Dermanyssus gallinae

Soulié, Anne-Sophie, Sleeckx, Nathalie & Review, Lise Roy, 2021, Repellent properties of natural substances against Dermanyssus gallinae: review of knowledge and prospects for Integrated Pest Management, Acarologia 61 (1), pp. 3-19 : 13-14

D. gallinae

The sustainability of the efficacy of a treatment against pests (3 rdprinciple of the IPM stated above; not to be confused with the persistence of products in the environment) depends largely on the speed of emergence of resistance. Resistance to pesticides is defined by the R4P network (researcher network for reflection and research on pesticide resistances) as “the heritable ability of an individual belonging to a pest species to survive a treatment applied correctly. When an individual is resistant to a [pesticide], it will be not (or little) affected by the treatment and will be able to produce viable offspring.” (R4P 2019). In field conditions, resistance results in the repeated failure of a product to achieve the expected level of control when it has been used according to its specific recommendations ( IRAC 2020). Any product dedicated to controlling a pest exerts a selective pressure on its populations. This natural selection operates on the genotypic diversity initially available in the pest population and gradually leads to an increase in the frequency of genotypes that are tolerant to the control method, leading to the emergence of resistance within a pest population. In case of repellent activity, the selective pressure exerted by volatile compounds may lead to the increase in the frequency of genotypes that are insensitive (physiological inability to perceive the compounds) or that do not respond to perceived compounds (lack of repellent avoidance behavior).

Pesticide resistance in various pest arthropods is, and has been, the subject of numerous studies ( REX Consortium 2007), but little is known about resistance to repellent substances.

Only a few insects, including mosquitoes, bedbugs and cockroaches, have been studied for resistance to repellents ( Stanczyk et al. 2010 ; Mengoni and Alzogaray 2018; Deletre et al.

2019; Vassena et al. 2019, Yang et al. 2019). These pioneering studies on insects, including two blood­feeding micropredators (mosquitoes and bedbugs), are likely to provide valuable insights to effectively advance the exploration of this topic in D. gallinae . Most of these studies have focused on synthetic repellents, although Deletre et al. (2019) also included plant secondary metabolites in their work.

N,N­Diethyl­m­toluamide (DEET) is the most commonly used active ingredient in insect repellents. Resistance to DEET has been reported in mosquitoes, bedbugs and cockroaches

( Stanczyk et al. 2010 ; Mengoni and Alzogaray 2018; Deletre et al. 2019 ; Vassena et al. 2019,

Yang et al. 2019). All of these studies demonstrated significant differences in behavioral responses to DEET amongst populations of the insects studied. In addition, Stanczyk et al. (2010) experimentally demonstrated that the “insensitive” trait to DEET was hereditary,

dominant in Aedes aegypti and based on a change in the function of one sensilla.

Interestingly, cross­resistance was reported between neurotoxic insecticides (pyrethroids,

organophosphates) and repellent substances in all three afforementioned insect taxa (mosquitoes,

bedbugs and cockroaches; Mengoni and Alzogaray 2018; Deletre et al. 2019 ; Vassena et al.

2019, Yang et al. 2019). In these studies, insecticide­resistant populations of Aedes aegypti

(mosquito), Cimex lectularius (bedbug) and Blattella germanica (cockroach) were shown to be less responsive to repellents than susceptible populations of the same taxa. Yang et al.

(2019) have also reported a decreased antennal sensitivity in populations of Ae. aegypti that were resistant to both pyrethroids and DEET, as well as to three other synthetic repellents.

Several compounds contained in plant essential oils, and known for their repellent properties against D. gallinae (e.g., geraniol, eugenol), have been shown to have true neurotoxic effects on insects, with molecular and cellular targets common to those of synthetic insecticides

( López and Pascual­Villalobos 2010, Regnault­Roger et al. 2012). Cross­resistance between plant­derived repellents and synthetic insecticides, especially when target­site resistance is involved, can therefore be explained by the functional basis of the latter.

However, consistent with this hypothesis, the effect of target protein modification is not always a decrease in susceptibility to repellents. In another mosquito Anopheles ( gambiae ), for example, Deletre et al. (2019) found an increase in sensitivity to certain repellents in mutant genotypes displaying target­site pyrethroid and organophosphorus resistances due to the kdr mutation in the voltage­dependent sodium channel and the Ace mutation in acetylcholinesterase,

respectively. In cases of target­site resistance, the target protein of the insecticide has a slightly modified amino acid sequence compared to the same protein in a susceptible individual, thereby inducing a decrease in the affinity of the pesticide. The alleles of the coding gene often differ between susceptible and resistant types by a simple nonsilent point mutation at a key site of the interaction between the two molecules. Thus, although plant­derived compounds can affect the same proteins as synthetic insecticides, they most likely do not do so in the same way (not at the same sites of action). Additionally, pleiotropic effects (single genes affecting multiple systems or determining more than one phenotype) of the alleles conferring insecticide resistance may also explain these patterns ( Deletre et al. 2019). Whatever the reason, it is not surprising that variations in protein­coding genes of the nervous system can affect the susceptibility to insecticides and repellents in a variety of ways, sometimes in contradictory directions.

We can therefore conclude that, at least in mosquitoes, target resistance to neurotoxic insecticides may be associated with resistance to repellents, but also with increased susceptibility to repellents. As there are several mutations responsible for target resistance to pyrethroids in

D. gallinae , and as they are relatively frequent in several regions of the world (Katsavou et al.

2020), taking these genotypes into account when assessing the risk of resistance developing to plant­derived repellents will constitute a point of interest for further work in this area.