Weicheng Li?Haiyan Sheng

Introduction

Bamboos,as a resource,are abundant and widely distributed throughout the world,consisting of approximately 70 genera and more than 2000 species.The genera exhibit several benefits such as rapid growth rates,rapid afforestation,and short rotation times(Zhang et al.1994).However,only 5%of bamboo species are currently utilized in the world,and most of them are at an early stage of research and development(Li et al.2009).Wine bamboo,Oxytenanthera abyssinica A.Rich.(Munro),is native to Tanzania where local farmers consider it an economically important species.Since the sap from the young stalks can be naturally fermented into low alcohol-content beverages rich in nutrients(Liese 1992),the government has developed and utilized this naturally fermented sap and protected the O.abyssinica resources(Ibeh et al.2013).Preliminary experiments on species protection and expanding cultivation have also been conducted here in China(Liese 1992;Ibeh et al.2013).Countries like India and the United States report introducing this species in the 1970s and 1980s(Mgheni 1983;Roy 2005).

In China,the introduction of wine bamboo has enriched the bamboo gene pool.In addition,the mountain-cultivated bamboo ensures increased revenue for the farmer.Previous studies(Roy 2005;Li et al.2009)have shown that wine bamboo shoots are high in nutrients,low in fat and starch,and high in crude fiber.They are rich in sugar with the total sugar content ranging 2.65–3.07%,significantly higher than that of the shoots of the sympodial bamboo Dendrocalamus brandisii(Munro)Kurz.The tannin content is 0.032–0.038%,far less than that of the shoots of most monopodial bamboos.Therefore,wine bamboo shows tremendous potential to be developed into green food.

Currently,healthy beverages that are beneficial,natural,and green are in demand.Wine bamboo stalks secrete large amounts of sap(fresh bamboo juice)after cutting.Due to root pressures,the sap overflows from the wounded or fractured plant tissues,producing fresh bamboo juice which is clear,transparent,and a safe and natural beverage.The southern provinces of China such as Guangdong,Yunnan,Hainan,and Guangxi have shown great interest in wine bamboo cultivation and in developing fresh juice products with prospects of a wide range of applications.Thus,studying the mechanism of wine bamboo sap production is imperative for improving silvicultural practices and management.

Studies have been conducted on the effects of biochar on nutrient availability(Xu et al.2013;Huang and Xue 2014),soil water and fertility retention(Yao et al.2012;Getachew et al.2015),soil microbial growth promotion(Marleena et al.2016),enhancement of soil carbon storage capacity(Homagain et al.2015),reduction of greenhouse gas emissions(Liu et al.2011;Getachew et al.2015;Zhang et al.2016),and improving crop yields(Chen et al.2013;Hussain et al.2016).Bamboo charcoal is a biochar produced by the pyrolysis of bamboo materials(Schmidt et al.2014).The morphological structure,nutrient composition,and growth characteristics of bamboo are different from other biomass materials,and therefore the charcoal has become a biochar with unique properties.The conditions of application of bamboo charcoal-based bio-fertilizer(hereinafter referred to as ‘bamboo charcoal fertilizer’)are well-developed(Xu et al.2013;Huang and Xue 2014;Getachew et al.2015).In this study,we analyze the changes in the amount of collected sap and nutrient composition under two cultivation conditions:with bamboo charcoal fertilizer and with organic fertilizer.We further examine the relationships to environmental parameters such as wind speeds,soil temperatures,soil water contents,air temperatures,and humidity,to develop a standard fertilization method and to provide efficient collection techniques suitable for wine bamboo cultivation on the southwest mountains in China.

Materials and methods

Study site

The experiment was located in Mojiang County,Yunnan Province,China(longitude,101°10′E;latitude,22°58′N;altitude,1600–1800 m),in the middle of the Ailao Mountains in southwest China.Due to the impact of the subtropical monsoon,differences in annual temperatures are small and the climate is not separated into four distinct seasons.However,the diurnal temperature range is large and the average annual temperature is 18.3°C with a maximum of 34.2 °C,≥ 10 °C;the accumulated temperature over the year is 6302.6°C.The total annual daylight hours are 2148.1,the average annual frost period is 15.3 days,and the frost-free period is 306 days.Rainfall is abundant and concentrated,with uneven annual distribution.The rainy and dry seasons are distinct,with the former occurring from May to October,and the dry season from November to April.Annual precipitation is 1338 mm,and annual evaporation is 1696.7 mm,slightly higher than the precipitation.Soils are mainly red soil and red earth soil(800–1500 m).Organic matter content was 11.2 mg g-1with a pH of 6.9.Total nitrogen was 0.72 mg g-1,total phosphorus was 0.27 mg g-1,and the cation exchange capacity was 11 cmol(+)kg-1.

