The effect of arbuscular mycorrhiza, rice husk compost and biochar on Iranian borage Echium amoenum Fisch & C. A. Mey and post-harvesting soil properties
Einfluss vesikulär-arbuskulärer Mykorrhiza, compostierter Reisspreu und Biochar auf Eigenschaften von iranischem Gurkenkraut Echium amoenum, Fisch & C. A. Mey und den Bodenzustand nach der Ernte
Journal für Kulturpflanzen, 71 (1). S. 14–25, 2019, ISSN 1867-0911, DOI: 10.5073/JfK.2019.01.02, Verlag Eugen Ulmer KG, Stuttgart
This study was conducted to investigate the effect of rice husk compost (RHC), rice husk biochar (RHB) and mycorrhization (MY) on some properties of Iranian Echium amoenum Fisch & C. A. Mey and also on some selected post-harvesting soil properties. A completely randomized design experiment was conducted with six treatments and six replications. Treatments comprised T1: control, T2: MY, T3: RHC, T4: RHB, T5: RHC + MY and T6: RHB + MY. Studied parameters included; shoot and root fresh weights, root and leaf length, shrub height, leaf number, shoot and root NPK content, shoot and root Fe, Zn, Cu and Mn concentration, root colonization percentage, soil NPK status, soil micronutrients concentrations, soil respiration and microbial biomass. Results revealed that application of RHC, RHB and MY individually or in combination with other treatments significantly affected studied parameters. In all cases except for root colonization, combined application (T5 and T6) had more satisfied impacts compared with a single application of treatments.
Key words: Rice husk compost, Rice husk biochar, Mycorrhiza, Echium growth, Soil properties
In einem Gewächshausversuch wurde der Einfluss von Bio-Düngern, wie vesikulär-arbuskulärer Mykorrhiza, Compost und Biochar aus Azolla-Algen auf Ertrag, Ertragsstruktur sowie die Aufnahme an Haupt- und Spurenelementen von iranischem Gurkenkraut geprüft. Gegenstand der Untersuchung war auch der Nährstoffgehalt der Böden nach der Ernte, sowie deren biologische Aktivität. Alle geprüften Behandlungen zeigten im Vergleich zu den Kontrollen signifikante Effekte auf Ertrag und Nährstoffaufnahme. Höhere Bodenatmung und eine höhere mikrobielle Biomasse indizieren eine Steigerung der Fruchtbarkeit der Böden durch die Behandlungen.
Stichwörter: Iranisches Gurkenkraut, Bio-Dünger, Nährstoffaufnahme, Bodenatmung, mikrobielle Biomasse
In recent years, the safe agriculture is one of the main concerns in the world (El-Kouny, 2002). Furthermore, in accordance with recent research reports there has been an increasing awareness of the harmful effect of chemical fertilizers on the environment, as well as the potentially dangerous effects of chemical residues in plant tissues on human and animal health (El-Quesni et al., 2010). Low input cropping systems and innovation of modern management of resources are considered in sustainable agriculture, therefore, using organic fertilizers instead of mineral fertilizers is the first step towards sustainability (Salehi et al., 2016). Soil organic matters are generally one of the most important criteria of soil quality and have an influence on the processes occurring in the soil and many soil properties (Gulser and Candemir, 2012; Cercioglu et al., 2014). There are different methods to achieve safe agricultural and using compost is one of them. Composting agricultural residues by supplying the natural microbial flora present on them, their requirements of inorganic nutrients such as nitrogen and phosphorus and applying a proper moistening finally produces a high able production to enhance plant growth (Awad et al., 2003) and improve soil fertility in terms of physical, chemical and biological properties (Evanylo et al., 2008). Using compost increases the organic material contents of processed and unprocessed soil (Adunga, 2016). Rice husk compost as a kind of compost has been used around the world (FAO, 2002). The changes of structural chemistry of rice husk during composting have not yet received attention. It is expected that composted rice husk may be able to improve soil properties by increasing soil organic C, releasing various essential and beneficial elements and suppressing toxic elements at the same time (Markus et al., 2008). Another method that has been implemented nowadays to achieve safe agriculture is biochar application. Biochar, produced through pyrolysis processing, has drawn a lot of international attention as a useful organic material (Anyanwua et al., 2018). In recent years, application of biochar into agricultural soil, which can improve can improve soil fertility, has been increasingly discussed (Glaser et al., 2003; Lehmann et al., 2006). Biochar has been noted to modify soil properties by affecting biological community composition (Egamberdieva et al., 2016), nutrient cycling (Zee et al., 2017), soil structure (Xu et al., 2014) and soil physical characteristics (Downie et al., 2009). Rice husk biochar is a by-product of rice husk gasification (Carter et al., 2013). There are few research reports on the agronomic impacts of rice husk biochar but as a form of biochar it has benefits when it is applied into agricultural soils (Shackley et al., 2012; Basha et al., 2005). The association between plant and fungi is assumed to play an important role in the land colonization by plants due to the ability of the symbiotic organisms in acquiring unavailable nutrients (Simon et al., 1993; Smith and Smith, 2011). A mycorrhizal system helps plants to increase growth and increase the productivity of host plants (Gupta and Janardhanan, 1991; Linderman and Bethlenfalvy, 1992). Nowadays, one third of human demands for medicine is obtained from plants (Agatonovic-Kustrin et al., 2015). Medicinal plant cultivation has been increased during the last two decades across the world (Salehi et al., 2016). Because of their great importance in modern and traditional medicine, they are also used as raw materials for pharmaceutical, cosmetic and fragrance industries (Karthikeyan et al., 2009). Iranian borage (Echium amoenum Fisch. & C. A Mey) from Boraginaceae is a valuable medicinal plant native to Iran and Syria (Mehrbani et al., 2005). Petals of E. amoenum have been advocated for a variety of effects, such as demulcent, anti-inflammatory and analgesic, especially for common cold, anxiolytic, sedative and other psychiatric symptoms (Morteza-Semnani and Saeedi, 2013). The amount of effective ingredients of medicinal plants depend on yield of these plants and is affected by nutritional status and fertility of soil (Glyn, 2002).
Considering what was described above and also rare investigations about the impact of mycorrhization on studied medicinal plants the objectives of the present study were to determine the effect of rice husk compost, rice husk biochar and mycorrhization on i) growth and nutrient status of the Iranian medicinal plant E. amoenum and, ii) on selected post-harvest calcareous soil.
