Antioxidant,nutritional and anti-nutritional composition of Garcinia kola and Chrysophyllum albidum from rainforest ecosystem of Ondo State,Nigeria

Jonathan C.Onyekwelu?Olufunmilayo Oyewale?Bernd Stimm?Reinhard Mosandl

Antioxidant,nutritional and anti-nutritional composition of Garcinia kola and Chrysophyllum albidum from rainforest ecosystem of Ondo State,Nigeria

Jonathan C.Onyekwelu1?Olufunmilayo Oyewale1?Bernd Stimm2?Reinhard Mosandl2

Tropical forests contain many tree species that have supplied edible fruits for centuries.These fruits have contributed to human diets due to their richness in nutrients,vitamins,minerals,antioxidants and their low antinutrients content.We investigated the antioxidant,nutritional and anti-nutritional composition of Garcinia kola and Chrysophyllum albidum fruit parts.The nutritional, anti-nutritional and antioxidant compositions differed depending on the fruitpart.Irrespective of fruitpart,moisture content was high(72–93%).While the edible part(fruit pulp)of C.albidum proved a better source of protein(4), fibre(17%)and fat(2%),the seed kernel was a better source of ash(2%)and carbohydrate(15%).Carbohydrate(22%),protein(2%),fat(1%)and fibre(3%)were higher in G.kola seed kernel(edible part)than in the pulp and pod.Anti-nutrient content in G.kola and C.albidum fruits was low,indicating thattheir consumption would not pose nutritional or health problems.The antioxidant compositions(especially phenolic content(10–21 mg·g-1)and DPPH(1,1-diphenyl–2 picrylhydrazyl)(26–55%))of C.albidum fruit pulp and G.kola seed kernel were high, implying that they could be good sources of natural antioxidants and could be used as supplements in food manufacturing.

Forest food trees·Livelihood·Antioxidant· Nutritional supplement·Tropical forests·Garcinia kola· Chrysophyllum albidum·Nigeria

Introduction

Fruits are essentialfor human growth,maintenance of good health and vitality because of their richness in essential nutrients,vitamins,minerals and natural antioxidants, coupled with their low anti-nutrients contents(Luna-Va′zquez etal.2013).Over the years,the importance of fruits to promote health,impart strength,give power of endurance, vigour of intellect,etc.has been pointed out(Siddhuraju and Becker 2007;Enujiugha 2010).The ingestion of sugar can be discouraged and replaced with taking fruits.More than 5000 phytochemicals have been identified in plant foods(Shahidi and Naczk 1995).Phenolic compounds are believed to be potent and important contributors to reducing oxidative stress due to their antioxidant activity,which is of great importance in diets(Richfort and Panozzo 2007).In recent times,natural antioxidants,which are obtained from fruits,have raised interest among nutritionists,food manufacturers and consumers because of their presumed safety and potential therapeutic value (Sreeramulu and Raghunath 2011).Current research trends indicate a shift towards identifying non-nutritional antioxidants in functional foods(Takeoka and Dao 2003).

