A nonexhaustive overview on potential impacts of the poultry red mite (Dermanyssus gallinae) on poultry production systems

Impact on Poultry Production Systems

The poultry red mite (PRM) (Dermanyssus gallinae) is a worldwide problem for the poultry production industry. Prevalence rates of more than 80% are common in many countries (Sparagano et al., 2009; Tomley and Sparagano, 2018). Complete development of D. gallinae, from egg to adult through one larval stage and two nymphal stages, typically occurs over 2 weeks. They usually feed for short periods and retrieve in cracks and crevices to digest blood contrary to other poultry mites.

Economic costs associated with both control and production losses due to D. gallinae have been estimated at €130 million per year for the European Union egg industry. There is a relationship between D. gallinae infestation and hen mortality; some reports record a 10-fold increase in death rates following severe infestation in Romania (Cosoroaba, 2001). Although causal factors may vary, in extreme cases D. gallinae numbers may be so high that hens become severely anemic, with mortality resulting from exsanguination. At a sublethal level, mite feeding may result in significant stress to hens, causing an increase in circulating corticosterone and adrenaline and a decrease in β- and γ-globulins. Bird sleep patterns can be disrupted by the need for increased preening, and changes in head-scratching and feather-pecking behavior could also be seen. Increases in aggressive feather-pecking and cannibalistic behaviors have been reported. These mites can survive for weeks if not months without a blood meal and can therefore reappear between flocks. As blood feeders, PRMs could induce anemia with economic losses related to smaller egg size, less eggs per hen per year, and higher mortality. A recent report in Belgium followed various production parameters for fluralaner-treated bird groups compared to control groups, highlighting the positive impact of such treatment (Sleeckx et al., 2019). These mites can harbor key symbionts needed for their survival (de Luna et al., 2009) and can be responsible for the transmission of bacterial and viral diseases such as Salmonella (Valiente Moro et al., 2007; Hamidi et al., 2011; Sylejmani et al., 2016), Avian Influenza (Sommer et al., 2016), Coxiella burnetii, and Borrelia burgdorferi (Raele et al., 2018) which can also decimate flocks in their own rights (Sparagano et al., 2014).

PRM is also known to attack humans, called gamasoidosis (Cafiero et al., 2018, de Sousa and Filho Bernardes, 2018; Navarrete-Dechent and Uribe, 2018; Cafiero et al., 2019) but is still underestimated in human medicine (Kavallari et al., 2018) and can attack other animals such as cats (Di Palma et al., 2018) and wild birds such as Barn Swallow (Ghalehjoughi et al., 2017).

Control and Monitoring Methods

Monitoring methods

To monitor D. gallinae mites, many traps have been either produced at an industrial level such as the AVIVET trap (Lammers et al., 2017) or by using simple cardboard and usually keeping such traps for a few days to a week. For a comparison of different trap efficiencies, see the work of Cunha et al. (2009). Recently, a more automatic way of monitoring and counting mites was published in the work of Mul et al. (2015). Such traps have shown in the past that mite colonies are not uniformly spread in a poultry shed or cages with parameters such as ventilation, humidity, dust, or temperature inside the poultry house affecting the colony growth.

Traps have also been used as a control method when acaricide/insecticide products were inserted inside such traps to kill the arthropods trying to hide inside them (Barimani et al., 2016).

Control methods

Chemical

Dermanyssus gallinae has typically been controlled using synthetic acaricides. Some recent formulations can be used in the presence of the birds to avoid delaying mite control procedures, in any case withdrawal periods for eggs or broiler meat have to be respected to ensure the highest food safety standards and consumer protection. Biopesticides are now emerging as a control alternative in organic poultry production systems (George et al., 2014). However, acaricide resistance has been reported for several decades and following the Fipronil scandal in Europe during summer 2017, national legislations have removed several products from the poultry market limiting the number of available products in some countries.

