via NH4HCO3 precipitation may exceed monolayer surface adsorption to multi-layered sorption through intermittent exposure to CO2[44]. Recent work demonstrated that exposure of biochar to NH3 re-functionalizes surfaces with amine groups[29] which are then able to adsorb CO2[41,44-46]. The incorporation of CO2 molecules may further enhance NH3 retention through the formation of NH4HCO3, creating NH4HCO3-intercalated biochar for use as a mineral-organic, slow-release fertilizer. The intimate association between the first layer of chemisorbed NH3 on biochar surfaces and NH4HCO3 precipitates projecting further out from the surface is expected to provide both long-term and immediately available N. Yet no study has evaluated the plant-availability of N incorporated into manure biochar through sequential NH3 and CO2 adsorption.

Therefore, we quantify the plant uptake of N adsorbed to dairy manure biochar using either liquid class="Chemical">NH4+ or gaseous class="Chemical">n class="Chemical">NH3 with prior CO2 conditioning. Crops grown in the greenhouse, tomato, marigold, and radish, were used in this small-scale study to demonstrate proof of concept. We benchmarked the performance of dairy manure biochar as an adsorber against wood biochar, a material reported to sorb up to 6 mg g−1 NH3-N[43,47]. We compare the plant-availability of N from biochars exposed to either liquid NH4+ or gaseous NH3 to the availability of N from urea fertilizer added in combination with each biochar. We expect greater plant-availability of N incorporated to dairy manure biochars compared to that incorporated into wood biochar. We expect greater N use efficiency from both biochars exposed to N compared to biochar added with inorganic fertilizer.

Results

The increase in total N of the amendments following class="Chemical">NH3 exposure was much larger for wood (1.13% poiclass="Chemical">nt chaclass="Chemical">nge iclass="Chemical">n N, from 0.75 to 1.88% N) thaclass="Chemical">n maclass="Chemical">nure biochars (a poiclass="Chemical">nt chaclass="Chemical">nge of 0.06% N, from 2.05 to 2.11% N). The iclass="Chemical">ncrease iclass="Chemical">n class="Chemical">n class="Chemical">KCl-extractable N (sum of NO3–N and NH4+-N) was similar between wood (0.005–3.1 g N kg−1) and manure biochars (0.026–3.4 g N kg−1). The KCl-extractable, or plant-available N in manure biochar following NH3 exposure increased 127 fold, in comparison to a 595 fold increase for wood biochar, with only 27% of the added N in wood biochar following NH3 exposure being plant-available. This increase in plant-available N versus total N following NH3 exposure was 21-fold greater for manure than wood biochar (Table 1). Furthermore, the increase in total N in manure biochar exposed to NH3 (0.06%-points), was smaller than the increase in plant-available N (0.34%-points) (Table 1). Exposure to NH3 therefore increased the plant-available N in both biochars to the same extent, apparently, irrespective of the total N increase.

Table 1

Total carbon and nitrogen and KCl-extractable ammonium (NH4+-N) and nitrate (NO3–N) in amendments used for the greenhouse trial ± the standard deviation.

Analysis	Unit	Wood biochar	Manure biochar	Slurry	Wood biochar NH3 + CO2	Manure biochar CO2 + NH3	Wood biochar + slurry	Manure biochar + slurry	Potting media (peat)
Nitrogen	% (w w−1)	0.75 ± 0.34a	2.05 ± 0.05a	2.75 ± 0.05a	1.88 ± 1.48a	2.11 ± 0.37a	1.84 ± 0.15a	2.21 ± 0.13a	0.74 ± 0.23a
Carbon	% (w w−1)	90.70 ± 0.35a	44.30 ± 0.41d	35.3 ± 0.15e	88.21 ± 1.78b	43.68 ± 0.75d	73.73 ± 0.14c	42.32 ± 0.32d	25.67 ± 1.41f
NH4+-N	(mg kg−1)	4.4 ± 4.7b	2.7 ± 3.1b	ND	3083.5 ± 143.2a	3363.7 ± 335.0a	15.5 ± 3.7b	23.7 ± 22.2b	606.2 ± 16.4b
NO3–N	(mg kg−1)	0.8 ± 0.1b	24.0 ± 2.1b	ND	4.7 ± 0.1b	20.6 ± 2.7b	0.5 ± 0.1b	2.3 ± 1.2b	635.1 ± 15.2a

ND not determined, as KCl extraction of slurry is not an appropriate measure plant-available N.

Letters indicate significant differences between amendments using a one-way anova (p < 0.05; n = 3).

Total class="Chemical">carbon aclass="Chemical">nd class="Chemical">n class="Chemical">nitrogen and KCl-extractable ammonium (NH4+-N) and nitrate (NO3–N) in amendments used for the greenhouse trial ± the standard deviation.

ND not determined, as n class="Chemical">KCl extractioclass="Chemical">n of slurry is class="Chemical">not aclass="Chemical">n appropriate measure placlass="Chemical">nt-available N.

Letters indicate significant difn class="Chemical">fereclass="Chemical">nces betweeclass="Chemical">n ameclass="Chemical">ndmeclass="Chemical">nts usiclass="Chemical">ng a oclass="Chemical">ne-way aclass="Chemical">nova (p < 0.05; class="Chemical">n = 3).

The change in total N in manure and wood biochars following immersion in the slurry was similar to that through class="Chemical">NH3 exposure, compared to uclass="Chemical">nexposed biochars. However, iclass="Chemical">n both biochars, a much smaller portioclass="Chemical">n of this added N was immediately placlass="Chemical">nt-available after immersioclass="Chemical">n iclass="Chemical">n slurry, 0.0–0.01 g N kg−1, compared to after exposure to class="Chemical">n class="Chemical">NH3, 0.005–3.4 g N kg−1 (Table 1). Thus, sorbed N on biochars following NH3 exposure is more plant-available than sorbed N from the slurry.

Manure biochar contained significantly greater total nutrients (acid-digestible) and plant-available (class="Chemical">Mehlich III extractable) class="Chemical">nutrieclass="Chemical">nts by mass thaclass="Chemical">n wood biochar, specifically Ca, class="Chemical">n class="Chemical">Mg, and P (Tables 2, 3). This corroborates with previous reports of large amounts of ash minerals in biochars from manure feedstocks compared to woody feedstocks[23,36]. Calcium (Ca) comprised more than 15% of manure biochar mass and less than 1% of wood biochar mass. The high Ca concentration in manure biochar resulted from the regular liming of fresh manure solids after screw-pressing. Significantly greater total micronutrients (B, Cu, Fe, Mn, Zn) were observed in manure biochar compared to wood biochar, 3.14 vs. 0.80 g kg−1, respectively. This trend was reversed for extractable elements: wood biochar contained 2.5-fold greater Mehlich III-extractable micronutrients (358.3 mg g−1) than manure biochar (146.1 mg g−1).

Table 2

Total nutrients measured in acid-digested (HClO4 + HNO3) amendments used for the greenhouse trial ± the standard deviation.

