A comprehensive survey of Rhinonyssid mites (Mesostigmata: Rhinonyssidae) in Northwest Russia: New mite-host associations and prevalence data.

BACKGROUND: Rhinonyssid mites are permanent parasites of birds that inhabit their respiratory tract. There are around 600 species described worldwide and almost all species of birds are found to have embedded rhinonyssid mites. Despite their presumed relevance, these mites are largely unstudied due to the difficulty in sampling them and, therefore, the majority of mite-host associations and species-prevalence data are unknown. NEW INFORMATION: In this study, 179 mite specimens belonging to 27 species and eight genera were identified. Notably, 18 new mite-bird associations were documented for the first time, thus increasing the known host range for these mite species. In addition, mite-host associations found in this study were compared with known associations from these species of birds in the European part of Russia and in Europe. Overall, this study represents the largest survey to date carried out on rhinonyssid mites in Russia and one of the most comprehensive datasets on rhinonyssid host-range. Manuel De Rojas, Jorge Doña, Ivan Dimov.

Introduction

Nasal mites of the family are permanent haematophagous endoparasites of birds that inhabit their respiratory tract (Vitzthum 1935; George 1961; Fain 1994; Dimov and de Rojas 2012). Most species live in the nasal cavity on the vascularised epithelial tissue; nevertheless, some species occupy the lungs, tracheal tissues and body cavity of their hosts (Lindquist et al. 2009; Krantz and Walter 2009). Rhinonyssids can not only cause damage to their hosts in a direct way () (Dimov 2011), but could also be reservoirs or vectors of other infections like West Nile fever, Q fever, avian influenza and Lyme disease, as have been shown in mites from the family (Reeves et al. 2006). Despite their ecological relevance, most aspects of the basic biology, ecology and evolution of these mites are still poorly understood. This lack of knowledge, amongst other reasons, is owing to their being very challenging to study; for example, due to most species having typically low prevalence on their hosts and being difficult to sample (being only possible to collect from dead birds).

The family currently includes about 600 described species arranged in eleven genera (Domrow 1969; Fain 1994; Dimov et al. 2015; Dimov 2018). In Parasitology, parasite host-specificity and prevalence are widely-studied parameters as they are informative of relevant processes, such as parasite degree of specialisation, population dynamics or transmission efficiency (Poulin 2011). Host specificity of rhinonyssid mites has been found to vary from one genus to another by surveys across different geographic areas (e.g. USA, Spicer 1987; Canada, Knee et al. 2008). In particular, some genera have been found to be constrained to a single host family, while others can inhabit hosts from different orders (Pence 1975; Butenko 1984). In addition, these studies have found that the prevalence of these mites varies across geographic areas (although the estimates may be biased by a low sample size; Spicer 1987). However, the host-specificity and prevalence of most rhinonyssid mites are still poorly understood, thus hampering further studies on the ecology and evolution of this host-parasite system.

In this study, 2,107 bird specimens from northwest of Russia, belonging to 75 species from 55 genera, 30 families and 10 orders were examined for rhinonyssid mites. The mites were identified and the prevalence (including confidence intervals to show how accurate the estimates are) of these species was calculated. Additionally, the mite-host associations, found in our study, were compared with the known rhinonyssids from these species of birds in the European part of Russia and Europe. Overall, this study represents the largest survey to date carried out on rhinonyssid mites in Russia and one of the most comprehensive datasets on rhinonyssid host-range and prevalence.

General description

Purpose

In this survey, 2,107 individual birds were collected in Russia representing 75 species belonging to 55 genera, 30 families and 10 orders and analysed for rhinonyssid mites. The mites were identified and the prevalence (including 95% confidence intervals to show how accurate the estimates are) of these species was calculated. Additionally, the mite-host associations found in our study were compared with the known rhinonyssids from these species of birds in the European part of Russia and Europe.

Sampling methods

Study extent

Individual birds were collected during four years (2010-2013).

Sampling description

Mites were collected from birds that died under various circumstances. Specifically, most of the surveyed hosts were birds found dead on the roads or that died because of high-voltage transmission lines. Host birds were morphologically classified according to Malchevsky and Pukinsky 1983. All the birds were examined for rhinonyssid mites and when they were found, a complete morphometrical study was conducted to identify each specimen (Butenko 1984; Pence 1975; Fain 1956; Dimov and de Rojas 2012; Dimov and Knee 2012; Dimov and Mironov 2012).

Quality control

The nasal cavity of birds was opened following Butenko's method (Butenko 1984), with some changes introduced by us. In particular, 1) the nasal cavity was opened with a scalpel and scissors under a binocular stereomicroscope. 2) The ossa mandibulae were removed along with the hyoid brush apparatus (apparatus hyobranchialis); the eyeballs were removed with tweezers. 3) Then, two incisions were made: a transverse incision in the region of the papillae pharyngeales and a medial incision, from the rima infundibuli (through the choana) to the ruga palatina mediana area. 4) Nostrils in the area of operculum were examined and then the os maxillare were opened. 5) Lastly, the maxillary bone was removed and the nasal cavity with three conchs was opened, including the largest of all rostral - concha nasalis rostralis, the middle - concha nasalis media and the caudal - concha nasalis caudalis. The examination of all nasal cavities was performed with tweezers and a dissecting needle under a binocular stereomicroscope. Rhinonyssid mites were placed in tubes with 70% ethanol for storage. Each tube was labelled with data on the type of host and a detailed description of the collection site. Mites were then cleared in lactic acid and mounted on slides with Fora-Berlese liquid, according to the generally-accepted technique for small mites (Walter and Krantz 2009; Krantz and Walter 2009). Finally, individual mites were identified, based on morphometrics analysis.

