The biological activity of Ferula assa-foetida, Aloe vera, Astragalus sarcocolla and Commiphora
myrrha gum resin powders and their methanol extracts were tested on 5th, fifth instar larvae of the Trogoderma granarium beetle. This evaluation was conducted using bioassays of the repellency effect of the gum resin powders at concentrations of 0.5,0.9,2 and 4%and the fumigants toxicity of the methanol extracts at concentrations of0.2,0.4,0.6 and 0.8%at exposure periods of 24, 48 and 72 hours. The descending order of effective powders starts with the repellency effect at applied concentrations: F.assa-foetida >A.vera >A.sarcocolla >C.myrrha. The F.assa-foetida gum resin powder lead in repellency by providing 100% repellency at all concentrations after 24 hours of exposure. A.vera, A.sarcocolla and C.myrrha (µ1/L air) of the methanol extracts had a descending rating for effectiveness: 0.99, 0.99, 0.98 and 8.33 µ1/L air for F.assa-foetida >A. vera >C. myrrha >A. sarcocolla, respectively, after 72 hours of exposure to the fumigants. This study discussed the potential biological activity of some chemical compounds that possess plant gum resin.
Keywords: monoterpenoids, neurotoxicity, polysulfides, sarcocolla, hing INTRODUCTION The pests that afflict stored grains are considered an economic hindrance for both developed and developing countries. The most dangerous of these pests is the beetle Trogoderma granarium Everts, which belongs to Coleoptera class and the Dermestidae family. The presence of this beetle has been recorded in Southern Europe, Western Africa, Asia and South America. Control measures for Trogoderma granarium Everts began in 1966 in America because the damage caused by the beetle led to an economic loss of $15 m for the United States of America (Kerr, 1988). There is a high probability that the larvae stage of this beetle is the destructive phase for this insect because of its ability to live and survive without food for up to 23 months(Kerr, 1988), as well as its ability to feed on different types of stored food, such as flour
products, oilseeds, dried fruits and dry animal products including milk powder and meat and fat powder and dry fish. Chemical control for this pest is complicated because the larvae can starve for a long time, and they infect food for a long duration(Banks, 1977; Benz, 1987). The use of chemical pesticides as well as fumigants for the control of the discovered species of this insect are methyl bromide and phosphine (OEPP/ EPPO, 1986), but there is a danger of direct, delayed or remaining impacts of the pesticides on humans and animals. Additionally, the repeated use of these chemicals causes biological resistance in controlling insects (Champ and Dyte,1977;Lindgren,1988; Rahman et al., 2009; Boyer et al.,2012). Using the natural alternative of temperature by exposing the seeds to 60 °C for 30 seconds caused a 100% mortality rate in T. granarium insects(Morner et
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al., 1987). Additionally, botanical alternatives with insecticidal properties, despite their use in cooking or medicine, especially in agricultural or rural areas, draws attention to the possibility of use in repelling some insects including arthropods or vermin due to the daily observations or odors of the plants. The most prominent of these plants include Chrysanthemum cinerariifolium (Trevir.) Pyrethrum (Bruce, 1940; Foil and Hogsette, 1994), Azadirachta indica neem(Chagas et al., 2010; Khater, 2012), Mentha piperita( Ehrh.)(Lachance and Grange, 2014),and Ociumum suaveWilld(Obeng-Ofori et al., 1998)because they succeed in toxicity, antifeedant and bioefficacy to many of the pests in stored grains.
Therefore, the objective of this study was to evaluate the repellency effect and the toxic fumigants of Aloe vera, L. Burm.f., Astragalus sarcocolla Dymock, Commiphora myrrha L and Ferula assa-foetida L. These plants have world-wide therapeutic uses in folk and local medicine (Eigner and Scholz, 1999; Abd El-Razek et al., 2001; Jaradat et al., 2017),as well as in the Kingdom of Saudi Arabia(Alqasoumi, 2012; Alshammari, 2016), against 5th, fifth instar larvae of Trogoderma granarium Everts.
MATERIALS AND METHODS Breeding the insect: The insects were collected from different types of stored grains including wheat, grit, and oats and were cultured for three months in the incubator at a temperature of 28 ± 2 °C with a relative humidity of 70-60%.The insects were placed in 200 g of sterile wheat in 500-ml containers. The cultures were covered with a muslin cloth, and the cap was fixed with a rubber band. The containers were incubated in the incubator and renewed after each generation. The newly molted 5 th instar larvae were used in all experiments with three replicates, with 10 larvae in each replicate. According to Musa et al.(2009),5 th instar larvae are considered the most gluttonous age.
