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. 2022 Jun 24;11(13):1682. doi: 10.3390/plants11131682

Novel Pesticidal Efficacy of Araucaria heterophylla and Commiphora molmol Extracts against Camel and Cattle Blood-Sucking Ectoparasites

Mohamed M Baz 1,*, Hanem F Khater 2, Rowida S Baeshen 3, Abdelfattah Selim 4, Emad S Shaheen 5, Yasser A El-Sayed 1, Salama A Salama 6,7, Maysa M Hegazy 1,6
Editors: Maria João Rodrigues, Catarina Guerreiro Pereira
PMCID: PMC9269226  PMID: 35807634

Abstract

Botanical insecticides are promising pest control agents. This research investigated the novel pesticidal efficacy of Araucaria heterophylla and Commiphora molmol extracts against four ectoparasites through treated envelopes. Seven days post-treatment (PT) with 25 mg/mL of C. molmol and A. heterophylla, complete mortality of the camel tick, Hyalomma dromedarii and cattle tick, Rhipicephalus (Boophilus) annulatus were reached. Against H. dromedarii, the median lethal concentrations (LC50s) of the methanol extracts were 1.13 and 1.04 mg/mL and those of the hexane extracts were 1.47 and 1.38 mg/mL, respectively. The LC50 values of methanol and hexane extracts against R. annulatus were 1.09 and 1.41 plus 1.55 and 1.08 mg/mL, respectively. Seven days PT with 12.5 mg/mL, extracts completely controlled Haematopinus eurysternus and Hippobosca maculata; LC50 of Ha. eurysternus were 0.56 and 0.62 mg/mL for methanol extracts and 0.55 and 1.00 mg/mL for hexane extracts, respectively, whereas those of Hi. maculata were 0.67 and 0.78 mg/mL for methanol extract and 0.68 and 0.32 mg/mL, respectively, for hexane extracts. C. molmol extracts contained sesquiterpene, fatty acid esters and phenols, whereas those of A. heterophylla possessed monoterpene, sesquiterpene, terpene alcohols, fatty acid, and phenols. Consequently, methanol extracts of C. molmol and A. heterophylla were recommended as ecofriendly pesticides.

Keywords: Boophilus annulatus, Hyalomma dromedarii, Hippobosca maculata, Haematopinus eurysternus, phenols, sesquiterpene

1. Introduction

Blood-feeding arthropods are serious pests of worldwide distribution, including the camel tick, Hyalomma dromedarii (Koch, 1844); cattle tick, Rhipicephalus (Boophilus) annulatus, formerly Boophilus annulatus (Say, 1821), (Acari: Ixodidae); the adult cattle louse fly, Hippobosca maculata Leach (Diptera: Hippoboscidae); and the shortnosed cattle louse, Haematopinus eurysternus (Nitzsch, 1818), (Psocodea: Haematopinidae). Haematophagous pests cause dermal damage to be grazing animals, leading to severe economic loss because of blood loss, irritation, general stress, damaged skin and hide, retarded growth, weight loss, depression of the immune system, decreased meat and milk production, and transmission of life-threatening diseases [1,2,3].

The prevention of arthropod-borne diseases relies on effective pest management strategies [4,5,6]. Even though the employment of conventional pesticides and repellents represent a worthy solution to avoid arthropod bites, they resulted in serious environmental risks and unfavorable effects on non-target creatures, animals, and humans, and contaminated dairy and meat products [6] and development of resistant strains of pests; therefore, searching for alternative ways of pests control is an urgent need [3,7,8,9,10,11,12,13,14,15].

Some other approaches could be used for controlling pests, such as botanicals and biological control, vaccination, photopesticides, and acids [16,17,18,19,20,21,22,23]. Searching for alternative control strategies, mainly from plant-based resources, is a promising field [5].

Botanicals have been well- known for their medicinal properties [24] since ancient times [25] and induce anthelmintic, antiprotozoal, antiviral, antifungal, and antibacterial [26,27,28,29,30,31,32] and pesticidal effects [14,15] such as ovicidal [33,34], larvicidal and insect growth regulating effects [19,35,36,37,38,39,40,41,42,43,44,45,46,47,48] as well as adulticidal and repellent properties [8,33,34,39,45,46,49,50,51,52,53]. Botanicals are characterized by high efficiency against pests and prevention of their associated diseases, safety to non-target organisms [5,10,44], and biodegradation [5,11].

Myrrh oil-resin, Commiphora molmol Engler (Sapindales: Burseraceae) is an oleo-gum resin that grows in North-east Africa and was used as a house fumigant for pest control by Ancient Egyptians [25]. It has antiparasitic [54] and molluscicidal effects [25,55] and its sesquiterpene-rich fractions induce antibacterial and antifungal activities [56]. C. molmol has pesticidal effects against the green bottle fly and mosquitoes [57,58,59].

The Polynesian pine, Araucaria heterophylla Salisb (A. excelsa) (Pinales: Araucariaceae) is an ornamental evergreen coniferous tree. Araucaria plants exhibit several pharmaceutical potentials, including anti-inflammatory, antiulcerative, antiviral, antimicrobial, neuroprotective, and anti-depressant [60]. A. heterophylla has an insecticidal effect against mosquitoes [61,62]. It is worth mentioning that the safety of C. molmol [63,64] and A. heterophylla [59] had been confirmed. Because botanicals decay faster than most synthetic pesticides, they are more environmentally friendly and less likely to kill beneficial insects [14,15]. As a result, we hypothesize that A. heterophylla and C. molmol plant resins contain a variety of active biological components that could be used to control pests without contaminating the environment, making them a viable alternative to industrial pesticides. The study’s main goals were to investigate the novel pesticidal effect of methanol and hexane extracts of myrrh and Polynesian pine against four camel and cattle blood-sucking ectoparasites, calculate their lethal concentration values to kill 50, 90, and 95% of the exposed ectoparasites (LC50, 60, and 95, respectively), and investigated their phytochemical analyses.

2. Results and Discussion

2.1. Effect of the Plant Resin Extracts on Arthropods

Bloodsucking arthropods have an elegant method of delivery for a wide range of infectious agents [4], and their safe control is very crucial. This work evaluated two plant extracts of A. heterophylla and C. molmol against four arthropods, H. dromedarii (camel tick), R. annulatus (cattle tick), Hi. maculata (cattle louse fly), and Ha. eurysternus (cattle louse). The data expressed dose and time-dependent efficacy, a similar response was observed [52,65].

All plant extracts in this study showed moderate to high toxic effects against cattle and camel ectoparasites after 24 h of exposure, and methanol extracts were more effective than hexane extracts. The mortality percent (MO%) seven days PT of H. dromedarii with 12.5 mg/mL methanol extracts of C. molmol and A. heterophylla were 100% with LC50 (50%, median lethal concentration) = 1.13 and 1.04 mg/mL, respectively); whereas those of hexane extracts were 100% PT with 25 mg/mL (LC50 = 1.47 and 1.38 mg/mL, respectively (Table 1 and Table 2).

Table 1.

The efficacy of the plant extracts of Commiphora molmol and Araucaria heterophylla against the Camel tick, Hyalomma dromedarii.

Mortality % (Mean ± SE)
Plant Extracts Concentration (mg/mL) Methanol Hexane
1 Day 3 Days 7 Days 1 Day 3 Days 7 Days
Commiphora molmol 0 0.00 ± 0.0 fC * 3.33 ± 3.33 fB 6.67 ± 3.33 eA 0.00 ± 0.0 fC 3.33 ± 3.33 fB 6.67 ± 3.33 fA
1.6 16.67 ± 6.67 eC 36.67 ± 3.33 eB 63.33 ± 3.33 dA 13.33 ± 3.33 eC 30.00 ± 5.77 eB 53.33 ± 6.67 eA
3.1 30.00 ± 5.77 dC 63.33 ± 3.33 dB 86.67 ± 3.33 cA 23.33 ± 3.33 dC 46.67 ± 3.33 dB 66.67 ± 6.67 dA
6.3 53.33 ± 3.33 cC 73.33 ± 3.33 cB 93.33 ± 3.33 bA 40.00 ± 5.77 cC 66.67 ± 6.67 cB 76.67 ± 6.67 cA
12.5 73.33 ± 8.82 bC 80.00 ± 5.77 bB 100.0 ± 0.00 aA 60.00 ± 5.77 bC 73.33 ± 8.82 bB 86.67 ± 8.82 bA
25 86.67 ± 6.67 aC 90.00 ± 5.77 aB 100.0 ± 0.00 aA 76.67 ± 13.33 aC 80.00 ± 5.77 aB 100.0 ± 0.00 aA
Araucaria heterophylla 0 0.00 ± 0.0 fC 3.33 ± 3.33 fB 6.67 ± 3.33 dA 0.00 ± 0.0 fC 3.33 ± 3.33 fB 6.67 ± 3.33 fA
1.6 20.00 ± 0.00 eC 46.67 ± 3.33 eB 73.33 ± 3.33 cA 13.33 ± 6.67 eC 33.33 ± 3.33 eB 56.67 ± 8.82 eA
3.1 43.33 ± 8.82 dC 73.33 ± 3.33 dB 86.67 ± 8.82 bA 30.00 ± 5.77 dC 56.67 ± 3.33 dB 76.67 ± 8.82 dA
6.3 63.33 ± 8.82 cC 80.00 ± 10.00 cB 100.0 ± 0.00 aA 43.33 ± 3.33 cC 66.67 ± 6.67 cB 80.00 ± 5.77 cA
12.5 80.00 ± 5.77 bC 90.00 ± 5.77 bB 100.0 ± 0.00 aA 60.00 ± 5.77 bC 76.67 ± 3.33 bB 90.0 ± 10.00 bA
25 93.33 ± 3.33 aC 100.0 ± 0.00 aB 100.0 ± 0.00 aA 76.67 ± 3.33 aC 90.00 ± 10.00 aB 100.0 ± 0.00 aA
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* letters refer to significant difference; a–f: There is no significant difference (p > 0.05) between any two means, those within the same column have the same superscript letter; A, B & C: There is no significant difference (p > 0.05) between any two means for the same solvent, those within the same row have the same superscript letter. Three replicates were used for each concentration and 10 adult pests per replicate were used.

Table 2.

Lethal concentration values of plant extracts of Commiphora molmol and Araucaria heterophylla against Hyalomma dromedarii.

Days Plant Extracts Solvents LC50 (95%CL) * LC90 (95%CL) LC95 (95%CL) Equation ** X2
1 Commiphora molmol Methanol 5.76 (4.91–6.75) 30.29 (22.91–44.26) 48.48 (34.50–77.54) 1.779 ± 0.157X 0.975
Hexane 36.08 (31.12–56.66) 442.56 (315.42–498.16) 1731 (1420.15–2125.02) 0.613 ± 0.140X 40.179
Araucaria heterophylla Methanol 4.16 (3.52–4.85) 19.94 (15.69–27.49) 31.10 (23.15–46.50) 1.880 ± 0.165X 0.705
Hexane 8.07 (6.71–9.86) 60.03 (40.13–107.74) 106.00 (64.94–217.67) 1.471 ± 0.149X 0.867
3 Commiphora molmol Methanol 2.47 (1.78–3.15) 24.22 (17.05–41.08) 46.25 (29.28–93.94) 1.293 ± 0.153X 4.165
Hexane 4.08 (3.12–5.11) 48.16 (30.61–97.54) 96.95 (54.49–241.38) 1.195 ± 0.144X 0.350
Araucaria heterophylla Methanol 1.78 (1.31–2.22) 9.85 (7.84–13.47) 15.99 (11.94–24.42) 1.726 ± 0.188X 6.546
Hexane 3.17 (2.42–3.93) 28.26 (19.87–47.55) 52.53 (33.48–103.88) 1.349 ± 0.151X 2.469
7 Commiphora molmol Methanol 1.13 (0.79–1.45) 4.55 (3.85–5.54) 6.76 (5.55–8.80) 2.121 ± 0.233X 1.488
Hexane 1.47 (0.79–2.13) 24.60 (15.41–56.27) 54.62 (28.92–175.54) 1.049 ± 0.167X 0.793
Araucaria heterophylla Methanol 1.04 (0.67–1.33) 3.13 (2.65–3.92) 4.27 (3.49–5.95) 2.687 ± 0.433X 0.199
Hexane 1.38 (0.90–1.84) 10.09 (7.80–14.53) 17.73 (12.65–29.71) 1.483 ± 0.182X 7.301
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* LC50, 60, and 95 values = lethal concentration that kills 50, 90, and 95% of the exposed ectoparasite; (95%CL) = lower and upper confidence limit; ** Regression line equation; X2 = chi-square; Significant at p < 0.05 level.

