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Medical and Veterinary Entomology (2010) 24, 1–8

Environmental interactions with the toxicity of plant


essential oils to the poultry red mite Dermanyssus
gallinae
1 1 2 1
D. R. G E O R G E , O. A. E. S P A R A G A N O , G. P O R T , E. O K E L L O ,
1 1
R. S. S H I E L and J. H. G U Y
1 Faculty
of Science, Agriculture and Engineering, School of Agriculture, Food and Rural Development, Newcastle University,
Newcastle upon Tyne, U.K. and 2 Faculty of Science, Agriculture and Engineering, School of Biology, Newcastle University,
Newcastle upon Tyne, U.K.

Abstract. The toxicity of a range of plant essential oils to the poultry red mite,
Dermanyssus gallinae (De Geer) (Acari: Dermanyssidae), a serious ectoparasitic pest
of laying hens throughout Europe and elsewhere, was assessed in the laboratory.
Dermanyssus gallinae may cause losses in egg production, anaemia and, in extreme
cases, death of hens. With changes in legislation and consumer demand, alternatives
to synthetic acaricides are needed to manage this pest. Fifty plant essential oils were
selected for their toxicity to arthropods reported in the literature. Twenty-four of
these essential oils were found to kill >75% of adult D. gallinae in contact toxicity
tests over a 24-h period at a rate of 0.21 mg/cm2 . Subsequent testing at lower rates
showed that the essential oils of cade, manuka and thyme were especially toxic to
adult D. gallinae. The toxicity of the seven most acaricidal essential oils was found
to be stable at different temperatures likely to be encountered in commercial poultry
housing (15◦ C, 22◦ C and 29◦ C), although results suggest that humidity and dust might
influence the toxicity of some of the oils tested. The toxicity of clove bud essential oil
to D. gallinae, for example, was increased at high humidity and dust levels compared
with ambient levels. The results suggest that certain essential oils may make effective
botanical pesticides for use against D. gallinae, although it is likely that issues relating
to the consistency of the toxic effect of some oils will determine which oils will be
most effective in practice.

Key words. Dermanyssus gallinae, botanical pesticide, essential oil, pest manage-
ment, poultry.

Introduction birds in these systems, of approximately 72 weeks, allows time


for large populations of D. gallinae to become established in
The poultry red mite, Dermanyssus gallinae (De Geer), is the poultry house (Höglund et al., 1995). A study by Guy et al.
the most economically deleterious parasite of laying hens in (2004) confirmed the widespread prevalence of D. gallinae in
Europe (Chauve, 1998). It is an obligatory haematophagous commercial laying hen housing systems in the U.K. with the
ectoparasite of both domestic and wild birds, known to obtain finding that 87.5% of premises surveyed were infested and
its bloodmeal from a range of alternative species, including population levels were higher in free-range units compared
man (Bruneau et al., 2001). Although not entirely species- with cage systems. Increased D. gallinae populations in
specific, D. gallinae is seen most frequently in systems for free-range systems have also been reported by Arkle et al.
laying hens. This is largely because the lengthy turnover of (2006).

Correspondence: Dr David George, School of Agriculture, Food and Rural Development, Newcastle University, Newcastle upon Tyne, NE1
7RU, U.K. Tel.: +44 191 222 8893; Fax: +44 191 222 6720; E-mail: D.R.George@ncl.ac.uk

© 2010 The Authors


Journal compilation © 2010 The Royal Entomological Society 1
2 D. R. George et al.