However, some new products have been launched which can be used in the presence of the poultry birds on the farms allowing rapid treatments such as the new Exoltz (Fluralaner-based product) from MSD Animal Health working on two molecular targets in these mites (Sigognault Flochlay et al., 2017).

The acaricidal effect of macrocyclic lactones has also recently been documented by researchers in China (Xu et al., 2019).

Biological

Biological control approaches using PRM predators (such as Androlaelaps casalis, Hypoaspis aculeifer, Hypoaspis miles, and Stratiolaelaps scimitus) seem to reduce the mite infestation but in some specific systems in which predators can hunt easily the mites. Cheyletus eruditus is now commercialized and can be used in combination with Androlaelaps spp. (anonymous reviewer’s comments). Cheyletus malaccensis has been used successfully in Brazil (Anonymous, 2017; Toldi et al., 2017). Interestingly, other arthropods could become part of the solution in controlling PRM and it is important to understand the interactions between different arthropod species such as highlighted by Roy et al. (2017) and Horn et al. (2019). Although PRM is widespread in Europe, Ornithonyssus sylviarum (the Northern fowl mite) in the United States and Ornithonyssus bursa (the tropical fowl mite, TFM) in Asia, we start to see reports showing that several of them can be found on the same farm such as in Myanmar (Takehara et al., 2019).

Recently, entomopathogenic fungi such as Aspergillus oryzae showed higher mortalities compared to control PRM groups on adult stages, while it seemed ineffective on nymphal stages (Wang et al., 2019); while Metarhizium spp. was reported to cause 56% to 95% of PRM adult stage mortality (depending on the strain and environmental conditions) (Tomer et al., 2018).

Other biological approaches relying on plant extracts/formulations have been highlighted for almost a decade now to control PRM in Europe (George et al., 2014; Camarda et al., 2018) and more recently in South Korea (Lee et al., 2019); using terrestrial (George et al., 2010) or aquatic plants (Rhimi et al., 2019), for the latter highlighting the importance of bufadienolides molecules in the extracts. Garlic extracts gave a 96% reduction against PRM in Iran (Faghihzadeh Gorji et al., 2014).

Physical methods

Physical methods such as steam and heat have reduced considerably while the use of silica-related products seems to become more widespread (Schulz et al., 2014).

However, recent work on genomics and proteomics focusing on a vaccination-driven approach seems to be a possible future option (Sparagano et al., 2014; Sparagano, 2017 for a review). In terms of vaccine development against PRM, research has been ongoing for over a decade.

Vaccine preparations started from crude antigens being used (Arkle et al., 2008), recombinant antigens (Harrington et al., 2009), PRM tropomyosin, and paramyosin (Wright et al., 2016) to new vaccine delivery systems (Price et al., 2019). For more information related to the development of subunit vaccines related to animal parasites, readers could refer to the PARAGONE EU Consortium work (https://www.paragoneh2020.eu)

Population Ecology of Dermanyssus Mites

Could the resistance/sensitivity to acaricide products or the difference observed in the behavior and aggression of Dermanyssus isolates be explained by a population heterogeneity within the D. gallinae species or D. gallinae sensu lato (s.l.)? Roy et al. (2010a, 2010b) have demonstrated the existence of at least two cryptic subspecies.

Genetic diversity at the farm level has been observed as widely as between farms from different countries (Marangi et al., 2009b). Relationships between different lineages and the way mites might infest through trade (less likely between wild and domesticated birds) have been studied in depth by Roy and Buronfosse (2011).

So far no studies have been done on Dermanyssus populations introduced on a farm and how subpopulations are adapting or being eliminated during control methods and how the D. gallinae lineages are made of at the end of the flock life. Such work could allow to see why some lineages are more sensitive or resistant to different control methods and if dilution effects between populations could also explain such variations between initial and terminal populations found in a poultry flock.