Similar to the response of camel ticks, the results of this work showed that plant extracts effectively controlled the cattle tick, R. annulatus because 100% mortality% was reached seven days PT with 12.5 mg/mL methanol extracts of C. molmol and A. heterophylla (LC50 = 1. 09 and 1.41 mg/mL, respectively) whereas those of hexane extracts were reached PT with 25 mg/mL (LC50 = 1.55 and 1.08%, respectively) (Table 3 and Table 4).

Table 3.

Efficacy of the plant extracts Commiphora molmol and Araucaria heterophylla on Cattle ticks, Rhipicephalus (Boophilus) annulatus.

Mortality % (Mean ± SE)
Plant Extracts Concentration (mg/mL) Methanol Hexane
1 Day 3 Days 7 Days 1 Day 3 Days 7 Days
Commiphora molmol 0 0.00 ± 0.0 fC * 3.33 ± 3.33 fB 6.67 ± 3.33 eA 0.0 ± 0.0 fC 3.33 ± 3.33 fB 6.67 ± 3.33 fA
1.6 20.00 ± 5.77 eC 40.00 ± 0.00 eB 66.67 ± 3.33 dA 16.67 ± 3.33 eC 33.33 ± 6.67 eB 56.67 ± 8.82 eA
3.1 33.33 ± 8.82 dC 70.00 ± 5.77 dB 90.00 ± 5.77 cA 26.67 ± 3.33 dC 50.00 ± 5.77 dB 70.00 ± 10.00 dA
6.3 56.67 ± 3.33 cC 76.67 ± 3.33 cB 96.67 ± 3.33 bA 43.33 ± 6.67 cC 70.00 ± 5.77 cB 80.00 ± 5.77 cA
12.5 70.00 ± 5.77 bC 83.33 ± 3.33 bB 100.0 ± 0.00 aA 56.67 ± 3.33 bC 76.67 ± 8.82 bB 90.00 ± 5.77 bA
25 83.33 ± 3.33 aC 93.33 ± 6.67 aB 100.0 ± 0.00 aA 70.00 ± 5.77 aC 83.33 ± 3.33 aB 100.0 ± 0.00 aA
Araucaria heterophylla 0 0.00 ± 0.0 f C 3.33 ± 3.33 fB 6.67 ± 3.33 dA 0.0 ± 0.0 fC 3.33 ± 3.33 fB 6.67 ± 3.33 fA
1.6 23.33 ± 3.33 eC 50.00 ± 5.77 eB 76.67 ± 6.67 cA 16.67 ± 8.82 eC 36.67 ± 3.33 eB 60 ± 10.00 eA
3.1 46.67 ± 12.02 dC 76.67 ± 3.33 dB 86.67 ± 8.82 bA 40.00 ± 5.77 dC 60.00 ± 5.77 dB 80 ± 11.55 dA
6.3 66.67 ± 12.02 cC 83.33 ± 12.02 cB 100.0 ± 0.00 aA 53.33 ± 8.82 cC 70.00 ± 10.00 cB 83.33 ± 8.82 cA
12.5 83.33 ± 8.82 bC 93.33 ± 3.33 bB 100.0 ± 0.00 aA 63.33 ± 6.67 bC 80.00 ± 0.00 bB 93.33 ± 6.67 bA
25 96.67 ± 3.33 aC 100.0 ± 0.00 aB 100.0 ± 0.00 aA 80.00 ± 5.77 aC 93.33 ± 6.67 aB 100.0 ± 0.00 aA
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* letters refer to significant difference; a–f: There is no significant difference (p > 0.05) between any two means, those within the same column have the same superscript letter; A, B & C: There is no significant difference (p > 0.05) between any two means for the same solvent, those within the same row have the same superscript letter. Three replicates were used for each concentration and ten numbers of adult pests per replicate were used.

Table 4.

Lethal concentration values of plant extracts of Commiphora molmol and Araucaria heterophylla against Rhipicephalus (Boophilus) annulatus.

Days Plant Extracts Solvents LC50 (95%CL) * LC90 (95%CL) LC95 (95%CL) Equation ** X2
1 Commiphora molmol Methanol 5.26 (4.62–6.65) 38.19 (27.18–61.90) 65.95 (43.34–120.72) 1.530 ± 0.150X 0.628
Hexane 9.24 (7.46–11.85) 96.45 (56.88–218.26) 187.47 (98.46–512.05) 1.258 ± 0.145X 0.172
Araucaria heterophylla Methanol 3.68 (3.10–4.28) 17.30 (14.05–22.58) 26.81 (20.77–37.55) 1.908 ± 0.153X 0.568
Hexane 6.09 (4.99–7.43) 51.83 (34.48–94.53) 95.07 (57.43–201.82) 1.379 ± 0.147X 3.420
3 Commiphora molmol Methanol 2.42 (0.75–3.58) 16.91 (13.56–88.54) 29.31 (26.34–256.46) 1.520 ± 0.150X 10.917
Hexane 3.40 (2.55–4.27) 37.60 (24.87–70.99) 74.29 (43.71–170.66) 1.228 ± 0.147X 2.769
Araucaria heterophylla Methanol 1.41 (0.82–2.25) 12.97 (8.12–17.10) 24.33 (18.12–32.14) 1.330 ± 0.200X 25.761
Hexane 2.71 (2.06–3.37) 21.64 (15.81–34.10) 38.96 (26.03–71.10) 1.422 ± 0.156X 2.660
7 Commiphora molmol Methanol 1.09 (0.70–1.40) 3.58 (2.98–4.72) 5.00 (3.96–7.56) 2.496 ± 0.423X 0.875
Hexane 1.55 (1.07–2.02) 10.62 (8.26–15.16) 18.31 (13.17–30.02) 1.537 ± 0.181X 5.304
Araucaria heterophylla Methanol 1.41 (0.72–1.89) 12.97 (11.52–18.78) 24.33 (22.14–34.15) 1.330.6 ± 0.433X 25.76
Hexane 1.08 (0.65– 1.86) 10.11 (8.44– 16.10) 19.03 (12.45– 27.10) 1.323±0.193X 11.720
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* LC50, 60, and 95 values = lethal concentration that kills 50, 90, and 95% of the exposed ectoparasite; (95%CL) = lower and upper confidence limit; ** Regression line equation; X2 = chi-square; Significant at p < 0.05 level.

Analogous to our study, Commiphora spp. has an acaricidal effect, as C. molmol extract effectively controlled the fowl tick, Argas persicus, and its mortalities reached 63, 67, 76, 87, and 94% PT for 12 days PT with 0.625, 1.25, 2.5, 5, and 10%, respectively (LC50 = 1.28, 0.88, 0.84, 0.50, and 0.42% PT for 1, 2, 3, 6, and 12 days, respectively) [65].

Commiphora swynnertonii (Burtt) exudate had a parallel strong acaricidal effect against ticks such as Rhipicephalus appendiculatus and Amblyioma variegatum (LC50 = 1.72 and 1.91 mg/mL, respectively, and LC99 were 3.5 and 3.7 mg/mL, respectively) and adversely affected their reproduction capability [66]. C. swynnertonii (Burtt) stem bark exudate also induced an acaricidal effect against Rhipicephalus appendiculatus and exhibited a significant (p < 0.05) mortality and inhibition of laid eggs of ticks PT with concentrations over 25 and 90 mg/mL, respectively, and no hatching of eggs was observed in all treated groups [67]. A similar study revealed the adulticidal effect of the C. swynnertonii stem bark ethyl acetate, petroleum ether, and methanolic extracts against R. appendiculatus and A. variegatum. The petroleum ether extract exhibited higher acaricidal activity (LC50 = 72.31 and 71.67 mg/mL, respectively) and its MO%, 156 h PT, were 100 and 87% against Amblyomma variegatum and Rhipicephalus appendiculatus, respectively [67].

The gum Haggar, Commiphora holtziana, resin repelled the cattle tick, Boophilus microplus for up to 5 h with the hexane extract [68]. Additionally, myrrh not only controls ticks but also inhibited the propagation of blood parasites transmitted by ticks as bovine (Babesia bovis, B. bigemina, and B. divergens) and equine piroplasms (Theileria equi and B. caballi) [54]. C. molmol also induced molluscicidal and biological activities against Biomphalaria alexandrina and Bulinus truncatus (Mollusca: Gastropoda) [55].

Furthermore, the C. molmol resin extract displays pesticide action against many pests. It effectively controlled the blowfly, Lucilia sericata and its LC50 values were 6.03, 7.96, and 6.55 mg/mL for the first, second and third larva stages, respectively, and induced morphological abnormalities in larvae, pupae, and adults [58]. C. molmol was toxic to the fowl tick Argas persicus (LC50 = 1.28, 0.88, 0.84, 0.50 and 0.42 PT for one, two, three, six, and 12 days, respectively. Mortalities reached 63, 67, 76, 87, and 94% PT with 0.625, 1.25, 2.5, 5, and 10%, respectively [69].

Analogous studies showed the acaricidal effect of other plant extracts against ticks. Recently, the ethanol extracts of Vitex castus and Zingiber officinale had an acaricidal effect against H. dromedarii, as the mortality 15 days PT reached 80.8 and 84.7%, respectively, and LC50 values three days PT were 12.2 and 11.8%, respectively, whereas their median lethal time (LT50) values PT was 2.6 and 2.5 days, respectively [52]. Moreover, Protium spruceanum on resistant strains against R. annulatus induced mortality > 80 and 90% PT with 100 and 50 mg/mL ethanolic extract and ethyl acetate extracts, respectively [70]; ethyl alcohol and petroleum ether extracts of Melia azedarach and Artemisia herba-alba were also effective acaricides against embryonated eggs and engorged nymphs of H. dromedarii when compared to Butox®5.0 (Deltamethrin) [71].

A related study showed that the methanol extract of neem and Citrullus colocynthis produced an acaricidal effect against adult females, eggs, and larvae, and neem was more effective against H. dromedarii [72]. Some other materials are also effective in vitro acaricides such as peracetic acid against Boophilus annulatus and the fowl tick, Argas persicus [17] and A. persicus, infesting laying hens [18]. Moreover, some photosensitizers such as safranin and rose bengal had a strong acaricidal effect against H. dromedarii and suppressed the reproductive potential of its engorged females [16].

Lice infestation in cattle is mainly controlled by conventional insecticides [73], and to the best of our knowledge, there are no natural treatments for controlling such pests as. Data from this work showed that the methanol extracts of C. molmol and A. heterophylla effectively controlled the cattle lice, Ha. eurysternus, reaching 100% mortality PT with 6.35% of methanol extracts (LC50 = 0.56 and 0.62 mg/mL, respectively, and 96.67 and 83.33%, respectively, PT with 6.3% hexane extracts (LC50 = 0.55 and 1.00 mg/mL, respectively) (Table 5 and Table 6).

Table 5.

Efficacy of the plant extracts of Commiphora molmol and Araucaria heterophylla on cattle lice, Haematopinus eurysternus.

