Зоологический журнал, 2023, T. 102, № 3, стр. 310-316

STUDY AREA, MATERIALS AND COLLECTION METHODS

All material was collected in the Lazovsky State Nature Reserve in 2017–2020, which is situated in the eastsouthern part of the Primorye Territory, between the Kievka and Chernaya Rivers, on the southern spurs of Sikhote-Alin, occupying the meridional ridge of Zapovedny at a height of 600–900 m with peaks Chernaya, Nogievskaya, and others more than 1000 m. Rivers and springs are numerous and belong to several basins. Musson climate is softer on the sea coast and colder in mountain parts of the territory. Forests occupy more than 95% of the territory with the dominance of oak forests (Quercus mongolica, 64%). Forests dominated by Pinus koreana are situated only in the continental parts of the Reserve. Upper parts of ridges and hills are covered with spruce-fir forests. Valley forests with high plant biodiversity occur along big rivers. Vegetation changes from sea meadows to mountain beach wood and mountain meadows. The research team captured birds using mist nets in two localities, which were 50 km apart from each other (Fig. 1).

Fig. 1.

South of Primorye Territory: 1, 2 – localities of collecting birds.

Locality 1. Valley of the Proselochnaya River (43°01′ N, 134°07′ E).

Locality 2. Petrov Bay (133°48′ N, 133°48′ E).

Five mist nets (4 nets 12 m long and a net 9 m long, height 2.5 m) were used in May–August and 5–11–in September–November every year in both localities. Mist nets were used for 150 days (1237 mist/day for four years: 2017–299; 2018–407; 2019–261; 2020–270). A total of 3833 individual birds of 103 species were captured over four years. All captured birds were ringed and released into the wild. Nine nestlings of four species (Cecropis daurica, Hirundo rustica, Passer montanus, and Apus pacificus) were also sampled for collecting louse flies. Each bird taken from the mist net was transported into a special tent in a small fabric bag, where the plumage of each captured bird was thoroughly examined to search for louse flies. A total of 1184 specimens of louse flies were collected from 646 birds of 62 species. All the captured flies were preserved in 70% ethanol. To identify the louse flies species, the following literature resources were used: Theodor, Oldroyd, 1964; Maa, 1963, 1966, 1969; Grunin, 1970; Farafonova, 2001; Doszhanov, 2003; Iwasa, Choi, 2013. The Latin names of birds are given according to Koblik and Arkhipov (2014).

RESULTS

The results for each year are presented separately as the collecting period and the number of sampled birds and their parasitic louse flies varied every year.

2017. Birds were captured over 35 days: 7 days in July, 11 days in September, 14 days in October, and 3 days in November. A total of 1161 birds of 55 species were captured and examined. It was found that 104 birds (8.96%) of 32 species were parasitised by louse flies of 7 species. Most specimens of infected birds were captured in July and September. Twenty-three species of examined birds were free from parasites. Twenty-seven species of birds were infected by Ornithoica momiyamai Kishida 1932, the most common parasite. Ten species of birds were infected by Ornithomya avicularia (L. 1758) s. l., the second most abundant parasite. Most species of birds were infected by one or two species of louse flies. Only four species of birds, Parus minor, Sitta europaea, Cristemberiza elegans, and Ocyris spodocephalus were infected by three species of louse flies. Most specimens of louse flies were collected from Sitta europaea and Cristemberiza elegans, representing 26 and 21 specimens of louse flies respectively. The degree of infection for different species of birds varied; for example, two individuals of Cristemberiza elegans were investigated and both presented louse flies, while only two out of 444 individuals of Aegithalos caudatus had louse flies. Only one individual of Paradoxornis webbianus was infected from 56 investigated specimens and only 12 out of 111 individuals of Zosterops erythropleurus were parasitised. Luscinia sibilans, Phylloscopus tenellipes, and Cristemberiza elegans were infected by two species of common mammal parasites, Lipoptena cervi (L. 1758) and L. fortisetosa (Maa, 1965).

