Anaerobically digested poultry slaughterhouse wastes as fertiliser in agriculture

Bioresource Technology 78 (2001) 81±88

Anaerobically digested poultry slaughterhouse wastes as fertiliser in agriculture E. Salminen *, J. Rintala, J. H ark onen, M. Kuitunen, H. H ogmander, A. Oikari Department of Biological and Environmental Science, University of Jyv askyl a, P.O. Box 35, FIN-40351 Jyv askyl a, Finland Received 19 December 1999; received in revised form 15 June 2000; accepted 2 October 2000

Abstract Chemical and physical analysis, 27-d plant growth assays with carrot (Daucus carota) and Chinese cabbage (Brassica campestris var. chinensis), and 5-d phytotoxicity assays with Chinese cabbage and perennial ryegrass (Lolium perenne) were used to investigate the suitability of anaerobically digested poultry slaughterhouse waste for fertiliser in agriculture and the e€ect of aerobic posttreatment on the properties of the digested material. The digested material appeared to be rich in nitrogen. In 27-d assays with digested material as nitrogen source, carrots grew almost as well as those fertilised with a commercial mineral fertiliser used as reference, whereas, the growth of Chinese cabbage was inhibited. In further 5-d phytotoxicity assays, the digested material inhibited the germination and root growth of ryegrass and Chinese cabbage, apparently because of organic acids present in it. Aerobic post-treatment of the material reduced its phytotoxicity but, probably due to the volatilisation of ammonia, resulted in loss of nitrogen. Ó 2001 Published by Elsevier Science Ltd. Keywords: Aerobic post-treatment; Ammonia; Anaerobically digested material; Organic acids; Phytotoxicity assays; Plant growth assays; Poultry slaughterhouse waste

1. Introduction Agroindustries produce high quantities of organic wastes which are typically rich in nutrients and which can well be used in agriculture to conserve and recycle nutrients and to reduce waste discharge and use of chemical fertilisers (Marchaim et al., 1991; Shih, 1987). However, without sucient treatment these wastes may pose severe health risks, odour, environmental pollution, and visual problems, or their use may be legally banned altogether. Treatments may help to improve the physical and chemical properties of the waste and reduce its phytotoxicity (Marchaim et al., 1991; Sudradjat, 1990; Vermeulen et al., 1992). Anaerobic digestion is becoming an increasingly important means of organic waste management for several good reasons. It helps to convert a large part of degradable organic carbon to biogas to be used for energy, and it reduces pathogens and minimises odour while allowing most nutrients to remain in the digested material (Shih, 1987). *

Corresponding author. Tel.: +358-14-260-1211; fax: +358-14-2602321. E-mail address: [email protected].® (E. Salminen).

Anaerobic digestion converts a major part of organic nitrogen to ammonia, which is then directly available, though also potentially phytotoxic, for plants as a nitrogen source (Sudradjat, 1990; Tiquia et al., 1996; Wang, 1991). Similarly, organic acids, which are intermediates of anaerobic degradation, are potentially phytotoxic, and because they are microbial substrates, enhance microbial growth and thereby deplete soil oxygen and cause immobilisation of soil nitrogen (DeVleeschauwer et al., 1981; Lynch, 1977, 1980; Manios et al., 1989; Marable et al., 1993). Aerobic post-treatment can be used to ensure the maturation of anaerobically digested material and reduce the content of volatile inhibitors such as ammonia and organic acids (Sudradjat, 1990; Vermeulen et al., 1992). This process, however, can also result in a signi®cant loss of nitrogen through the volatilisation of ammonia (Rubñk, 1996; Sudradjat, 1990). The use of waste-derived materials for agricultural purposes is risky unless the material properties are carefully evaluated. Phytotoxicity assays can herein strongly and holistically support chemical analysis (Baud-Grasset et al., 1993). Because of little information available on the subject, we used chemical and physical analysis and vascular

0960-8524/01/$ - see front matter Ó 2001 Published by Elsevier Science Ltd. PII: S 0 9 6 0 - 8 5 2 4 ( 0 0 ) 0 0 1 6 0 - 7

82

E. Salminen et al. / Bioresource Technology 78 (2001) 81±88

plant assays to investigate the suitability of anaerobically digested poultry slaughterhouse waste for fertiliser in agriculture and the e€ect of aerobic post-treatment on the properties of the digested material. 2. Methods

