Journal of Applied Botany and Food Quality 91, 219 - 225 (2018), DOI:10.5073/JABFQ.2018.091.029 1 Department of Plant Production, Soil Science and Agricultural Engineering, School of Agricultural and Environmental Science, University of Limpopo, South Africa 2 Risk and Vulnerability Science Centre (RVSC), University of Limpopo, South Africa Seasonal effect on Moringa oleifera gaseous exchange and water use efficiency under diverse planting densities Moshibudi Paulina Mabapa1,2,*, Kwabena Kingsley Ayisi2, Irvine Kwaramba Mariga1 (Submitted: May 21, 2018; Accepted: July 21, 2018) * Corresponding author Summary The study on Moringa oleifera was conducted over twelve months during 2014 -2015 to evaluate the impact of the growing season and varying planting densities on biomass yield and physiological at- tributes under dryland conditions. Trial was established at densities of 5000, 2500, 1667 and 1250 plants ha-1, with eight replicates. The increase in planting density led to an increase in biomass production. The monthly and seasonal data collected showed significant differ- ences in net photosynthetic rate, transpiration, sub-stomatal CO2 and stomatal conductance. However, planting densities of M. oleifera had no significant effect on all the gaseous exchange parameters mea- sured. The results further revealed that the amount of carbon dioxide assimilated by the tree is not attributable to photosynthetic and tran- spiration rates as well as stomatal conductance. Under water shortage condition and high temperature, M. oleifera used an adaptation stra- tegy by reducing stomatal conductance and transpiration and hence increasing water use efficiency. Moringa oleifera thus has the ability to sequester carbon even under water stress conditions. The tree can therefore be recommended for planting at a relatively high density of 5000 plants ha-1 in many parts of Limpopo province where tempera- tures are favorable for improved farmers’ livelihoods as well as for climate change mitigation. Keywords: Biomass; climate change; monthly; Moringa oleifera; physiological response; planting density Introduction Moringa oleifera is a highly valued tree that is widely distributed in many countries of the tropics and subtropics. It is considered as one of the most useful trees, since almost every part of the tree is a valu- able source of food, medication and industrial purposes (Morton, 1991; Foidl et al., 2001). Moringa oleifera is a fast growing plant tolerant to harsh climatic and environmental conditions where many agricultural plants would not survive, requiring only 400 mm of annual rainfall (Morton, 1991; reyes-sánchez, 2006; Pandey et al., 2011). Moringa oleifera trees can play a significant role in miti- gating adverse effects of climate change, due to its ability to capture carbon (DABA, 2016). It also has the potential to improve the income and livelihood of smallholder farmers as well as nutritional needs of rural communities (MabaPa et al., 2017; babu, 2000; Moyo et al., 2011). Through observations, South Africa and other countries globally are already affected by severe negative consequences of climate change. This is particularly evident in the smallholder farming sector that relies on natural resources for production. Best practices of agricul- ture can contribute towards climate change mitigation and adapta- tion by adopting various agricultural management practices that could minimize adverse effects of unpredictable rainfall patterns as well as other extreme weather conditions (hulMe, 2005; Pareek, 2017). Pareek (2017) reported that various agricultural adaptation management practices are available to attenuate the effects of cli- mate change on crop production. This include broader agronomic management strategies such as altering planting densities, row spac- ing, planting time as well as introducing new germplasms that are resistant to heat and drought stress. There is no information on lit- erature regarding carbon sequestration through M. oleifera trees as influenced by varying plant densities in the South African context. It is known from the literature that M. oleifera has been described as a tree that can be grown in the drier ecological zones (asante et al., 2014; seresinhe and MaraPana, 2011). However, no quantita- tive information is available in South Africa about the M. oleifera’s gaseous exchange response