2018. Birds were captured over 56 days: 6 days in May, 10 days in July, 8 days in August, 16 days in September, 14 days in October, and 2 days in November. A total of 1443 birds from 79 species were captured and examined. Thirty-three bird species were parasite-free. Only 296 specimens of 46 species of birds were infected (20.51%) by 7 species of louse flies. Louse flies were found on 10 species of birds on which they not were found in 2017. Thirty-seven species of birds were infected by Ornithoica momiyamai, the most numerous louse flies as in 2017. Twenty-four species of birds were infected by Ornithomya avicularia, the second most abundant louse fly. Only 3 species of birds were infected by Ornithoica unicolor Speiser 1900. Usually, a single species of louse fly was found on a specimen of bird, seldom two or three species. Sitta europaea was strongly infected: 85 louse flies of two species were taken from 29 examined birds. Parus minor, P. palustris, Phylloscopus coronatus, Turdus hortulorum, Motacilla cinerea, and Picus canus were infected by three species of louse flies. Cecropis daurica and Delichon urbica lagopodum were infected by monoxenous louse fly species Ornithomya comosa (Austen 1930) and Crataerina hirundinis (Linnaeus 1758). Parus palustris and Streptopelia orientalis were infected by the common mammal parasite Lipoptena cervi.

2019. Birds were sampled over 29 days: 3 days in May, 3 days in July, 7 days in August, 12 days in September, and 4 days in October. A total of 940 birds of 67 species were captured. 173 birds of 33 species were infected (18.40%) by 5 species of louse flies. 24 species of birds were infected by the most abundant louse fly Ornithoica momiyamai, 9 species of birds were infected by O. unicolor, and 22 species of birds were infected by Ornithomya avicularia. Usually, a single species of louse fly was found on a single species of bird, seldom two or three species. Sitta europaea was infected by 4 species of louse flies; 60 louse flies were taken from 27 birds. The highest number of louse flies were found on Ural Owl (Strix uralensis) – 77 flies belonging to two species from 5 examined birds, 73 of these louse flies were Ornithoica unicolor. One specimen of the common mammal parasite Lipoptena cervi was found on Phylloscopus schwarzi.

2020. Birds were sampled over 30 days: 8 days in July, 10 days in August, 8 days in September, and 4 days in October. A total of 289 birds of 47 species were captured. Louse flies belonging to 7 species were found on 73 birds of 25 species (25.26%). 16 species of birds were infected by Ornithoica momiyamai and 17 species by Ornithomya avicularia. A female Ornithomya comosa, a monoxenous parasite of Hirundinidae was found on the accidental host Parus palustris. As in preceding years, usually, only one or two species of louse flies were found on a species of bird. Three species of louse flies were taken from Cristemberiza elegans and Turdus hortulorum and four species of louse flies from Parus palustris. The highest number of louse flies were found on Turdus hortulorum – 40 specimens on 7 examined birds. The common mammal parasite Lipoptena fortisetosa was found on Cristemberiza elegans.

DISCUSSION

Birds of the following orders were investigated: Falconiformes 2 species, Galliformes 1, Charadriiformes 9, Columbiformes 1, Strigiformes 4, Apodiformes 1, Coraciiformes Piciformes 7, and Passeriformes 77 species. Six hundred forty-six birds (16.9% from captured and investigated) of 62 species were infected by louse flies: Falconiformes 2 species, Galliformes 1, Columbiformes 1, Strigiformes 2, Coraciiformes 1, Piciformes 4, Passeriformes 51 (Table 1). Passeriformes were the most numerous group of infected birds (82.25%), and no louse flies were found on 41 species of examined birds. Most birds were nesting, and 11 species were migrants: Anthus rubescens, Prunella montanella, Luscinia calliope, Muscicapa griseisticta, Ficedula albicilla, Phylloscopus borealis, Phylloscopus inornatus, Fringilla montifringilla, Ocyris rusticus, Ocyris personata, and Ocyris rutilus. Only two polyxenous species of louse flies (Ornithoica momiyamai and Ornithomya avicularia) were found on migrant birds. Migrant birds can transport louse flies north to their nesting sites.