The materials were used in plant assays as such (DM1, DM3 and DM4) or after aerobic post-treatment (DM2 and DM5). A commercial mineral fertiliser (total nitrogen content 160 g N/kg, Kemira Agro Oy, Finland) was used as reference in 27-d plant growth assays. 2.2. Aerobic post-treatments of digested materials

2.1. Test materials Five di€erent digested material samples (referred to as DM1±DM5) were obtained from two semi-continuously fed, laboratory-scale (3 l) mesophilic (32  1°C) continuously stirred digesters, treating poultry slaughterhouse waste (Salminen and Rintala, submitted). The waste (mixed fractions of bonemeal, blood, o€al and autoclaved feather from Atria, Nurmo, Finland) contained 31.2% of total solids (TS), 26.0% of volatile solids (VS), 24.3 g N/kg of Kjeldahl-N, ca. 152 g/kg of proteins and ca. 100 g/kg of lipids, and was diluted with distilled water to 3.1±9.4% of TS before use as feed in the digesters. Both the digesters were operated at a daily (5-days a week) loading of ca. 0.5 g of VS/l d, and a hydraulic retention time (HRT) of 50 d for 137 days and thereafter at a daily loading of ca. 0.8 g VS/l d and an HRT of 100 and 50 d. DM1, DM2, and DM5 were combinations of daily takes from the digesters, stored in an anaerobic storage vessel (21  1°C) between operation days 56±120, 125± 179 and 192±197, respectively. DM3 was material taken from the digesters on day 191, and DM4 was prepared by anaerobically incubating DM2 in batch-mode at 32  1°C for an additional 12 days. DM4 thus, served as anaerobic reference for aerobic treatments performed on DM2. Table 1 shows the characteristics of DM1±DM5.

The aerobic post-treatment of digested material samples DM2 and DM5 was conducted at 21  1°C in static Erlenmeyer ¯asks (250 ml), covered with aluminium foil. 100 ml of DM2 was incubated both with and without 100 ml of added inoculum (activated sludge, 1.7 g/l of suspended solids (SS), 1.2 g/l of volatile suspended solids (VSS)) from a municipal sewage treatment plant (Jyvaskyla, Finland). Incubations without DM2 were used to evaluate the decomposition of the inoculum alone, while those with DM2 and inoculum with 2 ml of added HgSO4 (2 g/l) served as abiotic controls. 100 ml of DM5 was incubated without inoculum and abiotic control. In all tests, distilled water was added to a volume of 202 ml. Air ¯ow was created with a Rena Air 100 aquarium air pump (USA) and introduced into the media through Penn Plax airstones (25 mm, USA) to maintain >2MgO2 /l. DM2 and DM5 were incubated for 7 days and 6 h, respectively. The pH, drifting in the range of 6.5±8.7, was adjusted to 7.0 (1 M HCl, 1 M NaOH) in 7-d incubations on days 1, 2 and 4, and in 6-h incubations after 30 min. 2.3. Plant assays The seeds of carrot (Daucus carota), Chinese cabbage (Brassica campestris var. chinensis), and perennial rye-

Table 1 Physical and chemical properties of digested material samples DM1±DM5 (D2 and D5 analysed before aerobic post-treatment)

a

Analysis

DM1 (mg/kg, except pH)

DM2

DM3

DM4

DM5

pH Soluble COD Acetic acid Propionic acid Butyric acid Iso-butyric acid Valeric acid Iso-valeric acid Caproic acid Myristic acid Palmitic acid Stearic acid Oleic acid Total solids Volatile solids Ammonia-N Kjeldahl-N

7.8 600 75 <1 <1 <1 <1 <1 <1 <1 240 <1 <1 9000 6600 1500 2100

7.5 1400 450 6 <1 <1 <1 3 <1 <1 16 <1 <1 10200 7400 1800 2100

7.3 4300 1800 76 14 24 <1 45 <1 9 52 8 <1 14400 11900 2200 Naa

7.4 760 11 <1 <1 <1 <1 11 <1 <1 63 <1 <1 8800 6700 1900 Na

7.7 2200 1100 37 6 17 <1 20 <1 7 37 10 <1 12200 9400 1900 2900

Na ˆ not analysed.