Analysis	Unit	Wood biochar	Manure biochar	Slurry
Al	(g kg−1)	0.38 + 0.02b	4.03 + 1.57a	0.35 + 0.28b
Ca	(g kg−1)	5.3 + 0.0b	158.1 + 12.4a	49.5 + 42.0a
K	(g kg−1)	5.5 + 0.3a	12.8 + 1.9a	37.5 + 32.4a
Mg	(g kg−1)	0.75 + 0.01b	15.93 + 0.12a	7.66 + 6.56ab
Na	(g kg−1)	0.47 + 0.01a	3.92 + 0.51a	8.78 + 7.55a
P	(g kg−1)	0.55 + 0.02b	11.90 + 0.90a	7.17 + 6.16ab
S	(g kg−1)	0.09 + 0.00a	2.30 + 0.20a	3.53 + 3.03a
Micronutrients (B + Cu + Fe + Mn + Zn)	(g kg−1)	0.80 + 0.03b	3.14 + 0.19a	0.99 + 0.75b
Heavy metals (Cd, Pb)	(mg kg−1)	3.04 + 0.33b	15.28 + 3.64a	2.34 + 1.08b

Letters indicate significant differences between amendments using a one-way anova (p < 0.05; n = 3).

Table 3

Plant-available nutrients in amendments, extracted with Mehlich III ± the standard deviation.

Analysis	Unit	Wood biochar	Manure biochar	Wood biochar NH3 + CO2	Manure biochar CO2 + NH3	Wood biochar + slurry	Manure biochar + slurry
Al	(mg kg−1)	130.4 ± 4.6a	0.8 ± 0.5d	83.5 ± 4.0b	0.0 ± 0.1d	17.4 ± 3.6c	10.8 ± 1.6c
Ca	(g kg−1)	3.46 ± 0.06e	25.92 ± 0.03a	2.53 ± 0.08f.	21.84 ± 0.16c	11.91 ± 0.36d	23.80 ± 0.33b
K	(g kg−1)	7.00 ± 0.05d	9.87 ± 0.14c	6.47 ± 0.07d	10.41 ± 0.20c	18.70 ± 0.82a	13.12 ± 0.31b
Mg	(g kg−1)	0.58 ± 0.02d	3.00 ± 0.01a	0.48 ± 0.00d	2.50 ± 0.03c	2.46 ± 0.09c	2.71 ± 0.04b
Na	(g kg−1)	0.81 ± 0.06b	2.40 ± 0.01a	0.68 ± 0.04c	2.41 ± 0.00a	2.36 ± 0.00a	2.39 ± 0.00a
P	(g kg−1)	0.32 ± 0.00d	1.08 ± 0.01b	0.23 ± 0.00e	0.91 ± 0.00c	1.71 ± 0.06a	0.17 ± 0.03a
S	(mg kg−1)	62 ± 2c	302 ± 4a	55 ± 1c	290 ± 3a	214 ± 9b	303 ± 8a
Micronutrients (B, Cu, Fe, Mn, Zn)	(mg kg−1)	358 ± 9a	146 ± 1c	260 ± 9b	122 ± 1d	264 ± 1b	143 ± 3c
Heavy metals (Cd, Pb)	(mg kg−1)	9.83 ± 3.91a	0.84 ± 0.02b	0.14 ± 0.32b	0.75 ± 0.01b	1.42 ± 0.16b	0.61 ± 0.06b

Letters indicate significant differences between amendments using a one-way anova (p < 0.05; n = 3).

Total nutrients measured in acid-digested (class="Chemical">HClO4 + class="Chemical">n class="Chemical">HNO3) amendments used for the greenhouse trial ± the standard deviation.

Letters indicate significant difn class="Chemical">fereclass="Chemical">nces betweeclass="Chemical">n ameclass="Chemical">ndmeclass="Chemical">nts usiclass="Chemical">ng a oclass="Chemical">ne-way aclass="Chemical">nova (p < 0.05; class="Chemical">n = 3).

Plant-available nutrients in amendments, extracted with n class="Chemical">Mehlich III ± the staclass="Chemical">ndard deviatioclass="Chemical">n.

Letters indicate significant difn class="Chemical">fereclass="Chemical">nces betweeclass="Chemical">n ameclass="Chemical">ndmeclass="Chemical">nts usiclass="Chemical">ng a oclass="Chemical">ne-way aclass="Chemical">nova (p < 0.05; class="Chemical">n = 3).

The total and Mehlich-III-extractable and therefore plant-available concentrations of heavy metals in both wood and manure biochars were below the EPA threshold values for biosolids intended for agriclass="Chemical">culture[40,48]. Maclass="Chemical">nure biochar coclass="Chemical">ntaiclass="Chemical">ned sigclass="Chemical">nificaclass="Chemical">ntly greater total coclass="Chemical">nceclass="Chemical">ntratioclass="Chemical">ns of heavy metals (class="Chemical">n class="Chemical">Cd, Pb) than wood biochar, 15.3 vs. 3.0 mg kg−1 (Table 2). However, Mehlich III-extractable heavy metals were 12-fold greater in wood biochar than manure biochar, reaching 9.8 mg g−1 vs. 0.84 mg g−1, respectively (Table 3).

Additions of wood biochar alone increased plant growth (dry weight of above and below-ground biomass) from 4.9 to 29% relative to no additions. class="Species">Radish placlass="Chemical">nts beclass="Chemical">nefited from additioclass="Chemical">ns of maclass="Chemical">nure biochar aloclass="Chemical">ne, with 18% greater placlass="Chemical">nt growth thaclass="Chemical">n class="Chemical">no additioclass="Chemical">ns. Wheclass="Chemical">n class="Chemical">n class="Chemical">urea alone (1×) was added to potting media, plant growth increased by 9–34% relative to unamended plants. Additions of manure or wood biochar together with urea (1×) increased plant growth by 14–63% relative to unamended plants (Fig. 1, Table 4).

Figure 1

Increase in plant biomass (sum of root and shoot biomass) grown with urea fertilizer (green points), manure biochar (brown points) or wood biochar (gray points) amendments relative to unamended plants (0×). The amount of plant-available N in each type of amendment in parentheses. Letters above the bars indicate significant differences between amendments within plant type (p < 0.05; n = 4; whiskers indicate standard errors).

Table 4

The average ± standard deviation of the pH of potting mix and amendments after 40 days, total plant biomass (shoot and root combined) and relative increase in plant biomass relative to unamended plants (0×), total N plant uptake (shoot and root combined), and relative increase in biomass N uptake in comparison to unamended plants.