Experimental design

Bamboo charcoal used in the experiment was prepared from residuals of bamboo processing under airtight conditions with low oxygen levels at 600°C,followed by sieving through a 100-mesh screen.The pH was maintained at 8.82–8.86;moisture content at 10.2–11.0%;and the surface area was 359 m2g-1(Huang et al.2014).Fine bran(ground rice husk passed through a 40-mesh sieve)for bamboo charcoal fertilizer and pig manure were obtained from an agricultural materials company and an intensive pig farm,respectively,in Jiaxing City,Zhejiang Province.Fine bran was mixed with composting materials to adjust for the C/N ratio and moisture content.Static pile composting with forced aeration combined with turning was used.The moisture content of the mixture was 57±5%after mixing the fine bran with pig manure.Mature compost was obtained after approximately 3 months of fermentation at 65–70 °C.The material properties were:N,11.9 wt%;P2O5,4.8 wt%;K2O,5.7 wt%;pH,8.13–8.50;electrical conductivity,5.47 mS cm-1;moisture content,30.5%;and C/N,14.7.Bamboo charcoal accounted for 35 wt%of the fertilizer.Bentonite was used as a binder for granulation and the prepared bamboo charcoal-based biomass fertilizer consisted of granules 1.2–1.5 mm in diameter.

Subsequent to soil preparation,a single application of phosphate(triple superphosphate;P2O5,52.7 kg ha-1)and potassium fertilizer(potassium sulfate;K2O,56.3 kg ha-1)was carried out in March 2010.Transplants were obtained from parent bamboo plants in May,with stalk diameters of 3–5 cm,stalk heights of 1–2 m,and the presence of 1–2 vegetative leaves.A randomized block design was used with two experimental sets:1.The bamboo charcoal fertilizer group (ZT) containing bamboo charcoal(35)+mature compost(57)+bentonite(8)and 4 kg granulated bamboo charcoal fertilizer in each hole;and,2.The control group CK containing no added charcoal+mature compost(57)+bentonite(8)and 2.6 kg granulated organic fertilizer in each hole.Five replicates of each treatment were set out,with the size of each hole 1.0 m×1.0 m,depth 0.5 m,and spacing between plants 5–6 m.Base fertilizer was added to each hole,covered with soil,followed by transplanting and watering.In June 2011,May 2012,April 2013,and May 2014,cyclic annular furrow application of fertilizer 30 cm away from the bamboo pouch was performed yearly.The ZT treatment consisted of a furrow application of 1.0 kg fertilizer,and the CK treatment a furrow application of 0.65 kg organic fertilizer,covered with soil.Until the end of the experiment in May 2015,no additional fertilizer was applied,and weeding was performed only after the rainy season.

Sap collection and measurement

Data for sap collection were recorded over two collection cycles from May 2013 to March 2015.Sap was collected on a sunny day(including during the rainy season)every month.An electronic drill was used to install a custommade sealed liquid receiver into a 1-to 2-year-old solid stalk(one in each clump),which was then connected to an external silicon tube and a container.Each collection took 48 h,and the wounds were subsequently covered with paraffin.In each cycle,sap collected in July was placed in a food-grade polyester sampling bag in an icebox and sent for measurement of nutritional elements,conventional nutritional composition,and amino acid content.Processing and analysis were performed within 24–48 h.

Five samples from each treatment were measured for mineral elements,total fat content,proteins,starch,reducing sugars,and yeast,and the differences between treatments were calculated.Free amino acids were measured with an automatic analyzer(Hitachi 835-50).

