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. 2020 Apr 21;147(7):731–739. doi: 10.1017/S0031182020000530

Control of Dermanyssus gallinae (De Geer 1778) and other mites with volatile organic compounds, a review

Marie Gay 1,✉, Laetitia Lempereur 2, Frédéric Francis 1, Rudy Caparros Megido 1
PMCID: PMC10318255  PMID: 32312341

Abstract

Dermanyssus gallinae (De Geer 1778), commonly named the poultry red mite (PRM), is considered to be the most harmful ectoparasite in poultry farms in Europe. This species feeds on the blood of laying hens, but spends most of its time hidden in cracks and crevices around hen nests. To control PRM populations in poultry houses, chemical pesticides are currently used; however, concern is growing regarding the harmful residues found in eggs and hens, along with the increased resistance of mites against several compounds. Alternatives to synthetic compounds are now being explored, including vaccines, biological control, physical control and semiochemical control based on the chemical ecology of PRM. This review focused on the different volatile organic compounds (VOCs) identified from D. gallinae and other mite species that have been discovered to control them. Pheromones (aggregation pheromone, sex pheromone and alarm pheromone) and kairomones promoting attraction behaviour in D. gallinae and other mite species are presented, while VOCs from essential oils and plant extracts with repellent properties are also explored. Finally, devices using VOCs on PRM in the field are described, with devices that have been tested on other Acari species being mentioned as potential directions for the future control of PRM.

Key words: Attractant, chemistry, Dermanyssus gallinae, pheromones, poultry, repellent

Introduction

The poultry red mite (PRM) Dermanyssus gallinae (De Geer 1778) is considered to be the most harmful ectoparasite in poultry farms in Europe (Höglund et al., 1995; Sparagano et al., 2014). Individuals mainly feed on the blood of laying hens and wild birds at night (Kirkwood, 1968), and remain hidden the rest of its time in dark places (e.g. crevices and cracks around hen nests), where they can survive for up to 9 months without feeding (Chauve, 1998; Nordenfors et al., 1999). PRM can also accidentally infest mammals, including horses, dogs and even humans (Ramsay et al., 1975; Mignon and Losson, 2008; George et al., 2015). The occurrence of D. gallinae negatively impacts the general health of hens and the quality of their eggs (i.e. blood marks on the shells of eggs), which leads to significant economic losses in the hen egg laying industry (Chauve, 1998; Kilpinen et al., 2005). In particular, PRM parasitism causes skin irritation, anaemia, vascular problems and, even, the death of the host (Chauve, 1998; Cosoroaba, 2001; Kilpinen et al., 2005).

At present, PRM in egg laying hen units is mainly controlled by using different chemical acaricides. However, the repeated use of chemical acaricides is responsible for the presence of residues in eggs and meat (with a potential impact on Public Health), and is associated with the emergence of PRM resistance to different acaricides, as reported in several European countries (Zeman and Zelezny, 1985; Beugnet et al., 1997; Marangi et al., 2009; Sparagano et al., 2009, 2014). This issue is exacerbated when chemical acaricides are used illegally (off-label), as recently demonstrated in Europe (Flochlay et al., 2017).

In addition, resistance to certain acaricides (such as carbaryl, amitraz and permethrin) has emerged in PRM populations over the last 40 years (Zeman and Zelezny, 1985; Beugnet et al., 1997; Marangi et al., 2009; Sparagano et al., 2009, 2014). Therefore, increasing awareness of the general public and changes to legislation have promoted the search for new and eco-friendly ways to control D. gallinae, including vaccines, entomopathogenic fungi and essential oils. Simultaneously, the chemical ecology of PRM is being increasingly studied to develop control strategies based on pheromonal communication.

Here, an overview of current information is provided, along with potential future directions, in controlling PRM. The different volatile organic compounds (VOCs) currently identified from D. gallinae and other mite species are presented, along with those already used to control them. Specifically, information is presented on (1) pheromones affecting mite behaviour with an attracting effect and (2) the repellent properties of VOCs on PRM. Finally, several devices using VOCs to control D. gallinae in field assays are described, as well as designs tested on other Acari species that could potentially be used on PRM.

Attractive substances

VOCs present an interesting alternative to classical acaricides for controlling acarian populations. Several types of VOCs could be used to manipulate the behaviour of Acari, potentially being integrated in « attract and kill » devices. Here, the potential of several pheromones (Table 1) and kairomones (Table 2) that have already been identified is focused on.

Table 1.

Chemical compounds of pheromones tested for their attractive and repulsive effect on mites

Species Tested substances Experiments Effect References
Acarus immobilis (Griffith 1964) 2-Hydroxy-6-methylbenzaldehyde Filter paper bioassays
Petri dishes experiments		 Attraction Sato et al. (1993)
Aleuroglyphus ovatus (Troupeau 1879) 2-Hydroxy-6-methylbenzaldehyde Filter paper bioassays
Petri dishes experiments		 Attraction Kuwahara et al. (1991)
Caloglyphus sp. (2R,3R)-Epoxyneral Petri dishes experiments Attraction Mori et al. (1996); Mori et al. (1998)
Rosefuran
Caloglyphus polyphyllae (Zakhvatkin 1941) β-Acaridial Petri dishes experiments Attraction Shimizu et al. (2001)
Carpoglyphus lactis (Linneaeus 1767) Lardolure Not described Attraction Kuwahara et al. (1994)
Cosmoglyphus hughesis (Samsinak 1966) 2-Hydroxy-6-methylbenzaldehyde Filter paper bioassays
Petri dishes experiments		 Attraction Ryono et al. (2001)
Dermanyssus gallinae (De Geer 1778) Aggregation pheromone Petri dishes experiments
Y-tube olfactometers
4 arms-olfactometers		 Attraction Entrekin and Oliver (1982); Birkett et al. (2010); Koenraadt and Dicke (2010)
Butyric acid
Decanoic acid
Heptanoic acid
Hexanoic acid
Nonanoic acid
Octanoic acid
Pentanoic acid
Dermatophagoides farinae (Hughes 1961) 2-Hydroxy-6-methylbenzaldehyde Filter paper bioassays
Petri dishes experiments
Y-tube olfactometers		 Attraction Tatami et al. (2001); Skelton et al. (2010)
Neryl formate
Dermatophagoides pteronyssinus (Trouessart 1897) (6Z,9Z)-6,9-heptadecadiene Long-range olfactometers
Y-tube olfactometers		 No effect Skelton et al. (2010); Steidle et al. (2014)
Neral
Neryl formate
Neryl propionate Attraction
Pentadecane
(Z)-8-heptadecene
Lardoglyphus konoi (Sasa and Asanuma 1951) Lardolure Not described Attraction Kuwahara et al. (1994)
Rhizoglyphus robini (Claparède 1869) α-Acaridial Petri dishes experiments Attraction Mizoguchi et al. (2003)
Rhizoglyphus setosus (Manson 1972) S-Isorobinal Petri dishes experiments Attraction Mizoguchi et al. (2005)
Schwiebea elongata (Banks 1906) Neral (low dose) Pasteur pipet experiments Attraction Nishimura et al. (2003)
Neral (high dose) Repulsion
Tetranychus urticae (Koch 1836) Citronellol
Farnesol
Nerolidol		 Petri dishes experiments Attraction Regev and Cone (1975), (1976), (1980)
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Table 2.