Plant	Amendment	pH after 40 days	Plant N uptake (mg pot−1)	Relative increase in plant N uptake (% w w−1)	Plant biomass (g pot−1)	Relative increase in plant biomass (% w w−1)
Marigold	0× fert	6.35 ± 0.13cd	35.63 ± 3.87de	NA	2.81 ± 0.36bc	NA
Marigold	0.25× fert	6.28 ± 0.14cd	40.37 ± 7.21bcde	13.28 ± 20.25bcde	3.38 ± 0.31abc	20.27 ± 10.89abc
Marigold	0.5× fert	6.30 ± 0.04cd	38.97 ± 6.45cde	9.36 ± 18.10cde	3.59 ± 0.57ab	27.73 ± 20.15ab
Marigold	1× fert	6.15 ± 0.14d	51.63 ± 4.49abc	44.89 ± 12.61abc	3.63 ± 0.60ab	28.98 ± 21.20ab
Marigold	1.5× fert	6.25 ± 0.11cd	61.36 ± 6.64a	72.20 ± 18.65a	3.66 ± 0.37ab	30.22 ± 13.25ab
Marigold	Manure biochar	7.46 ± 0.16a	31.50 ± 5.24e	− 11.60 ± 14.71e	2.69 ± 0.27bc	− 4.27 ± 9.67bc
Marigold	Manure biochar + slurry	7.35 ± 0.43a	34.10 ± 4.93de	− 4.30 ± 13.83de	2.93 ± 0.46bc	4.00 ± 16.51bc
Marigold	Manure biochar CO2 + NH3	7.41 ± 0.24a	42.74 ± 4.38bcde	19.95 ± 12.29bcde	2.43 ± 0.36c	− 13.72 ± 12.77c
Marigold	Manure biochar + 1×	7.35 ± 0.04a	52.28 ± 0.00abc	46.71 ± 0.00abc	3.20 ± 0.00abc	13.78 ± 0.00abc
Marigold	Wood biochar	6.53 ± 0.19cd	32.40 ± 2.46e	− 9.08 ± 6.92e	3.56 ± 0.31ab	26.58 ± 10.89ab
Marigold	Wood biochar + slurry	7.03 ± 0.18ab	33.20 ± 1.63de	− 6.84 ± 4.56de	3.14 ± 0.31bc	11.64 ± 11.16bc
Marigold	Wood biochar NH3 + CO2	6.62 ± 0.13bc	46.44 ± 9.15bcd	30.33 ± 25.67bcd	3.66 ± 0.44ab	30.22 ± 15.82ab
Marigold	Wood biochar + 1×	6.51 ± 0.15cd	53.33 ± 3.45ab	49.66 ± 9.67ab	4.30 ± 0.33a	52.80 ± 11.58a
Radish	0× fert	6.48 ± 0.12cd	29.60 ± 7.33d	NA	3.08 ± 0.27c	NA
Radish	0.25× fert	6.51 ± 0.16cd	40.06 ± 4.41bcd	35.33 ± 14.89bcd	3.87 ± 0.52abc	25.39 ± 16.91ab
Radish	0.5× fert	6.34 ± 0.14d	42.74 ± 7.71abcd	44.37 ± 26.04abcd	4.09 ± 0.28abc	32.69 ± 9.13ab
Radish	1× fert	6.35 ± 0.15d	53.04 ± 6.73ab	79.17 ± 22.74ab	4.13 ± 0.50abc	34.06 ± 16.35ab
Radish	1.5× fert	6.37 ± 0.14d	55.94 ± 8.38a	88.96 ± 28.30a	4.39 ± 0.83ab	42.25 ± 26.80ab
Radish	Manure biochar	7.22 ± 0.10ab	30.19 ± 4.82d	1.99 ± 16.27d	3.65 ± 0.84bc	18.25 ± 27.22b
Radish	Manure biochar + slurry	7.31 ± 0.12a	31.60 ± 1.78d	6.74 ± 6.00d	3.93 ± 0.22abc	27.33 ± 7.19ab
Radish	Manure biochar CO2 + NH3	7.25 ± 0.13a	55.28 ± 8.68a	86.75 ± 29.34a	4.48 ± 0.48ab	45.26 ± 15.45ab
Radish	Manure biochar + 1×	7.02 ± 0.56ab	46.72 ± 1.03abc	57.82 ± 3.49abc	5.04 ± 0.27a	63.42 ± 8.62a
Radish	Wood biochar	6.74 ± 0.04bcd	31.68 ± 3.45d	7.01 ± 11.64d	3.97 ± 0.35abc	28.79 ± 11.34ab
Radish	Wood biochar + slurry	6.90 ± 0.16abc	32.58 ± 2.55cd	10.05 ± 8.61cd	3.74 ± 0.35bc	21.17 ± 11.28b
Radish	Wood biochar NH3 + CO2	6.45 ± 0.06cd	50.52 ± 8.56ab	70.65 ± 28.92ab	5.05 ± 0.58a	63.67 ± 18.83a
Radish	Wood biochar + 1×	6.48 ± 0.14cd	48.51 ± 2.66ab	63.88 ± 8.97ab	5.03 ± 0.55a	63.10 ± 17.80a
Tomato	0× fert	6.11 ± 0.07d	39.70 ± 3.52def	NA	3.52 ± 0.43bcd	NA
Tomato	0.25× fert	6.15 ± 0.18d	46.36 ± 4.73cde	16.79 ± 11.92cde	3.93 ± 0.66abcd	11.81 ± 18.76abcd
Tomato	0.5× fert	6.33 ± 0.55cd	52.98 ± 2.68bc	33.46 ± 6.74bc	4.20 ± 0.40abcd	19.49 ± 11.37abcd
Tomato	1× fert	6.17 ± 0.02d	60.72 ± 3.40ab	52.95 ± 8.58ab	3.84 ± 0.78abcd	9.10 ± 22.11abcd
Tomato	1.5× fert	6.36 ± 0.30cd	71.55 ± 11.10a	80.23 ± 27.97a	3.11 ± 0.60d	− 11.59 ± 16.98d
Tomato	Manure biochar	7.08 ± 0.12a	34.26 ± 2.42f	− 13.69 ± 6.09f	3.36 ± 0.28cd	− 4.48 ± 7.89cd
Tomato	Manure biochar + slurry	7.07 ± 0.13a	36.95 ± 1.50ef	− 6.91 ± 3.78ef	3.63 ± 0.40bcd	3.13 ± 11.34bcd
Tomato	Manure biochar CO2 + NH3	6.83 ± 0.46abc	51.64 ± 4.60bc	30.09 ± 11.58bc	4.55 ± 0.24ab	29.30 ± 6.71ab
Tomato	Manure biochar + 1×	7.05 ± 0.03ab	49.75 ± 3.39bcd	25.32 ± 8.55bcd	4.40 ± 0.48abc	25.18 ± 13.67abc
Tomato	Wood biochar	6.30 ± 0.14cd	35.60 ± 3.47ef	− 10.33 ± 8.74ef	3.68 ± 0.21bcd	4.62 ± 5.89bcd
Tomato	Wood biochar + slurry	6.47 ± 0.12bcd	40.16 ± 2.27def	1.16 ± 5.73def	3.77 ± 0.50abcd	7.18 ± 14.22abcd
Tomato	Wood biochar NH3 + CO2	6.32 ± 0.11cd	51.79 ± 1.76bc	30.45 ± 4.42bc	4.33 ± 0.31abc	23.19 ± 8.73abc
Tomato	Wood biochar + 1×	6.25 ± 0.05cd	57.20 ± 4.41bc	44.10 ± 11.11bc	4.86 ± 0.44a	38.26 ± 12.56a
Marigold	0× fert	6.35 ± 0.13cd [ghij]	35.63 ± 3.87de [ghijklm]	NA	2.81 ± 0.36bc [hij]	NA
Marigold	0.25× fert	6.28 ± 0.14cd [hij]	40.37 ± 7.21bcde [efghijklm]	13.28 ± 20.25bcde [ghijklm]	3.38 ± 0.31abc [defghij]	20.27 ± 10.89abc [bcdefg]
Marigold	0.5× fert	6.30 ± 0.04cd [hij]	38.97 ± 6.45cde [efghijklm]	9.36 ± 18.10cde [ghijklm]	3.59 ± 0.57ab [cdefghij]	27.73 ± 20.15ab [abcdefg]
Marigold	1× fert	6.15 ± 0.14d [j]	51.63 ± 4.49abc [bcdef]	44.89 ± 12.61abc [bcdefghi]	3.63 ± 0.60ab [cdefghij]	28.98 ± 21.20ab [abcdefg]
Marigold	1.5× fert	6.25 ± 0.11cd [hij]	61.36 ± 6.64a [ab]	72.20 ± 18.65a [abcd]	3.66 ± 0.37ab [cdefghij]	30.22 ± 13.25ab [abcdef]
