Veterinary Parasitology 162 (2009) 129–134

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Veterinary Parasitology

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Repellence of plant essential oils to Dermanyssus gallinae and toxicity tothe non-target invertebrate Tenebrio molitor

D.R. George a,*, O.A.E. Sparagano a, G. Port b, E. Okello a, R.S. Shiel a, J.H. Guy a

a School of Agriculture, Food and Rural Development, Newcastle University, Newcastle upon Tyne NE1 7RU, UKb School of Biology, Newcastle University, Newcastle upon Tyne NE1 7RU, UK

A R T I C L E I N F O

Article history:

Received 12 December 2008

Received in revised form 26 January 2009

Accepted 4 February 2009

Keywords:

Essential oil

Repellent

Dermanyssus gallinae

Toxicity

Non-target

Tenebrio molitor

A B S T R A C T

With changes in legislation and consumer demand, alternatives to synthetic acaricides to

manage the poultry red mite Dermanyssus gallinae (De Geer) in laying hen flocks are

increasingly needed. These mites may cause losses in egg production, anaemia and even

death of hens. It may be possible to use plant-derived products as D. gallinae repellents,

especially if such products have a minimal impact on non-target organisms. An

experiment was conducted with D. gallinae to assess the repellence of a range of plant

essential oils, previously found to be of varying toxicity (relatively highly toxic to non-

toxic) to this pest. Experiments were also undertaken to assess the toxicity of these

products to mealworm beetles (Tenebrio molitor L.), a non-target invertebrate typical of

poultry production systems. Results showed that all seven essential oils tested (manuka,

thyme, palmarosa, caraway, spearmint, black pepper and juniper leaf) were repellent to D.

gallinae at 0.14 mg oil/cm3 (initial concentration) during the first 2 days of study. Thyme

essential oil appeared to be the most effective, where repellence lasted until the end of the

study period (13 days). At the same concentration toxicity to T. molitor differed, with

essential oils of palmarosa and manuka being no more toxic to adult beetles than the

control. There was neither a significant association between the rank toxicity and

repellence of oils to D. gallinae, nor the toxicity of oils to D. gallinae (as previously

determined) and T. molitor.

� 2009 Elsevier B.V. All rights reserved.

1. Introduction

The poultry red mite, Dermanyssus gallinae (De Geer) isthe most economically deleterious parasite of laying hensin Europe (Chauve, 1998) where control and productionlosses due to this pest have been estimated at s130 millionper annum (van Emous, 2005). Feeding mites can causefeather pecking, irritation, restlessness and either mild orsevere anaemia in hens, occasionally resulting in death(Kilpinen, 1999; Wojcik et al., 2000; Cosoroaba, 2001).

* Corresponding author at: School of Agriculture, Food and Rural

Development, Newcastle University, Agriculture Building, Newcastle

upon Tyne NE1 7RU, UK. Tel.: +44 1912228893; fax: +44 1912226720.

E-mail address: D.R.George@ncl.ac.uk (D.R. George).

0304-4017/$ – see front matter � 2009 Elsevier B.V. All rights reserved.

doi:10.1016/j.vetpar.2009.02.009

Production is affected through reduced development ratesof growing hens, reduced egg production and reduced eggquality (poor shell integrity and blood staining of the shellsurface) (Urquhart et al., 1996; Chauve, 1998; Fiddes et al.,2005). D. gallinae are also a threat in the spread of disease,since they may act as vectors for a number of pathogenicpoultry infections, both bacterial and viral (Chirico et al.,2003).

Control of D. gallinae has typically been achieved by theuse of synthetic contact acaricides such as carbaryl,diazinon, dichlorvos and permethrin. However, the con-tinued use of these products may be hampered by issues ofmite resistance (Beugnet et al., 1997; Kim et al., 2004;Fiddes et al., 2005), chemical residues in food andundesirable environmental effects (Dalton and Mulcahy,2001). With increasing D. gallinae resistance to synthetic

Table 1

Nomenclature, origin and mean D. gallinae percentage mortality at 0.14 mg/cm3 of selected essential oils used in repellence tests with D. gallinae and

toxicity tests with T. molitor. All means are displayed with �standard errors derived from original data. n = 4 for all means.