Mortality % (Mean ± SE)
Plant Extracts Concentration (mg/mL) Methanol Hexane
1 Day 3 Days 7 Days 1 Day 3 Days 7 Days
Commiphora molmol 0 0.00 ± 0.0 fC * 3.33 ± 3.33 fB 6.67 ± 3.33 eA 0.0 ± 0.0 eC 3.33 ± 3.33 fB 6.67 ± 3.33 fA
0.8 20.00 ± 5.77 eC 40.00 ± 0.00 eB 66.67 ± 3.33 dA 20.00 ± 0.00 dC 36.67 ± 8.82 eB 63.33 ± 3.33 eA
1.6 33.33 ± 8.82 dC 70.00 ± 5.77 dB 90.00 ± 5.77 cA 30.00 ± 5.77 C 60.00 ± 0.00 dB 83.33 ± 3.33 dA
3.1 56.67 ± 3.33 cC 76.67 ± 3.33 cB 96.67 ± 3.33 bA 50.00 ± 5.77 cC 76.67 ± 3.33 cB 90.00 ± 5.77 cA
6.3 83.33 ± 3.33 bC 90.00 ± 5.77 bB 100.0 ± 0.00 aA 73.33 ± 6.67 bC 83.33 ± 3.33 bB 96.67 ± 3.33 bA
12.5 100.0 ± 0.00 aC 100.0 ± 0.00 aB 100.0 ± 0.00 aA 86.67 ± 6.67 aC 93.33 ± 3.33 aB 100 ± 0.00 aA
Araucaria heterophylla 0 0.00 ± 0.0 fC 3.33 ± 3.33 fB 6.67 ± 3.33 eA 0.00 ± 0.0 fC 3.33 ± 3.33 fB 6.67 ± 3.33 fA
0.8 16.67 ± 3.33 eC 33.33 ± 6.67 eB 63.33 ± 6.67 dA 13.33 ± 3.33 eC 30.00 ± 5.77 eB 53.33 ± 8.82 eA
1.6 26.67 ± 3.33 dC 60.00 ± 5.77 dB 80.00 ± 5.77 cA 23.33 ± 8.82 dC 40.00 ± 10.00 dB 63.33 ± 3.33 dA
3.1 46.67 ± 3.33 cC 70.00 ± 10.00 cB 83.33 ± 8.82 bA 36.67 ± 3.33 cC 53.33 ± 3.33 cB 70.00 ± 0.00 cA
6.3 56.67 ± 3.33 bC 76.67 ± 3.33 bB 100.0 ± 0.00 aA 46.67 ± 6.67 bC 70.00 ± 10.00 bB 83.33 ± 6.67 bA
12.5 76.67 ± 3.33 aC 90.00 ± 5.77 aB 100.0 ± 0.00 aA 63.33 ± 3.33 aC 76.67 ± 3.33 aB 100.0 ± 0.00 aA
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* letters refer to significant difference; a–f: There is no significant difference (p > 0.05) between any two means, within the same column they have the same superscript letter; A, B & C: There is no significant difference (p > 0.05) between any two means for the same solvent, within the same row they have the same superscript letter. Three replicates were used for each concentration and ten numbers of adult pests per replicate were used.

Table 6.

Lethal concentration values of plant extracts of Commiphora molmol and Araucaria heterophylla against Haematopinus eurysternus.

Days Plant Extracts Solvents LC50 (95%CL) * LC90 (95%CL) LC95 (95%CL) Equation ** X2
1 Commiphora molmol Methanol 2.27 (1.97–2.59) 8.49 (6.94–11.04) 12.34 (9.66–17.05) 2.240 ± 0.180 5.034
Hexane 2.88 (2.43–3.39) 16.37 (12.16–24.66) 26.79 (18.61–44.58) 1.698 ± 0.561 1.345
Araucaria heterophylla Methanol 4.08 (3.36–5.04) 33.78 (21.83–64.49) 61.48 (36.10–136.45) 1.397 ± 0.148 1.329
Hexane 6.65 (5.20–9.21) 80.76 (42.32–229.34) 163.87 (75.16–581.83) 1.183 ± 0.148 0.397
3 Commiphora molmol Methanol 1.09 (086–1.32) 5.23 (4.22–6.99) 8.15 (6.21–11.93) 1.889 ± 0.190 6.631
Hexane 1.28 (0.97–1.57) 8.91 (6.73–13.25) 15.45 (10.78–26.14) 1.521 ± 0.161 2.058
Araucaria heterophylla Methanol 1.47 (1.11–1.84) 13.48 (9.49–22.75) 25.25 (16.06–50.33) 1.334 ± 0.152 4.287
Hexane 2.75 (2.14–3.47) 36.43 (21.46–84.85) 75.78 (39.01–221.81) 1.142 ± 0.143 0.662
7 Commiphora molmol Methanol 0.56 (0.38–0.71) 1.77 (1.49–2.24) 2.44 (1.99–3.38) 2.589 ± 0.379 0.876
Hexane 0.55 (0.35–0.73) 2.86 (2.32–3.80) 4.57 (3.49–6.85) 1.791 ± 0.234 1.514
Araucaria heterophylla Methanol 0.62 (0.24–1.12) 3.07 (2.24–4.15) 4.82 (2.68–6.20) 1.856 ± 0.229 11.223
Hexane 1.00 (0.64–1.68) 8.37 (5.88–11.32) 15.27 (9.85–21.15) 1.392 ± 0.159 11.114
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* LC50, 60, and 95 values = lethal concentration that kills 50, 90, and 95% of the exposed ectoparasite; (95%CL) = lower and upper confidence limit; ** Regression line equation; X2 = chi-square; Significant at p < 0.05 level.

Studies about using botanicals against lice infesting large animals are very rare. A comparable study indicated that essential oils had in vitro and in vivo lousicidal potential against the buffalo louse, Haematopinus tuberculatus (Burmeister, 1839), in Egypt. Through filter paper contact bioassays, the LC50 values, four minutes PT, were 2.74, 12.35, 7.28, 22.79, and 18.67% for camphor (Cinnamomum camphora, Laurales: Lauraceae), peppermint (Mentha piperita L., Lamiales: Lamiaceae), onion (Allium cepa, Asparagales: Amaryllidaceae), rosemary oils (Rosmarinus officinalis Linn, Lamiales: Lamiaceae), and chamomile (Matricaria chamomilla L., Asterales: Asteracea), respectively, and oils induced ovicidal effects except rosemary, which was not applied [33]. Moreover, essential oils of garlic, clove, pumpkin, onion, and marjoram effectively controlled the dog louse, Trichodectes canis in vitro [51] and camphor oil controlled the slender pigeon louse, Columbicola columbae, in vitro and in vivo [49].

This investigation indicated that complete mortalities were reached seven days PT for the cattle louse fly, Hi. maculata, with 12.5 mg/mL extracts of C. molmol and A. heterophylla (LC50 values PT with methanol extract were 0.67 and 0.78 mg/mL, respectively, whereas those of hexane extracts were 0.68 and 0.32 mg/mL, respectively. After treatment with a lower concentration, 6.3%, MO% reached 100 and 93.33% PT with methanol extracts and 90 and 100% PT with hexane extracts (Table 7 and Table 8).

Table 7.

Efficacy of the plant extracts of Commiphora molmol and Araucaria heterophylla against the cattle louse fly, Hippobosca maculata.

Mortality % (Mean ± SE)
Plant Extracts Concentration (mg/mL) Methanol Hexane
1 Day 3 Days 7 Days 1 Day 3 Days 7 Days
Commiphora molmol 0 0.00 ± 0.0 fC * 3.33 ± 3.33 fB 6.67 ± 3.33 eA 0.00 ± 0.0 fC 3.33 ± 3.33 fB 6.67 ± 3.33 fA
0.8 20.00 ± 5.77 eC 33.33 ± 6.67 eB 60.00 ± 5.77 dA 13.33 ± 6.67 eC 30.00 ± 5.77 eB 56.67 ± 3.33 eA
1.6 40.00 ± 5.77 dC 60.00 ± 5.77 dB 83.33 ± 3.33 cA 23.33 ± 8.82 dC 53.33 ± 6.67 dB 76.67 ± 3.33 dA
3.1 53.33 ± 3.33 cC 73.33 ± 3.33 cB 90.00 ± 5.77 bA 43.33 ± 8.82 cC 70.00 ± 10.00 cB 83.33 ± 12.02 cA
6.3 83.33 ± 3.33 bC 86.67 ± 8.82 bB 100 ± 0.00 aA 66.67 ± 13.33 bC 76.67 ± 3.33 bB 90.00 ± 5.77 bA
12.5 96.67 ± 3.33 aC 100.0 ± 0.00 aB 100 ± 0.00 aA 80.00 ± 11.55 aC 86.67 ± 8.82 aB 100 ± 0.00 aA
Araucaria heterophylla 0 0.00 ± 0.0 fC 3.33 ± 3.33 fB 6.67 ± 3.33 fA 0.00 ± 0.0 fC 3.33 ± 3.33 fB 6.67 ± 3.33 eA
0.8 10.00 ± 5.77 eC 26.67 ± 6.67 eB 56.67 ± 6.67 eA 23.33 ± 3.33 eC 50.00 ± 5.77 eB 76.67 ± 6.67 dA
1.6 20.00 ± 5.77 dC 53.33 ± 3.33 dB 73.33 ± 8.82 dA 46.67 ± 3.33 dC 76.67 ± 3.33 dB 86.67 ± 3.33 cA
3.1 40.00 ± 5.77 cC 63.33 ± 3.33 cB 76.67 ± 3.33 cA 66.67 ± 8.82 cC 86.67 ± 6.67 cB 93.33 ± 6.67 bA
6.3 50.00 ± 5.77 bC 70.00 ± 5.77 bB 93.33 ± 6.67 bA 86.67 ± 3.33 bC 93.33 ± 6.67 bB 100.0 ± 0.00 aA
12.5 70.00 ± 5.77 aC 83.33 ± 12.02 aB 100.0 ± 0.00 aA 96.67 ± 3.33 aC 100.0 ± 0.00 aB 100.0 ± 0.00 aA
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* letters refer to significant difference; a–f: There is no significant difference (p > 0.05) between any two means, within the same column they have the same superscript letter; A, B & C: There is no significant difference (p > 0.05) between any two means for the same solvent, within the same row they have the same superscript letter. Three replicates were used for each concentration and ten numbers of adult pests per replicate were used.

Table 8.

Lethal concentrations of plant extracts of Commiphora molmol and Araucaria heterophylla against Hippobosca maculata.

Days Plant Extracts Solvents LC50 (95%CL) * LC90 (95%CL) LC95 (95%CL) Equation ** X2
1 Commiphora molmol Methanol 2.31 (1.96–2.70) 11.24 (8.64–16.10) 17.60 (12.76–27.57) 1.866 ± 0.171 2.861
Hexane 3.84 (3.27–4.56) 21.60 (15.68–33.70) 35.23 (23.91–60.73) 1.714 ± 0.156 0.733
Araucaria heterophylla Methanol 5.58 (4.60–7.02) 41.19 (26.40–79.38) 72.59 (42.51–160.78) 1.476 ± 0.153 1.476
Hexane 1.80 (1.53–2.09) 7.47 (6.06–9.84) 11.18 (8.65–15.79) 2.079 ± 0.178 0.395
3 Commiphora molmol Methanol 1.40 (1.15–1.64) 6.19 (5.01–8.20) 9.43 (7.25–13.53) 1.988 ± 0.183 5.842
Hexane 1.72 (1.34–2.12) 15.08 (10.57–25.46) 27.86 (17.73–55.12) 1.326 ± 0.151 3.343
Araucaria heterophylla Methanol 2.07 (1.61–2.58) 22.23 (14.49–42.83) 43.53 (25.30–101.41) 1.245 ± 0.146 5.163
Hexane 0.77 (0.56–0.97) 4.01 (3.31–5.11) 6.40 (5.03–8.89) 1.794 ± 0.181 2.148
7 Commiphora molmol Methanol 0.67 (0.48–0.83) 2.51 (2.09–3.20) 3.65 (2.90–5.11) 2.2.33 ± 0.276 3.968
Hexane 0.68 (0.45–0.91) 4.70 (36.7–6.66) 8.12 (5.87–13.28) 1.533 ± 0.187 5.665
Araucaria heterophylla Methanol 0.78 (0.18–1.05) 4.91 (3.56–18.20) 8.28 (6.51–51.32) 1.602 ± 0.187 7.916
Hexane 0.32 (0.16–0.49) 2.06 (1.64–2.61) 3.49 (2.74–4.87) 1.586 ± 0.214 1.033
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* LC50, 60, and 95 values = lethal concentration that kills 50, 90, and 95% of the exposed ectoparasite; (95%CL) = lower and upper confidence limit; ** Regression line equation; X2 = chi-square; Significant at p < 0.05 level.

Parallel studies of using botanicals against Hi. maculata were also recorded. The leaf of Ricinus communis, Malabarica malabarica, and Gloriosa superba (methanol, chloroform, and chloroform extracts, respectively) effectively controlled Hi. maculata and the tick Haemaphysalis bispinosa [74]. The aqueous crude leaf extracts of Catharanthus roseus had insecticidal efficacy against the adults of Hi. maculata and the sheep-biting louse, Bovicola ovis (LD50 = 36.17 and 30.35 mg/L, respectively) [75].