Marigold	Manure biochar	7.46 ± 0.16a []	31.50 ± 5.24e [m]	− 11.60 ± 14.71e [lm]	2.69 ± 0.27bc [ij]	− 4.27 ± 9.67bc [efg]
Marigold	Manure biochar + slurry	7.35 ± 0.43a []	34.10 ± 4.93de [ijklm]	− 4.30 ± 13.83de [jklm]	2.93 ± 0.46bc [ghij]	4.00 ± 16.51bc [cdefg]
Marigold	Manure biochar CO2 + NH3	7.41 ± 0.24a []	42.74 ± 4.38bcde [defghijklm]	19.95 ± 12.29bcde [efghijklm]	2.43 ± 0.36c [j]	− 13.72 ± 12.77c [fg]
Marigold	Manure biochar + 1×	7.35 ± 0.04a []	52.28 ± 0.00abc [bcdefgh]	46.71 ± 0.00abc [abcdefghij]	3.20 ± 0.00abc [defghij]	13.78 ± 0.00abc [abcdefg]
Marigold	Wood biochar	6.53 ± 0.19cd []	32.40 ± 2.46e [jklm]	− 9.08 ± 6.92e [klm]	3.56 ± 0.31ab [defghij]	26.58 ± 10.89ab [abcdefg]
Marigold	Wood biochar + slurry	7.03 ± 0.18ab []	33.20 ± 1.63de [jklm]	− 6.84 ± 4.56de [jklm]	3.14 ± 0.31bc [efghij]	11.64 ± 11.16bc [bcdefg]
Marigold	Wood biochar NH3 + CO2	6.62 ± 0.13bc []	46.44 ± 9.15bcd [cdefghijk]	30.33 ± 25.67bcd [defghijkl]	3.66 ± 0.44ab [cdefghij]	30.22 ± 15.82ab [abcdef]
Marigold	Wood biochar + 1×	6.51 ± 0.15cd []	53.33 ± 3.45ab [bcde]	49.66 ± 9.67ab [abcdefgh]	4.30 ± 0.33a [abcdef]	52.80 ± 11.58a [ab]
Radish	0× fert	6.48 ± 0.12cd []	29.60 ± 7.33d [m]	NA	3.08 ± 0.27c [fghij]	NA
Radish	0.25× fert	6.51 ± 0.16cd []	40.06 ± 4.41bcd [efghijklm]	35.33 ± 14.89bcd [cdefghij]	3.87 ± 0.52abc [abcdefghi]	25.39 ± 16.91ab [abcdefg]
Radish	0.5× fert	6.34 ± 0.14d []	42.74 ± 7.71abcd [defghijklm]	44.37 ± 26.04abcd [bcdefghi]	4.09 ± 0.28abc [abcdefgh]	32.69 ± 9.13ab [abcde]
Radish	1× fert	6.35 ± 0.15d []	53.04 ± 6.73ab [bcde]	79.17 ± 22.74ab [abc]	4.13 ± 0.50abc [abcdefg]	34.06 ± 16.35ab [abcde]
Radish	1.5× fert	6.37 ± 0.14d []	55.94 ± 8.38a [bcd]	88.96 ± 28.30a [a]	4.39 ± 0.83ab [abcde]	42.25 ± 26.80ab [abcd]
Radish	Manure biochar	7.22 ± 0.10ab []	30.19 ± 4.82d [m]	1.99 ± 16.27d [ijklm]	3.65 ± 0.84bc [cdefghij]	18.25 ± 27.22b [bcdefg]
Radish	Manure biochar + slurry	7.31 ± 0.12a []	31.60 ± 1.78d [lm]	6.74 ± 6.00d [hijklm]	3.93 ± 0.22abc [abcdefghi]	27.33 ± 7.19ab [abcdefg]
Radish	Manure biochar CO2 + NH3	7.25 ± 0.13a []	55.28 ± 8.68a [bcd]	86.75 ± 29.34a [ab]	4.48 ± 0.48ab [abcd]	45.26 ± 15.45ab [abc]
Radish	Manure biochar + 1×	7.02 ± 0.56ab []	46.72 ± 1.03abc [bcdefghij]	57.82 ± 3.49abc [abcdef]	5.04 ± 0.27a [a]	63.42 ± 8.62a [a]
Radish	Wood biochar	6.74 ± 0.04bcd []	31.68 ± 3.45d [klm]	7.01 ± 11.64d [hijklm]	3.97 ± 0.35abc [abcdefghi]	28.79 ± 11.34ab [abcdefg]
Radish	Wood biochar + slurry	6.90 ± 0.16abc []	32.58 ± 2.55cd [jklm]	10.05 ± 8.61cd [ghijklm]	3.74 ± 0.35bc [bcdefghij]	21.17 ± 11.28b [bcdefg]
Radish	Wood biochar NH3 + CO2	6.45 ± 0.06cd []	50.52 ± 8.56ab [bcdef]	70.65 ± 28.92ab [abcd]	5.05 ± 0.58a [a]	63.67 ± 18.83a [a]
Radish	Wood biochar + 1×	6.48 ± 0.14cd []	48.51 ± 2.66ab [bcdefghi]	63.88 ± 8.97ab [abcde]	5.03 ± 0.55a [ab]	63.10 ± 17.80a [a]
Tomato	0× fert	6.11 ± 0.07d []	39.70 ± 3.52def [efghijklm]	NA	3.52 ± 0.43bcd [defghij]	NA
Tomato	0.25× fert	6.15 ± 0.18d []	46.36 ± 4.73cde [cdefghijkl]	16.79 ± 11.92cde [fghijklm]	3.93 ± 0.66abcd [abcdefghi]	11.81 ± 18.76abcd [bcdefg]
Tomato	0.5× fert	6.33 ± 0.55cd []	52.98 ± 2.68bc [bcde]	33.46 ± 6.74bc [defghijk]	4.20 ± 0.40abcd [abcdefg]	19.49 ± 11.37abcd [bcdefg]
Tomato	1× fert	6.17 ± 0.02d []	60.72 ± 3.40ab [abc]	52.95 ± 8.58ab [abcdefg]	3.84 ± 0.78abcd [abcdefghi]	9.10 ± 22.11abcd [cdefg]
Tomato	1.5× fert	6.36 ± 0.30cd []	71.55 ± 11.10a [a]	80.23 ± 27.97a [ab]	3.11 ± 0.60d [efghij]	− 11.59 ± 16.98d [g]
Tomato	Manure biochar	7.08 ± 0.12a []	34.26 ± 2.42f [hijklm]	− 13.69 ± 6.09f [m]	3.36 ± 0.28cd [defghij]	− 4.48 ± 7.89cd [efg]
Tomato	Manure biochar + slurry	7.07 ± 0.13a []	36.95 ± 1.50ef [fghijklm]	− 6.91 ± 3.78ef [jklm]	3.63 ± 0.40bcd [cdefghij]	3.13 ± 11.34bcd [defg]
Tomato	Manure biochar CO2 + NH3	6.83 ± 0.46abc []	51.64 ± 4.60bc [bcdef]	30.09 ± 11.58bc [defghijklm]	4.55 ± 0.24ab [abcd]	29.30 ± 6.71ab [abcdefg]
Tomato	Manure biochar + 1×	7.05 ± 0.03ab []	49.75 ± 3.39bcd [bcdefg]	25.32 ± 8.55bcd [efghijklm]	4.40 ± 0.48abc [abcde]	25.18 ± 13.67abc [abcdefg]
Tomato	Wood biochar	6.30 ± 0.14cd []	35.60 ± 3.47ef [ghijklm]	− 10.33 ± 8.74ef [klm]	3.68 ± 0.21bcd [cdefghij]	4.62 ± 5.89bcd [cdefg]
Tomato	Wood biochar + slurry	6.47 ± 0.12bcd []	40.16 ± 2.27def [efghijklm]	1.16 ± 5.73def [ijklm]	3.77 ± 0.50abcd [abcdefghij]	7.18 ± 14.22abcd [cdefg]
Tomato	Wood biochar NH3 + CO2	6.32 ± 0.11cd []	51.79 ± 1.76bc [bcde]	30.45 ± 4.42bc [defghijkl]	4.33 ± 0.31abc [abcdef]	23.19 ± 8.73abc [abcdefg]
Tomato	Wood biochar + 1×	6.25 ± 0.05cd []	57.20 ± 4.41bc [abcd]	44.10 ± 11.11bc [bcdefghi]	4.86 ± 0.44a [abc]	38.26 ± 12.56a [abcd]

