Agrochemical characterization of vermicomposts produced from residues of Palo Santo (Bursera graveolens) essential oil extraction

Waste Management xxx (2016) xxx–xxx

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Agrochemical characterization of vermicomposts produced from residues of Palo Santo (Bursera graveolens) essential oil extraction Vinicio Carrión-Paladines a,⇑, Andreas Fries b, Beatriz Gómez-Muñoz c, Roberto García-Ruiz d,⇑ a

Department of Agricultural Sciences and Food, Technical University of Loja (Ecuador), San Cayetano Alto s/n, C.P. 11 01 608 Loja, Ecuador Department of Geology, Mine and Civil Engineering (DGMIC), Technical University of Loja (Ecuador), San Cayetano Alto s/n, C.P. 11 01 608 Loja, Ecuador c Section for Plant and Soil Sciences, Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Thorvaldsensvej 40, DK-1871 Frederiksberg C, Denmark d Ecology Section, Dept. Animal and Plant Biology and Ecology, University of Jaén, Spain b

a r t i c l e

i n f o

Article history: Received 13 June 2016 Revised 31 August 2016 Accepted 1 September 2016 Available online xxxx Keywords: Vermicompost Bursera graveolens waste Maturity Agrochemical characterization

a b s t r a c t Fruits of Palo Santo (Bursera graveolens) are used for essential oil extraction. The extraction process is very efficient, because up to 3% of the fresh fruits can be transformed into essential oil; however, a considerable amount of waste is concurrently produced (>97% of the fresh biomass). Recent developments in Ecuadorian policies to foster environmentally friendly agroforestry and industrial practices have led to widespread interest in reusing the waste. This study evaluated the application of four vermicomposts (VMs), which are produced from the waste of the Palo Santo fruit distillation in combination with other raw materials (kitchen leftovers, pig manure, goat manure, and King Grass), for agrochemical use and for carbon (C) and nitrogen (N) decomposition in two soils with different textures. The results showed that the vermicompost mixtures (VMM) were valuable for agricultural utilisation, because total N (min. 2.63%) was relatively high and the C/N ratio (max. 13.3), as well as the lignin (max. 3.8%) and polyphenol (max. 1.6%) contents were low. In addition, N availability increased for both soil types after the application of the VMM. In contrast, N became immobile during decomposition if the VM of the pure waste was added. This likely occurred because of the relatively low total N (1.16%) content and high C/N ratio (35.0). However, the comparatively low C decomposition of this VM type makes its application highly recommendable as a strategy to increase the levels of organic matter and C, as well as for soil reclamation. Overall, these results suggest that the residues of the Palo Santo essential oil extraction are a potential source for vermicompost production and sustainable agriculture. Ó 2016 Elsevier Ltd. All rights reserved.

1. Introduction Palo Santo (Bursera graveolens) is one of the most representative natural tree species of the dry forest areas in Ecuador (Sánchez et al., 2006). Traditionally, different parts of the tree are used in the local medicinal culture (Tene et al., 2007). The timber and leafs of Palo Santo are applied to prevent mosquito bites and to treat pains of different origin, such as stomach pain and rheumatism (e.g. Alonso-Castro et al., 2011). However, recently the production of essential oils is more attractive (Young and Chao, 2007; Manzano et al., 2009) because of the economic benefits caused by global demand (e.g. fine perfumes). Oil is extracted from the fruits, which are collected between March and May, by distillation, ⇑ Corresponding authors. E-mail addresses: [email protected] (V. Carrión-Paladines), aefries@utpl. edu.ec (A. Fries), [email protected] (B. Gómez-Muñoz), [email protected] (R. García-Ruiz).

generally by small-scale distillers. The distillation process is very efficient and fresh fruits contain up to 3% of essential oil (e.g. Santos et al., 2016). To avoid the despoliation of the Palo Santo species and to guarantee the long-term sustainability and the socio-economic viability of the local population, the regional and national authorities have designed a sustainable management program. The regulation states that only small groups from the communities can collect one third of the fruits produced each year for essential oil extraction (Ministerio de Agricultura, Ganadería, Acuacultura y Pesca de Ecuador [MAGAP, 2013]). To date, the majority of the oil is produced within the campus of the Technical University of Loja/ Ecuador (Universidad Técnica Particular de Loja [UTPL]), but efforts are also being made so the oil can be extracted by local communities in the near future. Therefore, proper waste management is needed to fulfil the requirements of the integrative sustainable management program.

http://dx.doi.org/10.1016/j.wasman.2016.09.002 0956-053X/Ó 2016 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Carrión-Paladines, V., et al. Agrochemical characterization of vermicomposts produced from residues of Palo Santo (Bursera graveolens) essential oil extraction. Waste Management (2016), http://dx.doi.org/10.1016/j.wasman.2016.09.002