A similar study proved the adulticidal activity of Cissus quadrangularis through an aqueous extract, AgNO3 solution, and synthesized Ag NPs against the cattle tick, Rhipicephalus (Boophilus) microplus larvae (LC50 = 50.00, 21.72, and 7.61 mg/L, respectively) and the adult of Hi. maculata (LC50 = 37.08, 40.35 and 6.30 mg/L, respectively) via the contact toxicity method [76].

Moreover, essential oils had repellent, adulticidal, larvicidal, and ovicidal effects against cycloraphan flies [34,38,39,42,53,77]. Essential oils and d-phenothrin repelled biting and non-biting flies infesting water buffalo, Hippobosca equine, Haematobia irritans, Musca domestica, and Stomoxys calcitrans, for six and three days PT, respectively [33].

It is worth mentioning that the essential oil of Commiphora erythraea (Opoponax) induced a larvicidal effect against Culex restuans Theobald, Culex pipiens L., and Aedes aegypti L. (LC50 = 19.05, 22.61, and 29.83 ppm, respectively) [57].

Likewise, in our findings, some Oil-resins had larvicidal activity against Culex pipiens such as C. molmol, A. heterophylla, Boswellia sacra, Pistacia lentiscus, and Eucalyptus camaldulensis. After treatment for 24 and 48 h PT with 1500 ppm, the best effect was observed PT with acetone extracts of C. molmol, 83.3% and 100% with LC50 values were 623.52 and 300.63 ppm, as well as A. heterophylla, 75% and 95% with LC50 values, were 826.03 and 384.71 ppm, respectively. On the other hand, the aqueous extract of A. heterophylla was highly effective against Cx. pipiens (LC50 = 2819.85 and 1652.50 ppm) followed by C. molmol (LC50 = 3178.22 and 2322.53 ppm) 24 and 48 h PT, respectively [59]. As mosquito larvicides, A. heterophylla and Azadirachta indica (gum polysaccharides) were used for encapsulation of cyfluthrin-loaded superparamagnetic iron oxide nanoparticles [61].

2.2. Biochemical Analysis

It was noticed that most of the compounds belong to sesquiterpene, fatty acid esters and phenols were the most common compounds found in the methanol and hexane extracts of the myrrh, C. molmol plant while monoterpene, sesquiterpene, terpene alcohols, fatty acid, and phenols were found in in methanol and hexane extracts of A. heterophylla plant in larger amount.

Phytochemical analysis of this work revealed that the constituents of C. molmol and A. heterophylla extracts were identified by GC–MS analysis (Table 9, Table 10, Table 11 and Table 12) indicating that C. molmol and A. heterophylla contained the main chemical compounds 1,8,11,14-Heptadecatetraene, (Z,Z,Z)-(16.27%), 2(3H)-Benzofuranone, 6-ethenylhexahydro-6-methyl-3-methylene-7-(1-methylethenyl)-, [3aS-(3aà,6à,7á,7aá)]-(22.67%), Azuleno [4,5-b]furan-2(3H)-one, decahydro-3,6,9-tris(methylene)-, [3aS-(3aà,6aà,9aà,9bá)]-(47.28) and 1,8,11,14-Heptadecatetraene, (Z,Z,Z)-(7.43), 2(3H)-Benzofuranone, 6-ethenylhexahydro-6-methyl-3-methylene-7-(1-methylethenyl)-, [3aS-(3aà,6à,7á,7aá)]-(19.90), and ETHANONE, 1-(7,8-DIHYDRO-3-HYDROXY-4-PROPYL-2-NAPHTHALENYL)-(67.27%) for methanol and hexane extracts.

Table 9.

The major chemical constituents of Commiphora molmol methanol extracts.

No. M. F. * Chemical Name (99.98%) Area (%) RT Nature of Compound
1 C15H24 Cyclohexene, 4-ethenyl-4-methyl-3-(1-methylethenyl)-1-(1-methylethyl)-, (3R-trans)- 0.74 9.38 phenol
2 C15H24 (-)-á-Bourbonene 3.78 10.33 fatty acid esters
3 C15H24 Tricyclo [2.2.1.0(2,6)]heptane, 1,7-dimethyl-7-(4-methyl-3-pentenyl)-, (-)- 1.86 11.11 carboxylic acid
4 C15H24 ç-Elemene 2.11 11.40 fatty acid esters
5 C15H24 1,6-CYCLODECADIENE, 1-METHYL-5-METHYLENE-8-(1-METHYLETHYL)-, [S-(E,E)]- 1.78 12.34 fatty acid esters
6 C15H24 Aromandendrene 0.65 12.43 fatty acid ester
7 C15H24 Azulene, 1,2,3,3a,4,5,6,7-octahydro-1,4-dimethyl-7-(1-methylethenyl)-, [1R-(1à,3aá,4à,7á)]- 0.06 12.61 terpenoids
8 C15H20O Benzofuran, 6-ethenyl-4,5,6,7-tetrahydro-3,6-dimethyl-5-isopropenyl-, trans- 0.81 12.82 heterocyclic
9 C15H20O Benzofuran, 6-ethenyl-4,5,6,7-tetrahydro-3,6-dimethyl-5-isopropenyl-, trans- 15.35 13.17 heterocyclic
10 C15H24 ç-Muurolene 0.24 13.27 sesquiterpene
11 C15H24 Naphthalene, 1,2,3,5,6,8a-hexahydro-4,7-dimethyl-1-(1-methylethyl)-, (1S-cis)- 0.32 13.36 sesquiterpene
12 C15H24 á-Longipinene 0.20 13.51 sesquiterpene
13 C15H24 Azulene, 1,2,3,3a,4,5,6,7-octahydro-1,4-dimethyl-7-(1-methylethenyl)-, [1R-(1à,3aá,4à,7á)]- 0.08 13.61 sesquiterpene
14 C15H24 1,5-Cyclodecadiene, 1,5-dimethyl-8-(1-methylethylidene)-, (E,E)- 2.04 13.92 sesquiterpene
15 C15H18O 3,5,8a-Trimethyl-4,6,8a,9-tetrahydronaphtho [2,3-b]furan 0.99 14.36 phenol
16 C15H18O Azulen-2-ol, 1,4-dimethyl-7-(1-methylethyl)- 0.47 15.37 acetic acid
17 C15H18O 1-NAPHTHALENOL, 4,7-DIMETHYL-2-(1-METHYLETHYL)- 30.80 15.87 phenol
18 C15H18O (4aS,8aS)-3,8a-Dimethyl-5-methylene-4,4a,5,6,8a,9-hexahydronaphtho [2,3-b]furan 7.98 15.95 phenol
19 C15H20O Benzofuran, 6-ethenyl-4,5,6,7-tetrahydro-3,6-dimethyl-5-isopropenyl-, trans- 0.89 16.16 heterocyclic
20 C17H28O2 Cyclohexanemethanol, 4-ethenyl-à,à,4-trimethyl-3-(1-methylethenyl)-, acetate, [1R-(1à,3à,4á)]- 2.37 16.35 sesquiterpene
21 C16H22O2 (R,5E,9E)-8-Methoxy-3,6,10-trimethyl-4,7,8,11-tetrahydrocyclodeca[b]furan 12.72 17.25 sesquiterpene lactones
22 C15H24 AZULENE, 1,2,3,4,5,6,7,8-OCTAHYDRO-1,4-DIMETHYL-7-(1-METHYLETHYLIDENE)-, (1S-CIS)- 0.29 18.15 sesquiterpene
23 C17H24O4 Acetic acid, 6-(1-hydroxymethyl-vinyl)-4,8a-dimethyl-3-oxo-1,2,3,5,6,7,8,8a-octahydronaphthalen-2-yl ester 2.03 19.08 phenol
24 C15H20O3 Reynosin 0.11 19.24 fatty acid esters
25 C23H34O2 Methyl 4,7,10,13,16,19-docosahexaenoate 0.18 19.32 steroids
26 C17H24O4 6-[1-(HYDROXYMETHYL)VINYL]-4,8A-DIMETHYL-3-OXO-1,2,3,5,6,7,8,8A-OCTAHYDRO-2-NAPHTHALENYL ACETATE 10.35 20.16 fatty acid esters
27 C15H20O2 FUROSARDONIN A 0.42 20.36 fatty acid esters
28 C15H22O3 5,8-Dihydroxy-4a-methyl-4,4a,4b,5,6,7,8,8a,9,10-decahydro-2(3H)-phenanthrenone 0.36 21.82 fatty acid esters
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* Molecular formula.

Table 10.

The major chemical constituents of Commiphora molmol hexane extracts.

No. M. F. Chemical Name (100%) Area (%) RT Nature of Compound
1 C15H24 Cyclohexene, 4-ethenyl-4-methyl-3-(1-methylethenyl)-1-(1-methylethyl)-, (3R-trans)- 0.88 9.36 phenol
2 C10H12O2 PHENOL, 2-METHOXY-4-(2-PROPENYL)- 1.65 10.30 fatty acid esters
3 C15H24 CYCLOHEXANE, 1-ETHENYL-1-METHYL-2,4-BIS(1-METHYLETHENYL)-, [1S-(1à,2á,4á)]- 4.53 10.59 carboxylic acid
4 C15H24 Tricyclo [2.2.1.0(2,6)]heptane, 1,7-dimethyl-7-(4-methyl-3-pentenyl)-, (-)- 1.51 11.08 fatty acid esters
5 C15H24 ç-Elemene 1.32 11.42 fatty acid esters
6 C15H24 1,6-CYCLODECADIENE, 1-METHYL-5-METHYLENE-8-(1-METHYLETHYL)-, [S-(E,E)]- 1.72 12.32 sesquiterpene
7 C15H24 Aromandendrene 0.65 12.43 fatty acid ester
8 C15H24 Azulene, 1,2,3,3a,4,5,6,7-octahydro-1,4-dimethyl-7-(1-methylethenyl)-, [1R-(1à,3aá,4à,7á)]- 0.57 12.41 sesquiterpene
9 C15H20O 5-ISOPROPENYL-3,6-DIMETHYL-6-VINYL-4,5,6,7-TETRAHYDRO-1-BENZOFURAN # 1.10 12.82 sesquiterpene
10 C15H20O Benzofuran, 6-ethenyl-4,5,6,7-tetrahydro-3,6-dimethyl-5-isopropenyl-, trans- 12.09 13.07 heterocyclic
11 C15H24 ç-Muurolene 0.38 13.17 sesquiterpene
12 C15H24 GERMACRENE B 2.39 13.87 sesquiterpene
13 C15H18O 3,5,8a-Trimethyl-4,6,8a,9-tetrahydronaphtho [2,3-b]furan 1.25 14.33 sesquiterpene
14 C15H18O NAPHTHALENE, 4-METHOXY-1,2,6,8-TETRAMETHYL- 31.98 15.76 phenol
15 C15H18O (4aS,8aS)-3,8a-Dimethyl-5-methylene-4,4a,5,6,8a,9-hexahydronaphtho [2,3-b]furan 8.15 15.84 phenol
16 C15H20O Benzofuran, 6-ethenyl-4,5,6,7-tetrahydro-3,6-dimethyl-5-isopropenyl-, trans- 0.82 16.05 heterocyclic
17 C15H24 (5E)-3,6,10-TRIMETHYL-4,7,8,11-TETRAHYDROCYCLODECA[B]FURAN 7.94 16.62 sesquiterpene
18 C16H12O7 METHYL 3-(CIS-3’-HYDROXY-5’-OXOTETRAFURAN-2’-YL)-1,4-DIOXO-1,4-DIHYDRONAPHTHLENE-2-CARNOXYLATE 8.39 17.15 phenol
19 C15H24 AZULENE, 1,2,3,4,5,6,7,8-OCTAHYDRO-1,4-DIMETHYL-7-(1-METHYLETHYLIDENE)-, (1S-CIS)- 0.23 18.10 sesquiterpene
20 C17H24O4 Acetic acid, 6-(1-hydroxymethyl-vinyl)-4,8a-dimethyl-3-oxo-1,2,3,5,6,7,8,8a-octahydronaphthalen-2-yl ester 10.88 20.09 phenol
21 C13H14N2O 2-PYRAZOLIN-5-ONE, 4-ISOPROPYLIDENE-3-METHYL-1-PHENYL- 0.98 20.71 phenol
22 C15H22O3 5,8-Dihydroxy-4a-methyl-4,4a,4b,5,6,7,8,8a,9,10-decahydro-2(3H)-phenanthrenone 0.59 21.78 sesquiterpene
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Table 11.

The major chemical constituents of Araucaria heterophylla methanol extracts.