Chemical compounds of host kairomones with an attractive effect on mites

Species Tested substances Experiments Effect References
Dermanyssus gallinae (De Geer 1778) 1-Heptadecene Feeding experiments
Field experiments
Y-tube olfactometers		 Attraction Pageat (2005); Harrington et al. (2010); Koenraadt and Dicke (2010); Roy et al. (2018)
9-Octadecene-ol 1 (oleyl alcohol)
Carbone dioxide
Chicken skin extracts
(E)-non-2-enal
Ethyl acetate
Feathers (Aged and Fresh)
Heptadecane
Nonanal
Nonanoïc acid
Oct-1-en-3-ol
Octadecane
Octanal
Macrocheles muscaedomesticae (Scopoli 1972) N-Phenyl-N-glucoside No details available Attraction Carr and Roe (2016)
N-Phenyl-N-mannoside
Phytoseiulus macropilis (Banks 1904) VOC from Tetranychus urticae Y-Tube olfacometers Attraction Amin et al. (2010)
Varroa destructor (Anderson and Trueman 2000) Ethyl palmitate Mite wind tunnel experiments Attraction Calderone and Lin (2001)
Methyl linolenate
Methyl palmitate
Varroa jacobsoni (Oudemans 1904) Ethyl palmitate 4 arms-olfactometers Attraction Le Conte et al. (1989)
Methyl linolenate
Methyl palmitate
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Pheromones

Pheromones are molecules that are emitted by an individual of a species to influence the behaviour of another individual of the same species (Pageat, 2005). Several pheromones are considered to attract mites, including aggregation pheromones, immature female pheromones, female sex pheromones and, at low doses, alarm pheromones (Sonenshine, 1985; Carr and Roe, 2016). To identify the molecules present in the pheromonal mix released by a species, static headspace analyses (e.g. solid phase micro extraction or SPME) (Birkett et al., 2010; Steidle et al., 2014) and dynamic headspace analyses (e.g. thermodesorption) (Chen et al., 2019; Makarow et al., 2019) are performed. While dynamic headspace analysis has not yet been performed on mites, to our knowledge, it could prove useful, because it allows small amounts of volatile molecules to be detected and quantified (Pfannkoch and Whitecavage, 2000; Zhang and Li, 2010). The sampling technique must be coupled to gas chromatography-mass spectrometry (GC-MS) analysis to identify the different compounds (Zhang and Li, 2010). Following the identification and quantification of molecules within the pheromonal mix, behavioural tests could be performed, including Y-tube olfactometers bioassays or filter paper contact bioassays, to characterize the behaviour of mites when they are confronted with all or a part of the identified molecules (Entrekin and Oliver, 1982; Steidle et al., 2014).

Aggregation pheromones

The aggregation pheromones of mites cause non-feeding conspecific mites (male and female) of different developmental stages to aggregate in a safe environment (Carr and Roe, 2016). The aggregation behaviour in PRM was well studied before the aggregation pheromone was identified. Entrekin and Oliver (1982) studied two possible causes for this behaviour: thigmokinesis (i.e. increased locomotion in response to changes in contact with the immediate physical environment) and the release of an aggregation pheromone. Both stimuli impact the clustering of mites; however, the chemical ones form aggregates more efficiently. The aggregation phenomenon due to the perception of potential aggregation pheromones by PRM was evaluated by Koenraadt and Dicke (2010). The authors tested the attraction of two groups of conspecific mites (fed and unfed) by performing behavioural experiments. The authors showed that fed and unfed mites were attracted by volatiles emitted by fed conspecifics. This finding was consistent with a previous study showing that the aggregation of mites increases after feeding (Entrekin and Oliver, 1982). Koenraadt and Dicke (2010) proposed that unfed mites are motivated to find a host to feed, while fed ones were searching for a place to hide and reproduce after their blood meal.

Subsequently, Birkett et al. (2010) conducted SPME-GC analysis on fed adult PRM, and identified eight molecules, including seven carboxylic acids (including hexanoic acid and dodecanoic acid) and one aldehyde (an octanal) that could be components of the pheromonal mix driving aggregation-forming behaviour in PRM. Behavioural experiments confirmed the attractive effect of each compound, as well as a synergic effect when compounds are associated. It was concluded that the eight compounds attract PRM and could be applied simultaneously, separately or sequentially to each other (Birkett et al., 2010). It is possible that the aggregation pheromone of PRM is composed of only one or several molecules, as observed in other mite species. For example, Lardolure is the only aggregation pheromone that has been identified in Caloglyphus polyphyllae1 and Lardoglyphus konoi mites (Kuwahara et al., 1994; Carr and Roe, 2016). In comparison, the aggregation pheromone of the European House Dust Mite (EHDM) Dermatophagoides pteronyssinus is mostly composed of neryl propionate, pentadecane and neryl formate (Skelton et al., 2010; Steidle et al., 2014). Finally, neryl formate might be a component of the pheromonal mix of several different species, as it was identified as a major compound of the aggregation pheromone in the American House Dust Mite, Dermatophagoides farinae and EHDM (Skelton et al., 2010).

Alarm pheromones

Alarm pheromones are emitted by an individual that has been stressed by an unsafe environment or that has been injured through direct contact (Carr and Roe, 2016). Detection of low concentrations of alarm pheromones causes attraction and clustering behaviour in mites, as part of group survival strategies (i.e. formation of a ‘safety net’). Above a given concentration, the pheromone becomes repulsive, which causes the strategies of individuals changing (i.e. scattering and hiding) (Carr and Roe, 2016). To date, the alarm behaviour or the possible emission of this pheromone has not been studied in PRM; however, several compounds of this pheromone have been identified in other species of Astigmatid mites, including neryl formate and neral (Kuwahara, 2010, 2011; Carr and Roe, 2016). When neral is applied in low doses (1 and 3 ng) on filter paper, mites (Schwiebea elongata) are attracted to this compound; however, at higher doses (30 ng), they exhibited repulsive behaviour (Nishimura et al., 2003; Carr and Roe, 2016). Neryl formate was identified as an alarm pheromone for several species, including Tyrophagus putrescentiae (Schrank 1781), leading to alarm behaviour (Kuwahara, 2010); however, it attracts also other species, such as D. farinae and D. pteronyssinus at high doses (10 and 100 ng), and is considered to be an aggregation pheromone (Skelton et al., 2010). Therefore, it is essential to clearly differentiate alarm pheromones that attract mites at low doses from aggregation pheromone that attract mites at all doses. Studies on the PRM alarm behaviour or the potential alarm pheromone emission have yet to be conducted, which could represent an interesting future direction for research.