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During the distillation process, a huge amount of waste is generated (>97% of the fresh biomass), which consists mainly of the skin and seeds of the fruits (Andrade et al., 2010). Agroforestry waste recently became of interest in Ecuador, because new national policies foster environmentally friendly practices (MAGAP, 2013). Special attention is given to waste production in agroforestry, such as the residues from Palo Santo distillation. The organic waste should be recycled to provide nutrients through the generation of vermicomposts (VMs), which can be used as organic fertilizer in agriculture. This solution can improve soil fertility, reduce the application of inorganic fertilizer, and provide an additional source of revenue for the local communities. Vermicomposting is an option for the integral management of organic solid residues (Hussain et al., 2015; Madan and Rathore, 2015). Nevertheless, processing time and quality of the final product depend not only on the activity of the microorganisms and earthworms, but also on the initial composition of the raw materials (Singh et al., 2013). A wide and diverse range of residues and by-products have been valorised through vermicomposting; for example, residues originating from the seeds of Cyamopsis tetragonoloba (Suthar, 2006), waste from the sugar industry (Sen and Chandra, 2007), residues from the leather industry (Ravindran et al., 2008), mud from textile factories (Garg and Kaushik, 2005), and waste from distilleries (Suthar and Singh, 2008), as well as from industrial beverage production (Singh et al., 2010). Recent investigations have found that VMs contain appropriate levels of nutrients (Mondal et al., 2015) and a carbon-to-nitrogen ratio (C/ N) suitable for agriculture proposes (El-Haddad et al., 2014). Typically, the generated VMs include more available nutrients per kg than the organic substrate from which they were made (Buchanan et al., 1988). VMs also have demonstrated impressive effects on the growth of different cultivations under field conditions (Kashem et al., 2015). These organic fertilizers are widely used for vegetable growth because they facilitate nutrient transfer to the plants (Kaur et al., 2010). To our knowledge, there have been no studies evaluating the potential use of VMs produced from the waste of Palo Santo essential oil extraction in agricultural applications. To promote vermicomposting of this waste and to improve the composting procedure, more information on the agrochemical characterization and nutrient supply is needed. The pure waste has a semi-solid consistency and, in contrast to other organic waste (e.g. domestic waste), does not need an additional separation into different materials, nor does it require further improvements for VM generation (Sakawi, 2011). Generally, VMs only made of plant residues and bulking agents do not provide all the necessary properties (nutrients) for agricultural applications (Moldes et al., 2007), whereas mixtures with other organic raw materials are used to improve the quality of the final product (fertilizer). Thereby, mixtures with locally available and economic organic raw materials, such as cow dung and market waste, among others are preferable for long-term sustainability of VM production (Soobhany et al., 2015; Taeporamaysamai and Ratanatamskul, 2016). In southern Ecuador, the most common organic raw materials are kitchen leftovers and residues from livestock farming, such as goat and pig manure, as well as King Grass (Pennisetum purpureum).

The goals of the present study were the agrochemical characterization of four different VMs based on the waste from Palo Santo oil extraction and evaluation of the soil carbon (C) and nitrogen (N) dynamics after their application. The agrochemical characterization also included bioassays of phytotoxicity (Zucconi Test) to screen the suitability of the final products for field application. 2. Material and methods 2.1. Vermicompost preparation The waste of the essential oil extraction was obtained from the UTPL Natural Products Plant Institute (Loja, Ecuador). The pure waste consisted of the skin and seeds of the Palo Santo fruits, which contained mostly fibre, water, fatty acids, and ash with a pH of approximately 4.4 (Andrade et al., 2010). Besides the VM of the pure waste (BP), which was generated without any other organic material, three VM mixtures (VMM) were produced to compare their properties. The three VMM were made of the pure waste and other organic residues in different percentages. For this study, (i) King Grass residues, (ii) kitchen leftovers, and (iii) pig and goat manure were used because these organic wastes were common in the rural dry forest areas of Ecuador and therefore easy to collect from the local population (e.g. Pesántez et al., 2014). Some characteristics of the organic raw materials used are shown in Table 1. The first VMM was a 1:1 wet weight composition of pure waste and kitchen leftovers (BPK), the second was a 1:1 mixture of pure waste and pig manure (BPP), and the third VMM contained 50% pure waste, 25% goat manure, and 25% King Grass residue (BPS). A total of 111 kg (equivalent to 0.6 m3) of each substrate (BP, BPK, BPP, and BPS) were piled up in roofed boxes of clinker stone (size: 1 m wide, 2 m long, and 0.3 m high) on a cement surface to minimise nutrient loss caused by leaching and to avoid overwetting during rainfall events. After two weeks of precomposting, 1000 earthworms (here: Eisenia fetida; equivalent to 600 g) were added to each box to begin the vermicomposting process. To control the progress of vermicomposting, the temperature and humidity of the different VMs were measured weekly. Maximum temperature reached values between 31 °C and 36 °C, which is an acceptable environment for the growth and reproduction of earthworms (e.g. Adi and Noor, 2009). After 13 weeks of vermicomposting, the temperature of all substrates stayed constant (15 °C), indicating the maturation of the VMs (Majlessi et al., 2012). The vermicomposting process reduced the original amount of the substrates to approximately 66.6 kg. From the final VMs, five samples (200 g each) were collected at different sites within each box, merged, and transported on the same day to the laboratory, where they were air-dried and stored in a cold environment (4 °C) prior to analysis. 2.2. Analytical methods A fraction of the air-dried VM samples was used for electrical conductivity and pH determination. This was conducted in an aqueous extract (substrate/extractant ratio: 1/10 v/v). Other parts