No. M. F. Chemical Name (100%) Area (%) RT Nature of Compound
1 C4H9NO2S DL-Homocysteine 0.86 4.65 terpenoid
2 C10H16 1,4-CYCLOHEXADIENE, 1-METHYL-4-(1-METHYLETHYL)- 1.22 6.68 phenol
3 C10H16 (1R)-2,6,6-Trimethylbicyclo [3.1.1]hept-2-ene 4.38 8.74 phenol
4 C10H16 à-Pinene 3.24 9.40 monoterpene
5 C10H16 1,3,7-OCTATRIENE, 3,7-DIMETHYL- 1.44 10.09 fatty acid
6 C10H16 à-Pinene 0.66 10.19 monoterpene
7 C10H16 BICYCLO [3.1.0]HEXANE, 4-METHYLENE-1-(1-METHYLETHYL)- 1.99 11.04 monoterpene
8 C10H16 CYCLOHEXENE, 1-METHYL-4-(1-METHYLETHENYL)- 12.95 13.07 monoterpene
9 C10H16O cis-p-mentha-1(7),8-dien-2-ol 1.85 16.67 monoterpene ketone
10 C10H16O à-Campholenal 1.29 17.70 monoterpene
11 C10H16O Isopinocarveol 2.38 18.19 monoterpene
12 C10H16O cis-Verbenol 3.8 18.49 monoterpene
13 C10H16O Isopinocarveol 0.68 19.57 monoterpene
14 C10H16O Bicyclo [3.1.1]hept-2-ene-2-methanol, 6,6-dimethyl- 0.97 20.77 terpene alcohols
15 C13H26 6-Tridecene, (Z)- 9.34 20.90 fatty acid
16 C10H16O (-)-MYRTENOL 1.33 21.52 glycosides
17 C10H14O Bicyclo [3.1.1]hept-3-en-2-one, 4,6,6-trimethyl-, (1S)- 2.24 22.49 terpene alcohols
18 C15H24 .alfa.-Copaene 1.85 23.79 sesquiterpene
19 C15H24 Ylangene 1.13 24.79 sesquiterpene
20 C15H24 Copaene 7.96 25.41 sesquiterpene
21 C15H24 (-)-á-Bourbonene 3.41 25.58 sesquiterpene
22 C15H24 Caryophyllene 2.63 27.22 sesquiterpene
23 C15H24 á-ylangene 1.22 28.05 sesquiterpene
24 C15H24 á-copaene 0.84 28.48 sesquiterpene
25 C15H24 ç-Muurolene 3.48 29.64 sesquiterpene
26 C15H24 Germacrene D 2.34 2984 sesquiterpene
27 C15H24 ç-Muurolene 2.07 30.20 sesquiterpene
28 C15H24 Naphthalene, 1,2,3,5,6,8a-hexahydro-4,7-dimethyl-1-(1-methylethyl)-, (1S-cis)- 3.82 30.85 sesquiterpene
29 C15H24 á-copaene 1.4 31.59 sesquiterpene
30 C22H44O4Si OCTADECANOIC ACID, 9,10-EPOXY-18-(TRIMETHYLSILOXY)-, METHYL ESTER, CIS- 1.08 33.31 fatty acid
31 C15H24O Caryophyllene oxide 10.39 34.01 phenol
32 C15H24O 4,12,12-TRIMETHYL-9-METHYLENE-5-OXATRICYCLO [8.2.0.0~4,6~]DODECANE 0.98 34.40 sesquiterpene
33 C15H24O Caryophyllene oxide 1.18 35.04 sesquiterpene
34 C15H26O 1,1,4,7-TETRAMETHYLDECAHYDRO-1H-CYCLOPROPA[E]AZULEN-4-OL # 1.31 35.76 sesquiterpene
35 C15H24O Caryophyllene oxide 1.50 36.42 phenol
36 C18H34O3 Oxiraneoctanoic acid, 3-octyl-, cis- 0.79 37.75 sesquiterpene
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Table 12.

The major chemical constituents of Araucaria heterophylla hexane extracts.

No. M. F. Chemical Name (99.90%) Area (%) RT Nature of Compound
1 C10H16 BICYCLO [3.1.1]HEPT-2-ENE, 2,6,6-TRIMETHYL- 0.84 5.22 terpenoid
2 C10H16 2,6,6-TRIMETHYLBICYCLO [3.1.1]HEPT-2-ENE 6.5 6.31 phenol
3 C10H16 D-Limonene 1.35 7.12 monoterpene
4 C15H24 5,5-Dimethylimidazolidine-2,4-dione 3.57 8.34 sesquiterpene
5 C6H10O 3-PENTEN-2-ONE, 4-METHYL- 1.62 8.54 alkene
6 C3H6DN AZETIDINE-D1 8.28 9.41 saturated heterocyclic
7 C7H14O2 2-PENTANONE, 4-METHOXY-4-METHYL- 1.26 10.32 phenol
8 C10H16 CYCLOHEXENE, 1-METHYL-4-(1-METHYLETHENYL)- 4.11 12.62 monoterpene
9 C10H15NO2 Benzenemethanol, 4-hydroxy-à-[1-(methylamino)ethyl]-, (R*,S*)- 0.39 14.62 saturated heterocyclic
10 C10H16O à-Campholenal 0.69 15.04 monoterpene
11 C8H16O 2-OCTANONE 0.44 17.38 organic aldehyde
12 C10H16O Bicyclo [3.1.1]hept-3-en-2-ol, 4,6,6-trimethyl-, [1S-(1à,2á,5à)]- 2.90 21.19 terpenes
13 C15H24 ç-Elemene 0.23 23.62 terpenes
14 C18H34O2 9-OCTADECENOIC ACID (Z)- 14.60 25.95 terpenes
15 C15H24 BICYCLO [7.2.0]UNDEC-4-ENE, 4,11,11-TRIMETHYL-8-METHYLENE-, [1R-(1R*,4E,9S*)]- 0.22 26.72 terpenes
16 C15H24 à-Cubebene 0.31 27.23 terpenes
17 C15H24 1,4-METHANOAZULENE, DECAHYDRO-4,8,8-TRIMETHYL-9-METHYLENE-, [1S-(1à,3Aá,4à,8Aá)]- 0.49 28.09 terpenes
18 C15H24 (-)-á-Bourbonene 0.98 30.30 terpenes
19 C15H24 ç-Elemene 0.96 31.22 terpenes
20 C18H36O2 Hexadecanoic acid, ethyl ester 9.57 31.70 terpenes
21 C18H34O2 9-OCTADECENOIC ACID (Z)- 3.18 32.98 terpenes
22 C15H24O2 BICYCLO [4.4.0]DEC-2-EN-4-OL, 2-METHYL-9-(PROP-1-EN-3-OL-2-YL)- 1.42 33.79 terpenes
23 C16H22 4,4’-Dimethyl-2,2’-dimethylenebicyclohexyl-3,3’-diene 4.21 34.10 terpenes
24 C15H24 Aromandendrene 1.30 34.76 sesquiterpene
25 C15H24 á-Longipinene 0.45 35.01 sesquiterpene
26 C27H46O CHOLEST-5-EN-3-OL (3á)- 19.15 35.54 fatty acid
27 C26H44O5 Ethyl iso-allocholate 0.11 36.79 fatty acid
28 C18H34O2 9-OCTADECENOIC ACID (Z)- 5.19 37.2 fatty acid
29 C16H32O2 n-Hexadecanoic acid 2.13 37.63 fatty acid
30 C19H26O6 ISOCHIAPIN B 3.45 40.03 fatty acid
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C. molmol methanol extract in the present study mainly contained benzofuran, 6-ethenyl-4,5,6,7-tetrahydro-3,6-dimethyl-5-isopropenyl-, trans-(15.35%), 1-NAPHTHALENOL, 4,7-DIMETHYL-2-(1-METHYLETHYL)-(13.80%), (R,5E,9E)-8-Methoxy-3,6,10-trimethyl-4,7,8,11-tetrahydrocyclodeca[b]furan (12.72%), and 6-[1-(HYDROXYMETHYL)VINYL]-4,8A-DIMETHYL-3-OXO-1,2,3,5,6,7,8,8A-OCTAHYDRO-2-NAPHTHALENYL ACETATE (10.35). On the other hand, C. molmol hexane extract mainly contained benzofuran, 6-ethenyl-4,5,6,7-tetrahydro-3,6-dimethyl-5-isopropenyl-, trans-(12.09%), NAPHTHALENE, 4-METHOXY-1,2,6,8-TETRAMETHYL-931.98%), (4aS,8aS)-3,8a-Dimethyl-5-methylene-4,4a,5,6,8a,9-hexahydronaphtho [2,3-b]furan (8.15%).

The chemical analysis in this study indicated that A. heterophylla contains the main chemical compounds the à-Pinene (3.24%), CYCLOHEXENE, 1-METHYL-4-(1-METHYLETHENYL)-(12.95%), 6-Tridecene, (Z)-99.34%), Copaene (7.96%), and Caryophyllene oxide (10.39%) for methanol extract and AZETIDINE-D1 (8.28%), 9-OCTADECENOIC ACID (Z)-(14.60%), Hexadecanoic acid, ethyl ester (9.57%), and CHOLEST-5-EN-3-OL (3á)-(19.15%) for hexane extract.

Parallel studies demonstrated that the Araucariaceae family including A. heterophylla, produces several monoterpenes, such as pinene, camphene, and limonene as common compounds [78]. Araucaria spp. contains various sesquiterpenes like humulanes, cadinanes, caryophyllanes, and other compounds [79]. The resin of Araucaria columnaris is rich in aromadendrene and bicyclogermacrene and contains sesquiterpene hydrocarbons and oxygenated sesquiterpenes [80,81]. Similar studies indicated that A. heterophylla contained flavonoids, sesqui and di-terpenes, and phenylpropanoids [81]; two monoterpene resins, b-pinene and a-pinene, were commonly found in wood found in Araucaria angustifolia and such compounds were detected in Norway spruce with many monoterpenoids in wood and bark [82].

Similar to our findings, GC–MS analysis revealed the presence of 4,4’-Dimethyl-2,2’- dimethylenebicyclohexyl-3,3’-diene (14.62%) and Copaene (13.64%) as the most prevailing constituents in C. molmol and A. heterophylla, respectively [59]. Bisabolene was the most abundant component in Commiphora erythraea essential oil (33.9%), fraction 2 (62.5%), and fraction 4 (23.8%), curzerene (32.6%), and α-santalene (30.1%) were the dominant chemical constituents in fractions 1 and 3, respectively [57]. Similar studies indicated that two resins, Commiphora myrrha and Commiphora africana, are rich in sesquiterpenes and sesquiterpene lactones through GC-MS analysis with anti-inflammatory and anticancer potential [83].

Finally, our data and others confirm that the presence of many secondary metabolites such as sesquiterpenes, phenols, aromatic terpenoids, fatty alcohol, eugenol, and many other bio-effective compounds may explain the effectiveness of A. heterophylla and C. molmol resin extracts against insect pests [82,84,85].

Phenolics are linked to toxicity against because they are important in plant-herbivore and pathogen interactions. Antioxidant characteristics were found in phenolic chemicals, which are thought to be the primary cause of the pesticide effect in nature [86]. The mode of action of C. molmol extract was revealed through histopathological and transmission election microscope of treated A. persicus via penetrating the cuticle towards the body cavity of treated ticks, destroying the epithelial gut cells, and ultimately resulted in the death of ticks. Moreover, lysing of epithelial gut cells with an irregularly distributed nucleus was commonly PT with low concentrations and rarely PT with high concentrations of C. molmol, whereas lysed epithelial gut cells (without nucleus or with aggregated one beside the basal lamina) were commonly observed PT with high concentrations and rare recorded PT with low concentrations [65,69]. Using plant-based pesticides had minimum or low toxicity for non-target organisms [5]. Specifically, the safety of Commiphora spp. was confirmed after oral toxicity in mice and rats [63].

3. Materials and Methods

3.1. Pest Collections

The collection of the adult stage of four pests of mixed sex was done from May to July 2021. The camel tick, Hyalomma dromedarii (Koch, 1844) and cattle tick, Rhipicephalus (Boophilus) annulatus, formerly Boophilus annulatus (Say, 1821), (Acari: Ixodidae), were collected from areas around infested camel and cattle, respectively, at the slaughterhouse in Jazan Province, Saudi Arabia. The adult cattle louse fly, Hippobosca maculata Leach (Diptera: Hippoboscidae) was collected from infested cattle mainly in the ears and tails. The cattle louse, Haematopinus eurysternus, was collected from the dewlap, cheeks, neck, flank, withers, and back of infested cattle. Pests were collected from and around animals that had no previous exposure to pesticides.