A completely randomized design experiment was conducted with six treatments and six replications in order to investigate the effect of rice husk compost (RHC), rice husk biochar (RHB) and mycorrhization (MY) on growth and nutrient status of the medical plant E. amoenum and selected post-harvest calcareous soil properties. The experiment was carried out under greenhouse conditions at the College of Agriculture, Shiraz, Iran between January and August 2017. The greenhouse temperature was 25–27°C in the day and 16–17°C at night. The soil was collected from the top layer of research field of College of Agriculture, Shiraz, Iran and the soil texture was classified as a silt loam. The RHB was produced from the rice husk provided from research field of College of Agriculture, Shiraz University, Iran using a muffle furnace under limited oxygen conditions at 600°C for 3 hours. Previous studies indicated that higher temperature resulted in a higher C content (Liang et al., 2016). In addition, increasing the temperature lead to an increase of the ash and fixed C contents, and to a decrease of the content of volatile materials (Tag et al., 2016). To prepare RHC, rice husk was composted under aerobic conditions in the greenhouse for 2 months. Claroideoglomus etunicatum* was used to create mycorrhizal system. The treatments of the experiment comprised of T1: control, T2: MY, T3: RHC, T4: RHB, T5: RHC + MY and T6: RHB + MY. Five kilogram pots were used and filled with treated soil. One percent organic matter was applied for both RHC and RHB. Mycorrhizal infection was done by adding 100 g of C. etunicatum inoculum (800 spores, root colonization of 75%) into the top layer of soil (3–5 cm) before sowing. Two seeds were planted into each pot. Plants were irrigated using distilled water every day and nutrient elements were added to all pots uniformly based on soil testing results. Selected soil and organic matter properties used in the experiment are given in Tables 1 and 2. Plants were grown for 7 months and then harvested along with their roots. Roots were cleaned by dipping them into water 2 to 3 times until the adhering soil particles were removed. To perform plant analysis, the samples of shoots and roots were transferred to the laboratory and prepared after washing and drying in an oven at the temperature of 65°C for 48 hrs. To measure P, K, Fe, Zn, Cu and Mn, the plant samples were ashed using a muffle furnace at 550°C for 2 hrs. Soil samples were air-dried and passed through a 2 mm sieve. Selected soil, plant and organic matter characteristics were determined as follows: soil texture by the method described by Gee and Bauder (1986); soil reaction (pH) in soil saturated paste (Thomas, 1996) and electrical conductivity (EC) in saturated extract (Rhoades, 1996). Calcium carbonate equivalent (CCE) was determined by titration (Nelson, 1982). Total N was determined by the Kjeldahl method (Bremner, 1996). NaHCO3-extactable P was measured by colorimetric method using a spectrophotometer (Olsen, 1954). Amonium acetate extractable K was determined using flame photometer (Page et al., 1982). Organic matter (OM) content was measured by potassium dichromate oxidation method (Nelson and Sommers, 1996). Fe, Zn, Cu and Mn concentrations of soil samples were extracted with diethylene triamine pentaacetic acid (DTPA) method and measured using an atomic absorption spectrophotometer (Shimadzu AA 670 G, Japan) (Lindsay and Norvell, 1978). Soil microbial respiration was determined (mg CO2 day–1) by bottle closed method (Anderson, 1982). Microbial biomass C (MBC) was estimated following the fumigation extraction (FE) method (Vance et al., 1987). EC and pH of compost and biochar were determined in a 1:10 (water) ratio (Gillman and Sumpter, 1986). Fe, Zn, Cu and Mn concentrations of plant samples, RHC and RHB were determined by dry ashing and dissolving the ashed samples in HCl 2N and measuring using atomic absorption (Chapman and Pratt, 1961). Total concentration of N in plant samples, RHC and RHB were measured by Kjeldahl (Bremner, 1996). Total P in plant samples, RHC and RHB were determined by Vanadate-Molybdate yellow method using spectrophotometer (Chapman and Pratt, 1961). Total K was determined by the flame photometer in the extraction of the dry ash method (Chapman and Pratt, 1961). Ash content of RHB and RHC was measured by standard ASTMD-2866 method on weight basis, by which 1.0 g of oven-dried RHB and RHC was briefly heated at 600°C overnight, cooled and weighed again (Rajkovich et al., 2012). Colonization percent of root was done by coloring method (Kormanik and McGraw, 1982). Furthermore, fresh weigh of shoots and roots, height of shrub, length of roots and leaves and number of leaves were determined in each pot. Analysis of data was performed using SPSS 21 software package. The difference between treatments was determined using Duncan`s Multiple Range Test (DMRT), (P ≤ 0.05). Probability levels of 1% and 5% (P ≤ 0.01 or 0.05) were used to test the significance among the treatments. The figures were drawn using Excel 2013 software.
Table 1. Some physicochemical properties of the examined soil (0–30 cm)
Texture | Parameters | |||||||||||||
Sand | Silt | Clay | pH | EC | OM | CCE | N (T) | P (A) | K (A) | Fe (A) | Zn (A) | Cu (A) | Mn (A) | |
Silt Loam | 32.94 | 50.24 | 16.82 | 7.72 | 0.69 | 1.2 | 42.8 | 0.143 | 15.4 | 446.54 | 4.99 | 0.73 | 1.79 | 9.6 |
Unit | ||||||||||||||
– | % | % | % | – | dS m–1 | % | % | % | mg k–1 | mg k–1 | mg k–1 | mg k–1 | mg k–1 | mg k–1 |
T: Total value, A: Available value. |
Table 2. Some properties of the applied organic fertilizers
Parameters | |||||||||||
pH | EC | OM | N (T) | P (T) | K (T) | Fe (T) | Zn (T) | Cu (T) | Mn (T) | Ash | |
RHC | 6.77 | 2.13 | 11.4 | 0.653 | 0.07 | 0.29 | 1976 | 31.6 | 14.4 | 132 | 25 |
RHB | 6.85 | 2.25 | 24.3 | 0.965 | 0.255 | 1.45 | 5636 | 63.65 | 20.15 | 201 | 44 |
Unit | |||||||||||
– | dS m–1 | % | % | % | % | mg k–1 | mg k–1 | mg k–1 | mg k–1 | % | |
RHC: rice husk compost, RHB: rice husk biochar and T: Total value. |
Application of organic amendments significantly affected shoot and root fresh weights (SFW and RFW) (P ≤ 0.05) and increased them by the percentage ranged from 13.17%–28.48% and 13.99%–32.03%, respectively. The highest value of SFW was observed in RHB + MY treatments, which was 191.07 g pot–1 (Table 3), but there was no significant difference to RHC + MY treatments (Table 3). The similar result was obtained for RFW, whereby the maximum RFW was related to the RHB + MY, which was 263.37 g pot–1 (Table 3). In previous studies it is reported that plant growth and yield increased following biochar and compost additions. In most cases, this has been attributed to an optimization of the availability of plant nutrients (Gaskin et al., 2010; Agegnuhe et al., 2016). Fresh weights of shoots and roots were significantly affected using biochar for the medicinal plant Salvia miltiorrhiza Bunge (Amei et al., 2016) reasoned by high concentration of nutrients especially nitrogen in the organic fertilizer (Hosseini Vakili and Ghanbari, 2015). Based on our results, mycorrhization had a positive effect on SFW and RFW, which is probably due to the fact that arbsucular mycorrhizal fungi can increase the concentration of micronutrients and other mineral nutrients with low mobility. Similar to our findings, other researchers also reported that inoculation with mycorrhiza affects the development of the rooting system and causes to increase root biomass (Linderman and Bethlenfalvy, 1992; Li et al., 1991; Heikham et al., 2009). Furthermore, improved plant fresh yield may be reasoned by the important impact of mycorrhization on nutrient availability enhancing growth and biomass (Selvakumar and Thamizhiniyan, 2011). With respect to the root and leaf length (RL and LL), our results show that an addition of organic amendments had a positive and significant effect on RL and LL (P ≤ 0.05) (Fig. 1). Organic fertilizer application caused an increases of RL and LL by 14.28%–28.66% and 17.99%–27.01%, respectively, and the highest values are related to the combination treatments, too. The highest values of RL (15.76 and 16.15 cm were observed in co-application of RHC + MY and RHB + MY, respectively. The highest leaf length (28.38 cm) was measured after the RHB + MY treatment, however, there was no significant difference to the RHC + MY treatment. In addition, Brenann et al. (2014) stated an increase in root and leaf length as a result of biochar application. Biochar application in combination with compost significantly increased leaf length of Lactuca sativa L (Dalila et al., 2017). In fact, biochar and compost particles in the rhizosphere improve water retention and nutrient availability, which results in higher growth (Prendergast-Miller et al., 2014). According to the results of the present experiment, it was concluded that mycorrhization along with organic amendments application significantly affected RL and LL reasoned by several causes that the most likely of which is due to ideal conditions in terms of water and nutrient uptake for plant growth (Iverson and Maier, 2008). Furthermore, the results clarified that organic amendment application significantly (P ≤ 0.05) increased height of shrub and leaf number (HS and LN) by 12.53%–27.07% and 14.37%–32.67%, respectively. The maximum height of plants observed in RHB + MY and RHC + MY treatment was 25.25 and 24.89 cm, respectively and the maximum number of leaves were related to the RHB + MY treatment. However, there was no significant difference to RHC + MY treatments (Fig. 2 and Fig. 3). Our results are in agreement with other research reports (Brenann et al., 2014; Seehausen et al., 2017). Similarly, biochar application increased the number of leaves in medicinal plant S. miltiorrhiza (Amei et al., 2016). The conducted study with L. sativa and Brassica chinensis showed that biochar application increased both plant height and leaf number (Carter et al., 2013). In the present study mycorrhization had a significant effect on HS and LN (Fig. 2 and Fig. 3). In addition, it was observed that mycorrhization with arbuscular mycorrhiza increased plant height in both Zea mays and Lycopersicon esculentum (Taylor et al., 2008). Mycorrhizal infection in association with an important medicinal herb (Artemisia annua) significantly affected plant height, leaf number and other growth attributes (Raei and Weria, 2013). Furthermore, obtained results by Aguin et al. (2004), indicated that mycorrhizal inoculation increased leaf number of Grapevine compared to the control.
