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Two parasitic mite species on Phlebotominae sand flies (Diptera: Psychodidae) from Türkiye: Biskratrombium persicum (Microtrombidiidae) and Eustigmaeus johnstoni (Stigmaeidae)


Abstract and Figures

Sand flies (Diptera: Psychodidae) are biological vectors for Leishmania species, which are health problems for humans and animals, bacteria such as Bartonella baciliformis, and various viruses belonging to the arboviruses such as Phlebovirus, the families Flaviviridae and Reoviridae. They are also known to be in contact with entomoparasites, such as various nematodes, mites and fungi. For a faunistic study, sand flies were collected by CDC light traps set up in various localities within the scope of two separate field studies carried out in Muğla and Adana provinces, Türkiye. During this study, two ectoparasitic mite species, Eustigmaeus johnstoni Zhang and Gerson on Phlebotomus tobbi Adler, Theodor and Lourie in Muğla province and Biskratrombium persicum Majidi, Hahiqanbar and Saboori (Microtrombidiidae) on Phlebotomus alexandri (Sinton, 1928) in Adana province, were observed from Türkiye. More detailed studies are needed since there are not enough studies about parasitic mites belonging to different families that can infest sand flies, their hosts, and the damage caused by these mites.
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Acarological Studies
Vol 5 (1): 11-16
doi: 10.47121/acarolstud.1209774
Two parasitic mite species on Phlebotominae sand flies (Diptera: Psychodidae) from Türkiye:
Biskratrombium persicum (Microtrombidiidae) and Eustigmaeus johnstoni (Stigmaeidae)
Metin PEKAĞIRBAŞ1,6 , Mehmet KARAKUŞ2 , Ayda YILMAZ3 , Özge EŞÖZ KASAP3 , Sevgi SEVSAY4 , Yusuf
ÖZBEL5 , Seray TÖZ5 , Salih DOĞAN4
1Department of Parasitology, Faculty of Veterinary, Aydın Adnan Menderes University, Aydın, Türkiye
2Department of Medical Microbiology, Hamidiye Faculty of Medicine, University of Health Sciences, Istanbul, Türkiye
3Department of Biology, Ecology Section, Faculty of Science, VERG Laboratories, Hacettepe University, Ankara, Türkiye
4Department of Biology, Faculty of Arts and Sciences, Erzincan Binali Yıldırım University, Erzincan, Türkiye
5Department of Parasitology, Faculty of Medicine, Ege University, İzmir, Türkiye
6Corresponding author:
Received: 25 November 2022 Accepted: 20 December 2022 Available online: 30 January 2023
ABSTRACT: Sand flies (Diptera: Psychodidae) are biological vectors for Leishmania species, which are health problems
for humans and animals, bacteria such as Bartonella baciliformis, and various viruses belonging to the arboviruses such
as Phlebovirus, the families Flaviviridae and Reoviridae. They are also known to be in contact with entomoparasites, such
as various nematodes, mites and fungi. For a faunistic study, sand flies were collected by CDC light traps set up in various
localities within the scope                
study, two ectoparasitic mite species, Eustigmaeus johnstoni Zhang and G erson on Phlebotomus tobbi Adler, Theodor and
   province and Biskratrombium persicum Majidi, Hahiqanbar and Saboori (Microtrombidiidae) on
Phlebotomus alexandri (Sinton, 1928) in Adana province, we   
since there are not enough studies about parasitic mites belonging to different families that c an infest sand flies, their
hosts, and the damage caused by these mites.
Keywords: Acari, country record, host record, parasitic association, Prostigmata.
Zoobank: -837D-434D-B1F6-AE55C6B29A39
Sand flies (Diptera: Psychodidae) are biological vectors
for the species of Leishmania which have a health concern
for humans and animals, bacteria such as Bartonella bacil-
iformis, and various viruses belonging to the arboviruses
such as Phlebovirus, Flaviviridae and Reoviridae families
(Ready, 2013). They are also known to be in associated
with entomoparasites such as various nematodes, mites
15 different families of mites have been identified on sand
flies, including Microtrombidiidae and Stigmaeidae which
are usually attached to the exoskeleton of adult flies and
their presence c an be determined from visible scars
(Majidi et al., 2020). Some of the aforementioned organ-
isms have lethal effects on sand flies, reducing their lifes
pan or reproductive capacity. There are not enough stud-
ies on the mi tes that affect the life span of sand flies and
cause this condi tion, which c an also be defined as super-
parasitism (Lewis and MacFarlane, 1982; Gerson and
Smiley, 1990).
The mite family Stigmaeidae is represented by more than
600 species in the world (Fan et al., 2016, 2019; Beron,
2020). So far, 28 species of the genus Eustigmaeus Ber-
          
