- Email: [email protected]
Biomass production of a young plantation of Moringa stenopetala (Baker f.) Cufod. and Moringa oleifera Lam. in southern Ethiopia
ARTICLE IN PRESS
JID: SAJB
[m5G;January 28, 2020;10:32]
South African Journal of Botany 000 (2020) 18
Contents lists available at ScienceDirect
South African Journal of Botany journal homepage: www.elsevier.com/locate/sajb
Biomass production of a young plantation of Moringa stenopetala (Baker f.) Cufod. and Moringa oleifera Lam. in southern Ethiopia meca, Moana Ungrova a, Shiferaw Alema, Jaromír Nova kb, Hana Habrova a,* Petr Ne a b
Faculty of Forestry and Wood Technology, Mendel University in Brno, Zemedelska 3, 61300 Brno, Czech Republic Holistic Solutions s.r.o., Veveri 467/25, 60200 Brno, Czech Republic
A R T I C L E
I N F O
Article History: Received 30 March 2019 Revised 5 December 2019 Accepted 7 January 2020 Available online xxx Edited by NE Madala Keywords: Arba Minch Ethiopia Leaf biomass production Moringa oleifera Moringa stenopetala nutritional values
A B S T R A C T
In May 2017, a plantation of Moringa stenopetala and Moringa oleifera was established in southern Ethiopia using a spacing of 1 £ 1.5 m. The plantation was not artificially irrigated, and no fertilizers or pesticides have been applied. To assess the suitability of cultivation on the plantation, the average leaf biomass production and, secondarily, to evaluate the nutritional potential of both species, three harvests were carried out in November 2017, March 2018 and in November 2018. The leaf biomass was harvested in each trial from the same thirty trees. A principal objective of the study was to describe the suitability of Moringa stenopetala for cultivation in an intensive plantation and to compare these results with the results of cultivation of Moringa oleifera. The results show that in young plantations of M. stenopetala, dry matter biomass production could reach up to 2,824 kg/ha/year, while for M. oleifera, it could reach 6,060 kg/ha/year. One harvest of a M. oleifera plantation’s (705 trees) total estimated leaf biomass would yield a one day proper calorie intake for 340 adult humans (irrespective of gender), while M. stenopetala would supply only 123 people, i.e., 1 ha of M. oleifera plantation would supply a one day proper calorie intake to 3,213 adults, while M. stenopetala would supply a one day proper calorie intake to 1,159 adults. Based on the evaluated data, M. oleifera is considered to be more suitable for (growing on) plantations in southern Ethiopia due to its pest resistance and high leaf biomass production. © 2020 SAAB. Published by Elsevier B.V. All rights reserved.
1. Introduction Moringa oleifera (further abbreviated as MO) and Moringa stenopetala (MS), which belong to the monospecific family Moringaceae, are two of the 13 identified species of the family (Velazquez-Zavala et al., 2016; Edward et al., 2014; Gebregiorgis et al., 2012) and two in a group of four edible species (Olson 2017). Both species are the most common species in the family, and both have many characteristics in common (Schneemann, 2011). M. oleifera is a multi-purpose tree originally from India (Seifu, 2014), while M. stenopetala is native to eastern Africa, where it is grown in southern Ethiopia, northern Kenya and eastern Somalia (Bedane et al., 2013). Moringa oleifera, which is more well-known, grows in tropical and sub-tropical climates; it is drought-resistant and can be grown in a wide variety of poor soils, including barren ground, with soil pH between 4.5 and 9.0 (Ashfaq et al., 2012; Olson, 2002). It has tremendous potential uses, such as food for human beings, feed for livestock, medicine, dye, perfume, skin lotion, lubricant and water purification (Nouman et al., 2013; Melesse et al., 2011). The leaves are * Corresponding author. E-mail address: [email protected] (H. Habrova).
nutritionally rich and serve as an excellent source of concentrated proteins, vitamins and minerals (Isah et al., 2014; Amaglo et al., 2010). MO is attributed with properties for the treatment of certain ailments such as asthma, epilepsy, eye and skin diseases, fever and haemorrhoids (Sanjay and Dwivedi, 2015). The seeds are used to treat groundwater and water with suspended solids (Lijesh and Malhotra, 2016), and they can also serve as a source of oil for biodiesel production (Mofijur et al., 2014). MO is now widely cultivated and is found in most tropical countries (Africa, Asia and America) (Boukandoul et al., 2018; Olson et al., 2016; Sanjay and Dwivedi, 2015; Edward et al., 2014), and it has also received research and development attention worldwide (Seifu, 2014). Moringa stenopetala is still grown only in its area of origin, where farmers grow it in agroforestry systems or as individual trees. It is used for its nutritional and medicinal value (Habtemariam, 2016, Yisehak et al., 2011), especially for high iron content, their other uses seem similar to MO nevertheless, only a few scientific researches have been proved about its properties. In Ethiopia, MS is native in arid, semi-arid and semi-humid areas at altitudes ranging from 1000 to 1800 m a.s.l., and because of its palatable leaves, it is one of the most frequently cultivated indigenous species (Bedane et al., 2013). It is widely distributed in the Konso, Wolayta, D’irashe, Gamo Gofa,
https://doi.org/10.1016/j.sajb.2020.01.018 0254-6299/© 2020 SAAB. Published by Elsevier B.V. All rights reserved.
mec et al., Biomass production of a young plantation of Moringa stenopetala (Baker f.) Cufod. and Moringa Please cite this article as: P. Ne oleifera Lam. in southern Ethiopia, South African Journal of Botany (2020), https://doi.org/10.1016/j.sajb.2020.01.018
JID: SAJB
ARTICLE IN PRESS
[m5G;January 28, 2020;10:32]
P. Nemec et al. / South African Journal of Botany 00 (2020) 18
2
Sidama, Bale and Borana areas (Aynalem, 2008; Gebregiorgis et al., 2012). It is an especially important component of the local diet in the Gamo Gofa and Konso zones. Although MO is widely cultivated and has received research and development attention worldwide (Seifu, 2014), it has been introduced to Ethiopia very recently, which shows that much more research has to be conducted to evaluate the species in Ethiopian climatic conditions. There is also scant information on the native MS species, which has recently gained attention due to its multiple uses; little is known about its nutritional value and biomass production when it is managed as an intensive plantation. Therefore, the objectives of this study are 1) to assess the biomass production of M. stenopetala relative to M. oleifera plantation in Arba Minch Zuria Woreda, SNNPR, Ethiopia and 2) to evaluate the nutritional values of MS relative to MO. At the beginning of the study, it was hypothesized that 1) MS can produce higher biomass relative to MO in a monoculture plantation and 2) the nutritional value of MS is not significantly different from MO. 2. Materials and methods 2.1. Study area The study was conducted in the Permaculture Training and Demonstration Centre, which was established by Mendel University within the project “Implementation of holistic management and Climate Smart Agriculture in the Baso River catchment, Arba Minch Zuria Woreda, SNNPR, Ethiopia”. The centre (coordinates 6°060 52.100 N 37°360 34.300 E) lies just next to Chano Mile village, which lies within the Arba Minch Zuria Woreda in the Gamo Gofa zone. Arba Minch lies on the southwestern shores of Lake Abaya and Lake Chamo, which are located at the base of the western side of the Great Rift Valley at an elevation of 1285 m a.s.l. Arba Minch received its name from the 40 nearby springs. According to the € ppen climate classification (Peel et al., 2007), the climate type Ko in Arba Minch corresponds to category Aw: a tropical wet-dry climate. High temperatures throughout the year are typical in areas with distinct wet and dry seasons (extended dry season during winter), with most of the precipitation occurring in the high-sun (“summer”) season (Climate-data.org, 2018). According to the climate diagram, the average annual precipitation in Arba Minch is approximately 820 mm and the average temperature is 21.5 °C. The study area has alluvial sediments, which are, in addition to being good quality soil, typical of low river flows, lake depressions and valleys of former or current lakes. These sediments consist of gravel, sand and silt. Due to the study area’s proximity to Lake Abaya, groundwater is available and makes this area suitable for agroforestry purposes. The study area is situated in the kolla zone at an altitude of 1191 m a.s.l. As mentioned, the highest precipitation occurs from AprilJune and from OctoberDecember.
2.3. Data collection For the purpose of this study, MO and MS leaves were harvested three times through manual removal of all leaves from each tree. The first harvest occurred on 19 November 2017, the second harvest occurred on 20 March 2018 and the third harvest occurred on 15 November 2018. During each harvest, fifteen samples from each species (thirty samples per harvest) were collected in row 21, in the case of MS, and in rows 3536, in the case of MO; trees were taken from two rows because four samples in the 35th row were not suitable for the statistical data because they had been pruned. Each sample was given a number and was subsequently weighed on a laboratory scale. Fresh leaf biomass weight data were recorded. 1000 g of fresh leaves of each species from both first harvests (four kilograms in total) was separately dried at 65 °C for 48 h in a drying oven at Arba Minch University. After that, the values of dry leaf biomass (DM) obtained from each individual tree were calculated from the weight of one kilogram of dried leaves. Subsequently, all measured data were statistically analysed in Microsoft Excel, and the results were displayed graphically. Samples of 500 g of both MO crushed leaf powder and MS crushed leaf powder were sent to the laboratory ALS Czech Republic, s.r.o., in Prague, Czech Republic, to conduct amino acid and nutritional analysis. 2.4. Data analysis Since the samples were collected from the same trees three times in two different seasons, the data were processed using a repeated measures ANOVA with two factors: (1) month of the harvest and (2) species. The significance level p was set at 0.05. Due to increasing variability, logarithmically transformed data were used for the ANOVA. Statistical data were analysed using the open-source statistical program JASP. 3. Results 3.1. Leaf biomass production The biomass gain in different seasons of the fresh leaves that were dried using the drying oven in this study is presented in Table 1. The dry leaf biomass production of the individual sampled trees at different seasons of the study period for MS and MO are presented in Figs. 3 and 4, respectively. The mean dry leaf biomass production of M. stenopetala in November 2017, March 2018 and November 2018
2.2. Moringa plantation establishment The plantation (Fig 1) was established on 1 May 2017. Seeds of local origin were used, and grown plants were planted in an area of 30 £ 70.5 m with 1.5 m spaces within the row and 1 m spaces between rows, resulting in 705 of each tree species at the plantation (15 £ 47 rows for each species, 1410 trees in total). The plantation was not artificially irrigated, and no fertilizers or pesticides have been applied thus far. The first improvement cutting took place at the beginning of July: each plant was cut off at breast height (1.3 metres above ground). The very first harvest (with no data recorded) took place in August 2017.