3.2. Collection of Plant Materials

A. heterophylla and C. molmol were collected from different areas in Saint Catherine (28°33′42″ N, 33°56′57″ E, altitude 2624), South Sinai Governorate, Egypt in May 2021. C. molmol resin was obtained as amber solid crystals, while A. heterophylla resin was a flexible white colloidal form (Figure 1). Plants were identified at the Flora and Phytotaxonomic section of the Agricultural Research Center in Giza, Egypt.

Figure 1.

Figure 1

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The tree of Araucaria heterophylla in Saint Catherine area (A), massive resinous sap outpouring of the trunk Araucaria heterophylla (B).

3.3. Preparation of Plant Extracts

Stock solutions of the plant oil-resins A. heterophylla and C. molmol were extracted by mechanically grinding 50 g of both plant oil-resins using a stainless-steel electric mixer and placing the powder in a Soxhlet apparatus for 6–8 h according to the type of solvent. Methanol and hexane were used as solvent, individually. The solution was filtered using Whatman No. 1 filter paper through a Buchner funnel, and the extracts were dried in an oven at 30 °C for 6 h. The extracts were stored in a dark bottle in a refrigerator at −5 °C for 24 h prior to the experiment [52].

3.4. Bioassays

The pesticide effectiveness of methanol and hexane extracts of A. heterophylla and C. molmol was evaluated against four ectoparasites, H. dromedarii, R. annulatus, Hi. maculate, and Ha. eurysternus. Preliminary experiments each containing 30 adult pests, grouped in three replicates, were made to evaluate the range of concentrations used for each pest. Treated envelopes were used [74]. The adult cattle and camel ticks were treated with the following concentrations: 1.6, 3.1, 6.3, 12.5, 25 mg/mL, while adult cattle louse fly and cattle louse were treated with the following concentrations: 0.8, 1.6, 3.1, 6.3, 12.5 mg/mL. Three replicates (each contained ten adult pests) were used for each concentration.

Each group of pests were added to a filter paper envelope, Whatman filter paper No.1, 125 mm diameter, and treated with a single concentration of the plant extracts as 3 mL test solution uniformly distributed with a pipette on internal surfaces of the envelopes. The control envelopes were impregnated with distilled water. The opening of the envelopes was folded and secured with a metallic clip with its identification marks like tested solution and concentration. Each treated replicate of pests was transported to a Petri dish lined with a filter paper. Treated pests were kept at 28 ± 2 °C and a relative humidity of 80 ± 5%. Mortalities were recorded one, three and seven days post-treatment (PT).

3.5. Biochemical Analysis

Biochemical analyses were made using GC/MS, a Thermo Scientific Trace GC Ultra/ISQ Single Quadrupole MS, TG-5MS fused silica capillary column, 0.1 mm, 0.251 mm, and 30 m thick. An electronic ionizer with 70 eV ionization energy was used. Helium gas was utilized as a carrier gas (flow rate = 1 mL/min). The injector and MS transmission line were set at 280 °C. The oven temperature was set at 50 °C, then increased to 150 °C at a rate of 7 °C per minute, then to 270 °C at a rate of 5 °C per minute (wait for 2 min), and finally to 310 °C at a rate of 3.5 °C/min (continued for 10 min). To investigate the quantification of all components found, a relative peak area was used. By comparing the retention periods and mass spectra of the chemicals with those of NIST, Willy Library data from the GC-MS instrument, and the chemicals were tentatively identified. The collective spectra of user-generated reference libraries were used for identification. Single-ion chromatographic reconstructions were used to assess peak homogeneity. Co-chromatographic analysis of reference compounds was performed whenever possible to confirm GC retention times [87,88].

3.6. Data Analyses

The data were analyzed by the software, SPSS V23 (IBM, New York, NY, USA), for doing the Probit analyses to calculate the lethal concentration (LC) values and the one-way analysis of variance (ANOVA) (Post Hoc/Turkey’s HSD test). The significant levels were set at p < 0.05.

4. Conclusions

It is crucial to safeguard livestock and domesticate animals from blood-feeding ectoparasites and vector-borne diseases. Worldwide, pest control is dependent on conventional pesticides, but resistance has developed to almost all classes of pesticides. Botanicals as eco-friendly pesticides represent conspicuous alternatives because of the wide diversity and high effectiveness of several plant-borne compounds. This study revealed, for the first time according to our knowledge, the efficacy of methanol and hexane extracts of C. molmol and A. heterophylla against four camel and cattle blood-sucking arthropods.

Our results confirmed that cattle lice and the louse fly were more susceptible (12.5 mg/mL) than cattle and camel ticks (25.0 mg/mL) to A. heterophylla and C. molmol extracts. Both methanol extracts were recommended as an ideal eco-friendly and inexpensive pest control approach that could be incorporated into integrated pest management used for the protection of large animals from vectors and vector-borne diseases. Further studies could be directed towards the field application and safety profile of C. molmol and A. heterophylla against non-target organisms as well as studying the synergistic effects of surfactants.

Acknowledgments

The co-authors would like to thank the funding agency of this work, the Science, Technology, and Innovation Funding Authority, Egypt. [Grant number 41608] for funding the project title: “Eco-friendly Pesticides against Pests of Medical, Veterinary, and Agricultural Importance”.

Author Contributions

Conceptualization, M.M.B., A.S. and H.F.K.; methodology, M.M.B., M.M.H., A.S., H.F.K., E.S.S., S.A.S., Y.A.E.-S. and R.S.B.; software, M.M.B., S.A.S. and A.S.; validation, M.M.B., A.S., H.F.K., R.S.B. and Y.A.E.-S.; formal analysis, M.M.B., A.S., E.S.S., S.A.S. and H.F.K.; investigation, M.M.B., A.S., H.F.K. and R.S.B.; data management, M.M.B., H.F.K., E.S.S., M.M.H., Y.A.E.-S. and R.S.B.; writing—original draft preparation, M.M.B., M.M.H., A.S., E.S.S. and H.F.K.; writing—review and editing, M.M.B., A.S., H.F.K., R.S.B., S.A.S. and Y.A.E.-S.; supervision, M.M.B., A.S. and H.F.K.; All authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare that they have no conflict of interest.

Funding Statement

This work was supported by the Science, Technology, and Innovation Funding Authority, (STIFA) Egypt. [Grant number 41608]; Project title: “Eco-friendly Pesticides against Pests of Medical, Veterinary, and Agricultural Importance”.