Sex pheromones

Two types of sex pheromones have been detected in mites: (1) immature female pheromones, also known as arrestant sex pheromones and (2) female sex pheromones (Sonenshine, 1985; Carr and Roe, 2016). There is a competition between male mites to reproduce with conspecific females. Consequently, males might detect differences between a deutonymph (i.e. second nymphal stage) from a protonymph (i.e first nymphal stage) by using the immature pheromone signature emitted by deutonymph females, which is composed of citronellol, farnesol and nerolidol in Tetranychus urticae females (Regev and Cone, 1975, 1976, 1980). Following the discovery of a deutonymph female, males exhibit guarding behaviour (i.e. association of a male with a deutonymph female) in some acarian species [e.g. Hericia sp. (Canestrini 1888) or Tetranychus kanzawai (Kishida 1927)], until the deutonymph becomes an adult female (Sonenshine, 1985; Witaliński et al., 1992; Yasui, 1992; Fashing, 2003; Oku, 2009; Carr and Roe, 2016). Colloff (2009), cited by Carr and Roe (2016), highlighted that only deutonymphs are able to emit the immature female pheromone. Nevertheless, this pheromone has not been identified in D. gallinae so far.

The female sex pheromone is normally released by fed mature females to attract preferably fed males, as the two sexes have a high reproductive success status (Sonenshine, 1985; Carr and Roe, 2016). The female sex pheromone might also be released by males, explaining the mounting behaviour between males that is sometimes observed (Mori and Kuwahara, 2000; Mizoguchi et al., 2005; Carr and Roe, 2016). Again, the female sex pheromone was not studied in D. gallinae, but different compounds have been identified as female sex pheromones in mites (Table 1).

PRM is part of the Acari. The molecules identified in closely related species could be potential candidates for characterizing the sex pheromones of PRM, especially as some compounds are already shared by different species, including 2-hydroxy-6-methylbenzaldehyde in Acarus immobilis, Aleuroglyphus ovatus, Cosmoglyphus hughesi and D. farinae (Kuwahara et al., 1991; Sato et al., 1993; Ryono et al., 2001; Tatami et al., 2001).

Sexual chemical communication between mites has been extensively investigated in several species, but not in PRM. Thus, it would be interesting to fill this knowledge gap on chemical communication in PRM. The potential synergic effects between the sex pheromone and aggregation pheromone could potentially be identified, which could be used to control PRM.

Host kairomones

Kairomones are molecules emitted by individuals mediating interspecific interactions that are generally harmful to the emitters (Pageat, 2005). This section addresses kairomones that are attractive to some mites, including D. gallinae (Table 2). PRM aim to localize potential hosts to feed. The uropygial gland products of chicken might have potential kairomones in the host location process (Pageat, 2005; Koenraadt and Dicke, 2010). The identification of some of the compounds released by these products revealed the presence of alcools, alcanes and alcenes (described in Table 2). However, these compounds were directly identified from the chicken gland, and it was not confirmed that these compounds are volatiles that could be detected over a distance, as in olfactometer experiments (Roy et al., 2018). Following behavioural experiments in olfactometers, Koenraadt and Dicke (2010) observed that aged feathers of chicken (found on the floor of poultry houses and with potential microbial activity) were more attractive to PRM than fresh feathers (feathers cut from live hens). Mites responded to small numbers of feathers (10 feathers in a 2.5 L glass jar), indicating that they can detect very low amounts of these kairomones; however, no precise measurement was made (Koenraadt and Dicke, 2010). Carbon dioxide (CO2) can also be considered as a kairomone for PRM. A gradual increase to CO2 levels induces host-seeking behaviour in mites, whereas a quick increase induces mites to freeze. This attitude is probably linked to the potential presence of predators (Kilpinen, 2005). Finally, temperature is a powerful stimulus that activates mites and, coupled with vibrations, might contribute to host detection and localization (Kilpinen, 2001, 2005).

Following host localization, PRM are attracted by several kairomones produced by the host (Roy et al., 2018). Several compounds were identified from living hens by SPME, followed by GC/MS analyses. Their attracting effect to PRM was confirmed with tube olfactometer experiments. A synergic effect of four molecules characterizing gallinaceous bird scent [(E)-non-2-enal, nonanoic acid, octanal and oct-1-en-3-ol] was highlighted by olfactometry (Roy et al., 2018). More generally, the attracting capacity of VOCs from the skin and feather extracts of hens (composition not available in the paper) was identified in a study where it was necessary to attract PRM to feed on synthetic membranes (Harrington et al., 2010). However, it is not clear whether these molecules are involved in attracting D. gallinae to the host (i.e. detection of skin VOCs) or whether they serve as are contact cues for skin recognition. Several studies have investigated kairomones produced by hens; however, knowledge remains limited about the potential attracting role of VOCs in the environment of hens, with future studies being required on this subject.

Few studies have investigated the kairomones of other mite species. The methodology exploited with other species is similar to that used with PRM. After analysing the body extracts of male and female adult houseflies Musca domestica and after feeding experiments, N-phenyl-N-glucoside and N-phenyl-N-mannoside were identified as two kairomones that attracted the phoretic mite, Macrocheles muscaedomesticae (Wicht et al., 1971; Achiano and Giliomee, 2006 cited in ref of the review of Carr and Roe, 2015). In addition, female predator mites Phytoseiulus macropilis were attracted by unidentified kairomones from T. urticae in Y-tube olfactometer experiments (Amin et al., 2010). However, three kairomones (methyl palmitate, ethyl palmitate and methyl linolenate) were identified in Varroa jacobsoni and Varroa destructor, which are two species of honey bees parasites, following behavioural experiments with four-armed olfactometers and mite wind tunnels (Le Conte et al., 1989; Calderone and Lin, 2001). The use of a wind tunnel allows the long-range effect of different compounds to be tested. The use of this methodology on PRM could extend current knowledge on the potential attracting properties of pheromones and kairomones.

Repulsive substances

Olfactive repellents can be divided into two categories: (1) true repellents (also called expellents) or spatial repellents, and (2) odour masking compounds (or attraction inhibitors) (Deletre et al., 2016). A true repellent induces a shift in orientation from an odour source without direct contact. In comparison, odour masking compounds induce the attractiveness of the host to decline, or difficulties to localize the host using odour cues (Deletre et al., 2016).