Fig. 1. Established plantation of Moringa oleifera (left) and Moringa stenopetala (right).
mec et al., Biomass production of a young plantation of Moringa stenopetala (Baker f.) Cufod. and Moringa Please cite this article as: P. Ne oleifera Lam. in southern Ethiopia, South African Journal of Botany (2020), https://doi.org/10.1016/j.sajb.2020.01.018
ARTICLE IN PRESS
JID: SAJB
[m5G;January 28, 2020;10:32]
P. Nemec et al. / South African Journal of Botany 00 (2020) 18
The total leaf biomass (kg) production of MO at different seasons of harvest is presented in Fig. 7. The results indicated that the total dry leaf biomass production of MO harvested in November 2018 was higher relative to the total dry leaf biomass production in November 2017 and March 2018 (Fig. 5). However, the one-way ANOVA result revealed no significant difference (p = 0.483) in the dry leaf biomass of MO harvested at different periods (Fig. 7). Overall, the study results indicated that the MO dry leaf biomass production was higher than the dry leaf biomass production of MS. The statistical test results also revealed a significant difference in the mean dry leaf biomass production of MO and MS (Fig. 8, P < 0.001). Total leaf biomass production from the whole plantation was also estimated. The average dry biomass yield from each harvest was multiplied by 47 (number of rows by 15 trees). The leaf biomass production from the M. oleifera part of the plantation (15 £ 70.5 m) was approximately 200 kg in November 2017, 217 kg in March 2018 and 224 kg in November 2018. The same was done with M. stenopetala, and in November 2017, March 2018 and November 2018, the results were 117 kg, 102 kg and 80 kg, respectively. Extrapolation of these results could indicate that the average yearly production of MS dry leaf biomass could be approximately 2824 kg/ha, and for MO, it could be approximately 6060 kg/ha.
Table 1 Ratio of fresh leaf biomass to dry matter biomass. Weight loss caused by drying
M. oleifera M. stenopetala
Nov 2017
Mar 2018
270.4 g/kg 264.2 g/kg
266.1 g/kg 269.2 g/kg
3
were 165.4 (16.8) g/tree, 144.7 (13.9) g/tree and 113.4 (13.9) g/tree, respectively. In contrast, the mean dry leaf biomass production of M. oleifera in the periods of November 2017, March 2018 and November 2018 were 283.5 (48.0) gram/tree, 323.8 (52.5) gram/tree, and 325.9 (70.8) gram/ tree, respectively. As mentioned, leaves were harvested from 30 trees (15 from each species) three times. Comparing the weights of M. oleifera trees, they show a significant increase between the three harvests, while the difference in the obtained leaf biomass from all harvests of M. stenopetala trees decreased, as shown in the following figures (Figs. 2-4). The results of the total harvest of dry leaf biomass (kg) of the two studied species in different seasons are presented in Fig. 5. The results indicated that the total dry leaf biomass of MS harvested in November 2018 was lower relative to the total dry leaf biomass harvested in November 2017 and March 2018 (Fig. 5). The one-way ANOVA result also indicated a significant difference (p = 0.036) in the mean dry leaf biomass (g) production of MS harvested at different periods of the study (Fig. 6). These significant differences were between the dry leaf biomass production for the seasons of November 2017 and November 2018 (Fig. 6).
3.2. Nutritional potential The results of the nutritional analysis of Moringa are presented in Tables 2 and 3. Moringa in general is an excellent source of nutrition, especially because of its high iron (Fe) and calcium (Ca) content. This
M. stenopetala
M. oleifera
20.00 15.00 10.00 5.00 0.00
Nov 17
Mar 18
Nov 18
Fig. 2. Total harvest of 15 trees in different seasons (kg of fresh leaves).
350.00 Nov 17
Mar 18
Nov 18
300.00 250.00 200.00 150.00 100.00 50.00 0.00 1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
Fig. 3. Dry leaf biomass (g) production from 15 individual sampled trees of M. stenopetala for the study in different seasons of the year.
mec et al., Biomass production of a young plantation of Moringa stenopetala (Baker f.) Cufod. and Moringa Please cite this article as: P. Ne oleifera Lam. in southern Ethiopia, South African Journal of Botany (2020), https://doi.org/10.1016/j.sajb.2020.01.018
ARTICLE IN PRESS
JID: SAJB
[m5G;January 28, 2020;10:32]
P. Nemec et al. / South African Journal of Botany 00 (2020) 18
4
1,200.00 Nov 17
Mar 18
Nov 18
1,000.00 800.00 600.00 400.00 200.00 0.00 1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
Fig. 4. Dry leaf biomass (g) production from 15 individual sampled trees of M. oleifera for the study in different seasons of the year.
300
Leaf biomass (Grams)
250 a ab
200
b 150 100 50 0 November 2017
March 2018
November 2018
Period Fig. 5. One-way ANOVA result of the dry leaf biomass of M. stenopetala at different periods of leaf harvest at a 0.05% level of significance (p = 0.036). Means with the same letters are not significantly different.
fact has been demonstrated by laboratory analysis, which has also shown content of other components. The analysis was principally performed to obtain the energy amount of the plantation of both species and their comparison. Whole plantation of both species produced 12,166,430 kJ per year (3195,154 kJ MS and 8971,275 kJ MO). 4. Discussion 4.1. Leaf biomass production Although Moringa stenopetala is native in the study area, the results have shown significantly better growth of Moringa oleifera. Its leaf biomass production reached amounts more than 1/3 higher than MS during the first harvest, and its production has been increasing while native species production has decreased. One reason might be lower water requirements and thus higher resistance against
drought; the March harvest was relatively poor for the MS trees because there were dry months before. However, the third harvest was carried out again during November 2018 after the rainy season, and the decrease of produced biomass persisted. The reason could be in lower resistance to pests and diseases such as powdery mildew and Noorda blitealis which have been developed after the rains. This has been observed by phytopathology experts; nevertheless, this analysis was not included in this study and was described in an independent scientific paper (Bartikova et al., submitted). Another influence on total biomass production could be a borgent and Camire , 1985; Pontailler et al., 1997). The der effect (Pre trees growing at the edge of the plantation have significantly higher leaf biomass production; when these trees are excluded from the data, the results for MS remain the same, i.e., the total amount of leaf biomass decreases with tree age (7.6 kg, 6.5 kg and 5.2 kg of fresh leaves from 13 trees). However, for MO, the total leaf biomass slowly decreased, too (12.6 kg, 12.2 kg and
mec et al., Biomass production of a young plantation of Moringa stenopetala (Baker f.) Cufod. and Moringa Please cite this article as: P. Ne oleifera Lam. in southern Ethiopia, South African Journal of Botany (2020), https://doi.org/10.1016/j.sajb.2020.01.018
ARTICLE IN PRESS
JID: SAJB
[m5G;January 28, 2020;10:32]
P. Nemec et al. / South African Journal of Botany 00 (2020) 18
5
Leaf biomass (Grams)
800
600 a
a
a
400
200
0 November 2017 March 2018
November 2018
Period Fig. 6. One-way ANOVA result of the dry leaf biomass of M. oleifera at different periods of leaf harvest at the 0.05% level of significance (p = 0.483). Means with the same letters are not significantly different.
600
Leaf biomass (Grams)
500 a 400 300 b
200 100 0 M. oleifera
M. stenopetala
Fig. 7. Statistical t-test result on the dry leaf biomass of M. oleifera vs M. stenopetala at the 0.05% level of significance (P = 0.001). Means with the same letters are not significantly different.
11.6 kg of fresh leaves). The total MO biomass increase, then, was caused only by edge trees, but we could not exclude them because they are valid parts of the plantation, and all the edge trees were visibly large. As a result, wider tree spacing (3 £ 3 m) to increase biomass production could be taken into account; however, the spacing in plantations is usually even denser than 1 £ 1.5 m (Patricio et al., 2017; Basra et al., 2015; Nouman et al., 2013; Sanchez et al., 2006). At the current spacing of 1 £ 1.5 m, there are 705 MO and 705 MS trees. At a spacing of 3 £ 3 m, the number would decrease to 117 trees. Assuming that those trees would have more space for growth and provide equally high leaf biomass production as the edge trees currently do, the average estimated production has been calculated. The charts show that the leaf biomass production on the plantation would have
a surprisingly significant decrease to only approximately 1/4 of current production. Thus, wider spacing probably would not provide higher leaf biomass yield; however, due to better air circulation, it might help to reduce pests and diseases. This corresponds with findings of Mabapa et al. (2017) who reported that planting density had a significant influence on biomass production, where higher planting density resulted in greater biomass yield harvests. Their results show that the DM of MO is between 611 and 2867 kg/ha, while our results show 18902137 kg/ha of DM. During their study, no fertilizers were used. The first six weeks of better tree establishment were supported by irrigation, which was applied twice per week for four hours. Patricio et al. (2017) also performed an experiment to observe biomass production on plantations with different spacing (1040 thousand plants per ha) and different harvest frequencies (4, 6 and 8
mec et al., Biomass production of a young plantation of Moringa stenopetala (Baker f.) Cufod. and Moringa Please cite this article as: P. Ne oleifera Lam. in southern Ethiopia, South African Journal of Botany (2020), https://doi.org/10.1016/j.sajb.2020.01.018
ARTICLE IN PRESS
JID: SAJB
[m5G;January 28, 2020;10:32]
P. Nemec et al. / South African Journal of Botany 00 (2020) 18
6
The average amount of energy contained in the March harvest [kcal/ha] 8,000,000.00 7,000,000.00 6,000,000.00 5,000,000.00 4,000,000.00 3,000,000.00 2,000,000.00 1,000,000.00 0.00 M. oleifera
M. stenopetala
Fig. 8. The average amount of energy from the March harvest (kcal/ha).
