In uence of earthworm-processed pig manure on the growth and yield of greenhouse tomatoes

Bioresource Technology 75 (2000) 175±180 In uence of earthworm-processed pig manure on the growth and yield of greenhouse tomatoes R.M. Atiyeh a, *, N. Arancon a, C.A. Edwards a, J.D. Metzger b a Soil Ecology Laboratory, 105 Botany and Zoology Building, The Ohio State University, 1735 Neil Avenue, Columbus, OH 43210, USA b Department of Horticulture and Crop Sciences, The Ohio State University, 1735 Neil Avenue, Columbus, OH 43210, USA Received 2 December 1999; received in revised form 5 May 2000; accepted 6 May 2000 Abstract The e ects of earthworm-processed pig manure (vermicompost) on germination, growth, and yields of tomato (Lycopersicon esculentum Mill.) plants were evaluated under glasshouse conditions. Tomatoes were germinated and grown in a standard commercial greenhouse container medium (Metro-Mix 360), substituted with 10%, 20%, 30%, 40%, 50%, 60%, 70%, 80%, 90%, and 100% (by volume) pig manure vermicompost. The control consisted of Metro-Mix 360 alone without vermicompost. Plants were grown for 158 days and were frequently supplied with a complete mineral nutrient solution. The germination rates of tomato seeds increased signi cantly upon substitution of Metro-Mix 360 with 20%, 30%, and 40% vermicompost. Seedlings grown in 100% pig manure vermicompost were signi cantly shorter, had fewer leaves, and weighed less than those in Metro-Mix 360 controls. Incorporation of 10% or 50% vermicompost into Metro-Mix 360 increased the dry weights of tomato seedlings signi cantly compared to those grown in the Metro-Mix 360 controls. The largest marketable yield was in the substitution of Metro-Mix 360 with 20% vermicompost (5.1 kg/plant). The average weight of a tomato fruit in substitution of Metro-Mix 360 with 20% vermicompost was 12.4% greater than that in the Metro-Mix 360 control. Substitution of Metro-Mix 360 with 10%, 20%, and 40% vermicompost reduced the proportions of fruits that were non-marketable, and produced more large size (diameter > 6:4 cm) than small size (diameter < 5:8 cm) tomato fruits. There was no signi cant di erence in overall tomato yields between Metro-Mix 360 and 100% pig manure vermicompost. Some of the growth and yield enhancement resulting from substitution of Metro-Mix 360 with pig manure vermicompost could be attributed to the high mineral N concentration of the pig manure vermicompost. However, other factors might have also been involved since all plants were frequently supplied with all required nutrients. These factors need to be investigated in future studies. Ó 2000 Elsevier Science Ltd. All rights reserved. Keywords: Pig manure; Earthworms; Vermicompost; Tomato; Plant growth; Yield 1. Introduction Over the last few years, as regulations for application and disposal of animal manure has become more rigorous, the interest in using earthworms as an ecologically sound system for manure management has increased tremendously. Several research studies have already demonstrated the ability of some earthworms to consume a wide range of organic wastes such as sewage sludge, animal manure, crop residues, and industrial refuse (Mitchell et al., 1980; Chan and Gri ths, 1988; Hartenstein and Bisesi, 1989; Edwards, 1998). In the process of feeding, earthworms fragment the waste * Corresponding author. Tel.: +1-614-292-3786; fax: +1-614-292-2180. E-mail address: atiyeh.1@osu.edu (R.M. Atiyeh). substrate, accelerate rates of decomposition of the organic matter, alter the physical and chemical properties of the material, leading to a composting or humi cation e ect through which the unstable organic matter is oxidized and stabilized (Hartenstein and Hartenstein, 1981; Albanell et al., 1988; Orozco et al., 1996; Vinceslas-Akpa and Loquet, 1997). Earthworm-processed organic wastes, often referred to as vermicomposts, are nely divided peat-like materials with high porosity, aeration, drainage, and waterholding capacity (Edwards and Burrows, 1988). Compared to their parent materials, vermicomposts have reduced amounts of soluble salts, greater cation exchange capacity, and increased total humic acid content (Albanell et al., 1988). They contain nutrients in forms that are readily taken up by the plants, such as nitrates, exchangeable phosphorus, and soluble potassium, 0960-8524/00/$ - see front matter Ó 2000 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 0-8 5 2 4 ( 0 0 ) 0 0 064-X