E. Salminen et al. / Bioresource Technology 78 (2001) 81±88

grass (Lolium perenne), used in the plant assays, were purchased from Siemen (Finland). 2.3.1. Digested material as fertiliser (27-d plant growth assays) The standard practice of the American Society for Testing and Materials (1994) was applied to compare digested material sample DM1, and the reference, a commercial fertiliser, to fertilise the soil for the growth of carrot and Chinese cabbage. The soil substrate contained sieved and mixed sphagnum peat (Von Post humi®cation index H 2±4% of humus 97%, pH 3.5±4.5, conductivity 2±4 mS/m, Kekkila, Finland), the pH of which was raised to 7.0 by limestone (CaCO3 ‡ MgCO3 ‡ CaCO3 ; Ca 30%, Mg 2%, Kekkila, Finland). The seeds were then planted in the substrate in polyethylene plant pots (6 l), 19 seeds per pot to run a test. DM1 (72 g DM1/kg substrate) and the fertiliser (690 mg fertiliser/kg substrate) were diluted with tap water and poured on the top of the substrate to obtain the desired concentration of soluble nitrogen (110 mg N/kg substrate). The pots were placed in an environmental chamber at 20°C for 27 days and tap water was added daily to replace evaporation loss. 2.3.2. Germination assays To study the phytotoxicity of DM3 and DM4 and the aerobically post-treated DM2 and DM5, germination assays were conducted as described by Baud-Grasset et al. (1993) in triplicate 5 cm, sealable glass petri dishes, containing ®lter paper (Schleicher and Schuell). Test solutions were prepared using various dilutions of DM3 and DM4 (25 and 50 g/l) and aerobically post-treated DM2 and DM5 (in g/l: 25, 50, 125, 250), diluted with deionised water. Deionised water was used as control. Each dish contained 4 ml of test solution adsorbed on ®lter paper with 10 seeds placed on the paper. The dishes were sealed and statically incubated at 20  1°C for 120 h in dark. A 5-mm primary root was taken to de®ne germination.

83

to the methods of the Association of Ocial Agricultural Chemists (1990). Samples for soluble COD, ammonia and NOx were ®ltered through glass ®bre ®lter paper (Schleicher and Schuell). Short and medium-chain fatty acids (from C2 to C6 ) were analysed with a Perkin Elmer Autosystem XL gas chromatograph with a ¯ame-ionisation detector and a PE FFAP column, as described elsewhere (Lepist o and Rintala, 1995). Long-chain fatty acids (C14:0, myristate; 16:0, palmitate; C18:0, stearate, and C18:1(n-9), oleate) samples were analysed with a Hewlett±Packard HP 6890 series gas chromatograph with a 5973 mass selective detector and a HP-5 column, as described elsewhere (Salminen et al., 1999). Mo, Cd, Cr, Ni, Pb, and Hg were determined after acid digestion …HNO3 † and analysed with an atomic absorption spectrophotometer. S, P, K, Ca, Mg, Fe, Cu and Zn were determined after acid digestion …HNO3 † and analysed by inductively coupled plasma-atomic emission spectroscopy (ICP-AES). 2.5. Data analyses of plant assays The SPSSâ for Windows 8.0 was used for all the statistical procedures, except linear regression analysis, which was done using the Microsoft Excel 97 for Windows 98. The binomial test was used to study the equality of the samples as well as the samples and the control at a ˆ 0:05. The Kolmogorov±Smirnov test …n P 50† or the Shapiro±Wilk test …n < 50† was used to check the normality of the data with extreme observations excluded as outliers. The Levene test was used for the equality of variances at a ˆ 0:05 and one-way ANOVA to compare the equality of means of the samples against the control and to study the equality of means between the samples at a ˆ 0:05. Linear regression analysis was done to study the relationship between the phytotoxicity and chemical properties of the samples.

2.4. Analytical methods

3. Results

pH, TS, VS, SS and VSS were determined according to the Standard Methods (American Public Health Association, 1985). In plant assays the dry weights of roots and above-ground vegetation were determined upon drying for 18 h at 70°C. COD was determined according to the Finnish Standards (Finnish Standards Association, 1988). Ammonia, total oxidised nitrogen …NOx †, and total Kjeldahl-N (after acid digestion …H2 SO4 †) were determined by a Kjeldahl method (Perstorp Analytical/Tecator AB, 1995). Protein content was calculated from the KjeldahlN content using the conversion factor of KjeldahlN  6.25 (for meat). Lipids were determined according