The consequences of infestation by D. gallinae are severe by volatile oil preparations of either citronella or tea tree (Mägi
for both the welfare of the birds and the economic sustain- et al., 2006). After two applications, preparations of both of
ability of the enterprise. The feeding mite can cause irritation, these oils reduced in vivo mite infestation levels by 95%. In
restlessness and either mild or severe anaemia, occasionally addition, the mode of action of essential oils might benefit
resulting in death (Wojcik et al., 2000; Cosoroaba, 2001). their use as acaricides for D. gallinae. Kim et al. (2004, 2007)
Behavioural observations have also shown increases in canni- suggested that the acaricidal effect of selected essential oils
balistic feather pecking associated with D. gallinae infestation against D. gallinae was attributable to action in the vapour
(Kilpinen, 1999). Production is affected through reductions in phase. This would be beneficial in the management of pests
the growth rate of hens, egg production and egg quality, in that have a predisposition to seek refuge in cracks and crevices.
which poor shell integrity and blood-staining of the shell sur- The aim of the present study was to identify one or more
face may occur (Chauve, 1998). In a study of a caged housing botanical pesticides effective against D. gallinae from a range
system, mortality of birds rose from 1% to 4% as a result of of plant essential oils. This was achieved by a two-stage pro-
parasitism by D. gallinae and egg production was reduced by cess: firstly, by producing a shortlist of the most acaricidal
approximately 10% (Wojcik et al., 2000). Dermanyssus galli- essential oils and, secondly, by assessing the toxicity of the
nae is also a threat in the spread of disease, as it may act as most effective oils to D. gallinae under varying environmental
a vector for a number of pathogenic poultry infections, both conditions similar to those encountered in commercial poultry
bacterial and viral (Chirico et al., 2003). housing systems.
The tendency of D. gallinae to occupy small cracks and
crevices in the poultry house substructure (Bruneau et al.,
2001), its ability to survive for extended periods without taking Materials and methods
a bloodmeal (Axtell, 1999) and its rapid population growth
(under optimal conditions the lifecycle of D. gallinae from Selection of plant essential oils
egg to adult can be completed within 1 week) make eradication
very challenging (Kilpinen, 2001). The most common form of Fifty plant essential oils were chosen for study based
control for D. gallinae involves the application of synthetic on a review of the literature describing plant-derived prod-
pesticides. However, the number of effective pesticides ucts that have been shown to control ectoparasites, with
registered for application in poultry houses is relatively low for an emphasis on those effective against mites. The essential
various reasons, including the development of mite resistance oils were obtained from New Directions U.K. (Southampton,
(Beugnet et al., 1997; Kim et al., 2004; Fiddes et al., 2005), U.K.), Absolute Aromas (Alton, U.K.) and Fleur Aromatherapy
chemical and antibiotic residues in food and undesirable (Kingham, U.K.).
environmental effects (Dalton & Mulcahy, 2001).
Plant-derived products including essential oils may offer
an alternative and effective means of managing D. gallinae Dermanyssus gallinae source
populations. Such products may be attractive as botanical
pesticide candidates as they are environmentally non-persistent Dermanyssus gallinae were collected weekly from a com-
and generally possess low mammalian toxicities, unlike many mercial free-range unit in Northumberland, U.K., and stored in
of the available synthetic alternatives (Isman, 2000, 2006). sealed plastic bags at 22◦ C under a 16:8 h light : dark (L : D)
Several pesticides based on plant constituents are already used regime. Mites were collected by directly transferring groups of
widely in certain areas of pest management. For example, individuals from the poultry house structure into the bags used
products based on extracts from the neem tree, particularly its for storage. Mites were collected on Fridays and used in tests
seeds, are common. Indeed, neem extracts are reported to have within 6 days of collection. To ensure consistency of results,
biocidal effects against 200 species of arthropod pest (Choi only recently fed adult females were used where mites that
et al., 2004). were darker in colour were assumed to have fed more recently
In the case of veterinary ectoparasites, work has shown than paler individuals.
that an aqueous extract from camomile flowers (10%) resulted
in 100% mortality of Psoroptes cuniculi (Delafond), a mite
responsible for causing otoacariasis in domestic animals General methods
(Macchioni et al., 2004). Perrucci et al. (1995) found that
both thymol and eugenol, the primary components of thyme All of the following toxicity tests were conducted by
and clove bud essential oils, respectively, killed 100% of the impregnating filter papers (Whatman No. 2, 4.25 cm in diam-
same mite species in both contact and inhalation toxicity tests. eter; Fisher Scientific, Loughborough, U.K.) with the desired
In a study by Mignon and Losson (1996), a phyto-aromatic amount of essential oil in 50 μL ethanol. All experiments
gel based on more than a dozen plant-derived products was included control treatments in which filter papers were impreg-
effective in controlling the ear mite Otodectes cynotis (Hering) nated with 50 μL ethanol only. Following application of the
in both dogs and cats. A similar product had the same effect treatments, individual filter papers were placed in glass Petri
when used against the mange mite Sarcoptes scabiei (L.) on dishes (4.8 cm in diameter, 1.2 cm in height; Fisher Scien-
dogs (Das, 1996). Plant-derived products may also be of use tific) and left for 3 min in a fume cupboard. Approximately 23
in managing pests of livestock. The pig mange mite, Sarcoptes D. gallinae were then added to each dish, which was sealed
scabiei var. suis, for example, has been effectively controlled with a layer of cling-film and a layer of Parafilm and left for a
© 2010 The Authors
Journal compilation © 2010 The Royal Entomological Society, Medical and Veterinary Entomology, 24, 1–8
Plant essential oil toxicity to Dermanyssus gallinae 3

