Sci Parasitol 12(4):203-209, December 2011 ISSN 1582-1366 ORIGINAL RESEARCH ARTICLE

Gamasid (, ) in the nest holes of three passerine species from Kamchia Mountain (Northeastern Bulgaria)

Rositsa D. Davidova , Viktor M. Vasilev

Faculty of Natural Sciences, University of Shumen “Ep. K. Preslavsky”, 115 Universitetsca Str., 9700 Shumen, Bulgaria. Correspondence: Tel. + 35954830495/225, Fax +35954830371, E-mail [email protected]

Abstract. A total of 726 specimens belonging to 5 gamasid species were found in nests of great tit Parus major , semi-collared flycatcher Ficedula semitorquata and Eurasian nuthatch Sitta europaea . The mites were present in 73.3% (n = 30) nests, averaging 24.2 specimens per nest. The species casalis and were established in the nests of all three examined bird species, Ornithonyssus sylviarum was found in nests of Parus major and Ficedula semitorquata , and Dermanyssus hirundinis and Hirstrionyssus musculi – only in nests of Parus major . The highest dominance and prevalence were recorded of the species Dermanyssus gallinae and Ornithonyssus sylviarum , which were found in 11 and 8 of the surveyed 30 nests respectively and constituted 89.8% of the total number of specimens collected. Host species and the localities in Bulgaria where the studied mite species have been found up to now is provided.

Keywords: Gamasida; Bird; Dominance; Prevalence. Received 13/12/2011. Accepted 24/12/2011.

Introduction characteristics of mites inhabiting in nests of specific bird species (Cyprich et al., 1992; The first studies on mites living in bird nests Krištofík et al., 1993; 2001; 2003; 2005; 2007; were carried out more than 70 years ago by 2009; Mašán and Krištofík, 1993; 1995; Fenda Nordberg (1936) (Ambros et al., 1992). Since and Pinowski, 1997; Gwiazdowicz et al., 1999; then the gamasid mites in the nests of various Tryjanowski et al., 2001; Bloszyk et al., 2005; bird species in Europe have been investigated Bajerlein et al., 2006; Fenda and Kicková, 2009). by many authors. A part of the research on this subject is essentially faunistic in character or The gamasid mites in the nests of great tit discuss the structure of mite communities in (Parus major) have been studied by several different regions and countries (Borisova, 1977; authors. Ambros et al. (1992) investigated 69 Philips, 1981; Zeman and Jurik, 1981; Haitlinger, nests of great tit from Bratislava and recorded 1987; Ambros et al., 1992; Salmane, 2001; 11 species of Gamazida in 14 of them. Švaňa et Švaňa et al., 2006). Many authors focus their al. (2006) found five gamasid species in nests of works on a detailed study of ecological Parus major in SW Slovakia.