Tropical forests contain many tree species that produce edible fruits,seeds,vegetables and medicine.Notableexamples are:Afzelia africana,Irvingia gabonensis,Garcinia kola,Treculia africana,Chrysophyllum albidum,etc. (Africa),Bridelia tomentosa,Parkia speciosa,Eugenia rothii,Ziziphus rugosa,Ficus bengalensis,etc.(Asia), Carapa guianensis,Platonia insignis,Uncaria guianensis, Bertholletia excels,Caryocar villosum,etc.(South America)(Okafor 1991;Sundriyal and Sundriyal 2003;FAO 2011).Their contributions to diets as well as their potentials in alleviating poverty and ameliorating food problems are enormous(Okafor 1991;Leakey et al.2005).They have immense socio-economic,nutritional,medicinal and cultural importance,especially to rural dwellers(Ayuk etal.1999;Onyekwelu and Stimm 2006,2011;Gulatietal. 2012).They serve as alternative food sources,especially at the onsetof the farming season when farmers prepare their crops for planting and thus contribute to food security (Leakey et al.2005;Onyekwelu et al.2011).Many are valuable sources of nutrition(Leakey 1999)with significant health benefits against malnutrition and possible nutritional benefits conferring enhanced resilience to disease(Barany et al.2001;Gulati et al.2012).However,the continuous supply of the products of these valuable forest food trees is constrained by threat of extinction and senescence of their mother trees,lack of domestication and conservation,lack of appropriate storage and preservation technologies for their fruits and seeds.Chrysophyllum albidum(African star apple)and Garcinia kola(bitter kola) are among the widely consumed forest fruit tree species in West Africa(Adebisi 2004;Onyekwelu et al.2011).Their natural range is from West Africa through Central to East Africa(Keay 1989).C.albidum fruit(Fig.1a)is a source of vitamins,irons,and flavours to diets.The fleshy pulp of C.albidum fruit,which contains more ascorbic acid than orange,guava or cashew,is eaten as snack and food (Asenjo 1946 cited in Amusa et al.2003;Onyekwelu and Stimm 2011).G.kola has astringent and resinous taste and is used as a stimulant and aphrodisiac(Adebisi 2004).The seeds(Fig.1b)are chewed and used in traditional ceremonies and folk medicines.They have potential therapeutic benefits due largely to the activities of flavonoid and other bioactive compounds(Adegoke et al.1998; Farombi 2003).G.kola has potential for utilization as hop substitute in brewing(Dosunmu and Johnson 1995).

In Nigeria,C.albidum and G.kola are widely consumed by both rural and urban dwellers(Egharevba and Uwadiae 1995;Onyekwelu and Stimm 2011).Currently,there is huge local markets for their fruits while emerging international market has been identified(Onyekwelu et al. 2014).Despite their nutritional and economic importance, C.albidum and G.kola are classified among endangered tree species in Nigeria and are on IUCN listof endangered species(FORMECU 1999;Borokini 2014).For example, only few tree stands of the species were encountered during a survey to farms,homegardens and fallow fields in southwestern Nigeria,further buttressing their endangered status.Thus,these species might go into extinction except steps are taken to conserve them or increase their population(Onyekwelu et al.2014).In this study we examined the antioxidant,nutritionaland anti-nutritionalcomposition of G.kola and C.albidum fruits.

Materials and methods

Ripe C.albidum and G.kola fruits were harvested from agroforestry farmsin the rainforestecosystemofOndo State, Nigeria.The state lies between 5°45′and 7°52′N and 4°20′and 6°5′E in southwestern Nigeria.Most of the state is covered by tropical rainforest,which occupies the central and most of the southern regions.The climate is tropical, with distinct rainy and dry seasons.Most of the rains fall between March and Octoberwhile the months of Novemberto February are dry.Mean annualrainfallranges from 1700 to 2200 mm.Mean annualmonthly temperature and relative humidity are about27°C and 80%respectively.

Fig.1 a Chrysophyllum albidum fruits and b Garcinia kola seeds

For each species(C.albidum and G.kola),ten(10)ripe fruits were harvested from each of ten(10)mother trees and pooled.Thirty of the 100 fruits per species were randomly selected foranalyses.The ripe C.albidum fruitswere opened and the pulp and seeds extracted,washed with distilled water and dried.For G.kola,the ripe fruitpod wassplitopen and the seed extracted,washed with distilled water and dried.The extracted materials were then weighed to obtain their initial weights.The analysis of food was performed through proximate(or‘Wende’)analysis.The ripe C.albidum and G.kola fruits were tested for the following proximate compositions: moisture content,ash,fat,crude fibre,carbohydrate,and crude protein,while the anti-nutritional composition examined were tannin,saponin,alkaloid,phytin phosphorus, phytate and oxalate.Totalphenolic content,totalflavonoid, vitamin C and DPPH(1,1-diphenyl–2 picrylhydrazyl)were the antioxidants determined.Proximate chemical composition(moisture content,ash content,fat,crude fibre,carbohydrate,crude protein)was determined according to AOAC (2005)methods.Phytate content was determined following the method ofMarfo etal.(1990).Oxalate wasdetermined by titrating againstboric acid solution according to the AOAC (2005)method.Tannins were estimated by the Vanillin-HCl method of Price etal.(1978).Saponin was determined using the method of Birk et al.(1963)as modified by Hudson and El-Difrawi(1979).For alkaloid determination,chromatographic analysis was performed employing the modified method of Lee et al.(2007).Phytin phosphorus was determined using the method of Wheelerand Ferrel(1971).Total phenolic content was determined by Folin-Ciocalteu assay (Singleton and Lamuella-Raventos1999)using Gallic acid as standard(Enujiugha 2010).The total flavonoid contentwas determined using the colorimetric method(Heimler et al. 2005)while Vitamin C was determined using the titration method of AOAC(2005).The free radical-scavenging activity of the extracts was determined using DPPH.Seed extractswere measured in terms ofhydrogen donation orradical scavenging activity using the stable radical DPPH method (Chen and Ho 1995)as modified by Sanchez-Moreno et al. (1998).Data were analysed using one-way Analysis of Variance(ANOVA)at the significance level of alpha=0.05.Treatment means found to differ significantly were separated using Duncan’s Multiple Range Test.