Letters indicate significant differences from a one-way anova between amendments within plant type (p < 0.05; n = 4; results for a two-way anova include in supplementary online material Table SI 5).

Increase in plant biomass (sum of root and shoot biomass) grown with class="Chemical">urea class="Chemical">n class="Chemical">fertilizer (green points), manure biochar (brown points) or wood biochar (gray points) amendments relative to unamended plants (0×). The amount of plant-available N in each type of amendment in parentheses. Letters above the bars indicate significant differences between amendments within plant type (p < 0.05; n = 4; whiskers indicate standard errors).

Letters indicate significant difn class="Chemical">fereclass="Chemical">nces from a oclass="Chemical">ne-way aclass="Chemical">nova betweeclass="Chemical">n ameclass="Chemical">ndmeclass="Chemical">nts withiclass="Chemical">n placlass="Chemical">nt type (p < 0.05; class="Chemical">n = 4; results for a two-way aclass="Chemical">nova iclass="Chemical">nclude iclass="Chemical">n supplemeclass="Chemical">ntary oclass="Chemical">nliclass="Chemical">ne material Table SI 5).

Difclass="Chemical">fereclass="Chemical">nt forms of N added with biochars had difclass="Chemical">n class="Chemical">ferent effects on plant growth. Wood biochar applied together with urea (1×) promoted 0–18% greater plant growth than wood biochar treated with NH3 despite the fact that the total N content in both types of amendments was identical, 1.88%. Furthermore, wood biochar and urea promoted 29–37% more plant growth compared to slurry-immersed biochar despite the similar total N values between the two types of amendments, 1.88% vs 1.84% (Tables 1, 4).

Difclass="Chemical">fereclass="Chemical">nces iclass="Chemical">n placlass="Chemical">nt growth with the type of biochar aclass="Chemical">nd added N were also appareclass="Chemical">nt. Overall, placlass="Chemical">nt growth was 6–34% lower after addiclass="Chemical">ng maclass="Chemical">nure biochar exposed to class="Chemical">n class="Chemical">NH3 compared to adding wood biochar exposed to NH3. These effects of adding manure biochar exposed to NH3 on plant growth varied between plant type. In a one-way anova of the effect of amendment type on plant growth, between plant types, we observed that supplementing manure biochar with N by exposing it to NH3 significantly improved tomato growth above tomatoes grown with only manure biochar, by 35%. Supplementing manure biochar with urea fertilizer significantly improved radish growth by 38% compared to additions of manure biochar alone (Fig. 1, Table 4).

Using a two-way anova of the efclass="Chemical">fect of ameclass="Chemical">ndmeclass="Chemical">nts aclass="Chemical">nd placlass="Chemical">nt types oclass="Chemical">n growth, placlass="Chemical">nt growth iclass="Chemical">n class="Chemical">n class="Species">radishes amended with manure or wood biochar added with urea fertilizer and wood biochar treated with NH3 were significantly higher compared to the growth of all plant types grown with manure biochar alone. Furthermore, no significant differences in plant growth were apparent between radish and tomato amended with manure or wood biochars treated with NH3 or added with urea fertilizer, compared to adding urea alone, in any amount (Fig. SI 1, Table SI 5). Thus, supplementing wood or manure biochar with N from NH3 exposure or urea fertilizer proved just as good for plants as adding urea fertilizer alone.

Germination was afclass="Chemical">fected by placlass="Chemical">nt type aclass="Chemical">nd ameclass="Chemical">ndmeclass="Chemical">nt, aclass="Chemical">nd was lower with greater class="Chemical">nutrieclass="Chemical">nt additioclass="Chemical">ns for class="Chemical">n class="Species">marigold and radish, and higher with the highest nutrient additions for tomato. Unamended and manure biochar-amended marigold and radish had the highest germination rates, 80–90%, while tomato plants amended with the highest urea application rates, 1.5×, and wood biochar, reached 100% germination (Table SI 4).

After 40 days, the pH of pots amended with manure biochar (7.02–7.46) was significantly higher than the potting mix amended with class="Chemical">urea (1×) or the uclass="Chemical">nameclass="Chemical">nded potticlass="Chemical">ng mix (6.11–6.48), based oclass="Chemical">n both a oclass="Chemical">ne-way aclass="Chemical">nova of the efclass="Chemical">n class="Chemical">fect of amendment type on pH (Table 4) and a two-way anova of the effect of amendment type and plant type on pH (Table SI 5). The pH of pots with wood biochar immersed in the liquid manure (6.47–7.03) was highest among all wood biochar treatments (6.25–6.74). In contrast, wood biochar alone did not significantly increase the pH of the potting mix, relative to the unamended pots (Table 4, Table SI 5).

Plant N uptake increased with increasing N additions (Fig. 2). The range of class="Chemical">urea additioclass="Chemical">ns eclass="Chemical">ncompassed N additioclass="Chemical">ns of all other ameclass="Chemical">ndmeclass="Chemical">nts (Fig. 3) iclass="Chemical">ndicaticlass="Chemical">ng positive growth respoclass="Chemical">nses across all rates of added N. class="Chemical">n class="Chemical">Nitrogen from wood biochar exposed to NH3 appears to be as plant available as urea 1×, since N uptake was slightly higher per unit N added (Fig. 3). Furthermore, the N uptake of plants grown with wood biochar treated with NH3 was not significantly different than the N uptake of plants grown with urea 1×, based on either the one-way anova of the effect of amendment on N uptake, between plant types or the two-way anova evaluating N uptake as affected by both amendment and plant type (Fig. 2, Table 4, Fig. SI 2, Table SI 5). Nitrogen from manure biochar exposed to NH3 appears to be less plant available than urea, since N uptake was smaller per unit N added (Fig. 3), although these results varied between plant type. Radish plants grown with manure biochar treated with NH3 had similar N uptake as when grown with the highest urea treatment.

