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Assessment of antioxidant activity, minerals, phenols and flavonoid contents of common plant/tree waste extracts Saranya Kuppusamy a,b,c,∗ , Palanisami Thavamani c,d , Mallavarapu Megharaj b,c,d , Ramkrishna Nirola b,c , Yong Bok Lee a , Ravi Naidu b,c,d a
Institute of Agriculture and Life Science, Gyeongsang National University, Jinju 660-701, South Korea Centre for Environmental Risk Assessment and Remediation (CERAR), University of South Australia, Mawson Lakes, SA 5095, Australia c Cooperative Research Centre for Contamination Assessment and Remediation of Environment (CRC CARE), PO Box 486, Salisbury South, SA 5106, Australia d Global Centre for Environmental Remediation (GCER), Faculty of Science and Information Technology, The University of Newcastle, Callaghan, NSW 2308, Australia b
a r t i c l e
i n f o
Article history: Received 7 October 2015 Received in revised form 20 December 2015 Accepted 21 December 2015 Available online xxx Keywords: Agroforestry waste Essential nutrients Heavy metals Polyphenols DPPH activity
a b s t r a c t Extracts of 25 different plant/tree wastes were screened for their phenol and flavonoid contents, antioxidant activity, nutritional and toxicological elemental composition. The commercial exploitation potential of nutrient and polyphenol-rich tree/plant wastes was also discussed. This study is the first to recommend using non-toxic Melaleuca diosmifolia leaf, Melia azedarach pod, Alnus cordata leaf and Pinus radiata cones because they all contain the essential elements (N, P, K, S and Fe) for dietary intake, applications as soil amendments, contaminant biosorbents and substrates for composting or biofertilizer preparation. Fruit peel of Quercus robur, M. diosmifolia leaf and bark, Eucalyptus leucoxylon pod and leaf, Pyrus ussuriensis and Prunus cerasifera leaf aqueous extracts indicated high phenolic content (35–66 mg GAE/g) and antioxidant activity (70–90%). A. cordata and Morus alba pendula leaf emerged as a unique source of flavonoids (>95%). There are greater prospects for the green synthesis of metallic nanoparticles using these polyphenol-rich residues. © 2015 Elsevier B.V. All rights reserved.
1. Introduction One of the most important and overlooked constituents today is ‘minerals’. Polyphenolic compounds are ubiquitous in vegetation, constitute an important part of the human diet, and have aroused much interest due to their antioxidant properties. Flavonoids constitute the largest group of plant phenolics and are very effective antioxidants (Maisuthisakul et al., 2007). In recent days, efforts have been made to transform natural wastes into products of commercial utility as they are very rich in bioactive compounds such as vitamins, minerals, amino acids, polyphenols, etc. Among these bioactive compounds, some essential mineral elements play an important role as cofactors in many enzymatic processes involved in humans, plants, animals and soil microbes. Mineral and polyphenol-rich plant materials are of interest to the cosmetic, nutraceutical, remedial and food industries (Kuppusamy
et al., 2015). For this reason the search for cost-effective mineraland phenol-rich natural materials has continued to this day. To date only limited knowledge is available concerning the use of natural materials especially the abundantly available plant/tree wastes which we dispose of every year at nearly a rate of 24 billion tons (EnviraChar, 2013). Such disposals encompass leaves, fruits, barks, flowers and grass clippings, that are expected to have high levels of minerals and phenolic antioxidants. To date the available literature has not described the full elemental composition and the phenolic ranges of plant/tree wastes. In particular demarcated profiles of the essential, trace and toxic mineral composition of these natural residues are not available. Such information would facilitate their effective utilization. With this in mind, our study was conducted with a primary aim to: firstly, evaluate the elemental composition, phenol, flavonoid contents and antioxidant activity of the so far unexplored, commonly available plant/tree wastes for the first time; and secondly, suggest their potential and practical applications.
∗ Corresponding author at: Institute of Agriculture and Life Science, Gyeongsang National University, Jinju 660-701, South Korea. E-mail address: [email protected] (S. Kuppusamy). http://dx.doi.org/10.1016/j.indcrop.2015.12.060 0926-6690/© 2015 Elsevier B.V. All rights reserved.
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2. Materials and methods 2.1. Chemicals 2,2-diphenyl-1-picryl-hydrazyl (DPPH), Folin-Ciocalteau’s reagent, sodium carbonate anhydrous, aluminium chloride, potassium acetate, methanol and nitric acid (HNO3 ), all of analytical grade were purchased from Sigma–Aldrich (Steinheim, Germany). They included gallic acid, quercetin and ascorbic acid which serve as standards for spectrophotometric assays of total phenols, flavonoids and antioxidant activity, respectively. All solutions were prepared with Milli-Q water (18 cm−1 , Milli-Q, ELGA labwater, UK). 2.2. Plant material Specimens of 25 different plant/tree wastes consisting of 17 leaves [eucalyptus (Eucalyptus leucoxylon), olive (Olea europaea), flame tree (Brachychitona cerifolius), nerium (Nerium oleander), pear (Syzgium sp.), cherry plum (Prunus cerasifera), coastal tea tree (Leptospermum laevigatum), Italian alder (Alnus cordata), cockie’s tongue (Templetonia retusa), casuarina (Casuarina obesa), Manchurian pear (Pyrus ussuriensis), native hibiscus (Alyogyne hakeifolia), bracelet honey myrtle (Melaleuca armillaris), desert ash tree (Fraxinus angustifolia), green honey myrtle (M. diosmifolia), weeping white myrtle (Morus alba pendula) and red cottonwood (Hibiscus tiliaceous rubra)], 1 bark [bracelet honey myrtle (M. armillaris)], 6 fruit/seed pods [eucalyptus (E. leucoxylon), oak (Quercus robur), cow-itch (Lagunaria patersonii), oriental plane (Platanus orientalis), white cedar (Melia azedarach) and casuarina (C. obesa)] and 1 flower [pine (Pinus radiata)] that had fallen off from fullgrown plant/tree species were collected from Mawson Lakes, South Australia between June and December 2014. Collected residues (1 kg of each specimen) were washed with MQ water to remove the adhering soil particles. Then they were air dried at 40 ◦ C for 72 h, grounded to a fine powder and passed through a 0.5 mm sieve to a uniform powder. The powdered sections were stored in a desiccator with polythene sealing.
sodium carbonate), by using SynergyTM HT (Bio-Tek® instruments, Inc., Vermont, USA) multi-detection microplate reader. Samples were diluted (1:5) and were quantified using gallic acid (GAE) as standard. Results were expressed as mg of GAE equivalents per g of dry material. 2.5.2. Total flavonoids (TF) TF content was measured by a modified method described by Khomdram and Singh (2011). The reaction mixture comprised 100 L of extract, 100 L of 10% aluminium chloride and 100 L of 1 M potassium acetate solutions. After 30 min incubation at room temperature, absorbance of the yellow colored mixture was measured at 415 nm using a microplate reader. A standard curve was plotted using different concentrations of quercetin (0–50 g/mL) and the amount of total flavonoids was calculated as quercetin equivalents in mg per g of dry material. 2.5.3. Screening of the extracts for antioxidant potential—DPPH radical scavenging activity (DPPH inhibition) DPPH is a widely used stable free radical to evaluate the antioxidant potential of a sample. DPPH radical scavenging activity of the plant/tree waste extracts was evaluated according to a method outlined by Blois (1958) with slight modifications. Briefly, 60 M of DPPH radical solution in methanol was prepared and 3.9 mL of this solution was mixed with various concentrations of the sample solution. After 30 min, absorbance of the sample (As) was measured at 515 nm. Simultaneously, blank containing 100 L of water was treated as above and its absorbance was recorded as Ab . The DPPH radical scavenging activity was calculated as follows. %DPPH inhibition =
Ab − As × 100 Ab
2.6. Statistical analysis All experimental results were reported as mean values (n = 3; ± standard deviation). Analysis of variance (ANNOVA) and Tukey’s test were carried out using IBM SPSS statistics 20 software package (IBM® Corporation, USA).