period of 24 h. All experiments, unless otherwise stated, were seven essential oils were those of manuka, cade, pennyroyal,
conducted in a climate-controlled growth room (22◦ C, 16:8 h thyme, garlic, clove bud 1 and cinnamon bark (Table 1), which
L : D) at Newcastle University, U.K. Mortality was assessed displayed LD50 , LD90 and LD99 values of ≤0.1, ≤0.2 and
under a mounted lens at 4× magnification. In all experiments, ≤0.3 mg/cm2 , respectively. Separate tests were run to assess
mites were classed as dead if they exhibited no movement after the effect of temperature (15◦ C, 22◦ C, 29◦ C), humidity [40%
repeated agitation with an entomological pin. or 95% relative humidity (RH)] and dust level (0 mg or 18 mg
Where data have been transformed prior to statistical of dust per dish) on the toxicity of essential oils to D. gallinae.
analysis, this has been done to fit the residuals from the The dust used was collected from the poultry unit from
analysis to a normal distribution, as required by the statistical which the D. gallinae had been obtained, where a level of
methods used. Normality was assessed in all cases by the 18 mg of poultry house dust per Petri dish equated to the
Anderson–Darling test. Statistical analysis for all experiments average amount of dust to settle on an undisturbed surface
was performed using minitab (Version 14) (Minitab, Inc., in a 24-h period. The three temperature treatments were run
State College, PA, U.S.A.). concurrently in three different climate-controlled growth rooms
at Newcastle University in complete darkness. A humidity
level of 95% was achieved by adding 200 μL distilled water
Experiment 1. Screening 50 essential oils for toxicity to to the filter papers in addition to the essential oil or ethanol
D. gallinae. A total of 50 different plant essential oils prior to use. When this water was not added, RH values in
(Table 1) were used to impregnate filter papers at a rate Petri dishes were recorded at 40%. Relative humidity was
of 0.21 mg/cm2 . Four replicates were performed for each measured by a simple needle and dial-type herpetologist’s
essential oil. The mortality of D. gallinae after exposure humidity gauge in 1400-mL sealed glass vessels, scaled up
to Ficam W (bendiocarb 80% w/w; Bayer Environmental to have received treatment comparable with that of the Petri
Science, Cambridge, U.K.) at the manufacturer’s recommended dishes. Four replicates for each essential oil were carried out
rate, which equated to 0.21 mg of product in 50 μL ethanol per in all tests.
filter paper, was also assessed for comparison. The percentage mortality of D. gallinae was calculated
The percentage mortality of D. gallinae was calculated with for each essential oil and the control. Mortality between
Abbott’s correction (Abbott, 1925) to account for the control treatments, and between individual oils and the control, was
mortality for each essential oil and Ficam W. It was not then compared by a two-way anova. Data collected at varying
possible to test all essential oils at the same time, so seven temperatures were cube-root transformed prior to analysis.
runs of the experiment were conducted, each of which tested Humidity and dust data did not require transformation prior
selected essential oils, plus a Ficam W treatment and a control. to analysis.
Replicates for any given oil were completed in one run only.
Mortality was compared between treatments using a one-
way analysis of variance (anova) with corresponding Tukey’s Results
tests. Where mortality was 100% in all replicates for a given
treatment, only one treatment was used in the analysis. Data Experiment 1. Screening 50 essential oils for toxicity
to D. gallinae
were arcsine square-root transformed prior to analysis.
There was a significant difference in D. gallinae mortality
between the 50 essential oils (F(41,126) = 15.82, P < 0.001)
Experiment 2. Lethal dose determination for selected essen- (Table 1). Mortality ranged from 100% for 10 of the essential
tial oils. The 24 most toxic essential oils from Experiment 1 oils to <10% for a further six oils. The lowest level of
were used to impregnate filter papers at 0.42, 0.21, 0.11, 0.05, mortality (2.24%) resulted from exposure to the essential oil of
0.03 and 0.01 mg/cm2 . Control filter papers received 50 μL juniper leaf. The average D. gallinae mortality after exposure
ethanol only and hence 0.00 mg/cm2 of essential oil. Four to Ficam W was 97.62%.
replicates were carried out for each essential oil.
Lethal dose (LD) values of LD50 , LD90 and LD99 were
calculated for each essential oil using Probit analysis and com- Experiment 2. Lethal dose of selected essential oils
pared between oils by a one-way anova with corresponding for D. gallinae
Tukey’s tests. LD50 values were cube-root transformed, LD90
values were square-root transformed and LD99 values were There was a significant difference between the LD values
untransformed, prior to analysis. Following analysis, essential obtained for the different essential oils at all LD levels
oils were ranked for their increasing toxicity to D. gallinae. (LD50 : F(23,72) = 12.16, P < 0.001; LD90 : F(23,72) = 12.35,
P < 0.001; LD99 : F(23,72) = 9.16, P < 0.001). Table 2 shows
the essential oils ranked by mortality of D. gallinae. For most
Experiment 3. Determining the toxicity of seven selected essential oils, there was considerable consistency in the ranking
essential oils to D. gallinae under varying environmental of lethality levels; the top seven essential oils were ranked very
conditions. The seven essential oils inducing the greatest consistently in their toxicity to D. gallinae across LD50 , LD90
D. gallinae mortality in Experiment 2 were used to impregnate and LD99 levels. Eucalyptus, lavender 1, citronella, lemongrass
filter papers at each oil’s respective LD50 (in mg/cm2 ). The and pine essential oils were ranked notably differently for
© 2010 The Authors
Journal compilation © 2010 The Royal Entomological Society, Medical and Veterinary Entomology, 24, 1–8
4 D. R. George et al.

Table 1. Nomenclature, origin, source and acaricidal activity of selected essential oils against Dermanyssus gallinae at 0.21 mg oil/cm2 .