        
species of Eustigmaeus only parasitize sand flies (B adakh-
shan et al., 2013). Currently, six species of Eustigmaeus, E.
johnstoni Zhang and Gerson, 1995, E. gorgasi (Chaudhri,
1965), E. gammus (Chaudhri, 1965), E. parasiticus
(Chaudhri, 1965), E. dyemkoumai (Abonnenc, 1970), E.
lirellus (Summers and Price, 1961), have been detected on
sand flies in different studies conducted around the
world. Eustig maeus johnstoni, whose presence i n sand
    
          e-
ported to parasitize only Phlebotomus papatasi, P. alexan-
dri and P. longicuspis in the world (Shehata and Baker,
1996, Badakhshan et al., 2013., Majidi et al., 2019). In this
study, E. johnstoni was detected for the first time on a
host, an adult female of P. tobbi.
Trombidioidea constitutes the largest subgroup of terres-
trial Parasitengona. Microtrombidiidae belongs to this
superfamily (Wohltman et al., 2006). Some larval mem-
bers of the family Microtrombidiidae have previously
been observed as parasites on sand flies (Majidi et al.,
2020). Active postlarval stages (deutonymph and adult)
of this family are predators and feed on various arthro-
pods, so they may have economic importance (Robaux,
       
now, 13 genera belonging to the family Microtrombidi-
         
and Sevsay, 2020). The genus Biskratrombium is known
only from the larva ( Fan and Baker, 1993; Majidi et.,
2020). These larvae were reported as ectoparasites only
from phlebotomine s and flies. Two species belonging to
this genus; Biskratrombium coineaui larvae were reported
as ectoparasites on the adults of Phlebo tomus papatasi
from Algeria and another species B. persicum larvae were
observed as ectoparasites on the adults of Phleboto mus
Acarological Studies 5 (1): 11-16, 2023
alexandri, P. papatasi and Sergentomyia mervynae from
Iran (Fain and Izri, 1993; Majidi et al., 2020).
This study was prepared on the parasitic mites o bserved
during a study carried out to show the presence of Leish-
mania parasites by the microscopic and molecular meth-
ods in sand flies collected from Adac-
The main m aterial of the study constitutes the mite spec-
imens detected on the sand flies belonging to the genus
Phlebotomus, Eustigmaeus johnstoni and Biskratrombium
persicum. Ethics committee approval w as not required for
this study.
Collection and examination of sand flies
CDC (Jo hn W. Hock Co., Gainesville, FL, USA) light traps
were set up in various localities to collect sand flies as
         