Table 1 Main characteristics of the organic raw materials. Values are the mean and ± stands for standard deviation. Parameter

Bursera graveolens

Kitchen Leftovers

Goat Manure

Pig Manure

King Grass

Water content (%) C (%) N (%) C/N pH

72.4 47.3 ± 0.2 1.6 ± 0.1 30 ± 3.2 4.5 ± 0.1

81.8 46.1 ± 0.3 2.9 ± 0.2 16 ± 1.1 5.3 ± 0.3

21.8 33.3 ± 0.3 3.0 ± 0.0 11 ± 0,6 8.5 ± 0.3

72.9 40.3 ± 0.2 2.4 ± 0.1 17 ± 0.7 8.1 ± 0.3

73.03 41.5 ± 0.1 0.4 ± 0.0 97 ± 0.9 –

Please cite this article in press as: Carrión-Paladines, V., et al. Agrochemical characterization of vermicomposts produced from residues of Palo Santo (Bursera graveolens) essential oil extraction. Waste Management (2016), http://dx.doi.org/10.1016/j.wasman.2016.09.002

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of the air-dried samples were crushed to powder (<1.0 mm) using a ball mill, to analyse the organic matter content by loss on ignition (LOI) at 550 °C for 3 h (Nelson and Sommer, 1982). Total C (TC) and total N (TN) contents were determined using a CHN auto-analyser (Carlo Erba NA200, Milan Italy). Potential N mineralization (CNM) was determined following the method of Lober and Reeder (1993). To analyse the content of hot water C (HWC), 2 g of each VM were mixed with 35 mL of distilled water, shaken for 16 h at 80 °C, and following centrifugation (5000 rpm for 5 min) the supernatant was filtered (Ghani et al., 2003). Using the HWC extracts (filtered supernatants), total organic C was determined using a Skalar Formacs analyser and then soil available organic C (AOC) was calculated. Total extractable polyphenol content (TEP) was determined using Folin-Ciocalteu reagent, according to the method described by Anderson and Ingram (1993). Acid detergent fibre (ADF) was determined following the method of Van Soest (1963). Acid detergent lignin (ADL) was measured using an acid detergent solution with cetyltrimethyl ammonium bromide (CTAB) and H2SO4 for digesting. Additionally, the ADL data were corrected for ash content. VM phytotoxicity was determined by the Zucconi Test, whereby 10 seeds of Lepidium sativum were incubated in a Petri dish, loaded with 5 mL of the individual aqueous extracts (1:10) and stored for 7 days. The germination index (GI) was calculated as follows (Zucconi et al., 1981):



   G L   100 GI ¼ Go Lo

ð1Þ

where G is the germination percentage of the seeds in aqueous extract, Go the germination percentage of the seeds in the control solution (distilled water), L the root mean length in the aqueous extract and Lo the root mean length in the control solution.

2.3. Carbon and nitrogen mineralization To analyse the organic C and net N mineralization in soils amended with the different VMs, an aerobic incubation experiment was conducted. An assay was performed in 500 mL Kilner jars with two soils of different textures (loam soil and sandy soil with a particle size <2 mm). The calcisol (loam soil) contained 5.7% of LOI, 3.2% organic C, and 0.23% of TN, whereas the values of the sandy soil were 1.3% of LOI, 0.5% of organic C, and 0.05% TN. Three replicates of 150 g of each soil were mixed with the individual VMs, equivalent to adding 4000 lg C g1 of soil, and a control soil without any amendments was prepared. After mixing, deionized water was added to the soils to bring the moisture content to 60% of its water-holding capacity. Finally, samples were incubated in the dark for 45 days at 20 °C. During the incubation period C-CO2 production was measured following the NaOH trap method described by Anderson (1982). Briefly, small test tubes (12 mL) were filled with 10 mL of NaOH (1 N) and inserted into the Kilner jars, which were then hermetically closed. The CO2 production was recorded after day 3, 7, 16, 28, and 45 by means of titration with HCl (0.5 N). The CO2 emissions of the VMs were estimated by subtracting the C-CO2 emission of the control soil from the C-CO2 emission of the amended soils. Net N mineralization and nitrification was determined by measuring the nitrate and ammonium concentration of soil extracts during incubation. At each sampling day, 3.5 g of soil were collected from the Kilner jars and subjected to extraction with 35 mL of 2 M KCl (with agitation for 1 h). After filtration, N-nitrate and N-ammonium were determined following the methodology of Keeney and Nelson (1982). Net N mineralization