3.1. Aerobic post-treatments of the digested material The e€ects of 6-h and 7-d aerobic post-treatment on digested material characteristics are summarised in Table 2. During the 6-h treatment, a signi®cant drop was observed in organic acids concentrations (ca. 60% for acetic acid) and soluble COD and a sharp increase in pH from 7.0 to 8.6 within 30 min (Table 2). On the other hand, TS and VS declined less, ca. 10%, and ammonia concentrations fell by 30%. Similarly, 7-d treatments, with and without inoculum resulted in high organic acid reduction (ca. 99% for acetic acid) with a soluble COD reduction of 72±74%

b

a

7.7 1100 568 19 10 3 <1 10 4 <1 20 5 <1 5400 4100 970 1450

Initial 8.5 840 226 8 <1 6 <1 8 <1 <1 17 3 <1 4900 3900 680 1130

Final

a

6-h treatment of DM5

7.1 720 223 3 <1 <1 <1 2 <1 <1 8 <1 <1 5100 3700 920 1040

Initial

DM2 6.7 190 2 <1 <1 <1 <1 1 <1 <1 <1 <1 <1 3200 2400 230 580

Final

a

6.6 390 Nab Na Na Na Na Na Na Na Na Na Na Na Na 200 460

Final

a

DM2+HgSO4

7-day treatment of DM2 and controls

Water evaporation during the assays considered in calculated values. Na ˆ not analysed.

pH Soluble COD Acetic acid Propic acid Butyric acid Iso-butyric acid Valeric acid Iso-valeric acid Caproic acid Myristic acid Palmitic acid Stearic acid Oleic acid TS VS Ammonia-N Kjeldahl-N

Analysis

7.0 740 224 4 <1 <1 <1 2 <1 <1 8 <1 <1 6300 4400 920 1400

Initial

DM2+AS 6.8 210 4 <1 <1 <1 <1 <1 <1 Na Na Na Na 2900 2100 20 490

Final

a

6.5 460 Na Na Na Na Na Na Na Na Na Na Na Na Na 220 600

Final

a

DM2+AS+HgSO4

7.0 20 1 1 <1 <1 <1 <1 <1 <1 <1 <1 <1 1200 700 <10 360

Initial

AS 6.8 20 2 <1 <1 <1 <1 <1 <1 Na Na Na Na 800 600 <10 Na

Finala

Table 2 E€ects of aerobic post-treatment on characteristics of digested materials DM2 and DM5. DM2 was treated as such and with activated sludge (AS). Abiotic tests (with HgSO4 additions) and activated sludge alone were incubated as controls (all units mg/kg, except pH)

84 E. Salminen et al. / Bioresource Technology 78 (2001) 81±88

E. Salminen et al. / Bioresource Technology 78 (2001) 81±88

85

Table 3 E€ect of digested material (72 g DM1/kg substrate) on carrot and Chinese cabbage root and above ground lengths and dry weights as compared to reference fertiliser (690 g/kg) (110 mg soluble N/kg substrate, N ˆ 30) Material

Above-ground vegetation length (mm) Root length (mm) Above-ground vegetation dry weight (mg) Root dry weight (mg)

Carrot (Daucus carota)

Chinese cabbage (Brassica campestris var. chinensis)

DM1a

Fertiliser

DM1a

9.3 4.9 12.6 1.8

10.3 6.8 20.9 1.3

4.0 3.5 29.2 3.4

(1.6) (2.2) (4.1)b (1.1)c

(1.5) (1.9) (10.2) (0.5)c

(1.7)b (1.8)b (22.1)b (1.9)c

Fertiliser 13.4 11.8 340.5 24.2

(0.9) (2.3) (134.0) (10.3)c

a

Standard deviation in parenthesis. Signi®cantly di€erent from fertiliser at a ˆ 0:05 by one-way ANOVA. c Ln transformation applied to equalise variances. b