Geographic coverage

Description

Individual birds were collected across the northwest of the European part of Russia, mainly in the territory of the Leningrad Region, at 41 points and, to a lesser extent, in territories of Arkhangelsk, Kaliningrad and Pskov regions (Suppl. material 1; Table 2).

Table 2.

Data on the mite-host associations detected. Each row depicts an individual bird from mite-host associations, in which more than one mite was found. N = number of birds examined per mite-host association, Ni = Number of infected birds, I = number of mites isolated. Region (previous records) = NR: Northwest Russia, ER: European part of Russia, WE: Western Europe and * indicates a previously unrecorded mite host association. Note that values from N and Ni columns are duplicated between individual birds that belong to the same mite-host association.

Bird taxa	Mite species	N	Ni	I	Region (previous records)	Locality (this study)	Previous records
Accipiter nisus (Linnaeus, 1758)	NA	2	0	0	NA	NA	NA
Buteo buteo (Linnaeus, 1758)	NA	1	0	0	NA	NA	NA
Anas platyrhynchos Linnaeus, 1758	Rhinonyssus kadrae Dimov, 2013	38	1	2	NR*	Dubrovka, Leningrad Oblast, Russia	NA
Anas platyrhynchos Linnaeus, 1758	Rhinonyssus levinseni (Tragardh, 1904)	38	1	1	NR*	Volosovo, Leningrad Region, Russia	NA
Aythya nyroca (Güldenstädt, 1770)	Rhinonyssus nyrocae Butenko, 1971	1	1	1	NR, WE	Pskov, Pskov region, Russia	Butenko 1971, Butenko 1984
Somateria mollissima Linnaeus, 1758	Rhinonyssus polystictae Butenko, 1984	11	9	1	NR*	Ermilovo, Leningrad Region, Russia	NA
Somateria mollissima Linnaeus, 1758	Rhinonyssus polystictae Butenko, 1984	11	9	1	NR*	Ermilovo, Leningrad Region, Russia	NA
Somateria mollissima Linnaeus, 1758	Rhinonyssus polystictae Butenko, 1984	11	9	2	NR*	Ermilovo, Leningrad Region, Russia	NA
Somateria mollissima Linnaeus, 1758	Rhinonyssus polystictae Butenko, 1984	11	9	1	NR*	Ermilovo, Leningrad Region, Russia	NA
Somateria mollissima Linnaeus, 1758	Rhinonyssus polystictae Butenko, 1984	11	9	2	NR*	Ermilovo, Leningrad Region, Russia	NA
Somateria mollissima Linnaeus, 1758	Rhinonyssus polystictae Butenko, 1984	11	9	1	NR*	Ermilovo, Leningrad Region, Russia	NA
Somateria mollissima Linnaeus, 1758	Rhinonyssus polystictae Butenko, 1984	11	9	2	NR*	Ermilovo, Leningrad Region, Russia	NA
Somateria mollissima Linnaeus, 1758	Rhinonyssus polystictae Butenko, 1984	11	9	1	NR*	Ermilovo, Leningrad Region, Russia	NA
Somateria mollissima Linnaeus, 1758	Rhinonyssus polystictae Butenko, 1984	11	9	1	NR*	Ermilovo, Leningrad Region, Russia	NA
Anas crecca Linnaeus, 1758	Rhinonyssus subrhinolethrum Butenko, 1971	17	1	1	NR	Pikalevo, Leningrad Region, Russia	Butenko 1971, Butenko 1984
Caprimulgus europeus Linnaeus, 1758	Vitznyssus tsachevi Dimov et Rojas 2012	2	1	2	NR*	Pikalevo, Leningrad region, Russia	NA
Charadrius dubius Scopoli, 1786	Rhinonyssus bregetovae Butenko, 1974	27	3	4	NR	Voypala, Leningrad Region, Russia	Butenko 1984
Charadrius dubius Scopoli, 1786	Rhinonyssus bregetovae Butenko, 1974	27	3	2	NR	Voypala, Leningrad Region, Russia	Butenko 1984
Charadrius dubius Scopoli, 1786	Rhinonyssus bregetovae Butenko, 1974	27	3	1	NR	Voypala, Leningrad Region, Russia	Butenko 1984
Charadrius dubius Scopoli, 1786	Rhinonyssus neglectus Hirst 1921	27	1	1	NR*	Lavrovo, Leningrad Region, Russia	NA
Vanellus vanellus Linnaeus, 1758	Rhinonyssus dobromiri Dimov et Spicer, 2013	4	1	2	NR*	Leningrad Region, Russia	NA