Several experiments were conducted to test the repellent properties of substances studied on PRM, including contact experiments (i.e. Petri dishes with filter paper saturated with the compound) and olfactive experiments using olfactometers (Nechita et al., 2015; Masoumi et al., 2016). Globally, it is interesting to evaluate the repellent effect of a substance to: (1) test a potential negative repellent effect of a toxic substance (e.g. acaricide) (Lundh et al., 2005) and (2) confirm the repulsive effect of a substance that could be used as a pure repellent (Nechita et al., 2015). The different compounds tested on PRM are summarized in Table 3, showing the level of repulsive effect.

Table 3.

Chemical compounds with a high repellent effect on D. gallinae

Tested substances Species Experiments Effect References
2-Methoxycinnamaldehyde Dermanyssus gallinae Y-tube olfactometers High repellent effect Lee et al. (2019)
α-Thujone-rich Artemisia sieberi Besser essential oil Y-tube olfactometers Tabari et al. (2017)
β-Caryophyllene Y-tube olfactometers Lee et al. (2019)
Carvacrol Y-tube olfactometers Barimani et al. (2016); Masoumi et al. (2016)
Cinnamaldehyde Y-tube olfactometers Lee et al. (2019)
Cinnemon bark oil Y-tube olfactometers Lee et al. (2019)
Clove bud oil Y-tube olfactometers Lee et al. (2019)
Coumarin Y-tube olfactometers Lee et al. (2019)
Cnidium officinale Makino methanolic extract Y-tube olfactometers
Fumigation bioassays
Contact bioassays
Spray bioassays		 Kim et al. (2018)
Conocarpus erectus L. extract Filter paper bioassays Rajabpour et al. (2018)
Lavender oil Filter paper contact bioassays
Pasteur pipette bioassays		 Nechita et al. (2015)
Myrcia oblongata DC. leaves oil 10% Y-tube olfactometers
Fumigation bioassays		 Santana et al. (2018)
Neem oil Field assays
Cardboard traps
Filter paper in Petri dishes bioassays		 Lundh et al. (2005); Camarda et al. (2018)
Thyme oil Petri dishes bioassays
Y-tube olfactometers
Filter paper contact bioassays
Pasteur pipette bioassays		 George et al. (2009); Nechita et al. (2015); Masoumi et al. (2016); Pritchard et al. (2016)
(Z)-ligustilide Y-tube olfactometers
Fumigation bioassays
Contact bioassays
Spray bioassays		 Kim et al. (2018)
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Essential oils

The repulsive and/or acaricidal efficiency of essential oils has been extensively studied. For instance, Lundh et al. (2005) showed that neem oil, Azadirachta indica (Jussieu) (concentrations of 15 to 20%), has a good acaricide effect associated with a low repellent effect under laboratory conditions. In another study, Camarda et al. (2018) tested the effectiveness of this oil under field conditions. The authors showed that a 20% neem oil formulation (RP03TM) caused the mite population in poultry farms to decline by 94.65 to 99.80% after three nebulizations of the product over one week (Camarda et al., 2018). Other essential oils are also effective, particularly essential oils from the family of Lamiaceae (Martinov) such as Origanum (L.), Satureja (L.), Thymbra (L.) and Thymus (L.) species. These species are characterized by a major compound, carvacrol, which is a good acaricide candidate with a toxic effect on D. gallinae. It has no repellent effect at 1% concentration; however, above this concentration, repellence occurs (Kirimer et al., 1995; Barimani et al., 2016).

Out of several essential oils tested for their pure repellent properties during in vitro contact bioassays, thyme and lavender oils had the highest repellent activity with, respectively, 80 and 40% of the oil-treated surface area being avoided by PRM (Nechita et al., 2015; Pritchard et al., 2016). Nevertheless, in this type of experiment, it is not possible to distinguish whether mites are repelled by olfactory or contact cues, with complementary studies in olfactometers being required (Deletre et al., 2016). The association of thymol (i.e. the major compound of thyme essential oil) and carvacrol was evaluated in olfactometer bioassays for potential synergic repellent effects (Masoumi et al., 2016). The study, unfortunately, revealed that the addition of thymol to carvacrol decreased the repellent effect of carvacrol. Other studies analysed the different compounds present in a given essential oil by GC-MS experiments, and tested the repellent effect of the oil on PRM by Y-tube olfactometer experiments (Tabari et al., 2017; Santana et al., 2018). The essential oil of Artemisia sieberi (Besser) [rich in α-thujone (31.5%), β-thujone (11.92%), camphor (12.3%) and 1,8-cineole (10.09%)] and the essential oil of Myrcia oblongata (DC) [rich in caryophyllene oxide (22.03%) and trans-verbenol (11.94%)] showed a significative repellent effect to D. gallinae. Nevertheless, the effect of each of their constituent compounds was not evaluated (Tabari et al., 2017; Santana et al., 2018). Finally, a study by Lee et al. (2019) obtained interesting results, in which two essential oils (cinnamon bark and clove bud oils) and some of their constitutive compounds were tested for their repellent abilities. The two oils and their compounds were repellent to PRM, except for cinnamyl acetate from cinnamon bark oil, and for two compounds from clove bud oil (eugenol and eugenol acetate), which even showed an attractant effect, following 120 min of application. The concentration of the active compound over time might be an issue, as many essential oils exhibit high repellent activity against D. gallinae over the short-term due to their high volatility (George et al., 2008, 2009). A dose effect exists for several molecules, including thyme oil, which could be used as a repellent or as an acaricide, depending on the concentration. When used as an acaricide, essential oils have a short-term effect; however, it is possible to couple them with other biological control methods, such as entomopathogenic fungus. When these two methods are coupled, the short-term acaricide effect of essential oils is complemented with the delayed, but long-term effect, of the fungus. For example, an entomopathogenic fungus [Beauveria bassiana (Balsamo-Crivelli) Vuillemin] in combination with essential oils [Eucalyptus globulus (La Billardière), Eucalyptus citriodora (Hook), Thymus vulgaris (Linné), and Eugenia caryophyllata (Thunb.)] was tested to create a new way to control D. gallinae (Immediato et al., 2016). Following toxicity tests, it was found that the combination of B. bassiana and E. globulus at 0.2% might be the best combination for an acaricide effect against D. gallinae.

Plant extracts

Most studies on plant extracts have focused on the acaricide properties of the extracts, and are not evaluated in this review, because repellent properties are not discussed. Only two studies evaluated the repellent properties of two plant extracts. Rajabpour et al. (2018) showed that aquatic and ethanolic extracts of Conocarpus erectus are repellent for PRM using contact experiments. Nevertheless, the repellent effect described here was unclear, as it was not possible to distinguish the contact and olfactive repellent effects. In another study, the acaricidal and repellent activities of a methanolic extract and fractions from the rhizome of Cnidium officinale were tested to control D. gallinae (Kim et al., 2018). Kim et al. (2018) showed that the methanolic extract of C. officinale has a 91.3% repellent activity on PRM, while (Z)-ligustilide, which is an isolated compound from C. officinale roots, showed a repellent response rate equal to 100% using a T-tube olfactometer.