2.3. Determination of mineral elements 3. Results and discussion Analysis of mineral elements was carried out after HNO3 (70%) acid digestion of the powdered material by Agilent 7500 c (Agilent Technologies, Tokyo, Japan) Inductively-Coupled Plasma Mass Spectrometer (ICP–MS). The C and N contents of the samples were measured using a Trumac (Leco® Corporation, Michigan, USA) carbon–nitrogen–sulphur analyzer (CNS analyzer). 2.4. Extraction procedure for polyphenol compounds Five mL of boiled water was added to 0.20 g of the sample and the suspensions were left for 24 h in a shaker at room temperature (24 ± 2 ◦ C). The extracts were then centrifuged for 10 min at 3000 rpm and the supernatant collected at 4 ◦ C and used within 24 h to determine phenols, flavonoids and antioxidant activities of the selected plant/tree wastes. All samples were extracted in triplicate. 2.5. Determination of phenolic compounds and antioxidant activity 2.5.1. Total phenols (TP) TP content was determined by a modified version of the Folin-Ciocalteau’s method adapted to micro-scale (Singleton and Rossi, 1965). TP content was evaluated by measuring the variation in absorbance at 660 nm after 45 min of reaction (100 L of extract + 250 L of Folin-Ciocalteau phenol reagent + 1 mL of 20%
3.1. Mineral composition of plant/tree wastes Monitored metal concentrations are presented in Tables 1 and 2. As can be observed in Table 1, significant variability exists in the elemental composition of different tree wastes tested. These substantial differences are likely to account for their distinct beneficial activities when exploited. The highest levels of C were found in E. leucoxylon (506.8 ± 24 mg/g) and M. diosmifolia (502.1 ± 49 mg/g) leaves. M. azedarach pod and Hibiscus tiliaceous rubra leaf recorded substantially higher NPK and Mg followed by leaves of Morus alba pendula and P. cerasifera. The highest Ca, S and Na concentrations were found in dried leaves of A. cordata (52.5 ± 12 mg/g), A. hakeifolia (16.3 ± 5.2 mg/g) and M. armillaris (12.1 ± 2.6 mg/g), respectively. P. orientalis fruit and M. azedarach pod exhibited higher concentrations of Cu (Table 2). M. diosmifolia leaf showed a very high value of Mg (181 ± 19 g/g) and Co (0.7 ± 0.8 g/g) compared to the remaining samples analyzed. Dried leaves of E. leucoxylon were a rich source of Ni (5.4 ± 1.5 g/g). Zn was rich in dried leaves and bark of M. diosmifolia. Iron, the most essential mineral in human health and essential for good cardiovascular health, cognitive development and immune function (Trumbo et al., 2001) was the predominant one in P. radiata cones (514 ± 24 g/g) followed by leaves of M. armillaris (358 ± 58 g/g). The amount of a nutritionally essential mineral that helps in preventing diabetes,
Please cite this article in press as: Kuppusamy, S., et al., Assessment of antioxidant activity, minerals, phenols and flavonoid contents of common plant/tree waste extracts. Ind. Crops Prod. (2015), http://dx.doi.org/10.1016/j.indcrop.2015.12.060
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Table 1 Macro-elemental composition (mg/g dry weight) of the samples considered for the study. Sample
Primary macronutrients C
a. Leaf Eucalyptus leucoxylon Olea europaea Nerium oleander Syzgium sp. Prunus cerasifera Leptospermum laevigatum Alnus cordata Templetonia retusa Casuarina obesa Pyrus ussuriensis Alyogyne hakeifolia Melaleuca armillaris Fraxinus angustifolia Melaleuca diosmifolia Morus alba pendula Hibiscus tiliaceous rubra Brachychitona cerifolius
506.8 473.9 442.7 444.7 448.6 494.1 359.5 466.4 455.5 463.1 401.4 477.7 453.6 502.1 455.1 429.8 454.9
b. Bark Melaleuca armillaris
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
24 59 31 47 18 57 51 39 37 32 39 23 41 49 50 39 22
480.5 448.2 463.0 460.6 464.0 450.9
d. Flower Pinus radiata
± ± ± ± ± ±
P 11.9 11.2 11.7 15.2 14.7 7.6 12.5 16.3 15.4 16.7 21.4 14.1 21.6 9.8 19.1 26.7 14.0
472.8 ± 53
c. Fruit/seed pod Quercus robur Lagunaria patersonii Platanus orientalis Eucalyptus leucoxylon Melia azedarach Casuarina obesa
Secondary macronutrients
N ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
2.7 2.9 1.7 1.2 1.1 2.2 1.8 3.8 2.6 2.4 2.5 1.1 3.8 2.2 1.1 2.9 2.2
4.7 ± 1.9
27 41 24 49 38 32
5.7 9.4 11.7 4.7 21.1 10.7
478.8 ± 57
± ± ± ± ± ±
K 1.9 1.0 3.2 1.8 1.5 1.2 1.1 1.4 0.7 1.1 1.4 1.1 1.5 0.6 2.7 2.0 1.0
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.7 0.9 0.1 0.8 0.3 0.8 0.2 0.6 0.1 0.1 0.3 0.1 0.7 0.5 1.1 1.4 0.2
8.0 9.7 16.3 10.3 24.8 7.1 10.8 14.8 7.6 10.3 14.0 7.9 16.0 6.4 18.9 23.3 17.6
0.4 ± 0.1 1.3 2.7 2.4 1.6 3.7 1.9
4.6 ± 2.1
0.3 1.3 1.9 0.6 3.2 0.5
± ± ± ± ± ±
Ca ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
2.1 1.2 3.7 6.1 3.2 2.1 3.4 5.6 3.8 4.2 3.4 2.5 2.9 1.5 3.9 6.2 5.2
10.3 21.1 18.4 11.6 15.7 4.7 52.5 19.9 15.4 12.5 23.0 5.3 18.8 8.4 18.4 30.3 2.2
4.1 ± 1.5
0.1 0.1 0.1 0.5 1.2 0.1
4.0 21.1 6.6 4.5 18.5 3.5
0.1 ± 0.1
± ± ± ± ± ±
Mg ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
2.2 2.6 3.2 3.1 3.1 1.7 12 3.0 2.4 2.6 1.9 1.2 4.2 1.5 3.2 11 0.2
1.5 0.9 0.5 2.0 2.4 0.8 1.0 1.5 1.1 1.6 1.5 1.6 1.9 1.7 1.7 2.3 0.3
4.6 ± 1.1 1.6 6.3 2.4 1.3 3.6 1.1
2.7 6.3 9.9 7.0 9.4 25.3
0.8 ± 0.2
± ± ± ± ± ±
S ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.1 0.2 0.1 1.3 1.4 0.1 0.2 0.8 0.5 0.4 0.9 0.7 0.7 0.3 0.1 0.9 0.1
1.2 1.5 1.8 2.0 2.0 2.2 0.9 2.5 1.3 1.2 16.3 3.1 4.9 2.1 1.5 2.4 1.1
1.0 ± 0.8 1.0 1.2 3.4 2.8 2.0 9.2
1.3 3.3 0.7 1.0 2.1 0.8
2.0 ± 1.4
± ± ± ± ± ±
Na ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.2 0.7 0.3 1.1 1.0 1.2 0.2 1.1 0.5 0.6 5.2 1.6 2.1 1.0 0.2 0.9 0.8
1.8 ± 0.5
0.2 0.1 0.1 0.2 1.1 0.1
0.4 1.0 1.4 1.1 1.5 1.1
0.3 ± 0.1
± ± ± ± ± ±
4.4 1.0 0.7 3.3 1.2 4.8 0.7 0.8 2.7 0.5 9.2 12.1 1.4 3.9 1.6 0.9 3.7
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
1.0 0.3 0.1 0.9 0.4 1.5 0.2 0.1 0.2 0.1 0.9 2.6 0.1 1.0 0.9 0.2 1.2
8.6 ± 2.1 0.1 0.3 0.4 0.2 0.9 0.3
0.6 ± 0.2
0.8 1.0 1.3 10.3 0.3 2.3