Table 3. Means comparison effect of organic amendments on shoot and root fresh weights (g pot–1).
Fresh weight | ||
Shoot | Root | |
Control | 136.38c | 181.89d |
MY | 160.66b | 218.75c |
RHC | 174.74ab | 240.54b |
RHB | 177.85ab | 251.01ab |
RHC + MY | 189.19a | 256.32ab |
RHB + MY | 191.07a | 263.37a |
Different letters above the bars indicate statistically significant differences between treatments according to DMRT. |
Fig. 1. Means comparison effect of organic amendments on root and leaf length (cm). Different letters above the bars indicate statistically significant differences between treatments according to DMRT (P ≤ 0.05). T1: Control, T2: MY, T3: RHC, T4: RHB, T5: RHC + MY and T6: RHB + MY.
Fig. 2. Means comparison effect of organic amendments on height of shrub (cm). Different letters above the bars indicate statistically significant differences between treatments according to DMRT (P ≤ 0.05). T1: Control, T2: MY, T3: RHC, T4: RHB, T5: RHC + MY and T6: RHB + MY.
Fig. 3. Means comparison effect of organic amendments on leaf number. Different letters above the bars indicate statistically significant differences between treatments according to DMRT (P ≤ 0.05). T1: Control, T2: MY, T3: RHC, T4: RHB, T5: RHC + MY and T6: RHB + MY.
The percentage of root colonization was significantly (P ≤ 0.05) influenced in mycorrhizal treatments compared to the non-inoculated treatments. Non-inoculated treatments, control, RHC and RHB had only 9.21%, 15.13% and 15.12% colonization, respectively, from indigenous mycorrhizal fungus. The percentage of root colonization levels in mycorrhizal treatments ranged from 29.24% to 38.32%. The highest percentage was observed in single applications of MY (Fig. 4). In conformity to our findings Thapa et al. (2015), documented a significant variation in percentage of root colonization following mycorrhization, which can be due to some components of the rhizospheric soil that might have favored arbuscular mycorrhizal fungi growth. Similarly, the results of a carried out study indicated more percentage of root colonization in a medicinal plant Valutina A. Juss compared to non-mycorrhizal plants (Samina et al., 2015). The same was reported by Ohsowski et al. (2018). Based on the results of the present study, an effect of organic amendments on soil P status, that was 13.50, 15.48, 16.07 and 16.17 mg kg–1 for treatments of control, MY, RHC + MY and RHB + MY, respectively, it was concluded that lower root colonization in combined treatments (RHC + MY and RHB + MY) may cause an enhancement in presence of P in easily forms in the root zone of plants induced by organic amendment applications (Kowalska et al., 2015). Furthermore, Rayan and Graham suggested that high availability of P limits root colonization in mycorrhizal plants (Rayan and Graham, 2002). The same results were reported by Jimenze-Morenoa et al. (2018) who demonstrated a negative correlation between P level and root colonization in seedlings of Poncirus trifoliate.
Fig. 4. Means comparison effect of organic amendments on of root colonization (%). Different letters above the bars indicate statistically significant differences between treatments according to DMRT (P ≤ 0.05). T1: Control, T2: MY, T3: RHC, T4: RHB, T5: RHC + MY and T6: RHB + MY.
The concentration of N, P, and K in plant shoots and roots was significantly affected by single or combined application of organic amendments (P ≤ 0.05). The highest values were observed in co-application of RHB + MY. Maximum N, P and K concentrations in plant shoots were 2.32%, 0.22% and 2.39%, respectively. The similar result was observed for roots showing the highest concentrations of N, P and K (3.11%, 0.30% and 2.45%, respectively) (Fig. 5, 6 and 7). These findings are in agreement with other studies whose authors reported that bio-fertilizers are able to enhance plant macronutrient availability (Markus et al., 2008). According to the results of a further study it was revealed that organic amendments significantly influenced shoot N and P concentrations (Agegnuhe et al., 2016). Moreover, Zhang et al. (2016) documented that separate or combined application of biochar and compost had a significant influence on plant N, P and K concentrations in comparison with inorganic amendments. This observation was due to the impact of biochar on increasing fertilizer use efficiency (Schulz et al., 2013) and also temporary altering pH for low available nutrients (Amei et al., 2016). Hetikotter and Marschner (2015) revealed that the chemistry of biochar can lead to the retention of K by cation exchange capacity associated with acidic functional groups formed during oxidation process on biochar surfaces, hence, K can become more available for plants. The results of a conducted study showed more availability of N, P and K for plants treated with organic amendments in comparison with plants treated only with mineral fertilizers. This was due to the fact that supplied compost and biochar added nutrients to the soil and also improved their availability to plants by reducing the sorption and leaching potential of nutrients (Agegnuhe et al., 2015). Additionally, Subramanium et al. (2018) stated that improved soil N content following organic matter application may be because of more reduction of organic matter compared to the NH3 loss which usually increases N concentration. They also reported that the concentration of P and K through the plant showed an increase at the period of compost application, which was due to mineralization. In general, improvement of plant nutrition by using of organic amendments could be reasoned by the hypothesis describing that their application helps slowly releasing nutrients to plants and improveing soil ability to provide plant required nutrients (Inal et al., 2015). Mycorrhization has an influence on plant nutrition and our findings are in agreement with others who described that nutrient concentration was enhanced by mycorrhization due to the ability of mycorrhiza to translocate nutrients via extending hyphae and increasing root absorbing surface (Zhang et al., 2016; Kothari et al., 1991). Mycorrhizal fungi absorb non-mobile nutrients from the soil and translocate them to host plants. Beside this, they facilitate inter plant transfer of nutrients and beneficially modify plant water relations (Mondal and Dutta, 2017). Furthermore, Kumar et al. (2015), concluded that higher P content in mycorrhizal plants was attributed to higher influx of P into the plant system via an increase in P efficiency by mycorrhizal plants. They assumed that this may be because of morphological changes in the plant and a provision of an additional or more efficient absorbing surface in the fungal hyphae with subsequent transfer to the host and ability of the mycorrhizal root or hyphae to utilize the source of P not available to non mycorrhizal roots. Besides what mentioned above, the positive role of mycorrhiza in mobilization of macronutrients from the organic substrate via secretion of extracellular enzymes that mobilize mineral nutrients in the soil is also considered as an important effect of mycorrhization on plant macro-nutrients concentration (Hodge and Fitter, 2010; Kumar et al., 2017).
Fig. 5. Means comparison effect of organic amendments on shoot and root N content (%). Different letters above the bars indicate statistically significant differences between treatments according to DMRT (P ≤ 0.05). T1: Control, T2: MY, T3: RHC, T4: RHB, T5: RHC + MY and T6: RHB + MY.
Fig. 6. Means comparison effect of organic amendments on shoot and root P content (%). Different letters above the bars indicate statistically significant differences between treatments according to DMRT (P ≤ 0.05). T1: Control, T2: MY, T3: RHC, T4: RHB, T5: RHC + MY and T6: RHB + MY.