Table 2 Moringa oleifera and Moringa stenopetala nutritional values.
Protein Fibre Carbohydrates Fat Energy Zn Cu Fe Ca
g/100 g g/100 g g/100 g g/100 g kJ/100 g mg/g mg/g mg/g mg/g
M. oleifera
M. stenopetala
28.0 13.8 34.9 5.83 1400 7.035 6.84 173 21,300
26.6 44.9 2.17 5.99 1070 18.5 5.91 797 26,200
weeks). Their results show that the production of M. oleifera could be between 7.1 and 30 tonnes of fresh biomass per ha, which corresponds with our results, which reached between 7 and 7.9 tonnes of fresh biomass per ha. Nevertheless, they irrigated the plantation regularly and used fertilizers as well, while we did not. The design of their experiment was also very different.
Table 3 Amino acid content of Moringa oleifera and M. stenopetala plants in Arba Minch.
Our results correspond more closely with the study of Basra et al. (2015) from Pakistan, who reported the production of M. oleifera to be between 6.4 and 7.57 t/ha, but used a different experimental design. Another study conducted by Nouman et al. (2013) from the same place in Pakistan showed that 30 days of biomass production of MO could reach 151473 g of fresh biomass per plant depending on the height of the cut and the month of the harvest. Our results were between 1801299 g per plant for MS and 1974622 g per plant for MO. This production was from a longer period and from 130 cm tall plants. Nauman’s experiment also used irrigation and fertilizers, and the design was different in the number of plants. The comparisons mentioned above were made only for M. oleifera, which has been investigated more thoroughly than M. stenopetala. Only two relevant researches have been found about MS biomass. Debela et Tolera (2013) reported 242 g/kg of DM for MO and 205 g/kg for MS. This is considerably less than our results (266270 g/kg MO and 264269 for MS). Other investigations of M. stenopetala were conducted in Bako in eastern Ethiopia by Samuel et al. (2016), but they studied the total height, root collar diameter, diameter at breast height and survival rate of the two species. As an overall result of biomass production, it seems that MS is not suitable for growing on intensive plantations because it has problems with pests and diseases that reduce yields.
4.2. Nutritional potential
Amino Acid content (g/100 g)
Aspartic acid Serine Glutamic acid Glycine Histidine Arginine B Threonine Alanine Proline Cystine Tyrosine Valine Methionine Lysine Isoleucine Leucine Phenylalanine
M. oleifera
M. stenopetala
2.81 1.48 3.42 1.27 0.60 1.42 1.33 1.52 1.28 0.39 0.84 1.58 0.42 1.46 1.20 1.99 1.60
3.70 1.59 2.67 1.27 0.55 1.44 1.27 1.54 1.20 0.54 0.90 1.42 0.38 1.37 1.19 1.90 1.32
In Ethiopia, Moringa stenopetala is an important source of nutritionally rich food, especially during the dry season, due to its drought resistance. In addition to using it as a common food source, local people are familiar with its use in traditional medicine, though they are not familiar with its nutritional potential. Laboratory analysis of both MO and MS leaf powder was conducted to measure nutritional values, mineral supply and amino acid content. As observed in this comparison, the results show that MO and MS differ quite significantly in fibre content, carbohydrates content and therefore also energy value, there are also huge differences in Zn, Fe and Ca content. The fibre content in MS is more than 3.2 times higher, the carbohydrates content in MS is on the other hand very low reaching only 6% of the carbohydrates content in MO. MO is well known for its high iron content, nevertheless, MS reaches even 4.6 times more iron than MO according to our analyses. Also zinc content is much higher (2.6 times), the calcium content in MS reaches 123% of the calcium in MO.
mec et al., Biomass production of a young plantation of Moringa stenopetala (Baker f.) Cufod. and Moringa Please cite this article as: P. Ne oleifera Lam. in southern Ethiopia, South African Journal of Botany (2020), https://doi.org/10.1016/j.sajb.2020.01.018
JID: SAJB
ARTICLE IN PRESS
[m5G;January 28, 2020;10:32]
P. Nemec et al. / South African Journal of Botany 00 (2020) 18
For the majority of evaluated amino acids, the results seem nearly the same in both species; only aspartic acid, glutamic acid, cystine, and phenylalanine differ significantly; the differences in amounts of the rest of amino acid values in both species do not exceed 15%. We compared our results with similar data from different studies of Moringa oleifera to see if our results are ranging in similar values despite possible differences in soil and climate conditions. For example, Kumssa et al. (2017), who conducted wide analyses of 56 samples from various localities in south Ethiopia and Kenya; some of their results correspond with the ours. For Moringa oleifera, they reported similar values of calcium (mean 18,326, minimum 7037 and maximum 46,591), nearly the same values of Cu (6.923, 3.00513.9) and Fe (202, 711171) but higher Zn, where the mean value was 35.6, while maximum was 68.2 and minimum was 14.4, which is still 205% of our results. Melesse et al. (2012) reported higher copper content (9.84 mg/g, 143%) and calcium content (26,700 mg/g, 125%) and significantly higher content of zinc (24.7 mg/g, 351%) and iron (558 mg/g, 322%) in MO leaves than shown in our study. Their results correspond rather with results of MS than MO from our study. The authors noticed that Cu and Ca concentrations in leaves were higher in the dry season. However, they reported that the absence of seasonal effects on most nutrient contents suggested that the Moringa tree parts are capable of retaining important nutrients further into the dry season. Mabapa et al. (2017) reported the following concentrations of nutrients of MO from their study: Fe 136364 mg/g. Our Fe results are within the range of their results, but the Zn results are not: their reported Zn 2028.7 mg/g was at least three times (284398%) higher than in our study. Because high levels of Fe in the diet might interfere with the absorption of Zn, Cu and Mn (Gengelbach et al., 1994), the M. oleifera tested in this study seems to be more dietarily suitable. M. stenopetala has been investigated much less. One of the studies was conducted by Debela and Tolera (2013), who reported results from both MS and MO from Awassa, which is in the same region of Ethiopia as our experiment. They investigated (amongst other variables) mineral content in both species: their samples contained half the Ca concentration of ours (12,900 mg/g MO 60% and 12,100 mg/ g MS 47%), more Zn in MO (28.2 mg/g, 400%) and slightly less Zn in MS (22.7 mg/g, 79%), and more Cu for both species (17.7 mg/g 259% MO, 12.6 mg/g 157% MS), more Fe in MO (390.9 mg/g, 226%) and nearly the same Fe in MS (681.2 mg/g, 97%). Very similar study was made by Melesse et al. (2012) in which they investigated the variability in nutritive values of leaves of both Moringa species in response to elevation and season. Some of M. stenopetala samples were collected in Arba Minch in December during the dry season. This makes their data ideal for this comparison because our M. oleifera analysed samples were also harvested during the dry season (February). This study confirms that MS has more iron, calcium and zinc than MO, and less energy supply and protein content. They reported 25,500 mg/g Ca (97%), 703 mg/g Fe (88%), 28.9 mg/g Zn (156%), and 8.05 mg/g Cu (136%). The total energy content in the whole plantation biomass in March was estimated. The results show that the March harvest of MO (705 trees) total estimated leaf biomass yield would supply a one day proper calorie intake to 340 adult people (irrespective of gender according to Berkum et al. 2017 who state the daily per capita supply of calories in Ethiopia to be 2,131 kcal), while MS (705 trees) would supply only 123 people. It seems that significantly low carbohydrates content could be the main reason. Counted with the same values, MO total estimated leaf biomass yield from 1 ha would supply a one day proper calorie intake for 3213 adult people, while MS would supply 1159 people. A compositional study of M. stenopetala leaves by Abuye et al. (2004) found slightly different energy content in comparison with our M. oleifera analysis.