Larus argentatus Pontoppidan, 1763	Larinyssus orbicularis Strandtmann, 1948	22	1	2	NR*	Voybokalo, Leningrad Oblast, Russia	NA
Larus ridibundus Linnaeus, 1766	NA	19	0	0	NA	NA	NA
Scolopax rusticola Linnaeus, 1758	NA	1	0	0	NA	NA	NA
Sterna hirundo Linnaeus, 1758	Larinyssus iohanssenae Dimov, 2013	17	2	1	NR*	Kronstad, Leningrad Region, Russia; Apraksin, Leningrad Region, Russia	NA
Sterna hirundo Linnaeus, 1758	Larinyssus iohanssenae Dimov, 2013	17	2	2	NR*	Kronstad, Leningrad Region, Russia; Apraksin, Leningrad Region, Russia	NA
Columba livia Gmelin, 1789	Mesonyssus columbae Crossley, 1950	262	5	3	NR, WE	St. Petersburg, Russia; Voybokalo, Leningrad Oblast, Russia; Slantsy, Leningrad Region, Russia; Luga, Leningradskaya, Russia; Radogosh, Leningrad Region, Russia	Butenko 1984; Cerny 1970; Crossley 1951; Domrow 1965; Domrow 1966a; Domrow 1966b; Fain 1956; Fain 1957; Fain 1958; Fain 1962b; Fain et al. 1974; Pence 1975; Sixl 1971; Wilson 1964; Wilson 1966; Zumpt and Till 1955
Columba livia Gmelin, 1789	Mesonyssus columbae Crossley, 1950	262	5	1	NR, WE	St. Petersburg, Russia; Voybokalo, Leningrad Oblast, Russia; Slantsy, Leningrad Region, Russia; Luga, Leningradskaya, Russia; Radogosh, Leningrad Region, Russia	Butenko 1984; Cerny 1970; Crossley 1951; Domrow 1965; Domrow 1966a; Domrow 1966b; Fain 1956; Fain 1957; Fain 1958; Fain 1962b; Fain et al. 1974; Pence 1975; Sixl 1971; Wilson 1964; Wilson 1966; Zumpt and Till 1955
Columba livia Gmelin, 1789	Mesonyssus columbae Crossley, 1950	262	5	2	NR, WE	St. Petersburg, Russia; Voybokalo, Leningrad Oblast, Russia; Slantsy, Leningrad Region, Russia; Luga, Leningradskaya, Russia; Radogosh, Leningrad Region, Russia	Butenko 1984; Cerny 1970; Crossley 1951; Domrow 1965; Domrow 1966a; Domrow 1966b; Fain 1956; Fain 1957; Fain 1958; Fain 1962b; Fain et al. 1974; Pence 1975; Sixl 1971; Wilson 1964; Wilson 1966; Zumpt and Till 1955
Columba livia Gmelin, 1789	Mesonyssus columbae Crossley, 1950	262	5	2	NR, WE	St. Petersburg, Russia; Voybokalo, Leningrad Oblast, Russia; Slantsy, Leningrad Region, Russia; Luga, Leningradskaya, Russia; Radogosh, Leningrad Region, Russia	Butenko 1984; Cerny 1970; Crossley 1951; Domrow 1965; Domrow 1966a; Domrow 1966b; Fain 1956; Fain 1957; Fain 1958; Fain 1962b; Fain et al. 1974; Pence 1975; Sixl 1971; Wilson 1964; Wilson 1966; Zumpt and Till 1955
Columba livia Gmelin, 1789	Mesonyssus columbae Crossley, 1950	262	5	3	NR, WE	St. Petersburg, Russia; Voybokalo, Leningrad Oblast, Russia; Slantsy, Leningrad Region, Russia; Luga, Leningradskaya, Russia; Radogosh, Leningrad Region, Russia	Butenko 1984; Cerny 1970; Crossley 1951; Domrow 1965; Domrow 1966a; Domrow 1966b; Fain 1956; Fain 1957; Fain 1958; Fain 1962b; Fain et al. 1974; Pence 1975; Sixl 1971; Wilson 1964; Wilson 1966; Zumpt and Till 1955
Columba livia Gmelin, 1789	Mesonyssus melloi Castro, 1948	262	3	4	NR, WE	St. Petersburg, Russia; Voybokalo, Leningrad Oblast, Russia; Slantsy, Leningrad Region, Russia.	Butenko 1984; Castro 1948; Domrow 1966a; Domrow 1969; Domrow 1972a; Domrow 1972b; Fain 1959; Fain 1962b; Pence 1979; Sixl 1969; Wilson 1964; Wilson 1966; Zumpt and Till 1955
Columba livia Gmelin, 1789	Mesonyssus melloi Castro, 1948	262	3	4	NR, WE	St. Petersburg, Russia; Voybokalo, Leningrad Oblast, Russia; Slantsy, Leningrad Region, Russia.	Butenko 1984; Castro 1948; Domrow 1966a; Domrow 1969; Domrow 1972a; Domrow 1972b; Fain 1959; Fain 1962b; Pence 1979; Sixl 1969; Wilson 1964; Wilson 1966; Zumpt and Till 1955