(Table 3), while abiotic controls showed a 38±46% decrease in soluble COD. All the 7-d treatments, with and without added inoculum, resulted in high (>50%) nitrogen losses, apparently due to the volatilisation of free ammonia. Treatments with inoculum accounted for the highest Kjeldahl-N loss, 65%, with ammonia reduced by 98%, but with a minor nitri®cation pathway (ca. 20 mg/l of NOx analysed at the end of incubation). The ammonia volatilised apparently because of the high pH, as the latter kept rising until the day 4 and then declined. Treatment with added inoculum accounted for high TS (54%) and VS (52%) reduction, compared to that without added inoculum (37% and 35%). 3.2. Plant assays 3.2.1. Digested material as fertiliser Using 27-d plant growth assays and chemical and physical analysis, we investigated the e€ectiveness of anaerobically digested poultry slaughterhouse waste as fertiliser in agriculture. The digested material (DM1) appeared rich in nutrients and minerals and low in heavy metals (in g/kg TS: N 164, S 15, P 24, K 19, Ca 31, Mg 3.3, Fe 31; in mg/kg TS: Cu 93, Zn 336, Mo 3.5, Cr 31, Cd 0.42, Ni 15, Pb 10, Hg <0.05). DM1 and the reference fertiliser were compared in growth assays on carrot and Chinese cabbage. Compared to the reference fertiliser in terms of root length and the length and weight of above-ground vegetation (Table 3), DM1 inhibited the growth of Chinese cabbage. Also, the above-ground growth of carrot by weight in DM1 was inhibited in comparison to the reference (see Table 3), whereas the root growth and the length of above-ground vegetation of carrot in DM1 statistically equalled those in the reference fertiliser (see Table 3). 3.2.2. Germination assays As the digested material appeared phytotoxic in the 27-d plant growth assays, we conducted further germination assays using various dilutions of DM3 and DM4 (25 and 50 g/l) and aerobically post-treated DM2 and

DM5 (in g/l: 25, 50, 125, 250), diluted with deionised water, deionised water as control. In most cases and in comparison with the control, DM3 and DM4 signi®cantly inhibited the germination and the root growth of perennial ryegrass and Chinese cabbage (see Figs. 1 and 2). As a whole, DM3 was more phytotoxic than DM4, as indicated by germination (binomial test, at a concentration of 25 g/l, P < 0:01; at a concentration of 50 g/l, in DM3 no growth), and root growth (one-way ANOVA, at a concentration of 25 g/l, F1;26 ˆ 5:85; P ˆ 0:02). On the other hand, though the germination of ryegrass appeared more inhibited by DM4 than by DM3 (binomial test, P ˆ 0:02 and P < 0:01, at concentrations of 25 and 50 g/l, respectively). The root growth and germination of Chinese cabbage and ryegrass were overall less inhibited in aerobically post-treated DM2 and DM5 than in DM3 and DM4, which were not aerobically post-treated (Figs. 1 and 2). In most cases, no statistically signi®cant di€erence was observed in comparing the 6-h and 7-day aerobic posttreatments or the materials with 7-day aerobic posttreatment, with and without added inoculum. To ®nd the inhibiting factors in the assays, we did a regression analysis on the phytotoxicity assays and on selected chemical properties of the samples. The germination and root growth of Chinese cabbage showed a relatively high negative correlation only with palmitic acid (a linear regression, r2 0.68 for germination and 0.83 for root growth; N ˆ 16), whereas the germination of ryegrass correlated negatively with short and medium-chain fatty acids and soluble COD (r2 from 0.50 to 0.72; N ˆ 16). The root growth of ryegrass showed the highest correlation with soluble COD …r2 ˆ 0:55; N ˆ 16† and a lower dependence with any single organic acid compound (r2 from 0.31 to 0.44; N ˆ 16). Plants germination and root growth showed a slight correlation with ammonia, r2 from 0.45 to 0.50 …N ˆ 16†. On the other hand, the ammonia concentration typically followed the same general trends as the organic acid concentrations (linear regression between ammonia and acetic acid, r2 ˆ 0:43; N ˆ 16), and soluble COD …r2 ˆ 0:61; N ˆ 16†. Thus, we could not determine the inhibitor speci®cally.

86

E. Salminen et al. / Bioresource Technology 78 (2001) 81±88

Fig. 1. E€ect of digested materials DM3 and DM4 and aerobically post-treated digested materials DM2 and DM5 on: (a) ryegrass (Lolium perenne); (b) Chinese cabbage (Brassica campestris var. chinensis) germination frequency at di€erent material concentrations (in range of 25±250 g/l), diluted with deionised water, deionised water as control. The control germination frequency of ryegrass and Chinese cabbage 86% and 82%, respectively …N ˆ 19†; AS ˆ activated sludge. a Signi®cantly di€erent from the control at a ˆ 0:05 by binomial test.

