Introduction

Agaricus subrufescens, which is synonymous with Agaricus blazei ss. Heinemann and Agaricus brasiliensis, is a basidiomycete fungus that has aroused great interest in various parts of the world because of its medicinal properties, which is used in the prevention or treatment of diabetes, atherosclerosis, hepatitis, hypercholesterolemia, and heart disease (Dias et al. 2013; Zied et al. 2013).

Cultivation of mushrooms generates a large amount of spent mushroom compost (SMC) that must be rapidly discarded by the grower to avoid the contamination of new cultivation cycles and infestation by flies or other insects (Marques et al. 2014). Furthermore, after cultivation, uncovered SMC should not be stockpiled due to the risk of contaminating groundwater by leaching after rain events (Ribas et al. 2009).

Depending on the type of mushroom and substrate materials, the SMC can be directly used as animal feed because it is nutritionally rich in proteins, easy to digest and a stimulator of the immune system of animals (Sánchez 2004; Machado et al. 2007; Kwak et al. 2008; Azevedo et al. 2009).

Apart from use in animal feeds, compost produced by mushroom cultivation could be used directly as an organic fertilizer (Rinker 2002). However, under these conditions, the compost is not yet fully stable and can undergo changes if it is stored wet over long periods of time and may affect plant growth because of the presence of heavy metals, poor physical properties and excessive salts, that result in high electrical conductivity (Abad et al. 2001; Bustamante et al. 2008; Medina et al. 2009).

In addition to fertility and plant nutrition, SMC that is produced using the appropriate technology also has the advantage of containing a rich microbiota that can ensure the necessary balance to guarantee the phytosanitary requirements of plant cultures (Elo et al. 2000; Viji et al. 2003). It is also possible that some species of microorganisms have the potential to induce resistance in seedlings pre-grown on this substrate.

The use of microorganisms to induce plant resistance to pathogens of root and leaves is now well documented, showing the great potential of this strategy (Ishida et al. 2008; Fontenelle et al. 2011). The microbial community that is present in organic compost and in the substrate after cultivation of mushrooms might play an important role in controlling the microbiota in the rhizosphere region.

Therefore, this type of SMC could be an important source of microorganisms of different species with the potential to induce resistance against diseases. In addition, the mushroom species itself produce biotic resistance inducers, substances that elicit plant defense responses (Silva et al. 2013). Considering all this, the use of SMC can have a much greater potential than simply an organic fertilizer or soil conditioner.

In the present manuscript, tomato plants were chosen to evaluate the potential use of spent mushroom compost after cultivation of the mushroom A. subrufescens in different proportions in a mixture with a commercial substrate as growing media for tomato production in an organic system.

Materials and methods

Location of the experiment

The experiment was conducted under greenhouse conditions for the production of tomato seedlings and under field conditions for the production of tomatoes (Solanum lycopersicum) in the area located at 21°14′S and 45°00′W and at 920 m of altitude. The average annual temperature is 19.3 °C, and the average annual rainfall is 1411 mm, with a concentration of rainfall during summer. The average relative humidity is 78 %. The soil was an oxisol, and the soil showed good depth, a clayey texture, good water retention capacity, good aeration and a flat topography. The analysis of the soil is described in Table 1.

Table 1 Physicochemical characteristics of the soil at the experimental location
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Procurement of substrates for the production of seedlings

Bioplant© a commercial productFootnote 1 was used as a substrate for the production of tomato seedlings, both as a control and in combination with the spent A. subrufescens compost (SASC) in different proportions, depending on each treatment. The SASC was obtained from the study carried out by Figueiredo et al. (2013), who used the CS10 strains (University of Lavras, Brazil), compost based on sugarcane bagasse, and coastcross hay with a casing layer of soil. In total, there were six treatments: Treatment 1–100 % Bioplant; Treatment 2–80 % Bioplant +20 % SASC; Treatment 3–60 % Bioplant +40 % SASC; Treatment 4–40 % Bioplant +60 % SASC, Treatment 5–20 % Bioplant +80 % SASC; Treatment 6–100 % SASC. The moisture contents of both substrates were determined after drying the samples in an oven at 60 °C for 48 h. The dry weight was determined by the weight difference between dry and wet weight of each sample (Bioplant and SASC) used in each treatment. The analyses of the SASC and chemical properties of the mixtures were done with colorimetric determination methods and are described in Tables 2 and 3 (Ansorena 1994; Pardo-Gimenez et al. 2010).