such as stomatal conductance, stomatal CO2, transpiration and photosynthetic rate to planting density over the different seasons. This study was therefore established to evalu- ate the seasonal response of M. oleifera in terms of biomass yield and gaseous exchange under varying planting densities as a contribution towards climate change mitigation. Materials and methods Study location The study was conducted over twelve months to cater for four sea- sons, summer (December - February), autumn (March - May), winter (June - August) and spring (September - November) during 2014 – 2015, at NTL Baraka Eco-Farming Organic Farm (23°57.691’S and 30°35.205’E), situated in Eiland. The farm is situated about 50 km on the eastern side of Tzaneen in the Limpopo province. The area is a tropical region and receives about 429 mm of rain per annum, with most rainfall occurring during mid-summer. The annual rainfall data were derived from the total monthly values for Eiland averaged in the past 7 years. The area received the lowest average rainfall (<0.5mm) in June and July; the highest in December and January of more than 120 mm in the past 7 years. The monthly temperature distribution shows that, the average maximum monthly temperatures for Eiland could rise above 31 °C, while minimum temperatures could range between 7 to 25 °C, during winter and summer seasons, respectively. Experimental design, planting and management A 60 m length and 40 m breadth demarcated area was prepared by conventional tillage using disk ploughing, followed by two disk harrowing and manual digging of shallow holes for planting. The experiment was laid out in a two factor (months and plant spac- ing) factorial Randomized Complete Block Design (RCBD) with eight replicates. The blocks were divided into four plots where treat- ments were placed. The treatments consisted of 12 months: May’14, June’14, July’14, August’14, September’14, October’14, November’14, December’14, January’15, February’15, March’15 and April’15 as well as four levels of intra-row spacing: D1= 1 m, D2= 2 m, D3= 3 m and D4= 4 m, with a uniform inter-row spacing of 2 m, giving total populations of 5000, 2500, 1667 and 1250 plants ha-1, respectively. 220 M.P. Mabapa, K. Kingsley Ayisi, I. Kwaramba Mariga Untreated seeds of M. oleifera were used for planting by placing 2 seeds per hole at a depth of 2 cm during December 2013. Each plot measured 4 m × 12 m and plots were separated from each other by 2 meters walkways. Irrigation was applied for four hours twice a week using a micro jet irrigation system until the tenth week to encourage good tree establishment, after which the study was al- lowed to run under rainfed conditions. Eight weeks after trial es- tablishment, plants were thinned out to the right densities, retaining only the healthier plants during the thinning process. Prior to data collection, the whole experiment was uniformly cut at a height of 50 cm aboveground and all foliage was removed but not weighed. Leaf gaseous exchange and water use efficiency measurements Leaf gaseous exchange measurements were measured monthly on a fully-expanded leaf on the abaxial side of three selected leaves per experimental unit, using a portable photosynthesis system (ADC Bio Scientific, UK). Monthly measurements were averaged for each season to come up with seasonal data. The photosynthetic rate (A), stomatal conductance (gs), transpiration rate (E) and sub-stomatal CO2 (Ci) were simultaneously determined for each species using a non-destructive method. All the measurements were carried out under steady-state conditions in full sun between 10:00 am and 14:00 pm (cliFFord et al., 1997). The instantaneous water use ef- ficiency (WUE) which is defined as the ratio of photosynthetic capa- city to the rate of transpiration was calculated for each density as A/E (Field et al., 1983; rivas et al., 2013). Plant Biomass determination Leaf biomass was collected once from a net plot of 12 m2 during harvesting in April 2015. The leaf yield (kg) was determined by separating the leaves from the petiole. The fresh leaf biomass was shade-dried at room temperature for 72 hours and later weighed us- ing a battery-operated top loading weighing balance (RADWAG, W/ C6/12/C1/R Model). Statistical analysis Data were subjected to analysis of variance using Statistix 10.0 to compare the response of M. oleifera