# Occurrence of phoretic mites associated with flies in laying hens poultry houses in Brazil

Bianca P Valério, Leopoldo F O Bernardi, Khalid Haddi, Livia M S Ataide

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Bianca P Valério, Leopoldo F O Bernardi, Khalid Haddi, Livia M S Ataide. Occurrence of phoretic mites associated with flies in laying hens poultry houses in Brazil. Acarologia, 2024, 64 (3), pp.989-993. 10.24349/mod6-cu7p. hal-04695374

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# Occurrence of phoretic mites associated with flies in laying hens poultry houses in Brazil

Bianca P. Valério IDª, Leopoldo F. O. Bernardi IDª, Khalid Haddi IDª, Livia M. S. Ataide IDª

## Short note

### ABSTRACT

Flies are often found in poultry facilities due to the utilization of bird faeces as a substrate for their larval development. Despite the use of pesticides for fly control in poultry houses, the potential contribution of natural enemies in assisting with fly control deserves attention. This study aimed to assess the diversity and abundance of predatory and phoretic mites associated with flies in two laying hens poultry houses in Minas Gerais, Brazil (ASA and GSJ). By placing 24 pan traps around the sheds of each poultry house, we captured adult flies and mites adhering to these flies over the course of three samplings in each poultry house. *Musca domestica* was found to be the most abundant fly species in both places. Phoretic, predatory and saprophagous mites belonging to the genera *Prodinychus*, *Parasitus*, *Sejus*, *Callidosoma*, *Macrocheles*, *Eupodes* and the family Nothridae were collected at GSJ. In contrast, only one mite genus, *Trichotrombidium* was found at ASA. In addition, a notable contrast in mite abundance was observed between the two poultry houses, with a total of 181 mite specimens associated with flies in the GSJ, compared to 13 in the ASA. While these findings underscore the presence of a diverse mite community associated with flies in poultry houses, we discuss the potential factors contributing to the observed differences between them, shedding light on the ecological contribution of mites within poultry houses.

**Keywords** biological control; *Musca domestica*; pan traps; phoretic mites; poultry facilities

In the egg production industry, the high density of chickens housed in restricted spaces can lead to the accumulation of faeces resulting in a suitable substrate for fly development (Geden *et al.* 2021; Axtell 1986). More than 90% of the flies captured in poultry houses are houseflies (*M. domestica* (L.) (Muscidae)) (Valério *et al.* 2023), synanthropic insects that can negatively impact egg production when their population increase significantly (Geden *et al.* 2021). Problems associated with the high density of flies in poultry units are generally related to the inadequate management of their faeces. Interestingly, this substrate can also function as a habitat for several beneficial arthropods, some of which undergo partial development or complete their entire life cycle within it. These arthropods can serve as natural enemies of houseflies and other synanthropic flies found in the surrounding environment. For instance, mites of the family Macrochelidae are important predators of flies living in chicken faeces (Gerson, Smiley and Ochoa 2003; de Azevedo *et al.* 2015). Some of these predatory mite species exhibit phoretic behaviour, i.e., they attach themselves to adult flies and use them as vectors to disperse (Ho 1990), promoting colonization of new sites (Athias-Binche 1993). Since these predatory mites spend their entire life cycle in soil environments, such as chicken faeces, this phoretic behaviour can promote mite dispersal throughout the poultry house. Enhancing the spatial distribution of

Received 02 May 2024
Accepted 08 September 2024
Published 12 September 2024

Corresponding author
Livia M. S. Ataide ID:
liviaataide@gmail.com

Academic editor
Roy, Lise

https://doi.org/10.24349/mod6-cu7p

ISSN 0044-586X (print)
ISSN 2107-7207 (electronic)

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Valério B. P. *et al.*

Licensed under
Creative Commons CC-BY 4.0

<footnote>ªDepartment of Entomology, Federal University of Lavras, Lavras, Minas Gerais, Brazil.</footnote>
beneficial organisms within the poultry house has the potential to increase the efficiency of their biological control services. Incorporating the conservation or introduction of predatory mites into integrated pest management (IPM) strategies can be a valuable and effective approach. Therefore, understanding the diversity of natural enemies present in this given environment is of fundamental importance. This study aimed to investigate the occurrence of predatory and phoretic mite species associated with flies in laying hens poultry houses. To this end, we evaluated diversity and abundance of macrochelids, and other mites attacked to adult flies captured in two poultry houses, located in Minas Gerais, Brazil. The first was a conventional vertical laying poultry house, operated with a vertical automated/manual Californian system, hereafter ASA. The property has nine units (sheds) and 360,000 laying hens, located in the municipality of Nepomuceno (latitude: 21°12'17.8" S, longitude: 45°14'24.3" W). The second site was a conventional laying poultry house, hereafter GSJ. The property has six units (sheds) and currently has a total of 35,000 laying hens, located in the municipality of Lavras (latitude: 21°13'30.0" S, longitude: 45°02'55.8" W).