Essential oil Latin name Origin D. gallinae mortality (%) at 0.14 mg/cm3

Manuka Leptospermum scoparium Forst. New Zealand 100 � 0.00

Thyme Thymus vulgaris L. France 100 � 0.00

Palmarosa Cymbopogon martini Roxb. India 84.30 � 3.67

Caraway Carum carvi L. France 52.86 � 12.18

Spearmint Mentha spicata L. US 20.88 � 7.81

Black pepper Piper nigrum L. India 4.75 � 1.96

Juniper leaf Juniperus communis L. India 2.24 � 4.30

D.R. George et al. / Veterinary Parasitology 162 (2009) 129–134130

acaricides and changes in legislation and productionpractises that will soon see a move away from conven-tional cages (in the EU at least), it is likely that in the futuremany more of the world’s 2.8 billion laying hens (11.7% ofwhich are located in the EU) (Axtell, 1999) will suffer as aresult of D. gallinae infestation if alternatives to syntheticacaricides are not sought.

Several authors have investigated the use of plant-derived products in pest management with reviewsalready available both from an agricultural (Isman, 2000,2006) and veterinary (George et al., 2008) perspective.Furthermore, both Kim et al. (2004, 2007) and George et al.(in press) have investigated the use of plant essential oilsas acaricides for adult D. gallinae with promising results.Numerous essential oils, including cade, clove bud,lavender, pennyroyal, tea tree and thyme, were shownto be relatively highly toxic to D. gallinae in laboratoryscreening tests. Kim et al. (2004, 2007) also conductedexperiments investigating the mode of toxicity of essentialoils to D. gallinae and George et al. (in press) assessed theenvironmental stability of selected essential oils. Plant-derived products may also be of use as attractants (forattract-and-kill schemes and/or pest monitoring purposes)and/or repellents in pest control. For pests of veterinaryimportance, several such products have been identified ashaving pest-repellent properties. For example, the live-stock Brown Ear tick, Rhipicephalus appendiculatus (Neu-man) (a vector of East Coast fever) was repelled just aseffectively by the essential oil of Gynandropsis gyandra (L.)(an African shrub) as by the commercial arthropodrepellent DEET (N,N-diethyl-m-toluamide) (Lwandeet al., 1999). Similarly, research has found dilutedrhododendron oil to exhibit more than 95% repellencyagainst Ixodes ricinus (L.), a tick of both medical andveterinary importance (Jaenson et al., 2005).

Thus it might be possible to develop plant essential oilsas repellents for use in D. gallinae management, especiallyif these products can be shown to display minimal toxicityto non-target organisms. In the confines of a poultry unitthere are likely to be only limited non-target organismsthat could be considered as ‘beneficial’ and thus worthy ofconserving when applying products to control D. gallinae.Such species could include the histerid beetle (Carcinops

pumilio, Erichson) and several predatory mite species(Axtell, 1999). Tenebrio molitor (L.) also occurs frequentlyin poultry systems and though it may not be considered asbeneficial as some other organisms, this beetle maynevertheless play a role in litter decomposition. Therefore,the aims of this study were to evaluate the repellent

properties of plant-derived products to D. gallinae, and toassess the toxicity of these products to a non-targetinvertebrate typical of poultry production systems.

2. Methods

2.1. Selection of plant essential oils

From previous work (George et al., in press) theessential oils of manuka, thyme, palmarosa, caraway,spearmint, black pepper and juniper leaf (from a selectionof 50 essential oils tested) were found to show a range oftoxicities to D. gallinae at a concentration of 0.14 mg oil/cm3 of Petri-dish volume. These seven essential oils wereused in the current work and were obtained from NewDirections (Southampton, UK). Details of these oils andtheir previously determined toxicities (George et al., inpress) are provided in Table 1. All experiments wereconducted at 22 8C, 16:8 L:D cycle in a controlledenvironment growth room at Newcastle University, UK.

2.2. Test organisms

D. gallinae were collected on a weekly basis from acommercial free-range poultry unit in Northumberland,UK and stored in sealed plastic bags in the growth room.Mites were used in tests within 6 days of collection.

