Evaluation of Few Essential Oils for the Management of Parasitic Bee Mites, Varroa destructor (Acari: Varroidae) in Apis mellifera L. Colonies

Abstract

Varroa destructor (Anderson and Trueman), is a greatest rigorous and economical pest of Apis mellifera L. worldwide. Many control measures including application of chemicals are adapted to resistor the influx of mites in hives of honey bee. The indiscriminate use of pesticides involve many problems; cause resistance in mites, residual in honey, wax and potentially hazardous to man and environment. Plantderived mixtures are normally more easily degradable and could show a minor undesirable impact on environment with respect to synthetic compounds. This study was planned to check the efficacy of four different essential oils (neem oil, lemon oil, eucalyptus oil and orange oil) at different doses against percent mortality of Varroa mites. The essential oils were applied at two different doses (2.5ml and 5ml) and percent mortality data was recorded after 12, 24, 48 and 72 h of the application. As seen from results, all essential oils gave satisfactory control of Varroa mites except orange oil. The percent mortality was observed higher in eucalyptus oil (76.13%) at 2.5ml dose. Similarly, at 5ml dose, eucalyptus oil (90.27%), lemon oil (85.54%) and neem oil (82.69%) gave significant control of Varroa mites. With the passage of time, mite mortality percentage increases. Overall, eucalyptus oil at 5ml dose rate gave best result and can be recommended to manage the varroa mite in apiculture.

Full text

Evaluation of Few Essential Oils for the
Management of Parasitic Bee Mites, Varroa
destructor (Acari: Varroidae) in Apis mellifera L.
Colonies
Muhammad Abu Bakar1, Muhammad Anjum Aqueel1, Abu Bakar Muhammad
Raza1, Muhammad Irfan Ullah1,*, Muhammad Arshad1, Mubasshir Sohail1,2
and Jaime Molina-Ochoa3,4
1Department of Entomology, University of Sargodha, Sargodha-40100, Pakistan
2Nuclear Institute of Agriculture, Tando Jam-71000, Pakistan
3Universidad de Colima-Coordinación General de InvestigaciónCientíca-Centro
Universitario de Investigación y Desarrollo Agropecuario, Km. 40 autopista
Colima-Manzanillo, Tecomán, Colima 28930, México
4Universidad de Colima-Facultad de MedicinaVeterinaria y Zootecnia, Tecomán,
Colima 28930, México
Article Information
Received 03 April 2017
Revised 02 July 2017
Accepted 24 July 2017
Available online 13 October 2017
Authors’ Contribution
MAB designed and conducted study.
MAA helped in review and proof
reading; ABMR helped in data
collection and analysisand MIU helped
in review and data interpretation.
MA helped in statistical analysis and
preparation of manuscript; MS helped
in literature and experimentation
and JMO critically reviewed and
interpreted results
Key words
Essential oils, Percent mortality,
Varroa mites.
Varroa destructor (Anderson and Trueman), is a greatest rigorous and economical pest of Apis mellifera
L. worldwide. Many control measures including application of chemicals are adapted to resistor the
inux of mites in hives of honey bee. The indiscriminate use of pesticides involve many problems; cause
resistance in mites, residual in honey, wax and potentially hazardous to man and environment. Plant-
derived mixtures are normally more easily degradable and could show a minor undesirable impact on
environment with respect to synthetic compounds. This study was planned to check the efcacy of four
different essential oils (neem oil, lemon oil, eucalyptus oil and orange oil) at different doses against
percent mortality of Varroa mites. The essential oils were applied at two different doses (2.5ml and 5ml)
and percent mortality data was recorded after 12, 24, 48 and 72 h of the application. As seen from results,
all essential oils gave satisfactory control of Varroa mites except orange oil. The percent mortality was
observed higher in eucalyptus oil (76.13%) at 2.5ml dose. Similarly, at 5ml dose, eucalyptus oil (90.27%),
lemon oil (85.54%) and neem oil (82.69%) gave signicant control of Varroa mites. With the passage of
time, mite mortality percentage increases. Overall, eucalyptus oil at 5ml dose rate gave best result and can
be recommended to manage the varroa mite in apiculture.
INTRODUCTION
The haemolymph serving mite, Varroa destructor
(Anderson and Trueman), is a supreme rigorous pest
menacing honeybee worldwide (Lodesani et al., 1992).
