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Application of Herbal Essential Oil Extract Mixture for Honey Bees (Apis mellifera L.) Against Nosema ceranae and Nosema apis

Asli Özkırım
Asli Özkırım
 and 
Billur Küçüközmen
Billur Küçüközmen
   | Jun 24, 2021
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Article Category: Original Article
Published Online: Jun 24, 2021
Page range: 163 - 175
Received: Jul 22, 2020
Accepted: Feb 23, 2021
DOI: https://doi.org/10.2478/jas-2021-0010
Keywords
© 2021 Asli Özkırım et al., published by Sciendo
This work is licensed under the Creative Commons Attribution 4.0 International License.

Fig. 1

Experimental design of the cage experiment.
Experimental design of the cage experiment.

Fig. 2

HEOEM application method in the cage experiment by spraying the syrup on 190 adult bees in the 225 cm2 surface area of the experimental cages using a 30-ml glass spray bottle.
HEOEM application method in the cage experiment by spraying the syrup on 190 adult bees in the 225 cm2 surface area of the experimental cages using a 30-ml glass spray bottle.

Fig. 3

Experimental design of the field study.
Experimental design of the field study.

Fig. 4

The average numbers of Nosema spp. spores/bee during cage experiment in all groups.
The average numbers of Nosema spp. spores/bee during cage experiment in all groups.

Fig. 5

Comparative results of the average number of Nosema spp. spores in the apiaries differentiated by application method. *MVSN: Mean values of spore numbers at the beginning of the field study. SW:Mean values of the final spore numbers after the application of spraying with water at the end of the field study SS:Mean values of the final spore numbers after the application of spraying with syrup at the end of the field study FS:Mean values of the final spore numbers after the application of feeding with syrup at the end of the field study **Missing data belong to SS in 2,3,8,9th apiaries could not be shown because of robbing behaviour. All of the experiments’ data on individual basis are presented in supplementary table online.
Comparative results of the average number of Nosema spp. spores in the apiaries differentiated by application method. *MVSN: Mean values of spore numbers at the beginning of the field study. SW:Mean values of the final spore numbers after the application of spraying with water at the end of the field study SS:Mean values of the final spore numbers after the application of spraying with syrup at the end of the field study FS:Mean values of the final spore numbers after the application of feeding with syrup at the end of the field study **Missing data belong to SS in 2,3,8,9th apiaries could not be shown because of robbing behaviour. All of the experiments’ data on individual basis are presented in supplementary table online.

Plant properties and bioactivities considered in preparing HEOEM

Species Major components Bioactivities References
Rumex acetosella Oxalate (binoxalate) of potassium, tannic acid, and nitrogenous matter Refrigerant, asidic and diuretic https://www.henriettes-herb.com/eclectic/kings/rumex-acet.html
Achillea millefolium Artemisia ketone, camphor, linalyl acetate and 1,8-cineole Anti-inflammatory and disinfectant Ghanbari et al., 2017
Plantago lanceolata Flavonoids, alkaloids, terpenoids, phenolic compounds (caffeic acid derivatives), iridoid glycosides, fatty acids, polysaccharides and vitamins Anti-inflammatory antimicrobial activity, antioxidant and cytotoxic activity, anti-tumoural activity and antispasmodic Bajer et al., 2016
Salvia officinalis Cis-thujone, camphor, cineole, humulene, trans-thujone, camphene, pinene, limonene, bornyl acetate and linalool Antibacterial, antioxidant, antimicrobial, insecticidal and allelopathic activities antitumoral antidiabetic and antioxidant Khedher et al., 2017
Thymus vulgaris Geraniol, linalool, gamma-terpineol, carvacrol, thymol and trans-thujan-4-ol/terpinen-4-ol, p-cymene, γ-terpinene and thymol Antimicrobial, antitussive, antibroncholitic, antispasmodic, anthelmintic, carminative, antiseptic, antioxidant, diuretic Borugă et al., 2014
Rosmarinus officinalis Rosmarinic acid, caffeic acid, ursolic acid, betulinic acid, carnosic acid and carnosol, camphor, 1,8-cineole, α-pinene, borneol, camphene, β-pinene and limonene Antibacterial, antiviral, antioxidant and anti-inflammator, antidiabetic anti-inflammatory, antitumor and antioxidant Andrade et al., 2018
Laurus nobilis 1,8-cineole, sabinene, and linalool Antibacterial, antioxidant, antifungal, cytotoxic Caputo et al., 2017

Differences between groups regarding application doses classified by Duncan test

Subgroups Subset for alpha = .05 The number of Nosema spp. spores/bee±SE
Cages N (Sampling days) a* b* c* d* *e
ExpNa(2) 8 428703±21.3
ExpNc(2) 8 471887±24.2
ExpNa(1) 8 518812±28.1
ExpNc(1) 8 639750±24.6
PCNa 8 3337500±126.3
PCNc 8 3750000±131.7
NCNa 8 41519226±336.3
NCNc 8 40621143±321.8

Comparison of numbers of Nosema spp. spores following varying HEOEM application methods analysed by Duncan test

Subgroups Subset for alpha = .05 The number of Nosema spp. spores/bee (×106)±SE
Appl. methods N (apiaries) a* b* c* d*
SW 9 1.23±0.1
SS 9 2.27±0.4
FS 9 2.60±0.2
PC 9 4.48±0.2
MVSN 9 10.26±1.8

Number of dead bees and final mortality rates (%) during the cage experiments

Sampling Days Total number of dead bees Final mortality rates(%)
Cages Cage number 3 6 9 12 15 18 21 (190 newly emerged bees at the beginning point x10 cages)
ExpNa(1) 1–10 5 15 33 48 63 85 93 342 18.0
ExpNa(2) 1–10 5 15 17 29 34 51 64 215 11.3
PCNa 1–2 0 6 15 11 20 27 53 132 34.7
NCNa 1–2 1 11 20 31 59 95 117 334 87.8
ExpNc(1) 1–10 8 14 32 39 85 108 165 451 23.7
ExpNc(2) 1–10 8 11 29 33 51 81 102 315 16.5
PCNc 1–2 0 13 15 22 30 48 70 198 52.1
NCNc 1–2 15 25 46 59 70 105 59 380 100
Native 1–2 1 5 8 10 12 10 15 61 16.0
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