The research team found differences in the number of species of louse flies and the number of collected specimens of louse flies for each sampled year, where a total of 1184 louse flies of 8 species were collected and determined. The most numerous polyxenous louse fly was Ornithoica momiyamai, parasitising 47 bird species, closely followed by the polyxenous louse fly Ornithomya avicularia, which parasitised 42 bird species. Ornithoica unicolor was the third most abundant louse fly, parasitising 11 bird species of different orders but showing a preference for Strigiformes. The fourth most abundant louse fly species was Ornithomya fringillina, which parasitised 11 bird species. The closely related species O. chloropus Bergroth 1901was not recorded, although it is well known in the Primorye Territory and Amur Province (Belousova, 2012; Meissner et al., 2020). The research team found the monoxenous louse fly Ornithomya comosa usually associated with Hirundinidae, on Parus palustris (Paridae). Records of louse flies on accidental hosts help to understand how infection of isolated populations of Hirundinidae by the monoxenous O. comosa happens. The species was originally recorded in India (Austen, 1930) and later in Malaysia, Nepal, and Thailand (Maa, 1977), Japan, Kazakhstan, Kirgizstan (Doszhanov, 2003), Russian Far East (Nartshuk et al., 2019a), West Siberia, Eastern Europe in 2013, and finally in the Kaliningrad Region of Russia, on the ornithological station of Curonian Spit (Nartshuk et al., 2019). Now the species occurs in West Europe (Le Guillou, Chapelin-Visardi, 2022).

Streptopelia orientalis, Luscinia sibilans, Phylloscopus schwarzi, and Parus palustris were accidental avian hosts of the mammophilous louse fly species Lipoptena cervi, while Phylloscopus tenellipes and Cristemberiza elegans were accidental avian hosts of the mammophilous louse fly Lipoptena fortisetosa. The range of L. fortisetosa, which is assumed to have Eastern Palaearctic origin, has remarkably expanded to the West. It is presumed to be associated with the introduction of the sika deer to Europe (Kurina et al., 2019). In the authors’ opinion, transportation by birds must not be ruled out.

Considerably more female than male louse flies were found on birds. Infected birds were prevalent in July and September. The degree of infection significantly varied between bird species. Two individuals of Cristemberiza elegans were examined, and louse flies were found on each; out of the 444 Aegithalos caudatus individuals examined, only two birds were infected. Only one individual of Paradoxornis webbianus was infected out of 56 examined ones. The largest numbers of louse fly specimens, 26 and 21 respectively, were collected from Sitta europaea and Cristemberiza elegans. Of 111 examined birds Zosterops erythropleurus, only 12 were infected. Four species of louse flies were found only on Sitta europaea. Most specimens of louse flies were found on Strix uralensis–77 flies of two species from 5 examined birds, 73 of them were Ornithoica unicolor and four Ornithomya avicularia. It is known that Ornithoica unicolor prefers to feed on Strigiformes birds. Five birds of Strix uralensis were infected as follows: August 17, 2019–3 males and 3 females, September 2, 2019–11 males and 24 females, September 9, 2019–8 males and 15 females, September 13, 2019–1 male and 2 females, September 29, 2019–6 females. The thick and fluffy plumage of owls is favourable for the parasitism of louse flies. Sixty louse flies of four species were taken from 27 birds of Sitta europaea, 37 flies belonging to three species–on 15 birds of Turdus hortulorum, and 26 louse flies of two species on 19 birds of Cristemberiza elegans. Three species of louse flies were collected on Cristemberiza elegans and Turdus hortulorum, four species of louse flies on Parus palustris. Most louse flies were found on Turdus hortulorum–40 specimens on 7 examined birds. The distribution of polyxenous louse flies Ornithoica momiyamai and Ornithomya avicularia amongst individual birds was random. Monoxenous species O. comosa and Crataerina hirundinis, parasites of Hirundinea were found on each examined bird.