Results

The nutritional compositions of C.albidum and G.kola are presented in Table 1.The edible portion of C.albidum(i.e. fruit pulp)was low in carbohydrate and high in fat,fibre and protein compared to the seed kernel while the seed kernelhad higher ash content(Table 1).Both the fruitpulp and seed kernel had high moisture content.The edible portion of G.kola(i.e.seed kernel)was richer in carbohydrate,fibre,fat and protein compared to the fruit pulp and fruit pod of the species(Table 1).However,the seed kernel had the lowest ash content.While there were significant differences in some nutritional compounds(e.g. ash,fat,fibre and carbohydrate)of C.albidum fruit pulp and seed kernel,the differences in others(e.g.moisture and protein)were not significant.Fat(range 1–2%)and fibre (range 2–17%)contents were significantly higher while carbohydrate(range 1–15%)and ash(2%)contents were significantly lower in C.albidum fruitpulp than in the seed kernel(Table 1).There was no significant difference between the moisture(range 76–78%)and protein(range 3–4%)contents of C.albidum fruit pulp and seed kernel. For G.kola,the fruit pod had the highest ash content, which was significantly higher than that of the fruit pulp and seed kernel.G.kola fruit pulp had the significantly highest moisture content(range 72–93%),followed by fruit the pod and lastly by the seed kernel(Table 1).Protein(range 1–2%)and fat(range 0.4–1%)contents of G. kola seed kernel and fruit pod were statistically similar but significantly higher than that of the fruit pulp.G.kola seed kernel had the significantly highest fibre content(range: 1–3%),followed by fruit pod and lastly by fruit pulp. Carbohydrate content(range 6–22%)was significantly higher in seed kernel than in both fruit pulp or fruit pod, which were statistically similar.

The results of anti-nutritional contents showed that tannin (range 0.16–0.59 mg·g-1),alkaloid(range 0.05–0.11 mg·100g-1) andoxalate(range 0.89–1.01 mg·g-1)were higherin C.albidum seed kernel than in the fruit pulp while saponin(range (0.06–0.09)×100-2mg·g-1)andphytate(range 2.29–2.75 mg·g-1) content was higher in fruit pulp than in the seed kernel (Table 2).Phytin phosphorus content of the fruit pulp and seed kernelof C.albidum were almostequal(0.64–0.65 mg·g-1) (Table 2).For G.kola,phytate(range 1.64–2.47 mg·g-1) and phytin phosphorus(range 0.46–0.69 mg·g-1)contents were highestin the seed kernelbutequalin the fruitpulp and fruitpod(Table 2).Oxalate content(range 0.31–1.26 mg·g-1) of G.kola was highest in the seed kernel(1.26 mg·g-1), followed by the fruit pulp(0.31 mg·g-1)and lastly by the fruit pod(0.18 mg·g-1).G.kola fruit pod had the highest saponin(9.06 mg·100g)and alkaloid(1.50 mg·100g)contents while the lowest saponin(5.12 mg·100g)and alkaloid (1.00%)contentwas in fruitpulp.The seed kernelhad very low concentration of tannin(range 0.02–0.05 mg·g-1)(Table 2).