T. molitor is one of several species of Coleopteracommonly associated with poultry production. T. molitor

may play a role in waste decomposition and aeration of litterand was selected as a suitable non-target species for testing.Beetles were purchased as medium/large larvae from BladesBiological (Cowden, UK). These were then cultured on a dietof bran and potato slices under growth room conditions.Pupae were removed from this tank as they appeared andstored under the same conditions. Following eclosion, adultbeetles were moved to ‘ageing tanks’ where they werecultured under the same conditions and on the same diet aslarvae until 1–2 weeks old. At this stage adult beetles of bothsexes were used in experiments.

2.3. Repellence to D. gallinae

Four Y-tube olfactometers were assembled. Air waspumped through each arm of the Y-tube of the olfactometerat a rate of 1 L/min. Air passed through a two stage filtrationprocess prior to being humidified by bubbling throughdistilled water. The first filtration stage was achieved bypassing the air through activated carbon and the second

Fig. 1. Layout of an olfactometer. Air flow is depicted with lines and arrows. Key: pump = 1; activated carbon = 2; particulate filter = 3; distilled water = 4;

first Y-tube (to split air stream) = 5. Flasks containing filter papers impregnated with either essential oil (or no essential oil for the control) or no essential

oil = 6. Second Y-tube (containing mites and capped with mesh) = 7. Not to scale.

D.R. George et al. / Veterinary Parasitology 162 (2009) 129–134 131

stage involved passing the air through a particulate filter (in-line PTFE 50 mm diameter 0.2 mm, Fisher Scientific,Leicestershire, UK). Having been humidified, air flow wasdivided equally by a custom made glass Y-tube whichallowed each air stream to then be passed through a 250 mlconical flask (Fisher Scientific). Into one of these flasks19.21 ml of the pure essential oil (or distilled water for thecontrol) was added at an initial concentration of 0.14 mg oil/cm3 of flask volume. Oils where added to flasks on aWhatman No. 2 filter paper (4.25 cm diameter, FisherScientific). Into the other flask distilled water was added atthe same concentration as a control. Air from these flaskswas then passed down opposing arms of a further custommade glass Y-tube, in which mites were confined during theduration of the experiment by securing 0.2 mm mesh overall openings. An overview of this design is shown in Fig. 1. AllY-tubes were of the same design (10 mm internal diameter,two main arms each 100 mm, third arm of 10 mm) and allstages of the apparatus were connected using flexible plastictubing (5 mm internal diameter) coupled to hollow rigidglass rods (4 mm internal diameter) and plastic bungs of therequired size (Fisher Scientific). All glassware exposed toessential oils was acid washed (10% HCl) between successiveruns of the experiment. All plastics exposed to essential oilswere discarded and replaced between runs of the experi-ment, except bungs which were protected by ClingfilmTM

during runs (the Clingfilm was discarded at the end of therun).

For any one run of the experiment, four essential oiltreatments were tested simultaneously, such that two runswere required to test all seven oils and the water control.Eight replicates were undertaken for each treatment insuch a manner that all seven essential oils and the controlwere tested twice in each olfactometer, once in eachopposing arm (to remove any bias), in a randomisedmanner. Approximately 40 adult female D. gallinae wereadded to the Y-tube at time t0 and allowed 15 min to settle.The distribution of mites in the two opposing arms of theY-tube was then recorded at this time (t0 + 15 min) andagain at t0 + 30 min and t0 + 45 min. Following thisassessment, the essential oils were added to the flasksas necessary and the distribution of mites recorded again15, 30 and 45 min later. The same data were then collectedevery 24 h for a period of 13 days. The proportion of D.

gallinae in the untreated arm of the Y-tube of olfactometers

(number in untreated arm/total mites) was calculated foreach essential oil treatment on each sampling occasion.