Fig. 7. Means comparison effect of organic amendments on shoot and root K content (%). Different letters above the bars indicate statistically significant differences between treatments according to DMRT (P ≤ 0.05). T1: Control, T2: MY, T3
The results shown in Table 4, demonstrate that single or combined treatments had a positive and significant effect on shoot and root concentration of micro-nutrients and the highest values were observed in the RHB + MY treatment (P ≤ 0.01). The maximum concentration of Fe, Zn, Cu and Mn in shoots were 334.6, 33.02, 11.12 and 39.68 mg kg–1, respectively. The same was observed for roots where the highest concentrations of Fe, Zn, Cu and Mn were 365.1, 48.53, 13.19 and 41.73 mg kg–1, respectively. Improvements in plant performance are consistent with other studies, which indicated that RHC may be able to improve essential element status in plant (Basha et al., 2005). Several research findings have shown that improving plant nutrition using of organic amendments for plant production is a promising approach and their application helps slowly releasing nutrients to plants and improving soil ability to provide plant required nutrients (Inal et al., 2015). Based on the results of a further study, processed poultry manure and its biochar application significantly increased the concentrations of Zn, Cu and Mn in maize plants, which may be attributed to improved availability of nutrients and soil conditions (Inal et al., 2015, Zhang et al., 2016; Adunga, 2016). More plant available nutrients, particularly micro-elements, may be obtained since organic acids are provided as a decomposition product of organic matters (Conversa et al., 2015). With respect to the influence of mycorrhization, our findings are in agreement with those observed by other researchers who reported improved plant nutrition following mycorrhization (Zhang et al., 2016). According to a further experiment result, it was concluded that mycorrhization has a considerable ability to translocate nutrients including Zn, S, Ca, Cu, Mn, Fe and N via extending hyphae and increasing root absorbing surface. (Raei and Weria, 2013). One assessment indicated that increase in Zn and Cu concentration related to mycorrhization is due to higher mycorrhizal colonization on previously treated soils (David et al., 1998). One reason for high nutrient concentration after mycorrhization might be due to the ability of mycorrhiza to colonize roots completely (Neumann et al., 2009), which enhances nutrient content by the extraradical mycelium (Kumar et al., 2017). The same conclusion was reported by Briccoli et al. (2015), who studied the effect of mycorrhization and documented an increase in the percentage of Mn translocation to the leaves from 14% to 22%. This led to an increase of the photosynthetic activity in the mycorrhizal plants since Mn is a constitutive element of photosystem II (Enami et al., 2008). The carried out study by Ortas (2010) showed increased Cu and Zn value in inoculated plants. Mycorrhization create an elaborate web of hyphae that improves absorption of nutrients including Fe, Cu, Mn and Zn (Briccoli et al., 2015).
Table 4. Effect of organic amendments on micronutrients concentration in shoot and root (mg kg–1)
Treatments | Shoot | |||
Fe | Zn | Cu | Mn | |
Control | 316.38 d | 26.19 e | 9.167 d | 34.523 d |
MY | 323.47 c | 28.69 c | 9.52 c | 36.331 c |
RHC | 325.41 bc | 27.81 d | 9.793 b | 37.481 b |
RHB | 328.11 b | 28.33 cd | 9.836 b | 38.69 ab |
RHC + MY | 332.97 ab | 31.26 b | 11.033 a | 39.265 a |
RHB + MY | 334.59 a | 33.02 a | 11.175 a | 39.683 a |
Root | ||||
Control | 321.08 d | 40.458 d | 11.163 d | 37.56 c |
MY | 354.75 c | 44.775 b | 11.522 c | 38.35 bc |
RHC | 357.56 b | 43.36 c | 12.746 b | 39.92 b |
RHB | 358.94 b | 43.517 c | 12.798 b | 40.74 ab |
RHC + MY | 360.13 ab | 46.841 ab | 13.007 ab | 41.688 a |
RHB + MY | 365.1 a | 48.525 ab | 13.193 a | 41.733 a |
Different letters above the bars indicate statistically significant differences between treatments according to DMRT |
Status of macro-nutrients in soil. Data in Table 5 show that, all three organic amendments in a single or combined form significantly affected the concentration of soil macro-nutrients (P ≤ 0.05). The highest values of total concentrations of N, P and K were observed in the RHB + MY treatment, and were 0.15%, 16.17 mg kg–1 and 500 mg kg–1, respectively. Improvements in soil macro-element concentration are consistent with other studies, which indicated that combined application of compost and biochar significantly influenced concentrations of N, P, and K in soil (Schulz et al., 2013). Previous experiments have cleared that amending soil with biochar decreased leaching and improved soil nitrogen availability (Zhu et al., 2015). Similar results were obtained by Demir and Gulser (2015), who described that values of K and P concentration in soil increased by 9.49% and 25.56%, respectively, after application of 3% RHC. It was concluded that the amount of available N, P and K concentrations in soil increased as a result of compost application (Adunga, 2016). Furthermore, there was an increase in K concentration of planted soil with Cocoa following RHC application (Markus et al., 2008). Subramanium et al. (2018) documented that RHC application in soil had a positive impact on available P and K in comparison with control. They assumed that this was due to the fact that organic acids are formed during the decomposition of RHC, which helps to release P and K from a mineral bound insoluble form and also reduces the fixation processes. As a soil conditioner, biochar application can positively influence P and K concentrations in soil (Deluca et al., 2015). There are several mechanisms describing how biochar increases P value in soil. Biochar acts as a P source providing available P for soils, alerts P solubility via the alteration of soil pH, adsorbs specific chelates and improves the process of P mineralization and phosphatase enzyme activities (Madiba et al., 2016; Deluca et al., 2015). The chemistry of biochar demonstrates that it can lead to the retention of K by cation exchange capacity associated with acidic functional groups formed during oxidation process on biochar surfaces, thus retains K (Hetikotter and Marschner, 2015). Our results indicated that application of RHC or RHB in combination with mycorrhizal fungi was more effective in comparison with non-mycorrhizal treatments. Mycorrhiza alliance with other soil microbes improves soil fertility by mobilization of nutrients from the organic substrates (Kumar et al., 2017) and could perhaps perform a major function in mobilization of macro-nutrients from the organic substrate via secretion of extracellular enzymes, which mobilize, mineral nutrients in soil (Hodge and Fitter, 2010).
Table 5. Effect of organic amendments on micro and macro-nutrients concentration of planted soil
Micro-nutrients | ||||
Fe (mg kg–1) | Zn (mg kg–1) | Cu (mg kg–1) | Mn (mg kg–1) | |
Control | 3.688 c | 0.923 d | 1.113 d | 7.258 d |
MY | 4.113 b | 1.655 b | 1.343 c | 8.813 c |
RHC | 4.527 ab | 1.492 c | 1.679 b | 9.128 bc |
RHB | 4.696 ab | 1.513 c | 1.728 b | 9.236 bc |
RHC* MY | 4.897 a | 1.885 a | 1.871 a | 9.972 a |
RHB* MY | 5.035 a | 1.9 a | 1.895 a | 10.054 a |
Macro-nutrients | ||||
N (%) | P (mg kg–1) | K (mg kg–1) | ||
Control | 0.099 e | 13.495 d | 432.97 c | |
MY | 0.128 d | 15.483 b | 484.35 ab | |
RHC | 0.131 cd | 14.676 c | 473.06 b | |
RHB | 0.138 b | 14.752 c | 476.84 b | |
RHC* MY | 0.146 ab | 16.066 a | 499.11 a | |
RHB* MY | 0.148 a | 16.174 a | 500.06 a | |
Different letters above the bars indicate statistically significant differences between treatments according to DMRT |
Concentration of micro-nutrients in soil. Application of organic amendments significantly (P ≤ 0.05) enhanced soil micro-nutrients status (Table 5). Similar to what was observed for macro-nutrients, in combined treatments (RHC + MY and RHB + MY) the highest values for micro-nutrients occurred. The maximum concentrations belonged to RHC + MY and RHB + MY and a higher concentraton of Fe, Zn, Cu and Mn (50.35, 1.90, 1.90 and 10.05 mg kg–1, respectively) was observed in RHB + MY. Our findings were confirmed by other researches who illustrated that organic fertilization influences micro-nutrients contents such as Cu, Fe, Mn and Zn (Rutkowska et al., 2009). Demir and Gulser (2015) showed an increase in the availability of soil micro-nutrients induced by decomposition of organic acids after an application of rice husk compost. An increased concentration of micro-nutrients induced by compost and biochar application was reasoned by a high concentration of these elements in RHC and RHB. The same was found by Adunga (2016), who revealed that increased available micro-nutrient concentrations in soil as a result of compost application was due to a high content of these elements in compost. Agegnuhe et al. (2015) described that a combined application of compost and biochar significantly affected soil micro-nutrients. Micro-element mobility strongly depends upon soil pH. Fertilization with organic N resources, such as biochar and compost results in soil acidification through nitrification of this ion. Hence, by increasing soil acidification an increase in the availability of Cu, Fe, Mn and Zn content is observed in soil (Rutkowska et al., 2014). Regarding the lower pH of RHC and RHB compared to the bulk soil in the present research, it can be concluded that application of RHC and RHB in soil might have altered soil pH temporary and affected the availability of micro-nutrients. The results of further conducted experiments indicated the enhanced soil conditions in terms of Fe, Zn, Cu and Mn following biochar application suggested the importance of biochar’s pH altering capability of increasing the availability of micro-nutrients for plants (Lentz and Ippolito, 2011). Biochar may promote or inhibit microbial activity that influences micro-nutrients availability via changes in microbial populations and activities (Khodadad et al., 2011). Biochar is a promising resource for soil fertility management, which enhances the soil fertility status by a slow release of micro-nutrient (Yang et al., 2016). In conformity to our results, there are numerous reports on the enhancement of micro-nutrients content by mycorrhiza infection (Marschner and Dell, 1994). Mycorrhization positively affects the availability of micro-nutrients, such as Fe, Cu, and Zn. It provides a significant C sink in soil, which can be considered as a critical impact on cycling of microelements within the soil. Mycorrhizal fungi are also accountable for dynamically mobilizing nutrients from the mineral particles and the rock surfaces by means of weathering. This may occur either by mycorrhizal fungi alone or in alliance with other microbes like bacteria or any other fungi (Nikpey and Nikpey, 2016).
