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New records, a completed list and identification key of mites (Acari) associated with the stable fly, Stomoxys calcitrans (L.) (Diptera: Muscidae)

Kontschán, Jenő1 and Hornok, Sándor2

1✉ Plant Protection Institute, Centre for Agricultural Research, Hungarian Academy of Sciences, H-1525 Budapest, P.O. Box 102, Hungary.
2Department of Parasitology and Zoology, University of Veterinary Medicine, H-1400 Budapest Pf. 2, Hungary.

2019 - Volume: 59 Issue: 1 pages: 3-11

DOI: 10.24349/acarologia/20194306
ZooBank LSID: E7B6320D-49E5-4EE8-BF0E-77EB1924429E

Original article

Keywords

dog fly phoresy new host Hungary

Abstract

The stable fly, Stomoxys calcitrans (L.) is a blood-sucking muscid fly species, with a worldwide distribution and high veterinary-medical importance. In this study, four mite species were collected from stable flies in Hungary. One mite species (Trichotrombidium muscarum (Riley, 1878)) from the family Microtrombidiidae was parasitic on the flies, collected in high numbers from their bodies. The other three species were found in small numbers on the flies, which they use only for transportation. The latter included the phoretic female of Pediculaster mesembrinae (Canestrini, 1881) (Acari: Siteroptidae), the phoretic deutonymph of the Halolaelaps sexclavatus (Oudemans, 1902) (Acari: Halolaelapidae) and Macrocheles subbadius (Berlese, 1904) (Acari: Macrochelidae). This is the first record of an association between the stable fly and two mite species (Trichotrombidium muscarum and Halolaelaps sexclavatus). A new, completed list and identification key of known stable fly associated mites are also provided.

Introduction

The stable fly or dog fly, Stomoxys calcitrans (L.) (Diptera: Muscidae), is a widely distributed member of the genus Stomoxys. This fly species occurs both in the tropical and temperate climatic zones (Showler & Osbrink 2015) and, as an economically important pest, causes severe problems for livestock and pets due to blood sucking activity and transmission of vector-borne pathogens (Baldacchino et al. 2013).

To date numerous mite species have been recorded from different groups of flies (Samšiňák 1979, 1989, Mumcuoglu & Braverman 2010, Perez-Leanos 2017), but mites associated with the stable fly have been scarcely investigated. McGarry & Baker (1997) listed twelve mites species associated with Stomoxys calcitrans from the families Ereynetidae, Pygmephoridae, Winterschmidtiidae, Acaridae, Histiostomatidae, Macrochelidae, Digamasellidae, Halolaelpidae, Uropodidae, Eviphididae. Other studies only focused on stable fly associated mites from the family Macrochelidae (Beresford & Sutclife 2009, Mumcuoglu & Braverman 2010, Mašán 2003).

Recently, stable flies were collected in several regions of Hungary and a few fly specimens were found infested by mites. Mites living on the body of the flies constitute a highly neglected area of the Hungarian acarology (Horváth et al. 2010). Only Kobulej (1951) presented some mites form Musca domestica Linnaeus, 1758, whereas Erőss & Mahunka (1971) reported a macrochelid mite species from the stable fly.

Materials and methods

Stable flies were collected manually (by using butterfly nets) at two-week intervals, from September to November 2017, in six locations in Hungary (data not shown). Mite-infested stable flies were only found at the location providing the most fly specimens, i.e. near a beef cattle herd in northern Hungary (Pásztó, 47°55'34.5"N, 19°40'49.8"E). Mite specimens were removed from the flies using a 00 or 0 paint brush under a BTC binocular microscope. Mites were cleared in lactic acid and placed on slide for morphological identification. Drawings were made with the aid of a drawing tube on a Leica 1000 microscope. All specimens are stored in 75% ethanol and are deposited at the Plant Protection Institute, Centre for Agricultural Research, Hungarian Academy of Sciences and at the Department of Parasitology and Zoology, University of Veterinary Medicine. Photos were taken with a VHX-5000 digital microscope (Keyence Co., Osaka, Japan). Measurements are presented as ranges of minimum to maximum. Measurements and the scales in the figures are given in micrometres (μm).