2.4. Toxicity to T. molitor

The seven essential oils were tested against T. molitor at aconcentration of 0.14 mg/cm3. Four replicates were com-pleted over four runs, with one replicate of each essential oilprocessed per run. Fifteen adult beetles were exposed toeach essential oil in a sealed glass vessel (1400 ml) for 24 h.Each vessel contained a filter paper (Whatman No. 2,110 mm diameter, Fisher Scientific) onto which the neces-sary amount of essential oil had been added in 1 ml ofethanol. Filter papers were dried in a fume cupboard for3 min after treatment with oil/ethanol before being added tovessels to allow the ethanol to evaporate off. Control filterpapers received 1 ml of ethanol only. After 24 h, beetles wereassessed for mortality by observation under magnification(4�) and were considered dead if no movement wasobserved after repeated agitation with an entomological pin.

2.5. Statistical analysis

For the repellence experiment, the proportion of mitesin the untreated arm of the Y-tube of olfactometers wascompared between essential oil treatments for each datacollection time by a one-way analysis of variance (ANOVA)and Tukey’s multiple comparison tests where appropriate(Grafen and Hails, 2002). Data for 15, 30 and 45 min post-essential oil application were squared prior to analysis toimprove the fit of the residuals from the ANOVA to anormal distribution. No other data required transforma-tion to satisfy the assumptions of the test. For data fromtoxicity tests with T. molitor, percentage mortality wascompared between essential oil treatments by a one-wayANOVA with corresponding Tukey’s tests. Data did notrequire transformation prior to analysis. Essential oilswere ranked for their toxicity to D. gallinae from previouswork and their repellence to D. gallinae in the current work.Spearman’s Rank-Order Correlation was then used to lookfor an association between the two. The same analysis wasused to look for any association between the essential oilrank toxicity to D. gallinae from previous work and ranktoxicity to T. molitor in the current work. For the purposesof ranking, an oil was considered repellent to D. gallinae if

Table 2

Mean % repellence (proportional repellence � 100) of essential oils to D. gallinae after different exposure periods. Means are presented from the original

data. n = 8 for all means. Within a row, where data for a given period do not share a common letter, essential oil treatment means were significantly different

(P < 0.05) for that period according to Tukey’s multiple comparison tests. Where data are presented in bold italics, essential oil treatment means were

significantly different from the control treatment (P < 0.05) for that period. P values and corresponding F values are given for the ANOVA of data from each

period.

Essential oil treatment

Control Thyme Manuka Caraway Black pepper Palmarosa Spearmint Juniper leaf F(7,56) P

Minutes pre-treatment 15 50.92 56.48 51.16 49.65 54.55 50.97 56.96 48.01 1.07 0.395

30 53.69ab 54.14ab 55.71a 43.00b 54.04ab 52.04ab 56.54a 52.10ab 2.30 *

45 47.84 51.17 49.88 44.55 54.23 53.43 52.09 49.62 1.09 0.384

Minutes post-treatment 15 49.24b 88.07a 80.26a 87.31a 88.74a 86.87a 89.21a 82.69a 7.74 ***

30 50.86b 90.28a 83.10a 91.11a 90.82a 88.98a 91.71a 84.53a 10.28 ***

45 48.35b 89.80a 84.18a 90.62a 92.05a 89.06a 89.34a 83.99a 12.19 ***

Days post-treatment 1 49.82b 92.00a 82.96a 76.30a 85.18a 88.59a 86.01a 76.64a 8.37 ***