Preparation of plant powders: The finest gum types were purchased for the study, as shown in Table I, from the medicinal plants markets in Alkharj city. The plants were washed and dried in the shade for one month, and the fresh Ferul aassa-foetida gum took six complete months to dry. Then, the plants were ground by a high-voltage electric mill to a very fine powder. The resulting powder was passed through a 20 mess sieve to obtain a fine powder and was then kept refrigerated in a glass container until use.
Preparation of methanol extract: For the crude extraction, 100% methanol was used as a solvent, and 500 g of each gum powder sample was soaked in 750 ml of methanol and kept in the lab for 5 days with continuous manual stirring of the extract. The extract was then filtered by using a rotary evaporator. Preparations of solutions: According to (Asrar et al., 2016),solutions of crude methanol extract at 2%, 4%, 6% and 8% concentrations were prepared by dissolving 0.2,0.4,0.6 and 0.8ml of the crude methanol extract In 0.8, 0.6, 0.4 and 0.2 ml of methanol. Repellency bioassay: The (Naworth,1973) method was followed with some modifications in assessing the repellency effect of the gum resin plant powders against the 5 th instar larvae of the studied insect. We used a wide plastic dish with a diameter of 15 cm and a height of 2.5 cm and a small dish with a diameter of 8.5 cm and a height of 1.3 cm. The small dish was placed and fixed in the middle of the large dish with adhesive material after separately placing 15 g of wheat grain in each small dish. Then, the plant powder concentrations were mixed with a weight / weight ratio for each dish with three replicates, and 10 fifth-age newly molted larvae were then inserted into the small dish. The nozzle of the large dish was covered with a muslin cloth and tied with a rubber band. After that, the number of larvae that escaped from the small dish to the large plate after a period of 24,48 and 72 hours was recorded. The percentage for repulsion (PR)was calculated per (Talukder and Howse, 1994)where PR =Percent repellency NT=The number of larvae trapped in the dietary medium NE=The number of larvae escaped from the treated dietary medium PR% = NT-NE x100 NT+NE NT: The repellency was assessed and classified in according to McGovern et al.(1977): Class I= 0.1-20 weak repellence Class II= 20.1-40 repellent to some extent Class III= 40.1 -60 medium repellent Class IV = 60.1 – 80 very good repellent Class V= 80.1-100 high repellent
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Table I. Names the Gums resins tested of the Repellency and Fumigant Toxicity.
Scientific name
Family name
Plant part
Common
name
Active compound
References
Aloe vera ,L. Burm.f.
Liliaceae
leaves
aloe gum
Sesquiterpene
oxygenated compounds: lactones , limonene,
B-caryophyllen, Glycosides (alion,
barbalion)
Guenther 1972; Karr et al.,1990; Nerio et al.,2010
Celestino et al 2013; Khan et al.,2014;
Boudreau et al .,2006
Astragalus sarcocolla Dymock
Leguminosae
roots
sarcocolla
Triterpene, monoterpenes
glycosides and oxygenated compounds:
flavonoids saponins
Guenther 1972; Nerio et
al.,2010; Khan et al.,2014 Alshammari 2016; Jaradat
Table II. Repellent activity of A.sarcocolla A.vera, C.myrrha and F.assa-foetida gum resins powders on Larvae (5st instar) T.granarium after 72h.
The means followed by the same letter (in the same column) are not significantly different at the 0.05 level of probability.
**Differences
between means are highly significant at 0.01 level of probability.
Treatment Con. µg/cm
²
Repellent% ± S.E
Repellency class
F L.S.D.0.05
L.S.D.0.
01 Slope ±
SE Intercep
t 95%confidence
Ferula assa-foetida
0 .00±.000
V
--
--
--
4.590± 0.483
-1. 267
Lower upper
4 30.00±.000 -1.459-
-1.076-
2 30.00 ± .000
0.9 30.00 ± .000
0.5 30.00 ± .000
Aloe vera
0 .00±.000
IV 5.907* 14.33
24.66
0.506 ± 0.05
-0.856 -.952- -0.760-
4 24.67±1.667
2 18.33±4.667
0.9 14.33±4.667
0.5 11.00±5.000
Commiphora myrrha
0 .00±.000
III
1.618
15.00
15.00
0.276±0.044
-0.949
-1.047- -0.852-
4 15.00±5.000
2 12.67±1.667
0.9 7.33±7.333
0.5 11.00±4.933
Astragalus sarcocolla
0 .00±.000
IV 12.89**
22.00
10.00
0.497±0.048
-1.000 -1.099- -0.901-
4 21.67±.333
2 22.00±.577
0.9 10.00±3.512
0.5 7.67±4.702
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Table III. Fumigant toxicity of A.sarcocolla ,A.vera, C.myrrha and F.assa-foetida gum resins Methanol Extracts on
Larvae (5st instar) of T.granarium after 24 and 48 h.