Columba livia Gmelin, 1789	Mesonyssus melloi Castro, 1948	262	3	2	NR, WE	St. Petersburg, Russia; Voybokalo, Leningrad Oblast, Russia; Slantsy, Leningrad Region, Russia.	Butenko 1984; Castro 1948; Domrow 1966a; Domrow 1969; Domrow 1972a; Domrow 1972b; Fain 1959; Fain 1962b; Pence 1979; Sixl 1969; Wilson 1964; Wilson 1966; Zumpt and Till 1955
Cuculus canorus Linnaeus, 1758	Sternostoma zini Dimov et Knee, 2012	13	1	2	NR*	Vyritsa, Leningrad Region, Russia	NA
Coturnix coturnix Linnaeus, 1758	NA	31	0	0	NA	NA	NA
Tetrao urogallus Linnaeus, 1758	NA	1	0	0	NA	NA	NA
Gallinula chloropus Linnaeus, 1758	Rallinyssus caudistigmus Strandtmann, 1948	6	1	3	NR, WE	Gatchina, Leningrad Region, Russia; Sosnovy Bor, Leningrad Region, Russia	Domrow 1966a; Domrow 1969; Fain 1957; Fain et al. 1974; Pence 1975; Strandtmann 1948
Fulica atra Linnaeus, 1758	Rallinyssus caudistigmus Strandtmann, 1948	2	1	2	NR, ER, WE	Gatchina, Leningrad Region, Russia; Sosnovy Bor, Leningrad Region, Russia	Bregetova 1951; Butenko 1984; Domrow 1966a; Domrow 1969; Fain 1957; Fain 1959; Fain et al. 1974; Pence 1972d; Pence 1975; Strandtmann 1948
Alauda arvensis Linnaeus, 1758	Ptilonyssus schumili Butenko et Lavrovskaya, 1980	35	6	2	NR, ER	Rjbachii, Leningrad Region, Russia	Butenko and Lavroskaya 1980a; Butenko and Lavroskaya 1980b
Alauda arvensis Linnaeus, 1758	Ptilonyssus schumili Butenko et Lavrovskaya, 1980	35	6	1	NR, ER	Rjbachii, Leningrad Region, Russia	Butenko and Lavroskaya 1980a; Butenko and Lavroskaya 1980b
Alauda arvensis Linnaeus, 1758	Ptilonyssus schumili Butenko et Lavrovskaya, 1980	35	6	2	NR, ER	Rjbachii, Leningrad Region, Russia	Butenko and Lavroskaya 1980a; Butenko and Lavroskaya 1980b
Alauda arvensis Linnaeus, 1758	Ptilonyssus schumili Butenko et Lavrovskaya, 1980	35	6	1	NR, ER	Rjbachii, Leningrad Region, Russia	Butenko and Lavroskaya 1980a; Butenko and Lavroskaya 1980b
Alauda arvensis Linnaeus, 1758	Ptilonyssus schumili Butenko et Lavrovskaya, 1980	35	6	1	NR, ER	Rjbachii, Leningrad Region, Russia	Butenko and Lavroskaya 1980a; Butenko and Lavroskaya 1980b
Alauda arvensis Linnaeus, 1758	Ptilonyssus schumili Butenko et Lavrovskaya, 1980	35	6	2	NR, ER	Rjbachii, Leningrad Region, Russia	Butenko and Lavroskaya 1980a; Butenko and Lavroskaya 1980b
Aegithalos caudatus Linnaeus, 1758	NA	9	0	0	NA	NA	NA
Bombycilla garrulus Linnaeus, 1758	NA	1	0	0	NA	NA	NA
Corvus cornix Linnaeus, 1758	NA	38	0	0	NA	NA	NA
Garrulus glandarius Linnaeus, 1758	NA	3	0	0	NA	NA	NA
Pica pica Linnaeus, 1758	NA	32	0	0	NA	NA	NA
Emberiza citrinella Linnaeus, 1758	NA	29	0	0	NA	NA	NA
Emberiza hortulana Linnaeus, 1758	NA	1	0	0	NA	NA	NA
Emberiza rustica (Pallas, 1776)	NA	5	0	0	NA	NA	NA
Emberiza schoeniclus Linnaeus, 1758	NA	2	0	0	NA	NA	NA
Acanthis canabina Linnaeus, 1758	NA	28	0	0	NA	NA	NA
Acanthis flammea Linnaeus, 1758	NA	7	0	0	NA	NA	NA
Fringilla coelebs Linnaeus, 1758	Ptilonyssus hirsti (Castro et Pereira, 1947)	71	11	1	NR*	Grjazno, Kaliningrado Region, Russia	NA
Fringilla coelebs Linnaeus, 1758	Ptilonyssus hirsti (Castro et Pereira, 1947)	71	11	2	NR*	Grjazno, Kaliningrado Region, Russia	NA
Fringilla coelebs Linnaeus, 1758	Ptilonyssus hirsti (Castro et Pereira, 1947)	71	11	2	NR*	Grjazno, Kaliningrado Region, Russia	NA
Fringilla coelebs Linnaeus, 1758	Ptilonyssus hirsti (Castro et Pereira, 1947)	71	11	1	NR*	Grjazno, Kaliningrado Region, Russia	NA
Fringilla coelebs Linnaeus, 1758	Ptilonyssus hirsti (Castro et Pereira, 1947)	71	11	1	NR*	Grjazno, Kaliningrado Region, Russia	NA