(NM) and net N nitrification (NN) were calculated using the equations below:



NMðlg N g

1

1

d Þ¼

NO3 þ NH4

final

   NO3 þ NHþ4 initial

Incubation time ðdaysÞ 

NMðlg N g1 d Þ ¼



1

NO3

 final

   NO3 initial

Incubation time ðdaysÞ

ð2Þ

ð3Þ

2.4. Statistical analysis To analyse the differences in the measured variables between the VM samples, a one-way analysis of variance (ANOVA) and Fisher’s post hoc tests were applied. As necessary, a variance analysis (homoscedasticity and normality) was also tested by means of the totality of the transformed datasets (log [dependent variable value] + 1). The correlations between the measured variables were determined by the Pearson correlation coefficient; significance was accepted at P < 0.05 in all cases. 3. Results and discussion 3.1. Agrochemical characterization Table 2 shows the main biochemical properties of all VMs generated from the waste of the Bursera graveolens oil extraction. BP had the highest organic matter content (69%). This value exceeded the organic matter content of other VMs made from pure organic waste of fruits used in oil extraction, such as the olive mill pomace (60%; Gómez-Muñoz et al., 2011), but did not reach the high values of other plant residues, such as that from Oryza sativa (rice straw, 99%; El-Haddad et al., 2014). The organic matter content of the VMM showed significantly lower values (from 58.1–63.1%; Table 2) compared to BP, but these values were still higher than the organic matter content typically found in cow, sheep, and poultry manures (approximately 30%; Moral et al., 2009). However, the difference in organic matter content between the individual VMM was not significant. As expected, the TC content of BP (40.8%) and the VMM (34.7% on average) were closely related to the organic matter content (r = 0.91; P < 0.05). The soils of the dry forests of southern Ecuador and northern Peru are characterized by relatively low organic matter content (typically <1%; Rasal Sánchez et al., 2011). Therefore, BP and the VMM were highly suitable for application to soils to increase organic matter and TC content. The TN content of the VMM ranged from 2.6% to 2.9%, which was higher than the value of BP (1.2%, Table 2). Typically, the TN of VMs made from kitchen residues, animal excrement, or plant residues without additives ranges between 1.0% and 2.0% (e.g. Alidadi et al., 2016), but TN values of all VMM were higher. This was caused by the intermixture of the pure waste with other organic waste rich in N, for which reason TN of all VMs increased (Moldes et al., 2007). The C/N ratio of BP was approximately 35.0 (Table 2), which may cause the immobilization of nutrients during the decomposition process, because it has been reported that a source of organic matter with a C/N ratio over 25.0 causes N immobilization (e.g. Tognetti et al., 2006). In contrast, the C/N ratio of the VMM exhibited values between 11.9 and 13.3, close to the optimal values of <10.0 (Bernal et al., 2009). Therefore, in terms of N availability, the low C/N ratio of the VMM made them suitable for agricultural purposes. The lowest C/N ratio was achieved by BPK because of its relatively low TC and high TN content (Table 2). Potential N mineralization (CNM, Table 2) has been used as an indicator of material-derived N availability in the short term. BP

Please cite this article in press as: Carrión-Paladines, V., et al. Agrochemical characterization of vermicomposts produced from residues of Palo Santo (Bursera graveolens) essential oil extraction. Waste Management (2016), http://dx.doi.org/10.1016/j.wasman.2016.09.002

c

d

a

b

Acid detergent lignin. Total extractable polyphenolds. Capacity for N mineralisation. Negative value indicates that NH+4-N was consumed rather than released and thus a there was net N (biological and/or chemico-physical) immobilization. Available organic carbon (hot water extractable).