176 R.M. Atiyeh et al. / Bioresource Technology 75 (2000) 175±180 calcium, and magnesium (Edwards and Burrows, 1988; Orozco et al., 1996). Krishnamoorthy and Vajranabhaiah (1986), Grappelli et al. (1987) and Tomati et al. (1987, 1990) reported that vermicomposts contain biologically active substances such as plant growth regulators. Based on all these characteristics, earthworm-processed organic wastes should have great commercial potential in the horticultural industry as container media for growing bedding and vegetable plants. There are only few research studies that have examined the growth of vegetable and bedding plants in potting media mixed with earthworm-processed organic wastes (Edwards and Burrows, 1988; Wilson and Carlile, 1989; Subler et al., 1998; Atiyeh et al., 1999). In all of these studies, it was con rmed that earthworm-processed organic wastes have bene cial e ects on the growth and development of plant seedlings. However, none of these studies were carried beyond the seedling growth stage of plants, hence assessing the impact of earthworm-processed organic wastes on the yield and productivity of vegetable plants. The objective of this experiment was to assess the germination, growth, and yield of tomato (Lycopersicon esculentum Mill.) plants, grown for 158 days in a standard commercial potting medium (Metro-Mix 360) substituted with di erent concentrations of earthwormprocessed pig manure (vermicompost) under glasshouse conditions. To eliminate nutrient limitations, tomato plants in all potting mixtures were watered regularly with a complete plant nutrient solution. 2. Methods The plant growth study was in a Horticulture Department greenhouse at The Ohio State University, Columbus, Ohio. The plant growth media consisted of a control standard commercial greenhouse container medium, Metro-Mix 360 (Scotts, Marysville, OH), and of substitutions of Metro-Mix 360 with di erent concentrations of pig manure vermicompost. Metro-Mix 360 is prepared from vermiculite, Canadian sphagnum peat moss, bark ash and sand, and contains a starter nutrient fertilizer in its formulation. The pig manure-based vermicompost was provided by Vermicycle Organics, Charlotte, NC and consisted of separated pig solids processed by earthworms (Eisenia spp.) in indoor beds. The basic chemical properties of Metro-Mix 360 and the pig manure vermicompost are summarized in Table 1. Tomato (Rutgers) seedlings were germinated and grown in polystyrene trays, containing Metro-Mix 360 substituted with 0% (control), 10%, 20%, 30%, 40%, 50%, 60%, 70%, 80%, 90%, or 100% (by volume) vermicompost. There were four trays per Metro-Mix/vermicompost mixture, with each tray consisting of 50 inverted pyramid cells. After sowing, all trays were placed in a mist house. Eight days later, numbers of seedlings that had germinated were counted and the germination rates in each potting mixture (percentage of seeds germinating per day) were determined. Trays were then moved into a glasshouse where they were watered as needed with tap water and fertilized three times a week with 20±10±20 (200 ppm N) Peters Professional plant nutrient solution. Peters Professional is a watersoluble fertilizer that is recommended for continuous liquid feed programs of plants, and contains 7.77% NH 4 ±N, 12.23% NO 3 ±N, 10% P 2 O 5, 20% K 2 O, 0.15% Mg, 0.02% B, 0.01% Cu, 0.1% Fe, 0.056% Mn, 0.01% Mo, and 0.0162% Zn. Twenty days later, ten plants were selected at random from each potting mixture. Plant heights (distance from the soil level to the top node) and total leaf numbers (excluding cotyledons) of each of the seedlings were recorded, and the average plant heights and leaf numbers per potting mixture determined. Plants were then removed from the potting mixtures