Fig. 2. E€ect of digested materials DM3 and DM4 and aerobically post-treated digested materials DM2 and DM5 on: (a) ryegrass (Lolium perenne); (b) Chinese cabbage (Brassica campestris var. chinensis) root lengths at di€erent material concentrations (in range of 25±250 g/l), diluted with deionised water, deionised water as control. Mean of control root length of ryegrass and Chinese cabbage were 25.1 mm, with standard deviation of 10.1 and 26.9 mm, with standard deviation of 9.1, respectively …N ˆ 19†; AS ˆ activated sludge. a Signi®cantly di€erent from the control at a ˆ 0:05 by one-way ANOVA.

E. Salminen et al. / Bioresource Technology 78 (2001) 81±88

4. Discussion Using chemical and physical analysis and plant assays, we studied the suitability of anaerobically digested poultry slaughterhouse waste for fertiliser in agriculture and the e€ect of aerobic post-treatment on its material properties. Compared to digested biowaste (ca. 7% N of TS; Vermeulen et al., 1992) and digested municipal sewage sludge (typically 2.5% N of TS; Metcalf and Eddy, 1991), the digested material appeared rich in nitrogen (ca. 20% N of TS). It was also low in heavy metals but potentially phytotoxic with its inhibitive e€ect speci®c to plant species so that the growth of carrot with the material as nitrogen source was almost comparable to that in the reference fertiliser. On the other hand, it inhibited the growth of Chinese cabbage. In the germination assays, the digested material inhibited the germination of ryegrass and Chinese cabbage as well as their root growth. Regression analysis suggested that the inhibition was related to organic acids, which have previously been shown to inhibit root growth and cause ion loss from roots (Lee, 1977; Lynch, 1980). However, in our tests, organic acids concentrations were lower than those previously found inhibitory (DeVleeschauwer et al., 1981; Lynch, 1977, 1980; Manios et al., 1989; Marable et al., 1993). Regression analysis suggested a slight ammonia inhibition. Ammonia dissociates in solution depending on pH and temperature, and though both the unionised and ionised form of ammonia may a€ect plant growth the inhibition mechanisms are di€erent (Sudradjat, 1990). Both our unionised and ionised ammonia concentrations were very much lower than those reported earlier to be inhibitory (Hill et al., 1997; Tiquia and Tam, 1998; Wong et al., 1983). Our ammonia concentration followed the same general trend as the organic acid concentrations and soluble COD. Thus no single inhibitory factor emerged in the study. As a whole, aerobic post-treatment of the digested material considerably reduced the phytotoxicity of the material, suggesting that the inhibiting compounds in the material were readily degraded aerobically or volatilised during the treatment. Previous studies con®rm that aerobic post-treatment is capable of signi®cantly reducing the phytotoxicity of anaerobically digested biowaste (Vermeulen et al., 1992). In our study, the aerobic post-treatment of the digested material removed signi®cant amounts of organic matter and ammonia with the length of the post-treatment duration playing a key role, while the e€ect of the inoculum was less signi®cant. Apparently, both nonbiological (volatilisation) and biological (assimilation, dissimilation and nitri®cation) processes were involved, as indicated by the soluble COD and ammonia removals

87

in biotic assays and abiotic controls. Ecient pH control up to moderate acidity might have reduced the signi®cant nitrogen loss during the treatment, caused by the volatilisation of ammonia. To minimise emissions of volatile compounds and loss of ammonia during storage and spreading of treated materials, the storage tank and handling systems should be covered, and emissions should be recovered. In conclusion, our investigation shows that anaerobically digested solid poultry slaughterhouse wastes can well be used in agriculture if the material is appropriately treated before use.

Acknowledgements We thank Prasad Kaparaju for his assistance and gratefully acknowledge the ®nancial support from the Academy of Finland (grant no. 38044).