7
5. Conclusion Moringa oleifera and Moringa stenopetala are two of five species in the genus Moringa that can be found in Ethiopia and two of four edible species in the genus. M. oleifera is not native to this area; however, for its abundant expansion in the world, it is definitely the most well-known species of the whole genus. Due to its drought resistance, its ability to absorb extremely high levels of CO2, its ability to improve soil quality and the exceptionally high content of substances necessary for our health, this fast-growing tree is often grown on plantations. The aim of this work was to evaluate the possibility of cultivating Moringa oleifera and Moringa stenopetala species on intensive plantations in southern Ethiopia. Processed data on leaf biomass production from the plantation favours Moringa oleifera. Not only was the yield considerably higher, but this species, based on field observation, is more resistant to pests and diseases in southern Ethiopian conditions. A plantation counting 705 of M. oleifera and 705 of M. stenopetala trees with a 1 £ 1.5 m current spacing shows a higher yield of leaf biomass than expected yield if the spacing were changed to 3 £ 3 m. However, the wider spacing could have a positive impact on the reduction of pests and diseases that have been identified on trees and would most likely reduce the occurrence of powdery mildew. The nutritional value of both species was compared. The source of the data was, in the case of both species, from our own analyses. In general, most of the values did not differ between the species. Declaration of Competing Interest None. Acknowledgement This study was supported by the Czech Development Agency within project nr. 02/2016/03 “Implementation of holistic management and Climate Smart Agriculture in the Baso River catchment, Arba Minch Zuria Woreda, SNNPR, Ethiopia”, and project nr. PP2018-051-SO-25010 “Application of the economic and social potential of innovated products from moringa in Ethiopia”. References Abuye, C., Urga, K., Knapp, H., Selmar, D., Omwega, A.M., Imungi, J.K., Winterhalter, P., 2004. A compositional study of Moringa stenopetala leaves. East African Medical Journal 80 (5). https://doi.org/10.4314/eamj.v80i5.8695. Amaglo, N., Bennett, R.N., Lo Curto, R., Rosa, E., Lo Turco, V., Giuffrida, A., Lo Curto, A., Crea, F., Timpo, G.M., 2010. Profiling selected phytochemicals and nutrients in different tissues of the multipurpose tree Moringa oleifera L., grown in Ghana. Food Chemistry 122 (4), 1047–1054. https://doi.org/10.1016/j.foodchem.2010.03.073. Ashfaq, M., Basra, S.M.A., Ashfaq, U., 2012. Moringa: a miracle plant of agro-forestry. Journal of Agriculture and Social Science 8, 115–122. Aynalem, A.E., 2008. Moringa Stenopetala Seed Oil As a Potential Feedstock For Biodiesel Production in Ethiopia. Addis Ababa University, Ethiopia M. Sc. thesis. Bartikova, et al.Causal agents of powdery mildew on Moringa stenopetala (Baker f.) cuf. and Moringa oleifera lam. in Ethiopia (submitted to South African Journal of Botany). Basra, S.M.A., Nouman, W., Rehman, H.U., Usman, M., Nazli, Z.H., 2015. Biomass production and nutritional composition of Moringa oleifera under different cutting frequencies and planting spacings. International Journal of Agriculture & Biology 17 (5), 1055–1060. Bedane, T.M., Singh, S.K., Selvaraj, T., Negeri, M., 2013. Distribution and damage status of Moringa moth (Noorda blitealis walker) on Moringa stenopetala baker (Cufod.) in southern rift valley of Ethiopia. International Journal of Agricultural Technology 9 (4), 963–985. Berkum, S. van, Achterbosch, T.J., Linderhof, V.G.M., 2017. Dynamics of food systems in Sub-Saharan Africa; Implications for consumption patterns and farmers’ position in food supply chains. Wageningen, Wageningen Economic Research, Report 2017-072. 42 pp. Boukandoul, S., Casal, S., Zaidi, F., 2018. The potential of some Moringa species for seed oil production: a review. Agriculture 8 (150), 1–13. Climate-data.org, 2018[online], cited on March 29th, Available at: https://en.climatedata.org/location/3066/
mec et al., Biomass production of a young plantation of Moringa stenopetala (Baker f.) Cufod. and Moringa Please cite this article as: P. Ne oleifera Lam. in southern Ethiopia, South African Journal of Botany (2020), https://doi.org/10.1016/j.sajb.2020.01.018
JID: SAJB 8
ARTICLE IN PRESS
[m5G;January 28, 2020;10:32]
P. Nemec et al. / South African Journal of Botany 00 (2020) 18
Debela, E., Tolera, A., 2013. Nutritive value of botanical fractions of Moringa oleifera and Moringa stenopetala grown in the mid-Rift valley of southern Ethiopia. Agroforestry Systems 2013 (87), 1147–1155. https://doi.org/10.1007/s10457-013-9626-9. Edward, E., Chamshama, S.A.O., Ngaga, Y.M., Mndolwa, M.A., 2014. Survival, growth and biomass production of Moringa oleifera provenances at Gairo inland plateau and Ruvu coastal region in Tanzania. African Journal of Plant Science 8 (1), 54–64. https://doi.org/10.5897/AJPS12.158. Gebregiorgis, F., Negesse, T., Nurfeta, A., 2012. Feed intake and utilization in sheep fed graded levels of dried Moringa (Moringa stenopetala) leaf as a supplement to Rhodes grass hay. Tropical Animal Health and Production 44 (3), 511–517. https://doi. org/10.1007/s11250-011-9927-9. Gengelbach, G.P., Ward, J.D., Spears, J.W., 1994. Effect of dietary copper, iron, and molybdenum on growth and copper status of beef cows and calves. Journal of Animal Science 72 (10), 2722–2727. Isah, A.D., Bello, A.G., Zarumaye, S.A., 2014. Effects of cutting heights and interval of cutting on the yield of Moringa oleifera (horse raddish). International Journal of Development and Sustainability 3 (5), 1147–1151. Habtemariam, S., 2016. The African moringa is to change the lives of millions in Ethiopia and far beyond. Asian Pacific Journal of Tropical Biomedicine 6 (4), 355–356 April 2016. Kumssa, D.B., Joy, E.J.M., Young, S.D., Odee, D.W., Ander, E.L., Broadley, M.R., 2017. Variation in the mineral element concentration of Moringa oleifera lam. and M. stenopetala (Bak. f.) cuf.: Role in human nutrition. PLoS ONE 12 (4), e0175503. https://doi. org/10.1371/journal.pone.0175503. Lijesh, K.P., Malhotra, R., 2016. Reduction of turbidity of water using Moringa oleifera. International Journal of Applied Engineering Research 11 (2), 1414–1423. Mabapa, M.P., Ayisi, K.K., Mariga, I.K., 2017. Effect of planting density and harvest interval on the leaf yield and quality of moringa (Moringa oleifera) under diverse agroecological conditions of northern South Africa. International Journal of Agronomy 2017, 9. https://doi.org/10.1155/2017/2941432 Article ID 2941432. Melesse, A., Tiruneh, W., Negesse, T., 2011. Effects of feeding Moringa stenopetala leaf meal on nutrient intake and growth performance of Rhode Island red chicks under tropical climate. Tropical and Subtropical Agroecosystems 14, 485–492. Melesse, A., Steingass, H., Boguhn, J., Schollenberger, M., Rodehutscord, M., 2012. Effects of elevation and season on nutrient composition of leaves and green pods of Moringa stenopetala and Moringa oleifera. Agroforestry Systems 86 (3), 505–518. https://doi.org/10.1007/s10457-012-9514-8. Mofijur, M., Masjuki, H.H., Kalam, M.A., Atabani, A.E., Fattah, I.M.R., Mobarak, H.M., 2014. Comparative evaluation of performance and emission characteristics of Moringa oleifera and palm oil based biodiesel in a diesel engine. Industrial Crops and Products 53, 78–84. https://doi.org/10.1016/j.indcrop.2013.12.011. Nouman, W., Siddiqui, M.T., Basra, S.M.A., Farooq, H., Zubair, M., Gull, T., 2013. 2013. Biomass production and nutritional quality of Moringa oleifera as a field crop. Turkish Journal of Agriculture and Forestry 37, 410–419. https://doi.org/10.3906/ tar-1206-29.
Olson, M.E., Sankaran, R.P., Fahey, J.W., Grusak, M.A., Odee, D., Nouman, W., 2016. Leaf protein and mineral concentrations across the “Miracle tree. Genus Moringa. PLoS ONE 11 (7), e0159782. https://doi.org/10.1371/journal.pone.0159782. Olson, M.E., 2017. Moringa frequently asked questions. In: Ebert, A.W., Palada, M.C. (Eds.), Proceedings of the First International Symposium on Moringa. Acta Horticulturae 1158. ISHS 2017, pp. 19–32. https://doi.org/10.17660/ActaHortic.2017.1158.4. Olson, M.E., 2002. Combining data from dna sequences and morphology for a phylogeny of Moringaceae (Brassicales). Systematic Botany 27, 55–73. Patricio, H.G., Palada, M.C., Deloso, H.E., Garcia, D.E., 2017. Biomass yield of Moringa oleifera as influenced by plant density and harvest frequency. In: Ebert, A.W., Palada, M.C. (Eds.), Proceedings of the First International Symposium on Moringa. Acta Horticulturae 1158, pp. 97–104. € ppenPeel, M.C., Finlayson, B.L., McMahon, T.A., 2007. Updated world map of the Ko Geiger climate classification. Hydrology and Earth System Sciences Discussions 4 (2), 439–473. Pontailler, J.Y., Ceulemans, R., Guittet, J., Maum, F., 1997. Linear and non-linear functions of volume index to estimate woody biomass in high density young poplar stands. Annals of Forest Sciences 54 (4), 335–345. https://doi.org/10.1051/forest:19970402. , C., 1985. Biomass production by alders on four abandoned agricultural Pregent, G., Camire bec. In: Lalonde, M., Camire , C., Dawson, J.O. (Eds.), Frankia and Actinorhisoils in Que zal Plants. Developments in Plant and Soil Sciences, Vol 18. Springer, Dordrecht. Sanchez, N.R., Ledin, S., Ledin, I., 2006. 2006. Biomass production and chemical composition of Moringa oleifera under different management regimes in Nicaragua. Agroforestry Systems 66, 231–242. Samuel, D., Terefe, R., Senbeto, M., Daba, M., 2016. Evaluation of two Moringa species for adaptability and growth performance under Bako conditions. Journal of Natural Sciences Research 6 (9), 76–82 ISSN 2224-3186. Schneemann, J., 2011. Moringa (stenopetala) Production and Use For Water Purification in Ethiopia. Fair and Sustainable Advisory Service. Utrecht, The Netherlands. Seifu, E., 2014. Actual and potential applications of moringa stenopetala, underutilized indigenous vegetable of southern Ethiopia: a review. International Journal of Agricultural and Food Research 3, 8–19. Sanjay, P., Dwivedi, K.N., 2015. Shingru (Moringa oleifera lam.): A critical review. International Journal of Ayurveda and Pharmaceutical Chemistry 3 (1), 217–227. n-Escalante, I.E., Zepeda-Bautista, R., Jime nez-Arellanes, M.A., Velazquez-Zavala, M., Peo 2016. Moringa (Moringa oleifera lam.): potential uses in agriculture, industry and medicine. Revista Chapingo Serie Horticultura 22 (2), 95–116. https://doi.org/ 10.5154/r.rchsh.2015.07.018. Yisehak, K., Solomon, M., Tadelle, M., 2011. Contribution of Moringa (Moringa stenopetala, bac.) a highly nutritious vegetable tree, for food security in south Ethiopia: A review. Asian Journal of Applied Sciences 4 (5), 477–488 ISSN 1996-3343.