Figure 2

Total nitrogen uptake in shoot and root biomass of plants grown with urea fertilizer, manure biochar or wood biochar amendments or no amendments (0×). Letters above the bars indicate significant differences between amendments within plant type (p < 0.05; n = 4).

Figure 3

Nitrogen uptake of shoots and roots of plants grown with amendments varying in initial N content (points). “Added N” refers to the KCl-extractable N of all amendments, with the assumption that all urea-N is KCl-extractable. A linear regression was conducted for urea-based amendments (urea, biochar + urea). The 95% confidence interval is shown by the gray shaded line, and the R2 value for the quadratic equation is presented (n = 4).

Total class="Chemical">nitrogen uptake iclass="Chemical">n shoot aclass="Chemical">nd root biomass of placlass="Chemical">nts growclass="Chemical">n with class="Chemical">n class="Chemical">urea fertilizer, manure biochar or wood biochar amendments or no amendments (0×). Letters above the bars indicate significant differences between amendments within plant type (p < 0.05; n = 4).

class="Chemical">Nitrogen uptake of shoots aclass="Chemical">nd roots of placlass="Chemical">nts growclass="Chemical">n with ameclass="Chemical">ndmeclass="Chemical">nts varyiclass="Chemical">ng iclass="Chemical">n iclass="Chemical">nitial N coclass="Chemical">nteclass="Chemical">nt (poiclass="Chemical">nts). “Added N” reclass="Chemical">n class="Chemical">fers to the KCl-extractable N of all amendments, with the assumption that all urea-N is KCl-extractable. A linear regression was conducted for urea-based amendments (urea, biochar + urea). The 95% confidence interval is shown by the gray shaded line, and the R2 value for the quadratic equation is presented (n = 4).

When added with class="Chemical">urea, biochar did class="Chemical">not iclass="Chemical">ncrease N uptake, compared to N uptake with class="Chemical">n class="Chemical">urea additions alone. However, adsorption of NH3 onto biochars provided both immediately-available plant-available N and longer-term mineralizable N, allowing for greater plant uptake than equivalent amendments of urea. The initial KCl-extractable N in manure biochar exposed to NH3 was comparable to urea 0.5× additions, indicating the mineralizability of N incorporated through NH3-exposure of manure biochar (Fig. 3). The difference in total N in wood biochar following NH3 exposure was equal to the amount of N in urea 1× addition, yet the KCl-extractable N was comparable to the amount of N in urea 0.25×. Nevertheless, compared to urea 0.25×, plant N uptake in wood biochar sorbed with NH3 was 12–26% greater. Moreover, in all experiments, NH3-exposed biochars outperformed biochars immersed in the liquid fraction, increasing N uptake by 29–55% for wood biochar and 25–75% for manure.

Discussion

The class="Chemical">feedstock aclass="Chemical">nd pyrolysis coclass="Chemical">nditioclass="Chemical">ns used to produce biochar for these experimeclass="Chemical">nts did class="Chemical">not result iclass="Chemical">n class="Chemical">n class="Disease">phototoxicity, as no difference in germination was detectable between plants with or without biochar. The moderately high temperatures used for pyrolysis, 500 °C may have reduced the phototoxicity reported from lower-temperature biochars[49]. The greater increase in KCl-extractable N than in total N in manure biochar exposed to NH3 may be related to CO2 exposure that increased extractability of the N already present in the biochar. Yet it is unclear whether CO2 can solubilize trapped inorganic N species or cleave bonds of organic N. Either way, all N from NH3 added to manure biochar was KCl-extractable. On the other hand, the increase in total N in wood biochar exposed to NH3 was 19-fold greater than manure biochar exposed to NH3, even though both materials contained the same amount of KCl-extractable N. This means that the majority of N in wood biochar treated with NH3 more strongly interacted with the biochar than the NH3-derived N in manure biochar, in alignment with previous studies[29,40] and was therefore not plant-available.

Capturing volatile class="Chemical">NH3 from the liquid fractioclass="Chemical">n of dairy waste oclass="Chemical">nto sorbeclass="Chemical">nts such as biochars was more successful for recycliclass="Chemical">ng class="Chemical">nutrieclass="Chemical">nts for use as potticlass="Chemical">ng media thaclass="Chemical">n immersiclass="Chemical">ng sorbeclass="Chemical">nts iclass="Chemical">n the liquid fractioclass="Chemical">n. Placlass="Chemical">nt N uptake was 25–75% aclass="Chemical">nd 29–55% greater iclass="Chemical">n maclass="Chemical">nure aclass="Chemical">nd wood biochars, respectively, for the class="Chemical">n class="Chemical">NH3 treatment compared to slurry immersion. Lower plant growth and N uptake with biochar treated with the slurry could be attributed to a combination of both the lower amount of readily plant-available N (i.e., KCl-extractable) and lower rates of mineralization of organic N. The plant-availability of organic N in the liquid fraction is time-dependent and varies with manure age and processing. Pettygrove et al.[50] determined that 27–44% of total N in fresh lagoon slurry was mineralized after 6 weeks when incubated in a sandy loam soil. The low pH of our peat potting media may have slowed microbial mineralization rates of slurry N compared to rates reported for mineral soils[51].

Delivering N from class="Chemical">NH3-eclass="Chemical">nriched maclass="Chemical">nure biochar to placlass="Chemical">nts was just as efclass="Chemical">n class="Chemical">fective as adding urea with manure biochar. The increase in plant N uptake relative to the control was 43–55% vs. 47–52%, respectively. The high plant-availability of N in manure biochar doped with N may indicate that an NH4+ salt such as NH4HCO3 formed from repeated exposure to NH3 and CO2, preserving all sorbed N in a plant-available form, as observed with CO2 captured within NH3 solvents[52-54]. Mineral forms of N were detected in human manure biochars and wood biochars exposed to repeated intervals of NH3 and CO2 using XPS, although two-fold more electrostatically-sorbed NH4+ was detected in NH3- and CO2-exposed wood biochar compared to NH3- and CO2-exposed manure biochar[40].

Using median international prices for class="Chemical">fertilizer class="Chemical">nutrieclass="Chemical">nts, the value of extractable N iclass="Chemical">n biochars exposed to class="Chemical">n class="Chemical">NH3 is 1.7 USD Mg−1 for manure biochar and 1.5 USD Mg−1 for wood biochar[39]. The benefit of plant-extractable minerals (Mehlich-III extractable) in dairy manure biochar on plant growth was not evaluated experimentally, since equivalent extractable nutrients in manure biochar were added to all other treatments. Nevertheless, we can estimate the added monetary value of plant-extractable P and K in manure biochar, together with plant-available N, as 15.4 USD Mg−1 for manure biochar exposed to NH3 and 9.5 USD Mg−1 for wood biochar exposed to NH3 using literature values[39].