The mite is a parasite on brood of bees causing brood
abnormality, loss of the bees and consequent colony
weakening or escaping (Hosamani et al., 2006). Varroa
mites are external parasites of honey bee that violence both
brood, honeybee’s adult and with a divergent preference
for drone brood (Peng et al., 1987). They slurp the body
uid from both the adults and developing larva, waning
them and curbing life period of the bees which they
* Corresponding author: mirfanullah@uos.edu.pk
0030-9923/2017/0006-2005 $ 9.00/0
Copyright 2017 Zoological Society of Pakistan
nourish on. Developing brood might stay instinctive with
deformed wings. Unprocessed in uxes of V. destuctor
can reason of colonies of honeybee to downfall (Martin,
1994). Mites instigated 30-70% colony loss of A. mellifera
and also condensed the honey production and (Woo and
Lee, 1997). Unfortunately, ectoparasitic mites attack on
honeybees, resulting low yield of honey and also cause
absconding and swarming (Mahmood et al., 2011).
Altered approaches have been functional to
accomplish Varroa mite in modern hives including
chemical, mechanical and ordinary measures. While
organic techniques condensed mite inux and ourished
to a countless level, resistance of mite to most acaricides
used for control was a major problem. Similarly, misuse of
organic compound clues to inappropriate excesses in hive
yields e.g., beeswax and honey (Wallner, 1999).
Liable on unconventional practices in monitoring
ABSTRACT
Pakistan J. Zool., vol. 49(6), pp 2005-2010, 2017. DOI: http://dx.doi.org/10.17582/journal.pjz/2017.49.6.2005.2010

2006
Varroa mites, natural constituents e.g., botanical extracts
and vital oils were employed and exible efcacies were
succeeded as well as integrated controlling of the mite
(Balhareth et al., 2012).
A variety of vital oils have been originated to
revelation acaricides action opposing to V. destructor.
These are distilled from fragrant plants, have passionate
smell, exhibit little injuriousness to animals and bees and
have less detrimental inuence over surroundings and
aeclectic public approval (Isman, 2000). A signicant
quantity of necessary oils and their constituents have been
proven to control the mite, with diverse consequences.
Their miticides or attractant/ repellent properties on insects
and their impact on its reproduction have been calculated.
Vital oils are being locally ordered, useful in liquidation or
in an inert vaporization form (Imdorf et al., 1999).
The beekeepers have been mandatory to practice
unapproved chemicals such as amitraz, sulphur,
phenothiazine, chloro benzilate or diverse pyrethroids
to switch the mite inux. Unrestrained use of these
compounds ran to the expansion of resistance, revival of
the inux and the hazard of residues in the honey which
potency pose a hazard for human consumption (Farooqi
et al., 2016). Keeping in vision the prominence of
nontoxic and non-stained control approaches to destroy
mite residents in bee colonies as well as to emission from
resistance problematic, the present study was planned to
dene the efcacy of different essential oils as miticides
against V. destructor.
MATERIALS AND METHODS
The eld experiment was conducted at Apiary of
University of Sargodha. For conducting this experiment,
four essential oils (neem oil, lemon oil, eucalyptus oil and
orange oil) at two different doses (2.5ml and 5ml) were
used to evaluate their effectiveness against varroa mite. The
experiment was replicated three times. Before application,
entirely the crevices and cracks in the hive were plowed
with mud. Mite collection trays (mite excluders) were
placed through the back side of the hive covered by a
wire screen to prevent the bees from coming into contact
with the debris. A white sticky paper piece was hired on
the lowest line of each box covered with wire mesh. Two
strips of staining paper (5x2 inches each) were drenched
for 24 h in each dose of all treatments (Goswami and
Khan, 2013). Treated strips were hanged between frames
of each hive. Four colonies of equal bee population with
ten frames were selected for each treatment and control.
Data was recorded once before treatment application to
estimate the initial population of varroa mites in each
colony. Sugar shake method was used to estimate mite
infestation by the method used by Ellis and Ellis (2005).
From each colony, 250 adult bees were evaluated to check
the effects of different essential oils. Acetone was applied
on bee hives as control treatment.
Data was recorded after 12, 24, 48, and 72 h of
application by counting the fallen/ dead mite on white
sheet. Sheet was changed daily after data recording.
The number of fallen/dead mites was used to determine
mite mortality percentage. Percent mite mortality in bee
colonies was calculated by using formula (Abbott, 1925):
Where, n is mite population, Co is control and T is treated.
Statistical analysis
The data of percent mortality was statistically analyzed
by three factor factorial analysis of variance considering
essential oils, time interval and doses as variables. Means
of percent mortality were separated using tukey HSD all
pair wise comparison test. All the experimental analysis
was performed using Minitab 16.1 software.