% mortality
Essential oil Latin name Country of origin Supplier (with Abbott’s correction)

Cade Juniperus oxycedrus L. France New Directions 100.00 ± 0.00a


Clove bud 1 Eugenia caryphyllata L. Madagascar Absolute Aromas 100.00 ± 0.00a
Garlic Allium sativum L. Mexico New Directions 100.00 ± 0.00a
Lavender 5 Lavandula officinalis Chaix Croatia New Directions 100.00 ± 0.00a
Lemongrass Cymbopogon citratus Stapf. Madagascar Absolute Aromas 100.00 ± 0.00a
Manuka Leptospermum scoparium Forst. New Zealand New Directions 100.00 ± 0.00a
Pennyroyal Mentha pulegium L. France New Directions 100.00 ± 0.00a
Pine (Scots) Pinus sylvestris L. Hungary New Directions 100.00 ± 0.00a
Tea tree Melaleuca alternifolia Cheel Zimbabwe Absolute Aromas 100.00 ± 0.00a
Thyme Thymus vulgaris L. France New Directions 100.00 ± 0.00a
Citronella Cymbopogon nardus L. Sri Lanka Fleur 98.81 ± 1.19ab
Pimento leaf Pimenta dioica L. Jamaica New Directions 98.69 ± 1.31abc
Ficam W NA—synthetic positive control — Bayer Environmental Science 97.62 ± 0.01abcd
Peppermint Mentha piperita L. England Absolute Aromas 97.39 ± 2.61abcd
Lavender 6 Lavandula dentata L. France New Directions 89.97 ± 0.27abcde
Lavender 3 Lavandula angustifolia Miller France/Pop* New Directions 89.96 ± 2.07abcde
Clove leaf Eugenia caryophyllata Thumb. India New Directions 86.83 ± 10.14abcde
Lavender 4 Lavandula officinalis Chaix France New Directions 86.58 ± 6.64abcde
Lavender 1 Lavandula angustifolia Miller Australia New Directions 86.52 ± 5.29abcdef
Cinnamon bark Cinnamomum zeylanicum Breyn. France New Directions 84.74 ± 7.63abcdef
Palmarosa Cymbopogon martini Roxb. India New Directions 84.30 ± 3.67abcdefg
Coriander Coriandrum sativum L. Russia New Directions 78.94 ± 5.02abcdefgh
Eucalyptus 3 Eucalyptus citriodora Hook China New Directions 78.83 ± 11.55abcdefg
Savory Satureja Montana L. France New Directions 77.80 ± 8.00abcdefg
Clove bud 2 Syzgium aromaticum L. India New Directions 75.61 ± 10.42abcdefgh
Lavender 2 Lavandula angustifolia Miller France/MB* New Directions 64.74 ± 7.84bcdefghij
Cinnamon leaf Cinnamomum verum Presl. France New Directions 63.95 ± 12.23abcdefghi
Eucalyptus 4 Eucalyptus staigeriana Muel. Australia New Directions 61.05 ± 13.53bcdefghij
Cinnamon seed Cinnamomum burmanii Blume Sri Lanka New Directions 58.25 ± 8.23cdefghijk
Neroli Citrus aurantium L. France New Directions 54.46 ± 7.12defghijkl
Caraway Carum carvi L. France New Directions 52.86 ± 12.18efghijklm
Geranium Pelargonium graveolens L’Herit France New Directions 51.08 ± 4.41efghijklm
Tansy Tanacetum vulgare L. U.S.A. New Directions 50.65 ± 14.07efghijklmn
Marjoram Origanum marjorana L. France New Directions 44.82 ± 12.04efghijklmno
Oregano Origanum vulgare L. Spain New Directions 37.14 ± 12.89fghijklmno
Sage Salvia officinalis L. Croatia New Directions 32.05 ± 6.75ghijklmno
Wormwood Artemisia scoparia Waldst. China New Directions 30.84 ± 4.41ghijklmno
Absinthe Artemisia absinthium L. China New Directions 29.98 ± 9.70hijklmno
Fir needle Abies siberica Ledeb. Siberia New Directions 27.04 ± 8.37hijklmno
Bay Pimenta racemosa Miller West Indies New Directions 25.85 ± 5.47hijklmno
Spearmint Mentha spicata L. U.S.A. New Directions 20.88 ± 7.81ijklmno
Lime (pressed) Citrus aurantifolia Swing. Italy New Directions 20.58 ± 7.68ijklmno
Eucalyptus 2 Eucalyptus radiata Sieber Australia New Directions 20.23 ± 7.40ijklmno
Rosemary Rosmarinus officinalis L. France New Directions 20.21 ± 6.16ijklmno
Eucalyptus 1 Eucalyptus globulus Labill. China New Directions 13.03 ± 6.10jklmno
Ginger Zingiber officinalis Roscoe France New Directions 9.91 ± 1.69klmno
Lime (distilled) Citrus aurantifolia Swing. Italy New Directions 6.86 ± 4.10mno
Chamomile Chamaemelum nobile L. Hungary New Directions 6.39 ± 2.34lmno
Juniper berry Juniperus communis L. India New Directions 6.26 ± 5.04lmno
Pepper (black) Piper nigrum L. India New Directions 4.75 ± 1.96no
Juniper leaf Juniperus communis L. India New Directions 2.24 ± 4.30o

Percentage mortality rates (± standard errors) have been corrected using Abbott’s correction and are displayed as derived from the original
untransformed data. n = 4 for all means corresponding to essential oils and n = 28 for Ficam W (the positive control). Values followed by the
same letter do not differ significantly (P < 0.05) (Tukey’s test).
∗ For Lavender 2 and 3 essential oils, trade names are MB, Mont Blanc and Pop, Population, respectively.