(Dalaman-Kayadibi-   
 -Otluk-       
E). Light traps were set in the evening (6:00-8:00 PM) and
were collected the following morning (07:00-09:30 AM).
Sand flies c aught alive were taken from the traps with the
help of mouth aspirators and transferred to separate
resting bowls according to their collection localities. Head
and genitalia of the captured sand flies were cut and pre-
pared for species identification. Sand fly specim ens were
identified according to available morphological identifica-
tion keys (Lewis, 1982; Killick-Kendrick et al., 1991).
Midgut dissection of female sand flies was performed
under a stereo microscope (Olympus Co., Japan).
Examination of mite specimens
During the study, the obs erved mites were removed from
the sand fly body with a fine needle and washed in a peni-
cillin-streptomycin solution. The slide-mounting was
done in Swan solution (chloral hydrate-50 gr/acetic acid-
5 ml/Arabic gum-15 gr/glucose-3 gr, water-20 ml) (Arse-
rim et al., 2017). The mi tes detected on the sand flies
during midgut dissection were also identified according
to their morphological characters. Identification of the
specimens was carried out as described by Fain and Izri
(1993), Zhang and Gerson (1995), and Majidi et al.
Order Trombidiformes Reuter, 1909
Suborder Prostigmata Kramer, 1877
Superfamily Raphignathoidea Kramer, 1877
Family Stigmaeidae Oudemans, 1931
Genus Eustigmaeus Berlese, 1910
Eustigmaeus johnstoni Zhang and Gerson, 1995
Figure 1. A. Dorsal view of Eustigmaeus johnstoni (female), 400x, B. Scars on the lateral sides of the abdominal sternites
belongs to a Phlebotomus tobbi individual, 40x.
Sand flies collected during field studies in Adana were
dissected for species identification. During the dissection,
mite specimens were detected on some sand flies and
were examined. Accordingly, three adult females of
Eustigmaeus johnstoni (Fig. 1A) were identified on the
thorax of the adult female Phlebotomus tobbi during the
field study in Adana. The scars caused by E. johnstoni on
the lateral side of the abdominal tergites belongs to P.
tobbi individual were viewed under a stereo microscope
(Fig. 1B).
  i-
ye are completely similar to those of the known speci-
mens of E. johnstoni. Since the description of the species is
well and it has been previously recorded and described in
  not been repeated here.
Host information
Phlebotomus papatasi, S. magna, S. dreyfussi, S. africana, P.
longicuspis, P. bergeroti, P. sergenti, Sergentomyia clydei, S.
sintoni (Zhang and Gerson, 1995; Fan et al., 2016), and
newly recorded host P. tobbi (present study).
Acarological Studies 5 (1): 11-16, 2023
Cyprus, Egypt, India, Iran, Israel, Pakistan, Saudi Arabia,
       
         a-
        
2019; Majidi et al., 2019).
Order Trombidiformes Reuter, 1909
Suborder Prostigmata Kramer, 1877
Superfamily Trombidioidea Leach, 1815
Family Microtrombidiidae Thor, 1935
Genus Biskratrombium Fain and Izri, 1993
Biskratrombium persicum Majidi, Hajiqanbar and
Saboori, 2020
Biskratrombium persicum (Fig. 2) was determined as ec-
toparasitic on adult female Phlebotomus alexandri. The
      Biskratrombium
persicum by the presence of eupathidia on palpal tarsus;
the longest seta on palpal tarsus is not a solenidion; scu-
tum, scutellum and platelets smooth; setae on scutellum
       
Figure 2. Biskratrombium persicum (larva).
Short description
Cheliceral blade curved and simple. Palpfemur and
palpgenu without seta. Eyes absent. Scutum trapezoidal in
shape; lateral borders slightly concave, posterior border
convex, slightly concave at anterior border. Scutum with
three pairs of non-sensillary (AM, AL and PL) and one pair
of sensillary setae (S). The width of scutellum less than
the scutum, bearing one pair of barbed setae c1. Legs seg-
mentation formula: 666. Tarsi I and II each bearing only
two trifurcate claws, while tarsus III with two trifurcate
claws and a claw-like empodium.
Host information
Phlebotomus papatasi , P. alexandri and Sergen tomyia
mervynae (Majidi et al., 2020).
     