± ± ± ± ± ±
0.1 0.2 0.5 2.0 0.1 0.9
0.8 ± 0.2
Values are means ± standard deviation (n = 3)
Table 2 Trace and toxic elemental composition (g/g dry weight) of analyzed samples. Sample
Essential trace elements Mn
a. Leaf Eucalyptus leucoxylon Olea europaea Nerium oleander Syzgium sp. Prunus cerasifera Leptospermum laevigatum Alnus cordata Templetonia retusa Casuarina obesa Pyrus ussuriensis Alyogyne hakeifolia Melaleuca armillaris Fraxinus angustifolia Melaleuca diosmifolia Morus alba pendula Hibiscus tiliaceous rubra Brachychitona cerifolius
91.0 28.1 59.1 18.0 44.4 28.7 47.7 55.6 75.9 24.0 44.2 38.7 32.8 181 44.7 52.9 4.2
Cu ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
11 3.9 13 4.2 19 11 18 11 19 11 16 9.4 9.6 19 12 18 1.1
7.8 4.9 9.9 10.7 7.7 7.7 7.9 10.4 7.0 5.8 10.7 9.4 7.2 7.8 10.1 6.8 3.3
Toxic metals Zn
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
3.1 1.8 1.9 2.8 2.1 2.4 2.2 3.1 2.7 2.1 3.2 2.8 2.6 4.1 3.4 2.4 0.2
Fe
BDL 19.6 ± 4.2 18.9 ± 4.9 10.7 ± 2.1 10.2 ± 2.4 19.1 ± 3.8 9.3 ± 1.8 17.5 ± 3.9 14.5 ± 4.2 14.7 ± 3.8 22.0 ± 9.1 40.8 ± 6.8 13.1 ± 1.9 12.3 ± 2.8 29.3 ± 10 13.0 ± 6.8 7.4 ± 2.1
51.9 173 54.4 78.1 121 59.7 70.6 116 158 63.1 275 358 138 148 107 103 65.8
Ni ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
12 48 17 21 19 12 11 28 21 19 41 58 11 28 19 26 19
5.4 1.4 0.6 3.4 1.7 0.9 1.2 0.7 2.5 0.6 1.2 1.6 0.5 2.5 1.0 0.7 0.9
Co ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
1.5 0.4 0.1 0.9 0.4 0.1 0.2 0.1 1.0 0.1 0.8 0.4 0.1 0.7 0.1 0.2 0.2
0.03 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.2 0.1 0.2 0.1 0.7 0.2 0.1 0.04
Cr ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.1 0.2 0.9 0.4 0.2 0.2 0.6 0.7 0.5 0.1 0.2 0.9 0.8 0.8 0.9 0.7 0.1
BDL 0.5 ± 0.2 0.4 ± 0.1 0.4 ± 0.2 0.3 ± 0.1 0.3 ± 0.1 0.5 ± 0.1 0.5 ± 0.2 0.6 ± 0.1 0.3 ± 0.1 0.9 ± 0.5 1.5 ± 0.6 0.6 ± 0.1 0.5 ± 0.1 0.3 ± 0.1 0.4 ± 0.1 0.9 ± 0.2
Al 54.6 115 55.0 30.0 64.8 43.0 24.9 89.8 93.9 28.6 174 248 85.8 89.4 66.0 39.8 52.4
As ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
9.2 32 19 7.2 31 17 11 29 27 11 45 36 24 13 21 14 15
0.05 0.1 0.05 0.05 0.1 0.03 0.1 0.1 0.1 0.03 0.1 0.2 0.1 0.1 0.1 0.1 0.02
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.1 0.9 0.1 0.1 0.8 0.1 0.6 0.7 0.5 0.1 0.5 0.8 0.5 0.4 0.2 ± 0.7 0.1
Cd
Pb
0.1 ± 0.09 0.02 ± 0.1 0.1 ± 0.7 0.01 ± 0.1 0.01 ± 0.1 0.02 ± 0.1 BDL 0.2 ± 0.9 0.02 ± 0.1 0.03 ± 0.1 0.1 ± 0.7 0.03 ± 0.1 0.01 ± 0.1 0.01 ± 0.1 0.2 ± 0.8 0.1 ± 0.6 0.1 ± 0.5
BDL 1.0 ± 0.6 0.9 ± 0.2 0.3 ± 0.1 0.6 ± 0.2 0.4 ± 0.1 0.4 ± 0.1 0.6 ± 0.1 0.9 ± 0.2 0.2 ± 0.1 1.3 ± 0.4 2.8 ± 1.2 0.8 ± 0.2 0.7 ± 0.2 0.8 ± 0.2 0.5 ± 0.1 0.3 ± 0.1
b. Bark Melaleuca armillaris
29.5 ± 8.2
9.2 ± 2.4
39.4 ± 11
186 ± 21
0.9 ± 0.2
0.1 ± 0.4
1.0 ± 0.7154 ± 15
0.1 ± 0.7
0.1 ± 0.5
1.8 ± 1.0
c. Fruit/seed pod Quercus robur Lagunaria patersonii Platanus orientalis Eucalyptus leucoxylon Melia azedarach Casuarina obesa
24.7 ± 6.2 17.4 ± 2.7 26.2 ± 10 47.0 ± 14 12.1 ± 5.1 82.5 ± 20
2.1 ± 1.0 4.0 ± 2.5 16.7 ± 2.4 6.7 ± 1.5 16.9 ± 1.9 7.6 ± 2.1
BDL BDL 13.7 ± 6.2 22.7 ± 3.5 29.8 ± 6.4 17.2 ± 2.4
9.2 ± 3.8 37.4 ± 10 110 ± 31 117 ± 41 54.8 ± 11 300 ± 29
0.2 ± 0.1 0.4 ± 0.1 1.5 ± 0.9 1.9 ± 0.6 0.8 ± 0.1 2.2 ± 1.0
BDL BDL 0.1 ± 0.3 0.1 ± 0.4 0.04 ± 0.1 0.2 ± 0.8
BDL 3.9 ± 1.1 BDL 18.8 ± 3.5 0.9 ± 0.1101 ± 29 1.4 ± 0.994.7 ± 14 0.5 ± 0.114.5 ± 9.1 1.0 ± 0.1216 ± 48
BDL 0.04 ± 0.1 0.04 ± 0.1 0.1 ± 0.7 0.05 ± 0.2 0.1 ± 0.5
BDL BDL 0.04 ± 0.1 0.05 ± 0.2 0.1 ± 0.2 0.03 ± 0.1
BDL BDL 0.4 ± 0.1 0.9 ± 0.1 0.2 ± 0.1 2.6 ± 1.0
d. Flower Pinus radiata
11.0 ± 6.4
6.5 ± 2.7
24.5 ± 11
514 ± 24
0.9 ± 0.2
0.3 ± 0.2
1.7 ± 0.3388 ± 21
0.2 ± 0.9
0.04 ± 0.1
5.4 ± 1.1
Values are means ± standard deviation (n = 3). BDL—Below detection limit of ICPMS (Zn = 0.2 g/L; Co = 0.1 g/L; Cr = 1 g/L; As = 0.1 g/L; Cd = 0.1 g/L; Pb = 0.1 g/L).
Please cite this article in press as: Kuppusamy, S., et al., Assessment of antioxidant activity, minerals, phenols and flavonoid contents of common plant/tree waste extracts. Ind. Crops Prod. (2015), http://dx.doi.org/10.1016/j.indcrop.2015.12.060
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Table 3 Total phenol (TP) and flavonoid (TF) contents with antioxidant activity (IP) of the aqueous fractions obtained from the selected plant/tree residues. Plant/tree residue
TPI
TFII
IPIII
a. Leaf Eucalyptus leucoxylon Olea europaea Nerium oleander Syzgium sp. Prunus cerasifera Leptospermum laevigatum Alnus cordata Templetonia retusa Casuarina obesa Pyrus ussuriensis Alyogyne hakeifolia Melaleuca armillaris Fraxinus angustifolia Melaleuca diosmifolia Morus alba pendula Hibiscus tiliaceous rubra Brachychitona cerifolius
42.0 ± 3.6 25.7 ± 1.8 17.4 ± 3.6 32.9 ± 2.7 37.5 ± 5.1 e 22.6 ± 3.1 9.0 ± 0.6 19.9 ± 2.4 13.4 ± 1.3 42.5 ± 4.7 b 19.5 ± 2.4 39.0 ± 3.1 d 22.4 ± 3.6 42.7 ± 6.7 b 20.2 ± 1.5 27.4 ± 3.1 15.7 ± 1.9
13.7 ± 0.9 10.4 ± 1.4 16.2 ± 1.8 23.5 ± 1.2 27.7 ± 1.1 d 6.5 ± 0.2 8.9 ± 0.8 13.2 ± 0.5 8.0 ± 0.8 30.0 ± 3.1 c 16.9 ± 1.1 30.7 ± 0.7 b 19.7 ± 1.9 39.0 ± 3.5 a 19.4 ± 2.1 25.4 ± 1.8 14.2 ± 2.7
70.0 ± 2.8 66.7 ± 1.2 21.6 ± 2.8 86.0 ± 1.9 88.4 ± 1.6 d 70.5 ± 2.2 8.1 ± 3.1 56.7 ± 6.1 43.0 ± 2.6 78.7 ± 4.3 34.1 ± 4.2 81.7 ± 1.1 50.6 ± 1.1 90.6 ± 3.9 b 48.4 ± 1.8 62.2 ± 2.9 21.6 ± 4.2
b. Bark Melaleuca armillaris
27.0 ± 2.7
8.7 ± 1.1
87.9 ± 4.2 e
c. Fruit/seed pod Quercus robur Lagunaria patersonii Platanus orientalis Eucalyptus leucoxylon Melia azedarach Casuarina obesa
66.7 ± 4.1 a 5.2 ± 0.6 7.4 ± 0.2 35.4 ± 5.8 6.4 ± 2.1 8.5 ± 0.6
9.2 ± 0.7 4.2 ± 1.2 4.0 ± 0.8 9.5 ± 1.8 5.9 ± 1.6 5.2 ± 0.2
90.7 ± 2.0 a 14.9 ± 3.2 13.7 ± 2.8 90.1 ± 1.8 c 12.1 ± 3.6 23.0 ± 1.6
d. Flower Pinus radiata
3.7 ± 1.1
0.4 ± 0.1
11.9 ± 2.5
Values are means ± standard deviation (n = 3). Values with different superscript letter are significantly different at p ≤ 0.05. I Values expressed as mg GAE/g dry extracts. II Values expressed as mg quercetin/g dry extracts. III Values expressed as per cent DPPH radical scavenging activity of the extracts.