Footnotes

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  • 1.Perveen N., Muzaffar S.B., Vijayan R., Al-Deeb M.A. Microbial communities associated with the camel tick, Hyalomma dromedarii: 16S rRNA gene-based analysis. Sci. Rep. 2020;10:17035. doi: 10.1038/s41598-020-74116-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Hussain S., Saqib M., Ashfaq K. First Molecular Evidence of Coxiella Burnetii in Ticks Collected from Dromedary Camels in Punjab. Pakistan. Pak. Vet. J. 2022;42:276–280. [Google Scholar]
  • 3.Rahman A., Kashif M., Nasir A., Idrees A., Jamil M., Qadir A., Qasim M., Khan I., Aziz H., Qazi I., et al. A Review of Tick and Tick Control Strategies in Pakistan. Pak. J. Med. Health Sci. 2022;16:652–655. doi: 10.53350/pjmhs22161652. [DOI] [Google Scholar]
  • 4.Benelli G., Duggan M.F. Management of Arthropod Vector Data–Social and Ecological Dynamics Facing the One Health Perspective. Acta. Trop. 2018;182:80–91. doi: 10.1016/j.actatropica.2018.02.015. [DOI] [PubMed] [Google Scholar]
  • 5.Khater H.F. Prospects of botanical biopesticides in insect pest management. J. Appl. Pharm. Sci. 2012;3:641–656. doi: 10.7324/japs.2012.2546. [DOI] [Google Scholar]
  • 6.Abbas R.Z., Zaman M.A., Colwell D., Gilleard J., Iqbal Z. Acaricide resistance in cattle ticks and approaches to its management: The state of play. Vet. Parasitol. 2014;203:6–20. doi: 10.1016/j.vetpar.2014.03.006. [DOI] [PubMed] [Google Scholar]
  • 7.Pavoni L., Benelli G., Maggi F., Bonacucina G. Nano-Biopesticides Today and Future Perspectives. Academic Press; Cambridge, MA, USA: 2019. Green Nanoemulsion Interventions for Bi-opesticide Formulations; pp. 133–160. [Google Scholar]
  • 8.Khater H.F., Selim A.M., Abouelella G.A., Abouelella N.A., Murugan K., Vaz N.P., Govindarajan M. Commercial Mosquito Repellents and Their Safety Concerns. In: Fyson K., editor. Malaria. IntechOpen; London, UK: 2019. pp. 1–27. [Google Scholar]
  • 9.Pinheiro L.A., Dáder B., Wanumen A.C., Pereira J.A., Santos S.A.P., Medina P. Side Effects of Pesticides on the Olive Fruit Fly Parasitoid Psyttalia concolor (Szépligeti): A Review. Agronomy. 2020;10:1755. doi: 10.3390/agronomy10111755. [DOI] [Google Scholar]
  • 10.Khater H.F. Ecosmart Biorational Insecticides: Alternative Insect Control Strategies. In: Farzana P., editor. Insecticides—Advances in Integrated Pest Management. IntechOpen; Rijeka, Croatia: 2012. pp. 17–60. [Google Scholar]
  • 11.Khater H.F. Bioactivity of Essential Oils as Green Biopesticides: Recent Global Scenario. In: Govil J.N., Bhattacharya S., editors. Recent Progress in Medicinal Plants. Studium Press LLC; Houston, TX, USA: 2013. pp. 151–218. [Google Scholar]
  • 12.El-Ashram S., Aboelhadid S.M., Kamel A.A., Mahrous L.N., Fahmy M.M. First Report of Cattle Tick Rhipicephalus (Boophilus) annulatus in Egypt Resistant to Ivermectin. Insects. 2019;10:404. doi: 10.3390/insects10110404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Steve P., Jan T. Insecticides—Advances in Integrated Pest Management. IntechOpen; London, UK: 2012. The Sophisticated Peptide Chemistry of Venomous Animals as a Source of Novel Insecticides Acting on Voltage-Gated Sodium Channels; pp. 213–250. [DOI] [Google Scholar]
  • 14.Ahmed N., Alam M., Saeed M., Ullah H., Iqbal T., Al-Mutairi K.A., Shahjeer K., Ullah R., Ahmed S., Ahmed N.A.A.H., et al. Global Decline of Insects. IntechOpen; London, UK: 2021. Botanical Insecticides Are a Non-Toxic Alternative to Conventional Pesticides in the Control of Insects and Pests. [DOI] [Google Scholar]
  • 15.Iqbal T., Ahmed N., Shahjeer K., Ahmed S., Al-Mutairi K.A., Khater H.F., Ali R.F. Global Decline of Insects. IntechOpen; London, UK: 2021. Botanical Insecticides and Their Potential as Anti-Insect/Pests: Are They Successful against Insects and Pests? [Google Scholar]
  • 16.Khater H., Hendawy N., Govindarajan M., Murugan K., Benelli G. Photosensitizers in the fight against ticks: Safranin as a novel photodynamic fluorescent acaricide to control the camel tick Hyalomma dromedarii (Ixodidae) Parasitol. Res. 2016;115:3747–3758. doi: 10.1007/s00436-016-5136-9. [DOI] [PubMed] [Google Scholar]
  • 17.Khater H.F., Ramadan M.Y. The acaricidal effect of peracetic acid against Boophilus annulatus and Argas persicus. Acta Sci. Veter. 2018;35:29–40. doi: 10.22456/1679-9216.15806. [DOI] [Google Scholar]
  • 18.Khater H.F., Seddiek S.A., El-Shorbagy M.M., Ali A.M. Erratum To: The Acaricidal Efficacy of Peracetic Acid and Deltamethrin against the Fowl Tick, Argas persicus, infesting laying hens. Parasitol. Res. 2013;112:3669–3678. doi: 10.1007/s00436-013-3563-4. [DOI] [PubMed] [Google Scholar]
  • 19.Seddiek S.A., Khater H.F., El-Shorbagy M.M., Ali A.M. The Acaricidal Efficacy of Aqueous Neem Extract and Ivermectin against Sarcoptes Scabiei Var. Cuniculi in Experimentally Infested Rabbits. Parasitol. Res. 2013;112:2319–2330. doi: 10.1007/s00436-013-3395-2. [DOI] [PubMed] [Google Scholar]
  • 20.Khater H.F., Hendawy N.I. Photoxicity of Rose Bengal against the Camel Tick. Hyalomma dromedarii. Int. J. Vet. Sci. 2014;3:78–86. [Google Scholar]
  • 21.Pavela R., Benelli G. Essential Oils as Ecofriendly Biopesticides? Challenges and Constraints. Trends Plant Sci. 2016;21:1000–1007. doi: 10.1016/j.tplants.2016.10.005. [DOI] [PubMed] [Google Scholar]
  • 22.Benelli G., Pavela R., Canale A., Mehlhorn H. Tick Repellents and Acaricides of Bo-tanical Origin: A Green Roadmap to Control Tick-Borne Diseases? Parasitol. Res. 2016;115:2545–2560. doi: 10.1007/s00436-016-5095-1. [DOI] [PubMed] [Google Scholar]
  • 23.Muhammad G., Naureen A., Firyal S., Saqib M. Tick Control Strategies in Dairy Production Medicine. Pak. Vet. J. 2018;28:43–50. [Google Scholar]
  • 24.Ara C., Arshad A., Faheem M., Khan M., Shakir H.A. Protective Potential of Aqueous Extract of Allium cepa against Tartrazine Induced Reproductive Toxicity. Pak. Vet. J. 2022 doi: 10.29261/pakvetj/2022.029. [DOI] [Google Scholar]
  • 25.Khater H.F. Introductory Chapter: Back to the Future-Solutions for Parasitic Problems as Old as the Pyramids. In: Govindarajan M., Khater H.F., editors. Natural Remedies in the Fight against Parasites. IntechOpen; London, UK: 2017. Benelli G 4–19. [Google Scholar]
  • 26.Khater H.F. Herbal and Horticultural Remedies: Gardening for the Elderly and Physically and Mentally Disabled. Authorhouse UK Ltd.; London, UK: 2020. [Google Scholar]
  • 27.Khater H.F., Ziam H., Abbas A., Abbas R.Z., Raza M.A., Hussain K., Selim A. Avian Coccidiosis: Recent Advances in Alternative Control Strategies and Vaccine Development. Agrobiol. Rec. 2020;1:11–25. doi: 10.47278/journal.abr/2020.003. [DOI] [Google Scholar]
  • 28.Seddiek S.A., El-Shorbagy M.M., Khater H.F., Ali A.M. The Antitrichomonal Efficacy of Garlic and Metronidazole against Trichomonas gallinae Infecting Domestic Pigeons. Parasitol. Res. 2014;113:1319–1329. doi: 10.1007/s00436-014-3771-6. [DOI] [PubMed] [Google Scholar]
  • 29.Vaz N.P., De Oliveira D.R., Abouelella G.A., Khater H.F. The Black Seed, Nigella Sativa (Ranunculaceae), for Prevention and Treatment of Hypertension. In: Govil J.N., Bhardwaj N., editors. Recent Progress in Medicinal Plants. Studium Press LLC; Houston, TX, USA: 2018. pp. 221–244. [Google Scholar]
  • 30.Seddiek S.A., Ali M.M., Khater H.F., El-Shorbagy M.M. Anthelmintic Activity of the White Wormwood, Artemisia herba-Alba against Heterakis gallinarum Infecting Turkey Poults. J. Med. Plants Res. 2011;5:3946–3957. [Google Scholar]
  • 31.Mohsin M., Li L., Huang X., Aleem T.M., Habib J.Y., Ismael A. Immunogenicity and Protective Efficacy of Probiotics with Etimp1c against Eimeria Tenella Challenge. Pak. Vet. J. 2021;41:274–278. [Google Scholar]
  • 32.Abbas R.Z., Zaman M.A., Sindhu D., Sharif M., Rafique A., Saeed Z., Ahmad M. Anthelmintic Effects and Toxicity Analysis of Herbal Dewormer against the Infection of Haemonchus contortus and Fasciola hepatica in Goat. Pak. Vet. J. 2020;40:2074–7764. [Google Scholar]
  • 33.Khater H.F., Ramadan M.Y., El-Madawy R.S. Lousicidal, Ovicidal and Repellent Efficacy of Some Essential Oils against Lice and Flies Infesting Water Buffaloes in Egypt. Vet. Parasitol. 2009;164:257–266. doi: 10.1016/j.vetpar.2009.06.011. [DOI] [PubMed] [Google Scholar]
  • 34.Khater H.F., Geden C.J. Potential of essential oils to prevent fly strike and their effects on the longevity of adult Lucilia sericata. J. Vector Ecol. 2018;43:261–270. doi: 10.1111/jvec.12310. [DOI] [PubMed] [Google Scholar]
  • 35.Govindarajan M., Khater H., Panneerselvam C., Benelli G. One-pot fabrication of silver nanocrystals using Nicandra physalodes: A novel route for mosquito vector control with moderate toxicity on non-target water bugs. Res. Vet. Sci. 2016;107:95–101. doi: 10.1016/j.rvsc.2016.05.017. [DOI] [PubMed] [Google Scholar]
  • 36.Govindarajan M., Rajeswary M., Muthukumaran U., Hoti S., Khater H., Benelli G. Single-step biosynthesis and characterization of silver nanoparticles using Zornia diphylla leaves: A potent eco-friendly tool against malaria and arbovirus vectors. J. Photochem. Photobiol. B Biol. 2016;161:482–489. doi: 10.1016/j.jphotobiol.2016.06.016. [DOI] [PubMed] [Google Scholar]
  • 37.Khater H.F. Biocontrol of Some Insects. Benha University; Benha, Egypt: 2003. Parasitology Egypt. [Google Scholar]
  • 38.Khater H.F., Ali A.M., Bsc G.A.A., Marawan M.A., Govindarajan M., Murugan K., Abbas R.Z., Vaz N.P., Benelli G. Toxicity and growth inhibition potential of vetiver, cinnamon, and lavender essential oils and their blends against larvae of the sheep blowfly, Lucilia sericata. Int. J. Dermatol. 2018;57:449–457. doi: 10.1111/ijd.13828. [DOI] [PubMed] [Google Scholar]
  • 39.Khater H.F., Geden C.J. Efficacy and Repellency of Some Essential Oils and Their Blends against Larval and Adult House Flies, Musca domestica L. (Diptera: Muscidae) J. Vector Ecol. 2019;44:256–263. doi: 10.1111/jvec.12357. [DOI] [PubMed] [Google Scholar]
  • 40.Khater H.F., Hanafy A., Abdel-Mageed A.D., Ramadan M.Y., El-Madawy R.S. Control of the Myiasis-Producing Fly, Lucilia sericata, with Egyptian Essential Oils. Int. J. Dermatol. 2011;50:187–194. doi: 10.1111/j.1365-4632.2010.04656.x. [DOI] [PubMed] [Google Scholar]
  • 41.Khater H.F., Khater D.F. The insecticidal activity of four medicinal plants against the blowfly Lucilia sericata (Diptera: Calliphoridae) Int. J. Dermatol. 2009;48:492–497. doi: 10.1111/j.1365-4632.2009.03937.x. [DOI] [PubMed] [Google Scholar]
  • 42.Khater H.F., Ramadan M.Y., Mageid A.D.A. In Vitro Control of the Camel Nasal Botfly, Cephalopina titillator, with Doramectin, Lavender, Camphor, and Onion Oils. Parasitol. Res. 2013;112:2503–2510. doi: 10.1007/s00436-013-3415-2. [DOI] [PubMed] [Google Scholar]
  • 43.Khater H.F., Shalaby A.A.S. Potential of Biologically Active Plant Oils to Control Mosquito Larvae (Culex pipiens, Diptera: Culicidae) from an Egyptian Locality. Rev. Inst. Med. Trop. Sao Paulo. 2008;50:107–112. doi: 10.1590/S0036-46652008000200008. [DOI] [PubMed] [Google Scholar]
  • 44.Murugan K., Priyanka V., Dinesh D., Madhiyazhagan P., Panneerselvam C., Subramaniam J., Suresh U., Chandramohan B., Roni M., Nicoletti M., et al. Predation by Asian bullfrog tadpoles, Hoplobatrachus tigerinus, against the dengue vector, Aedes aegypti, in an aquatic environment treated with mosquitocidal nanoparticles. Parasitol. Res. 2015;114:3601–3610. doi: 10.1007/s00436-015-4582-0. [DOI] [PubMed] [Google Scholar]