Application of VOCs in field assays

Here, current applications of VOCs to control PRM are described along with potential other strategies from other Acari species relevant for PRM control. The introduction of repulsive substances to hen feed could make the emission of repellent VOCs against the PRM possible (El Adouzi et al., 2019). For instance, Nor-Mite® (mostly composed of >2% eugenol) was added to hen feed, and the VOCs emitted by hens were analysed. GC-MS analysis showed that Nor-Mite® fed hens released several VOCs, including eugenol. Following olfactometer experiments, the repellent effect of eugenol and other VOCs from Nor-Mite® fed hens was confirmed. In addition, the authors suggested that other molecules present in Nor-Mite®, such as trans-caryophyllene and geraniol, might contribute to this repellent effect, with possible additive/synergic effects (not tested in this paper) (El Adouzi et al., 2019).

Several devices have been tested to control other Acari species. For example, one design using attracting VOCs is an ‘attract and kill’ trap has been applied to others species of Acari. A system based on the encapsulation of an attracting pheromone coupled to an acaricide was developed for the brown dog tick Rhipicephalus sanguineus (Latreille 1806) by Dhivya et al. (2014). The capsule was made of a natural polymer (i.e. chitosan). The species assembly pheromone was chosen as an attractant, and was coupled with deltamethrin as acaricide. Laboratory and field tests showed a reduction of infestation, as the ticks were discovered dead around the traps. Another study using aggregation-attachment pheromone together with deltamethrin to attract and kill Amblyomma variegatum (Fabricius 1794) (the tropical bont tick) demonstrated an overall tick control efficiency of 92% (Kelly et al., 2014). Similar studies could be conducted for D. gallinae by coupling the aggregation pheromone with a natural acaricide (e.g. an essential oil) or entomopathogenic fungi.

Conclusions

PRM is a world economic problem for the poultry industry, and the development of solutions with low risk on human health should be promoted to control their populations, especially in hen egg laying farms. The development of sustainable pest control based on an understanding of chemical ecology is being increasingly implemented, and should be applied to PRM. New insights on pheromonal communication of PRM are fundamental to create efficient control strategies.

Knowledge remains more limited about chemical communication in mites including PRM compared to ticks, mainly due to their smaller size and, consequently, the lower emission of VOCs. In the last decade, the identification of attractants in mites has increased, along with more information on their associated effects on mite behaviour. Nevertheless, a large knowledge gap exists on VOCs that attract PRM that should be addressed in the future.

The lack of knowledge, especially on PRM pheromones, could be explained by the difficulties encountered to maintain an artificial breeding of PRM (Kirkwood, 1971; Zeman, 1988; Bruneau et al., 2001; Harrington et al., 2010). This hurdle prevents the availability of fed mites reducing the implementation of pheromones studies. For the development of further PRM pheromone studies, an efficient artificial or semi-artificial breeding system must be developed to facilitate the supply of fed individual as well as to allow a control of several parameters (e.g. time since the last meal, female fertilization or not etc…). Among the current possible alternative, the use of a semi-artificial laboratory breeding on alive chicken (i.e. a plastic bag filled with PRM in contact with the chicken) seems to be a promising solution as it provides a high number of individuals in a short period of time (Nunn et al., 2019).

Concerning PRM's kairomones, several studies are currently available with no assays of these molecules in field conditions (Pageat, 2005; Koenraadt and Dicke, 2010; Roy et al., 2018). Different implementations are still to be needed to consider these molecules as an efficient field attractant such as the emission source apposition or the concentration of the synthetic molecule. Moreover, the interference of kairomones from hosts when synthesized kairomones are applied in layer farms would be difficult to avoid and should decrease the efficacy of the product.

In contrast to the limited number of studies on attracting VOCs, many studies exist on repulsive VOCs to PRM. This phenomenon might be explained by the fact that repelling PRM outside poultry farms is the first solution that comes to mind in terms of control strategies. Essential oils and plant extracts seem to represent promising repellents, despite their short-term efficiency. Several designs using VOCs on PRM have been elaborated and tested under field conditions. Further studies are needed to optimize these strategies, or to create new ones based on ‘attract and kill’ or ‘push-pull’ principles.

Finally, although mites and ticks are two separated groups in the Acari taxon, similarities exist in how they communicate. Therefore, researchers investigating the chemical communication of mites should refer to studies on chemical communication in ticks, for which there is extensive published literature.

Financial support

This work was supported by the Federal Public Service, Health, Food chain safety and Environment (grant number RF18/6325)

Ethical standards

Not applicable.

Footnotes

1

All complete species names could be found in Table 1.

Conflict of interest

None.