Fringilla coelebs Linnaeus, 1758	Ptilonyssus hirsti (Castro et Pereira, 1947)	71	11	3	NR*	Grjazno, Kaliningrado Region, Russia	NA
Fringilla coelebs Linnaeus, 1758	Ptilonyssus hirsti (Castro et Pereira, 1947)	71	11	1	NR*	Grjazno, Kaliningrado Region, Russia	NA
Fringilla coelebs Linnaeus, 1758	Ptilonyssus hirsti (Castro et Pereira, 1947)	71	11	1	NR*	Grjazno, Kaliningrado Region, Russia	NA
Fringilla coelebs Linnaeus, 1758	Ptilonyssus hirsti (Castro et Pereira, 1947)	71	11	3	NR*	Grjazno, Kaliningrado Region, Russia	NA
Fringilla coelebs Linnaeus, 1758	Ptilonyssus hirsti (Castro et Pereira, 1947)	71	11	2	NR*	Grjazno, Kaliningrado Region, Russia	NA
Fringilla coelebs Linnaeus, 1758	Ptilonyssus hirsti (Castro et Pereira, 1947)	71	11	1	NR*	Grjazno, Kaliningrado Region, Russia	NA
Carduelis carduelis Linnaeus, 1758	NA	39	0	0	NA	NA	NA
Carpodacus erythrinus (Pallas, 1770)	NA	3	0	0	NA	NA	NA
Chloris chloris Linnaeus, 1758	NA	31	0	0	NA	NA	NA
Fringilla montifringilla Linnaeus, 1758	NA	1	0	0	NA	NA	NA
Loxia curvirostra Linnaeus, 1758	NA	51	0	0	NA	NA	NA
Pinicola enucleator Linnaeus, 1758	NA	16	0	0	NA	NA	NA
Pyrrhula pyrrhula Linnaeus, 1758	NA	9	0	0	NA	NA	NA
Serinus serinus Linnaeus, 1766	NA	5	0	0	NA	NA	NA
Serinus canaria Linnaeus, 1758	Sternostoma marchae Dimov, 2012	29	1	10	NR*	St. Petersburg, Russia	NA
Spinus spinus Linnaeus, 1758	NA	13	0	0	NA	NA	NA
Delichon urbica Linnaeus, 1758	NA	47	0	0	NA	NA	NA
Hirundo rustica Linnaeus, 1758	NA	63	0	0	NA	NA	NA
Riparia riparia Linnaeus, 1758	NA	23	0	0	NA	NA	NA
Anthus pratensis Linnaeus, 1758	NA	1	0	0	NA	NA	NA
Anthus trivialis Linnaeus, 1758	NA	17	0	0	NA	NA	NA
Motacilla flava Linnaeus, 1758	NA	7	0	0	NA	NA	NA
Motacilla alba Linnaeus, 1758	NA	86	0	0	NA	NA	NA
Oenanthe oenanthe Linnaeus, 1758	Ptilonyssus motacillae Fain, 1956	91	3	3	NR*	Tikhvin, Leningrad Oblast, Russia; Sinyavino, Leningrad Oblast, Russia	NA
Oenanthe oenanthe Linnaeus, 1758	Ptilonyssus motacillae Fain, 1956	91	3	2	NR*	Tikhvin, Leningrad Oblast, Russia; Sinyavino, Leningrad Oblast, Russia	NA
Oenanthe oenanthe Linnaeus, 1758	Ptilonyssus motacillae Fain, 1956	91	3	3	NR*	Tikhvin, Leningrad Oblast, Russia; Sinyavino, Leningrad Oblast, Russia	NA
Ficedula hypoleuca (Pallas, 1764)	NA	2	0	0	NA	NA	NA
Luscinia luscinia Linnaeus, 1758	NA	8	0	0	NA	NA	NA
Muscicapa striata (Pallas, 1764)	NA	27	0	0	NA	NA	NA
Saxicola rubetra Linnaeus, 1758	NA	1	0	0	NA	NA	NA
Parus caeruleus Linnaeus, 1758	Ptilonyssus mironovi Dimov, 2012	19	1	3	NR*	Lomonosov, Leningrad Region, Russia	NA
Parus major Linnaeus, 1758	Ptilonyssus sairae Castro, 1948	118	3	2	NR*	St. Petersburg, Russia	NA
Parus major Linnaeus, 1758	Ptilonyssus sairae Castro, 1948	118	3	2	NR*	St. Petersburg, Russia	NA
Parus major Linnaeus, 1758	Ptilonyssus sairae Castro, 1948	118	3	1	NR*	St. Petersburg, Russia	NA
Parus major Linnaeus, 1758	Ptilonyssus pari Fain et Hyland 1963	118	9	2	NR, WE	St. Petersburg, Russia	Fain and Bafort 1963; Fain and Hyland 1963; Fain et al. 1974; Kadosaka et al. 1983; Pence 1972a; Pence 1972b; Pence 1975; Pence and Casto 1976; Shumilo and Lunkashu 1970; Sixl 1969; Sixl 1970; Spicer 1977; Spicer 1978
Parus major Linnaeus, 1758	Ptilonyssus pari Fain et Hyland 1963	118	9	1	NR, WE	St. Petersburg, Russia	Fain and Bafort 1963; Fain and Hyland 1963; Fain et al. 1974; Kadosaka et al. 1983; Pence 1972a; Pence 1972b; Pence 1975; Pence and Casto 1976; Shumilo and Lunkashu 1970; Sixl 1969; Sixl 1970; Spicer 1977; Spicer 1978