RESULTS AND DISCUSSION
Analysis of variance for percent mortality of
Varroa mites for different essential oils at different
doses after different time interval showed in Table I.
The results showed that treatment (F=146.76, P<0.005),
dose (F=1350.1, P<0.005) and time interval (F=965.8,
P<0.005) was highly signicant. Interaction of doses with
treatment and time interval (F=2.95, P<0.05, F=3.95,
P<0.05), respectively, also showed signicant variation in
percent mortality of mites. Interaction between treatment,
dose and time interval was not signicant at 5% level of
signicance.
Table I.- Efcacy of different essential oils against
Varroa mite at different time interval.
Source DF SS MS F-value P-value
Dose 1 3700.17 3700.17 1350.63 P<0.001
Treatment 3 1206.04 402.01 146.74 P<0.001
Time 3 2897.46 965.82 352.54 P<0.001
Dose × Treatment 324.25 8.08 2.95 P<0.05
Dose × Time 3 32.50 10.83 3.95 P<0.05
Treatment × Time 9 31.13 3.46 1.26 P>0.05
Dose × Treatment ×
Time
9 31.08 3.45 1.26 P>0.05
Error 64 175.33 2.74
Total 95 8097.96
P<0.05, Signicant; P<0.001, highly signicant; P>0.05, non-signicant.
M. Abu Bakar et al.

2007
Mean percent mortality data showed that eucalyptus
oil was best compound against Varroa mites as compared
to other treatment. At 2.5ml dose, the highest mortality of
Varroa mite was observed 72.54 % and 76.17% at 48 and
72 h, respectively, which was signicantly different from
other treatment. Overall percent mortality was observed
less in case of orange oil (Fig. 1A).
At 5ml dose rate, percent mortality of Varroa mites
remains similar. The percent mortality of Varroa mites
was observed higher (84.18%, 90.27%) after 48 and 72
h, respectively, in case of eucalyptus oil. After 72 h, there
was no signicant difference among treatments. Percent
mortality was also observed signicant (85.54%, 82.69%)
in lemon oil and neem oil, respectively, at 72 h (Fig. 1B).
Maximum effect of orange oil at 5ml dose did not exceed
79.2% after 72 h (Fig. 1B). Percent mortality of mites was
increased with the passage of time in all selected essential
oils.
Fig. 1. Mortality (%) of Varroa mites at 2.5 ml (A) and 5
ml (B) dose after application of essential oils at different
time interval, P<0.05. (Similar letters show that means are
not signicantly different from each other within each h
after application).
Overall higher dose (5ml) gave signicant mortality
of Varroa mites at different time interval as compared to
low dose (2.5ml). Overall, the essential oils at 5ml dose
showed 13.83% greater response compared to 2.5ml dose
after 72 h of application. Essential oils have fumigant
action (Kim et al., 2003) and volatile oil could penetrate
organism via the respiratory system resulting in enhanced
efcacy (Choi et al., 2004). Essential oils can inhibit with
basic behavioral functions of certain arthropods (Imdorf
et al., 1999). Some reveal acute noxiousness while others
may action as repulsive substances (Watanabe et al., 1993),
antifeedant (Hough-Goldstein, 1990), or may stay the
development or reproduction or affect with physiological
and biological manners.
The unadventurous pesticides show noxiousness to
the surroundings and injurious effects on human health.
In this situation, there is an emergent attention in botanical
pesticides due to their negligible charges and absence of
environmental side effects (Khater, 2012), which brands
them required replacements to synthetic compound for
controlling pests.
As the risk of resistance growth in mites and
dangerous residues in bee yields, practice of carbon-based
mixtures has develop prevalent all over the world.
Botanic extracts gained from diverse plant species
have been given away to have a wide-ranging variety of
acaricidal action counter to varroosis and also against
other creatures such as bacteria, mites, insects, nematodes
and fungi (Damiani et al., 2009).