References

  1. Achiano KA and Giliomee JH (2006) Feeding behaviour of the potential predators of the house flies, Musca domestica L. and Fannia canicularis (L.) (Diptera: Muscidae). African Entomology 14, 69–75. [Google Scholar]
  2. Amin MM, Mizell RF and Flowers RW (2010) Response of the predatory mite Phytoseiulus macropilis (Acari: Phytoseiidae) to pesticides and kairomones of three spider mite species (Acari: Tetranychidae), and non-prey food. Florida Entomologist 92, 554–562. [Google Scholar]
  3. Barimani A, Youssefi MR and Tabari MA (2016) Traps containing carvacrol, a biological approach for the control of Dermanyssus gallinae. Parasitology Research 115, 3493–3498. [DOI] [PubMed] [Google Scholar]
  4. Beugnet F, Chauve C, Gauthey M and Beert L (1997) Resistance of the red poultry mite to pyrethroids in France. Veterinary Record 140, 577–579. [DOI] [PubMed] [Google Scholar]
  5. Birkett M, Pickett J, Dewhirst S, Jespersen JB and Kilpinen OO (2010) Use of a carboxylic acid or an aldehyde. Patent WO 2010/130990 A2, 1–23.
  6. Bruneau A, Dernburg A, Chauve C and Zenner L (2001) First in vitro cycle of the chicken mite. Dermanyssus gallinae (De Geer 1778), utilizing an artificial feeding device. Parasitology 123, 583–589. [DOI] [PubMed] [Google Scholar]
  7. Calderone NW and Lin S (2001) Behavioural responses of Varroa destructor (Acari: Varroidae) to extracts of larvae, cocoons and brood food of workers and drone honey bees, Apis mellifera (Hymenoptera: Apidae). Physiological Entomology 26, 341–350. [Google Scholar]
  8. Camarda A, Pugliese N, Bevilacqua A, Circella E, Gradoni L, George D, Sparagano O and Giangaspero A (2018) Efficacy of a novel neem oil formulation (RP03TM) to control the poultry red mite Dermanyssus gallinae. Medical and Veterinary Entomology 32, 290–297. [DOI] [PubMed] [Google Scholar]
  9. Carr AL and Roe M (2016) Acarine attractants: Chemoreception, bioassay, chemistry and control. Pesticide Biochemistry and Physiology 131, 60–79. 10.1016/j.pestbp.2015.12.009 [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chauve C (1998) The poultry red mite Dermanyssus gallinae (De Geer, 1778): current situation and future prospects for control. Veterinary Parasitology 79, 239–245. [DOI] [PubMed] [Google Scholar]
  11. Chen Y, Martin C, Fingu Mabola JC, Verheggen F, Wang Z, He K and Francis F (2019) Effects of host plants reared under elevated CO2 concentrations on the foraging behavior of different stages of corn leaf aphids Rhopalosiphum maidis. Insects 10, 1–11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Collof M (2009) Dust mites. Melbourne: CSIRO Publishing. [Google Scholar]
  13. Cosoroaba I (2001) Massive Dermanyssus gallinae invasion in battery-husbandry raised fowls. Revue de médecine vétérinaire 152, 89–96. [Google Scholar]
  14. Deletre E, Schatz B, Bourguet D, Chandre F, Williams L, Ratnadass A and Martin T (2016) Prospects for repellent in pest control: current developments and future challenges. Chemoecology 26, 127–142. [Google Scholar]
  15. Dhivya B, Latha BR, Raja MD, Sreekumar C and Leela V (2014) Control of brown dog tick, Rhipicephalus sanguineus using assembly pheromone encapsulated in natural polymer, chitosan. Experimental and Applied Acarology 63, 85–92. [DOI] [PubMed] [Google Scholar]
  16. El Adouzi M, Arriaga A, Dormont L, Nicolas B, Labalette A, Lapeyre B, Bonato O and and Roy L (2019) Modulation of feed composition is able to make hens less attractive to the poultry red mite Dermanyssus gallinae. Parasitology 147(2), 171–181. doi: 10.1017/S0031182019001379 [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Entrekin DL and Oliver JH (1982) Aggregation of the chicken mite, Dermanyssus gallinae (Acari: Dermanyssidae). Journal of Medical Entomology 19, 671–678. [DOI] [PubMed] [Google Scholar]
  18. Fashing NJ (2003) Morphological adaptations associated with mate-guarding behavior in the genus Hericia (Acari: Algophagidae). In Halliday RB, Walter DE, Proctor HC, Norton RA and Collof MJ (eds), Acarology: Proceedings of the 10th International Congress. Melbourne: CSIRO publishing, pp. 176–179. [Google Scholar]
  19. Flochlay AS, Thomas E and Sparagano O (2017) Poultry red mite (Dermanyssus gallinae) infestation: a broad impact parasitological disease that still remains a significant challenge for the egg-laying industry in Europe. Parasites & Vectors 10, 357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. George DR, Callaghan K, Guy JH and Sparagano OAE (2008) Lack of prolonged activity of lavender essential oils as acaricides against the poultry red mite (Dermanyssus gallinae) under laboratory conditions. Research in Veterinary Science 85, 540–542. [DOI] [PubMed] [Google Scholar]
  21. George DR, Shiel RS, Sparagano OAE, Port G, Guy JH and Okello E (2009) Repellence of plant essential oils to Dermanyssus gallinae and toxicity to the non-target invertebrate Tenebrio molitor. Veterinary Parasitology 162, 129–134. [DOI] [PubMed] [Google Scholar]
  22. George DR, Finn RD, Graham KM, Mul MF, Maurer V, Moro CV and Sparagano OA (2015) Should the poultry red mite Dermanyssus gallinae be of wider concern for veterinary and medical science? Parasites and Vectors 8, 1–10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Harrington DWJ, Guy JH, Robinson K and Sparagano OAE (2010) Comparison of synthetic membranes in the development of an in vitro feeding system for Dermanyssus gallinae. Bulletin of Entomological Research 100, 127–132. [DOI] [PubMed] [Google Scholar]
  24. Höglund J, Nordenfors H and Uggla A (1995) Prevalence of the poultry red mite, Dermanyssus gallinae, in different types of production systems for egg layers in Sweden. Poultry science 74, 1793–1798. [DOI] [PubMed] [Google Scholar]
  25. Immediato D, Figueredo LA, Iatta R, Camarda A, de Luna RLN, Giangaspero A, Brandão-Filho SP, Otranto D and Cafarchia C (2016) Essential oils and Beauveria bassiana against Dermanyssus gallinae (Acari: Dermanyssidae): towards new natural acaricides. Veterinary Parasitology 229, 159–165. [DOI] [PubMed] [Google Scholar]
  26. Kelly PJ, Lucas HM, Randolph CM, Ackerson K, Blackburn JK and Dark MJ (2014) Efficacy of slow-release tags impregnated with aggregation-attachment pheromone and deltamethrin for control of Amblyomma variegatum on St. Kitts. West Indies. Parasites and Vectors 7, 182. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kilpinen O (2001) Activation of the poultry red mite, Dermanyssus gallinae (Acari: Dermanyssidae), by increasing temperatures. Experimental and Applied Acarology 25, 859–867. [DOI] [PubMed] [Google Scholar]