Treatment Interval Mean± S.E F
95% Confidence Interval
Lower Bound Upper Bound
Ferula assa-
foetida
24 9.600
a±1.794 4.528 3.889 15.311
48 7.200 a±1.131 9 3.599 10.801
Aloe vera
24 .000
a±.00 -- .000 .000
48 3.400
a±.392 37.696 2.154 4.646
Commiphora
myrrha
24 5.600
a± 0.535 50.860 3.896 7.304
48 7.000a±0.748 24.143 4.618 9.382
Astragalus
sarcocolla
24 2.200
a± 0.216 34.714 1.513 2.887
48 2.400a±1.068 7.737 -.998- 5.798
The means followed by the same letter (in the same column) are not significantly different at the 0.05 level of
probability
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Table.IV. Fumigant toxicity of A.sarcocolla ,A.vera, C.myrrha and F.assa-foetida gum resins Methanol Extracts on Larvae of T.granarium after 72h.
Treatment
Con.µ1/
L
Mortality % ±
SE
F
L.S.D.0.0
5
LC50 (µ1/ L air)
LC95 (µ1/ L air)
Slope ±
SE
95%confidence
F.assa-foetida
0 .00±.000
10**
10
0.997
2.497
1.097± 0.240
Lower Upper
0.8 10.00±2.309
-1.219-
-0.969- 0.6 10.00 ±0.577
0.4 10.00 ±0.577
0.2 10.00 ±2.000
A.vera 0 .00±.000
0.452 -
0.984
2.212
1.340 ± 0.253
-1.454- -1.183-
0.8 10.00±7.211
0.6 9.33±6.566
0.4 8.67±6.766
0.2 7.00±6.506
C.myrrha 0 .00±.000
2.256
10
0.997
2.497
1.097± 0.240 -1.219- -0.969-
0.8 10.00±0.577
0.6 10.00± 0.577
0.4 10.00 ±
2.517
0.2 10.00±6.110
A.sarcocolla 0 .00±.000
3.762*
22
8.333
1.843
2.102± 0.353
-
2.443-
-
2.016-
0.8 8.33± 2.333
0.6 5.00± 2.000
0.4 3.00± 2.082
0.2 1.33± 0.667
The means followed by the same letter (in the same column) are not significantly different at the 0.05 level of
probability. **Differences between means are highly significant at 0.01 level of probability.
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Fumigants bioassay: In accordance with (Ling et al., 2009), with some modifications, the activity of the fumigants for the methanol extracts was tested on 30 newly molted 5 th instar larvae. The methanol extracts were distributed evenly over three 500-ml glass jars with a 20 g cotton ball with a diameter of 1 cm treated with 1 µof each of the concentrations of the methanol extracts for all tested resins. The control cotton ball was treated with methanol only. The oil was injected in the middle of each cotton ball to allow volatilization to avoid direct contact with the remaining residues. Before being placed inside the jars, both the oil and methanol were left to enter the treated inserts after being left to dry for five minutes in the laboratory conditions in the fume hood. Food (a few wheat grains) was placed in the treatment and control containers, and three replicates were used per concentration and the control in a completely randomized design. The mortality number was recorded after 24, 48 and 72 hours of the exposure time by average and accumulative percentages, respectively.
Statistical analysis: All data were statistically analyzed using SPSS statistical analysis one way analysis of variance (ANOVA, version 11) (Bluman, 2007). Means were compared using the least significant difference (L.S.D) at the 0.10 level.
RESULTS
The repellency impact of the gum resin plants powders on the 5 th instar larvae are displayed in Table II ,depicting that all treatments have the mean significant difference at the 0.10 level. The F. assa-foetida powder is superior in the repellency activity to the larval exposed for all exposure periods and at all tested concentrations, while treatment with A.vera, A.sarcocolla and C.myrrha repellency after 72 hours.In contrast, the highest tested concentration gave a 4% repellency ratio: 83.3%, 76.7%, and 73.3% when treated with A. sarcocolla, A. vera and C. myrrh after 72 hours of exposure to the powders of these plants. It is interesting to note that the direct repellent impact on the larvae after 24 hours of exposure to 4% concentration of F. assa-foetida, A. vera, A. sarcocolla and C. myrrh had repellent ratios of 100%,76.7%,70% and 36.7%, respectively. Additionally, another important observation is the low rate of repellency from 76.7 to 73.3 and the corresponding stability at a ratio of 73.3 after 48 and
72 hours when treated with A. sarcocolla concentrations of 2% and 4%, respectively.