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Some data on mites occurring in the nests of without covering. The Sitta europaea is Eurasian nuthatch (Sitta europaea) in Europe widespread species in Europe, mostly in forests. have been published by Ambros et al. (1992). The nests were built from dry pieces of leaves The authors analised four nests of Sitta with sizes 1.5 to 2 X 2 to 2.5 cm, without europaea and found one specimen of Parasitidae covering. – Pergamasus brevicornis . All of the nest material was collected from There is no study of gamasid mites in nests of wooden nest boxes. The nest boxes were set up semi-collared flycatcher (Ficedula in deciduous forest dominated by hornbeam semitorquata). However there is information on (Carpinus betulus) and oak (Quercus sp.). All mesostigmatic mites in nests of two other boxes were made of untreated wood (mainly European flycatchers. Ambros et al. (1992) pine). Over 90% of the nest boxes were located recorded 4 gamasid mites in nest boxes of F. about 4m above the ground, on tree trunks. In albicollis . Madej and Stañska (1999) found 12 the natural hollows nest the same species that mite species in nests of collared flycatcher (F. were found in the artificial nests. albicollis) and pied flycatcher (F. hypoleuca). Švaňa et al. (2006) found two species of In the laboratory the mites were extracted from Gamazida in nests of F. albicollis . the nests in Tulgren’s funells, according to Krantz, 1978 (by Hartini and Saim, 2005). After The Bulgarian gamasid mite fauna, inhabiting that, a manual search of nests was done under a nests of birds, is poorly studied. Koyumdjieva is stereomicroscope and all ectoparasites were the only one who have investigated nest collected. The collected individuals were inhabiting Gamasids. In a nest of Eurasian green preserved in 75% ethanol. Temporary whole woodpecker Picus viridis the author (1979) mounts were made in lactophenol in order to discovered a new species of family Laelaptidae - examine the specimens using a microscope. Hypoaspis (Stratiolaelaps) gibbosus (Koyumdjieva, 1981). Later Koyumdjieva Species identification was made according to (1981) analyzed 25 nests from 11 bird species Bregetova (1956), Till (1963) and Roy and in southwestern Bulgaria and found a total of 22 Chauve (2009). mites belonging to 6 families of Gamasida. The material of gamasid mites was analysed, Here we present some first results of study on according to Margolis et al. (1982) (by Krištofík the gamasid mites in nests of Parus major , et al., 2007) considering the following indices: Ficedula semitorquata and Sitta europaea in prevalence (P%) (percentage of nests in which Bulgaria. the species occurred) and dominance (D%) (ratio of the number of individuals of every Material and methods species to the number of all the individuals, in percent). According to their dominance the The material was collected in 2009, after the species were divided into 5 groups: eudominant birds finished nesting. The investigation was (>10%); dominant (5–10%); subdominant (1– conducted in a study area near the village of 5%); recedent (0.5–1%), and subrecedent Goritsa, Varna District, Kamchia Mountain (<0.5%). (Northeastern Bulgaria) (42°55'6.37" N, 27°49'15.64" E) (figure 1). Results and discussion

The Parus major is a widespread species in A total of 726 specimens belonging to 5 parks, gardens and forests of Europe. The nests mesostigmatic mite species were found in the were built from moss, twisted hair, mainly from collected material from 30 nests of Parus major , the badger, deer and vague and single feathers Ficedula semitorquata and Sitta europaea (table from other birds. The Ficedula semitorquata is 1). The mites were present in 22 (73.3%) of distributed mainly in Bulgaria, Greece, Turkey. nests. The average number of specimens per The nests were built from woven dry grass 10- nest was 24.2 (1-163). 15 cm in length and about 0.5 cm in width,

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Figure 1. Location of the sampling sites (▪▪▪▪ )

Table 1. Number of specimens, dominance and prevalence of gamasid mites found in the investigated nest boxes

Parus major Ficedula semitorquata Sitta europaea Number of (great tit) (semi-collared flycatcher) (eurasian nuthatch) specimens N D% P% N D% P% N D% P% Androlaelaps casalis 6 1.04 10.53 1 0.96 14.29 3 6.98 25 10 (Berlese, 1887) Dermanyssus gallinae 339 58.55 47.37 8 7.69 14.29 40 93.02 25 387 (De Geer, 1778) Dermanyssus hirundinis 11 1.90 5.26 ------11 (Hermann, 1804) Hirstio nyssus musculi 53 9.15 15.79 ------53 (Johnston, 1849) Ornithonyssus sylviarum (Canestrini and Fanzago, 170 29.36 26.32 95 91.35 42.86 - - - 265 1877) Number of collected nests 19 7 4 30 Number of nests with 16 4 2 22 gamaside mites Number of spe cies 5 3 2 5 Number of specimens 579 104 43 726 Average number of 30.47 14.86 10.75 24.2 specimens per nest Average number of specimens in nest with 36.19 26 21.5 33 mites