Results
List of species found in Hungary
Acari
Mesostigmata
Macrochelidae
Macrocheles subbadius (Berlese, 1904)

Distinguishing characters of female. All dorsal setae smooth and needle-like, except setae j1 which are smooth and robust. Ventral setae also smooth and needle-like, sternal shield ornamented with small pits. Ventrianal shield pentagonal with three pairs of needle-like setae anterior to anal opening (Figure 1, A & B).

Figure 1. Mites associated with stable fly I: A – dorsal view of Macrocheles subbadius (Berlese, 1904), female, B – ventral view; C – dorsal view of Halolaelps sexclavatus (Oudemans, 1902), deutonymph, D – ventral view. Scale bars in μm

Notes. This is the species most frequently collected from the bodies of stable flies. This association was reported from Hungary (Erős & Mahunka 1971), France (Niogret et al. 2008), Slovakia (Mašán 2003), Israel (Mumcuoglu & Braverman 2010), United Kingdom (McGarry & Baker 1997) and Canada (Beresford & Sutcliffe 2009). Macrocheles subbadius is a coprophilous detriticole species and a typical phoretic mite, which does not parasitize the stable fly, but use it only for transportation between different habitats (like dung pads, compost heaps etc.).

Halolaelpidae
Halolaelps sexclavatus (Oudemans, 1902)

Distinguishing characters of the deutonymphs. All dorsal setae short, smooth and needle-like. Ventral setae also smooth and needle-like, three pairs club-like setae visible on the gnathosoma (setae h4 or subcoxal setae), and on coxae II and III (Figure 1, C & D).

Notes. This is the first report of this mite in association with the stable fly. The deutonymph of H. sexclavatus is known to be present on the body of various insect species (like: beetles Bahrami et al. 2011) or in bird nests (Krištofík et al 2013), but it was never collected from stable flies. Nevertheless, McGarry & Baker (1997) listed a Halolaelaps species from this fly species in the UK. Halolaelps sexclavatus is not a parasitic mite: this species occurs in compost and dung, therefore we suppose that this species uses the host only for dispersal between different sites.

Prostigmata
Siteroptidae
Pediculaster mesembrinae (Canestrini, 1881)

Distinguishing characters of the phoretomorphic female. First sternal plates with 6-6 setae. Setae e shorter than setae f, setae ps2 two times longer than setae ps1 and ps3 (Figure 2, A & B).

Figure 2. Mites associated with stable fly II. A – dorsal view of Pediculaster mesembrinae (Canestrini, 1881), phoretic female, B – ventral view; C – dorsal view of Trichotrombidium muscarum, larva, D – ventral view. Scale bars in μm

Notes. This mite species was recorded from stable flies (McGarry & Baker 1997) in the UK. Pediculaster mesembrinae occurs in places where dung or dung inhabiting flies are found (Mahunka 1972). This species is not parasitic on stable flies, and similarly to the previously mentioned two species, uses them only for transportation.

Trombidiformes
Microtrombidiidae
Trichotrombidium muscarum (Riley, 1878)

Distinguishing characters of the larvae. Scutellum 3.5 times wider than long, wider than scutum. Scutum and scutellum with punctuation on central part and with longitudinal striae on lateral parts. Number of dorsal setae 28, setae AM smooth, other setae on dorsum slightly barbed, trichobothria narrow and very finely barbed (Figure 2, C & D).