There is gradual increase for the activity of repellency for all treatments after 72 hours. One of the behavioral changes observed on the larvae after 24 hours of treatment with all concentrations of F. assa-foetida and high concentrations 2 and 4% of C. myrrha, A. sarcocolla and A. vera was the escape of the larvae to the cloth cover with a clinging action, and with an increased treatment time, there was a disturbance in their motion and curling. However, the larvae exposed to F. assa-foetida were clinging to the cover of the treatment dishes and were calmer., Table II depicts the rate of repellency from the 6 levels of repellency for F. assa-foetida C. myrrha, A. vera and A .sarcocolla at levels V, IV and III. All treatments proved significant effects at levels of probability 0.05 and 0.10 for A. vera, A. sarcocolla, and. F. assa-foetida
The toxic effects of methanol extract fumigants: Tables III and IV compare the effectiveness of gum resin methanol extracts on 5 th instar T. granarium larvae. The LC50 (µ1/L air) of the methanol extracts are listed in a descending rating for effectiveness: 0.99, 0.99, 0.98 and 8.33 for the F. assa-foetida>A. vera>C. myrrha>A. sarcocolla after 72 hours of exposure to their respective fumigants. The treatments proved significant effects at levels of 0.05 and 0.10 for A. sarcocolla and F. assa-foetida . The F. assa-foetida methanol extract exhibited a high toxicity effectiveness that killed100 percent of 5 th instar larvae after 24 hours at all concentrations of F. assa-foetida , and this also occurred the highest concentration of 0.8% percent for A. vera after the same duration and at all concentrations after 72 hours of exposure to C. myrrha. The fumigants of the methanol extracts from F. assa-foetida and C. myrrha demonstrated a considerable effective toxicity after 24 hours of larval exposure at the concentration of 8%, with a mortality rate of 14% and 10% for the two plants. In contrast to the toxic effect of the methanol extract of A. vera, which demonstrated a 70% mortality rate after 72 hours, the methanol extract of A. sarcocolla had a lethal effect, gradually increasing with increased concentration and exposure time, with a mortality rate of13.3% and 83.3% for concentrations of 2% and 8%, respectively, after the 72 hours of exposure. Changes in the larvae behavior during their exposure to the methanol extract fumigants for the experimental plants included impaired mobility and appearing semi-narcotic with
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the treatment of F. assa-foetida , with black coloring of the body and a movement disorder with curling during the treatments with A. sarcocolla, A. vera and C. myrrha. DISCUSSION The powders and extracts of plant methanol tested in this study proved effective in the repulsion and induction of toxicity of vapors in the 5th instar larvae of T. granarium. Based on previous research on the efficacy of certain plant products for the safe control of human food pests in the store and the field without residues harmful to humans, animals, plants and environmental health, this activity can be attributed to the biochemical content of tested plants and their toxic effects on insects(Ansari et al.,2000;Chaubey, 2007;Sultana et al.,2016; Showler, 2017). The effectiveness of the repellent was evident from the beginning of the experiment, especially for the F. assa-foetida, A. vera and C. myrrha powders, which included persistence with the progression of the exposure time. Related to F. assa-foetida, Rafi (2002),evaluated the high repellent and toxicity activity of the F. assa-foetida resin extract to Tribolium castaneum and Ephestia kuebneilla . Additionally, Peyrovi et al.(2011), indicated that there was a strong repellent and toxicity activity for the F. assa-foetida resin essential oil against the adult carob moth. Bhalerao (2014) reported a toxicity efficiency of Aloe vera gum extract when mixed with 4 g/4 g of Tribolium castaneum food after 72 hours of treatment. The methanol extracts have a rapid efficiency during the first a hours of the exposure for all tested plants. According to Wei et al.(2007), some plants use their biochemical defenses for protection against attacking insects, while Schardl and Chen(2010), and Subramaniam and Kaushik(2014),considered the biochemical defense compounds to be secondary metabolites since they include phenols, resins, and saponins. Adeyemi and Mohammed(2014)reported that the secondary metabolites contain various concentrations of pathogens and cellular structures. While Nawrot et al.(1986),Jacobson(1966)and Chapman(2003),indicated the mixture of secondary plant metabolites increases diversification, which provides plants with an ability to attract or deter most natural enemies, including arthropods or insects, and this treatment has led to a decrease in the development of resistance to insecticides (Chiu,
1989). Banchio et al.(2003), Tunón et al.(2006), Pulpati et al.(2008) and IIeke and Oni(2011) reported toxicity, growth inhibition, feeding deterrent, molting disorders and repellent properties as a result of some medicinal plants because they possess a variety of biological compounds; moreover, plants induce antimicrobial, antioxidant, cytotoxic, phytotoxic, insecticidal and anticancer growth properties. Accordingly, those biological impacts could be a main reason for the effectiveness of the tested risen plants in this study. Additionally, the studied plants possess the biological compounds. Table I summarizes some of the biological compounds that have potent insecticide effects, as demonstrated in previous studies(Shaaya et al., 1997; Erler, 2005; Bakkali et al., 2008; Asrar et al., 2016). The monoterpenoids are the main toxic component of plant extracts used against insects (Coats et al., 1991; Ahn et al., 1998; Khan et al., 2014).The monoterpenoids have a high volatility and are lipophilic and these characteristics could have effects on the physiological functions of the treated larvae by penetrating the insect's cuticle(Richards, 1978; Lee et al., 2002).