21.7b ± 2.2 1.56c ± 0.49 0.51c ± 0.11 1.11d ± 0.1 3.0d ± 0.1 44.9c ± 14.7 34.4b ± 1.4 Pure waste of Bursera graveolens, King grass residues and goat manures; 50:25:25. BPS

61.7b ± 4.3

2.76b ± 0.12

12.4b ± 0.9

3.8c ± 0.3 35.0b ± 1.9 63.1b ± 5.2 Pure waste of Bursera graveolens and pig manure; 50:50. BPP

34.8 ± 0.4 Pure waste of Bursera graveolens and kitchen leftovers; 50:50. BPK

58.1 ± 2.7

2.63b ± 0.17

11.9 ± 0.4 2.93 ± 0.12

13.3c ± 0.1

97.5a ± 18.8

1.4c ± 0.3

33.8c ± 3.2 2.23b ± 0.86 0.60c ± 0.12 1.44c ± 0.1

0.88 ± 0.1 0.8 ± 0.3 2.6 ± 0.2 63.9 ± 22.0

1.6c ± 0.2

26.8b ± 3.4 2.74 ± 1.14 0.27 ± 0.11

b

0.26a ± 0.12 2.5a ± 0.27

b b

9.4a ± 0.4 2.8a ± 0.2

b b

11.0a ± 0.9 103.6a ± 34.3

b b

35.0a ± 1.9

b

1.16a ± 0.04 40.8a ± 1.4

b

Pure waste of Bursera graveolens BP

69.3a ± 3.4

b

CNMc (mg N g1 residue) TEP-to-N ratio ADL-to-N ratio TEPb (%) ADLa(%) Germination index (%) C-to-N ratio Total N content (%) Total C content (%) Organic matter (%) Raw materials Final product

Table 2 Main biochemical characteristics of the VMs made of waste of the Bursera graveolens oil extraction. Different letter means significant differences (P < 0.05; n = 3).

12.8a ± 3.1

V. Carrión-Paladines et al. / Waste Management xxx (2016) xxx–xxx

AOCd (mg TOC g1 residue)

4

showed values of approximately 0.26 mg (N) g1, which was notably lower compared to the VMM (1.56–2.74 mg (N) g1). Generally, negative CNM-values indicate that NH+4 - N is consumed rather than released during decomposition, which leads to a net N immobilization (biological, chemical, and/or physical) when applied to soils (Hu et al., 2015). In the present study, all values were positive, indicating a feasible application to soils; although the CNM value of BP was close to zero, which signified low potential N availability during decomposition but agrees well with the relatively high C/N ratio (Singh et al., 2014). Values of TN and the C/N ratio of the VMM were acceptable, therefore, agricultural applications can be recommended, especially on soils of the dry forests in Ecuador, which are characterized by low TN content (Rasal Sánchez et al., 2011). The germination index (GI) is an indicator for phytotoxicity. GI values below 50% indicate high phytotoxicity, values between 50% and 80% moderate phytotoxicity, and values over 80% no phytotoxicity (Zucconi et al., 1985; Emino and Warman, 2004). BP (103.6%) and BPP (97.5%) had values above 80% (Table 2) and therefore can be recommended for agricultural purposes. In contrast, BPK (63.9%) showed moderate phytotoxicity and BPS (44.9%) high phytotoxicity. Low GI values were also reported from VMs made of herbs from the pharmaceutical industry (Suthar and Singh, 2012), municipal green waste, and yard waste (Haynes and Zhou, 2016). The increased phytotoxicity complicates the germination of the seeds, which may be caused by the herbs inside the VMs because of their allelopathic substances (Suthar and Sharma, 2013). 3.2. Carbon decomposition The CO2 emission of soils without amendment (control soil) displayed higher values for loam soil (334.9 lg C-CO2 g1) than for sandy soil (207.0 lg C-CO2 g1) after 45 days of decomposition (Fig. 1). In addition, average daily C-CO2 emission rate was 2.2 times higher for loam soil than for sandy soil. The differences were likely caused by the levels of organic matter, the TC content, and the organic C availability (Lozano-García and Parras-Alcántara, 2013), which were significantly higher in the loam soil. The addition of BP and VMM resulted in greater CO2 production compared to the control soils, which were also independent of soil texture (Fig. 1). This effect was caused by the use of labile C for the synthesis of new microbial biomass and its loss through respiration (approximately 40%; Millar and Baggs, 2004). Generally, the rate of CO2 production declines throughout incubation, when the source of labile C becomes depleted. After 45 days of incubation, the rate of CO2 production stabilized at relatively low values (Fig. 1), likely because most of the labile C was consumed. Highest values of cumulative C-CO2 emissions after 45 days were found for BPP (loam: 1865.3 lg C-CO2 g1, sandy: 1142.1 lg C-CO2 g1), followed by BPK (loam: 1712.9 lg C-CO2 g1, sandy: 1027.7 lg C-CO2 g1) and BPS (loam: 1376.8 lg C-CO2 g1, sandy: 725.6 lg C-CO2 g1), independent of soil type. Cumulative C-CO2 emissions of the BP was lower (loam: 853.1 lg C-CO2 g1; sandy: 398.5 lg C-CO2 g1) compared to the VMM, but significantly higher than for the control soils. This result was confirmed by Paradelo et al. (2010), who indicated an increase in CO2 production in soils amended with VMs, because of greater microbial respiration. After 45 days of decomposition 12.9% (BP), 24.0% (BPS), 34.4% (BPK), and 38.2% (BPP) of organic C was emitted as CO2 in the loam soils (Table 3). Similar values of CO2 emission were reported by Ajwa and Tabatabai (1994), who analysed the decomposition of different organic materials in soils. The relatively low organic C decomposition of BP was likely caused by its refractory features.