For the collection of flies and their associated mites, 24 white pan traps were placed randomly in a radius of 200 metres from the sheds of each poultry house, following the procedure described at Valerio *et al.* (2023). Each trap (1 L), filled with 400 mL of a mixture of water with detergent and salt, was left in the field for five consecutive days, and on the last day, the entire contents were stored in glass jars (300 mL) and taken to the laboratory. The flies and mites were stored in a Falcon tube (50 mL) containing ethanol (99%). Three collections were performed over time, between March and April 2021. The flies and mites collected were identified in the laboratory using a stereomicroscope (Nikon® SMZ1270, New York, USA). The identification of the flies was based on the identification keys proposed by Grella (2011) and Carvalho and Mello-Patiu (2008), and the identification of mites was based on Krantz and Walter (2009), Takaku *et al.* (2012), Hyatt (1980), Trach and Tolstikov (2016), Felska *et al.* (2018), Mineiro and De Moraes (2002).

The differences in the relative abundance of mites attached to the flies between the two poultry houses were analysed using Wilcoxon-signed rank test using the wilcox.test function of the R program (R Core Team 2022). Our findings revealed significant variations in the abundance (W= 1388.5; d.f= 1; *P* < 0.001) and diversity of mite species associated with flies between poultry houses (Table 1). In addition, *M. domestica* was found to be the most abundant fly species in both poultry houses. Identifying mites to species level was challenging due to absence of males, adult stages, and inadequate knowledge of the Brazilian fauna and they were identified to its genus level. Regarding the biology and ecology of those mites, the deutonymphs of *Prodinychus* sp.1 exhibit phoretic behaviour, and it is likely that their females are mycophagous (Flechtmann 1968). The deutonymphs of *Parasitus* sp.1 commonly engage in phoretic interactions with insects, while the adults occupy transient habitats, such as soil, small mammals, and bird nests, among others (Hrúzová and Fendá 2018; Hyatt 1980). Nothridae and *Eupodes* sp.1 mites are soil-dwelling mites, primarily found in environments with high organic matter content, where they are typically saprophagous and mycophagous. Their association with flies is probably accidental in nature (Mineiro and Moraes 2002; Norton and Behan-Pelletier 2009). The species *Callidosoma* sp.1 and *Trichotrombidium* sp.1 collected in this study are the larval stage of new species records in Minas Gerais, Brazil and will be described in a separate manuscript. *Callidosoma* and *Trichotrombidium*, both belonging to the suborder Prostigmata, share a similar life cycle. In this mite subgroup, with only rare exceptions, the larvae act as parasites of either vertebrates or invertebrates while the deutonymph and the adult stages exhibit predatory behaviour, inhabiting the soil and preying on larvae or small invertebrates (Wohltmann 2000). Mites of the genus *Sejus* are predators of small invertebrates and worms, and their deutonymphs and adults are phoretic on small invertebrates (Walter and Proctor 1998; Krantz and Walter 2009). *Macrocheles* mites are predominantly predators, with many species preying on various fly species. Their demonstrated ability to prey on eggs and larval stages of *M. domestica* underscores their potential as biological control agents of this pest across various environments (Azevedo *et al.* 2018; Perotti 2001). They develop in dung
<table><caption>Table 1 Adult flies and associated mites collected in two poultry houses (ASA and GSJ).</caption><thead><tr><th>Taxon of flies</th><th>Taxon of mites*</th><th>Number of mites/ fly</th><th>Poultry House</th></tr></thead><tbody><tr><td>Musca domestica</td><td>Prodinychus sp.1 (DN)</td><td>13</td><td>GSJ</td></tr><tr><td>Calliphoridae</td><td>Macrocheles merdarius (F)</td><td>3</td><td>GSJ</td></tr><tr><td>Calliphoridae</td><td>Callidosoma sp.1 (L)</td><td>1</td><td>GSJ</td></tr><tr><td>Calliphoridae</td><td>Prodinychus sp.1 (DN)</td><td>20</td><td>GSJ</td></tr><tr><td>Calliphoridae</td><td>Prodinychus sp.1 (DN)</td><td>22</td><td>GSJ</td></tr><tr><td>Calliphoridae</td><td>Macrocheles merdarius (F)</td><td>1</td><td>GSJ</td></tr><tr><td>Calliphoridae</td><td>Nothridae sp.1 (F)</td><td>1</td><td>GSJ</td></tr><tr><td>Calliphoridae</td><td>Eupodes sp.1 (F)</td><td>1</td><td>GSJ</td></tr><tr><td>Sarcophagidae</td><td>Prodinychus sp.1 (DN)</td><td>11</td><td>GSJ</td></tr><tr><td>Sarcophagidae</td><td>Prodinychus sp.1 (DN)</td><td>25</td><td>GSJ</td></tr><tr><td>Calliphoridae</td><td>Macrocheles merdarius (F)</td><td>1</td><td>GSJ</td></tr><tr><td>Calliphoridae</td><td>Callidosoma sp.1 (L)</td><td>2</td><td>GSJ</td></tr><tr><td>Stomoxys calcitrans</td><td>Trichotrombidium sp.1 (L)</td><td>8</td><td>ASA</td></tr><tr><td>Stomoxys calcitrans</td><td>Trichotrombidium sp.1 (L)</td><td>5</td><td>ASA</td></tr><tr><td>Musca domestica</td><td>Prodinychus sp.1 (DN)</td><td>2</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Macrocheles merdarius (F)</td><td>1</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Prodinychus sp.1 (DN)</td><td>3</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Prodinychus sp.1 (DN)</td><td>1</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Prodinychus sp.1 (DN)</td><td>2</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Macrocheles merdarius (F)</td><td>1</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Prodinychus sp.1 (DN)</td><td>3</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Prodinychus sp.1 (DN)</td><td>1</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Macrocheles merdarius (F)</td><td>15</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Macrocheles merdarius (F)</td><td>6</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Callidosoma sp.1 (L)</td><td>1</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Prodinychus sp.1 (DN)</td><td>2</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Prodinychus sp.1 (DN)</td><td>2</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Macrocheles merdarius (F)</td><td>1</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Prodinychus sp.1 (DN)</td><td>1</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Sejus sp.1 (F)</td><td>2</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Prodinychus sp.1 (DN)</td><td>3</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Prodinychus sp.1 (DN)</td><td>2</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Prodinychus sp.1 (DN)</td><td>2</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Parasitus sp.1 (DN)</td><td>1</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Macrocheles merdarius (F)</td><td>2</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Callidosoma sp.1 (L)</td><td>1</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Prodinychus sp.1 (DN)</td><td>1</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Prodinychus sp.1 (DN)</td><td>3</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Macrocheles merdarius (F)</td><td>9</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Callidosoma sp.1 (L)</td><td>1</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Macrocheles merdarius (F)</td><td>1</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Prodinychus sp.1 (DN)</td><td>3</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Prodinychus sp.1 (DN)</td><td>1</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Macrocheles merdarius (F)</td><td>1</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Macrocheles merdarius (F)</td><td>1</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Prodinychus sp.1 (DN)</td><td>1</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Prodinychus sp.1 (DN)</td><td>1</td><td>GSJ</td></tr><tr><td>Musca domestica</td><td>Prodinychus sp.1 (DN)</td><td>2</td><td>GSJ</td></tr><tr><td>Total</td><td>-</td><td>194</td><td>-</td></tr></tbody></table>