mec et al., Biomass production of a young plantation of Moringa stenopetala (Baker f.) Cufod. and Moringa Please cite this article as: P. Ne oleifera Lam. in southern Ethiopia, South African Journal of Botany (2020), https://doi.org/10.1016/j.sajb.2020.01.018
JID: SAJB
[m5G;January 28, 2020;10:32]
South African Journal of Botany 000 (2020) 18
Contents lists available at ScienceDirect
South African Journal of Botany journal homepage: www.elsevier.com/locate/sajb
Biomass production of a young plantation of Moringa stenopetala (Baker f.) Cufod. and Moringa oleifera Lam. in southern Ethiopia meca, Moana Ungrova a, Shiferaw Alema, Jaromír Nova kb, Hana Habrova a,* Petr Ne a b
Faculty of Forestry and Wood Technology, Mendel University in Brno, Zemedelska 3, 61300 Brno, Czech Republic Holistic Solutions s.r.o., Veveri 467/25, 60200 Brno, Czech Republic
A R T I C L E
I N F O
Article History: Received 30 March 2019 Revised 5 December 2019 Accepted 7 January 2020 Available online xxx Edited by NE Madala Keywords: Arba Minch Ethiopia Leaf biomass production Moringa oleifera Moringa stenopetala nutritional values
A B S T R A C T
In May 2017, a plantation of Moringa stenopetala and Moringa oleifera was established in southern Ethiopia using a spacing of 1 £ 1.5 m. The plantation was not artificially irrigated, and no fertilizers or pesticides have been applied. To assess the suitability of cultivation on the plantation, the average leaf biomass production and, secondarily, to evaluate the nutritional potential of both species, three harvests were carried out in November 2017, March 2018 and in November 2018. The leaf biomass was harvested in each trial from the same thirty trees. A principal objective of the study was to describe the suitability of Moringa stenopetala for cultivation in an intensive plantation and to compare these results with the results of cultivation of Moringa oleifera. The results show that in young plantations of M. stenopetala, dry matter biomass production could reach up to 2,824 kg/ha/year, while for M. oleifera, it could reach 6,060 kg/ha/year. One harvest of a M. oleifera plantation’s (705 trees) total estimated leaf biomass would yield a one day proper calorie intake for 340 adult humans (irrespective of gender), while M. stenopetala would supply only 123 people, i.e., 1 ha of M. oleifera plantation would supply a one day proper calorie intake to 3,213 adults, while M. stenopetala would supply a one day proper calorie intake to 1,159 adults. Based on the evaluated data, M. oleifera is considered to be more suitable for (growing on) plantations in southern Ethiopia due to its pest resistance and high leaf biomass production. © 2020 SAAB. Published by Elsevier B.V. All rights reserved.
1. Introduction Moringa oleifera (further abbreviated as MO) and Moringa stenopetala (MS), which belong to the monospecific family Moringaceae, are two of the 13 identified species of the family (Velazquez-Zavala et al., 2016; Edward et al., 2014; Gebregiorgis et al., 2012) and two in a group of four edible species (Olson 2017). Both species are the most common species in the family, and both have many characteristics in common (Schneemann, 2011). M. oleifera is a multi-purpose tree originally from India (Seifu, 2014), while M. stenopetala is native to eastern Africa, where it is grown in southern Ethiopia, northern Kenya and eastern Somalia (Bedane et al., 2013). Moringa oleifera, which is more well-known, grows in tropical and sub-tropical climates; it is drought-resistant and can be grown in a wide variety of poor soils, including barren ground, with soil pH between 4.5 and 9.0 (Ashfaq et al., 2012; Olson, 2002). It has tremendous potential uses, such as food for human beings, feed for livestock, medicine, dye, perfume, skin lotion, lubricant and water purification (Nouman et al., 2013; Melesse et al., 2011). The leaves are * Corresponding author. E-mail address: [email protected] (H. Habrova).
nutritionally rich and serve as an excellent source of concentrated proteins, vitamins and minerals (Isah et al., 2014; Amaglo et al., 2010). MO is attributed with properties for the treatment of certain ailments such as asthma, epilepsy, eye and skin diseases, fever and haemorrhoids (Sanjay and Dwivedi, 2015). The seeds are used to treat groundwater and water with suspended solids (Lijesh and Malhotra, 2016), and they can also serve as a source of oil for biodiesel production (Mofijur et al., 2014). MO is now widely cultivated and is found in most tropical countries (Africa, Asia and America) (Boukandoul et al., 2018; Olson et al., 2016; Sanjay and Dwivedi, 2015; Edward et al., 2014), and it has also received research and development attention worldwide (Seifu, 2014). Moringa stenopetala is still grown only in its area of origin, where farmers grow it in agroforestry systems or as individual trees. It is used for its nutritional and medicinal value (Habtemariam, 2016, Yisehak et al., 2011), especially for high iron content, their other uses seem similar to MO nevertheless, only a few scientific researches have been proved about its properties. In Ethiopia, MS is native in arid, semi-arid and semi-humid areas at altitudes ranging from 1000 to 1800 m a.s.l., and because of its palatable leaves, it is one of the most frequently cultivated indigenous species (Bedane et al., 2013). It is widely distributed in the Konso, Wolayta, D’irashe, Gamo Gofa,
https://doi.org/10.1016/j.sajb.2020.01.018 0254-6299/© 2020 SAAB. Published by Elsevier B.V. All rights reserved.
mec et al., Biomass production of a young plantation of Moringa stenopetala (Baker f.) Cufod. and Moringa Please cite this article as: P. Ne oleifera Lam. in southern Ethiopia, South African Journal of Botany (2020), https://doi.org/10.1016/j.sajb.2020.01.018
JID: SAJB
ARTICLE IN PRESS
[m5G;January 28, 2020;10:32]
P. Nemec et al. / South African Journal of Botany 00 (2020) 18
2
Sidama, Bale and Borana areas (Aynalem, 2008; Gebregiorgis et al., 2012). It is an especially important component of the local diet in the Gamo Gofa and Konso zones. Although MO is widely cultivated and has received research and development attention worldwide (Seifu, 2014), it has been introduced to Ethiopia very recently, which shows that much more research has to be conducted to evaluate the species in Ethiopian climatic conditions. There is also scant information on the native MS species, which has recently gained attention due to its multiple uses; little is known about its nutritional value and biomass production when it is managed as an intensive plantation. Therefore, the objectives of this study are 1) to assess the biomass production of M. stenopetala relative to M. oleifera plantation in Arba Minch Zuria Woreda, SNNPR, Ethiopia and 2) to evaluate the nutritional values of MS relative to MO. At the beginning of the study, it was hypothesized that 1) MS can produce higher biomass relative to MO in a monoculture plantation and 2) the nutritional value of MS is not significantly different from MO. 2. Materials and methods 2.1. Study area The study was conducted in the Permaculture Training and Demonstration Centre, which was established by Mendel University within the project “Implementation of holistic management and Climate Smart Agriculture in the Baso River catchment, Arba Minch Zuria Woreda, SNNPR, Ethiopia”. The centre (coordinates 6°060 52.100 N 37°360 34.300 E) lies just next to Chano Mile village, which lies within the Arba Minch Zuria Woreda in the Gamo Gofa zone. Arba Minch lies on the southwestern shores of Lake Abaya and Lake Chamo, which are located at the base of the western side of the Great Rift Valley at an elevation of 1285 m a.s.l. Arba Minch received its name from the 40 nearby springs. According to the € ppen climate classification (Peel et al., 2007), the climate type Ko in Arba Minch corresponds to category Aw: a tropical wet-dry climate. High temperatures throughout the year are typical in areas with distinct wet and dry seasons (extended dry season during winter), with most of the precipitation occurring in the high-sun (“summer”) season (Climate-data.org, 2018). According to the climate diagram, the average annual precipitation in Arba Minch is approximately 820 mm and the average temperature is 21.5 °C. The study area has alluvial sediments, which are, in addition to being good quality soil, typical of low river flows, lake depressions and valleys of former or current lakes. These sediments consist of gravel, sand and silt. Due to the study area’s proximity to Lake Abaya, groundwater is available and makes this area suitable for agroforestry purposes. The study area is situated in the kolla zone at an altitude of 1191 m a.s.l. As mentioned, the highest precipitation occurs from AprilJune and from OctoberDecember.
2.3. Data collection For the purpose of this study, MO and MS leaves were harvested three times through manual removal of all leaves from each tree. The first harvest occurred on 19 November 2017, the second harvest occurred on 20 March 2018 and the third harvest occurred on 15 November 2018. During each harvest, fifteen samples from each species (thirty samples per harvest) were collected in row 21, in the case of MS, and in rows 3536, in the case of MO; trees were taken from two rows because four samples in the 35th row were not suitable for the statistical data because they had been pruned. Each sample was given a number and was subsequently weighed on a laboratory scale. Fresh leaf biomass weight data were recorded. 1000 g of fresh leaves of each species from both first harvests (four kilograms in total) was separately dried at 65 °C for 48 h in a drying oven at Arba Minch University. After that, the values of dry leaf biomass (DM) obtained from each individual tree were calculated from the weight of one kilogram of dried leaves. Subsequently, all measured data were statistically analysed in Microsoft Excel, and the results were displayed graphically. Samples of 500 g of both MO crushed leaf powder and MS crushed leaf powder were sent to the laboratory ALS Czech Republic, s.r.o., in Prague, Czech Republic, to conduct amino acid and nutritional analysis. 2.4. Data analysis Since the samples were collected from the same trees three times in two different seasons, the data were processed using a repeated measures ANOVA with two factors: (1) month of the harvest and (2) species. The significance level p was set at 0.05. Due to increasing variability, logarithmically transformed data were used for the ANOVA. Statistical data were analysed using the open-source statistical program JASP. 3. Results 3.1. Leaf biomass production The biomass gain in different seasons of the fresh leaves that were dried using the drying oven in this study is presented in Table 1. The dry leaf biomass production of the individual sampled trees at different seasons of the study period for MS and MO are presented in Figs. 3 and 4, respectively. The mean dry leaf biomass production of M. stenopetala in November 2017, March 2018 and November 2018
2.2. Moringa plantation establishment The plantation (Fig 1) was established on 1 May 2017. Seeds of local origin were used, and grown plants were planted in an area of 30 £ 70.5 m with 1.5 m spaces within the row and 1 m spaces between rows, resulting in 705 of each tree species at the plantation (15 £ 47 rows for each species, 1410 trees in total). The plantation was not artificially irrigated, and no fertilizers or pesticides have been applied thus far. The first improvement cutting took place at the beginning of July: each plant was cut off at breast height (1.3 metres above ground). The very first harvest (with no data recorded) took place in August 2017.