The mean antioxidant concentrations in C.albidum and G.kola fruit are presented on Table 3.Mean total phenolic content(range 11–17 mg·g-1)was significantly higher in C.albidum fruit skin and seed kernel than in thefruit pulp while there was no significant difference in the DPPH scavenging activities of the various fruit parts (Table 3).Mean flavonoid(range 0.3–0.6 mg·g-1)concentration was similar in C.albidum fruit pulp and seed kernel but significantly lower in the fruit skin.There was no significant difference in the mean vitamin C contents (range 0.6–0.8 mg·g-1)of the various C.albidum parts (Table 3).For G.kola,mean total phenolic content varied from 9.22 mg·g-1in fruit pulp to 21.08 mg·g-1in the seed kernel,with the seed kernel having a significantly higher total phenolic content than the other fruit parts (Table 3).Mean total flavonoid content(range 0.37–1.15 mg·g-1)of G.kola was statistically similar for the seed kernel and fruit pulp but significantly lower in the fruit pod.Mean vitamin C content ranged from 0.69 mg·g-1in G.kola fruit pod and seed kernel to 1.25 mg·g-1in fruit pulp,with fruit pulp having a significantly higher value than the other parts of the fruit (Table 3).The vitamin C content of the seed kernel and fruit pod were equal(0.69 mg·g-1).There was significant difference in the mean DPPH scavenging activities(range 26–55%)of the various G.kola parts,with the seed kernel having the significantly highest value,followed by fruit pod and lastly by the fruit pulp(Table 3).

Table 1 Nutritional composition(wet wt.basis)of the fruit and seed parts of Chrysophyllum albidum and Garcinia kola

Table 2 Anti-nutritional composition(wet wt.basis)of the fruit and seed parts of Chrysophyllum albidum and Garcinia kola

Table 3 Antioxidant composition of the fruit and seed parts of Chrysophyllum albidum and Garcinia kola

Discussion

Non-cereal plant foods from the forest have contributed immensely to the diets of Africans(Getachew et al.2005). C.albidum and G.kola are among the among the widely consumed forest fruit species in West Africa(Adebisi 2004;Onyekwelu etal.2011).Presently,only the fruitpulp of C.albidum and the seed kernelof G.kola are eaten,they are usually eaten raw.Both species are consumed by both young and old in rural and urban settlements in tropical countries of West Africa(Onyekwelu and Stimm 2011). Knowledge of the nutritional and antioxidantcompositions of various parts C.albidum and G.kola fruits(including the non-edible parts)could provide insight into their potential health benefits and industrial uses.

The moisture contents of the different parts of C.albidum and G.kola fruits(range 76–78%for C.albidum and 72–93%for G.kola)was high.The quality and stability of some fruits has been attributed to their moisture contents(Frazier and Westhoff 1988).The high moisture content of C.albidum fruits could imply fast perishability and shortshelf-life,since high moisture contentencourages microbial growth,increases the rate of enzymatic reaction and hence deterioration(Abidemi et al.2009).C.albidum fruits spoils within 3 to 5 days after natural fruit fall (Amusa et al.2003;Onyekwelu and Stimm 2011),which was attributed mainly to its high moisture content.The implication of this is that the fruit deteriorates quickly and cannot be stored for a long time.Thus,an appropriate storage technology must be developed for C.albidum fruits.The high moisture content of Butryospermum parkii (Shea butter)was associated with its high rate of deterioration(Abidemi et al.2009).On the contrary,the high moisture content of G.kola seeds may be very important for quality preservation in storage.Upon drying,the seed of the species easily loses moisture,shrinks,becomes very tough and loses its value.Dosunmu and Johnson(1995) observed that rapid loss of moisture leads to change in texture,sensory and nutritional attributes of G.kola seeds and recommended storage methods that retain or increase the moisture content of the seed.