F: Female, DN: Deutonymph, L: Larvae.
accumulations and adults exhibit a remarkable ability for phoresy (Krantz 1998). It is possible
that these mites are actively contributing to housefly control within poultry houses, but their
role as biological agents remain to be tested.

Finally, the low presence of mites attached to flies in the ASA poultry house suggests some major factors disrupting mite occurrence. Mites, as well as other soil invertebrates, are sensitive to several abiotic and/or biotic factors, such as food availability, temperature, humidity, presence of other organisms, latitude, and longitude. The two poultry houses chosen in this study are located 30 kilometres away from each other, which means that factors such as topography, humidity, and temperature are relatively similar. However, none of these factors were monitored during the study but they may have influenced the diversity and abundance of mites in the poultry houses.

Acknowledgements

We thank Granja São Jorge, Mr. Galeno, Mr. Elias M. Castro, and Dr. Stephan Malfitano Carvalho for their assistance in the execution of the experiments. BPV and LFOB thanks the Coordination for the Improvement of Higher Education Personnel (CAPES) for the scholarships.

ORCID

Bianca P. Valério https://orcid.org/0000-0003-4279-6193

Leopoldo F. O. Bernardi https://orcid.org/0000-0002-0611-0134

Khalid Haddi https://orcid.org/0000-0002-2655-4365

Livia M. S. Ataide https://orcid.org/0000-0003-2159-7267

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