Eucalyptus oil was proved as best to control Varroa
mites at 5ml dose. Minimum mortality percentage was
recorded in orange oil at both dose rate of application. Our
ndings were similar to Su et al. (2006) who also reported
the insect killing activity of eucalyptus oils against Varroa
which has been owed to the constituents such as citronellyl
acetate, eucamalol, 1, 8-cineole, p-cymene, citronellal,
limonene and citro nellol. Gonzalez-Gomez et al. (2006)
worked with crude extracts of neem seeds and evaluated
the effects on mites and bees separately. They also found
an important repellency effect against mites. No toxic
effect was found for bees. Similarly, Gonzalez-Gomez et
al., (2012) found more repellency of mite population using
neem extract. According to Melathopoulos et al., (2000a)
neem and canola can be used to suppress the population of
parasitic mites on bees. Kraus et al. (1994) also described
repulsive properties of necessary oils on Varroa. Colin
(1990) assumed that long-term repellency may diminish
Varroa fertility. Djenontin et al. (2012) reported that
Azadirachtin is the supreme vigorous constituent for
preventing and killing pests and can be taking out from
neem oil. Active ingredients in neem oil are azadirachtin,
quercetin nimbin, sodium nimbinate, nimbidin, gedunin,
nimbidol, and salannin.
With the passage of time, mite mortality percentage
increases using essential oils. Calderone and Spivak (1995)
and El-Zemity et al. (2006) also found that essential oils
showed good result against Varroa mite after 48 h of
exposure.
Increasing the mean number of Varroa mite fallen
Management of Parasitic Bee Mites 2007

2008
on the sheet in tested honey bee colonies treated with
essential oils may be due to the activation of the defense
behavior mechanisms of honey bee workers by these
plant oils against Varroa mite. We succeeded to achieve
signicant Varroa mites mortality from eucalyptus and
neem oil without toxicity to the bees. Ghasemi et al. (2011)
reported that essential oil, Thymus kotschyanus gave better
management of mite population with least adverse effects
of insecticidal activity against honeybees. General insect
mortality is dose and exposure time dependent. With the
passage of time the toxicity of essential oils against Varroa
mites increase and proved more potent against Varroa
mites. Salem et al. (1998) initiate that honey bee clusters
which nourished on neem extract exposed the maximum
number of Varroa mite dropped on the sheet. Our result
is closely related with Mahmood et al. (2014) who found
that the efcacy (85.3 %) of neem oil against varroa mites.
They proposed that these extracts affected deviations in
the blood of worker bees and consequently amplied
the number of Varroa mite fallen on the sheet. Neem oil
has the ability to kill phoretic adults of varroa and also
disrupt the reproduction and growth of mites within the
cell (Melathopoulos et al., 2000b). However, Abd El-
Wahab and Ebada (2006) indicated that specic protection
behavior appliances counter to Varroa mite were noticed
in some hybrids and races of honey bee. These appliances
caused in growing the number of fallen Varroa mite on
the end board of bee box. According to Lee et al. (2003),
the monoterpenes that may be lipophilic and volatiles can
enter over breathing and rapidly interfere in physiological
functions of insect. These mixtures can also action openly
as neurotoxic compounds, disturbing octopamine receptors
or acetylcholine esterase activity (Isman, 2000).
CONCLUSION
Essential oils gave best result to control Varroa mites
and did not affect the colony strength of honeybees. The
nding of present study indicated that all essential oils
except orange oil are promising as safe natural product for
control of Varroa mites. Also these essential oils proved to
be harmless to the bees and quite save to the environment.
The use of essential oils may t well into integrated pest
management (IPM) programs for alternative use with
other control measures for the management of Varroa mite
and other pests in honeybee colonies while they enhance
probabilities for colony existence and ensure residue-free
hive products.
Statement of conict of interest
Authors have declared no conict of interest.
REFERENCES
Abbott, W.S., 1925. A method of computing the
effectiveness of an insecticide. J. econ. Ent., 18:
265-267.
Abd El-Wahab, T.E. and Ebada, M.A., 2006. Evaluation
of some volatile plant oils and mavrik against
Varroa destuctor in honeybee colonies. J. appl. Sci.
Res., 2: 514-521.
Balhareth, H.M., Alqarni, A.S. and Owayss, A.A., 2012.
Comparison of hygienic and grooming behaviors
of indigenous and exotic honeybee, Apis mellifera
races in central Saudi Arabia. Int. J. Agric. Biol.,
14: 1005-1008.
Calderone, N.W. and Spivak, M., 1995. Plant extracts
for control of the parasitic mite Varroa jacobsoni
(Acari: Varroidae) in colonies of the western honey
bee (Hymenoptera: Apidae). J. econ. Ent., 88:
1211-1215. https://doi.org/10.1093/jee/88.5.1211
Choi, W.I., Lee, S.G., Park, H.M. and Ahn, Y.J., 2004.