© 2010 The Authors


Journal compilation © 2010 The Royal Entomological Society, Medical and Veterinary Entomology, 24, 1–8
Plant essential oil toxicity to Dermanyssus gallinae 5

Table 2. Lethal doses (LD) in mg oil/cm2 and rank order for 24 essential oils against Dermanyssus gallinae.

LD mg/cm2 Rank order


Essential oil LD50 LD90 LD99 LD50 LD90 LD99 Overall

Cade 0.01 ± 0.00a 0.04 ± 0.01a 0.06 ± 0.02a 1 1 1 1


Thyme 0.02 ± 0.01a 0.07 ± 0.02ab 0.11 ± 0.03ab 2 2 3 2
Manuka 0.03 ± 0.00ab 0.07 ± 0.00abc 0.10 ± 0.01ab 3 3 2 3
Pennyroyal 0.09 ± 0.01bcd 0.16 ± 0.00bcd 0.22 ± 0.01abc 5 4 4 4
Cinnamon bark 0.08 ± 0.00bc 0.18 ± 0.01cde 0.26 ± 0.01abcd 4 5 5 5
Garlic 0.10 ± 0.01bcd 0.19 ± 0.03def 0.27 ± 0.04bcde 6 6 6 6
Clove bud 1 0.10 ± 0.00cd 0.20 ± 0.01def 0.28 ± 0.01bcde 7 7 7 7
Clove bud 2 0.11 ± 0.01cd 0.23 ± 0.02def 0.32 ± 0.03cdef 9 8 9 8
Lavender 4 0.12 ± 0.03cd 0.23 ± 0.05def 0.33 ± 0.06cdef 11 10 10 9
Lavender 1 0.13 ± 0.03cd 0.23 ± 0.04ef 0.31 ± 0.05cde 15 9 8 10
Pine 0.11 ± 0.01cd 0.24 ± 0.00def 0.35 ± 0.01cdef 8 12 13 11
Lemongrass 0.14 ± 0.03cd 0.24 ± 0.06def 0.33 ± 0.07cdef 17 11 11 12
Coriander 0.12 ± 0.02cd 0.25 ± 0.04def 0.36 ± 0.06cdef 12 14 15 13
Savory 0.14 ± 0.01cd 0.25 ± 0.02def 0.34 ± 0.02cdef 16 13 12 13
Tea tree 0.13 ± 0.01cd 0.26 ± 0.01def 0.36 ± 0.02cdef 14 15 14 15
Citronella 0.16 ± 0.04cd 0.27 ± 0.05def 0.36 ± 0.06cdef 21 16 16 16
Lavender 6 0.15 ± 0.03cd 0.29 ± 0.04def 0.41 ± 0.05cdef 18 17 18 16
Palmarosa 0.13 ± 0.02cd 0.30 ± 0.02def 0.43 ± 0.03def 13 18 22 16
Clove leaf 0.16 ± 0.01cd 0.30 ± 0.02def 0.41 ± 0.03cdef 19 19 19 19
Eucalyptus 3 0.11 ± 0.04cd 0.36 ± 0.08f 0.53 ± 0.11f 10 24 24 20
Lavender 5 0.17 ± 0.02cd 0.31 ± 0.02def 0.42 ± 0.02cdef 23 20 20 21
Peppermint 0.20 ± 0.01d 0.31 ± 0.03def 0.41 ± 0.06cdef 24 22 17 21
Pimento leaf 0.17 ± 0.01cd 0.31 ± 0.02def 0.43 ± 0.02def 22 21 21 23
Lavender 3 0.16 ± 0.01cd 0.33 ± 0.01def 0.47 ± 0.01ef 20 23 23 24

All values are derived from the original untransformed data and presented with ± standard errors. n = 4 for all means, except eucalyptus 3 LD90
and LD99 values, for which n = 3. Values followed by the same letter do not differ significantly (P < 0.05) according to Tukey’s tests. Overall
ranks were obtained by taking the average ranking from LD50 , LD90 and LD99 values.