2 48.51b 95.07a 83.38a 77.53a 79.19a 92.01a 90.69a 77.50a 10.22 ***

3 48.83d 96.69a 78.97abc 66.14cd 77.19abc 90.47ab 86.24abc 71.64bcd 9.20 ***

4 47.61c 93.83a 76.21ab 68.07bc 74.09ab 88.54ab 82.21ab 78.36ab 8.95 ***

5 50.89c 90.54a 69.80abc 59.58bc 71.67abc 81.95ab 81.17ab 71.69abc 5.78 ***

6 49.83c 93.78a 65.74bc 62.26bc 60.07bc 79.23ab 77.60ab 63.35bc 6.86 ***

7 52.27d 95.10a 59.63cd 57.39cd 59.12cd 74.30bc 78.40ab 61.91cd 13.12 ***

8 50.73c 90.80a 58.63bc 62.48bc 63.11bc 72.03b 68.69bc 63.80bc 7.82 ***

9 52.68c 87.85a 56.64bc 56.25bc 54.62bc 73.45ab 69.44abc 55.32bc 7.36 ***

10 53.20c 84.92a 50.43c 56.75bc 59.13bc 71.91ab 62.94bc 57.03bc 8.37 ***

11 52.77b 82.23a 48.75b 56.67b 57.56b 60.49b 58.15b 56.68b 7.09 ***

12 52.31b 81.23a 50.88b 53.87b 52.36b 63.07b 56.05b 51.37b 11.51 ***

13 54.64b 77.31a 49.11b 53.41b 54.03b 61.72b 52.22b 49.07b 8.44 ***

* P < 0.05.*** P < 0.001.

D.R. George et al. / Veterinary Parasitology 162 (2009) 129–134132

its use had caused significant repellence of mites, ascompared to the control, for two consecutive samplingperiods. Statistical analyses for this test and the subse-quent experiment were performed using Minitab version14 (Minitab Inc., State College, USA).

3. Results

3.1. Repellence to D. gallinae

Significant differences (P < 0.001) in D. gallinae dis-tribution in olfactometers were observed among treat-

Fig. 2. Toxicity of selected essential oils to T. molitor after 24 h of exposure at 0

original data. n = 4 for all means. Bars with different letters were significantly dif

ments for all data collection times following the addition ofessential oils to the olfactometer apparatus. For the first 2days of observation, all essential oils showed significantrepellence to D. gallinae, as compared to the control(Table 2). Thyme essential oil was the only product toremain significantly repellent to D. gallinae throughout theduration of the 13 day study period (Table 2). During pre-treatment, a significant difference in D. gallinae distribu-tion in the arms of olfactometers was reported on onesampling occasion due to a lower proportion of mites in theolfactometer of the caraway treatment (F(7,56) = 2.30,P < 0.05), as compared to those of two other treatments

.14 mg/cm3. All means are displayed with �standard errors derived from

ferent (P < 0.05) according to Tukey’s multiple comparison tests.

Fig. 3. Association between D. gallinae rank mortality vs. D. gallinae rank

repellence and D. gallinae rank mortality vs. T. molitor rank mortality

when exposed to the seven plant essential oils used.

D.R. George et al. / Veterinary Parasitology 162 (2009) 129–134 133

(Table 2). As comparisons were made between 24 sets ofdata overall, it is likely that this lower-than-expected valuecan be considered to have occurred by chance.

3.2. Toxicity to T. molitor

There was a significant difference in toxicity to T.

molitor between the essential oil treatments(F(7,24) = 69.32, P < 0.001) (Fig. 2). Oils could be dividedinto three distinct categories: namely those that were nomore toxic than the control (palmarosa and manuka),those that were most toxic (juniper leaf, spearmint andcaraway), and those that showed intermediate toxicity(black pepper and thyme) (Fig. 2).

There was a positive association between the toxicityand repellence of essential oils to D. gallinae which was notsignificant (rs = 0.578, P = 0.174) (Fig. 3). The associationbetween toxicity of essential oils to D. gallinae and T.

molitor was negative and not significant (rs = �0.491,P = 0.263) (Fig. 3).

4. Discussion

The aim of this study was to evaluate the repellentproperties of plant-derived products to D. gallinae, and toassess the toxicity of these products to T. molitor, a non-target invertebrate typical of poultry production systems.The current work suggests that whilst all essential oilstested were repellent to some degree, thyme essential oilmay be especially useful in D. gallinae management as itwas found to remain repellent to adult mites for up to 13days.