Soil respiration and microbial biomass. A positive relationship exists between soil respiration rate and organic amendments application (P ≤ 0.05). The same was true for microbial biomass. The highest values of soil respiration and microbial biomass was observed in combined treatments of RHB + MY and were 14.53 mg CO2-C kg soil–1 h –1 and 26.92 mg C kg soil –1, respectively (Fig. 8). The results are in agreement with other studies describing that an increase of organic materials, such as compost and bichar in soil, a maximum respiration and microbial biomass in soil occurs via improving soil physical, chemical and biological properties and increasing different enzyme and growth hormone secretion by microbes (Nikpey and Nikpey, 2016; Zhang et al., 2014). The conducted study by Urbankova et al. (2014), indicated that biochar application significantly affected soil respiration in both rhizosphere and non-rhizosphere soil. Similarly, the results of a further study suggested that cattle compost changed microbial biomass in soil bacteria by increasing the carbon pool of soil and improving the living conditions for indigenous microbial populations (Zhen et al., 2014). Furthermore, Slapakova et al. (2018), observed significantly higher respiration rates following biochar treatment. As expected, mycorrhization significantly increased soil respiration and microbial biomass which might be reasoned by the role of mycorrhiza in food sources for soil microbes, which increases soil microbial community and also soil respiration (Chenga and Kendra, 2006). On the other hand, Stamou et al. (2017), illustrated that total microbial biomass was affected by mycorrhization because of promoting soil microbial activity causing development of microbial community in soil.
Fig. 8. Means comparison effect of organic amendments on of soil respiration and microbial biomass. T1: Control, T2: MY, T3: RHC, T4: RHB, T5: RHC + MY and T6: RHB + MY.: RHC, T4: RHB, T5: RHC + MY and T6: RHB + MY.
The findings of the present research revealed that all examined treatments significantly affected nutrient element (N, P, K, Fe, Zn, Cu and Mn) concentration, growth/yield indexes of the plants, soil nutrient status (N, P, K, Fe, Zn, Cu and Mn), soil respiration and microbial biomass in soil. An important result of the present study is the considerable effect of enriched RHC and RHB with mycorrhiza on the studied parameters. Combined application of organic amendments was superior to individual application of treatments. A positive role of mycorrhization on nutrient concentration in plants was observed via creating an elaborate web of hyphae, which enhanced nutrient uptake by the plant. Furthermore, mycorrhization affected soil nutrients status due to the role of mycorrhiza in mobilization of nutrients from organic substrate via secretion of extracellular enzymes, which mobilized mineral nutrients in soil. Moreover, mycorrhization significantly increased soil respiration and microbial biomass, which might be reasoned by the role of mycorrhiza in food sources for soil microbes, which increases the soil microbial community and also soil respiration. Our results suggest that RHC, RHB, and MY application in soil led to enhanced soil properties and improved plant growth/yield indices. Further research is needed to determine long-term impacts of these soil conditioners on the soil and plant traits.
Adunga, G., 2016: A review on impact of compost on soil properties, water use and crop productivity. Journal of Agricultural Science and Research 4 (3), 93–104, DOI: 10.14662/ARJASR2016.010.
Agatonovic-Kustrin, S., D. Babazadeh Ortakand, D. W. Morton, A. P. Yusof, 2015: Rapid evaluation and comparison of natural products and antioxidant activity in calendula, feverfew, and German chamomile extracts. Journal of Chromatography A 1385, 103-110. DOI: 10.1016/j.chroma.2015.01.067.
Agegnuhe, G., A.B. Michaeal, M.I. Bird, P.N. Nelson, M. Adrian, P. Bass, 2015: The ameliorating effects of biochar and compost on soil quality and plant growth on a Ferralsol. Soil Research 53 (1), 1–12, DOI: 10.1071/SR14118.
Agegnuhe, G., A.M. Bass, P.N. Nelson, M.I. Bird, 2016: Benefits of biochar, compost and biochar-compost for soil quality, maize yield and greenhouse gas emissions in a tropical agricultural soil. Science of the Total Environment 1 (543), 295–306, DOI: 10.1016/j.scitotenv.2015.11.054.
Aguin, O., J.M. Pedro, Ua, V. Anton, M.J. Sainz, 2004: Effects of mycorrhizal inoculation on root morphology and nursery production of three grapevine rootstocks. American journal of Ecology and viticulture 55 (1), 108–111.
Amei, L., T. Daike, X. Yanci, M. Haibo, 2016: Biochar improved growth of an important medicinal plant (Salvia miltiorrhiza Bunge) and inhibited its cadmium uptake. Journal of Plant Biology and Soil Health 3 (2), 6.
Anderson, J.P.E., 1982: Soil respiration. In Methods of soil analysis. Part 2. Chemical and microbiological properties, ed. A. L. Page,. R. H. MIller and D. R. KEENEY, 831–871. 2nd ed. Madison, WI: American Society of Agronomy, Inc.
Anyanwua, I.N., M.N. Alo, A.M. Onyekwere, J.D. Crossea, O. Nworie, E.B. Chamba., 2018: Influence of biochar aged in acidic soil on ecosystem engineers and two tropical agricultural plants. Ecotoxicology and Environmental Safety 30 (153), 116–126. DOI: 10.1016/j.ecoenv.2018.02.005.
Awad, Y.H., A. Ahmed, O.F. El-Sedfy, 2003: Some chemical properties and NPK availability of sandy soil and yield production as affected by some soil organic amendments. Egyptian Journal of Basic and Applied Sciences 18 (2), 356–365.
Basha. E.A., R. Hashim, H.B. Mahmud, A.S. Muntohar, 2005: Stabilization of clay and residual soils using cement-rice husk ash mixtures. Construction and Building Materials 19 (6), 448–453.
Bremner, J.M., 1996: Nitrogen total. In: Methods of soil analysis, part 3. Chemical Methods, ed. D. L. Sparks et al., 1085–1122. 3rd ed. Madison, WI: American Society of Agronomy, Inc.
Brennan, A., E. M. Jiménez, M. Puschenreiter, J. A. Alburquerque, C. Switzer, 2014: Effects of biochar amendment on root traits and contaminant availability of maize plants in a copper and arsenic impacted soil. Plant and Soil 379 (1-2), 351-360, DOI: 10.1007/s11104-014-2074-0.
Bremner, A., E.M. Jimenze, M. Puschenreiter, J.A. Alburquerque, C. Switzer, 2014: Effects of biochar amendment on root traits and contaminant availability of maize plants in a copper and arsenic impacted soil. Published online Plant Soil, DOI: 10.1007/s11104-014-2074-0.