The mite species found in the nests, according to predaceous mite – Hirstrionyssus musculi with their relation to the host, belong to three dominance 7.3% and prevalence 10.0% (figure ecological groups. The first group are obligatory 2). haematophagous ectoparasites – Dermanyssus gallinae, D. hirundinis and Ornithonyssus 19 out of 30 nest boxes which were occupied, sylviarum , with total dominance 91.3% and were inhabited by Parus major , 7 – by Ficedulla prevalence 66.7%. The nidicol species semitorquata and 4 – by Sitta europea . In some Androlaelaps casalis is in the second group. It of the artificial nests are placed permanently or does not have a trophic relation to nesting birds temporarily dormice. Most often this is the (Krištofík et al., 2007) and was sparsely forest dormouse Dryomys nitedula , but one represented in nests. Its dominance and occasion is great dormouse Glis glis . prevalence in all investigated nests was 1.4% and 13.3% respectively. A representative of the third ecological group is a free-living

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60 were found only in one of the nests and had a 53,31 Dominance, % 50 Prevalence, % 25.0% prevalence. The average number of specimens per nest was 21.5. 40 36,67 36,50

30 26,67 Short information about the mite species found, their hosts and localities is given below. 20 13,34 10,00 10 7,30 Family LAELAPTIDAE Berlese, 1892 3,34 1,52 1,38 0 Dermanyssus Dermanyssus Ornithonyssus Androlaelaps Hirstionyssus • Androlaelaps casalis (Berlese, 1887) gallinae hirundinis sylviarum casalis musculi

A. casalis is facultative parasite of birds with Figure 2. Dominance and prevalence of gamasid cosmopolitan distribution. It is found in mites in all investigated nests association with a wide variety of birds and their nests and can be abundant in poultry 579 specimens belonging to 5 species of houses (Bregetova, 1956; Till, 1963; Philips, gamasid mites were found in 19 examined nests 1981; Zeman and Jurik, 1981; Ambros et al., of P. major . In 16 (84.2%) of the studied nests, 1992; Madej and Stañska, 1999; Krištofík et al., mites occurred. The average number of 2003; 2007; Švaňa et al., 2006). specimens in mite inhabited nests was 36.2. Two species were dominant, Dermanyssus This species was for the first time found in gallinae (58.6%) and Ornithonyssus sylviarum Bulgaria by Mrciak (1959) in the Pirin Mountain (29.4%). They can be classified as eudominant. on A. flavicollis (Koyumdjieva, 1971a). Single Hirstrionyssus musculi (9.2%) was dominant, specimens of the species have been found on and from the other two species only fewer small mammals in Rila Mountain (Koyumdjieva, specimens were found and they belonged to the 1971a), reported under the name Haemolaelaps group of subdominants. The highest prevalence fenilis and in the Varna district (Sarbova and were recorded again in the species D. gallinae Koyumdjieva, 1973), reported as Haemolaelaps (47.4%) and O. sylviarum (26.3%), which were casalis . It has been found also in moss, pine found in 9 and 5 of the studied nests wood and hollow oak in the Rhodope Mountains respectively. The rest of the species were found (Koyumdjieva, 1983). In birds nest the species is only in 3 – H. musculi , 2 – Androlaelaps casalis or reported only once in Bulgaria – in the region of 1 – Dermanyssus hirundinis of the nests and had Smolyan, where it has been found in a nest of significantly lower prevalence (table 1). Lophophanes cristatus (Koyumdjieva, 1981).

The total number of gamasid mite specimens In the present study A. casalis was found in found in nests of F. semitorquata was 104 from nests of the three birds studied in a small 3 species – Dermanyssus gallinae, Ornithonyssus number of individuals (table 1). sylviarum and Androlaelaps casalis . The mites were present in 4 of 7 nests (57.1%). The Family DERMANYSSIDAE Koleant, 1859 average number of specimens in mite inhabited nests was 26.0. With the greatest number of • Dermanyssus gallinae (De Geer, 1778) individuals and most frequent was O. sylviarum . It was found in three of the surveyed nests D. gallinae is one of the most common blood- (prevalence 42.9%). To this species belong feeding nest mite and has a cosmopolite 91.4% of all specimens found in the nests and it distribution. It is often found hidden in the was eudominant. cracks and crevices of poultry houses during the day and comes out to feed on birds at night. From 4 nests of S. europaea , only in two gamasid About a 30 bird species as hosts, from 12 bird mites were found (50.0%). 43 specimens of families and eight orders are known to be Dermanyssus gallinae and Androlaelaps casalis parasitized by D. gallinae (Ambros et al., 1992; were collected from them. Almost all specimens Cyprich et al., 1992; Madej and Stañska, 1999; belonged to D. gallinae (93.0%). These species Krištofík et al., 2003; Švaňa et al., 2006; Fenda