Please cite this article in press as: Carrión-Paladines, V., et al. Agrochemical characterization of vermicomposts produced from residues of Palo Santo (Bursera graveolens) essential oil extraction. Waste Management (2016), http://dx.doi.org/10.1016/j.wasman.2016.09.002

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Fig. 1. C-CO2 emission (lg C-CO2 g1) following the addition of the pure waste of the essential oil extraction of the fruit of Palo de Santo (BP) and vermicompost made of this by-product and kitchen residues (BPK), pig manure (BPP) and a mixture of goat manure and King grass (BPS) in a loam (a) and sandy (b) soil. Error bars represent the standard deviation (n = 3).

Table 3 45-d cumulative CO2 emission and net nitrification in loam and sandy soils amended with VMs. Different letter mean significant differences (One way ANOVA; P < 0.05). Loam soil

BP BPK BPP BPS

Sandy soil

Cumulative C-CO2 emission (lg C-CO2 g1 45-d)

% of C-CO2 emission of that added

Net nitrification (lg N g1 d1)

Cumulative C-CO2 emission (lg C-CO2 g1 45-d)

% of C-CO2 emission of that added

Net nitrification (lg N g1 d1)

518.1a ± 10.8 1377.9b ± 20.8 1530.3c ± 31.4 1041.9d ± 19.2

12.9a ± 0.2 34.4b ± 0.5 38.2c ± 1.1 26.4d ± 0.4

0.98a ± 0.02 0.81b ± 0.13 0.69b ± 0.08 0.53c ± 0.17

191.4a ± 24.6 820.6b ± 38.0 935.0b ± 72.1 518.5c ± 28.4

4.8a ± 0.6 20.5b ± 0.9 23.4b ± 1.8 12.9c ± 0.7

0.3a ± 0.01 0.28b ± 0.09 0.20c ± 0.14 0.11d ± 0.12

As Adamczyk et al. (2013) mentioned, organic C decomposition depends on lignin (ADL) and polyphenol (TEP) contents. The higher the ADL and TEP content are, the lower the availability of organic carbon (AOC; see Table 2). The percentage of emitted CO2 was much lower in the sandy soil (BP: 4.8%, BPS: 12.9%, BPK: 20.5%, BPP: 23.4%), because organic soil C was significantly lower than that of the loam soils (see Section 2.3). The cumulative C-CO2 emission in both loam and sandy soils (Table 4) was positively correlated with AOC (loam: r = 0.91,

sandy: r = 0.89; P < 0.05) and TN (loam: r = 0.85, sandy: r = 0.81; P < 0.05), but negatively correlated with the C/N ratio (loam: r = 0.87, sandy: 0.83; P < 0.05), ADL (loam: r = 0.85, sandy: r = 0.79; P < 0.05), TEP (loam: r = 0.77, sandy: r = 0.73; P < 0.05), and TC (loam: r = 0.73, sandy: r = 0.67; P < 0.05). These correlations were expected, because the higher ADL, TEP, and the C/N ratio are, the lower the C decomposition rate becomes. In contrast, the higher the AOC and TN are, the higher C decomposition (Qiu et al., 2015).

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Table 4 Pearson correlation coefficient between cumulative CO2 emission and net nitrification of the pure waste and vermicomposts including some agrochemical properties. Correlations were significant (P < 0.05) except for Germination index (‘‘n” means not significant correlation).

LCCEa SCCEb LNNc SNNd

Total C content (%)

Total N content (%)

C-to-N ratio

Germination index (%)

ADL (%)

TEP (%)

AOCf (mg TOC g1)

ADL-to-N ratio

TEP-to-N ratio

CNMe (mg N g1)