Cr existed at relatively high levels in pine cones (1.7 ± 0.3 g/g). We also determined the levels of toxic metals (Table 2) that do not have any biological role before recommending the above screened essential mineral-rich plant/tree wastes for utility. The observed concentrations of toxic metals (As, Cd) and metalloids (Al, Pb) were below the environmental safety limits and monthly human intake levels, and are not barred from utility. 3.2. Amount of TP and TF in the studied plant/tree wastes Significant differences in TP and TF content were noticed between different types and parts of plant/tree wastes tested (Table 3). In general the majority of dried leaf extracts showed larger amounts of phenolic compounds when compared to other plant/tree parts (pod, bark and flower). However, one sample, namely the fruit peel of Q. robur had exceptionally high amounts of phenolic constituents and was 2–18× greater than the TP values of the remaining samples investigated. In the case of leaf extracts, M. diosmifolia followed by Pyrus ussusriensis, E. leucoxylon and M. armillaris showed the highest TP level (39.0–42.7 mg GAE/g). P. radiata cones had the lowest phenolic content (3.7 mg/g), followed in rank order by L. patersonii seed pod (5.2 mg/g) < M. azedarach pod (6.4 mg/g) < A. cordata leaf (9.0 mg/g) among all the extracts tested. Since the sample preparation, extraction and determination procedures were exactly the same in all cases, the significant differences observed among their phenolic content in this study is probably due to the intrinsic properties of the plant/tree wastes. The reason for the observed variance in levels of phenolic compounds may be due to the variation in accumulation of these substances in very different tissues and cells (central vacuoles of
guard cells and epidermal as well as sub epidermal cells of leaves and shoots, cell walls, waxes or on external surfaces of fruits and flowers) under the influence of external environmental factors (seasonality, nutrients, salinity, depth, light) and intrinsic factors such as type of tissues, size and age (Hutzler et al., 1998). The TF content in dried leaves of M. diosmifolia, M. armillaris, P. ussuriensis was remarkably high (30–39 mg quercetin/g) compared to that obtained from other tree parts. However, extracts with higher TP value did not always have a higher TF value, as evident for the fruit peel of Q. robur which had a lower TF content (9.2 ± 0.7 mg/g) compared to M. diosmifolia leaf, although the phenol content was higher (66.7 and 42.7 mg/g). The results suggest that different plant/tree extracts contain different levels of TF as a portion of (poly) phenolics. One significant finding of this study is that the prime source of flavonoids for all tree wastes, i.e., A. cordata leaf, accounted for 97.8% flavonoids among the total phenols detected. Flavonoids were also the major constituent in leaves of Morus alba pendula, N. oleander and M. diosmifolia including M. azedarach pod with a concentration between 90 and 95% of the total phenols. Reports are not available in the literature to compare the values determined in the present analysis particularly in case of selected species, specific tree parts and flavonoid content. 3.3. Antioxidant activity by DPPH radical scavenging activity The DPPH free radical scavenging activity of tree wastes is shown in Table 3. Significant differences (p < 0.05) were detected among the 25 tree wastes evaluated. Similar to the total phenolic contents, fruit peel of Q. robur and leaf of M. diosmifolia exhibited the highest (90% DPPH inhibition) and A. cordata leaf followed by P. radiata cone recorded the lowest (8–12% DPPH inhibition) antioxidant potential. All the remaining extracts other than E. leucoxylon leaf and pod, M. armillaris leaf and bark, leaves of Olea europea, Syzgium sp., P. cerasifera, L. laevigatum, P. ussuriensis and Hibiscus tiliaceous rubra (>60%) exhibited intermediate (40–60%) to low (0–40%) antioxidant potential. The percentage of DPPH radical scavenging activity of oak fruit peel found in this study agrees with the findings by Dudonne et al. (2009) on oak wood. However, according to another study documenting eucalyptus leaf extract the value is more than 3 times less that reported here. Lee et al. (2009) discovered a very different antioxidant potential for olive leaf aqueous extracts (37.9% DPPH inhibition) compared to the present study’s results. However, Lee et al. (2009) observed a significantly higher content of phenolic antioxidants in the 80% ethanol, butanol and ethylacetate fractions, thus indicating that the type of solvent used for extraction is an important factor that affects the concentration and activity of (poly) phenols. Li et al. (2014) suggested pear peel as an excellent source of phenolic antioxidants with more than 80% DPPH inhibition, and the pear extracts assayed in the present study displayed similar values. No reports are available in the literature on the other samples to make a comparison possible. 3.4. Exploitation potentials—directions for future research The C-rich E. leucoxylon and M. diosmifolia can be used as substrates in fermentations or biofertilizer preparations, as C is the most significant nutrient that stimulates the growth and activity of the microbes involved. As soil amendments (compost/mulch/manure/biochar), NPK-rich M. azedarach pod and Hibiscus tiliaceous rubra leaf could help to improve soil health and make nutrients more amenable for crop growth and enhance agricultural productivity (Haynes et al., 2015). As N and P are the most limiting nutrients in bioremediation (Kuppusamy et al., 2016), as nutrient additives in problematic soils, these wastes could potentially enhance the natural biodegradation of long-term contaminated sites. M. diosmifolia leaf may be of use as a promising
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source for covering Mg and Co recommended intake. Zn, a mineral element with chemo-preventive features in cancer, needs to be ingested from dietary sources (Dhawan and Chadha, 2010). Owing to its concentration, dried leaves and bark of M. diosmifolia could be highlighted as an alternative to food supplements, which are commonly used to ease deficiencies of this essential element. Elemental composition of P. radiata cones stresses its potential for exploitation as industrial drugs to promote public health particularly to alleviate Fe deficiencies. Notably, fruit peel and whole leaf extracts of Q. robur and M. diosmifolia which are found to be rich in total phenols and polyphenol compounds such as flavonoids may act as powerful reducing agents for the production of nanoparticles (NPs) such as AuNPs, AgNPs, FeNPs, CuNPs or PdNPs (Machado et al., 2013). 4. Conclusions This study provides new knowledge on the metal content and phenol range for a majority of the common plant/tree wastes, and assists in identifying the most resourceful genera of plant/tree wastes. These new data are valuable additions to the database for the fertilizer, remedial, pharmaceutical and food processing industries and represent a significant step toward efficient waste management with economic return. Future research is warranted to confirm the forecasted commercial exploitation possibilities of the potential plant/tree waste extracts screened in this study following a detailed evaluation of the chemical composition, bioavailability and toxicity of each compounds contained in the extracts. Acknowledgments Financial support was provided by the Australian Government and the University of South Australia in the form of an International Postgraduate Research Scholarship (IPRS) to the first author in association with the Cooperative Research Centre for Contamination Assessment and Remediation of Environment (CRC CARE).