Research Progress

The knowledge gaps in PRM should start shrinking very quickly since Schicht et al. (2013) published the secretome and transmembranome of D. gallinae. It allowed other researchers to start assembling the genome information now known to be circa 959 MB and responsible for 14,608 protein-coding genes (Burgess et al., 2018). Such knowledge would allow identifying new drug or vaccine targets to generate more effective treatments and preventative approaches.

To counter-react acaricide resistance reports have shown that detoxification P450 complexes could be a successful target (Graham et al., 2016) or targeting another pathway such as glutathione S-transferase (Bartley et al., 2015).

Furthermore, if knocking down D. gallinae still create some technical challenges, as always with ectoparasites not staying long on their host, then another approach could be to target the symbionts and microbiome populations, which can be absolutely necessary for their survival. Impacting negatively of such microbes has already been attempted by several researchers (Hubert et al., 2017; Lima-Barbero et al., 2019) and could open new control strategies.

Predictive models are becoming more and more important to develop early treatments as correlating stained eggs and mite population growth (Odaka et al., 2017) or a more performant counter (compared to traditional cardboard traps to help poultry farmers to decide when to treat; Mul et al., 2017).

Conclusions

PRM is a major pest responsible for economical and welfare issues in many different types of poultry production systems. Prevalence still seems very high in Europe (Sparagano et al., 2009, 75% to 93%; Waap et al., 2019, 95.8%) or in Brazil (Faleiro et al., 2015, 98.9%), some other countries in North Africa are showing more moderate prevalence rates with 34% in Tunisia (Gharbi et al., 2013) or 40.9% in Egypt (Eladl et al., 2018), which could support the idea that hot dry climates are less favorable than mild humid ones.

Dermanyssus gallinae is a serious threat to laying hens and egg production systems in many parts of the world, and acaricide resistance (Marangi et al., 2009a; Abbas et al., 2014; Eladl et al., 2018) and changes in pesticide and hen welfare legislation are set to exacerbate this issue in many countries. As the role of D. gallinae as a disease vector becomes better understood, its pest status increases commensurately (direct transmission of Salmonella and Avian Influenza has been reported) (Valiente Moro et al., 2007, 2009; Hamidi et al., 2011; Sommer et al., 2016). Recent reports of D. gallinae infestations in a range of alternative hosts further contribute to this status. Should existing trends continue, D. gallinae could soon be problematic for other domestic fowl, pets, and even humans, as it is for poultry birds. If the versatility of PRM, in attacking different animal hosts, is well documented, another issue of considerable importance is based on the possible variability in PRM species and dispersion of wild and farm strains, which could in turn create hybrids able to colonize other natural and artificial biotopes (Roy and Buronfosse, 2011). Interestingly could the variation in PRM aggressive behavior linked to the different Dermanyssus lineage/strains/species isolated (Roy and Buronfosse, 2011; Pezzi et al., 2017).

Hazard Analysis and Critical Control Point method can help preventing D. gallinae establishment in all types of poultry production systems (Mul and Koenraadt, 2009), while automated modeling of PRM populations on farms would better assist poultry farmers to decide when starting effective treatments (Mul et al., 2017). Integrated Pest Management should become a norm to avoid mites being able to develop counter mechanisms to the control methods presented in this review.

Targeting PRM itself has certainly been a challenge and new approaches are considering targeting symbionts in those mites or evaluating what successes could be transferable from other controlled mites or tick. Other researchers are even going further under the “One Health” concept to identify successes in medical sciences to be applied to veterinary medicine. Genomic, proteomic, and transcriptomic databases in other parasites could help designing new prevention or treatment approaches against D. gallinae (Fischer and Walton, 2014). Through such a “One Health” approach it will be paramount to engage further with the farming communities, medical and veterinary practitioners, environmental agencies and policymakers dealing with pest control, consumer protection, and animal welfare.

Glossary

Abbreviation

PRM

poultry red mite

This paper was presented at the 17th International Conference on Production Diseases in Farm Animals, Bern, Switzerland (June 27–29, 2019).

Conflict of interest statement

The authors declare no real or perceived conflicts of interest.