  • 45.Radwan I.T., Baz M.M., Khater H., Alkhaibari A.M., Selim A.M. Mg-LDH Nanoclays Intercalated Fennel and Green Tea Active Ingredient: Field and Laboratory Evaluation of Insecticidal Activities against Culex pipiens and Their Non-Target Organisms. Molecules. 2022;27:2424. doi: 10.3390/molecules27082424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.Radwan I.T., Baz M.M., Khater H., Selim A.M. Nanostructured Lipid Carriers (NLC) for Biologically Active Green Tea and Fennel Natural Oils Delivery: Larvicidal and Adulticidal Activities against Culex pipiens. Molecules. 2022;27:1939. doi: 10.3390/molecules27061939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47.Roni M., Murugan K., Panneerselvam C., Subramaniam J., Nicoletti M., Madhiyazhagan P., Benelli G. Characterization and Biotoxicity of Hypnea musciformis-Synthesized Silver Nanoparticles as Potential Eco-Friendly Control Tool against Aedes aegypti and Plutella xylostella. Ecotoxicol. Environ. Saf. 2015;121:31–38. doi: 10.1016/j.ecoenv.2015.07.005. [DOI] [PubMed] [Google Scholar]
  • 48.Alkenani N.A., Ahmed M.M.M., Al-Solami H.M., Anwar Y., Alghamdi K.M., Ahmad M.S. Molecular Identification and Bio-Control of Mosquitoes Using Black Seeds Extract in Jeddah. Pak. Vet. J. 2021;41:2074–7764. [Google Scholar]
  • 49.Khater H.F., El-Shorbagy M.M., Seddiek S.A. Lousicidal Efficacy of Camphor Oil, D-Phenothrin, and Deltamethrin against the Slender Pigeon Louse, Columbicola columbae. Int. J. Vet. Sci. Med. 2014;2:7–13. doi: 10.1016/j.ijvsm.2013.12.003. [DOI] [Google Scholar]
  • 50.Baz M.M., Selim A., Radwan I.T., Alkhaibari A.M., Khater H.F. Larvicidal and adulticidal effects of some Egyptian oils against Culex pipiens. Sci. Rep. 2022;12:4406. doi: 10.1038/s41598-022-08223-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.Abdel-Meguid A.D., Ramadan M.Y., Khater H.F., Radwan I.T. Louicidal Efficacy of Essential Oils against the Dog Louse, Trichodectes canis (Mallophaga: Trichodectidae) Egypt. Acad. J. Biol. Sci. E. Med. Entomol. Parasitol. 2022;14:1–16. doi: 10.21608/eajbse.2022.218673. [DOI] [Google Scholar]
  • 52.Eltaly R., Mohamed M.B., Ibrahim T.R., Mohamed Y., Hosam S.A., Aabdelfattah S., Hanan A.A.T., Ahmed A.G.F., Khater H.F. Novel Acaricidal Activity of Vitex castus and Zingiber officinale Extracts against the Camel Tick, Hyalomma dromedarii. Int. J. Vet. Sci. 2022;11:479–483. doi: 10.47278/journal.ijvs/2022. [DOI] [Google Scholar]
  • 53.Baz M.M., Eltaly R.I., Debboun M., Selim A., Radwan I.T., Ahmed N., Khater H.F. The Contact/Fu-migant Adulticidal Effect of Egyptian Oils against the House Fly, Musca domestica (Diptera: Muscidae) Int. J. Vet. Sci. 2021;10:355. [Google Scholar]
  • 54.AbouLaila M., El-Sayed S., Omar M., Al-Aboody M., Aziz A.A., Abdel-Daim M., Rizk M., Igarashi I. Myrrh Oil in Vitro Inhibitory Growth on Bovine and Equine Piroplasm Parasites and Babesia microti of Mice. Pathogens. 2020;9:173. doi: 10.3390/pathogens9030173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 55.Rizk E.S.T. Toxicity of Commiphora molmol (Myrrh) Water Suspension to Some Non-Target Aquatic Organisms and Its Molluscicidal and Biological Activities on Bulinus truncatus and Biomphalaria alexandrina (Mollusca, Gastropoda) Egypt. J. Exp. Biol. Zool. 2015;2:207–219. [Google Scholar]
  • 56.Abdul-Ghani R.A., Loutfy N., Hassan A. Myrrh and Trematodoses in Egypt: An Overview of Safety, Efficacy and Effectiveness Profiles. Parasitol. Int. 2009;58:210–214. doi: 10.1016/j.parint.2009.04.006. [DOI] [PubMed] [Google Scholar]
  • 57.Muturi E.J., Hay W.T., Doll K.M., Ramirez J.L., Selling G. Insecticidal Activity of Commiphora erythraea Essential Oil and Its Emulsions Against Larvae of Three Mosquito Species. J. Med. Èntomol. 2020;57:1835–1842. doi: 10.1093/jme/tjaa097. [DOI] [PubMed] [Google Scholar]
  • 58.Hoda S.M., Fahmy M.M., Attia M.M., Rabab M., Shalaby H.A., Massoud A.M. The Insecticidal Activity of Two Medicinal Plants (Commiphora molmol) and (Balanites aegyptiaca) against the Blowfly Lucilia sericata (Diptera: Calliphoridae) Int. J. Adv. Res. Biol. Sci. 2016;3:144–158. [Google Scholar]
  • 59.Baz M.M., Hegazy M.M., Khater H.F., El-Sayed Y.A. Comparative Evaluation of Five Oil-Resin Plant Extracts against the Mosquito Larvae, Culex pipiens Say (Diptera: Culicidae) Pak. Vet. J. 2021;41:2074–7764. [Google Scholar]
  • 60.Elshamy A.I., Ammar N.M., Hassan H.A., Al-Rowaily S.L., Ragab T.I., El Gendy A.E.N.G., Abd-ElGawad A.M. Essential Oil and Its Nanoemulsion of Araucaria heterophylla Resin: Chemical Characterization, Anti-Inflammatory, and Antipyretic Activities. Ind. Crops Prod. 2020;148:112272. doi: 10.1016/j.indcrop.2020.112272. [DOI] [Google Scholar]
  • 61.Samrot A.V., Bhavya K.S., Angalene J.L.A., Roshini S.M., Preethi R., Steffi S.M., Kumar S.S. Utilization of Gum Polysaccharide of Araucaria heterophylla and Azadirachta indica for Encapsulation of Cyfluthrin Loaded Super Paramagnetic Iron Oxide Nanoparticles for Mosquito Larvicidal Activity. J. Biol. Macromol. 2020;153:1024–1034. doi: 10.1016/j.ijbiomac.2019.10.232. [DOI] [PubMed] [Google Scholar]
  • 62.Divvela H.N.D., Duppala L., Kolapalli V.R.M. Isolation and Acute Oral Toxicity Studies of Araucaria heterophylla Novel Natural Polysaccharide Gum in Albino Mice. World J. Pharm. Pharm. Sci. 2016;5:702–711. [Google Scholar]
  • 63.Jasim G.A., Al-Zubaidy A.A., Hussein S.M., Sahib H.B., Ahmed B.S. The Acute Toxicity of Commiphora molmol Oleo-Gum-Resin Methanol Extract. Int. J. Pharm. Sci. Rev. Res. 2015;33:109–114. [Google Scholar]
  • 64.Kalala W., Magadula J., Mdegela H. Evaluating Acaricidal Activity of Commiphora swynnertonii (Burtt.) Bark Exudates against Common Ticks in Tanzania. Int. J. Herb. Med. 2014;2:19–25. [Google Scholar]
  • 65.Massoud A.M., Kutkat M.A., El-Khateeb R.M., Labib I.M. Acaricidal Efficacy of Myrrh [Commiphora molmol] on the Fowl Tick Argas persicus [Acari: Argasidae] J. Egypt. Soc. Parasitol. 2005;35:667–686. [PubMed] [Google Scholar]
  • 66.Temba S.G. Ph.D. Thesis. NM-AIST; Arushac, Tanzania: 2017. Acaricidal Investigation of Commiphora swynnertonii (Burtt) Stem Bark Exudate. [Google Scholar]
  • 67.Mkangara M., Erasto P., Chacha M. Acaricidal Activity of Commiphora Swynnertonii (Burtt) Stem Bark Extracts against Adult Rhipicephalus appendiculatus Newman and Amblyomma variegatum. Am. J. Res. Commun. 2014;2:82–92. [Google Scholar]
  • 68.Birkett M.A., Al Abassi S., Kröber T., Chamberlain K., Hooper A.M., Guerin P.M., Wadhams L.J. Antiectoparasitic Activity of the Gum Resin, Gum Haggar, from the East African Plant, Commiphora holtziana. Phytochemistry. 2008;69:1710–1715. doi: 10.1016/j.phytochem.2008.02.017. [DOI] [PubMed] [Google Scholar]
  • 69.Nisbet A.J. Azadirachtin from the neem tree Azadirachta indica: Its action against insects. Anais Sociedade Entomológica Brasil. 2000;29:615–632. [Google Scholar]
  • 70.Figueiredo J.C.G., Nunes Y.R.F., Vasconcelos V.D.O., Arruda S.R., Morais-Costa F., Santos G.S.C., Alvez F.S., Duarte E.R. Effects of leaf extracts of Protium spruceanum against adult and larval Rhipicephalus microplus. Exp. Appl. Acarol. 2019;79:447–458. doi: 10.1007/s10493-019-00447-4. [DOI] [PubMed] [Google Scholar]
  • 71.Abdel-Ghany H.S., Abdel-Shafy S., Abuowarda M., El-Khateeb R.M., Hoballah E.M., Fahmy M.M. Acaricidal Activity of Artemisia Herba-Alba and Melia azedarach Oil Nanoemulsion against Hyalomma dromedarii and Their Toxicity on Swiss Albino Mice. Exp. Appl. Acarol. 2021;84:241–262. doi: 10.1007/s10493-021-00618-2. [DOI] [PubMed] [Google Scholar]
  • 72.Mahran M.O., Wahba A.A., Mansour K.M. In Vitro Acaricidal Effect of Neem Leaves (Azadirachta Indica) and Citrullus colocynthis Extracts against the Camel Ticks, Hyalomma dromedarii (Acari: Ixodidae) J. Ecosyst. Ecography. 2020;10:264–300. [Google Scholar]
  • 73.Campbell J., Boxler D., Davis R. Comparative efficacy of several insecticides for control of cattle lice (Mallophaga: Trichodectidae and Anoplura: Haematopinidae) Veter. Parasitol. 2001;96:155–164. doi: 10.1016/S0304-4017(00)00415-5. [DOI] [PubMed] [Google Scholar]
  • 74.Zahir A.A., Rahuman A.A., Bagavan A., Santhoshkumar T., Mohamed R.R., Kamaraj C., Rajakumar G., Elango G., Jayaseelan C., Marimuthu S. Evaluation of Botanical Extracts against Haemaphysalis bispinosa Neumann and Hippobosca maculata Leach. Parasitol. Res. 2010;107:585–592. doi: 10.1007/s00436-010-1898-7. [DOI] [PubMed] [Google Scholar]
  • 75.Velayutham K., Rahuman A.A., Rajakumar G., Santhoshkumar T., Marimuthu S., Jayaseelan C., Bagavan A., Kirthi A.V., Kamaraj C., Zahir A.A., et al. Evaluation of Catharanthus roseus Leaf Extract-Mediated Biosynthesis of Titanium Dioxide Nanoparticles against Hippobosca maculata and Bovicola ovis. Parasitol. Res. 2012;11:2329–2337. doi: 10.1007/s00436-011-2676-x. [DOI] [PubMed] [Google Scholar]
  • 76.Santhoshkumar T., Rahuman A.A., Bagavan A., Marimuthu S., Jayaseelan C., Kirthi A.V., Kamaraj C., Rajakumar G., Zahir A.A., Elango G., et al. Evaluation of stem aqueous extract and synthesized silver nanoparticles using Cissus quadrangularis against Hippobosca maculata and Rhipicephalus (Boophilus) microplus. Exp. Parasitol. 2012;132:156–165. doi: 10.1016/j.exppara.2012.06.009. [DOI] [PubMed] [Google Scholar]
  • 77.Khater H.F. Bioactivities of Some Essential Oils against the Camel Nasal Botfly, Cephalopina titillator. Parasitol. Res. 2014;113:593–605. doi: 10.1007/s00436-013-3688-5. [DOI] [PubMed] [Google Scholar]
  • 78.Wang X., Liu Y.-S., Nair U.B., Armstrong D.W., Ellis B., Williams K.M. Enantiomeric composition of monoterpenes in conifer resins. Tetrahedron Asymmetry. 1997;8:3977–3984. doi: 10.1016/S0957-4166(97)00600-9. [DOI] [Google Scholar]
  • 79.Otto A., Wilde V. Sesqui-, Di-, and Triterpenoids as Chemosystematic Markers in Extant Co-nifers—A Review. Bot. Rev. 2001;67:141–238. doi: 10.1007/BF02858076. [DOI] [Google Scholar]
  • 80.Lebouvier N., Hüe T., Hnawia E., Lesaffre L., Menut C., Nour M. Acaricidal Activity of Essential Oils from Five Endemic Conifers of New Caledonia on the Cattle Tick Rhipicephalus (Boophilus) microplus. Parasitol. Res. 2013;112:1379–1384. doi: 10.1007/s00436-012-3268-0. [DOI] [PubMed] [Google Scholar]
  • 81.Abdel-Sattar E., Monem A.R.A., Ezzat S.M., El-Halawany A., Mouneir S.M. Chemical and Biological Investigation of Araucaria heterophylla Salisb. Z. Naturforsch. C. 2009;64:819–823. doi: 10.1515/znc-2009-11-1211. [DOI] [PubMed] [Google Scholar]
  • 82.Perotti J.C., da Silva Rodrigues-Corrêa K.C., Fett-Neto A.G. Control of Resin Production in Araucaria angustifolia, an Ancient South American Conifer. Plant Biol. 2015;17:852–859. doi: 10.1111/plb.12298. [DOI] [PubMed] [Google Scholar]
  • 83.Gadir S.A., Ahmed I.M. Commiphora Myrrha and Commiphora africana Essential Oils. J. Chem. Pharm. Res. 2014;6:151–156. [Google Scholar]
  • 84.Shameem I. Phytochemical & Therapeutic Potentials of Murr Makki (Commiphora myrrha): A review. Indian J. Appl. Res. 2018;8:102–104. [Google Scholar]
  • 85.Da Silva J.P., Florean E.O.P.T., Silva R.B., Santos Y.D., Pereira M.M.S., da Silva L.R. Relationship of the Species Commiphora Leptophloeos with Aedes Aegypti: A Review. Res. Soc. Dev. 2022;11:e48711326735. doi: 10.33448/rsd-v11i3.26680. [DOI] [Google Scholar]
  • 86.Ukoroije B.R., Otayor A.R. Review on the Bio-Insecticidal Properties of Some Plant Secondary Metabolites: Types, Formulations, Modes of Action, Advantages and Limitations. Asian J. Res. Zool. 2020;3:27–60. [Google Scholar]
  • 87.Ashmawy N.A., Salem M.Z.M., El-Hefny M., Abd El-Kareem M.S.M., El-Shanhorey N.A., Mohamed A.A., Salem A.Z.M. Antibacterial activity of the bioactive compounds identified in three woody plants against some pathogenic bacteria. Microb. Pathog. 2018;121:331–340. doi: 10.1016/j.micpath.2018.05.032. [DOI] [PubMed] [Google Scholar]
  • 88.El-Hefny M., Mohamed A.A., Salem M.Z.M., Abd El-Kareem M.S.M., Ali H.M. Chemical composition, antioxidant capacity and antibacterial activity against some potato bacterial pathogens of fruit extracts from Phytolacca dioica and Ziziphus spinachristi grown in Egypt. Sci. Hortic. 2018;233:225–232. doi: 10.1016/j.scienta.2018.01.046. [DOI] [Google Scholar]

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