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References Blois, M.S., 1958. Antioxidant determination by the use of a stable free radical. Nature 181, 1199–1200. Dhawan, D.K., Chadha, V.D., 2010. Zinc: a promising agent in dietary chemoprevention of cancer. Indian J. Med. Res. 132, 676–682. Dudonne, S., Vitrac, X., Coutiere, P., Woillez, M., Meerillon, J.M., 2009. Comparative study of antioxidant properties and total phenolic content of 30 plant extracts of industrial interest using DPPH, ABTS, FRAP, SOD, and ORAC assays. J. Agric. Food Chem. 57, 1768–1774. EnviraChar, 2013. Challenges. Available from: http://envirachar.com/challenges. php (accessed 18.1.14). Haynes, R.J., Belyaeva, O.N., Zhou, Y.F., 2015. Particle size fractionation as a method for characterizing the nutrient content of municipal green waste used for composting. Waste Manag. 35, 48–54. Hutzler, P., Fischbach, R., Heller, W., Jungblut, T.P., Reuber, S., Schmitz, R., Veit, M., Weissenbock, G., Schnitzler, J.P., 1998. Tissue localization of phenolic compounds in plants by confocal laser scanning microscopy. J. Exp. Bot. 49, 953–965. Khomdram, S.D., Singh, P.K., 2011. Polyphenolic compounds and free radical scavenging activity in eight Lamiaceae herbs of Manipur. Not. Sci. Biol. 2, 108–113. Kuppusamy, S., Palanisami, T., Megharaj, M., Venkateswarlu, R., Naidu, R., 2016. In-situ remediation approaches for the management of contaminated sites: a comprehensive overview. Rev. Environ. Contam. Toxicol. 236, 1–115. Kuppusamy, S., Thavamani, P., Megharaj, M., Naidu, R., 2015. Bioremediation potential of natural polyphenol rich green wastes: a review of current research and recommendations for future directions. Environ. Technol. Innov. 4, 17–28. Lee, O.H., Lee, B.Y., Lee, J., Lee, H.B., Son, J.Y., Park, C.S., Shetty, K., Kim, Y.C., 2009. Assessment of phenolics-enriched extract and fractions of olive leaves and their antioxidant activities. Bioresour. Technol. 100, 6107–6113. Li, X., Wang, T., Zhou, B., Gao, W., Cao, J., Huang, L., 2014. Chemical composition and antioxidant and anti-inflammatory potential of peels and flesh from 10 different pear varieties (Pyrus spp.). Food Chem. 152, 531–538. Machado, S., Pinto, S.L., Grosso, J.P., Nouws, H.P.A., Albergaria, J.T., Delerue-Matos, C., 2013. Green production of zero-valent iron nanoparticles using tree leaf extracts. Sci. Total Environ. 445, 1–8. Maisuthisakul, P., Suttajit, M., Pongsawatmanit, R., 2007. Assessment of phenolic content and free radical-scavenging capacity of some Thai indigenous plants. Food Chem. 100, 1409–1418. Singleton, V.L., Rossi, J.A., 1965. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am. J. Enol. Vitic. 16, 144–158. Trumbo, P., Yates, A.A., Schlicker, S., Poos, M., 2001. Dietary reference intakes: vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc. J. Am. Diet. Assoc. 101, 294–301.
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Assessment of antioxidant activity, minerals, phenols and flavonoid contents of common plant/tree waste extracts Saranya Kuppusamy a,b,c,∗ , Palanisami Thavamani c,d , Mallavarapu Megharaj b,c,d , Ramkrishna Nirola b,c , Yong Bok Lee a , Ravi Naidu b,c,d a
Institute of Agriculture and Life Science, Gyeongsang National University, Jinju 660-701, South Korea Centre for Environmental Risk Assessment and Remediation (CERAR), University of South Australia, Mawson Lakes, SA 5095, Australia c Cooperative Research Centre for Contamination Assessment and Remediation of Environment (CRC CARE), PO Box 486, Salisbury South, SA 5106, Australia d Global Centre for Environmental Remediation (GCER), Faculty of Science and Information Technology, The University of Newcastle, Callaghan, NSW 2308, Australia b
a r t i c l e
i n f o
Article history: Received 7 October 2015 Received in revised form 20 December 2015 Accepted 21 December 2015 Available online xxx Keywords: Agroforestry waste Essential nutrients Heavy metals Polyphenols DPPH activity
a b s t r a c t Extracts of 25 different plant/tree wastes were screened for their phenol and flavonoid contents, antioxidant activity, nutritional and toxicological elemental composition. The commercial exploitation potential of nutrient and polyphenol-rich tree/plant wastes was also discussed. This study is the first to recommend using non-toxic Melaleuca diosmifolia leaf, Melia azedarach pod, Alnus cordata leaf and Pinus radiata cones because they all contain the essential elements (N, P, K, S and Fe) for dietary intake, applications as soil amendments, contaminant biosorbents and substrates for composting or biofertilizer preparation. Fruit peel of Quercus robur, M. diosmifolia leaf and bark, Eucalyptus leucoxylon pod and leaf, Pyrus ussuriensis and Prunus cerasifera leaf aqueous extracts indicated high phenolic content (35–66 mg GAE/g) and antioxidant activity (70–90%). A. cordata and Morus alba pendula leaf emerged as a unique source of flavonoids (>95%). There are greater prospects for the green synthesis of metallic nanoparticles using these polyphenol-rich residues. © 2015 Elsevier B.V. All rights reserved.
1. Introduction One of the most important and overlooked constituents today is ‘minerals’. Polyphenolic compounds are ubiquitous in vegetation, constitute an important part of the human diet, and have aroused much interest due to their antioxidant properties. Flavonoids constitute the largest group of plant phenolics and are very effective antioxidants (Maisuthisakul et al., 2007). In recent days, efforts have been made to transform natural wastes into products of commercial utility as they are very rich in bioactive compounds such as vitamins, minerals, amino acids, polyphenols, etc. Among these bioactive compounds, some essential mineral elements play an important role as cofactors in many enzymatic processes involved in humans, plants, animals and soil microbes. Mineral and polyphenol-rich plant materials are of interest to the cosmetic, nutraceutical, remedial and food industries (Kuppusamy
et al., 2015). For this reason the search for cost-effective mineraland phenol-rich natural materials has continued to this day. To date only limited knowledge is available concerning the use of natural materials especially the abundantly available plant/tree wastes which we dispose of every year at nearly a rate of 24 billion tons (EnviraChar, 2013). Such disposals encompass leaves, fruits, barks, flowers and grass clippings, that are expected to have high levels of minerals and phenolic antioxidants. To date the available literature has not described the full elemental composition and the phenolic ranges of plant/tree wastes. In particular demarcated profiles of the essential, trace and toxic mineral composition of these natural residues are not available. Such information would facilitate their effective utilization. With this in mind, our study was conducted with a primary aim to: firstly, evaluate the elemental composition, phenol, flavonoid contents and antioxidant activity of the so far unexplored, commonly available plant/tree wastes for the first time; and secondly, suggest their potential and practical applications.
∗ Corresponding author at: Institute of Agriculture and Life Science, Gyeongsang National University, Jinju 660-701, South Korea. E-mail address: [email protected] (S. Kuppusamy). http://dx.doi.org/10.1016/j.indcrop.2015.12.060 0926-6690/© 2015 Elsevier B.V. All rights reserved.
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2. Materials and methods 2.1. Chemicals 2,2-diphenyl-1-picryl-hydrazyl (DPPH), Folin-Ciocalteau’s reagent, sodium carbonate anhydrous, aluminium chloride, potassium acetate, methanol and nitric acid (HNO3 ), all of analytical grade were purchased from Sigma–Aldrich (Steinheim, Germany). They included gallic acid, quercetin and ascorbic acid which serve as standards for spectrophotometric assays of total phenols, flavonoids and antioxidant activity, respectively. All solutions were prepared with Milli-Q water (18 cm−1 , Milli-Q, ELGA labwater, UK). 2.2. Plant material Specimens of 25 different plant/tree wastes consisting of 17 leaves [eucalyptus (Eucalyptus leucoxylon), olive (Olea europaea), flame tree (Brachychitona cerifolius), nerium (Nerium oleander), pear (Syzgium sp.), cherry plum (Prunus cerasifera), coastal tea tree (Leptospermum laevigatum), Italian alder (Alnus cordata), cockie’s tongue (Templetonia retusa), casuarina (Casuarina obesa), Manchurian pear (Pyrus ussuriensis), native hibiscus (Alyogyne hakeifolia), bracelet honey myrtle (Melaleuca armillaris), desert ash tree (Fraxinus angustifolia), green honey myrtle (M. diosmifolia), weeping white myrtle (Morus alba pendula) and red cottonwood (Hibiscus tiliaceous rubra)], 1 bark [bracelet honey myrtle (M. armillaris)], 6 fruit/seed pods [eucalyptus (E. leucoxylon), oak (Quercus robur), cow-itch (Lagunaria patersonii), oriental plane (Platanus orientalis), white cedar (Melia azedarach) and casuarina (C. obesa)] and 1 flower [pine (Pinus radiata)] that had fallen off from fullgrown plant/tree species were collected from Mawson Lakes, South Australia between June and December 2014. Collected residues (1 kg of each specimen) were washed with MQ water to remove the adhering soil particles. Then they were air dried at 40 ◦ C for 72 h, grounded to a fine powder and passed through a 0.5 mm sieve to a uniform powder. The powdered sections were stored in a desiccator with polythene sealing.
sodium carbonate), by using SynergyTM HT (Bio-Tek® instruments, Inc., Vermont, USA) multi-detection microplate reader. Samples were diluted (1:5) and were quantified using gallic acid (GAE) as standard. Results were expressed as mg of GAE equivalents per g of dry material. 2.5.2. Total flavonoids (TF) TF content was measured by a modified method described by Khomdram and Singh (2011). The reaction mixture comprised 100 L of extract, 100 L of 10% aluminium chloride and 100 L of 1 M potassium acetate solutions. After 30 min incubation at room temperature, absorbance of the yellow colored mixture was measured at 415 nm using a microplate reader. A standard curve was plotted using different concentrations of quercetin (0–50 g/mL) and the amount of total flavonoids was calculated as quercetin equivalents in mg per g of dry material. 2.5.3. Screening of the extracts for antioxidant potential—DPPH radical scavenging activity (DPPH inhibition) DPPH is a widely used stable free radical to evaluate the antioxidant potential of a sample. DPPH radical scavenging activity of the plant/tree waste extracts was evaluated according to a method outlined by Blois (1958) with slight modifications. Briefly, 60 M of DPPH radical solution in methanol was prepared and 3.9 mL of this solution was mixed with various concentrations of the sample solution. After 30 min, absorbance of the sample (As) was measured at 515 nm. Simultaneously, blank containing 100 L of water was treated as above and its absorbance was recorded as Ab . The DPPH radical scavenging activity was calculated as follows. %DPPH inhibition =
Ab − As × 100 Ab
2.6. Statistical analysis All experimental results were reported as mean values (n = 3; ± standard deviation). Analysis of variance (ANNOVA) and Tukey’s test were carried out using IBM SPSS statistics 20 software package (IBM® Corporation, USA).