  28. Kilpinen O (2005) How to obtain a bloodmeal without being eaten by a host: the case of poultry red mite, Dermanyssus gallinae. Physiological Entomology 30, 232–240. [Google Scholar]
  29. Kilpinen O, Roepstorff A, Permin A, Nørgaard-Nielsen G, Lawson LG and Simonsen HB (2005) Influence of Dermanyssus gallinae and Ascaridia galli infections on behaviour and health of laying hens (Gallus gallus domesticus). British Poultry Science 46, 26–34. [DOI] [PubMed] [Google Scholar]
  30. Kim HK, Lee SJ, Hwang BY, Yoon JU and Kim GH (2018) Acaricidal and repellent effects of Cnidium officinale-derived material against Dermanyssus gallinae (Acari: Dermanyssidae). Experimental and Applied Acarology 74, 403–414. [DOI] [PubMed] [Google Scholar]
  31. Kirimer N, Başer KHC and Tümen G (1995) Carvacrol-rich plants in Turkey. Chemistry of Natural Compounds 31, 37–41. [Google Scholar]
  32. Kirkwood A (1968) Some observations on the feeding habits of the poultry mites Dermanyssus gallinae and Liponyssus sylviarum. Entomologia Experimentalis et Applicata 11, 315–320. [Google Scholar]
  33. Kirkwood A (1971) In vitro feeding of Dermanyssus gallinae. Experimental Parasitology 29, 1–6. [DOI] [PubMed] [Google Scholar]
  34. Koenraadt CJM and Dicke M (2010) The role of volatiles in aggregation and host-seeking of the haematophagous poultry red mite Dermanyssus gallinae (Acari: Dermanyssidae). Experimental and Applied Acarology 50, 191–199. [DOI] [PubMed] [Google Scholar]
  35. Kuwahara Y (2010) How astigmatic mites control the emission of two or even three types of pheromones from the same gland. In Trends in Acarology: Proceedings of the 12th International Congress, pp. 241–247. doi: 10.1007/978-90-481-9837-5_39. [DOI]
  36. Kuwahara Y (2011) Chemical ecology of astigmatid mites. Journal of the agricultural chemical society of Japan 64, 1754–1757. [Google Scholar]
  37. Kuwahara Y, Sato M, Koshii T and Suzuki T (1991) Chemical ecology of astigmatid mites XXXII. 2-Hydroxy-6-methyl-benzaldehyde, the sex pheromone of the brown-legged grain mite Aleuroglyphus ovatus (TROUPEAU) (Acarina: Acaridae). Applied Entomology and Zoology 27, 253–260. [Google Scholar]
  38. Kuwahara Y, Asami N, Morr M, Matsuyama S and Suzuki T (1994) Chemical ecology of astigmatid mites XXXVIII aggregation pheromone and kairomone activity of lardolure and its analogues against Lardoglyphus konoi and Carpoglyphus lactis. Applied Entomology and Zoology 29, 253–257. [Google Scholar]
  39. Le Conte Y, Arnold G, Trouiller J, Masson C, Chappe B and Ourisson G (1989) Attraction of the parasitic mite Varroa To the drone larvae of honey bees by simple aliphatic esters. Science (New York, N.Y.) 245, 638–639. [DOI] [PubMed] [Google Scholar]
  40. Lee SJ, Kim HK and Kim GH (2019) Toxicity and effects of essential oils and their components on Dermanyssus gallinae (Acari: Dermanyssidae). Experimental and Applied Acarology 78, 65–78. [DOI] [PubMed] [Google Scholar]
  41. Lundh J, Wiktelius D and Chirico J (2005) Azadirachtin-impregnated traps for the control of Dermanyssus gallinae. Veterinary Parasitology 130, 337–342. [DOI] [PubMed] [Google Scholar]
  42. Makarow R, Schäfer S, Albrecht S, Robert S, Schütz S and Kaul P (2019) Investigation of volatile organic compounds emitted by Anoplophora glabripennis (Moschulsky) using thermal desorption and gas chromatography-mass spectrometry. Microchemical Journal 146, 142–148. [Google Scholar]
  43. Marangi M, Cafiero MA, Capelli G, Camarda A, Sparagano OAE and Giangaspero A (2009) Evaluation of the poultry red mite, Dermanyssus gallinae (Acari: Dermanyssidae) susceptibility to some acaricides in field populations from Italy. Experimental and Applied Acarology 48, 11–18. [DOI] [PubMed] [Google Scholar]
  44. Masoumi F, Youssefi MR and Tabari MA (2016) Combination of carvacrol and thymol against the poultry red mite (Dermanyssus gallinae). Parasitology Research 115, 4239–4243. [DOI] [PubMed] [Google Scholar]
  45. Mignon B and Losson B (2008) Dermatitis in a horse associated with the poultry mite (Dermanyssus gallinae). Veterinary Dermatology 19, 38–43. [DOI] [PubMed] [Google Scholar]
  46. Mizoguchi A, Mori N, Nishida R and Kuwahara Y (2003) α-acaridial a female sex pheromone from an alarm pheromone emitting mite Rhizoglyphus robini. Journal of Chemical Ecology 29(7), 1681–1690. 10.1023/A:1024235100289 [DOI] [PubMed] [Google Scholar]
  47. Mizoguchi A, Murakami K, Shimizu N, Mori N, Nishida R and Kuwahara Y (2005) S-isorobinal as the female sex pheromone from an alarm pheromone emitting mite, Rhizoglyphus setosus. Experimental and Applied Acarology 36, 107–117. [DOI] [PubMed] [Google Scholar]
  48. Mori N and Kuwahara Y (2000) Comparative studies of the ability of males to discriminate between sexes in Caloglyphus spp. Journal of Chemical Ecology 26, 1299–1309. [Google Scholar]
  49. Mori N, Kuwahara Y and Kurosa K (1996) Chemical ecology of astigmatid mites—XLV. (2R,3R)-Epoxyneral: Sex pheromone of the acarid mite Caloglyphus sp. (acarina: acaridae). Bioorganic & Medicinal Chemistry 4(3), 289–295. 10.1016/0968-0896(96)00005-3 [DOI] [PubMed] [Google Scholar]
  50. Mori N, Kuwahara Y and Kurosa K (1998) Rosefuran: The sex pheromone of an acarid mite, Caloglyphus sp.. Journal of Chemical Ecology 24(11), 1771–1779. 10.1023/A:1022399331397 [DOI] [Google Scholar]
  51. Nechita IS, Poirel MT, Cozma V and Zenner L (2015) The repellent and persistent toxic effects of essential oils against the poultry red mite, Dermanyssus gallinae. Veterinary Parasitology 214, 348–352. [DOI] [PubMed] [Google Scholar]
  52. Nishimura K, Shimizu N, Mori N and Kuwahara Y (2003) Chemical ecology of astigmatid mites. LXIV. The alarm pheromone neral functions as an attractant in Schwiebea elongata(Banks)(Acari: Acaridae). Applied Entomology and Zoology 37, 13–18. [Google Scholar]
  53. Nordenfors H, Höglund J and Uggla A (1999) Effects of temperature and humidity on oviposition, molting, and longevity of Dermanyssus gallinae (Acari: Dermanyssidae). Journal of Medical Entomology 36, 68–72. [DOI] [PubMed] [Google Scholar]