The increase in plant N uptake with additions of manure biochar exposed to class="Chemical">NH3 relative to uclass="Chemical">nameclass="Chemical">nded placlass="Chemical">nts reached 20–87% or 7.1–25.7 class="Chemical">n class="Chemical">mg N pot−1, which, accounting for the amount of biochar added to each pot, is equivalent to 1–3.6 kg N Mg−1 manure biochar. If we account for more than 624,000 dairy cows in NY State[55], each generating approximately 18.8 Mg (dry) manure year−1[56], this amount of available N in NH3-exposed manure biochar scales to 11,732–42,232 Mg N year−1 or 6–21.5 million USD year−1, based on the average price of N fertilizer (0.51 USD kg−1[39]). With approximately 51,360 Mg N applied to grain corn in NY State in 2018[4,6], separated dairy manure treated with NH3 can offset 23–82% of N fertilizer needs while stabilizing both the solid and liquid fraction of manure for addressing both environmental pollution as well as recycling N to agriculture.

A novel class="Chemical">fertilizer has beeclass="Chemical">n developed from N-rich dairy waste which performs equally well compared to coclass="Chemical">nveclass="Chemical">ntioclass="Chemical">nal class="Chemical">n class="Chemical">urea fertilizer per unit applied N. Not only did NH3-sorbed wood biochar contain similar amounts of plant-available N as NH3-manure biochar, but promoted greater plant biomass growth and plant-N uptake than manure biochar or conventional urea fertilizer. Despite the greater NH3-derived N enrichment in wood than manure biochar, the precipitation of NH3-salts on manure biochar in comparison to chemisorption of NH3 to wood, points at manure biochar being a more efficient approach to recycle manure N as a fertilizer.

This research demonstrates that it is possible to convert dairy manure solids into a biochar that can adsorb volatile class="Chemical">NH3 for use as a N class="Chemical">n class="Chemical">fertilizer. Conversion of dairy manures with high water contents into a dry and N-rich soil amendment with N use efficiency by plants commensurate with urea fertilizer may provide life-cycle benefits to water quality and greenhouse gas emissions that should be studied in the future. Future studies should include scaling up CO2 and NH3 exposure of biochar. Multi-year field studies with crops such as corn should examine the long-term availability of N-doped biochars and potential differences in leaching and gaseous N losses. The feasibility of cost-effectively operating dairy manure pyrolysis as well as adsorption of N to biochars should be studied on farms and by small industry. Techno-economic studies should quantify the ability to optimize the production and distribution of such fertilizers at different scales and under different economic conditions.

Materials and methods

Enriching biochar amendments with nitrogen

We evaluated the efclass="Chemical">fect of N-eclass="Chemical">nriched dairy maclass="Chemical">nure biochar aclass="Chemical">nd N-eclass="Chemical">nriched wood biochar oclass="Chemical">n placlass="Chemical">nt growth. The first type of biochar was created from aclass="Chemical">naerobically-digested dairy maclass="Chemical">nure solids (‘solid fractioclass="Chemical">n’), screw-pressed at a dairy farm iclass="Chemical">n upstate New York iclass="Chemical">n April 2018. The solid fractioclass="Chemical">n was charred iclass="Chemical">n a modified muffle furclass="Chemical">nace with a rotaticlass="Chemical">ng paddle at 500 °C for 30 miclass="Chemical">n. The liquid fractioclass="Chemical">n of the screw-pressed dairy maclass="Chemical">nure was also collected, sieved with a 425 μm mesh sieve to remove solids, aclass="Chemical">nd stored at − 4 °C. The secoclass="Chemical">nd type of biochar made from class="Chemical">n class="Species">Douglas fir wood (Pseudotsuga menziesii) using high-temperature gasification, was provided by Green Tree Garden Supply (Ithaca, NY). Both biochars were sieved to below 2 mm particle size.

Manure biochar and wood biochar were enriched with N through two methods: (1) repeated, sequential exposure to class="Chemical">CO2 aclass="Chemical">nd class="Chemical">n class="Chemical">NH3, or (2) immersion in the sieved liquid fraction ('liquid fraction'), which contained a mixture of N species. The effect of these two N-enriched amendments on plant growth was compared to (3) separate additions of each biochar (manure or wood biochar) with urea fertilizer, (4) urea additions without biochar, (5) separate additions of each biochar without urea fertilizer, or (6) no additions of biochar or urea.

For the first N-enrichment method, 200 g of biochar were loaded in a 4-L Buechner funnel suspended upright inside a drying oven at 30 °C. The bottom of the funnel was connected to gas flow via class="Chemical">silicone tubiclass="Chemical">ng, aclass="Chemical">nd the top covered with a lid aclass="Chemical">nd with parafilm. Maclass="Chemical">nure biochar was first exposed to class="Chemical">n class="Chemical">CO2 gas (Instrument grade, Airgas, Ithaca, NY) for one hour. After one hour, CO2 flow ceased, and NH3 flow commenced for one hour. Ammonia gas was generated by pumping air at 4.72 × 10–4 m3 s−1 through a sealed Erlenmeyer flask containing 1 L of 2 M NH4OH (pH 12.43) kept on a hot plate at 30 °C. This process was repeated three times (manure biochar CO2 + NH3). To enrich wood biochar with N, we reversed the order of gas exposure, first NH3 then CO2, also for three exposure intervals (wood biochar NH3 + CO2).

For the second N-enrichment method, biochars were immersed in the liquid fraction for 1.5 h at a ratio of 143 g:1 L. The biochar-slurry suspension was contained in a large glass beaker on a hot plate at 30 °C. After the immersion period, the suspension was sieved through a 425-μm mesh sieve to remove residual liquid. Biochars were dried at 80 °C for 2 days. We did not expose slurry-treated biochars to n class="Chemical">CO2.

Duplicate sets of each biochar-N mixture were homogenized and stored in sealed glass jars. The four biochar treatments evaluated were: (1) manure biochar treated with class="Chemical">CO2 + class="Chemical">n class="Chemical">NH3; (2) wood biochar treated with NH3 + CO2; (3) dairy manure biochar immersed in the liquid fraction; and (4) wood biochar immersed in the liquid fraction. To simplify notation, when describing biochars treated with CO2 + NH3 (manure) or NH3 + CO2 (wood), we will refer to NH3 exposure without referring to CO2, as NH3 uptake was our focus.

Chemical analysis of amendments

Subsamples of amendments were milled and analyzed for total C and N by dry combustion (Elementar; vario EL class="Chemical">cube, Laclass="Chemical">ngeclass="Chemical">nselbold, Germaclass="Chemical">ny). Noclass="Chemical">n-milled ameclass="Chemical">ndmeclass="Chemical">nt subsamples were extracted with 2 M class="Chemical">n class="Chemical">KCl at a ratio of 0.1 g biochar mL−1 KCl and tested for NH4+ and NO3− through a colorimetric method on an auto-flow analyzer (AA3 HR AutoAnalyzer, Seal Analytical, Mequon, WI).

Non-milled amendment samples were also analyzed for plant-available and total elements. Plant-available nutrients were extracted using a class="Chemical">Mehlich III solutioclass="Chemical">n at a ratio of 0.1 g mL−1. Total elemeclass="Chemical">ntal aclass="Chemical">nalysis was coclass="Chemical">nducted oclass="Chemical">n 0.5 g of uclass="Chemical">nmilled biochar spiked with 0.25 class="Chemical">n class="Chemical">mg L−1 yttrium as an internal standard. Samples were dissolved in a mixture of 30% perchloric acid in nitric acid (70%) at 180 °C. Both Mehlich III extracts and digestate solutions were analyzed by inductively-coupled plasma optical emission spectroscopy (ICP-OES; Spectro Arcos, Ametek Materials Analysis, Kleve, Germany).