0.73 0.67 0.83 0.82

0.85 0.81 0.95 0.84

0.87 0.83 0.97 0.88

n n n n

0.85 0.79 0.96 0.89

0.77 0.73 0.87 0.76

0.91 0.89 0.79 0.78

0.88 0.82 0.98 0.90

0.86 0.82 0.96 0.86

0.78 0.78 0.78 0.77

LCCE; cumulative C-CO2 emission (lg C-CO2 g1 45-d) in loam soil. SCCE; cumulative C-CO2 emission (lg C-CO2 g1 45-d) in sandy soil. c LNNRC; net N nitrification (lg N g1 d1) in loam soil. d LNNRC; net N nitrification (lg N g1 d1) in sandy soil. e Capacity for N mineralisation. Negative value indicates that NH+4-N was consumed rather than released and thus a there was net N (biological and/or chemico-physical) immobilization. f Available organic carbon (hot water extractable). a

b

3.3. Nitrogen mineralization 1 Concentrations of nitrate (lg N-NO ) in the loam soil 3 g amended with the VMM were significantly higher than those in the control soil and BP after 7 days of incubation (Fig. 2a). After 45 days, soil nitrate concentrations of the amended soils were

1.35 to 1.61 times higher compared with that of the control soil, and 8.01–9.64 times higher than that of the BP amended soil. During the decomposition of organic N in the VMM, nitrate is produced continuously and the highest values were achieved for BPK 1 1 (84.80 lg N-NO ), BPP (78.26 lg N-NO ), and BPS 3 g 3 g 1 (70.46 lg N-NO ). As shown in Fig. 2a, the soil nitrate 3 g

1 Fig. 2. Concentration of soil nitrate (lg N-NO ) following the addition of the pure waste of the essential oil extraction of the fruit of Palo de Santo (BP) and vermicompost 3 g made of this by-product and kitchen residues (BPK), pig manure (BPP) and a mixture of goat manure and King grass (BPS) in a loam (a) and sandy (b) soil. Error bars represent the standard deviation (n = 3).

Please cite this article in press as: Carrión-Paladines, V., et al. Agrochemical characterization of vermicomposts produced from residues of Palo Santo (Bursera graveolens) essential oil extraction. Waste Management (2016), http://dx.doi.org/10.1016/j.wasman.2016.09.002

V. Carrión-Paladines et al. / Waste Management xxx (2016) xxx–xxx

decreased for BP, which can be explained by negative net N mineralization and nitrification rate caused by the relatively high ADL and TEP content and low TN content (Table 2). After 45 days of 1 incubation, the N concentration of BP was 8.9 lg N-NO and 3 g 5.9 times lower than that of the control soil (Fig. 2a). Overall, patterns were similar in the sandy soils, but nitrate concentrations were notably lower, because of the extremely low TN content of the soil (0.05%, see chapter 2.3). After 45 days of 1 incubation, nitrate concentration of 28.4 lg N-NO (BPK), 3 g 1  1 25.9 lg N-NO g (BPP), 22.1 l g N-NO g (BPS), 17.1 lg N3 3 1 1 NO (sandy control soil), and 0.5 lg N-NO (BP) were mea3 g 3 g sured (Fig. 2b). Thus, the VMM (BPK, BPP, and BPS) were sources of available N once applied to soils. This indicated that a direct application of the VMMs might be an appropriate strategy to provide available N for crops. Ammonium concentrations in the loam soil amended with VMM quickly increased after 3 days of incubation (Fig. 3a). Maximum values were observed between day 7 and day 16 (BPK: 17.3 lg N-NH+4 g1; BPP: 14.8 lg N-NH+4 g1, BPS: 14.2 lg N-NH+4 g1), which afterwards declined to their initial values. The ammonium concentration of BP and the control soil (loam) displayed a

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different behaviour; values were stable during the first 3 days of incubation, but then decreased rapidly to values near zero. The sandy soil showed the same pattern as the loam soil, but with notably lower values for all samples (lower than 3.0 lg NNH+4 g1, Fig. 3b), likely caused by the low content of organic matter in this soil. Furthermore, the extreme values of VMM were not as pronounced; the ammonium concentrations were more or less stable during the 45 days of incubation, although a small maximum could be observed between day 3 and day 7 (BPK: 2.3 lg N-NH+4 g1; BPP: 2.8 lg N-NH+4 g1, BPS: 1.7 lg N-NH+4 g1). Net N mineralization and net N nitrification were used as indicators to estimate the plant available N (Neill et al., 1999). Net N nitrification for BP and VMM is shown in Table 3. In loam soils the values ranged from 0.98 lg N g1 d1 (BP) to 0.81 lg N g1 d1 (BPK), whereas for sandy soil they were between 0.30 lg N g1 d1 (BP) and 0.28 lg N g1 d1 (BPK). The negative values of BP indicated net N immobilization in both soil types, which was caused by the high C/N ratio (Table 2) and relatively high lignin and polyphenol content of BP (Padmavathiamma et al., 2008) In contrast, BPK, BPP, and BPS showed positive values for both soil types (Table 3), which indicated an increase in N

Fig. 3. Concentration of soil ammonium (lg N-NH+4 g1) following the addition of the pure waste of the essential oil extraction of the fruit of Palo de Santo (BP) and vermicompost made of this by-product and kitchen residues (BPK), pig manure (BPP) and a mixture of goat manure and King grass (BPS) in a loam (a) and sandy (b) soil. Error bars represent the standard deviation (n = 3).