LD50 values than for the other two lethality levels. There were oils to D. gallinae (F(7,48) = 29.25, P < 0.001), with the
significant differences between the top and lower oils in lethal toxicity of thyme, cade and the control treatment being similar
rates at all levels considered (Table 2). For LD90 and LD99 and significantly lower (P < 0.05) than the toxicity of the
results, one of the data points for eucalyptus 3 essential oil other oils (Fig. 2).
was removed from the analysis as a rank outsider. Dust had a significant effect on the mortality of D. gallinae
overall (F(1,48) = 89.41, P < 0.001) (Fig. 3). There was also a
significant interaction between dust and essential oil (F(7,48) =
Experiment 3. Determining the toxicity of seven selected 4.61, P < 0.01). High dust led to increased D. gallinae
essential oils to D. gallinae under varying environmental mortality, but this increase was again significant only for
conditions cinnamon bark and clove bud 1 (P < 0.05). There was also
a significant difference in the toxic effect of different essential
Temperature had no significant effect on D. gallinae mor- oils on D. gallinae (F(7,48) = 65.12, P < 0.001). Pairwise
tality overall (F(2,72) = 1.53, P = 0.224) and there was no differences are given in Fig. 3.
interaction between temperature and effect of essential oil
(F(14,72) = 0.39, P = 0.973) (Fig. 1). There was a significant
difference between essential oils in the mortality of D. gallinae Discussion
(F(7,72) = 9.84, P < 0.001). The toxicity of the seven essen-
tial oils to D. gallinae was significantly higher than that of The aim of the present study was to identify an effective
the control (P < 0.05), and pennyroyal and garlic were more botanical pesticide for D. gallinae by producing a shortlist of
acaricidal than cade (P < 0.05). the most acaricidal essential oils and assessing the toxicity
Humidity had a significant effect on the mortality of of these under varying environmental conditions. Of the 50
D. gallinae overall (F(1,48) = 21.59, P < 0.001). There was essential oils initially selected for study, a high proportion were
a significant interaction between humidity and essential oil effective as acaricides for D. gallinae. Although some, such as
(F(7,48) = 4.77, P < 0.001). High humidity led to increased black pepper and juniper leaf essential oils, resulted in low
D. gallinae mortality; this increase was significant (P < 0.05) mortality, 24 oils exhibited mortality ≥75% at 0.21 mg/cm2
for both cinnamon bark and clove bud 1. There was also a and were as toxic as Ficam W applied at the manufacturer’s
significant difference in the toxic effect of different essential recommended rate.
© 2010 The Authors
Journal compilation © 2010 The Royal Entomological Society, Medical and Veterinary Entomology, 24, 1–8
6 D. R. George et al.

Fig. 1. Mean mortality (± standard error) (n = 4) of selected essential oils against Dermanyssus gallinae at the LD50 concentration for each oil
at three temperatures. All values are derived from the original untransformed data.

Fig. 2. Mean mortality (± standard error) (n = 4) of selected essential oils against Dermanyssus gallinae at the LD50 concentration for each oil
at high (95%) and ambient (40%) relative humidity.

Garlic essential oil was toxic to D. gallinae in the current Kim et al. (2004) tested 56 plant essential oils for their
study. Garlic-based products are available in several countries acaricidal effects on D. gallinae. Oils from bay, cade, cin-
for use against ectoparasites of poultry. Birrenkott et al. (2000) namon, clove bud, coriander, horseradish, lime (distilled 5F),
found topical application of Garlic Barrier® (Garlic Research mustard, pennyroyal, pimento berry, spearmint and thyme pro-
Labs, Inc., Glendale, CA, U.S.A.) reduced Ornithonyssus duced 100% mite mortality in contact toxicity tests at a rate of
sylviarum (Canestrini & Fanzago) incidence on treated hens 0.07 mg/cm2 . In the present study, several of the same essential
in the U.S.A. and Breck-a-Sol™ (ECOspray Ltd., Hilborough, oils were tested, but were found to be less toxic to D. gallinae
U.K.), a garlic-based acaricide advertised for use against than in the experiments reported by Kim et al. (2004). This
D. gallinae, has recently been approved for use in the U.K. difference for essential oils of the same plant species may
© 2010 The Authors
Journal compilation © 2010 The Royal Entomological Society, Medical and Veterinary Entomology, 24, 1–8
Plant essential oil toxicity to Dermanyssus gallinae 7

Fig. 3. Mean mortality (± standard error) (n = 4) of selected essential oils against Dermanyssus gallinae at the LD50 concentration for each oil
at high (18 mg per dish) and zero (0 mg per dish) dust levels. Values for treatments for which pairs of bars share a common letter do not differ
significantly (P < 0.05).