Table 2 Chemical composition of the spent A. subrufescens compost (SASC)
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Table 3 Chemical properties of the growing medium SASC based on tomato seedlings production
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Production and evaluation of tomato seedlings

The seedlings were grown in a greenhouse covered with a plastic sheet and sided with white screens. The seeds were sown in plastic trays with 200 cells, each containing the substrate of each of the six treatments, totaling 1200 seedlings. The seedlings were irrigated daily and were transferred to the field after 17 days, when they showed four true leaves.

At the transfer to the field, ten seedling samples from each of the six treatments were randomly selected to evaluate and quantify the level of growth of the tomato seedlings based on measurements and fresh weight of the seedlings. The following characteristics were analyzed: mass of the aerial portion, height of aerial portion, mass of root, length of root and total fresh weight.

Tomato cultivation from seedlings produced on different substrates

The tomato plants were cultivated with a spacing of 45 × 60 cm in three rows with staking. The experiment was a randomized block design with six repetitions, in which each plant is considered as a repetition. The buds were thinned when they were 3–5 cm long, and the tip was pruned when the last bunch had sprouted, reaching the desired amount of 4 bunches per plant.

To analyze the production of tomatoes, all the fruits from each plant were harvested in each of the four production flushes. The fruits were harvested when the “breaker” stage was attained, that is, when each tomato showed a reddish color on the apex in the weekly harvest. Only the commercially acceptable production was evaluated, and all damaged fruits were discarded.

The fruits were then evaluated with regard to the number of fruits per plant, the size according to the classification of the Ministry of Agriculture of Brazil (Table 4) and the total weight (tomato production, g plant−1).

Table 4 Classification of tomato fruits with regard to size, according to the norms of the Ministry of Agriculture of Brazil
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Regarding culture management, insecticides and fungicides were not used to control pests and diseases. Nutrients were also not supplemented through the use of fertilizers. Likewise, the weed growth was controlled manually rather than through the use of herbicides. Irrigation was performed daily from the moment of transplanting until the harvest period.

Statistical analysis

All the parameters were subjected to regression analysis using the program SISVAR.

Results and discussion

Production of the tomato seedlings

In the production of the tomato seedlings, the use of different proportions of SASC resulted in a decreasing tendency of all the parameters (Figs. 1, 2, 3).

Fig. 1
figure 1

Influence of spent A. subrufescens compost on the fresh mass and size of aerial part of tomato seedlings

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Fig. 2
figure 2

Influence of spent A. subrufescens compost on the fresh mass and length of roots of tomato seedlings

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Fig. 3
figure 3

Influence of spent A. subrufescens compost on the total fresh weight of tomato seedlings

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Considering the treatments with SASC, the best results were generally obtained with the treatments using 20 and 40 % SASC. The fresh mass of roots and size of the root were the parameters most negatively affected by the use of SASC, sharply decreasing with the addition of SASC, which may indicate a deficiency in the physical characteristics of the SASC.

Costa et al. (2012) used different substrates for the production of tomato seedlings. The results reported for all the tested parameters (plant height, stem diameter, total weight, mass of the shoots and mass of the root) were worse than those shown here. Steffen et al. (2010) tested substrates of rice husk and cow manure and also obtained worse results for plant height and fresh weight of the aerial portion than those obtained in this work with the use of SASC.

Medina et al. (2009) evaluated the use of SMC of Agaricus bisporus and Pleurotus ostreatus for the seedlings’ production of different vegetables species. None of the treatments containing SMC matched the peat (control) as growing medium for tomato seedlings production, but SMC from A. bisporus was better than P. ostreatus as component of the growing media. In the present study, although the best results were obtained with the control substrate (100 % Bioplant), all the treatments with different ratios of SASC achieved results as good as or even better than those obtained with other substrates in other studies.

Cultivation of tomatoes from seedlings grown on substrates based on SASC

In all flushes of tomato production, a positive effect was observed when the seedlings were produced with SASC in comparison to the control (Fig. 4). For each flush, variations among the treatments regarding the best production were observed. However, the treatment with 100 % SASC generally led to the best production in two flushes and the second-best production in the remaining two flushes. Considering the total production, the seedlings produced in the substrate with 100 % SASC had the greatest tomato production (Fig. 5). It is worth noting that, in addition to the treatment with 100 % of SASC, all the other treatments led to a larger production than the control, showing the positive effect of this substrate.