Please cite this article in press as: Carrión-Paladines, V., et al. Agrochemical characterization of vermicomposts produced from residues of Palo Santo (Bursera graveolens) essential oil extraction. Waste Management (2016), http://dx.doi.org/10.1016/j.wasman.2016.09.002

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V. Carrión-Paladines et al. / Waste Management xxx (2016) xxx–xxx

availability. Highest values were obtained when BPK was added to the soils (loam: 0.81 lg N g1 d1; sandy: 0.28 lg N g1 d1), followed by BPP (loam: 0.69 lg N g1 d1; sandy: 0.20 lg N g1 d1), and BPS (loam: 0.53 lg N g1 d1; sandy: 0.11 lg N g1 d1). The highest nitrification rate observed in BPK was likely because the mixture of kitchen waste contained more TN (2.9%) and the lowest C/N ratio (11.9). In both soil types, net nitrification rates were positively correlated with TN content (loam: r = 0.95, sandy: r = 0.84; P < 0.05), AOC (loam: r = 0.79, sandy: r = 0.78; P < 0.05), and CNM (loam: r = 0.78, sandy: r = 0.77; P < 0.05), whereas they were negatively correlated with TC (loam: r = 0.83, sandy: r = 0.82; P < 0.05), ADL (loam: r = 0.96, sandy: r = 0.89; P < 0.05), and TEP (loam: r = 0.87, sandy: r = 0.76; P < 0.05). The biochemical composition or quality of organic matter sources determined the N release in soils. The negative correlations indicated that the quality descriptor of these elements had a strong influence on reducing N release during decomposition, throughout N immobilization. The contents of ADL and TEP of added organic matter are known to delay N release during its decomposition (e.g. Baggs et al., 2000), either by forming recalcitrant N compounds, or binding to soil microbial enzymes and lowering available N in soil. In general, TN, ADL, and TEP contents of VMs were robust indices for the prediction of N mineralization after incorporation into soils (Palm and Sanchez, 1991). Typical thresholds for immediate net N mineralization were >1.7% TN, <15% ADL, and <30– 40% TEP content. These criteria fit well with the VMM, but not with BP, which contained a low TN and a relatively high ADL and TEP content. Using only the pure waste of the oil-extraction (BP), available N would be insufficient to match the available C, resulting in N immobilization in the soil. Our results supported the hypothesis that tannins, like TEP, reduce N availability by sequestering organic N sources, as well as increasing N immobilization when acting as a source of C. The application of BP to soils might promote temporary immobilization of the available N, but offers the potential to lower losses of N by denitrification and leaching when soil available N is not demanded by plants (Celaya-Michel and Castellanos-Villegas, 2011).

4. Conclusions The study confirmed that the VM made only of the pure waste (BP), produced during the essential oil extraction from the fruits of Bursera graveolens, did not provide available N during decomposition, at least in the short term. However, BP was an excellent source to stabilize organic matter and organic C. Indeed, the high contents of lignin and polyphenols of BP, led to N immobilization (negative net N mineralization and nitrification). Nevertheless, the high levels of organic matter and TC made it suitable for application to soil if the objective was to increase the soil organic matter and total carbon content, as well as for soil reclamation, which is required for the soils of the dry forests in Ecuador, characterized by low levels of organic matter. Mixing the pure waste with other sources of locally available organic raw materials improved the final products in terms of N and C. The generated VMM were valuable for agricultural utilisation as total nitrogen was relatively high, whereas the C/N ratio, and lignin and polyphenol content was relatively low. Net N mineralization and net nitrification were positive in both loam and sandy soils, and therefore N availability increased after addition of the VMM. However, BPK and BPS should be improved (e.g. other proportions of raw materials), because of their moderate to high phytotoxicity. In the near future essential oil extraction from the fruits of Bursera graveolens will be conducted directly by the local popula-

tion of the dry forest areas in Ecuador. The produced organic waste from the distillation process will be recycled to generate different types of VMs. Hence, the different VMs can be examined under field conditions and the pros and cons of each VMM proved and tested.

Acknowledgements This work has been possible thanks to the generous contribution of the Secretariat of Science and Technology of Ecuador and the Department of Agricultural Sciences and Food of the Universidad Técnica Particular de Loja.

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Please cite this article in press as: Carrión-Paladines, V., et al. Agrochemical characterization of vermicomposts produced from residues of Palo Santo (Bursera graveolens) essential oil extraction. Waste Management (2016), http://dx.doi.org/10.1016/j.wasman.2016.09.002