Concurrently,seven indicators:wind speed(SW),temperature(TA),humidity(MA),soil temperature at 5-cm depth(TS5),soil temperature at 15-cm depth(TS15),soil water at 0–5 cm depth(WS5),and soil water at 10–15 cm depth(WS15)were measured.TS5,TS15,WS5and WS15were used to determine whether there were relationships between the top soil layer and sap yield,or with deeper layers.Average monthly wind speed data from May 2013 to March 2015 were obtained from the weather station near the experimental site(distance 700 m)in Lianzhu Town,Mojiang County.A SATO digital thermohygrometer PC-6800 measured air temperatures and humidity 1.5 m above the ground and 1.5 m away from the wine bamboo clump.After removal of surface litter,a ZDR-41 temperature logger was used to measure soil temperatures at 5 and 15-cm depths and at 0.5 m periphery from the stalks(Zhao et al.2014).For soil water measurement,samples from two layers,0–5 cm(topsoil)and 10–15 cm(deeper soil)were collected in sampling bags,oven dried and weighed using an electronic balance(0.1 g readability).

Two-cycle average values of the above parameters were used to facilitate a comparison.Multiple linear regression(stepwise method)and factor analysis analyzed the effects of the environmental parameters on the amount of sap collected(CSap)(Li et al.2013).

Results

Annual change in the amount of wine bamboo sap and affecting factors

Under ZT conditions,sap was available from May to January,whereas under CK conditions,sap could only be collected in the rainy season(Fig.1).Differences in TAand MAbetween the ZT and CK groups were not significant(p＞0.05;Fig.2a,b).During the transition from dry to rainy seasons,SWweakened(Fig.2c)and TAand MAincreased.The amount of sap collected between the ZT and CK groups were not significantly different(p＞0.05)(Fig.1).The average amount of sap collected per stalk was low,and the mean values of the ZT group were higher than those of the CK group;this was mainly due to the transition from dry to rainy seasons when humidity and soil water were lower and there was a time lag in the response of plants to the change in seasons.In July(mid-rainy season),differences between the amounts of sap collected between the two groups were significant(p＜0.05).Further,in September,sap amounts of both ZT and CK groups reached a maximum level of the two cycles,they were 2.34±0.42 and 2.63±0.55 L stalk-1for ZT,and 1.28±0.20 and 1.23±0.60 L stalk-1for CK,respectively.The differences were highly significant(p＜0.01).The average amounts collected of the ZT group were 1.84 and 2.13 times higher than those of the CK group,respectively.From October to November(the dry season),SWincreased(Fig.2c),TAand MAbegan to decrease(Fig.2a,b),and sap collected rapidly declined.However,differences were still observed between the ZT and CK groups(p＜0.05).In the 2 cycles of CK,sap quantities were 0.019±0.003 and 0.242±0.101 L stalk-1in November,respectively.The average values in November for the ZT group were significantly higher than those for the CK group,with values 15 times and 4.45 times higher than those in the CK group,respectively.In the second cycle,however,the increase in sap collection of the CK group was significantly higher than in the ZT group;this may be attributed to the establishment of the wine bamboo forest which improved the microhabitat,increased plant growth and root activity required for root pressure.Subsequently,during the dry season from January to March,sap production of the ZT group continued to decrease until it was no longer produced.In the CT group,in January of the dry season sap could no longer be collected.Data in Fig.1 show that bamboo charcoal fertilizer prolonged the collection period for wine bamboo sap,and increased sap yields in the rainy season and during the transition from rainy to the dry season.

Fig.1 Wine bamboo sap gathering in two annual cycles

Fig.2 a Average air temperature,b average air moisture and c wind speed

As a rule,soil temperature is directly affected by air temperature and soil water by precipitation or directly related to air humidity(Zhao et al.2014).In the second cycle,SWfluctuation was large(Fig.2c);soil temperature and water content in both ZT and CK groups showed a similar trend;TS5and TS15changed in accordance with TAfluctuations(Fig.3a,b).The correlation between TS5,TS15and TAwas significant(p＜0.01;Table 1);and changes in TS15were steady.Except for July,TS5and TS15values in the second cycle both groups were not significantly different(p＞0.05).After reaching a peak in September,WS5and WS15values continued to decline until January–March of the following year(Fig.3c,d),corresponding to MAchanges(Fig.2b;Table 1).In the two cycles,except for individual months,differences in WS5values between the ZT and CK groups were not significant(p＞0.05);the average values of WS5and WS15of the ZT group were larger than the CK group(Fig.3c,d).Figures 2a,b,and 3,show that,in addition to the significant difference in WS15values between the two conditions in the dry season,average values of other environmental parameters of the ZT group indicated that ZT affected the microenvironment.