reflect variations in the chemical composition of products are consistent in their chemistry and toxicity to D. gallinae.
used in different studies. Variations have been reported in the Although between-study variability in the acaricidal effects of
chemical composition of essential oils obtained from differ- essential oils is an issue that may need to be addressed, there
ent varieties of the same plant species (Eyres et al., 2007; are nevertheless numerous factors supporting the use of plant
Moreno et al., 2007) or different parts of a single plant (Talal essential oils as acaricides for D. gallinae.
et al., 2005; Moreno et al., 2007). Numerous factors may affect
the composition of essential oils obtained from the same or
Acknowledgements
similar species of plant. Geographic origin (Muñoz-Bertomeu
et al., 2007; Raal et al., 2007), seasonality (Barra et al., 2007; This work was carried out as part of the MITEeHEN project
Flamini & Cioni, 2007), method of oil extraction (Chiasson to develop plant-based acaricides to control Dermanyssus
et al., 2001), year of harvest (Chalchat et al., 2007) and even gallinae, for which funding from Defra, U.K., is gratefully
storage conditions (Chalchat et al., 2007) have been reported acknowledged. The authors are also grateful to representatives
to influence the constituents of essential oils and so could influ- of the U.K. poultry industry, including British Free Range
ence their toxicity to D. gallinae. Egg Producers Association (BFREPA), the National Farmers
The seven essential oils most toxic to D. gallinae tested Union (NFU) and Noble Foods Ltd., Tring, U.K., for providing
in the present study had a consistent effect across three technical advice on the development of alternative control
temperatures (15◦ C, 22◦ C, 29◦ C). In most cases, the toxic strategies for D. gallinae.
effects of these essential oils remained consistent at different
humidity and dust levels. However, both dust and humidity
influenced cinnamon bark and clove bud 1 toxicity to References
D. gallinae. The remaining essential oils (manuka, cade,
Abbott, W.S. (1925) A method of computing the effectiveness of an
pennyroyal, thyme and garlic) all appeared to be relatively
insecticide. Journal of Economic Entomology, 18, 265–267.
constant in acaricidal effect across a range of environmental
Arkle, S., Guy, J.H. & Sparagano, O. (2006) Immunological effects
conditions in which they might be utilized in poultry systems
and productivity variation of red mite (Dermanyssus gallinae) on
(in temperate climates at least). laying hens—implications for egg production and quality. World’s
In summary, the results obtained identify a number of Poultry Science Journal , 62, 249–257.
essential oils that are acaricidal to D. gallinae and are stable Axtell, R.C. (1999) Poultry integrated pest management; status and
under different environmental conditions. The future challenge future. Integrated Pest Management Reviews, 4, 53–73.
to using plant essential oils as acaricides for D. gallinae may Barra, A., Coroneo, V., Dessi, S., Cabras, P. & Angioni, A. (2007)
lie in identifying oils that are reliable when sourced from Characterization of the volatile constituents in the essential oil of
different countries, years or plant varieties. Alternatively, it Pistacea lentiscus L. from different origins and its antifungal and
may be possible to develop standards for commercial plant antioxidant activity. Journal of Agricultural and Food Chemistry,
growth and oil extraction which yield essential oils that 55, 7093–7098.

© 2010 The Authors


Journal compilation © 2010 The Royal Entomological Society, Medical and Veterinary Entomology, 24, 1–8
8 D. R. George et al.