Notes. This species is the senior synonym of T. hemistriatum (Womerslay, 1942) (Welbourn 1985) and T. rafieiae Saboori, 2002 (Hakimtabar & Saboori 2018). Kobulej (1951) described a new species Trichotrombidium muscae Kobulej, 1951, which is also a junior synonym of T. muscarum (Riley, 1878). Saboori (2002) mentioned T. muscarum in the key to Trichotrombidium species as T. hemistriatum Kobulej, 1951 which is an erroneous name (maybe mixed names of the species of Womersay and Kobulej). The name T. muscarum was also mentioned in Suhas and Rhao (1986) as "Trichotrombidium muscarum Kolonev" (sic!), which is another misuse of this name.

This is a true parasitic species, known from Musca domestica only from Iran (Saboori 2002) and from Turkey (Karakurt & Sevsay 2013), and from a species of the family Ulidiidae (Diptera) (Hakimtabar & Saboori 2018), but never mentioned from stable fly. McGarry et al. (1992) reported Trichotrombidium muscarum (Riley) from flies from Libya and mentioned it from stable fly from Romania without citing references, so this association is questionable.

The rate of the infection

Only 5 stable flies were infested by mites from the collected 350 specimens. During our investigation of mites associated with stable flies only four mite species were collected. Two species were represented by only single specimens, namely the halolaelapid Halolaelaps sexclavatus and the siteroptid Pediculaster mesembrinae. The other two species were more abundant, one or two specimens of M. subbadius were found on the venter of the body of the flies (Figure 3). High numbers (8-37 specimens) of T. muscarum infested the flies (Figure 4) and these were found all over the body, adhering to the membranous cuticle between the tergites and sternites of abdomen and the parts of thorax.

Figure 3. Macrocheles subbadius (Berlese, 1904) female attached to stable fly. Scale bars in μm

Figure 4. Trichotrombidium muscarum (Riley, 1878) larvae attached to stable fly. Scale bars in μm
Discussion

To date only few records are available on the mites of stable flies (Table 1). Most known associations were reported from the Palearctic, from the UK, Israel, France, Slovakia and Hungary. Only two mite species are known from the Nearctic region and another two species are described from the Afrotropical region.



Mite catagory Mite family Mite species Biogeographical region Country References
Mesostigmata Macrochelidae Macrocheles subbadius (Berlese, 1904) Palearctic Hungary Erős & Mahunka (1971)
Palearctic UK McGarry & Baker (1997)
Palearctic Slovakia Mašán (2003)
Palearctic France Niogret et al. (2006)
Palearctic Israel Mumcuoglu & Braverman (2010)
Nearctic Canada Beresford & Sutcliffe (2009)
Macrocheles muscadomesticae (Scopoli, 1772) Palearctic UK McGarry & Baker (1997)
Palearctic Israel Mumcuoglu & Braverman (2010)
Palearctic France Niogret et al. (2006)
Nearctic Canada Beresford & Sutcliffe (2009)
Macrocheles bertrandi Niogret & Nicot,2008 Afrotopical Gabon Niogret & Nicot (2008)
Macrocheles ovoidalis Niogret & Nicot, 2008 Afrotopical Gabon Niogret & Nicot (2008)
Macrocheles glaber (J. Müller, 1860) Palearctic France Niogret et al. (2006)
Macrocheles perglaber Filipponi & Pegazzano, 1962 Palearctic France Niogret et al. (2006)
Digamasellidae Digamasellus sp. Palearctic UK McGarry & Baker (1997)
Halolaelapidae Halolaelaps sp. Palearctic UK McGarry & Baker (1997)
Halolaelaps sexclavatus (Oudemans, 1902) Palearctic Hungary present study
Protodinychidae Protodinychus sp. Palearctic UK McGarry & Baker (1997)
Eviphididae Thinoseius sp. Palearctic UK McGarry & Baker (1997)
Prostigmata Ereynetidae Ereynetes sp. Palearctic UK McGarry & Baker (1997)
Siteroptidae Pediculaster mesembrinae (Canestrini, 1881) Palearctic UK McGarry & Baker (1997)
Palearctic Hungary present study
Astigmata Winterschmidtiidae Procalvolia zacheri (Oudemans, 1929) Palearctic UK McGarry & Baker (1997)
Acaridae Acarus farris (Oudemans, 1905) Palearctic UK McGarry & Baker (1997)
Histiostomatidae Copronomia (=Bonomia) spherocerae Vitzthum, 1922 Palearctic UK McGarry & Baker (1997)
Histiostomatidae Myianoetus sp. Palearctic UK McGarry & Baker (1997)
Trombidiae Microtrombidiidae Trichotrombidium muscarum (Riley, 1878) Palearctic  Hungary present study
Table 1. Mites associated with stable flies.