Fig. 1. Established plantation of Moringa oleifera (left) and Moringa stenopetala (right).
mec et al., Biomass production of a young plantation of Moringa stenopetala (Baker f.) Cufod. and Moringa Please cite this article as: P. Ne oleifera Lam. in southern Ethiopia, South African Journal of Botany (2020), https://doi.org/10.1016/j.sajb.2020.01.018
ARTICLE IN PRESS
JID: SAJB
[m5G;January 28, 2020;10:32]
P. Nemec et al. / South African Journal of Botany 00 (2020) 18
The total leaf biomass (kg) production of MO at different seasons of harvest is presented in Fig. 7. The results indicated that the total dry leaf biomass production of MO harvested in November 2018 was higher relative to the total dry leaf biomass production in November 2017 and March 2018 (Fig. 5). However, the one-way ANOVA result revealed no significant difference (p = 0.483) in the dry leaf biomass of MO harvested at different periods (Fig. 7). Overall, the study results indicated that the MO dry leaf biomass production was higher than the dry leaf biomass production of MS. The statistical test results also revealed a significant difference in the mean dry leaf biomass production of MO and MS (Fig. 8, P < 0.001). Total leaf biomass production from the whole plantation was also estimated. The average dry biomass yield from each harvest was multiplied by 47 (number of rows by 15 trees). The leaf biomass production from the M. oleifera part of the plantation (15 £ 70.5 m) was approximately 200 kg in November 2017, 217 kg in March 2018 and 224 kg in November 2018. The same was done with M. stenopetala, and in November 2017, March 2018 and November 2018, the results were 117 kg, 102 kg and 80 kg, respectively. Extrapolation of these results could indicate that the average yearly production of MS dry leaf biomass could be approximately 2824 kg/ha, and for MO, it could be approximately 6060 kg/ha.
Table 1 Ratio of fresh leaf biomass to dry matter biomass. Weight loss caused by drying
M. oleifera M. stenopetala
Nov 2017
Mar 2018
270.4 g/kg 264.2 g/kg
266.1 g/kg 269.2 g/kg
3
were 165.4 (16.8) g/tree, 144.7 (13.9) g/tree and 113.4 (13.9) g/tree, respectively. In contrast, the mean dry leaf biomass production of M. oleifera in the periods of November 2017, March 2018 and November 2018 were 283.5 (48.0) gram/tree, 323.8 (52.5) gram/tree, and 325.9 (70.8) gram/ tree, respectively. As mentioned, leaves were harvested from 30 trees (15 from each species) three times. Comparing the weights of M. oleifera trees, they show a significant increase between the three harvests, while the difference in the obtained leaf biomass from all harvests of M. stenopetala trees decreased, as shown in the following figures (Figs. 2-4). The results of the total harvest of dry leaf biomass (kg) of the two studied species in different seasons are presented in Fig. 5. The results indicated that the total dry leaf biomass of MS harvested in November 2018 was lower relative to the total dry leaf biomass harvested in November 2017 and March 2018 (Fig. 5). The one-way ANOVA result also indicated a significant difference (p = 0.036) in the mean dry leaf biomass (g) production of MS harvested at different periods of the study (Fig. 6). These significant differences were between the dry leaf biomass production for the seasons of November 2017 and November 2018 (Fig. 6).
3.2. Nutritional potential The results of the nutritional analysis of Moringa are presented in Tables 2 and 3. Moringa in general is an excellent source of nutrition, especially because of its high iron (Fe) and calcium (Ca) content. This
M. stenopetala
M. oleifera
20.00 15.00 10.00 5.00 0.00
Nov 17
Mar 18
Nov 18
Fig. 2. Total harvest of 15 trees in different seasons (kg of fresh leaves).
350.00 Nov 17
Mar 18
Nov 18
300.00 250.00 200.00 150.00 100.00 50.00 0.00 1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
Fig. 3. Dry leaf biomass (g) production from 15 individual sampled trees of M. stenopetala for the study in different seasons of the year.
mec et al., Biomass production of a young plantation of Moringa stenopetala (Baker f.) Cufod. and Moringa Please cite this article as: P. Ne oleifera Lam. in southern Ethiopia, South African Journal of Botany (2020), https://doi.org/10.1016/j.sajb.2020.01.018
ARTICLE IN PRESS
JID: SAJB
[m5G;January 28, 2020;10:32]
P. Nemec et al. / South African Journal of Botany 00 (2020) 18
4
1,200.00 Nov 17
Mar 18
Nov 18
1,000.00 800.00 600.00 400.00 200.00 0.00 1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
Fig. 4. Dry leaf biomass (g) production from 15 individual sampled trees of M. oleifera for the study in different seasons of the year.
300
Leaf biomass (Grams)
250 a ab
200
b 150 100 50 0 November 2017
March 2018
November 2018
Period Fig. 5. One-way ANOVA result of the dry leaf biomass of M. stenopetala at different periods of leaf harvest at a 0.05% level of significance (p = 0.036). Means with the same letters are not significantly different.
fact has been demonstrated by laboratory analysis, which has also shown content of other components. The analysis was principally performed to obtain the energy amount of the plantation of both species and their comparison. Whole plantation of both species produced 12,166,430 kJ per year (3195,154 kJ MS and 8971,275 kJ MO). 4. Discussion 4.1. Leaf biomass production Although Moringa stenopetala is native in the study area, the results have shown significantly better growth of Moringa oleifera. Its leaf biomass production reached amounts more than 1/3 higher than MS during the first harvest, and its production has been increasing while native species production has decreased. One reason might be lower water requirements and thus higher resistance against
drought; the March harvest was relatively poor for the MS trees because there were dry months before. However, the third harvest was carried out again during November 2018 after the rainy season, and the decrease of produced biomass persisted. The reason could be in lower resistance to pests and diseases such as powdery mildew and Noorda blitealis which have been developed after the rains. This has been observed by phytopathology experts; nevertheless, this analysis was not included in this study and was described in an independent scientific paper (Bartikova et al., submitted). Another influence on total biomass production could be a borgent and Camire , 1985; Pontailler et al., 1997). The der effect (Pre trees growing at the edge of the plantation have significantly higher leaf biomass production; when these trees are excluded from the data, the results for MS remain the same, i.e., the total amount of leaf biomass decreases with tree age (7.6 kg, 6.5 kg and 5.2 kg of fresh leaves from 13 trees). However, for MO, the total leaf biomass slowly decreased, too (12.6 kg, 12.2 kg and
mec et al., Biomass production of a young plantation of Moringa stenopetala (Baker f.) Cufod. and Moringa Please cite this article as: P. Ne oleifera Lam. in southern Ethiopia, South African Journal of Botany (2020), https://doi.org/10.1016/j.sajb.2020.01.018
ARTICLE IN PRESS
JID: SAJB
[m5G;January 28, 2020;10:32]
P. Nemec et al. / South African Journal of Botany 00 (2020) 18
5
Leaf biomass (Grams)
800
600 a
a
a
400
200
0 November 2017 March 2018
November 2018
Period Fig. 6. One-way ANOVA result of the dry leaf biomass of M. oleifera at different periods of leaf harvest at the 0.05% level of significance (p = 0.483). Means with the same letters are not significantly different.
600
Leaf biomass (Grams)
500 a 400 300 b
200 100 0 M. oleifera
M. stenopetala
Fig. 7. Statistical t-test result on the dry leaf biomass of M. oleifera vs M. stenopetala at the 0.05% level of significance (P = 0.001). Means with the same letters are not significantly different.
11.6 kg of fresh leaves). The total MO biomass increase, then, was caused only by edge trees, but we could not exclude them because they are valid parts of the plantation, and all the edge trees were visibly large. As a result, wider tree spacing (3 £ 3 m) to increase biomass production could be taken into account; however, the spacing in plantations is usually even denser than 1 £ 1.5 m (Patricio et al., 2017; Basra et al., 2015; Nouman et al., 2013; Sanchez et al., 2006). At the current spacing of 1 £ 1.5 m, there are 705 MO and 705 MS trees. At a spacing of 3 £ 3 m, the number would decrease to 117 trees. Assuming that those trees would have more space for growth and provide equally high leaf biomass production as the edge trees currently do, the average estimated production has been calculated. The charts show that the leaf biomass production on the plantation would have
a surprisingly significant decrease to only approximately 1/4 of current production. Thus, wider spacing probably would not provide higher leaf biomass yield; however, due to better air circulation, it might help to reduce pests and diseases. This corresponds with findings of Mabapa et al. (2017) who reported that planting density had a significant influence on biomass production, where higher planting density resulted in greater biomass yield harvests. Their results show that the DM of MO is between 611 and 2867 kg/ha, while our results show 18902137 kg/ha of DM. During their study, no fertilizers were used. The first six weeks of better tree establishment were supported by irrigation, which was applied twice per week for four hours. Patricio et al. (2017) also performed an experiment to observe biomass production on plantations with different spacing (1040 thousand plants per ha) and different harvest frequencies (4, 6 and 8
mec et al., Biomass production of a young plantation of Moringa stenopetala (Baker f.) Cufod. and Moringa Please cite this article as: P. Ne oleifera Lam. in southern Ethiopia, South African Journal of Botany (2020), https://doi.org/10.1016/j.sajb.2020.01.018
ARTICLE IN PRESS
JID: SAJB
[m5G;January 28, 2020;10:32]
P. Nemec et al. / South African Journal of Botany 00 (2020) 18
6
The average amount of energy contained in the March harvest [kcal/ha] 8,000,000.00 7,000,000.00 6,000,000.00 5,000,000.00 4,000,000.00 3,000,000.00 2,000,000.00 1,000,000.00 0.00 M. oleifera
M. stenopetala
Fig. 8. The average amount of energy from the March harvest (kcal/ha).