and ovendried at 60 C for 5 days to determine total plant dry weights. Two additional tomato seedlings were also removed randomly from each tray, and transplanted into small pots (10 cm in diameter) lled with the same Metro-Mix/ vermicompost potting mixture as that they had been germinated and grown in. Forty days later, the seedlings in the small pots were transplanted into larger pots (40 cm in diameter), containing the same composition of Metro-Mix/vermicompost mixture as that they had been in originally. Because of limitations in greenhouse space and amounts of vermicompost available, the transplanting into the 40 cm pots was conducted only on the tomato seedlings grown in Metro-Mix 360 substituted with 0% (control), 10%, 20%, 40%, 60%, 80%, and 100% pig manure vermicompost. There were eight 40 cm pots Table 1 Chemical properties of the commercial potting medium (Metro-Mix 360) and the vermicompost Medium ph Conductivity Total N (%) Organic C (%) Total P (%) Total K (%) (mmhos/cm) Commercial medium Metro-Mix 360 5.9 1.35 0.43 31.78 0.15 1.59 Vermicompost Pig manure 5.3 11.76 2.36 27.38 4.50 0.40

R.M. Atiyeh et al. / Bioresource Technology 75 (2000) 175±180 177 per Metro-Mix/vermicompost mixture. All pots were fertilized three times weekly with 20±10±20 (200 ppm N) Peters Professional plant nutrient solution. Vegetative suckers were removed up to the rst ower cluster, plants were staked, and insects (mostly white ies) controlled as required with the chemical s-kinoprene (Enstar â ). Thirty days after, the nal transplant into the 40 cm pots, tomato fruits were harvested twice weekly, and separated into marketable and non-marketable (cracked, damaged, diseased) fruits. The numbers and weights of marketable and non-marketable tomatoes were recorded, and the average weights of the tomato fruits, marketable yields per plant, as well as percentages of marketable and non-marketable tomatoes per potting mixture were determined. Marketable tomatoes, from each potting mixture, were separated into three sizes according to their diameters (Peterson, 1973): small (<5:8 cm), medium (between 5.8 and 6.4 cm), and large (>6:4 cm). The numbers and percentages of marketable tomatoes in each size category were then determined. Tomato fruits were harvested for 60 days, after which the shoots of all tomato plants were removed from the potting mixtures, oven-dried at 60 C for 8 days, and the mean shoot dry weights determined. Five grams potting mixture samples were taken for mineral N analysis prior to seedling, 28 days after seedling, and 158 days after seedling. The mineral N concentration (NH 4 N NO 3 N) in each potting mixtures was determined calorimetrically in 0.5 M K 2 SO 4 extracts in the ratio of 1:10 potting mixture to extractant, using a modi ed indophenol blue technique (Sims et al., 1995) with a Bio-Tek EL311sx automated microplate reader (Bio-Tek â Instruments, Winooski, Vermont). Data were analyzed statistically by one-way ANOVA in a general linear model using SAS (SAS Institute, 1990). At each sampling date and for each measured parameter, the means were separated statistically using DunnettÕs multiple range tests with Metro-Mix 360 without vermicompost set as the control. Signi cance was de ned as P 6 0:05, unless otherwise indicated. 3. Results and discussion The substitution of Metro-Mix 360 with 20%, 30%, and 40% pig manure vermicompost increased the rates of germination of tomato seeds signi cantly by 12.9%, 12.3%, and 14.7%, respectively, over those in the Metro- Mix 360 controls (Table 2). Tomato seedlings grown in potting mixtures containing 50% pig manure vermicompost had more leaves and weighed more than those grown in the Metro-Mix 360 controls. Even with a relatively small concentration of pig manure vermicompost (10% by volume) in the container medium, the dry weights of tomato seedlings increased signi cantly (30.8%) over those of plants grown in the Metro-Mix 360 controls (Table 2). On the other hand, seedlings grown in 100% pig manure vermicompost were signi cantly shorter, had fewer leaves, and weighed less than those in Metro-Mix 