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and Kicková, 2009; Roy and Chauve, 2009; Roy necked mouse Apodemus flavicolis in the Varna et al., 2009). district. There is no data about the occurrence of O. sylviarum in nests of birds in Bulgaria. In Bulgaria the species was found in single specimens in nests of Sturnus vulgaris near In the present study the species was found in Sofia, Troglodytes troglodytes in the region of nests of Parus major and Ficedula semitorquata , Pamporovo, Picus viridis and Motacilla alba in where it occurred frequently with a high Kyustendil district, Delichon urbica and Passer number of specimens (table 1). domesticus in the region of Petrich (Koyumdjieva, 1981). Family HIRSTIONYSSIDAE Evans et Till, 1966

In the present investigation D. gallinae was • Hirstionyssus musculi (Johnston, 1849) found in nests of all species studied. It was most frequent in nests of Parus major and Sitta It is a common parasite of rodents, with europaea (table 1). cosmopolite distribution (Bregetova, 1956). Ambros et al. (1992) found one specimen of H. • Dermanyssus hirundinis (Hermann, 1804) musculi in nest of Parus major which had been visited of yellow-necked mouse Apodemus The fowl mite D. hirundinis is a blood-feeding, flavicolis . nest-dwelling ectoparasite with a cosmopolitan distribution that infests both domesticated and In Bulgaria this species has been found on small wild birds. D. hirundinis has a rather broad host mammals in different regions – Gotse Delchev spectrum, as it has up to 40 bird species as by Sarbova (1962), Plovdiv district by Rossitskii hosts, from over 18 families and nine orders et al. (1962), Sarbova and Christov (1966) (Krištofik et al., 1993, 2007; Salmane, 2001; (Beron, 1974), Vitosha mountain (Koyumdjieva, Švaňa et al., 2006; Roy and Chauve, 2009). 1967), Western Balkan Range (Koyumdjieva, 1968), Pirin (Koyumdjieva, 1971a), the region of In Bulgaria the species have been found with the Srebarna reserve (Koyumdjieva, 1971b), the single specimens in nests of Hirundo rustica and vicinity of village Rezovo, Bourgas district Delichon urbica in the region of Petrich (Koyumdjieva, 1973), in the Varna district (Koyumdjieva, 1981). (Sarbova and Koyumdjieva, 1973), Sofia district (Koyumdjieva, 1974), the Ropotamo and In the current research D. hirundinis was found Parangalica reservs (Koyumdjieva, 1978). There in one nest of Parus major with a small number is no data about the occurrence of this mite in of individuals (table 1). birds nests in Bulgaria.

Family MACRONYSSIDAE Oudemans, 1936 In the current research H. musculi was found in three nests of Parus major with a small number • Ornithonyssus sylviarum (Canestrini & of individuals (table 1). Probable reason for the Fanzago, 1877) ocurrence of this species is previous use of these nests by rodents. An evidence for that is the O. sylviarum is one of the most common blood- finding of faeces of Dryomys nitedula in the feeding nest mites. It breeds among the feathers nests. of the host and may complete development without leaving the host. It occurs throughout Acknowledgements the temperate regions and is typically found on both domestic fowl and wild bird species This study was carried out under a project (Ambros et al., 1992; Krištofík et al., 2003; 2005; №D002-191/17.12.08 supported by the 2007; Švaňa et al., 2006; Knee and Proctor, Bulgarian National Science Fund. We wish to 2007; Mullens et al., 2009). thank the colleagues: Dr Mihaela Ilieva and Dr Pavel Zehtindzhiev (Institute of Biodiversity and In Bulgaria Sarbova and Koyumdjieva (1973) Ecosystem Research, Sofia) for their insightful found one specimen of O. sylviarum on yellow-

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