  54. Nunn F, Bartley K, Palarea-Albaladejo J, Innocent GT, Turnbull F, Wright HW and Nisbet AJ (2019) A novel, high-welfare methodology for evaluating poultry red mite interventions in vivo. Veterinary Parasitology 267, 42–46. [DOI] [PubMed] [Google Scholar]
  55. Oku K (2009) Effects of density experience on mate guarding behavior by adult male Kanzawa spider mites. Journal of Ethology 27, 279–283. [Google Scholar]
  56. Pageat P (2005) Allomone repulsive and kairomone attractive compositions for controlling arachnids. US Patent No. US 200,.
  57. Pfannkoch E and Whitecavage J (2000) Comparison of the sensitivity of static headspace GC, Solid Phase Microextraction, and Direct Thermal Extraction for analysis of volatiles in solid matrices. AppNote 6/2000.
  58. Pritchard J, Küster T, George D, Sparagano O and Tomley F (2016) Impeding movement of the poultry red mite, Dermanyssus gallinae. Veterinary Parasitology 225, 104–107. [DOI] [PubMed] [Google Scholar]
  59. Rajabpour A, Mashhadi ARA and Ghorbani MR (2018) Acaricidal and repellent properties of some plant extracts against poultry red mite, Dermanyssus gallinae (Mesostigmata: Dermanyssidae). Persian Journal of Acarology 7, 85–91. doi: 10.22073/PJA.V7I1.34098 [DOI] [Google Scholar]
  60. Ramsay GW, Mason PC and Hunter AC (1975) Chicken mite (Dermanyssus gallinae) infesting a dog. New Zealand Veterinary Journal 23, 155–155. [DOI] [PubMed] [Google Scholar]
  61. Regev S and Cone WW (1975) Evidence of Farnesol as a male sex attractant of the twospotted spider mite, Tetranychus urticae Koch (Acarina: Tetranychidae). Environmental Entomology 4, 307–311. [Google Scholar]
  62. Regev S and Cone WW (1976) Analyses of Pharate female twospotted spider mites for Nerolidol and Geraniol: evaluation for sex attraction of males. Environmental Entomology 5, 133–138. [Google Scholar]
  63. Regev S and Cone WW (1980) The Monoterpene Citronellol, as a male sex attractant of the twospotted spider mite, Tetranychus urticae (Acarina: Tetranychidae). Environmental Entomology 9, 50–52. [Google Scholar]
  64. Roy L, Arriaga A and El Adouzi M (2018) Composition anti-acariens. 1–23.
  65. Ryono A, Mori N, Okabe K and Kuwahara Y (2001) Chemical ecology of astigmatid mites. LVIII. 2-Hydroxy-6-methylbenzaldehyde: female sex pheromone of Cosmoglyphus hughesi Samsinak(Acari: Acaridae). Applied Entomology and Zoology 36, 77–81. [Google Scholar]
  66. Santana CB, de L. Souza JG, Coracini MDA, Walerius AH, Soares VD, da Costa WF and da S. Pinto FG (2018) Chemical composition of essential oil from Myrcia oblongata DC and potential antimicrobial, antioxidant and acaricidal activity against Dermanyssus gallinae (De geer, 1778). Bioscience Journal 34, 996–1009. [Google Scholar]
  67. Sato M, Kuwahara Y, Matsuyama S and Suzuki T (1993) Chemical ecology of astigmatid mites XXXVII. Fatty acid as food attractant of astigmatid mites, its scopte and limitation. Applied Entomology and Zoology 28, 565–569. [Google Scholar]
  68. Shimizu N, Mori N and Kawahara Y (2014) Aggregation Pheromone Activity of the Female Sex Pheromone, β-Acaridial, in Caloglyphus polyphyllae (Acari: Acaridae). Bioscience, Biotechnology, and Biochemistry 65(8), 1724–1728. 10.1271/bbb.65.1724 [DOI] [PubMed] [Google Scholar]
  69. Skelton AC, Cameron MM, Pickett JA and Birkett MA (2010) Identification of neryl formate as the airborne aggregation pheromone for the American House Dust Mite and the European House Dust Mite (Acari: Epidermoptidae). Journal of Medical Entomology 47, 798–804. [DOI] [PubMed] [Google Scholar]
  70. Sonenshine DE (1985) Pheromones and other semiochemicals of the Acari. Annual Review of Entomology 30, 1–28. [DOI] [PubMed] [Google Scholar]
  71. Sparagano O, Pavlićević A, Murano T, Camarda A, Sahibi H, Kilpinen O, Mul M, Van Emous R, Le Bouquin S, Hoel K and Cafiero M A (2009) Prevalence and key figures for the poultry red mite Dermanyssus gallinae infections in poultry farm systems. Control of Poultry Mites (Dermanyssus) 48, 3–10. doi: 10.1007/978-90-481-2731-3_2 [DOI] [PubMed] [Google Scholar]
  72. Sparagano OAE, George DR, Harrington DWJ and Giangaspero A (2014) Significance and control of the poultry red mite, Dermanyssus gallinae. Annual Review of Entomology 59, 447–466. [DOI] [PubMed] [Google Scholar]
  73. Steidle J, Barcari E, Hradecky M, Trefz S, Tolasch T, Gantert C, Schulz S, Steidle JLM, Barcari E, Hradecky M, Trefz S, Tolasch T, Gantert C and Schulz S (2014) Pheromonal communication in the European House Dust Mite, Dermatophagoides pteronyssinus. Insects 5, 639–650. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Tabari MA, Youssefi MR and Benelli G (2017) Eco-friendly control of the poultry red mite, Dermanyssus gallinae (Dermanyssidae), using the α-thujone-rich essential oil of Artemisia sieberi (Asteraceae): toxic and repellent potential. Parasitology Research 116, 1545–1551. [DOI] [PubMed] [Google Scholar]
  75. Tatami K, Mori N, Nishida R and Kuwahara Y (2001) 2-Hydroxy-6-methylbenzaldehyde: the female sex pheromone of the house dust mite Dermatophagoides farinae (Astigmata: pyroglyphidae). Medical Entomology and Zoology 52, 279–286. [Google Scholar]
  76. Wicht MC, Rodriguez JG, Smith WT and Jalil M (1971) Attractant to Macrocheles muscaedomesticae (Acarina) present in the housefly, Musca domestica. Journal of Insect Physiology 17, 63–67. [Google Scholar]
  77. Witaliński W, Dabert J and Walzl MG (1992) Morphological adaptation for precopulatory guarding in astigmatic mites (Acari: Acaridida). International Journal of Acarology 18, 49–54. [Google Scholar]
  78. Yasui Y (1992) The receptor sites of sex pheromone eliciting precopulatory mate guarding behavior of male predatory mite Macrocheles muscaedomesticae (Scopoli). Journal of Ethology 10, 81–83. [Google Scholar]
  79. Zeman P (1988) Surface skin lipids of birds – a proper host kairomone and feeding inducer in the poultry red mite, Dermanyssus gallinae. Experimental and Applied Acarology 5, 163–173. [DOI] [PubMed] [Google Scholar]
  80. Zeman P and Zelezny J (1985) The susceptibility of the poultry red mite, Dermanyssus gallinae (De Geer, 1778), to some acaricides under laboratory conditions. Experimental & Applied Acarology 1, 17–22. [DOI] [PubMed] [Google Scholar]
  81. Zhang Z and Li G (2010) A review of advances and new developments in the analysis of biological volatile organic compounds. Microchemical Journal 95, 127–139. [Google Scholar]

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