In both ZT and CK treatments,the CSapcorrelated with TA,MA,SW,TS5,TS15,WS5,and WS15(Table 1),and the correlation between CSapand soil water was highly significant(p＜0.01).Multiple linear regression and factor analysis suggest that environmental factors affecting CSapwere different for the ZT and CK groups(Table 2).Under the ZT treatment,CSapof the two cycles could be explained by three parameters,WS15,TA,and SW(parameter signif icance p＜0.05;collinearity threshold VIF＜5).The variance contribution rate of the three parameters reached 78.5%,and the coefficient of determination R2of linear regression at 0.703 was highly significant(p＜0.01).For the rainy season,CSapcould also be explained by three parameters,WS15,SW,and TA(parameter significance p＜0.1;collinearity threshold VIF＜5).However,for parameter significance,SWwas higher than TA,the total variance contribution rate of the three parameters was 84.79%,and the coefficient of determination R2of linear regression was 0.650,significant at p＜0.05.For the dry season,CSapdynamics could only be explained by WS15,and the total variance contribution rate was 70.19%.For the CK group,the two cycles of CSapcould be explained by WS5and MAcoinciding with the rainy season.Sap was rarely produced during the dry season and therefore there were no corresponding parameters(Table 2).

Fig.3 a Soil temperature at 0–5 cm depth,b temperature at 5–15 cm,c soil water at 0–5 cm depth and d soil water at 5–15 cm depth

Table 1 Correlation and significance between the traits in two annual cycles

Table 2 Main influencing factors to sap gathering in different seasons of two annual cycles

Analysis of minerals and conventional nutrient composition of sap

Mineral content of the sap can reflect the influence of mineral availability on plant development.Growth and development are processes of soil nutrient consumption and exogenous application and supplementation is often essential(Eduardo et al.2016),especially for species such as wine bamboo that are sensitive to soil fertility(Li et al.2013).Potassium,calcium,iron,manganese,copper,and total phosphorus content of the ZT group were significantly different from those of the CK group(p＜0.05;Table 3),their average values being 2.81,1.39,3.44,2.84,2.14,and 3.10 times higher respectively,than those in the CK group.The significantly increased iron and manganese contents might be because of the oven used for pyrolysis(special steel for high-temperature bamboo charcoal production).In compliance with food safety standards,no lead or inorganic arsenic was detected in this experiment.Mineral element contents of the CK group were slightly lower than the ZT group,and the average values suggest that the ZT treatment increased the contents of most minerals.

Total fat and starch contents were not determined;protein and reducing sugar contents were significantly different between the two treatments(p＜0.05).The ZT treatment markedly increased protein and reducing sugar contents.The mean protein content was 1.71 times higher than in the CK group;the mean reducing sugar content was2.19 times higher than in the CK group.Wine bamboo sap is acidic,and there was no difference in acidity between the ZT and CK groups(p＞0.05).The mean pH values indicated that sap of the ZT group was slightly more acidic.

Table 3 Mineral elements and general nutritive components of wine bamboo’s sap in two annual cycles

Amino acid content of sap

Wine bamboo sap contained all 18 amino acids tested in the analysis(Table 4).In the two cycles,the mean total amino acid content of the ZT group reached 1049.22 mg L-1,1.34 times higher than in the CK group.Eight of these were essential amino acids:threonine(THR),valine(VAL),methionine(MET),isoleucine(ILE),leucine(LEU),phenylalanine(PHE),lysine(LYS),and tryptophan(TRP).The mean value of the eight amino acids of the ZT group was 218.27 mg L-1,accounting for 20.80% of the total and for the CK group it was 173.92 mg L-1,accounting for 22.29%of the total amino acids.The three most abundant amino acids for both groups were glutamic acid(GLU),proline(PRO),and alanine(ALA).These accounted for 66.95 and 62.06%of the total amino acids of the ZT and CK groups,respectively.GLU,VAL,tyrosine(TYR),PRO,and TRP contents of the ZT group were significantly different from the CK group(p＜0.05).With the exception of aspartic acid(ASP),THR,glycine(GLY),and ILE,the average values of other amino acids in the ZT group were higher than those in the CK group.These results indicate that under the ZT treatment,the content of several amino acids and the total amino acid content were enhanced.