Briccoli, B.C., E. Santilli, L. Lombardo, 2015: Effect of arbuscular mycorrhizal fungi on growth and on micronutrient and macronutrient uptake and allocation in olive plantlets growing under high total Mn levels. Mycorrhiza 25 (2), 97–108, DOI: 10.1007/s00572-014-0589-0.
Carter, S., S. Shackley, S. Sohi, T.B Suy, S. Haefele, 2013: The impact of biochar application on soil properties and plant growth of pot grown lettuce (Lactuca sativa) and cabbage (Brassica chinensis). Agronomy 3 (2), 404–418, DOI: 10.3390/agronomy3020404.
Cercioglu, M., B. Okur, S. Delibacak, A, R. Ongun, 2014: Changes in physical conditions of a coarse textured soil by addition of organic wastes. Eurasian Journal of Soil Science 3 (1), 7–12, DOI: 10.18393/ejss.47968.
Chapman, H.D, P.F. Pratt, 1961: Methods of analysis for soils, plants and waters. Berkeley, California, USA: The Universityof California’s Division of Agricultural Science.
Chenga, X., B. Kendra, 2006: Effects of mycorrhizal roots and extraradical hyphae on 15N uptake from vineyard cover crop litter and the soil microbial community. Soil Biology and Biochemistry 38 (9), 2665–2675, DOI: 10.1016/j.soilbio.03.023.
Conversa, G., A. Bonasia, C. Lazzizeraand, A. Elia, 2015: Influence of biochar, mycorrhizal inoculation,and fertilizer rate on growth and flowering of Pelargonium (Pelargonium zonal L.) plants. Original Research, DOI: 10.3389/fpls.2015.00429.
Dalila, T., C. Cocozza, S. Baronti, C. Amendola, F.P. Vaccari, G. Lustrato, S.DI Lonardo, F. Fantasma, R. Togentti, G.S. Scippa, 2017: The effects of biochar and its combination with compost on lettuce (Lactuca sativa L.) growth, soil properties, and soil microbial activity and abundance. International Journal of Agronomy, DOI: 10.1155/2017/3158207.
David, D., T.V.D. Jolley, C.W. Robbins, R.E. Terry, 1998: Mycorrhizal colonization and nutrient uptake of dry bean in manure and compost manure treated subsoil and untreated topsoil and subsoil. Journal of Plant Nutrition 21 (9), 1867–1878.
Deluca, T.H., M.J. Gundale, M.D. Mac Kenzie, D.L. Jones., 2015: Biochar effects on soil nutrient transformations. In: Biochar for Environmental Management: Science, Technology and Implementation, J. Lehman, S. Joseph (Eds), 421–454. 2nd ed. Routledge.
Demir, Z., C. Gulser, Effects of rice husk compost application on soil quality parameters in greenhouse conditions., 2015: Eurasian Journal of Soil Science 4 (3), 185–190, DOI: DOI: 10.18393/ejss.2015.3.185-190.
Downie, A., A. Crosky, P. Munroe., 2009: Physical properties of biochar. In: Biochar for Environmental Management: Science and Technology, J. Lehmann, S. Joseph (Eds), 13–32. 1st ed. London. Earthscan.
Egamberdieva, D., S. Wirth, U. Behrendt, E.F. Abd Allah, G. Berg, 2016: Biochar treatment resulted in a combined effect on soybean growth promotion and a shift in plant growth promoting rhizobacteria. Frontiers in Microbiology 25 (7), 209, DOI: 10.3389/fmicb.2016.00209.
El-Kouny, H.M., 2002: Effect of organic fertilizer in different application rates under salinity stress Goudvion on soil and plant. Paper presented at international symposium and optimum resources utilization in salt affected soil. Ecosystems in arid and semi-arid regions. Cairo, Egypt April 8-11.
El-Quesni, F.E.M., M.Z. Sahar, S.S. Hanan, 2010: Effect of microbien and compost on growth and chemical composition of Schefflera arboricola L. under salt stress. Journal of American Science 6 (10), 1073–1080.
Enami, I., A. Okumura, R. Nagao, 2008: Structures and functions of the extrinsic proteins of photosystem II from different species. Photosynthesis Research 98 (1–3), 349–363, DOI: 10.1007/s11120-008-9343-9.
Evanylo, G.K., C. Sherony, J. Spargo, K. Haering, 2008: Soil and water environmental effects of fertilizer-, manure-, and compost-based fertility practices in an organic vegetable cropping system. Agriculture Ecosystems and Environment 127 (1–2), 50–58, DOI: 10.1016/j.agee.2008.02.014.
FAO, 2002: Food and agriculture organization of the United Nations. Statistical database, Available at http://apps.fao.org.
Gaskin, J.W., R.A. Speir, K. Harris, K. Das, R.D. Lee, L.A. Morris, D.S. Fisher, 2010: Effect of peanut hull and pine chip biochar on soil nutrients, corn nutrient status, and yield. Agronomy Journal 102 (2), 623–633.
Gee, G.W., J.W. Bauder, 1986: Particle-size analysis. In Methods of soil analysis: Part 1. Physical and mineralogical methods, S. CAMPBELL et al., (Eds), 383–409. 2nd ed. Madison, WI: American Society of Agronomy, Inc.
Gillman, G.P., E.A. Sumpter, 1986: Modification to the compulsive exchange method for measuring exchange characteristics of soils. Australian Journal Soil Researcher 24 (1), 61–66, DOI: 10.1071/SR9860061.
Glaser, B., J. Lehmann, W. Zech, 2003: Ameliorating physical and chemical properties of highly weathered soils in the tropics with charcoal—a review. Biology and Fertility of Soils 35 (4), 219–230.
Glyn, M.F., 2002: Mineral nutrition, production and artemisin content in Artemisia annual. Acta Horticulturae 426, 721–728, DOI: 10.17660/ActaHortic.1996.426.62.
Gupta, M.L.K.K. Janardhanan, 1991: Mycorrhizal association of glomus aggregatum with palmarosa enhances growth and biomass. Plant Soil 131, 261–263.
Gulser, C., F. Candemir., 2012: Changes in penetration resistance of a clay field with organic waste applications. Eurasian Journal of Soil Science 1 (1), 16–21.
Hetikotter, J., B. Marschner, 2015: Interactive effects of biochar ageing in soils related to feedstock, pyrolysis temperature, and historic charcoal production. Geoderma 245, 56–64, DOI: 10.1016/j.geoderma.2015.01.012.
Heikham, E., K. Rupam, G. Bhoopander, 2009: Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Annals of Botany 104 (7), 1263–1280, DOI: 10.1093/aob/mcp251.
Hodge, A., A.H. Fitter, 2010: Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proceedings of the National Academy of Sciences 107 (31), 13754–13759, DOI: 10.1073/pnas.1005874107.
Hosseini Vakili, S.R., S. Ghanbari, 2015: Comparative examination of the effect of manure and chemical fertilizers on yield and yield components of rosemary (Rosemarinus officinalis L.). International Journal of Agronomy and Agricultural Research 6 (2), 29–37.
Inal, A., A. Gunes, O. Sahin, M. Taskin, E. Kaya, 2015: Impacts of biochar and processed poultry manure, applied to a calcareous soil, on the growth of bean and maize. Soil Use and Management 31 (1), 106–113, DOI: 10.1111/sum.12162.
Iverson, S.L., R.M. Maier, 2008: Effects of compost on colonization of roots of plants grown in metalliferous mine tailings, as examined by fluorescence in situ hybridization. Applied and Environmental Microbiology 75 (3), 842-7, DOI: 10.1128/AEM.01434-08.
Jiménez-Moreno, M.J., M. D. C. Moreno-Márquez, I. Moreno-Alías, H. Rapoport, R. Fernández-Escobar, 2018: Interaction between mycorrhization with Glomus intraradices and phosphorus in nursery olive plants. Scientia Horticulturae 233, 249-255, DOI: 10.1016/j.scienta.2018.01.057.