The seven essential oils that were used in the currentstudy have been reported to show different levels oftoxicity to D. gallinae (George et al., in press). Variation inrepellence of these oils to D. gallinae was observed in thecurrent work. For example, thyme essential oil was themost repellent of the essential oils tested and was also oneof the most highly toxic oils according to previous study,where exposure to thyme essential oil provided 100% mitemortality (George et al., in press). Similarly, juniper leafwas only significantly repellent to D. gallinae up to 4 daysafter application and had previously been identified asbeing relatively non-toxic. Nevertheless, other oils tested

did not conform to this relationship and the associationbetween essential oil toxicity and repellence to mitesoverall was not found to be significant. Manuka, forexample, was also only significantly repellent up to 4 dayspost-application, yet was previously identified as beingequally as toxic to D. gallinae as thyme essential oil (Georgeet al., in press). Such contrasts in the repellency andtoxicity of plant-based products have been reportedelsewhere (Boeke et al., 2004), where it was even foundthat the powder of leaves from the violet tree (Securidacea

longepedunculata, Fresen) displayed toxicity to the cowpeaweevil (Callosobruchus maculatus F.) whilst being attrac-tive. In the present study, no essential oil tested wasattractive to D. gallinae, although as D. gallinae is known tolocate hosts using cues such as carbon dioxide andtemperature gradients that would be able to lead mitesto live birds (Kilpinen, 2005), this was not surprising.

Research has shown that essential oil products work todisrupt binding of invertebrate nerve cord proteins,specifically 3H-octopamine (Enan, 2005). Thus, it couldhave been expected that if the essential oils tested in thepresent study were toxic to T. molitor, this toxicity wouldhave been related to the effect these oils had on D. gallinae

in previous work as shown in Table 1. However, the levelsof mortality achieved with T. molitor were not consistentwith those seen previously for D. gallinae. This suggeststhat there are inter-species differences in the susceptibilityof the test organisms to certain essential oils. Support forinter-specific differences in the susceptibility of inverte-brates to essential oils and their constituents is providedelsewhere in the literature (Isman, 2000) and could beregarded as favourable to the development of theseproducts as repellents for use against D. gallinae. Suchdifferences suggest that essential oils could be selected fordevelopment that, whilst repellent to D. gallinae, wouldhave a minimal effect on non-target organisms if employedas repellents in poultry systems.

It might even be the case that with inter-speciesdifferences in toxicity, certain essential oils could beselected for use as repellents against D. gallinae that notonly conserved populations of beneficials, but also servedto reduce populations of D. gallinae and other pestinvertebrates present in the poultry system. Mites(including species other than D. gallinae), lice, bedbugs,fleas, ticks and various species of Diptera may serve aspests to varying degrees in these systems (Axtell, 1999),and research suggests that certain plant products, includ-ing essential oils and their constituents, can be used aspesticides/repellents for many such species (George et al.,2008). Thyme essential oil, for example, has been identifiedpreviously as being relatively highly toxic to D. gallinae

(George et al., in press) and thymol, its main constituent,was effective against another parasitic mite Psoroptes

cuniculi (Delafond) in work by Perrucci et al. (1995). Thymewas only intermediately toxic to a non-target invertebratein the current work and in addition, thymol is oftenrecommended as an acaricide in bee hives (Calderone et al.,1997; Rice et al., 2002; Floris et al., 2004), furthersuggesting that it is relatively non-toxic to certaininvertebrates. If developed as a D. gallinae repellent, it istherefore possible that thyme essential oil would have a

D.R. George et al. / Veterinary Parasitology 162 (2009) 129–134134

minimal impact on non-target invertebrates, whilstsimultaneously serving as a pesticide for D. gallinae andother poultry pests.

In conclusion, certain plant essential oils such as thymemay be of use as repellents in D. gallinae pest management.Whilst further study will be needed to confirm that anyessential oil can be as effective under field conditions as itis in the laboratory, the results suggest that pursuing thisarea of research may be worthwhile. It is possible that ifcarefully selected and deployed appropriately, certainessential oils would not only act as D. gallinae repellents,but also serve as general pesticides in poultry systemswhilst having a minimal impact on non-target inverte-brates.

Acknowledgements

This work was carried out as part of the MITEeHENproject to develop alternative, plant-based acaricides tocontrol D. gallinae, for which funding from the Departmentfor Environment, Food and Rural Affairs, UK, is gratefullyacknowledged. The authors are also grateful to represen-tatives of the UK poultry industry, including BFREPA, NFUand Noble Foods for providing technical advice on thedevelopment of alternative control strategies for D.

gallinae.

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