Various studies have been carried out on the distribution
of the genus Eustigmaeus in the world (Fan et al., 2016,
2019; Beron, 2020). To date, E. dyemkou mai, E. gamma, E.
gorgosi, E. parasitica, E. johnstoni and E. lirella species
have been detected on sand flies. In previous studies, it
has been reported that Phlebotomus alexandri, P. papatasi,
P. bergeroti, P. longicuspis and P. sergenti were hosts for E.
johnstoni (Chaudri, 1965; Abonnenc, 1970; Lewis and
Macfarlane, 1982; Zhang and Gerson, 1995; Ozbel et al.,
        
Majidi et al., 2019). In this study, the presence of E. john-
stoni was reported for the first time on adult female of
Phlebotomus tobbi , which is known to be the proven v ec-
tor of L. infantum   
for sucking blood from humans (Svobodova et al., 2009).
Eustigmaeus species have been detected on proven vector
sand fly species of different Leishmania parasites such as
P. alexandri, P. papatasi, P. sergenti, and P. longicuspis
(Zhang and Gerson, 1995; Yaghoobi-Ershadi et al., 2005;
Azizi et al., 2006, Berdjane-Brouk et al., 2012; Fan et al.,
2016), and i n this study showing the presence of Eustig-
maeus johnstoni on P. tobbi that is also proven vector
species of L. infantum. These findings suggest the possibil-
ity that Eustigmaeus species may show tropism to sand
flies that are vectors for Leishmania parasites.
Sand flies spend most of their lives in dark and damp
areas such as animal shelters, wall cracks and crevices,
and rodent burrows (Dinesh et al., 2014). Since immature
Eustigmaeus has not been reported on sand flies so far, it
is thought that the development and m ating of the
abovementioned mite took pl ace in these habitats. The
relationship between the mite-fly pair encountered in
these habitats is supported by few publications showing
          
al., 2013; Dinesh et al., 2014). Although there are different
opinions about whether the relationship between Eustig-
maeus johnstoni and sand flies is parasitic or phoretic
(Badakhshan et al., 2013), the scars o n the bodies of the
sand flies shown in the present study indicate parasitism.
Parasitic association between the parasitengone mites
and the sand flies is little reported probably due to low
frequency of the phenomenon (Majidi et al., 2020). Alt-
hough five microtrombidiids species, Microtrombidium
hindustanicum, M. nigeriense, M. lewisi, Kenyatrombium
macfarlanei, Biskratrombium coineaui, as ectoparasites
have been detected on the sand flies, only one species
belonging to the genus Biskratrombium has been detected
so far in the Phlebotominae sand flies around the world
(Hirst, 1926; Fain and Baker, 1993; Fain and Izri, 1993).
Biskratrombium persicum was described by Majidi et al.
(2020) as ectoparasite on P. alexandri. In this study, the
presence of a larval stage, ectoparasitic of adult female P.
Acarological Studies 5 (1): 11-16, 2023
alexandri which is most third prevalent Phlebotomus spe-
             
genus Biskratrombium was reported for the first time in
There is a need for more detailed studies on issues that
lack information, such as the damage caused by parasitic
mites from different families infesting sand flies in differ-
ent parts of the world and their relations with the host.
Authors’ contributions
Metin Pekağırbaş: Field studies, dissection for sand flies,
writing-original draft. Mehmet Karakuş: Field studies,
dissection for sand flies writing-review & editing. Ayla
Yılmaz: Field studies, dissection of sand flies, identifica-
tion of sand flies, writing-review. Özge Erişöz Kasap:
Field studies, dissection of sand flies, identification of
sand flies, writing-review. Sevgi Sevsay: Identification of
the mites, writing-review & editing. Seray Töz: Field
studies, dissection of sand flies, identification of sand flies,
writing-review. Yusuf Özbel: Identification of sand flies
and editing of manuscript. Salih Doğan: Identification of
the mites, writing-review & editing.
Statement of ethics approval
Not applicable.
This work was supported by the the Scientific and Tech-
    