Table 4 Free amino acid content of wine bamboo’s sap in two annual cycles

Discussion

Application of bamboo charcoal fertilizer(ZT)extended sap collection period and improved yields

Sap secretion is a natural metabolic phenomenon and an indicator of the function and activity of the plant’s root system.Studies have shown that individual moso bamboo,bamboo forest quality,and growth and development affected sap to some extent(Zhang et al.1994).The diameter of the bamboo did not significantly correlate with sap yield(Zhang et al.1994;Li 1997),indicating that sap is associated more with underground plant parts.Results of this study showed that the rainy season was the period for abundant sap yield.The highest record of CSapwas 3.18 L stalk-1under the ZT condition in September of the fifth year of afforestation,still lower than the 4.637 L stalk-1of the moso bamboo sap(Li 1997).This was likely due to the scale of sap production of monopodial bamboos,(the community scale of uniaxial rhizomes),being different from sympodial bamboos.For large sympodial bamboos,such as wine bamboo,a single clump(scale within a population)is the main body for sap collection,and the rhizome system that integrates the underground physiological function plays a decisive role in sap quality and yield.Soil nitrogen,phosphorus,and potassium contents directly affect root growth and expansion(Wright et al.2011).Biochar added to the soil absorbs ammonium,nitrate and phosphate and makes them available during plant growth(Yao et al.2012).Manuel et al.(2016)reported that the combined use of biochar and fertilizer could change the morphology of the root system,an important indicator for studying soil science and plant growth.Schmidt et al.(2014)and Marleena et al.(2016)found that the addition of biochar improved soil function,increasing above-and below-ground biomass,which improved the microenvironment for plant growth.Sap yield data in this experiment also suggested that bamboo charcoal fertilizer helped the development of the rhizome system,facilitating sap production.Into the dry season in January,there were trace amounts of sap collected.Although the yield was small,and not significant in terms of sap production,it suggested that bamboo charcoal fertilizer affected the growth of wine bamboo,especially the underground parts.WS15and TS15data indicate that bamboo charcoal fertilizer,as a base fertilizer,was effective in maintaining temperature and moisture,resulting in a relatively steady change in response to the atmospheric features.Therefore,it was considered that the combined use of biochar and fertilizer acts as a controlled-release fertilizer,which is more beneficial for plant growth(Kim et al.2014;Manuel et al.2016).

Effect of different environmental parameters on seasonal sap yields

Under the ZT and CK conditions,CSapand environmental parameters showed a strong correlation;however,the impact of the environmental factors was not identical.Those that affected the two cycles were similar to the rainy season,and were mainly WS15,TA,WS,WS5,and MA,only different at the significance level.Under both conditions,sap yields of the rainy season accounted for 80.89 and 92.81%,respectively,of the total annual yield,suggesting that sap was mainly produced in the rainy season.Hence,data from the rainy season largely determined the interpretation of values of the two cycles,consistent with the period where wine bamboo showed a rapid growth(Li et al.2013).Under the ZT condition,the effect of WS15on CSapwas greatest,suggesting the dependence of CSapon the fluctuation of water content of the soil.Under the CK condition,CSapwas more sensitive to WS5,indicating that WS5and WS15had high similarity (correlation and collinearity).In the CK group,the rainy season surface water content could explain CSapyields.Thus,it could be inferred that ZT treatment improved the soil environment(Lehmann et al.2006),and increased soil water content(Atkinson et al.2010)and root pressure,thereby increasing the CSapamount re flected by the water transport conditions of the plant(Xu et al.2009).The results of this experiment suggest that the amount of sap collected was closely associated with the soil environment at the bamboo clump growth site;also,it was affected by the micro-environmental factors around the bamboo clumps.