Toxicity of plant essential oils to Tetranychus
urticae (Acari: Tetranychidae) and Phytoseiulus
persimilis (Acari: Phytoseiidae). J. econ. Ent.,
97: 553-558. https://doi.org/10.1093/jee/97.2.553;
https://doi.org/10.1603/0022-0493-97.2.553
Colin, M., 1990. Essential oils of Labiatae for controlling
honey bee varroosis. J. appl. Ent., 110: 19-25.
Damiani, N., Gende, L.B., Bailac, P., Marcangeli,
J.A. and Eguaras, M.J., 2009. Acaricidal and
insecticidal activity of essential oils on Varroa
destructor (Acari: Varroidae) and Apis mellifera
(Hymenoptera: Apidae). Parasitol. Res., 106: 145-
152. https://doi.org/10.1007/s00436-009-1639-y
Djenontin, T.S., Wotto, V.D., Avlessi, F., Lozano,
P., Sohounhloué, D.K. and Pioch, D., 2012.
Composition of Azadirachta indica and Carapa
procera (Meliaceae) seed oils and cakes obtained
after oil extraction. Ind. Crops Prod., 38: 39-45.
https://doi.org/10.1016/j.indcrop.2012.01.005
El-Zemity, S., Rezk, R.H.A. and Zaitoon, A.A., 2006.
Acaricidal activity of some essential oils and their
monoterpenoidal constituents against the parasitic
bee mites, Varroa destructor (Acari: Varroidae). J.
appl. Sci. Res., 2: 1032-1036.
Ellis, A.M. and Ellis, J.D., 2005. The efcacy of dusting
honey bee colonies with powdered sugar to reduce
varroa mite population. Agric. Res. Bee World, 48:
72-79.
Farooqi, M.A., Hasan, M.U. and Arshad, M., 2016.
Toxicity of three commonly used Nicotinoids
M. Abu Bakar et al.

2009 Management of Parasitic Bee Mites 2009
and Spinosad to Apis mellifera L. (Hymenoptera:
Apidae) using surface residual bioassays. Pakistan
J. Zool., 48: 1983-1983.
Ghasemi, V., Moharramipour, S. and Tahmasbi, G.,
2011. Biological activity of some plant essential
oils against Varroa destructor (Acari: Varroidae), an
ectoparasitic mite of Apis mellifera (Hymenoptera:
Apidae). Exp. appl Acarol., 55: 147–154. https://
doi.org/10.1007/s10493-011-9457-1
Gonzalez-Go´mez, R., Otero-Colina, G., Villanueva-
Jimenez, J.A., Pena-Valdivia, C.B. and Antonio
Santizo-Rincon, J., 2012. Repellency of the oily
extract of neem seeds (Azadirachta indica) against
Varroa destructor (Acari: Varroidae). Exp. appl.
Acarol., 56: 261–270. https://doi.org/10.1007/
s10493-012-9517-1
Gonzalez-Gomez, R., Otero-Colina, G., Villanueva-
Jiménez, J.A., Perez-Amaro, J.A. and Soto-
Hernández, R.M., 2006. Azadirachta indica
toxicity and repellence of Varroa destructor (Acari:
Varroidae). Agrociencia, 40: 741-751.
Goswami, V. and Khan, M.S., 2013. Management of
varroa mite, Varroa destructor by essential oil and
formic acid in Apis mellifera Linn. Colonies. J.
Nat. Prod., 6: 206–210.
Hosamani, R.K., Gulati, R. and Sharma, S., 2006.
Bioecology and management of honeybee mite,
Tropilaelaps clareae Delnado and Baker-a review.
Agric. Rev., 27: 191-199.
Hough-Goldstein, J., 1990. Antifeedant effects of
common herbs on the Colorado potato beetle
(Coleoptera: Chrysomelidae). Environ. Ent., 19:
234-238. https://doi.org/10.1093/ee/19.2.234
Imdorf, A., Bogdanov, S., Iba ez Ochoa, R. and
Calderone, N.W., 1999. Use of essential oils for
the control of Varroa jacobsoni Oud. in honey
bee colonies. Apidologie, 30: 209-228. https://doi.
org/10.1051/apido:19990210
Isman, M.B., 2000. Plant essential oils for pest and
disease management. Crop Protect., 19: 603-608.
https://doi.org/10.1016/S0261-2194(00)00079-X
Khater, H.F., 2012. Prospects of botanical biopesticides
in insect pest management. Pharmacologia,
3: 641-656. https://doi.org/10.5567/
pharmacologia.2012.641.656
Kim, S.I., Roh, J.Y., Kim, D.H., Lee, H.S. and Ahn,
Y.J., 2003. Insecticidal activities of aromatic plant
extracts and essential oils against Sitophilus oryzae
and Callosobruchus chinensis. J. Stored Prod.