The mite species most frequently collected from stable flies are Macrocheles subbadius and M. muscadomesticae (Scopoli, 1772). Both species use the fly only for transportation from one habitat to another. In general, most mite species reported from stable flies are phoretic, except Trichotrombidium muscarum, which is an obligate parasitic mite of Muscidae. Knowledge of mites associated with stable flies is fragmented, therefore we can expect to find more species in future. To help with their identification, we compiled a key to the known mites associated with stable flies.

Key to the known mites associated with stable fly

1. Stigmata present
...... 2

— Stigmata absent
...... 14

2. Stigmata close to coxae of legs
...... 3

— Stigmata close to gnathosoma
...... 12

3. Dorsal shield divided into two plates
...... 4

— Dorsal shield entire
...... 6

4. Anal opening large
...... Digamasellus sp., deutonymph

— Anal opening small
...... 5

5. Subcoxal setae, and setae on coxae II and III club-like
...... Halolaelaps sexcavatus, deutonymph

— Subcoxal setae, and setae on coxae II and III needle-like
...... Halolaelaps sp., deutonymph

6. Large and separate metapodal shields present
...... Protodinychus sp., deutonymph

— Large and separate metapodal shields absent
...... 7

7. Anal shield present
...... Thinoseius sp., deutonymph

— Ventrianal shield present
...... 8

8. Setae j1 short, smooth and robust
...... Macrocheles subbadius

— Setae j1 long and pilose
...... 9

9. All setae smooth, except j1 and J5
...... 10

— Some setae on dorsal shield pilose
...... 11

10. Dorsal setae shorter, length ¼ the distances between insertions of setae next behind
...... Macrocheles bertrandi

— Dorsal setae longer, length 1/2 the distances between insertions of setae next behind
...... Macrocheles glaber/Macrocheles perglaber*

11. Setae j3 and j4 pilose
...... Macrocheles muscadomesticae

— Setae j3 and j4 smooth
...... Macrocheles ovoidalis

12. Dorsal body with two large and some smaller shields
...... Trichotrombidium muscarum, larvae

— Dorsal body without visible shields
...... 13

13. Setae sc1 bulbous
...... Pediculaster mesemrinae, phoretic female

— Setae sc1 narrow, flagelliform and pilose
...... Ereynetes sp., tritonymph

14. Terminal eyes present
...... Procalviola zacheri, hypopi

— Terminal eyes absent
...... 15

15. Suckers present on coxal field I
...... Miyanoetus sp., hypopi

— Suckers absent on coxal field I
...... 16

16. Eye-like structure present on lateral margins of idiosoma
...... Bonomia spheroceratae, hypopi

— Eye-like structure absent on lateral margins of idiosoma
...... Acarus farris, hypopi

*Notes: The differences between the M. glaber and M. perglaber are very weak based on female morphology (Halliday 1986), but Mašán (2003) listed some characters (e.g. shape of some dorsal setae) of females, which can help to separate these two species. On the other hand, the level of individual variability is very high, therefore identification without the males seems to be impossible.

Acknowledgements

This study was supported by NKFIH 108663 and 115854.

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Article editorial history

Date received:
2018-05-29
Date accepted:
2018-11-30
Date published:
2018-12-19

Edited by:
Faraji, Farid

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© 2019 Kontschán, Jenő and Hornok, Sándor

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