Fig. 4
figure 4

Flushes of tomato production from the seedlings grown using different proportions of spent A. subrufescens compost

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Fig. 5
figure 5

Total tomato production from seedlings grown using different proportions of spent A. subrufescens compost

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In comparison to the results obtained with conventional crops, the tomato production was lower in this study because pesticides and fertilizers were not used. The maximum production (53 t ha−1) was obtained when treating with 100 % SASC resulting in a yield of 1.43 kg of tomatoes per plant. When comparing organic and conventional cultivation, Bettiol et al. (2004) concluded that organic farming production corresponds to only 36.5 % of conventional production. Wamser et al. (2012) studied the productivity of tomato hybrids in super-high-density cultivation fields (44,444 plants ha−1), reporting a maximum yield of 170.7 t ha−1, whereas in traditional cultivation (22,222 plants ha−1), the maximum yield was 128.5 t ha−1. Assuming that the proportion of 36.5 % proposed by Bettiol et al. (2004) is correct, yields of 62.2 and 46.9 t ha−1 should be expected for super-dense and traditional cultivation, respectively, under an organic cultivation system. Therefore, the maximum yield obtained in the present work, 53 t ha−1, falls in the expected range for organic system.

In hydroponic cultivation, Albuquerque Neto and Peil (2012) reported a maximum total production of 54.6 t ha−1. The highest total yield reported by these authors is therefore practically the same as the maximum yield obtained in the present work. In addition to the numbers that were presented above, it is also important to emphasize that no fertilization procedures of any kind were used in the present work, either before or during the crop, because we aimed to evaluate the behavior of seedlings in the simplest crop management conditions possible. This information is important because despite the need to avoid chemical fertilizers in organic farming, the use of organic compost, green manure, bone meal and so forth is recommended.

Costa et al. (2011) evaluated the productivity of tomato cultivars tolerant to high temperature in an organic farming system using organic manure, bone meal and biofertilizer, with a maximum total production of 36.3 t ha−1. Marouelli et al. (2011) evaluated the effect of this type of irrigation system (dripping vs. sprinkler) on organic tomato cultivation using green fertilization with Crotalaria (Crotalaria pumila), applying organic compost and thermophosphate as well as applying Bordeaux mixture and a biopesticide (Bacillus thuringiensis). Under these conditions, these authors obtained a total production of 58.8 and 64.8 t ha−1 for the dripping and the sprinkler systems, respectively. These results were better than those obtained in this study (53 t ha−1). Nonetheless, it is important to emphasize that the authors used green fertilization, organic fertilizer and thermophosphate.

Spent mushroom compost and Trichoderma harzianum were effective when used against Meloidogyne javanica in tomato under field conditions in Dargai in Malakand Agency, Pakistan (Irfan-ud-Din et al. 2005). The author conclude that SMC stimulated flowering, plant height, fresh and dry shoot weight and increased yield by 101.9, 61.5, 27.9, 38.3 and 102.5 %, respectively; moreover, it reduced the number of galls/plant by 73.5 %. Modolon et al. (2012) used homeopathic preparations for pest control during the organic cultivation of tomatoes, also employing green fertilization procedures and applying compost. Under these conditions, the largest total production obtained was 15.5 t ha−1 in field cultivation and 29.8 t ha−1 in greenhouse cultivation.

The treatment without SASC induced a higher proportion of small and very small fruit in the tomato production, whereas the treatment with 100 % SASC led to a higher proportion of large and medium-sized fruit (Table 5).

Table 5 Influence of spent A. subrufescens compost on the classification of the total tomato production regarding the fruit size
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Therefore, the use of this substrate in the production stage of the seedlings resulted in more vigorous plants, leading not only to greater yields but also to fruits with greater size compared to the commercial control. Interestingly, the treatment with 80 % SASC led to the highest number of fruits among all the treatments. However, compared to the treatment with 100 % SASC, the production consisted almost exclusively of small and very small fruit, with not a single large fruit harvested.

Conclusions

We can conclude that the use of SASC for seedling production led to a higher, or at least equal, total tomato production compared to previously reported production levels in organic cultivation systems with green, organic and other types of fertilization. These results demonstrate the great potential of SASC for use in organic tomato production because of the better quality of harvested fruit.