Fruits are generally not considered as excellent sources of proteins(Edem et al.1984;Kuhnlein 1989).However, plant protein constitutes essential animal protein supplement,especially in rural areas of developing countries where animal protein can be very scarce(Heinritz et al. 2012;Martens et al.2012).The protein content of C.albidum in this study was lower than the range(6–8%)reported for the species by Edem et al.(1984)and Amusa et al.(2003)but within the range(2.89–4.16%)reported for Dacryodes edulis and six forest fruits species in the Himalaya(Sundriyal and Sundriyal 2003;Omogbai and Ojeaburu 2010).Dosunmu and Johnson(1995)and Odebunmi et al.(2009)reported higher crude protein for G. kola(3.90–7.8%)than was recorded in this study.The crude protein values obtained in this work were lower than those of other vegetable protein sources commonly consumed in tropical regions,namely:melon(28.4%),peanut flour(24.3%)and canola(25%).However,although the protein contents of C.albidum and G.kola were low,their consumption(especially C.albidum)can make significant contribution to rural diets by ameliorating protein deficiency.In addition to contributing to human protein,the fruitpulp and the seed kernelof the two species can also be used as supplementto animalprotein in formulating animal feed in developing countries.The protein contents of the pulp and seed kernel of C.albidum fruit were statistically comparable;implying that equal amounts of protein can be obtained from either the fruit pulp or seed kernel,which is also true for G.kola seed kernel and fruit pod.

While C.albidum fruit pulp is a better source of fibre and fat,the seed kernel is a better source of ash and carbohydrate.The carbohydrate and fatcontents of C.albidum fruit pulp and seed kernel in this study were lower than what was reported by Amusa et al.(2003).Carbohydrate (22%),protein(2%),fat(1%)and fibre(3%)were higher in G.kola seed kernelthan in the fruit pulp and pod but lower than the values reported for the species by Odebunmietal.(2009).Only G.kola seed kernelcontained moderate amount of carbohydrate(22%)which was slightly higher than the values for fruits like mango(17%) and pomegranate(17%)but lower than what was reported for six forest species in the Himalaya(Sundriyal and Sundriyal 2003;Mahapatra etal.2012).The edible portion of C.albidum(fruit pulp)had low carbohydrate content. Carbohydrates are essentialcomponents of human nutrition that enables the body to produce the energy required for normal function.The human diet contains a wide range of carbohydrates,the vast majority of which are of plant origin(Sa′nchez-Castillo et al.2002).Compared to some published results(Sundriyal and Sundriyal 2003),the ash contents of our study species was low.

The low fat contents of C.albidum and G.kola in this study corroborate the widely held view that fruits are not good sources of dietary fat and explains why fruits are usually recommended as part of weight reducing diets. Based on our results,C.albidum fruitpulp and G.kola seed kernel would not be good sources of dietary fibre.This confirms the results of Sundriyal and Sundriyal(2003)who reported low fatcontents for some Indian forest fruits.The higher fibre content of C.albidum seed kernel implies that itmight be a good source of dietary fibre.Dietary fibre has health-promoting properties and has been noted to be important for reducing cholesterol levels in the body tominimize risks of cardiovascular diseases caused by high plasma cholesterol.Diets with high fiber contenthave been used for weight control and fat reduction,as they give a sense of satiety even when small amounts of food are eaten.Thus,the low fat and high fibre contents of C.albidum fruit pulp is an indication that its consumption will not lead to increase in body fat but might be good for dieting and reducing cholesterol levels in the body.

The presence of toxic substances known as anti-nutritional factors is one of the major drawbacks limiting the direct use of some foods(NRC 1993).The contents of these anti-nutrients such phytate,tannin,saponin,alkaloid and flavonoid in C.albidum and G.kola seed kernel and fruit pulp were low.It has been established that only high contents of these anti-nutrients prevent the absorption of minerals like iron,magnesium,potassium,calcium and amino acid,which are essential for metabolism(Abidemi et al.2009).High contents of anti-nutrients would also affect homeostasis of zinc and iron,inhibit enzymatic digestion of proteins by forming complexes with large quantities of protein and would therefore be toxic(AOAC 2005;Abidemi et al.2009).In research conducted in Nigeria,flavonoids were not detected in C.albidum fruit pulp.Similarly,we recorded low flavonoid content in this study.Exceptfor alkaloid,saponin and tannin,G.kola seed kernel contained higher anti-nutrients than the fruit pulp and fruit pod.The tannin composition reported for G.kola by Dosunmu and Johnson(1995)was much higher than the value recorded in this study.On the other hand,G.kola in this study had higher phytate composition than reported by Dosunmu and Johnson(1995).Comparatively,G.kola had higher saponin,alkaloid and oxalate contents than C.albidum;C.albidum had higher tannin than G.kola while both species had comparable phytate and phytin phosphorus contents.Adepoju(2009)reported phytate and saponin compositions of 1.64 and 1.82,respectively in Mordii whytii fruits as well as oxalate and tannin contents of 1.88 and 2.41,respectively in Spondias mombin fruits,which are generally higher than the values reported for the two species in this study.The oxalate and tannin contents of C. albidum and G.kola were lower than the values reported for eight Indian fruits species(Rathod and Valvi 2011). However,both species contained higher phytate than the eight Indian species(Rathod and Valvi 2011).Consequently,based on the low level of anti-nutrients in C.albidum fruit pulp and G.kola seeds in this study,it can be concluded that the consumption of the two species would not be detrimental to human health.