Parus major Linnaeus, 1758	Ptilonyssus pari Fain et Hyland 1963	118	9	1	NR, WE	St. Petersburg, Russia	Fain and Bafort 1963; Fain and Hyland 1963; Fain et al. 1974; Kadosaka et al. 1983; Pence 1972a; Pence 1972b; Pence 1975; Pence and Casto 1976; Shumilo and Lunkashu 1970; Sixl 1969; Sixl 1970; Spicer 1977; Spicer 1978
Parus major Linnaeus, 1758	Ptilonyssus pari Fain et Hyland 1963	118	9	1	NR, WE	St. Petersburg, Russia	Fain and Bafort 1963; Fain and Hyland 1963; Fain et al. 1974; Kadosaka et al. 1983; Pence 1972a; Pence 1972b; Pence 1975; Pence and Casto 1976; Shumilo and Lunkashu 1970; Sixl 1969; Sixl 1970; Spicer 1977; Spicer 1978
Parus major Linnaeus, 1758	Ptilonyssus pari Fain et Hyland 1963	118	9	1	NR, WE	St. Petersburg, Russia	Fain and Bafort 1963; Fain and Hyland 1963; Fain et al. 1974; Kadosaka et al. 1983; Pence 1972a; Pence 1972b; Pence 1975; Pence and Casto 1976; Shumilo and Lunkashu 1970; Sixl 1969; Sixl 1970; Spicer 1977; Spicer 1978
Parus major Linnaeus, 1758	Ptilonyssus pari Fain et Hyland 1963	118	9	1	NR, WE	St. Petersburg, Russia	Fain and Bafort 1963; Fain and Hyland 1963; Fain et al. 1974; Kadosaka et al. 1983; Pence 1972a; Pence 1972b; Pence 1975; Pence and Casto 1976; Shumilo and Lunkashu 1970; Sixl 1969; Sixl 1970; Spicer 1977; Spicer 1978
Parus major Linnaeus, 1758	Ptilonyssus pari Fain et Hyland 1963	118	9	1	NR, WE	St. Petersburg, Russia	Fain and Bafort 1963; Fain and Hyland 1963; Fain et al. 1974; Kadosaka et al. 1983; Pence 1972a; Pence 1972b; Pence 1975; Pence and Casto 1976; Shumilo and Lunkashu 1970; Sixl 1969; Sixl 1970; Spicer 1977; Spicer 1978
Parus major Linnaeus, 1758	Ptilonyssus pari Fain et Hyland 1963	118	9	2	NR, WE	St. Petersburg, Russia	Fain and Bafort 1963; Fain and Hyland 1963; Fain et al. 1974; Kadosaka et al. 1983; Pence 1972a; Pence 1972b; Pence 1975; Pence and Casto 1976; Shumilo and Lunkashu 1970; Sixl 1969; Sixl 1970; Spicer 1977; Spicer 1978
Parus major Linnaeus, 1758	Ptilonyssus pari Fain et Hyland 1963	118	9	1	NR, WE	St. Petersburg, Russia	Fain and Bafort 1963; Fain and Hyland 1963; Fain et al. 1974; Kadosaka et al. 1983; Pence 1972a; Pence 1972b; Pence 1975; Pence and Casto 1976; Shumilo and Lunkashu 1970; Sixl 1969; Sixl 1970; Spicer 1977; Spicer 1978
Parus ater Linnaeus, 1758	NA	2	0	0	NA	NA	NA
Parus cristatus Linnaeus, 1758	NA	9	0	0	NA	NA	NA
Parus montanus (Conrad von Baldenstein, 1827)	NA	29	0	0	NA	NA	NA
Parus palustris Linnaeus, 1758	NA	6	0	0	NA	NA	NA
Passer domesticus Linnaeus, 1758	Ptilonyssus degtiarevae Dimov et Mironov, 2012	74	1	5	NR*	Gavrilovo, Leningradskaya Region, Russia	NA
Passer montanus Linnaeus, 1758	Ptilonyssus lovottiae Dimov et Mironov, 2012	91	3	18	NR*	Leningrad Region Russia; Boronichevo, Leningrad Region, Russia; Novaya LadogaLeningrad Oblast, Russia	NA
Passer montanus Linnaeus, 1758	Ptilonyssus lovottiae Dimov et Mironov, 2012	91	3	3	NR*	Leningrad Region Russia; Boronichevo, Leningrad Region, Russia; Novaya LadogaLeningrad Oblast, Russia	NA
Passer montanus Linnaeus, 1758	Ptilonyssus lovottiae Dimov et Mironov, 2012	91	3	5	NR*	Leningrad Region Russia; Boronichevo, Leningrad Region, Russia; Novaya LadogaLeningrad Oblast, Russia	NA
Regulus regulus Linnaeus, 1758	NA	27	0	0	NA	NA	NA
Sitta europea Linnaeus, 1758	NA	3	0	0	NA	NA	NA
Phylloscopus sibilatrix (Bechstein, 1793)	NA	1	0	0	NA	NA	NA
Phylloscopus trochilus Linnaeus, 1758	NA	16	0	0	NA	NA	NA
Dendrocopos major Linnaeus, 1758	NA	16	0	0	NA	NA	NA
Sturnus vulgaris Linnaeus, 1758	NA	39	0	0	NA	NA	NA
Sylvia atricapilla Linnaeus, 1758	NA	7	0	0	NA	NA	NA