360 controls (Table 2). These results agree with those of Subler et al. (1998) who reported that the addition of 10% or 20% of vermicomposted pig manure to a standard commercial potting medium increased the weights of tomato seedlings signi cantly, after three weeks of growth in plug trays in the greenhouse. Substituting the commercial medium with di erent concentrations of pig manure vermicompost not only improved the growth of tomato seedlings, but it also increased tomato yields signi cantly. The greatest marketable yield (5.1 kg/plant) was in the potting mixtures containing 20% pig manure vermicompost, which was 58% greater than the yield in the Metro-Mix 360 control (Fig. 1(a)). Similar results were noted by Maynard Table 2 Germination and growth of tomato seedlings in a standard commercial potting medium (Metro-Mix 360) substituted with di erent concentrations of vermicompost Percentage of vermicompost in Metro-Mix 360 Germination rate (% per day) a Seedling growth Height (cm) Number of leaves Plant dry weight (g) Control b 10.2 11.0 4.5 0.117 10 10.7 10.7 4.7 0.140 20 11.5 10.8 4.7 0.124 30 11.4 11.7 4.8 0.139 40 11.7 10.5 4.6 0.122 50 10.7 11.4 5.0 0.153 60 11.2 11.8 4.6 0.119 70 10.8 11.2 4.5 0.138 80 11.2 10.8 4.3 0.110 90 11.2 10.7 4.4 0.126 100 10.1 9.3* 4.0** 0.092* a Means within the same column followed by * and ** are signi cantly di erent from the control at P 6 0:05 and P 6 0:01, respectively. b Control represents 100% Metro-Mix 360.

178 R.M. Atiyeh et al. / Bioresource Technology 75 (2000) 175±180 Fig. 1. Yield and sizes of tomato fruits (mean standard error) produced in a standard commercial potting medium (Metro-Mix 360) substituted with di erent concentrations of pig manure vermicompost. Columns followed by * are signi cantly di erent from Metro-Mix 360 control (0% vermicompost) at P 6 0:05: (1993, 1995) who reported that tomato yields in eld soils amended with compost were signi cantly greater than those in the unamended plots. Maynard attributed the increases in yields to increases in the number of tomatoes per plant and average weight of each fruit. In this experiment, the average weight of a tomato fruit in potting mixtures containing 20% pig manure vermicompost was 12.4% greater than that of a tomato fruit grown in the Metro-Mix 360 control (Fig. 1(b)). Substitution of Metro-Mix 360 with 10%, 20%, 40%, and 60% pig manure vermicompost decreased the proportion of non-marketable fruits produced in these mixtures by 82.1%, 88.6%, 81.9%, and 83.0% respectively, increasing the proportion of marketable yield signi cantly (Fig. 1(c). Substitution of Metro-Mix 360 with 10%, 20%, and 40% pig manure vermicompost resulted also in more large size marketable tomatoes (diameter > 6:4 cm) than small ones (diameter < 5:8) (Fig. 1(d)). The most marked e ect was in the potting mixtures containing 20% pig manure vermicompost, where only 3% of the marketable fruits were small, 18% medium, and 80% large in size; whilst 37% of the marketable tomatoes in the Metro-Mix 360 controls were small, 25% medium, and 45% large in size. The 100% pig manure vermicompost produced 76% more large size marketable tomatoes and 10% fewer small size tomatoes than the Metro-Mix 360 controls (Fig. 1(d)). However, this did not result in signi cant di erences in yields between the 100% pig manure vermicompost and Metro-Mix 360 controls (Figs. 1(a) and (b)). Both the Metro-Mix 360 controls and the 100% pig manure vermicompost produced similar ratios of marketable to non-marketable fruits (Fig. 1(c)). The shoot dry weights of the tomato plants grown in the 100% pig manure vermicompost (499.9 g) were also signi cantly smaller than those in the Metro-Mix 360 controls (717.7 g) (Fig. 2). This decrease in plant growth, upon substitution of Metro-Mix 360 with large concentrations (above 60%) of pig manure vermicompost, has also been observed in container media substituted with compost (Shiralipour et al., 1992), and has been attributed to either high soluble salt concentrations, poor aeration, heavy metal toxicity, and/or plant phytotoxicity. Mineral N concentrations in the potting mixtures increased signi cantly with increasing concentrations of pig manure vermicompost incorporated into the container medium (Table 3). Some of the enhancement in seedling growth 28 days after seedling, based upon substitutions of Metro-Mix 360 with pig manure vermicompost could be due partly to di erences in mineral N concentrations between Metro-Mix 360 and pig