planting density on measured variables. A significance level of p<0.05 was used for determining differences among the interaction of months and plant spacing on leaf gaseous exchange and water use efficiency. The differences among the obtained mean values of measured parameters were compared and computed by using Tukey’s HSD test considering 5% probability level (GoMez and GoMez, 1996). Where significant F-values from density treatment effects were observed on biomass yield, means were separated by Least Significant Difference (LSD) at probability level of 0.05 (GoMez and GoMez, 1996). Correlation and regression analyses were performed using both Statistix 10.0 and Microsoft Excel, to determine the relationship between gaseous exchanges. Results Weather parameters of the study area Data on weather parameters measured during the study and anomaly in rainfall distribution are presented in Tab. 1 and Fig. 1. Rainfall dropped during summer season (November - February) of 2014/15, whereby the rainfall was below 100 mm as compared to the past two years during which the amount exceeded 200 mm. The temperatures Fig. 1: Total monthly rainfall (mm), average maximum (Tx) and minimum (Tn) temperatures collected at Eiland from during the production seasons. Tab. 1: Total monthly rainfall (mm), mean minimum and maximum tempera- tures recorded between May 2014 and April 2015 at the study site. Month/Year Total monthly Min Temp Max Temp rainfall (mm) (oC) May’14 0.00 10.29 28.06 June’14 0.00 6.29 26.23 July’14 0.51 6.19 24.79 August’14 8.38 8.31 26.41 September’14 0.51 12.37 30.15 October’14 25.91 15.26 29.48 November’14 13.97 18.99 30.39 December’14 95.49 20.40 30.94 January’15 17.26 21.39 31.91 February’15 99.31 21.06 32.41 March’15 12.18 19.37 32.47 April’15 41.15 16.65 29.42 Gaseous exchange and water use efficiency of Moringa oleifera 221 Tab. 2: Leaf gaseous exchange parameters and instantaneous water use efficiency of M. oleifera as influenced by month and planting density. Treatments/Factor Transpiration rate (E) Stomatal conductance (gs) Photosynthetic rate (A) Sub-stomatal CO2 (Ci) WUE inst mmol m-2 s-1 mol m-2 s-1 μmol m-2 s-1 vpm μmol mol-1 Month/Year May’14 2.88abc 0.15b 6.73bc 276.91ab 2.33cde June’14 3.49a 0.09d 6.73bc 220.75bcd 1.91de July’14 2.53bc 0.07de 10.65a 133.38f 4.37a August’14 2.46bc 0.07de 9.04ab 152.12ef 3.72ab September’14 3.14ab 0.05fg 4.31cde 246.22abcd 1.29e October’14 2.10cd 0.19a 8.96ab 270.41abc 4.29a November’14 2.19cd 0.05ef 5.54cd 190.81def 2.68bcd December’14 2.65abc 0.07de 5.85cd 207.31cde 2.38bcde January’15 1.47de 0.03g 3.46de 195.53def 3.40abc February’15 1.06e 0.04fg 1.76e 297.03a 2.16cde March’15 3.28ab 0.13c 8.98ab 229.03bcd 2.55bcde April’15 1.39de 0.06ef 4.667cde 215.50bcde 4.2659a Significance *** *** *** *** *** Density (Plants ha-1) 5000 2.29 0.08 6.57 221.75 3.24 2500 2.51 0.09 6.30 224.69 2.71 1667 2.30 0.08 6.09 213.10 2.83 1250 2.46 0.09 6.60 218.79 3.00 Significance ns ns ns ns ns Interaction (Month × Density) Significance levels: *P<0.05, ** P<0.01, *** P<0.05, ns: not significant. Means with different letters are statistically significant. increased during summer season with the maximum temperature exceeding 32 oC (Fig. 1). The drought that was experienced during 2015 had a significant influence on rainfall anomaly. The accelerated heat accompanied by moisture deficit led to below average rainfall anomaly mainly during the year 2015 as compared with the years 2013 and 2014, in which the rainfall anomaly was above average in many instances, mainly during the rainy season (Fig. 2). Monthly gaseous exchange and water use efficiency of M. oleifera as influenced by planting density The monthly data collected showed highly significant differences in all gaseous exchange parameters and water use efficiency (Tab. 2). However, planting density of M. oleifera had no effect on photo- synthetic rate, transpiration rate, sub-stomatal CO2 and stomatal con- ductance as well as water use efficiency (Tab. 2). Fig. 2: Rainfall (mm) anomaly at Eiland as compared to long term average rainfall from 2009 to 2015. ns ns ns ns ns 222 M.P. Mabapa, K. Kingsley Ayisi, I. Kwaramba Mariga Seasonal effect on M. oleifera gaseous exchange The seasonal effect significantly influenced all the measured gaseous exchange parameters (Fig. 3). Photosynthetic rate, stomatal conduc- tance and transpiration rate