2.3. Determination of mineral elements 3. Results and discussion Analysis of mineral elements was carried out after HNO3 (70%) acid digestion of the powdered material by Agilent 7500 c (Agilent Technologies, Tokyo, Japan) Inductively-Coupled Plasma Mass Spectrometer (ICP–MS). The C and N contents of the samples were measured using a Trumac (Leco® Corporation, Michigan, USA) carbon–nitrogen–sulphur analyzer (CNS analyzer). 2.4. Extraction procedure for polyphenol compounds Five mL of boiled water was added to 0.20 g of the sample and the suspensions were left for 24 h in a shaker at room temperature (24 ± 2 ◦ C). The extracts were then centrifuged for 10 min at 3000 rpm and the supernatant collected at 4 ◦ C and used within 24 h to determine phenols, flavonoids and antioxidant activities of the selected plant/tree wastes. All samples were extracted in triplicate. 2.5. Determination of phenolic compounds and antioxidant activity 2.5.1. Total phenols (TP) TP content was determined by a modified version of the Folin-Ciocalteau’s method adapted to micro-scale (Singleton and Rossi, 1965). TP content was evaluated by measuring the variation in absorbance at 660 nm after 45 min of reaction (100 L of extract + 250 L of Folin-Ciocalteau phenol reagent + 1 mL of 20%
3.1. Mineral composition of plant/tree wastes Monitored metal concentrations are presented in Tables 1 and 2. As can be observed in Table 1, significant variability exists in the elemental composition of different tree wastes tested. These substantial differences are likely to account for their distinct beneficial activities when exploited. The highest levels of C were found in E. leucoxylon (506.8 ± 24 mg/g) and M. diosmifolia (502.1 ± 49 mg/g) leaves. M. azedarach pod and Hibiscus tiliaceous rubra leaf recorded substantially higher NPK and Mg followed by leaves of Morus alba pendula and P. cerasifera. The highest Ca, S and Na concentrations were found in dried leaves of A. cordata (52.5 ± 12 mg/g), A. hakeifolia (16.3 ± 5.2 mg/g) and M. armillaris (12.1 ± 2.6 mg/g), respectively. P. orientalis fruit and M. azedarach pod exhibited higher concentrations of Cu (Table 2). M. diosmifolia leaf showed a very high value of Mg (181 ± 19 g/g) and Co (0.7 ± 0.8 g/g) compared to the remaining samples analyzed. Dried leaves of E. leucoxylon were a rich source of Ni (5.4 ± 1.5 g/g). Zn was rich in dried leaves and bark of M. diosmifolia. Iron, the most essential mineral in human health and essential for good cardiovascular health, cognitive development and immune function (Trumbo et al., 2001) was the predominant one in P. radiata cones (514 ± 24 g/g) followed by leaves of M. armillaris (358 ± 58 g/g). The amount of a nutritionally essential mineral that helps in preventing diabetes,
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Table 1 Macro-elemental composition (mg/g dry weight) of the samples considered for the study. Sample
Primary macronutrients C
a. Leaf Eucalyptus leucoxylon Olea europaea Nerium oleander Syzgium sp. Prunus cerasifera Leptospermum laevigatum Alnus cordata Templetonia retusa Casuarina obesa Pyrus ussuriensis Alyogyne hakeifolia Melaleuca armillaris Fraxinus angustifolia Melaleuca diosmifolia Morus alba pendula Hibiscus tiliaceous rubra Brachychitona cerifolius
506.8 473.9 442.7 444.7 448.6 494.1 359.5 466.4 455.5 463.1 401.4 477.7 453.6 502.1 455.1 429.8 454.9
b. Bark Melaleuca armillaris
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
24 59 31 47 18 57 51 39 37 32 39 23 41 49 50 39 22
480.5 448.2 463.0 460.6 464.0 450.9
d. Flower Pinus radiata
± ± ± ± ± ±
P 11.9 11.2 11.7 15.2 14.7 7.6 12.5 16.3 15.4 16.7 21.4 14.1 21.6 9.8 19.1 26.7 14.0
472.8 ± 53
c. Fruit/seed pod Quercus robur Lagunaria patersonii Platanus orientalis Eucalyptus leucoxylon Melia azedarach Casuarina obesa
Secondary macronutrients
N ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
2.7 2.9 1.7 1.2 1.1 2.2 1.8 3.8 2.6 2.4 2.5 1.1 3.8 2.2 1.1 2.9 2.2
4.7 ± 1.9
27 41 24 49 38 32
5.7 9.4 11.7 4.7 21.1 10.7
478.8 ± 57
± ± ± ± ± ±
K 1.9 1.0 3.2 1.8 1.5 1.2 1.1 1.4 0.7 1.1 1.4 1.1 1.5 0.6 2.7 2.0 1.0
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.7 0.9 0.1 0.8 0.3 0.8 0.2 0.6 0.1 0.1 0.3 0.1 0.7 0.5 1.1 1.4 0.2
8.0 9.7 16.3 10.3 24.8 7.1 10.8 14.8 7.6 10.3 14.0 7.9 16.0 6.4 18.9 23.3 17.6
0.4 ± 0.1 1.3 2.7 2.4 1.6 3.7 1.9
4.6 ± 2.1
0.3 1.3 1.9 0.6 3.2 0.5
± ± ± ± ± ±
Ca ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
2.1 1.2 3.7 6.1 3.2 2.1 3.4 5.6 3.8 4.2 3.4 2.5 2.9 1.5 3.9 6.2 5.2
10.3 21.1 18.4 11.6 15.7 4.7 52.5 19.9 15.4 12.5 23.0 5.3 18.8 8.4 18.4 30.3 2.2
4.1 ± 1.5
0.1 0.1 0.1 0.5 1.2 0.1
4.0 21.1 6.6 4.5 18.5 3.5
0.1 ± 0.1
± ± ± ± ± ±
Mg ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