R.M. Atiyeh et al. / Bioresource Technology 75 (2000) 175±180 179 container medium, increases in enzymatic activity, and the presence of bene cial microorganisms or biologically active plant growth-in uencing substances (Grappelli et al., 1987; Tomati and Galli, 1995; Subler et al., 1998). 4. Conclusions Fig. 2. Shoot dry weights of tomato plants (mean standard error) grown for 158 days in a standard commercial potting medium (Metro- Mix 360) substituted with di erent concentrations of pig manure vermicompost. Columns followed by * are signi cantly di erent from Metro-Mix 360 control (0% vermicompost) at P 6 0:05: manure vermicompost, although the plants were watered frequently with a complete nutrient solution. Associated with the enhanced seedling growth in the potting mixtures containing 10% or 50% pig manure vermicomposts, there were low concentrations of mineral N in the potting medium (Table 3), a nitrogen pool that plants can readily assimilate. However, 158 days after seeding, there were no signi cant di erences in mineral N concentrations (Table 3) between the Metro-Mix 360 controls and any of the Metro-Mix/ vermicompost mixtures, which could possibly explain the signi cant increases in tomato yields upon substitutions of Metro-Mix 360 with low concentrations of pig manure vermicompost (20%). It is possible that there are other growth enhancing factors resulting from introduction of small concentrations of pig manure vermicompost into Metro-Mix 360 under conditions of nutrient availability. These factors could include improvements in the physical structure of the The pig manure vermicompost used in this experiment o ers great potential as a component of greenhouse container media. It could be used bene cially to maximize the production of greenhouse tomatoes when incorporated at relatively small concentrations (20% by volume) into Metro-Mix 360, a standard commercial greenhouse container medium, with greater proportions of vermicomposts in the medium decreasing plant productivity. Such e ects could be attributed to a variety of factors that still need to be investigated. It is possible that the pig manure vermicompost a ected containerized tomato growth and yields by modifying the physicochemical, microbial and biological characteristics of the container medium. The decline in growth and yields after incorporation of large concentrations of pig manure vermicompost into Metro-Mix 360 could probably be due to reduced aeration and porosity in the medium, increased salt concentrations, induced toxicity due to heavy metal concentrations, and/or presence of phytotoxic substances. Whereas the increases in growth and yields at low concentrations could probably result from combined optimal physical conditions and nutritional factors in the medium and/or presence of biologically active substances. Therefore, more in-depth study of the attributes of this pig manure vermicompost and further research involving its e ect on eld-grown tomatoes still need to be undertaken prior to its application on a large scale. Table 3 The concentration of mineral nitrogen in the various potting mixtures before seeding, and 28 and 158 days after seeding Percentage of vermicompost in Metro-Mix 360 Mineral N concentration (mg/g) a Before seeding 28 days after seeding 158 days after seeding Control b 0.08 0.32 0.053 10 0.69 0.14 0.030 20 0.90 0.28 0.044 30 1.33 0.34 ± 40 1.59 0.24 0.043 50 2.03 0.14 ± 60 2.19 0.17 0.039 70 2.31 0.09 ± 80 2.91 0.18 0.054 90 2.58 0.16 ± 100 2.88 0.35 0.063 a Means within the same column, at each sampling date, followed by *, **, and *** are signi cantly di erent from the control at P 6 0:05; P 6 0:01, and P 6 0:001, respectively. b Control represents 100% Metro-Mix 360.