were reduced during summer season, whilst the sub-stomatal CO2 concentration increased during the same season. Furthermore, the photosynthetic rate and stomatal conduc- tance were higher during winter season when temperatures were low. No significant differences in transpiration were found during winter, autumn and spring seasons, while sub-stomatal CO2 was found not to change during the three seasons except in the winter season. Correlations and regression of M. oleifera gaseous exchange parameters Seasonal relationships between gaseous exchange are presented in Fig. 4. Transpiration rate and photosynthetic rate showed a strong positive relationship. A similar relationship was observed between stomatal conductance and photosynthetic rate as well as between stomatal conductance and transpiration rate (Fig. 4). However, sub- stomatal CO2 had a negative relationship with photosynthetic rate, transpiration rate and stomatal conductance. Biomass production of M. oleifera as influenced by planting density Tab. 3 shows the effect of planting density on biomass production at harvest in April 2015. The planting density had a significant influ- ence on both total and leaf biomass yields, where increasing planting density led to an increase in biomass yield. Leaf and total biomass yields had no significant difference at the densities of 1667 and 1250 plants ha-1. Leaf biomass yield increased by 118.1 and 63.0 kg ha-1 at densities 5 000 and 2500 plants ha-1, respectively, relative to a popu- lation of 1250 plants ha-1. On the other hand, total biomass yield in- creased by 93.2 and 55.5 kg ha-1 at densities 5000 and 2500 plants ha-1, respectively relative to a population of 1250 plants ha-1. Discussion Weather parameters of the study area During data collection between 2014 and 2015, the study area expe- rienced extreme drought and high temperatures. A total rainfall of 432 mm was received during this period. It was observed from the 2014 and 2015 summer season, that Eiland received below average rainfall with the situation worsening during 2015 where the rainfall anomaly was greater than 100 mm below average. These data show the magnitude of abiotic stress experienced in the study area. Study by anjuM et al. (2011), reported that environmental abiotic stresses, mainly drought, salinity and extreme temperatures could impair plant growth and development and as such limit the productivity of many agricultural crops. Monthly gaseous exchange and water use efficiency of M. oleifera as influenced by planting density The effect of planting density on gaseous exchange was not signifi- cant during the study period. However, there was noticeable signifi- cant effect on monthly gaseous exchange parameters. This might be due to variable monthly temperatures and rainfall which influenced Fig. 3: (A) Photosynthetic rate (A), (B) Transpiration rate (E), (C) Sub-stomatal CO2 (Ci) and (D) Stomatal conductance (gs) as affected by season irrespective of planting density. Means with different letters are statistically significant. Gaseous exchange and water use efficiency of Moringa oleifera 223 the response of M. oleifera trees. Findings from this study revealed the survival mechanism utilized by M. oleifera to tolerate harsh en- vironmental and climatic conditions. It was observed that M. oleifera does not rely on moisture from immediate rainfall; instead, the tree absorbs and stores water within the roots and other succulent tissues to utilize it when there is water deficit in the soil. This was evident because when rainfall was low or in deficit, M. oleifera still exhi- bited high transpiration rate which was influenced by high tempera- ture. However, when temperature continues to rise under moisture shortage, M. oleifera showed adaptation strategy by also reducing the transpiration rate. These results concur with findings by rivas et al. (2013) who reported that M. oleifera can maintain a high leaf relative water content (RWC) under low soil moisture which helps to maintain cellular physiological processes and growth. Another study conducted on drought resistant bread wheat cultivars showed that, under drought stress conditions, the cultivars had more RWC (keyvan, 2010). Fig. 4: Seasonal linear regression for M. oleifera gaseous exchanges. Tab. 3: Biomass yield (kg. ha -1) production of M. oleifera under different densities at Eiland during the harvest in April 2015. Density Dry leaf yield Total dry biomass yield (Plants ha-1) (kg ha-1) (kg ha-1) 5000 447.91a 1250.6a 2500 338.80b 1006.6ab 1667 263.13bc 805.2bc 1250 205.33c 647.3c P value 0.000 0.001 CV% 23.79 28.18 Significance (0.05) ** ** Significance levels: *P<0.05, ** P<0.01, *** P<0.05, ns: not significant. Means with different letters are statistically significant. 