Karthikeyan, B., M.M. Joe, A.J. Cheruth, 2009: Response of some medicinal plants to vesicular arbuscular mycorrhizal inoculations. Journal of scientific research 1 (1), 381–189, DOI: 10.3329/jsr.v1i2.1675.
Khodadad, C.L.M., A.R. Zimmerman, S.J. Green, S. Uthandi, J.S. Foster, 2011: Taxa – specific changes in soil microbial community composition induced by pyrogenic carbon amendments. Soil Biology and Biochemistry 43 (2), 385–392, DOI: 10.1016/j.soilbio.2010.11.005.
Kormanik, p. p., A.C. McGraw, 1982: Qualification of vesicular arbuscular mycorrhizae in plant root. Method and Principles of mycorrhiza research, N. C. Schenek (Eds), 37–45, American Phytopathological Society.
Kothari, S.K.H. Marschner, V. Romheld, 1991: Contribution of VA mycorrhizal hyphae in acquisition of phosphorus and zinc by maize grown in a calcareous soil. Plant Soil 131 (2), 177–185.
Kowalska, I., A. Konieczny, M. Gastol, W. Sady, E. Hanus-Fajerska, 2015: Effect of mycorrhizal and phosphorous content in nutrient solution on the yield and nutritional status of tomato plants grown on rockwool or coconut coir. Agricultural and Food Science 24 (1), 39–51, DOI: 10.23986/afsci.47204.
Kumar, A., C. Mangla, A. Aggarwal, 2015: Significant effect of mycorrhization on some physiological parameters of Salvia officinalis Linn plant. International Journal of Current Microbiology and Applied Science 4 (5), 90–96.
Kumar, M., R. Prasad, V. Kumar, N. Tuteja, A. Varma, 2017: mobilization of micronutrients by mycorrhizal fungi. In: Mycorrhiza – Function, Diversity, State of the Art: Springer International Publishing, A. Varma, R. Prasad, N. Tuteja, (Eds), 9–26. 4th ed., DOI: 10.1007/978-3-319-53064-2_2.
Lehmann, J., J. Gaunt, M. Rondon, 2006: Bio-char sequestration in terrestrial ecosystems. A review. Mitigation and Adaptation Strategies for Global Change 11(2), 403 427, DOI: 10.1007/s11027-005-9006-5.
Lentz, R.D., J.A. Ippolito, 2011: Biochar and manure affect calcareous soil and corn silage nutrient concentrations and uptake. Journal of Environmental Quality 41 (4), 1033-43, DOI: 10.2134/jeq2011.0126. 41.
Li, X.L., H. Marschner, E. Georg, 1991: Acquisition of phosphorus and copper by VA-mycorrhizal hyphae and root-to-shoot transport in white clover. Plant Soil 136 (1), 49–57.
Liang, C., G. Gasco, S. Fu, A. Mendez, J. Paz-Ferreiro, 2016: Biochar from pruning residues as a soil amendment: effects of pyrolysis temperature and particle size. Soil and Tillage Research 164, 3–10. DOI: 10.1016/j.still.2015.10.002.
Linderman, R.G., G.J. Bethlenfalvy, 1992: Vesicular-arbuscular mycorrhizae and soil microbial interactions. In Mycorrhizae in Sustainable Agriculture, ed. W. I. Madison, 54, 45–70. Published by: American Society of Agronomy DOI: 10.2134/asaspecpub54.c3.
Lindsay, W.L., W.A. Norvell, 1978: Development of a DTPA soil test for zinc, iron, manganese, and copper1. Soil Science Society of America Journal 42 (3), 421–428, DOI: 10.2136/sssaj1978.03615995004200030009x.
Madiba, O.F., Z.M. Solaiman, J.K. Carson, D.V. Murphy, 2016: Biochar increases availability and uptake of phosphorus to wheat under leaching conditions. Biology and Fertility of Soils 52 (4), 439–446.
Markus, A.S., R. Syed Omar, J. Shmsuddin, C.I. Fauziah, 2008: Changes in properties of composting rice husk and their effects on soil and cocoa growth. Communications in Soil Science and Plant Analysis 39 (15–16), 2221–2249, DOIS: 10.1080/00103620802289117.
Marschner, H., B. Dell, 1994: Nutrient uptake in mycorrhizai symbiosis. Plant and Soil 159 (1), 89–102.
Mehrbani, M., N. Ghassemi, E. Sajjadi, A. Ghannadi, M. Shams-Ardakani, 2005: Main phenolic compounds of petals of Echium amoenum Fisch. & C.A. Mey., a famous medicinal plant of Iran. DARU 13 (2), 65–69.
Mondal, T., S. Dutta, 2017: Study of arbuscular mycorrhizal association in some medicinal herbs of Acanthaceae family from Datjeeling district, west Bengal, India. International Journal of Pharma and Bio Sciences 8 (1), 137 – 142, DOI: 10.22376/ijpbs.2017.8.1.b137-142.
Morteza-Semnani, K., M. Saeedi, 2013: Essential oil composition of Echium amoenum Fisch and C.A. Mey. Journal of Essential Oil Bearing Plants 8 (1), 61–64, DOI: 10.1080/0972060X.2005.10643422.
Nelson, D.W., L.E. Sommers., 1996: Total carbon, organic carbon, and organic matter. Methods of soil analysis, part 3. Chemical Methods, D. L. Sparks et al., (Ed), 961–1010. 3rd ed. Madison, WI: American Society of Agronomy, Inc.
Nelson, R.E., 1982: Carbonate and gypsum. Methods of soil analysis. Part 2. Chemical and microbiological properties,. A. L. Page, R. H. Miller, D. R. Keeney (Eds), 181–197. 2nd ed. Madison, WI: American Society of Agronomy, Inc.
Neumann, E., E. George, J. Emir, 2009: The effect of arbuscular mycorrhizal root colonization on growth and nutrient uptake of two different cowpea (Vigna unguiculata L. Walp.) genotypes exposed to drought stress. Journal of the Science of Food and Agriculture 21 (2), 01–17, DOI: 10.9755/ejfa.v21i2.5160.
Nikpey, M.A., M. Nikpey, 2016: Evaluating the impact of compost and bio compost enriched with chemical fertilizer on soil biological properties. Advances in Agricultural Science 4 (1), 01–07.
Ohsowski, B.M., K. Dunfield, J.N. Klironomus, M.M. Hart, 2018: Plant response to biochar, compost, and mycorrhizal fungal amendments in post-mine sandpits. Journal of Society for Ecological Restoration 26 (1). 63–72, DOI: 10.1111/rec.12528.
Olsen, S.R., 1954: Estimation of available phosphorus in soils by extraction with sodium bicarbonate. Circ No 939, united states department of agriculture, Washington, DC.
Ortas, I., 2010: Effect of mycorrhiza application on plant growth and nutrient uptake in cucumber production under field conditions. Spanish Journal of Agricultural Research 8 (S1), S116-S122, DOI: 10.5424/sjar/201008S1-1230.
Page, A.L., R.H. Miller, D.R. Keeney, 1982: Methods of soil analysis. Part 2. Chemical and microbiological properties. American Society of Agronomy. 2nd ed. Madison, WI:, Inc.
Prendergast-Miller, M.T., M. Duvall, S.P. Sohi, 2014: Biochar–root interactions are mediated by biochar nutrient content and impacts on soil nutrient availability. European Journal of Soil Science 65, 173–185, DOI: 10.1111/ejss.12079.
Raei, Y., W. Weria, 2013: Arbuscular mycorrhizal fungi associated with some aromatic and medicinal plants. Bulletin of Environment, Pharmacology and Life Sciences 2 (11), 129–138.
Rajkovich, S., A. Enders, K. Hanley, C. Hyland, A.R. Zimmerman, J. Lehmann, 2012: Corn growth and nitrogen nutrition after additions of biochars with varying properties to a temperate soil. Biology and Fertility of Soils, 48, 271–284, DOI: 10.1007/s00374-011-0624-7.
Rayan, M.H., J.H. Graham, 2002: Is there a role for arbuscular mycorrhizal fungi in production agriculture? Plant and soil 244 (1–2), 263–271.