180 R.M. Atiyeh et al. / Bioresource Technology 75 (2000) 175±180 References Albanell, E., Plaixats, J., Cabrero, T., 1988. Chemical changes during vermicomposting (Eisenia fetida) of sheep manure mixed with cotton industrial wastes. Biol. Fertil. Soils 6, 266±269. Atiyeh, R.M., Subler, S., Edwards, C.A., Metzger, J., 1999. Growth of tomato plants in horticultural potting media amended with vermicompost. Pedobiologia 43, 1±5. Chan, P.L.S., Gri ths, D.A., 1988. The vermicomposting of pretreated pig manure. Biol. Wastes 24, 57±69. Edwards, C.A., 1998. The use of earthworms in the breakdown and management of organic wastes. In: Edwards, C.A. (Ed.), Earthworm Ecology. CRC Press, Boca Raton, FL, pp. 327±354. Edwards, C.A., Burrows, I., 1988. The potential of earthworm composts as plant growth media. In: Edwards, C.A., Neuhauser, E. (Eds.), Earthworms in Waste and Environmental Management. SPB Academic Press, The Hague, The Netherlands, pp. 21±32. Grappelli, A., Galli, E., Tomati, U., 1987. Earthworm casting e ect on Agaricus bisporus fructi cation. Agrochimica 21, 457±462. Hartenstein, R., Bisesi, M.S., 1989. Use of earthworm biotechnology for the management of e uents from intensively housed livestock. Outlook Agric. 18, 3±7. Hartenstein, R., Hartenstein, F., 1981. Physicochemical changes in activated sludge by the earthworm Eisenia foetida. J. Environ. Qual. 10, 377±382. Krishnamoorthy, R.V., Vajranabhaiah, S.N., 1986. Biological activity of earthworm casts: an assessment of plant growth promoter levels in the casts. Proc. Anim. Sci. Indian Acad. Sci. 95, 341±351. Maynard, A.A., 1993. Evaluating the suitability of MSW compost as a soil amendment in eld-grown tomatoes. Compost Sci. Util. 1, 34± 36. Maynard, A.A., 1995. Cumulative e ect of annual additions of MSW compost on the yield of eld-grown tomatoes. Compost Sci. Util. 3, 47±54. Mitchell, M.J., Hornor, S.G., Abrams, B.I., 1980. Decomposition of sewage sludge in drying beds and the potential role of the earthworm, Eisenia foetida. J. Environ. Qual. 9, 373±378. Orozco, F.H., Cegarra, J., Trujillo, L.M., Roig A, 1996. Vermicomposting of co ee pulp using the earthworm Eisenia fetida: E ects on C and N contents and the availability of nutrients. Biol. Fertil. Soils 22, 162±166. Peterson, E.L., 1973. United States standards for grades of fresh tomatoes. US Fed. Reg. (38 F.R. 23932). SAS Institute, 1990. SAS Procedures Guide, Version 6, 3rd ed., SAS Institute, Cary. Sims, G.K., Ellsworth, T.R., Mulvaney, R.L., 1995. Microscale determination of inorganic nitrogen in water and soil extracts. Commun. Soil Sci. Plant Anal. 26, 303±316. Shiralipour, A., McConnell, D.B., Smith, W.H., 1992. Uses and bene ts of MSW compost: a review and an assessment. Biomass and Bioenergy 3, 267±279. Subler, S., Edwards, C.A., Metzger, J., 1998. Comparing vermicomposts and composts. Biocycle 39, 63±66. Tomati, U., Galli, E., 1995. Earthworms soil fertility and plant productivity. Acta Zoologica Fennica 196, 11±14. Tomati, U., Galli, E., Grappelli, A., Dihena, G., 1990. E ect of earthworm casts on protein synthesis in radish (Raphanus sativum) and lettuce (Lactuca sativa) seedlings. Biol. Fertil. Soils 9, 288±289. Tomati, U., Grappelli, A., Galli, E., 1987. The presence of growth regulators in earthworm-worked wastes. In: Bonvicini Paglioi, A.M., Omodeo, P. (Eds.), On Earthworms. Modena, Italy, pp. 423±436. Vinceslas-Akpa, M., Loquet, M., 1997. Organic matter transformation in lignocellulosic waste products composted or vermicomposted (Eisenia fetida andrei): chemical analysis and 13 C CPMAS NMR spectroscopy. Soil Biol. Biochem. 29, 751±758. Wilson, D.P., Carlile, W.R., 1989. Plant growth in potting media containing worm-worked duck waste. Acta Horticulturae 238, 205± 220.