224 M.P. Mabapa, K. Kingsley Ayisi, I. Kwaramba Mariga Plants use several physiological mechanisms that contribute to their drought tolerance. The first mechanism utilized by most plants, is through decreased stomatal conductance. When the resistance to H2O is greater than that to CO2, there is an increase in the water use efficiency (rivas et al., 2013; Galle et al., 2011). Photosynthetic rate was reduced when there was water deficit in the soil and the plant itself and these response negatively affected water use efficiency (Tab. 1). Low moisture experienced until November 2014 and in January 2015 with increased temperature decreased stomatal con- ductance, photosynthetic rate and the extent of sub-stomatal CO2. Gaseous exchange activities, mainly photosynthetic rate, are among the primary processes to be negatively affected by drought and high- er temperatures (chaves, 1991). Similar findings were reported by Frosi et al. (2017) on the response of two tropical evergreen species to drought stress. They found that gaseous exchange under severe drought stress showed a significant decrease with the average val- ues of 0.01 (mol m-2s-1), 0.66 (mmol m-2s-1) and 0.4 (mmol m-2s-1) for stomatal conductance, photosynthetic rate and transpiration rate, respectively. rivas et al. (2013) also reported a drop in gaseous exchange due to water stress as compared to irrigated M. oleifera plants. When plants encounter water deficit, they respond by lower- ing stomatal conductance in order to reduce water loss which eventu- ally results in decreased photosynthetic rate (Munjonji et al., 2016). Seasonal effect on M. oleifera as influenced by gaseous exchange This study revealed a significant influence of season on gaseous exchange of M. oleifera. The higher temperatures that were expe- rienced during summer led to a decrease in photosynthetic rate, stomatal conductance, transpiration rate, while lower temperatures decreased the concentration of sub-stomatal CO2. Under mild water stress, plants showed small decline in stomatal conductance which is a protective mechanism against stress, by allowing water saving and improving plant water use efficiency (chaves et al., 2009). Water use efficiency increased in stressed plants compared to irrigated M. oleifera plants. However, overtime, a rapid recovery from stress was observed on rehydrated plants through increased stomatal conduc- tance (gs), net CO2 assimilation (Pn), transpiration (E) and decreased water use efficiency (rivas et al., 2013). A nursery study on irrigation interval revealed that irrigating M. oleifera seedlings at 8 days interval had a negative effect on gas- eous exchange; however, the internal CO2 concentration displayed significantly higher values as compared to shorter intervals (WaFa, 2015). The long taproot of M. oleifera and its succulent tubers en- hances the drought resistance properties of the tree (jaGadheesan et al., 2011). Succulent plants often resist moderate water stress by storing water in their succulent tissues and utilizes it during the drought stress period (jaGadheesan et al., 2011). Findings from this study showed that higher temperature favored as- similation of carbon dioxide by M. oleifera tree (Tab. 1). Results from current study concur with findings by ndubuaku et al. (2014) who reported that the higher rate of sub-stomatal CO2 concentration is an indication that M. oleifera is able to partition carbon into different parts of the plants. No literature is available on seasonal effect of M. oleifera on gas- eous exchange. However, results from this study showed that higher temperatures, which prevail mainly in summer months, had a nega- tive effect on transpiration, photosynthetic rate and stomatal conduc- tance, but favored the accumulation of carbon dioxide in three out of four seasons of the year. During winter season, there was an excessive leaf fall and less soil moisture and this significantly affected carbon assimilation and plant growth. Under water