Conflict of interest
No potential conflict of interest was reported by the au-
          p-
port for the study. The authors also would like to thank
villagers who helped the study group find suitable sand
fly collection sites.
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Edited by: Adem Keskin
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Citation:                    2023. Two
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Trombidiid akarlar, larva döneminde çeşitli canlılar üzerinde parazit olarak yaşarlar. Trombidium holosericeum’un larvaları ilk kez Rhagionidae familyasına ait Rhagio sp.’dan, Trombidium brevimanum’un larvaları da ilk defa Neobisiidae familyasına ait Neobisium crassifemoratum (Beier 1928)’dan parazit olarak kaydedildi. Her iki türün bugüne kadar verilen konakçıları tartışıldı
Due to its geographical location, Muğla province is one of the most frequently used places by refugees. Although leishmaniasis have been previously reported in this region, there is a lack of information on the etiological agent and possible vectors. The main objectives of this study were; i) to investigate the sand fly fauna, ii) to reveal the natural Leishmania spp. infection in wild caught sand flies using molecular tools, and iii) to determine the annual seasonal dynamics of the sand flies in Muğla region. Totally, 2093 specimens belonging to 15 species [12 Phlebotomus, three Sergentomyia; 51 unidentified] were collected during the one-year (June 2016- June 2017) period. Of the collected sand flies, 1928 (92.12%) were caught by the Centers for Disease Control (CDC) light traps, while 165 (7.88%) of them were caught by sticky traps. Phlebotomus major sensu lato (s.l.), the potential vector of visceral leishmaniasis (VL) and canine leishmaniasis (CanL) in the Mediterranean and Aegean region, was detected in all sampling locations and found as the dominant taxon (n=1035; 49.45%) of the study area and followed by Phlebotomus tobbi (n=371; 17.72%). During the sampling period, sand fly activity was started in March and peaked in August. Sand fly population size reduced dramatically between mid-September and early October. The number of collected specimens was peaked in August, while there is only one sample collected both in November and March. The majority of the sand flies (78.66%) were collected at an altitude range of 200-400 m. Seventy-two monospecific pools were screened for the presence of Leishmania DNA by real time ITS1 PCR and 24 (nine P. major s.l., eight P. tobbi, two P. papatasi, two S. minuta, one P. alexandri, one P. similis, and one Phlebotomus (Transphlebotomus spp.) of them (33.8%) were found positive (L. infantum, L. tropica, and L. major). To the best of our knowledge, the presence of fifteen sand fly species and their distribution, seasonal dynamics, molecular detection of Leishmania parasites in Muğla province was reported for the first time. The presence of vector species in the study area, appropriate temperature and humidity conditions, long sand fly activity season, and presence of Leishmania parasite suggests that there is a serious risk in the transmission of leishmaniasis in Muğla.
Stigmaeid mites parasitizing phlebotomine sandflies were collected in Fars province, Southern Iran, during 2016–2017. The present study has revealed records of four species of stigmaeid mites, namely, Eustigmaeus johnstoni, Stigmaeus furcatus, Stigmaeus sinai, and Stigmaeus youngi. Among them, two species S. furcatus and S. youngi are recognized as new records for fauna of Iran. Meanwhile, S. furcatus is new report for mite fauna associated with sandflies in the world (S. furcatus is collected from sandflies for the first time in the world). Also, prevalence of stigmaeid mites on sandflies is evaluated. These parasitic mites were collected from phlebotomine sandflies comprising Phlebotomus (Paraphlebotomus) alexandri (Sinton), P. (Phlebotomus) papatasi (Scopoli), Sergentomyia (Sintonius) clydei (Sinton), Se. (Se.) sintoni Pringle, and Se. (Se.) theodori (Parrot). Moreover, wound scars resulting from mites’ activities have been observed on abdomen of infested sandflies.