2.2 2.6 3.2 3.1 3.1 1.7 12 3.0 2.4 2.6 1.9 1.2 4.2 1.5 3.2 11 0.2
1.5 0.9 0.5 2.0 2.4 0.8 1.0 1.5 1.1 1.6 1.5 1.6 1.9 1.7 1.7 2.3 0.3
4.6 ± 1.1 1.6 6.3 2.4 1.3 3.6 1.1
2.7 6.3 9.9 7.0 9.4 25.3
0.8 ± 0.2
± ± ± ± ± ±
S ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.1 0.2 0.1 1.3 1.4 0.1 0.2 0.8 0.5 0.4 0.9 0.7 0.7 0.3 0.1 0.9 0.1
1.2 1.5 1.8 2.0 2.0 2.2 0.9 2.5 1.3 1.2 16.3 3.1 4.9 2.1 1.5 2.4 1.1
1.0 ± 0.8 1.0 1.2 3.4 2.8 2.0 9.2
1.3 3.3 0.7 1.0 2.1 0.8
2.0 ± 1.4
± ± ± ± ± ±
Na ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.2 0.7 0.3 1.1 1.0 1.2 0.2 1.1 0.5 0.6 5.2 1.6 2.1 1.0 0.2 0.9 0.8
1.8 ± 0.5
0.2 0.1 0.1 0.2 1.1 0.1
0.4 1.0 1.4 1.1 1.5 1.1
0.3 ± 0.1
± ± ± ± ± ±
4.4 1.0 0.7 3.3 1.2 4.8 0.7 0.8 2.7 0.5 9.2 12.1 1.4 3.9 1.6 0.9 3.7
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
1.0 0.3 0.1 0.9 0.4 1.5 0.2 0.1 0.2 0.1 0.9 2.6 0.1 1.0 0.9 0.2 1.2
8.6 ± 2.1 0.1 0.3 0.4 0.2 0.9 0.3
0.6 ± 0.2
0.8 1.0 1.3 10.3 0.3 2.3
± ± ± ± ± ±
0.1 0.2 0.5 2.0 0.1 0.9
0.8 ± 0.2
Values are means ± standard deviation (n = 3)
Table 2 Trace and toxic elemental composition (g/g dry weight) of analyzed samples. Sample
Essential trace elements Mn
a. Leaf Eucalyptus leucoxylon Olea europaea Nerium oleander Syzgium sp. Prunus cerasifera Leptospermum laevigatum Alnus cordata Templetonia retusa Casuarina obesa Pyrus ussuriensis Alyogyne hakeifolia Melaleuca armillaris Fraxinus angustifolia Melaleuca diosmifolia Morus alba pendula Hibiscus tiliaceous rubra Brachychitona cerifolius
91.0 28.1 59.1 18.0 44.4 28.7 47.7 55.6 75.9 24.0 44.2 38.7 32.8 181 44.7 52.9 4.2
Cu ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
11 3.9 13 4.2 19 11 18 11 19 11 16 9.4 9.6 19 12 18 1.1
7.8 4.9 9.9 10.7 7.7 7.7 7.9 10.4 7.0 5.8 10.7 9.4 7.2 7.8 10.1 6.8 3.3
Toxic metals Zn
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
3.1 1.8 1.9 2.8 2.1 2.4 2.2 3.1 2.7 2.1 3.2 2.8 2.6 4.1 3.4 2.4 0.2
Fe
BDL 19.6 ± 4.2 18.9 ± 4.9 10.7 ± 2.1 10.2 ± 2.4 19.1 ± 3.8 9.3 ± 1.8 17.5 ± 3.9 14.5 ± 4.2 14.7 ± 3.8 22.0 ± 9.1 40.8 ± 6.8 13.1 ± 1.9 12.3 ± 2.8 29.3 ± 10 13.0 ± 6.8 7.4 ± 2.1
51.9 173 54.4 78.1 121 59.7 70.6 116 158 63.1 275 358 138 148 107 103 65.8
Ni ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
12 48 17 21 19 12 11 28 21 19 41 58 11 28 19 26 19
5.4 1.4 0.6 3.4 1.7 0.9 1.2 0.7 2.5 0.6 1.2 1.6 0.5 2.5 1.0 0.7 0.9
Co ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
1.5 0.4 0.1 0.9 0.4 0.1 0.2 0.1 1.0 0.1 0.8 0.4 0.1 0.7 0.1 0.2 0.2
0.03 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.2 0.1 0.2 0.1 0.7 0.2 0.1 0.04
Cr ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.1 0.2 0.9 0.4 0.2 0.2 0.6 0.7 0.5 0.1 0.2 0.9 0.8 0.8 0.9 0.7 0.1
BDL 0.5 ± 0.2 0.4 ± 0.1 0.4 ± 0.2 0.3 ± 0.1 0.3 ± 0.1 0.5 ± 0.1 0.5 ± 0.2 0.6 ± 0.1 0.3 ± 0.1 0.9 ± 0.5 1.5 ± 0.6 0.6 ± 0.1 0.5 ± 0.1 0.3 ± 0.1 0.4 ± 0.1 0.9 ± 0.2
Al 54.6 115 55.0 30.0 64.8 43.0 24.9 89.8 93.9 28.6 174 248 85.8 89.4 66.0 39.8 52.4
As ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
9.2 32 19 7.2 31 17 11 29 27 11 45 36 24 13 21 14 15
0.05 0.1 0.05 0.05 0.1 0.03 0.1 0.1 0.1 0.03 0.1 0.2 0.1 0.1 0.1 0.1 0.02
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.1 0.9 0.1 0.1 0.8 0.1 0.6 0.7 0.5 0.1 0.5 0.8 0.5 0.4 0.2 ± 0.7 0.1
Cd
Pb
0.1 ± 0.09 0.02 ± 0.1 0.1 ± 0.7 0.01 ± 0.1 0.01 ± 0.1 0.02 ± 0.1 BDL 0.2 ± 0.9 0.02 ± 0.1 0.03 ± 0.1 0.1 ± 0.7 0.03 ± 0.1 0.01 ± 0.1 0.01 ± 0.1 0.2 ± 0.8 0.1 ± 0.6 0.1 ± 0.5
BDL 1.0 ± 0.6 0.9 ± 0.2 0.3 ± 0.1 0.6 ± 0.2 0.4 ± 0.1 0.4 ± 0.1 0.6 ± 0.1 0.9 ± 0.2 0.2 ± 0.1 1.3 ± 0.4 2.8 ± 1.2 0.8 ± 0.2 0.7 ± 0.2 0.8 ± 0.2 0.5 ± 0.1 0.3 ± 0.1
b. Bark Melaleuca armillaris
29.5 ± 8.2
9.2 ± 2.4
39.4 ± 11
186 ± 21
0.9 ± 0.2
0.1 ± 0.4
1.0 ± 0.7154 ± 15
0.1 ± 0.7
0.1 ± 0.5
1.8 ± 1.0
c. Fruit/seed pod Quercus robur Lagunaria patersonii Platanus orientalis Eucalyptus leucoxylon Melia azedarach Casuarina obesa
24.7 ± 6.2 17.4 ± 2.7 26.2 ± 10 47.0 ± 14 12.1 ± 5.1 82.5 ± 20
2.1 ± 1.0 4.0 ± 2.5 16.7 ± 2.4 6.7 ± 1.5 16.9 ± 1.9 7.6 ± 2.1
BDL BDL 13.7 ± 6.2 22.7 ± 3.5 29.8 ± 6.4 17.2 ± 2.4
9.2 ± 3.8 37.4 ± 10 110 ± 31 117 ± 41 54.8 ± 11 300 ± 29
0.2 ± 0.1 0.4 ± 0.1 1.5 ± 0.9 1.9 ± 0.6 0.8 ± 0.1 2.2 ± 1.0
BDL BDL 0.1 ± 0.3 0.1 ± 0.4 0.04 ± 0.1 0.2 ± 0.8
BDL 3.9 ± 1.1 BDL 18.8 ± 3.5 0.9 ± 0.1101 ± 29 1.4 ± 0.994.7 ± 14 0.5 ± 0.114.5 ± 9.1 1.0 ± 0.1216 ± 48
BDL 0.04 ± 0.1 0.04 ± 0.1 0.1 ± 0.7 0.05 ± 0.2 0.1 ± 0.5
BDL BDL 0.04 ± 0.1 0.05 ± 0.2 0.1 ± 0.2 0.03 ± 0.1
BDL BDL 0.4 ± 0.1 0.9 ± 0.1 0.2 ± 0.1 2.6 ± 1.0
d. Flower Pinus radiata
11.0 ± 6.4
6.5 ± 2.7
24.5 ± 11
514 ± 24
0.9 ± 0.2
0.3 ± 0.2
1.7 ± 0.3388 ± 21
0.2 ± 0.9
0.04 ± 0.1
5.4 ± 1.1
Values are means ± standard deviation (n = 3). BDL—Below detection limit of ICPMS (Zn = 0.2 g/L; Co = 0.1 g/L; Cr = 1 g/L; As = 0.1 g/L; Cd = 0.1 g/L; Pb = 0.1 g/L).