stress conditions, plants generally produce a lower number of leaves, with general reduction in their size (jaGadheesan et al., 2011). Muhl et al. (2011) conclu- ded that higher temperatures favor growth of M. oleifera, while low temperature leads to thickening of leaves which is symptomatic of an adaptation against temperature stress, resulting in reduced growth. Furthermore, jaGadheesan et al. (2011), reported that M. oleifera is sensitive to prolonged water stress which may result in a prominent decrease in cellular growth. Nevertheless, the tree is still able to pro- duce satisfactory yields and high nutritional content from the leaves under such condition. Correlation of M. oleifera gaseous exchange parameters The findings from this study showed a strong positive relationship between photosynthetic rate and transpiration rate as well as stoma- tal conductance. Sub-stomatal CO2 showed a moderate to weak nega- tive relationship with photosynthetic and transpiration rates as well as stomatal conductance. Therefore, the amount of carbon dioxide assimilated by the tree cannot be determined by photosynthetic rate and transpiration rate as well as its stomatal conductance. The results from this study are in line with findings by araújo et al. (2016), who reported that the impairment of net CO2 assimilation rate cannot be attributed to stomatal effects, since stresses did not reduce the inter- cellular CO2 availability. This study further showed a positive relationship between measured stomatal conductance and photosynthetic rate, whereby, the increase in stomatal conductance led to an increase in photosynthetic rate. This relation was mainly influenced by higher temperature and stored moisture in the plant. Similar results were reported by Muhl et al. (2011) who found out that the reduction in leaf stomatal conduc- tance leads to a decrease in net photosynthetic rate. A study by rivas et al. (2013), further reported that M. oleifera can maintain high leaf relative water content even under drought stress and this helps the plant to maintain physiological processes and growth. Leaf biomass production of M. oleifera as influenced by planting density The effect of planting density on biomass was evident whereby the highest planting density of 5000 plants ha-1 produced the highest total leaf dry biomass yield of 1251kg ha-1, with the leaf biomass yield of 448kg ha-1, relative to lower planting densities of 2500, 1667 and 1250 plants ha-1. Several authors have reported similar findings, where increase in planting density led to an increase in dry matter yield (Foidl et al., 2001; sánchez et al., 2006; basra et al., 2015). Planting density of 250 000 and 500 000 plants ha-1 established un- der dryland conditions had a total dry matter yield of 7.6 and 8.1 tons ha-1, with leaf yield of 4.6 and 4.9 tons ha-1 (sánchez et al., 2006). Conclusions In conclusion, this study showed that M. oleifera can survive harsh climatic and environmental conditions such as high temperatures and moisture deficit which commonly occur under the tropical climates. The study further revealed that planting density has no influence on various gaseous exchange parameters of M. oleifera tree. Under soil water deficit and high temperature, M. oleifera uses an adaptation strategy by reducing stomatal conductance and transpiration, there- by increasing the water use efficiency. The results also revealed that M. oleifera plant has the ability to sequester more carbon in its succu- lent parts throughout the growing seasons. Therefore, M. oleifera can be recommended for planting at a higher density of 5000 plants ha-1 in many parts of Limpopo province that experiences high tempera- tures, as the potential crop to contribute to climate change mitigation and nutritional security given its many nutritional attributes. 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WAFA, E.A.A., 2015: Effect of irrigation interval on physiological and growth parameters of Moringa oleifera and Moringa peregrina seedlings [Masters Dissertation, University of Khartoum (UOFK)]. Address of the author: University of Limpopo, Private Bag X1106, Sovenga, 0727 E-mail: paulina.mabapa@ul.ac.za © The Author(s) 2018. This is an Open Access article distributed under the terms of the Creative Commons Attribution Share-Alike License (http://creative- commons.org/licenses/by-sa/4.0/).