Greenhouse trial to evaluate amendments

A six-week growth trial was conducted to test amendment performance. Three types of plants, either class="Species">marigold, class="Chemical">n class="Species">radish, and tomato, were grown in a peat potting mix (TH6, Theriault and Hachey Peat Moss Ltd., Baie Sainte-Anne, New Brunswick Canada) in square pots 0.3 L by volume to which biochars were added. Seeds were obtained from commercial companies (radish and tomato from Burpee and marigold from Park Seed) and its use complies with relevant institutional, national, and international guidelines and legislation. Wood biochar amendments were added at 10% bulk volume of the square pots, while manure biochar amendments were added at an equivalent C amount as wood biochar. This resulted in unequal mass and nutrients additions (other than C) between wood biochar and manure biochar. To correct for the increased non-N nutrient addition from manure biochar a mixture of dry nutrients was added to all non-manure biochar treatments based on the Mehlich III extractable nutrient content of manure biochar (Tables SI 1, Table SI 2).

We tested the efclass="Chemical">fect of class="Chemical">n class="Chemical">urea additions to compare the effect of N source on plant growth (Table SI 2). Nitrogen sources included biochars enriched in N through exposure to NH3, biochars enriched in N through immersion into the liquid fraction, and urea fertilizer additions. Urea additions were adjusted to equal the increase in total N on wood biochar after sequential exposure to NH3 and CO2 (Table SI 3), 4.9 g N kg biochar−1. We did not add slurry alone, as we focused on adding nutrients and fertilizers as dry materials.

For each plant type, five seeds were planted in each pot after filling with the respective media and nutrient additions. Seedlings were thinned to a single seedling after two weeks, and the germination rate recorded for each pot. Pots in which no seeds germinated received seedlings from replicate pots of the same treatment in which more than one seed germinated.

The N equivalency of the N added with the biochar was quantified in comparison to an N-response class="Chemical">curve measured from placlass="Chemical">nts growclass="Chemical">n with class="Chemical">n class="Chemical">urea fertilizer but without biochar (Urea 99% reagent grade, Sigma Aldrich). Five urea application rates were tested based on the increase in total N on wood biochar + NH3 (Table 1, Table SI 3): (1) 1.5 times the N increase of wood biochar after NH3 and CO2 exposure (1.5×) = 52.65 mg N pot−1 or 176.8 kg N ha−1, (2) the equivalent N-application rate as the N increase of wood biochar (1×) = 35.10 mg N pot−1 or 117.9 kg N ha−1, (3) half of the N increase (0.5×) = 17.55 mg N pot−1 or 58.95 kg N ha−1, (4) one quarter of the N increase (0.25×) = 8.78 mg N pot−1 or 29.47 kg N ha−1, and (5) no added fertilizer (0×). The urea 1 × addition is in the range of the suggested N application for corn production in New York State (78–146 kg N ha−−1 without sod history, legume mixture or manure additions), which is highly variable with soil type and with cropping history[57]. As mentioned above, we also tested the plant effect of each biochar added with urea (1×) (Table SI 3).

All plants were irrigated daily with reverse osmosis class="Chemical">water to 90% of field capacity, determiclass="Chemical">ned gravimetrically. The field capacity of class="Chemical">n class="Chemical">TH6 media amended with wood biochar or manure biochar was calculated as the amount of water remaining in a 0.3 L PVC cylinder filled with soil after saturation and draining overnight. Irrigation was lowered from field capacity by 10% to prevent leaching during the experiment.

To overcome the hydrophobicity of the potting mixtures, pots were initially placed in trays of class="Chemical">water to moisteclass="Chemical">n them from the bottom-up. From the secoclass="Chemical">nd day of the experimeclass="Chemical">nt uclass="Chemical">ntil day 12, pots were misted from the top daily. After germiclass="Chemical">natioclass="Chemical">n oclass="Chemical">n day 12, pots were weighed to determiclass="Chemical">ne the amouclass="Chemical">nt of class="Chemical">n class="Chemical">water needed to reach 90% of field capacity. A description of the thirteen potting mixtures and irrigation amounts is provided in the supplementary information (Table SI 2).

Plants were harvested after 40 days, and wet shoot and root biomass recorded. Shoots were class="Chemical">cut at the soil surface, aclass="Chemical">nd roots were excavated from each pot. Roots were isolated via washiclass="Chemical">ng aclass="Chemical">nd sieviclass="Chemical">ng. Dry root aclass="Chemical">nd shoot biomass was determiclass="Chemical">ned after dryiclass="Chemical">ng at 65 °C for 3 days. The potticlass="Chemical">ng mix was dried at 105 °C for 3 days. Total C aclass="Chemical">nd N coclass="Chemical">nteclass="Chemical">nts iclass="Chemical">n shoots aclass="Chemical">nd roots were determiclass="Chemical">ned by dry combustioclass="Chemical">n. After the experimeclass="Chemical">nt, all potticlass="Chemical">ng mixtures were extracted with class="Chemical">n class="Chemical">Mehlich III to determine changes in plant-available nutrients. The pH of potting mixtures was measured before and after the growth trial in 1 g potting mixture in 20 mL deionized water.

For each of three plant types (class="Species">marigold = i1, class="Chemical">n class="Species">tomato = i2, radish = i) and biomass type (roots = j1, shoots = j2), the proportional increase in biomass and N uptake across four replicates (k = 1:4) of amended plants relative to the average of four replicates of unamended plants for the same plant and biomass type was calculated as follows:

The N-class="Chemical">fertilizer equivaleclass="Chemical">ncy of ameclass="Chemical">ndmeclass="Chemical">nts was calclass="Chemical">n class="Chemical">culated based on the difference in N uptake of plants grown with urea alone (1×) and plants grown with biochar amendments. Using market prices for mineral fertilizers[39], we also calculated the replacement value of the plant-available N, P, and K in amendments.

Statistics

Data analysis was carried out in RStudio[58] and graphs created using ggplot2[59]. Least squares of treatment means (LS means) were calclass="Chemical">culated usiclass="Chemical">ng emmeaclass="Chemical">ns[60]. Order-iclass="Chemical">ndepeclass="Chemical">ndeclass="Chemical">nt p values determiclass="Chemical">ned with the Studeclass="Chemical">nt-t test were adjusted usiclass="Chemical">ng Tukey’s method for compariclass="Chemical">ng a family of five estimates at the α = 0.05 threshold. Compact letter displays of pairwise comparisoclass="Chemical">ns for a sigclass="Chemical">nificaclass="Chemical">nce level of p < 0.05 were created usiclass="Chemical">ng multcompView[61]. Type I aclass="Chemical">nalysis of variaclass="Chemical">nce (ANOVA) was calclass="Chemical">n class="Chemical">culated using an order-dependent F test within the emmeans package. We present a one-way anova of the effect of amendment types on plant growth (dry weight) and plant N uptake in the main manuscript, and include both one-way anova and two-way anova evaluating the effect of amendment type and plant type, and the interaction between them, on plant growth (dry weight) and N uptake in the supplementary material. All mention of ‘significant differences’ refers to the probability of observing an F ratio greater than 0.05 given the null hypothesis, Pr(> F), or a p value < 0.05.

Supplementary Information.