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Table 3 Total phenol (TP) and flavonoid (TF) contents with antioxidant activity (IP) of the aqueous fractions obtained from the selected plant/tree residues. Plant/tree residue
TPI
TFII
IPIII
a. Leaf Eucalyptus leucoxylon Olea europaea Nerium oleander Syzgium sp. Prunus cerasifera Leptospermum laevigatum Alnus cordata Templetonia retusa Casuarina obesa Pyrus ussuriensis Alyogyne hakeifolia Melaleuca armillaris Fraxinus angustifolia Melaleuca diosmifolia Morus alba pendula Hibiscus tiliaceous rubra Brachychitona cerifolius
42.0 ± 3.6 25.7 ± 1.8 17.4 ± 3.6 32.9 ± 2.7 37.5 ± 5.1 e 22.6 ± 3.1 9.0 ± 0.6 19.9 ± 2.4 13.4 ± 1.3 42.5 ± 4.7 b 19.5 ± 2.4 39.0 ± 3.1 d 22.4 ± 3.6 42.7 ± 6.7 b 20.2 ± 1.5 27.4 ± 3.1 15.7 ± 1.9
13.7 ± 0.9 10.4 ± 1.4 16.2 ± 1.8 23.5 ± 1.2 27.7 ± 1.1 d 6.5 ± 0.2 8.9 ± 0.8 13.2 ± 0.5 8.0 ± 0.8 30.0 ± 3.1 c 16.9 ± 1.1 30.7 ± 0.7 b 19.7 ± 1.9 39.0 ± 3.5 a 19.4 ± 2.1 25.4 ± 1.8 14.2 ± 2.7
70.0 ± 2.8 66.7 ± 1.2 21.6 ± 2.8 86.0 ± 1.9 88.4 ± 1.6 d 70.5 ± 2.2 8.1 ± 3.1 56.7 ± 6.1 43.0 ± 2.6 78.7 ± 4.3 34.1 ± 4.2 81.7 ± 1.1 50.6 ± 1.1 90.6 ± 3.9 b 48.4 ± 1.8 62.2 ± 2.9 21.6 ± 4.2
b. Bark Melaleuca armillaris
27.0 ± 2.7
8.7 ± 1.1
87.9 ± 4.2 e
c. Fruit/seed pod Quercus robur Lagunaria patersonii Platanus orientalis Eucalyptus leucoxylon Melia azedarach Casuarina obesa
66.7 ± 4.1 a 5.2 ± 0.6 7.4 ± 0.2 35.4 ± 5.8 6.4 ± 2.1 8.5 ± 0.6
9.2 ± 0.7 4.2 ± 1.2 4.0 ± 0.8 9.5 ± 1.8 5.9 ± 1.6 5.2 ± 0.2
90.7 ± 2.0 a 14.9 ± 3.2 13.7 ± 2.8 90.1 ± 1.8 c 12.1 ± 3.6 23.0 ± 1.6
d. Flower Pinus radiata
3.7 ± 1.1
0.4 ± 0.1
11.9 ± 2.5
Values are means ± standard deviation (n = 3). Values with different superscript letter are significantly different at p ≤ 0.05. I Values expressed as mg GAE/g dry extracts. II Values expressed as mg quercetin/g dry extracts. III Values expressed as per cent DPPH radical scavenging activity of the extracts.
Cr existed at relatively high levels in pine cones (1.7 ± 0.3 g/g). We also determined the levels of toxic metals (Table 2) that do not have any biological role before recommending the above screened essential mineral-rich plant/tree wastes for utility. The observed concentrations of toxic metals (As, Cd) and metalloids (Al, Pb) were below the environmental safety limits and monthly human intake levels, and are not barred from utility. 3.2. Amount of TP and TF in the studied plant/tree wastes Significant differences in TP and TF content were noticed between different types and parts of plant/tree wastes tested (Table 3). In general the majority of dried leaf extracts showed larger amounts of phenolic compounds when compared to other plant/tree parts (pod, bark and flower). However, one sample, namely the fruit peel of Q. robur had exceptionally high amounts of phenolic constituents and was 2–18× greater than the TP values of the remaining samples investigated. In the case of leaf extracts, M. diosmifolia followed by Pyrus ussusriensis, E. leucoxylon and M. armillaris showed the highest TP level (39.0–42.7 mg GAE/g). P. radiata cones had the lowest phenolic content (3.7 mg/g), followed in rank order by L. patersonii seed pod (5.2 mg/g) < M. azedarach pod (6.4 mg/g) < A. cordata leaf (9.0 mg/g) among all the extracts tested. Since the sample preparation, extraction and determination procedures were exactly the same in all cases, the significant differences observed among their phenolic content in this study is probably due to the intrinsic properties of the plant/tree wastes. The reason for the observed variance in levels of phenolic compounds may be due to the variation in accumulation of these substances in very different tissues and cells (central vacuoles of
guard cells and epidermal as well as sub epidermal cells of leaves and shoots, cell walls, waxes or on external surfaces of fruits and flowers) under the influence of external environmental factors (seasonality, nutrients, salinity, depth, light) and intrinsic factors such as type of tissues, size and age (Hutzler et al., 1998). The TF content in dried leaves of M. diosmifolia, M. armillaris, P. ussuriensis was remarkably high (30–39 mg quercetin/g) compared to that obtained from other tree parts. However, extracts with higher TP value did not always have a higher TF value, as evident for the fruit peel of Q. robur which had a lower TF content (9.2 ± 0.7 mg/g) compared to M. diosmifolia leaf, although the phenol content was higher (66.7 and 42.7 mg/g). The results suggest that different plant/tree extracts contain different levels of TF as a portion of (poly) phenolics. One significant finding of this study is that the prime source of flavonoids for all tree wastes, i.e., A. cordata leaf, accounted for 97.8% flavonoids among the total phenols detected. Flavonoids were also the major constituent in leaves of Morus alba pendula, N. oleander and M. diosmifolia including M. azedarach pod with a concentration between 90 and 95% of the total phenols. Reports are not available in the literature to compare the values determined in the present analysis particularly in case of selected species, specific tree parts and flavonoid content. 3.3. Antioxidant activity by DPPH radical scavenging activity The DPPH free radical scavenging activity of tree wastes is shown in Table 3. Significant differences (p < 0.05) were detected among the 25 tree wastes evaluated. Similar to the total phenolic contents, fruit peel of Q. robur and leaf of M. diosmifolia exhibited the highest (90% DPPH inhibition) and A. cordata leaf followed by P. radiata cone recorded the lowest (8–12% DPPH inhibition) antioxidant potential. All the remaining extracts other than E. leucoxylon leaf and pod, M. armillaris leaf and bark, leaves of Olea europea, Syzgium sp., P. cerasifera, L. laevigatum, P. ussuriensis and Hibiscus tiliaceous rubra (>60%) exhibited intermediate (40–60%) to low (0–40%) antioxidant potential. The percentage of DPPH radical scavenging activity of oak fruit peel found in this study agrees with the findings by Dudonne et al. (2009) on oak wood. However, according to another study documenting eucalyptus leaf extract the value is more than 3 times less that reported here. Lee et al. (2009) discovered a very different antioxidant potential for olive leaf aqueous extracts (37.9% DPPH inhibition) compared to the present study’s results. However, Lee et al. (2009) observed a significantly higher content of phenolic antioxidants in the 80% ethanol, butanol and ethylacetate fractions, thus indicating that the type of solvent used for extraction is an important factor that affects the concentration and activity of (poly) phenols. Li et al. (2014) suggested pear peel as an excellent source of phenolic antioxidants with more than 80% DPPH inhibition, and the pear extracts assayed in the present study displayed similar values. No reports are available in the literature on the other samples to make a comparison possible. 3.4. Exploitation potentials—directions for future research The C-rich E. leucoxylon and M. diosmifolia can be used as substrates in fermentations or biofertilizer preparations, as C is the most significant nutrient that stimulates the growth and activity of the microbes involved. As soil amendments (compost/mulch/manure/biochar), NPK-rich M. azedarach pod and Hibiscus tiliaceous rubra leaf could help to improve soil health and make nutrients more amenable for crop growth and enhance agricultural productivity (Haynes et al., 2015). As N and P are the most limiting nutrients in bioremediation (Kuppusamy et al., 2016), as nutrient additives in problematic soils, these wastes could potentially enhance the natural biodegradation of long-term contaminated sites. M. diosmifolia leaf may be of use as a promising
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source for covering Mg and Co recommended intake. Zn, a mineral element with chemo-preventive features in cancer, needs to be ingested from dietary sources (Dhawan and Chadha, 2010). Owing to its concentration, dried leaves and bark of M. diosmifolia could be highlighted as an alternative to food supplements, which are commonly used to ease deficiencies of this essential element. Elemental composition of P. radiata cones stresses its potential for exploitation as industrial drugs to promote public health particularly to alleviate Fe deficiencies. Notably, fruit peel and whole leaf extracts of Q. robur and M. diosmifolia which are found to be rich in total phenols and polyphenol compounds such as flavonoids may act as powerful reducing agents for the production of nanoparticles (NPs) such as AuNPs, AgNPs, FeNPs, CuNPs or PdNPs (Machado et al., 2013). 4. Conclusions This study provides new knowledge on the metal content and phenol range for a majority of the common plant/tree wastes, and assists in identifying the most resourceful genera of plant/tree wastes. These new data are valuable additions to the database for the fertilizer, remedial, pharmaceutical and food processing industries and represent a significant step toward efficient waste management with economic return. Future research is warranted to confirm the forecasted commercial exploitation possibilities of the potential plant/tree waste extracts screened in this study following a detailed evaluation of the chemical composition, bioavailability and toxicity of each compounds contained in the extracts. Acknowledgments Financial support was provided by the Australian Government and the University of South Australia in the form of an International Postgraduate Research Scholarship (IPRS) to the first author in association with the Cooperative Research Centre for Contamination Assessment and Remediation of Environment (CRC CARE).
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Please cite this article in press as: Kuppusamy, S., et al., Assessment of antioxidant activity, minerals, phenols and flavonoid contents of common plant/tree waste extracts. Ind. Crops Prod. (2015), http://dx.doi.org/10.1016/j.indcrop.2015.12.060