Sylvia borin (Boddaert, 1783)	NA	3	0	0	NA	NA	NA
Sylvia curruca Linnaeus, 1758	NA	41	0	0	NA	NA	NA
Turdus iliacus Linnaeus, 1766	Ptilonyssus euroturdi Fain et Hyland, 1963	27	7	1	NR*	Arkhangelsk Region, Russia	NA
Turdus iliacus Linnaeus, 1766	Ptilonyssus euroturdi Fain et Hyland, 1963	27	7	2	NR*	Arkhangelsk Region, Russia	NA
Turdus iliacus Linnaeus, 1766	Ptilonyssus euroturdi Fain et Hyland, 1963	27	7	1	NR*	Arkhangelsk Region, Russia	NA
Turdus iliacus Linnaeus, 1766	Ptilonyssus euroturdi Fain et Hyland, 1963	27	7	3	NR*	Arkhangelsk Region, Russia	NA
Turdus iliacus Linnaeus, 1766	Ptilonyssus euroturdi Fain et Hyland, 1963	27	7	2	NR*	Arkhangelsk Region, Russia	NA
Turdus iliacus Linnaeus, 1766	Ptilonyssus euroturdi Fain et Hyland, 1963	27	7	2	NR*	Arkhangelsk Region, Russia	NA
Turdus iliacus Linnaeus, 1766	Ptilonyssus euroturdi Fain et Hyland, 1963	27	7	1	NR*	Arkhangelsk Region, Russia	NA
Turdus merula Linnaeus, 1758	Sternostoma dureni Fain, 1956	78	1	1	NR*	Hervir, Leningrad Region, Russia	NA
Turdus philomelos Brehm, 1831	Sternostoma turdi Zumpt et Till, 1955	19	7	2	NR, ER WE	Severodvinsk, Arkhangelsk, Russia	Butenko 1965; Fain 1956; Fain 1957; Fain 1959; Fain 1962a; Fain 1963; Fain and Aikten 1967; Fain et al. 1974; Furman 1957; Pence 1972c; Shumilo and Lunkashu 1970; Sixl 1971; Spicer 1984; Spicer 1987; Zumpt and Till 1955
Turdus philomelos Brehm, 1831	Sternostoma turdi Zumpt et Till, 1955	19	7	2	NR, ER WE	Severodvinsk, Arkhangelsk, Russia	Butenko 1965; Fain 1956; Fain 1957; Fain 1959; Fain 1962a; Fain 1963; Fain and Aikten 1967; Fain et al. 1974; Furman 1957; Pence 1972c; Shumilo and Lunkashu 1970; Sixl 1971; Spicer 1984; Spicer 1987; Zumpt and Till 1955
Turdus philomelos Brehm, 1831	Sternostoma turdi Zumpt et Till, 1955	19	7	1	NR, ER WE	Severodvinsk, Arkhangelsk, Russia	Butenko 1965; Fain 1956; Fain 1957; Fain 1959; Fain 1962a; Fain 1963; Fain and Aikten 1967; Fain et al. 1974; Furman 1957; Pence 1972c; Shumilo and Lunkashu 1970; Sixl 1971; Spicer 1984; Spicer 1987; Zumpt and Till 1955
Turdus philomelos Brehm, 1831	Sternostoma turdi Zumpt et Till, 1955	19	7	1	NR, ER WE	Severodvinsk, Arkhangelsk, Russia	Butenko 1965; Fain 1956; Fain 1957; Fain 1959; Fain 1962a; Fain 1963; Fain and Aikten 1967; Fain et al. 1974; Furman 1957; Pence 1972c; Shumilo and Lunkashu 1970; Sixl 1971; Spicer 1984; Spicer 1987; Zumpt and Till 1955
Turdus philomelos Brehm, 1831	Sternostoma turdi Zumpt et Till, 1955	19	7	1	NR, ER WE	Severodvinsk, Arkhangelsk, Russia	Butenko 1965; Fain 1956; Fain 1957; Fain 1959; Fain 1962a; Fain 1963; Fain and Aikten 1967; Fain et al. 1974; Furman 1957; Pence 1972c; Shumilo and Lunkashu 1970; Sixl 1971; Spicer 1984; Spicer 1987; Zumpt and Till 1955
Turdus philomelos Brehm, 1831	Sternostoma turdi Zumpt et Till, 1955	19	7	1	NR, ER WE	Severodvinsk, Arkhangelsk, Russia	Butenko 1965; Fain 1956; Fain 1957; Fain 1959; Fain 1962a; Fain 1963; Fain and Aikten 1967; Fain et al. 1974; Furman 1957; Pence 1972c; Shumilo and Lunkashu 1970; Sixl 1971; Spicer 1984; Spicer 1987; Zumpt and Till 1955
Turdus philomelos Brehm, 1831	Sternostoma turdi Zumpt et Till, 1955	19	7	1	NR, ER WE	Severodvinsk, Arkhangelsk, Russia	Butenko 1965; Fain 1956; Fain 1957; Fain 1959; Fain 1962a; Fain 1963; Fain and Aikten 1967; Fain et al. 1974; Furman 1957; Pence 1972c; Shumilo and Lunkashu 1970; Sixl 1971; Spicer 1984; Spicer 1987; Zumpt and Till 1955
Turdus pilaris Linnaeus, 1758	NA	121	0	0	NA	NA	NA
Dendrocopos major Linnaeus, 1758	NA	16	0	0	NA	NA	NA