Table 2 Moringa oleifera and Moringa stenopetala nutritional values.
Protein Fibre Carbohydrates Fat Energy Zn Cu Fe Ca
g/100 g g/100 g g/100 g g/100 g kJ/100 g mg/g mg/g mg/g mg/g
M. oleifera
M. stenopetala
28.0 13.8 34.9 5.83 1400 7.035 6.84 173 21,300
26.6 44.9 2.17 5.99 1070 18.5 5.91 797 26,200
weeks). Their results show that the production of M. oleifera could be between 7.1 and 30 tonnes of fresh biomass per ha, which corresponds with our results, which reached between 7 and 7.9 tonnes of fresh biomass per ha. Nevertheless, they irrigated the plantation regularly and used fertilizers as well, while we did not. The design of their experiment was also very different.
Table 3 Amino acid content of Moringa oleifera and M. stenopetala plants in Arba Minch.
Our results correspond more closely with the study of Basra et al. (2015) from Pakistan, who reported the production of M. oleifera to be between 6.4 and 7.57 t/ha, but used a different experimental design. Another study conducted by Nouman et al. (2013) from the same place in Pakistan showed that 30 days of biomass production of MO could reach 151473 g of fresh biomass per plant depending on the height of the cut and the month of the harvest. Our results were between 1801299 g per plant for MS and 1974622 g per plant for MO. This production was from a longer period and from 130 cm tall plants. Nauman’s experiment also used irrigation and fertilizers, and the design was different in the number of plants. The comparisons mentioned above were made only for M. oleifera, which has been investigated more thoroughly than M. stenopetala. Only two relevant researches have been found about MS biomass. Debela et Tolera (2013) reported 242 g/kg of DM for MO and 205 g/kg for MS. This is considerably less than our results (266270 g/kg MO and 264269 for MS). Other investigations of M. stenopetala were conducted in Bako in eastern Ethiopia by Samuel et al. (2016), but they studied the total height, root collar diameter, diameter at breast height and survival rate of the two species. As an overall result of biomass production, it seems that MS is not suitable for growing on intensive plantations because it has problems with pests and diseases that reduce yields.
4.2. Nutritional potential
Amino Acid content (g/100 g)
Aspartic acid Serine Glutamic acid Glycine Histidine Arginine B Threonine Alanine Proline Cystine Tyrosine Valine Methionine Lysine Isoleucine Leucine Phenylalanine
M. oleifera
M. stenopetala
2.81 1.48 3.42 1.27 0.60 1.42 1.33 1.52 1.28 0.39 0.84 1.58 0.42 1.46 1.20 1.99 1.60
3.70 1.59 2.67 1.27 0.55 1.44 1.27 1.54 1.20 0.54 0.90 1.42 0.38 1.37 1.19 1.90 1.32
In Ethiopia, Moringa stenopetala is an important source of nutritionally rich food, especially during the dry season, due to its drought resistance. In addition to using it as a common food source, local people are familiar with its use in traditional medicine, though they are not familiar with its nutritional potential. Laboratory analysis of both MO and MS leaf powder was conducted to measure nutritional values, mineral supply and amino acid content. As observed in this comparison, the results show that MO and MS differ quite significantly in fibre content, carbohydrates content and therefore also energy value, there are also huge differences in Zn, Fe and Ca content. The fibre content in MS is more than 3.2 times higher, the carbohydrates content in MS is on the other hand very low reaching only 6% of the carbohydrates content in MO. MO is well known for its high iron content, nevertheless, MS reaches even 4.6 times more iron than MO according to our analyses. Also zinc content is much higher (2.6 times), the calcium content in MS reaches 123% of the calcium in MO.
mec et al., Biomass production of a young plantation of Moringa stenopetala (Baker f.) Cufod. and Moringa Please cite this article as: P. Ne oleifera Lam. in southern Ethiopia, South African Journal of Botany (2020), https://doi.org/10.1016/j.sajb.2020.01.018
JID: SAJB
ARTICLE IN PRESS
[m5G;January 28, 2020;10:32]
P. Nemec et al. / South African Journal of Botany 00 (2020) 18
For the majority of evaluated amino acids, the results seem nearly the same in both species; only aspartic acid, glutamic acid, cystine, and phenylalanine differ significantly; the differences in amounts of the rest of amino acid values in both species do not exceed 15%. We compared our results with similar data from different studies of Moringa oleifera to see if our results are ranging in similar values despite possible differences in soil and climate conditions. For example, Kumssa et al. (2017), who conducted wide analyses of 56 samples from various localities in south Ethiopia and Kenya; some of their results correspond with the ours. For Moringa oleifera, they reported similar values of calcium (mean 18,326, minimum 7037 and maximum 46,591), nearly the same values of Cu (6.923, 3.00513.9) and Fe (202, 711171) but higher Zn, where the mean value was 35.6, while maximum was 68.2 and minimum was 14.4, which is still 205% of our results. Melesse et al. (2012) reported higher copper content (9.84 mg/g, 143%) and calcium content (26,700 mg/g, 125%) and significantly higher content of zinc (24.7 mg/g, 351%) and iron (558 mg/g, 322%) in MO leaves than shown in our study. Their results correspond rather with results of MS than MO from our study. The authors noticed that Cu and Ca concentrations in leaves were higher in the dry season. However, they reported that the absence of seasonal effects on most nutrient contents suggested that the Moringa tree parts are capable of retaining important nutrients further into the dry season. Mabapa et al. (2017) reported the following concentrations of nutrients of MO from their study: Fe 136364 mg/g. Our Fe results are within the range of their results, but the Zn results are not: their reported Zn 2028.7 mg/g was at least three times (284398%) higher than in our study. Because high levels of Fe in the diet might interfere with the absorption of Zn, Cu and Mn (Gengelbach et al., 1994), the M. oleifera tested in this study seems to be more dietarily suitable. M. stenopetala has been investigated much less. One of the studies was conducted by Debela and Tolera (2013), who reported results from both MS and MO from Awassa, which is in the same region of Ethiopia as our experiment. They investigated (amongst other variables) mineral content in both species: their samples contained half the Ca concentration of ours (12,900 mg/g MO 60% and 12,100 mg/ g MS 47%), more Zn in MO (28.2 mg/g, 400%) and slightly less Zn in MS (22.7 mg/g, 79%), and more Cu for both species (17.7 mg/g 259% MO, 12.6 mg/g 157% MS), more Fe in MO (390.9 mg/g, 226%) and nearly the same Fe in MS (681.2 mg/g, 97%). Very similar study was made by Melesse et al. (2012) in which they investigated the variability in nutritive values of leaves of both Moringa species in response to elevation and season. Some of M. stenopetala samples were collected in Arba Minch in December during the dry season. This makes their data ideal for this comparison because our M. oleifera analysed samples were also harvested during the dry season (February). This study confirms that MS has more iron, calcium and zinc than MO, and less energy supply and protein content. They reported 25,500 mg/g Ca (97%), 703 mg/g Fe (88%), 28.9 mg/g Zn (156%), and 8.05 mg/g Cu (136%). The total energy content in the whole plantation biomass in March was estimated. The results show that the March harvest of MO (705 trees) total estimated leaf biomass yield would supply a one day proper calorie intake to 340 adult people (irrespective of gender according to Berkum et al. 2017 who state the daily per capita supply of calories in Ethiopia to be 2,131 kcal), while MS (705 trees) would supply only 123 people. It seems that significantly low carbohydrates content could be the main reason. Counted with the same values, MO total estimated leaf biomass yield from 1 ha would supply a one day proper calorie intake for 3213 adult people, while MS would supply 1159 people. A compositional study of M. stenopetala leaves by Abuye et al. (2004) found slightly different energy content in comparison with our M. oleifera analysis.