Moreover, the monoterpenoids may be responsible for the treated larvae mortality and cause the color changes in the body of the larvae prior to death via the methanol extracts. The methanol extract of the A. sarcocolla caused to the appearance the white spots with some scratches in the larval cuticle, although the larvae were not fed the food that was served in the fumigant experiment jars. The scratches may be due to the loss of water content from the larval bodies, which then distributed the physiological functions(Sousa et al., 2005; Asrar et al., 2016).All the tested plants are rich with oxygenated compounds (see Table I). Tunón et al.(2006),indicated high repellent activities of the oxygenated compounds on the tick Ixodes ricinus.
The expected shocking effect or impairment of the respiratory activity for treated larvae for the F. assa-foetida and A. vera treatments is likely caused by the strong odor due to a high content of as disulphide(Kapoor, 1990)and by the bitter taste of glycoside alion, Celestino et al.(2013),from F. assa-foetida and A. vera, which may also be responsible for the strong odor.
Bisseleua et al.(2008), Kumar et al.(2008) and Muto-Fujita et al.(2017)considered the important role of the host plant odors; the air pollution by the odors of the non-host plant impacts the food searching behavior
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of insects. This suggests that the strong odors cause impairment on respiratory activity by overlapping with the air around the treated larvae, and this led to the compulsory closing the respiratory spiracle and thus a high mortality of larvae when exposed to methanol extracts fumigants F. assa-foetida, A. vera, and C. myrrha. This conclusion agrees with an opinion from Ivbijaro(1984),that plant products that distinguish larvicidal activity may have a chemical and physical toxicity. Clearly, the resin plants tested in this study have a larvicidal activity. The continued reduction of the repellency activity of the A. sarcocolla powder on the larvae with time progression in comparison with the beginning of treatment indicates that the plant powder loses ’repellency activity or become acceptable to the larvae since a number of larvae that previously escaped at the beginning of the treatment returned. This result is consistent with previous studies, which revealed a high mortality versus a lower repellency with increased exposure times after treatment(Haq et al., 2005; Nana et al., 2014; Asrar et al., 2016). Neurotoxicity is apparent for the treated larvae with the methanol extracts fumigants for all the tested plants. The most important and prominent evidence is the disturbance in movement, coiling and lying on the back, where the larvae were less active and weak at the first hours of their exposure when treated with the methanol extract from F. assa-foetida. A number of previous researchers have explained that the occurrence of neurotoxicity is the result of the effect of the monoterpenoide, which inhibits the acetyle-cholinesterase enzyme activity(Enan, 2001) and cytochrome P450 (De-Oliveira et al., 1997). However, (Omolo et al., 2004; Odalo et al., 2005; Wang et al., 2006, 2014) suggest that the terpenoids, sesquiterpenoid and some compounds from monoterpenoide are repellants against Anopheles gambia(Diptera) and coleopterans(Papachristos and Stamopoulos, 2002; Khan et al., 2014).
CONCLUSION
This study highlights the effectiveness and high capacity of methanol extract powders from the gum resins of A. sarcocolla, C. myrrha, A. vera and F. assa-foetida for the protection of stored wheat grains against the T. granarium beetle larvae. The success in our discovery and development of the plants for use as natural insecticides have great and direct
benefits for generations of humanity and agricultural wealth.
ACKNOWLEDGMENTS
I would like to thank M. Al-roees, A. Al-Dosari, S.Qahtaniand, M. Al-Dosari for the technical assistance from the Prince Sattam Bin Abdul-Aziz University, the College of Science and Humanities, and the Department of Biology for their invaluable help to complete this study.
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