Beugnet, F., Chauve, C., Gauthey, M. & Beert, L. (1997) Resistance Isman, M.B. (2000) Plant essential oils for pest and disease manage-
of the red poultry mite to pyrethroids in France. Veterinary Record , ment. Crop Protection, 19, 603–608.
140, 577–579. Isman, M.B. (2006) Botanical insecticides, deterrents, and repellents
Birrenkott, G.P., Bockenfelt, G.E., Greer, J.A. & Owens, M.D. (2000) in modern agriculture and an increasingly regulated world. Annual
Topical application of garlic reduces northern fowl mite infestation Review of Entomology, 51, 45–66.
in laying hens. Poultry Science, 79, 1575–1577. Kilpinen, O. (1999) Problems caused by the chicken mite, Dermanys-
Bruneau, A., Dernburg, A., Chauve, C. & Zenner, L. (2001) First in sus gallinae, in Danish egg production. Mange and Myiasis of Live-
vitro cycle of the chicken mite, Dermanyssus gallinae (De Geer stock (ed. by M. Good, M. S. Hall, B. Losson, K. Pithan & J. Sol),
1778), utilizing an artificial feeding device. Parasitology, 123, pp. 61–65. Commission of the European Communities, Brussels.
583–589. Kilpinen, O. (2001) Activation of the poultry red mite, Dermanys-
Chalchat, J.C., Ozcan, M.M., Dagdelden, A. & Akgul, A. (2007) sus gallinae (Acari: Dermanyssidae), by increasing temperatures.
Variability of essential oil composition of Echinophora tenuifolia Experimental and Applied Acarology, 25, 859–867.
subsp. sibthorpiana Tutin by harvest location and year and oil Kim, S., Yi, J., Tak, J. & Ahn, Y. (2004) Acaricidal activity of plant
storage. Chemistry of Natural Compounds, 43, 225–227. essential oils against Dermanyssus gallinae (Acari: Dermanyssidae).
Chauve, C. (1998) The poultry red mite Dermanyssus gallinae (De Veterinary Parasitology, 120, 297–304.
Geer, 1778): current situation and future prospects for control. Kim, S., Na, Y., Yi, J., Kim, B. & Ahn, Y. (2007) Contact and fumi-
Veterinary Parasitology, 79, 239–245. gant toxicity of oriental medicinal plant extracts against Dermanys-
Chiasson, H., Bélanger, A., Bostanian, N., Vincent, C. & Poliquin, A. sus gallinae (Acari: Dermanyssidae). Veterinary Parasitology, 145,
(2001) Acaricidal properties of Artemisia absinthium and Tanacetum 377–382.
vulgare (Asteraceae) essential oils obtained by three methods of Macchioni, F., Perrucci, S., Cecchi, F., Cioni, P.L., Morelli, I. &
extraction. Journal of Economic Entomology, 94, 167–171. Pampiglione, S. (2004) Acaricidal activity of aqueous extracts
Chirico, J., Eriksson, H., Fossum, O. & Jansson, D. (2003) The of camomile flowers, Matricaria chamomilla, against the mite
poultry red mite, Dermanyssus gallinae, a potential vector of Psoroptes cuniculi. Medical and Veterinary Entomology, 18,
Erysipelothrix rhusiopathiae causing erysipelas in hens. Medical 205–207.
and Veterinary Entomology, 17, 232–234. Mägi, E., Järvis, T. & Miller, I. (2006) Effects of different plant
Choi, W., Lee, S., Park, H. & Ahn, Y. (2004) Toxicity of plant products against pig mange mites. Acta Veterinaria Brunensis, 75,
essential oils to Tetranychus urticae (Acari: Tetranychidae) and 283–287.
Phytoseiulus persimilis (Acari: Phytoseiidae). Journal of Economic Mignon, B.R. & Losson, B.J. (1996) Efficacy of a phyto-aromatic
Entomology, 97, 553–558. gel against auricular mange in rabbits and carnivores. Veterinary
Cosoroaba, I. (2001) Massive Dermanyssus gallinae invasion in Record , 138, 329–332.
battery-husbandry raised fowls. Revue de Médecine Vétérinaire, 152, Moreno, P.H.R., Lima, M.E.L., Sobral, M. et al. (2007) Essential oil
89–96. composition of fruit colour varieties of Eugenia brasiliensis Lam.
Dalton, J.P. & Mulcahy, G. (2001) Parasite vaccines—a reality? Scientia Agricola, 64, 428–432.
Veterinary Parasitology, 98, 149–167. Muñoz-Bertomeu, J., Arrillaga, I. & Segura, J. (2007) Essential oil
Das, S.S. (1996) Effect of a herbal compound for treatment of variation within and among natural populations of Lavendula
sarcoptic mange infestations on dogs. Veterinary Parasitology, 68, latifolia and its relation to their ecological areas. Biochemical
303–306. Systematics and Ecology, 35, 479–488.
Eyres, G.T., Marriott, P.J. & Dufour, J. (2007) Comparison of odour- Perrucci, S., Macchioni, G., Cioni, P.L., Flamini, G. & Morelli, I.
active compounds in the spicy fraction of hop (Humulus lupulus L.) (1995) Structure/activity relationship of some natural monoterpenes
essential oil from four different varieties. Journal of Agricultural as acaricides against Psoroptes cuniculi. Journal of Natural Prod-
and Food Chemistry, 55, 6252–6261. ucts—Lloydia, 58, 1261–1264.
Fiddes, M.D., Le Gresley, S., Parsons, D.G., Epe, C., Coles, G.C. & Raal, A., Orav, A. & Arak, E. (2007) Composition of the essential oil
Stafford, K.A. (2005) Prevalence of the poultry red mite (Dermanys- of Salvia officinalis L. from various European countries. Natural
sus gallinae) in England. Veterinary Record , 157, 233–235. Products Research, 21, 406–411.
Flamini, G. & Cioni, P.L. (2007) Seasonal variation of the chemical Talal, A., Mohammad, H. & Vanni, C. (2005) Chemical composition
constituents of the essential oil of Santolina etrusca from Italy. of the essential oil from different aerial parts lavender (Lavendula
Chemistry and Biodiversity, 4, 1008–1019. coronopfolia Poiert) grown in Jordan. Journal of Essential Oil
Guy, J.H., Khajavi, M., Hlalele, M.M. & Sparagano, O. (2004) Red Research, 17, 49–51.
mite (Dermanyssus gallinae) prevalence in laying units in Northern Wojcik, A.R., Greygon-Franckiewicz, B., Zbikowska, E. &
England. British Poultry Science, 45 (Suppl. 1), 15 (Abstract). Wasielewski, L. (2000) Invasion of Dermanyssus gallinae (De Geer,
Höglund, J., Nordenfors, H. & Uggla, A. (1995) Prevalence of the 1778) in poultry farms in the Torun Region. Polish Parasitological
poultry red mite, Dermanyssus gallinae, in different types of Society, 46, 511–515.
production systems for egg layers in Sweden. Poultry Science, 74,
1793–1798. Accepted 30 October 2008

© 2010 The Authors


Journal compilation © 2010 The Royal Entomological Society, Medical and Veterinary Entomology, 24, 1–8

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