Rhoades, J.D., 1996: Salinity: Electrical conductivity and total dissolved solids. Methods of soil analysis, part 3. Chemical Methods, D. L. Sparks et al., (Ed), 417–435. 3rd ed. Madison, WI: American Society of Agronomy, Inc.
Rutkowska, B., W. Szulc, J. Labetowicz., 2009: Influence of soil fertilization on concentration of microelements in soil solution of sandy soil. Journal of Elementology 14 (2), 349–355.
Rutkowska, B., W. Szulc, T. Sosulski, W. Stepien, 2014: Soil micronutrient availability to crops affected by long-term inorganic and organic fertilizer applications. Plant, Soil and Environment 60 (5), 198–203.
Salehi, A., H. Tasdighi, M. Gholamhosseini, 2016: Evaluation of proline, chlorophyll, soluble sugar content and uptake of nutrients in the German chamomile (Matricaria chamomilla L.) under drought stress and organic fertilizer treatments. Asian Pacific Journal of Tropical Biomedicine 6 (10), 886–891, DOI: 10.1016/j.apjtb.2016.08.009.
Samina, A., M.M. Abu Sayeed, I. Faridul, M. Romel, C.J. Jagadish, A. Sadiqul, K. Rezaul, T. Hridika, R. Saidur, 2015: Prevalence of arbuscular mycorrhiza fungi (AMF) colonization in medicinal plant root and response of prevalence with some selected medicinal plants rhizosphere soil properties in BCSIR forest, Chittagong, Bangladesh. Milton Halder1. Journal of Pure and Applied Microbiology 9 (1), 131–140.
Schulz, H., G. Dunst, B. Glaser, 2013: Positive effects of composted biochar on plant growth and soil fertility. Agronomy for Sustainable Development 33 (4), 817–827.
Seehausen, M.L., V.G. Nigel, S. Dranga, V. Hudson, N. Liu, J. Michener, E. Thurston, C. Williams, S.M. Smith, S.C. Thomas, 2017: Is There a Positive Synergistic Effect of Biochar and Compost Soil Amendments on Plant Growth and Physiological Performance? Agronomy 7 (1), 13, DOI: 10.3390/agronomy7010013.
Selvakumar, G., P. Thamizhiniyan, 2011: The effect of the arbuscular mycorrhizal (AM) fungus glomus intraradices on the growth and yield of Chilli (Capsicum annuum L.) under salinity stress. World Applied Sciences Journal 14 (8), 1209–1214.
Shackley, S., S. Carter, T, Knowels, E. Middelink, S. Haefele, S. Sohi, A. Cross, S. Haszeldin, 2012: Sustainable gasification-biochar systems? A case study of rice-husk gasification in Cambodia Part I: Context, chemical properties, environmental and health and safety issues. Energy Policy 42, 49–58, DOI: 10.1016/j.enpol.2011.11.026.
Simon, L., J. Bousquet, R.C. Levesque, M. Lalonde, 1993: Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363, 67–69.
Slapakova, B., J. Jerabkova, K. Vorisek, V. Tejnecky, O. Drabek, 2018: The biochar effect on soil respiration and nitrification. Plant, Soil and Environment 64 (3), 114–119, DOI: 0.17221/13/2018-PSE.
Smith, S.E., F.A. Smith, 2011: Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annual Review of Plant Biology 62, 227–250, DOI: 10.1146/annurev-arplant-042110-103846.
Stamou, G.P., S. Konstadinou, N. Monokrousos, A. Mastrogianni, M. Orfanoudakis, C. Hassiotis, U. Menkissoglu-Spiroudi, D. Vokou, E.M. Papatheodorou., 2017: The effects of arbuscular mycorrhizal fungi and essential oil on soil microbial community and N-related enzymes during the fungal early colonization phase. AIMS Microbiology 3 (4), 938-959, DOI: 10.3934/microbiol.2017.4.938.
Subramanium, T., G. Pandurangan, K. Ramasamy, A. Rangasamy, P. Diby, 2018: Exploration of rice husk compost as an alternate organic manure to enhance the productivity of blackgram in typic haplustalf and typic rhodustalf. International Journal of Environmental Research and public health 15 (2), 358, DOI: 10.3390/ijerph15020358.
Tag, A.T., G. Duman, S. Ucar, J. Yanik, 2016: Effect of feedstock type and pyrolysis temperature on potentialapplications of biochar. Journal of Analytical and Applied Pyrolysis 120, 200–206, DOI: 10.1016/j.jaap.2016.05.006.
Taylor, J.H., A. Waltenbaugh, M. Shields, 2008: Impact of vesicular arbuscular mycorrhiza on root anatomy in Zea mays and Lycopersicon esculentum. African Journal of Agricultural Research 3 (1),001–006.
Thapa, T., D.U. Kumar, B. Chakraborty, 2015: Association and root colonization of some medicinal plants with arbuscular mycorrhizal Fungi. Journal of Medicinal Plants Studies 3 (2), 25–35.
Thomas, G.W., 1996: Soil pH and soil acidity. Methods of soil analysis, part 3. Chemical Methods,. D. L. Sparks et al., (Ed), 475–490. 3rd ed. Madison, WI: American Society of Agronomy, Inc.
Urbankova, O., J. Elbl, J. Zahora, 2014: The effects of biochar on soil respiration in rhizosphere and non-rhizosphere soil. Mendel Net 326–329.
Vance, E.D., P.C. Brookes, D.S. Jenkinson, 1987: An extraction method for measuring soil microbial biomass C. Soil biology and Biochemistry 19 (6), 703–707, DOI: 10.1016/0038-0717(87)90052-6.
Xu, H.J., X.H. Wang, H. Li, H.Y, Yao, J.Q Su, Y.G Zhu, 2014: Biochar impacts soil microbial community composition and nitrogen cycling in an acidic soil planted with rape. Environmental Science and Technology 48 (16), 9391–9399, DOI: 10.1021/es5021058.
Yadav, R.L., G.L. Keshwa, S.S Yadav., 2003: Effect of integrated use of FYM and sulphure on growth and yield of Isabgol (Plantago ovata). Journal of Medicinal and Aromatic Plant Sciences 25, 668–671.
Yang, D., L. Yunguo, L. Shaobo, L. Zhongwu, T. Xiaofei, H. Xixian, Z. Guangming, Z. Lu, Z. Bohong, 2016: Biochar to improve soil fertility. A review. Agronomy for Sustainable Development 36 (36), 18, DOI: 10.1007/s13593-016-0372-zm.
Zee, T.E., N.O. Nelson, G. Newdigger, 2017: Biochar and nitrogen effects on winter wheat growth. Kansas Agricultural Experiment Station Research Reports 3 (3), DOI: 0.4148/2378-5977.1397.
Zhang, Q.Z., A.D. Feike, X. Liu, Y. Wang, J. Huang, N. Lu, 2014: Effects of biochar on soil microbial biomass after four years of consecutive application in the north China plain. Public Library of Science 9 (7), e102062.
Zhang, D., G. Pan, G. Wu, G.W. Kibue, L. Li, X. Zhang, J. Zheng, K. Cheng, S. Joseph, 2016: Biochar helps enhance maize productivity and reduce greenhouse gas emissions under balanced fertilization in a rainfed low fertility inceptisol. Chemosphere 142, 106–113, DOI: 10.1016/j.chemosphere.2015.04.088.
Zhen, Z., H. Liu, N. Wang, L. Guo, J. Meng, N. Ding, G. Wu, G. Jiang, 2014: Effects of manure compost application on soil microbial community diversity and soil microenvironments in a temperate cropland in china. Public Library of Science 9 (10), e108555, DOI: 10.1371/journal.pone.0108555.
Zhu, Q., X. Peng, T. Huang, 2015: Contrasted effects of biochar on maize growth and N use efficiency depending on soil conditions. International Agrophysics 29 (2), 257–266, DOI: 10.1515/intag-2015-0023.
Footnotes:
Classification: Fungi, Mucoromyceta, Glomeromycota, Glomeromycotina, Glomeromycetes, Glomerales, Claroideoglomeraceae, Claroideoglomus |