Bamboo charcoal fertilizer(ZT)elevated sap mineral element and conventional nutrient contents

The plant root system synthesizes amino acids,organic acids,growth regulators,and macromolecules such as proteins(Xu et al.2009;Pandey and Ojha 2012)which are transported to the above-ground parts through the xylem.Thus,changes in nutrient content of the wine bamboo sap indirectly re flect factors affecting root physiology.Eduardo et al.(2016)found that the combined use of biochar,organic matter,and trace element fertilizer showed selectivity toward trace elements in barley and significantly increased grain Zn,Cu,and Ni contents,and reduced Cd and Pb levels.The research further shows similar selectivity toward trace elements:ZT mainly increased potassium,calcium,iron,manganese,copper and total phosphorus.Increased potassium and copper suggests that ZT could improve cold and drought resistance of wine bamboo,and enhance substance synthesis and transport by the plant(Wright et al.2011).Calcium and potassium coregulate stomatal closure,and iron,manganese,and copper are involved in photosynthesis and respiration.Appropriate elevation of these elements suggests that ZT treatment improved light utilization and regulated transpiration,critical for the introduction and domestication of wine bamboo in the middle and high mountain areas in Yunnan.Along with increasing mineral elements,ZT treatment increased the sap yields and protein content,and reduced sugar content as well as sap pH,thereby presenting an opportunity for preparing natural wine bamboo beverages.

Bamboo charcoal fertilizer(ZT)increased sap amino acid content

The amino acid evaluation revealed a total of 18 amino acids in the wine bamboo sap,which was the same number as found in the shoots(Li et al.2013),and more than the 14–16 amino acids found in moso bamboo sap(Zhang et al.1994;Li 1997).The amino acid content varied greatly,which may be due to differences in geography,experimental environment,collection times,parameter preset,and pretreatments.The amino acid composition was more absolute in wine bamboo sap,with a higher total amount,including almost half the amount of essential amino acids in the shoots(442 mg kg-1under enclosed conditions)(Li et al.2009),Therefore,the sap has a higher application value,providing a better basis for development and utilization.The Pro content,one of the components of plant proteins,can be a physiological indicator for breeding for cold and drought resistance.Therefore,high Pro content holds great importance for the geographic scope of wine bamboo introduction and breeding practices.Amino acid levels reflect the pharmacological effect of sap to some extent(Xu et al.2009).However,the relationship between amino acids and medicinal values of wine bamboo sap needs further study.

Results of the experiment with bamboo charcoal fertilizer show that various parameters and indicators had different degrees of enhancement.The potassium and total phosphorus content of sap was high,consistent with the findings by Kim et al.(2014)who reported that the controlled release of carbon-based compound fertilizer(potassium–phosphorus–humus fertilizer)was significantly effective in providing K and P required for plant growth.The addition of bamboo charcoal in the fertilizer could increase ammonium,nitrate and total nitrogen contents,and increase the nitrogen fixation rate by 28.3–65.4%(Chen et al.2013).However,there is risk of antagonism between NH4+–N competition and K+absorption(Xu et al.2009).Our results indicate that combination fertilization augmented the wine bamboo growth environment,increased physiological activity and absorption capacity of the plant root system,and thereby promoted growth.Deep soil water and temperature changed slowly,particularly in the dry season,maintaining plant sap production.This was consistent with findings that,under water stress,the addition of NH4+–N significantly improved rice sap flow rate,P content,and water-use efficiency(Song and Li 2004).Moreover,it also supports the observation that bamboo charcoal fertilizer used in this experiment had an adequate C/N ratio,and a large surface area and porosity,allowing for optimum absorption of ammonia and ammonium nitrogen(Xu et al.2013).This is significant to reduce the loss of N fertilizer by alleviating N leaching into the surrounding water body,thus checking pollution(Homagain et al.2015;Hussain et al.2016).

Conclusions

ZT treatment could be more beneficial to the development of root systems because the function of heat preservation and moisture retention prolong the sap collection period,increase sap yields,and elevate mineral elements,conventional nutrients,and amino acid contents with evident fertilization effects and broader application prospects.

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