Antioxidants,which are essential for human health,are nature’s way of protecting the body and cells from damaging free radicals(Hamid etal.2010;Capasso 2013).Free radicals are unstable molecules that are generated from exposure to sun,stress and as part of the natural aging process(Nikki2001;Valko etal.2007;Hamid et al.2010). Dietary antioxidants play important roles in controlling oxidative stress(Nikki 2001).There are indications that antioxidant contents of the edible portions of C.albidum (fruit pulp)and G.kola(seed kernel)fruits are high.Total phenolic contentand flavonoid compositions of C.albidum fruitpulp and G.kola seed kernel in this study were higher than what were reported for some nuts and oil seeds (Enujiugha 2010;Sreeramulu and Raghunath 2011). Phenolic compounds are known to be responsible for antioxidant activities in fruits.Sim et al.(2010)reported that fruits with higher phenolic contents generally show stronger antioxidant activities.The DPPH scavenging activities of C.albidum fruit pulp and G.kola seed kernel were higher than the values reported for some nuts and seed oil (Enujiugha 2010;Sreeramulu and Raghunath 2011).The DPPH scavenging activities of C.albidum and G.kola indicate their free radical scavenging potentials and thus their potential effectiveness as natural antioxidants.Gulati et al.(2012)reported high antioxidant activities of the Australian and Indian species,Euphorbia drumondii and Mucuna pruriens,respectively.Cao et al.(1996)noted that supplementing natural antioxidants with a balanced diet containing antioxidants could be effective in protecting the human body against various oxidative stressors.Antioxidants have been associated with prevention of nutritionally related diseases such as cancers,diabetes mellitus, coronary heartdisease and obesity(Larraurietal.1996).In recent times,natural antioxidants have raised interest among nutritionists,food manufacturers and consumers because of their presumed safety and potential therapeutic value(Sreeramulu and Raghunath 2011).The high composition of antioxidants in G.kola seed kernel and C.albidum fruit pulp suggests that they could be potential sources of natural antioxidant,thus they could be used as supplements in food manufacturing and the developmentof nutritional drinks.

Conclusion

Forest fruits are good nutrient and antioxidant sources that contribute significantly to human diets.C.albidum and G. kola fruits are promising sources of essentialnutrients,thus their consumption can make significant contributions to rural diets by ameliorating nutrient deficiencies.Based on the low level of anti-nutrients in C.albidum fruit pulp and G.kola seeds,their consumption would not be detrimental to human health.The high antioxidant content in G.kola seed kernel and C.albidum fruit pulp suggests that they could be potential sources of natural antioxidant,thus they could be used as supplements in food manufacturing and the development of nutritional drinks.

AcknowledgmentsThis study was part of a larger study on‘Domestication of some important indigenous forest food tree species—phenotype variation,selection and nursery investigation’sponsored by Alexandervon HumboldtFoundation(AvH),Bonn,Germany.The authors are grateful to the AvH for financially supporting this work under the Research Group Linkage Programme of the AvH.

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20 February 2013/Accepted:21 July 2014/Published online:30 April 2015

?Northeast Forestry University and Springer-Verlag Berlin Heidelberg 2015

Project funding:This work was supported by Alexander von Humboldt Foundation(AvH),Bonn,Germany.

The online version is available at http://www.springerlink.com

Corresponding editor:Zhu Hong

?Jonathan C.Onyekwelu onyekwelujc@yahoo.co.uk

1Department of Forestry and Wood Technology,Federal University of Technology,Akure,P.M.B.704,Akure, Ondo State,Nigeria

2Institute of Silviculture,Technische Universita¨t Muenchen, Hans-Carl-von-Carlowitz-Platz 2,85354 Freising,Germany