7
5. Conclusion Moringa oleifera and Moringa stenopetala are two of five species in the genus Moringa that can be found in Ethiopia and two of four edible species in the genus. M. oleifera is not native to this area; however, for its abundant expansion in the world, it is definitely the most well-known species of the whole genus. Due to its drought resistance, its ability to absorb extremely high levels of CO2, its ability to improve soil quality and the exceptionally high content of substances necessary for our health, this fast-growing tree is often grown on plantations. The aim of this work was to evaluate the possibility of cultivating Moringa oleifera and Moringa stenopetala species on intensive plantations in southern Ethiopia. Processed data on leaf biomass production from the plantation favours Moringa oleifera. Not only was the yield considerably higher, but this species, based on field observation, is more resistant to pests and diseases in southern Ethiopian conditions. A plantation counting 705 of M. oleifera and 705 of M. stenopetala trees with a 1 £ 1.5 m current spacing shows a higher yield of leaf biomass than expected yield if the spacing were changed to 3 £ 3 m. However, the wider spacing could have a positive impact on the reduction of pests and diseases that have been identified on trees and would most likely reduce the occurrence of powdery mildew. The nutritional value of both species was compared. The source of the data was, in the case of both species, from our own analyses. In general, most of the values did not differ between the species. Declaration of Competing Interest None. Acknowledgement This study was supported by the Czech Development Agency within project nr. 02/2016/03 “Implementation of holistic management and Climate Smart Agriculture in the Baso River catchment, Arba Minch Zuria Woreda, SNNPR, Ethiopia”, and project nr. PP2018-051-SO-25010 “Application of the economic and social potential of innovated products from moringa in Ethiopia”. References Abuye, C., Urga, K., Knapp, H., Selmar, D., Omwega, A.M., Imungi, J.K., Winterhalter, P., 2004. A compositional study of Moringa stenopetala leaves. East African Medical Journal 80 (5). https://doi.org/10.4314/eamj.v80i5.8695. Amaglo, N., Bennett, R.N., Lo Curto, R., Rosa, E., Lo Turco, V., Giuffrida, A., Lo Curto, A., Crea, F., Timpo, G.M., 2010. Profiling selected phytochemicals and nutrients in different tissues of the multipurpose tree Moringa oleifera L., grown in Ghana. Food Chemistry 122 (4), 1047–1054. https://doi.org/10.1016/j.foodchem.2010.03.073. Ashfaq, M., Basra, S.M.A., Ashfaq, U., 2012. Moringa: a miracle plant of agro-forestry. Journal of Agriculture and Social Science 8, 115–122. Aynalem, A.E., 2008. Moringa Stenopetala Seed Oil As a Potential Feedstock For Biodiesel Production in Ethiopia. Addis Ababa University, Ethiopia M. Sc. thesis. Bartikova, et al.Causal agents of powdery mildew on Moringa stenopetala (Baker f.) cuf. and Moringa oleifera lam. in Ethiopia (submitted to South African Journal of Botany). Basra, S.M.A., Nouman, W., Rehman, H.U., Usman, M., Nazli, Z.H., 2015. Biomass production and nutritional composition of Moringa oleifera under different cutting frequencies and planting spacings. International Journal of Agriculture & Biology 17 (5), 1055–1060. Bedane, T.M., Singh, S.K., Selvaraj, T., Negeri, M., 2013. Distribution and damage status of Moringa moth (Noorda blitealis walker) on Moringa stenopetala baker (Cufod.) in southern rift valley of Ethiopia. International Journal of Agricultural Technology 9 (4), 963–985. Berkum, S. van, Achterbosch, T.J., Linderhof, V.G.M., 2017. Dynamics of food systems in Sub-Saharan Africa; Implications for consumption patterns and farmers’ position in food supply chains. Wageningen, Wageningen Economic Research, Report 2017-072. 42 pp. Boukandoul, S., Casal, S., Zaidi, F., 2018. The potential of some Moringa species for seed oil production: a review. Agriculture 8 (150), 1–13. Climate-data.org, 2018[online], cited on March 29th, Available at: https://en.climatedata.org/location/3066/
mec et al., Biomass production of a young plantation of Moringa stenopetala (Baker f.) Cufod. and Moringa Please cite this article as: P. Ne oleifera Lam. in southern Ethiopia, South African Journal of Botany (2020), https://doi.org/10.1016/j.sajb.2020.01.018
JID: SAJB 8
ARTICLE IN PRESS
[m5G;January 28, 2020;10:32]
P. Nemec et al. / South African Journal of Botany 00 (2020) 18
Debela, E., Tolera, A., 2013. Nutritive value of botanical fractions of Moringa oleifera and Moringa stenopetala grown in the mid-Rift valley of southern Ethiopia. Agroforestry Systems 2013 (87), 1147–1155. https://doi.org/10.1007/s10457-013-9626-9. Edward, E., Chamshama, S.A.O., Ngaga, Y.M., Mndolwa, M.A., 2014. Survival, growth and biomass production of Moringa oleifera provenances at Gairo inland plateau and Ruvu coastal region in Tanzania. African Journal of Plant Science 8 (1), 54–64. https://doi.org/10.5897/AJPS12.158. Gebregiorgis, F., Negesse, T., Nurfeta, A., 2012. Feed intake and utilization in sheep fed graded levels of dried Moringa (Moringa stenopetala) leaf as a supplement to Rhodes grass hay. Tropical Animal Health and Production 44 (3), 511–517. https://doi. org/10.1007/s11250-011-9927-9. Gengelbach, G.P., Ward, J.D., Spears, J.W., 1994. Effect of dietary copper, iron, and molybdenum on growth and copper status of beef cows and calves. Journal of Animal Science 72 (10), 2722–2727. Isah, A.D., Bello, A.G., Zarumaye, S.A., 2014. Effects of cutting heights and interval of cutting on the yield of Moringa oleifera (horse raddish). International Journal of Development and Sustainability 3 (5), 1147–1151. Habtemariam, S., 2016. The African moringa is to change the lives of millions in Ethiopia and far beyond. Asian Pacific Journal of Tropical Biomedicine 6 (4), 355–356 April 2016. Kumssa, D.B., Joy, E.J.M., Young, S.D., Odee, D.W., Ander, E.L., Broadley, M.R., 2017. Variation in the mineral element concentration of Moringa oleifera lam. and M. stenopetala (Bak. f.) cuf.: Role in human nutrition. PLoS ONE 12 (4), e0175503. https://doi. org/10.1371/journal.pone.0175503. Lijesh, K.P., Malhotra, R., 2016. Reduction of turbidity of water using Moringa oleifera. International Journal of Applied Engineering Research 11 (2), 1414–1423. Mabapa, M.P., Ayisi, K.K., Mariga, I.K., 2017. Effect of planting density and harvest interval on the leaf yield and quality of moringa (Moringa oleifera) under diverse agroecological conditions of northern South Africa. International Journal of Agronomy 2017, 9. https://doi.org/10.1155/2017/2941432 Article ID 2941432. Melesse, A., Tiruneh, W., Negesse, T., 2011. Effects of feeding Moringa stenopetala leaf meal on nutrient intake and growth performance of Rhode Island red chicks under tropical climate. Tropical and Subtropical Agroecosystems 14, 485–492. Melesse, A., Steingass, H., Boguhn, J., Schollenberger, M., Rodehutscord, M., 2012. Effects of elevation and season on nutrient composition of leaves and green pods of Moringa stenopetala and Moringa oleifera. Agroforestry Systems 86 (3), 505–518. https://doi.org/10.1007/s10457-012-9514-8. Mofijur, M., Masjuki, H.H., Kalam, M.A., Atabani, A.E., Fattah, I.M.R., Mobarak, H.M., 2014. Comparative evaluation of performance and emission characteristics of Moringa oleifera and palm oil based biodiesel in a diesel engine. Industrial Crops and Products 53, 78–84. https://doi.org/10.1016/j.indcrop.2013.12.011. Nouman, W., Siddiqui, M.T., Basra, S.M.A., Farooq, H., Zubair, M., Gull, T., 2013. 2013. Biomass production and nutritional quality of Moringa oleifera as a field crop. Turkish Journal of Agriculture and Forestry 37, 410–419. https://doi.org/10.3906/ tar-1206-29.
Olson, M.E., Sankaran, R.P., Fahey, J.W., Grusak, M.A., Odee, D., Nouman, W., 2016. Leaf protein and mineral concentrations across the “Miracle tree. Genus Moringa. PLoS ONE 11 (7), e0159782. https://doi.org/10.1371/journal.pone.0159782. Olson, M.E., 2017. Moringa frequently asked questions. In: Ebert, A.W., Palada, M.C. (Eds.), Proceedings of the First International Symposium on Moringa. Acta Horticulturae 1158. ISHS 2017, pp. 19–32. https://doi.org/10.17660/ActaHortic.2017.1158.4. Olson, M.E., 2002. Combining data from dna sequences and morphology for a phylogeny of Moringaceae (Brassicales). Systematic Botany 27, 55–73. Patricio, H.G., Palada, M.C., Deloso, H.E., Garcia, D.E., 2017. Biomass yield of Moringa oleifera as influenced by plant density and harvest frequency. In: Ebert, A.W., Palada, M.C. (Eds.), Proceedings of the First International Symposium on Moringa. Acta Horticulturae 1158, pp. 97–104. € ppenPeel, M.C., Finlayson, B.L., McMahon, T.A., 2007. Updated world map of the Ko Geiger climate classification. Hydrology and Earth System Sciences Discussions 4 (2), 439–473. Pontailler, J.Y., Ceulemans, R., Guittet, J., Maum, F., 1997. Linear and non-linear functions of volume index to estimate woody biomass in high density young poplar stands. Annals of Forest Sciences 54 (4), 335–345. https://doi.org/10.1051/forest:19970402. , C., 1985. Biomass production by alders on four abandoned agricultural Pregent, G., Camire bec. In: Lalonde, M., Camire , C., Dawson, J.O. (Eds.), Frankia and Actinorhisoils in Que zal Plants. Developments in Plant and Soil Sciences, Vol 18. Springer, Dordrecht. Sanchez, N.R., Ledin, S., Ledin, I., 2006. 2006. Biomass production and chemical composition of Moringa oleifera under different management regimes in Nicaragua. Agroforestry Systems 66, 231–242. Samuel, D., Terefe, R., Senbeto, M., Daba, M., 2016. Evaluation of two Moringa species for adaptability and growth performance under Bako conditions. Journal of Natural Sciences Research 6 (9), 76–82 ISSN 2224-3186. Schneemann, J., 2011. Moringa (stenopetala) Production and Use For Water Purification in Ethiopia. Fair and Sustainable Advisory Service. Utrecht, The Netherlands. Seifu, E., 2014. Actual and potential applications of moringa stenopetala, underutilized indigenous vegetable of southern Ethiopia: a review. International Journal of Agricultural and Food Research 3, 8–19. Sanjay, P., Dwivedi, K.N., 2015. Shingru (Moringa oleifera lam.): A critical review. International Journal of Ayurveda and Pharmaceutical Chemistry 3 (1), 217–227. n-Escalante, I.E., Zepeda-Bautista, R., Jime nez-Arellanes, M.A., Velazquez-Zavala, M., Peo 2016. Moringa (Moringa oleifera lam.): potential uses in agriculture, industry and medicine. Revista Chapingo Serie Horticultura 22 (2), 95–116. https://doi.org/ 10.5154/r.rchsh.2015.07.018. Yisehak, K., Solomon, M., Tadelle, M., 2011. Contribution of Moringa (Moringa stenopetala, bac.) a highly nutritious vegetable tree, for food security in south Ethiopia: A review. Asian Journal of Applied Sciences 4 (5), 477–488 ISSN 1996-3343.
mec et al., Biomass production of a young plantation of Moringa stenopetala (Baker f.) Cufod. and Moringa Please cite this article as: P. Ne oleifera Lam. in southern Ethiopia, South African Journal of Botany (2020), https://doi.org/10.1016/j.sajb.2020.01.018