Res., 39: 293-303. https://doi.org/10.1016/S0022-
474X(02)00017-6
Kraus, B., Koeniger, N. and Fuchs, S., 1994. Screening
of substances for their effect on Varroa jacobsoni:
attractiveness, repellency, toxicity and masking
effects of ethereal oils. J. Api. Res., 33: 34-43.
https://doi.org/10.1080/00218839.1994.11100847
Lee, S., Peterson, C.J. and Coats, J., 2003. Fumigation
toxicity of monoterpenoids to several stored
product insects. J. Stored Prod. Res., 39: 77-85.
https://doi.org/10.1016/S0022-474X(02)00020-6
Lodesani, M., Pellacani, A., Bergomi, S., Carpana,
E., Rabitti, T. and Lasagni, P., 1992. Residue
determination from some products used against
Varroa infestation in bees. Apidologie, 23: 257-
272. https://doi.org/10.1051/apido:19920309
Mahmood, R., Asad, S., Raja, S., Moshin, A.,
Wagchoure, E.S., Sarwar, G., Islam, N. and
Ahmad, W., 2014. Control of Varroa destructor
(Acari: Varroidae) in Apis mellifera (Hymenoptera:
Apidae) by using plant oils and extract. Pakistan J.
Zool., 46: 609-615.
Mahmood, R., Wagchoure, E.S., Raja, S., Sarwar, G.
and Aslam, M., 2011. Effect of thymol and formic
acid against ectoparasitic brood mite Tropilaelaps
clareae in Apis mellifera colonies. Pakistan J.
Zool., 43: 91-95.
Martin, S.J., 1994. Ontogenesis of the mite Varroa
jacobsoni Oud. in worker brood of the honeybee
Apis mellifera L. under natural conditions. Exp.
appl. Acarol., 18: 87-100. https://doi.org/10.1007/
BF00055033
Melathopoulos, A.P., Winston, M.L., Whittington, R.,
Higo, H. and Doux, M.L., 2000a. Field evaluation
of neem and canola oil for the selective control
of the honey bee (Hymenoptera: Apidae) mite
parasites Varroa jacobsoni (Acari: Varroidae) and
Acarapis woodi (Acari: Tarsonemidae). J. econ.
Ent., 93: 559-567. https://doi.org/10.1603/0022-
0493-93.3.559
Melathopoulos, A.P., Winston, M.L., Whittington, R.,
Smith, T., Lindberg, C., Mukai, A. and Moore,
M., 2000b. Comparative laboratory toxicity of
neem pesticides to honey bees (Hymenoptera:
Apidae), their mite parasites Varroa jacobsoni
(Acari: Varroidae) and Acarapis woodi (Acari:
Tarsonemidae), and brood pathogens Paenibacillus
larvae and Ascophaera apis. J. econ. Ent., 93: 199-
209.
Peng, Y.S., Fang, Y., Xu, S. and Ge, L., 1987. The
resistance mechanism of the Asian honey bee,

2010 M. Abu Bakar et al.
Apiscerana Fabr., to an ectoparasitic mite, Varroa
jacobsoni Oudemans. J. Inverteb. Pathol., 49: 54-
60. https://doi.org/10.1016/0022-2011(87)90125-X
Salem, M., Nour, M., El Maasarawy, S. and Zakaria, M.,
1998. Testing medical plants extracts compounds
on haemocytes and varoatosis in honey bees. J.
Agric. Sci. Mansoura Univ., 23: 447-460.
Su, Y.C., Ho, C.L., Wang, E. and Chang, S.T., 2006.
Antifungal activities and chemical compositions of
essential oils from leaves of four eucalypts. Taiwan
J. For. Sci., 21: 49-61.
Wallner, K., 1999. Varroacides and their residues in
bee products. Apidologie, 30: 235-248. https://doi.
org/10.1051/apido:19990212
Watanabe, K., Shono, Y., Kakimizu, A., Okada, A.,
Matsuo, N., Satoh, A. and Nishimura, H., 1993. New
mosquito repellent from Eucalyptus camaldulensis.
J. Agric. Fd. Chem., 41: 2164-2166. https://doi.
org/10.1021/jf00035a065
Woo, K. and Lee, J., 1997. Current status of honey bee
mites in Korea. Honeybee Sci., 18: 175-177.