References American Public Health Association, 1985. Standard methods for the examination of water and wastewater, 16th ed. American Public Health Association, Washington, DC. American Society for Testing and Materials, 1994. Designation: E 1598-94. Standard Practise for Conducting Early Seeding Growth Test, American Society for Testing and Materials, pp. 1061±1067. Association of Ocial Agricultural Chemists, 1990. Ocial Methods of Chemical Analysis. 16th ed. Association of Ocial Agricultural Chemists, Washington, DC. Baud-Grasset, F., Baud-Grasset, S., Sa€erman, S.I., 1993. Evaluation of the bioremediation of a contaminated soil with phytotoxicity tests. Chemosphere 26, 1365±1374. DeVleeschauwer, D., Verdonck, O., Van Assche, P., 1981. Phytotoxicity of refuse compost. BioCycle 22, 44±46. Finnish Standards Association, 1988. SFS 5504, Determination of chemical oxygen demand (CODCr ) in water with the closed tube method, oxidation with dichromate. Finnish Standards Association, Helsinki, Finland. Hill, D.T., Payne, V.W.E., Rogers, J.W., Kown, S.R., 1997. Ammonia e€ects on the biomass production of ®ve constructed wetland plant species. Bioresource Technol. 62, 109±113. Lee, R.B., 1977. E€ects of organic acids on the loss of ions from barley roots. J. Experimental Botany 28, 17±29. Lepist o, R., Rintala, J., 1995. Acetate treatment in 70°C UASB reactors: start-up with thermophilic inocula and the kinetics of the UASB sludges. Appl. Microbiol. Biotechnol. 43, 1001±1005. Lynch, J.M., 1977. Phytotoxicity of acetic acid produced in the anaerobic decomposition of wheat straw. J. Appl. Bacteriol. 42, 81±87. Lynch, J.M., 1980. E€ects of organic acids on the germination of seeds and growth of seedlings. Plant Cell Environ. 3, 255±259. Manios, V.I., Tsikalas, P.E., Siminis, H.I., 1989. Phytotoxicity of olive tree leaf compost in relation to the organic acid concentration. Biol. Wastes 27, 307±317. Marable, B., Nagaoka, T., Ando, T., 1993. Identi®cation and biological activity of germination-inhibiting long-chain fatty acids in animal-waste composts. Plant Cell Physiol. 34, 605±612. Marchaim, U., Levanon, D., Danai, O., Musaphy, S., 1991. A suggested solution for slaughterhouse wastes: uses of the residual

88

E. Salminen et al. / Bioresource Technology 78 (2001) 81±88

materials after anaerobic digestion. Bioresource Technol. 37, 127± 134. Metcalf & Eddy, Inc., 1991. Wastewater engineering, Treatment, Disposal, and Reuse, third ed. McGraw-Hill, New York. Perstorp Analytical/Tecator AB, 1995. Tecator application note. The determination of nitrogen according to Kjeldahl using block digestion and steam distillation. Rubñk, G.H., Henriksen, K., Petersen, J., Rasmussen, B., Sommer, S.G., 1996. E€ects of application technique and anaerobic digestion on gaseous nitrogen loss from animal slurry applied to ryegrass (Lolium perenne). J. Agric. Sci. 126, 481±492. Salminen, E., Rintala, J., Semi-continuous anaerobic digestion of solid poultry slaughterhouse waste: e€ect of hydraulic retention time and loading. Water Research (submitted). Salminen, E., Rintala, J., Lokshina, L.Ya., Vavilin, V.A., 1999. Anaerobic batch degradation of solid poultry slaughterhouse waste. In: Proceedings of the Second International Symposium on Anaerobic Digestion of Solid Waste, Barcelona, Spain, pp. 41±48. Shih, J.C.H., 1987. Ecological bene®ts of anaerobic digestion. Poultry Science 66, 946±950.

Sudradjat, R., 1990. Transformations and uses of digested solid organic residues. PhD thesis, Rijksuniversiteit Gent. Tiquia, S.M., Tam, N.F.Y., 1998. Elimination of phytotoxicity during co-composting of spent pig-manure sawdust litter and pig sludge. Bioresource Technol. 65, 43±49. Tiquia, S.M., Tam, N.F.Y., Hodgkiss, I.J., 1996. E€ects of composting on phytotoxicity of spent pig-manure sawdust litter. Environ. Pollut. 93, 249±256. Vermeulen, J., Huysmans, A., Crespo, M., van Lierde, A., de Rycke, A., Verstraete, W., 1992. Processing of biowaste by anaerobic composting to plant growth substrates. In: Proceedings of International Symposium on Anaerobic Digestion of Solid Waste, April 14±17, 1992, Venice, Italy, pp. 147±157. Wang, W., 1991. Ammonia toxicity to macrophytes (common duckweed and rice) using static and renewal methods. Environ. Toxicol. Chem. 10, 1173±1177. Wong, M.H., Cheung, Y.H., Cheung, C.L., 1983. The e€ect of ammonia and ethylene oxide in animal manure and sewage sludge on the seed germination and root elongation of Brassica parachinensis. Environ. Pollut. A 30, 109±123.