Coordinates

and 60.05 Latitude; and 31.75 Longitude.

Taxonomic coverage

A total of 2,107 individual birds were collected, representing 75 species belonging to 55 genera, 30 families and 10 orders. The majority of the studied hosts (59 species from 36 genera) belonged to the order (the most numerous and widely-distributed order of birds of the northwest of Russia) (Table 1). Specifically, sampled passerine species comprise up to 58% out of the total number of species of passerine species inhabiting the territory of the northwest of Russia (Malchevsky and Pukinsky 1983). In general, 179 mite specimens belonging to 27 species and 8 genera were identified. From a total of 27 host-mite associations, we report 18 novel host-mite associations (Table 2). As expected, due to the higher sampling effort in Passerifoms, the number of new host-mite associations was the highest in this order (9 out of 18), followed by waterbirds belonging to and (with 4 and 3 new host-mite associations, respectively). Only a single new host-mite association was detected in and . Lastly, no new association was found in , or .

Table 1.

Data of prevalence of rhinonyssid mites in different orders of hosts and the number of families, genera and species of birds studied. Confidence intervals of prevalence (95%) are provided between parentheses.

Bird order	Bird families	Bird genera	Bird species	Analysed individuals	Infected individuals	Prevalence
Anseriformes	1	3	4	105	13	12.38% (7.38-20.04)
Caprimulgiformes	1	1	1	2	1	50% (2.56-97.44)
Charadriiformes	4	5	6	117	8	6.8% (3.51-12.91)
Columbiformes	1	1	1	262	10	3.8% (2.09-6.88)
Cuculiformes	1	1	1	13	1	7.69% (0.39-33.31)
Accipitriformes	1	2	2	3	0	0% (0-56.15)
Galliformes	1	2	2	32	0	0% (0-10.71)
Gruiformes	1	2	2	8	2	25% (4.44-59.07)
Passeriformes	18	37	55	1549	58	3.7% (2.91-4.81)
Piciformes	1	1	1	16	0	0% (0-19.36)
Total	30	55	75	2107	93	4.41% (3.62-5.38)

Usage rights

Use license

Creative Commons Public Domain Waiver (CC-Zero)

Data resources

Data package title

Host-mite associations of rhinonyssid mites (: ) in Northwest Russia.

Number of data sets

1

Data set 1.

Data set name

Table S2

Number of columns

5

Description

Host-mite associations form a total of 2,107 individual hosts totalling 75 bird species from 30 avian families and 10 orders (Suppl. material 3). Information on eight mite genera and 28 mite species from is presented. Each row depicts an individual bird from mite-host associations, in which more than one mite was found. See Table 2 for more information (e.g. prevalence).

Additional information

Discussion

In the present study, the rhinonyssid mite species collected from 2,107 bird individuals from 75 bird species at 41 sites in Northwest Russia were reported. A total of 27 host-mite associations were found, from which 18 were novel (Table 2).

The prevalence of rhinonyssid mites was found to vary between bird taxa, as found by previous studies (Spicer 1987; Table 1). Interestingly, the prevalence values found here were lower overall (particularly low in ) than those found by previous studies (e.g. 4.41%, this study vs. 17%, USA, Spicer 1987; or 15-16%, Canada, Knee 2018). The lower values found here may be due to differences in climatic conditions, as have been found by previous studies (e.g. Spicer 1987). Overall, our results support current expectations that rhinonyssid mites are generally associated with low prevalence with their hosts (Spicer 1987;Knee 2018).

The mite-host associations found in this study were compared with those known from the same host species inhabiting the European part of Russia and Europe (see Suppl. material 2). In particular, a higher number of mite species of rhinonyssid genera was found in the northwest of Russia compared to the European part of Russia and Western Europe (Suppl. material 2). This pattern was particularly noticeable for species-rich genera, such as and . In addition, the pattern was most acute between the northwest of Russia and western Europe. For instance, there were almost no common species between these two areas (only 14 common species from six genera). In contrast, almost all genera (five out of eight) of were shared.

On the other hand, some species that have been found in the European part of Russia and Europe were not found in this study (e.g. from from from from ). Overall, these differences in diversity could be the outcome of the lack of knowledge about these mites in these regions. Indeed, differences in sampling effort (i.e. some groups have been more extensively sampled in Northwest Russia than in other geographic areas) may be biasing these interpretations. Overall, further studies aimed at ascertaining whether specific rhinonyssid mite species are found throughout all their host distribution are encouraged. In this vein, global syntheses are needed to draw more general conclusions on the distribution of rhinonyssid mites. Additionally, future studies describing new species are required to catalogue the unknown diversity of this group of mites. In addition, new molecular approaches (e.g. DNA metabarcoding of complex samples; Doña et al. 2019) would help to accelerate the discovery of new species along with validating the species status of previously-described rhinonyssid species, as cryptic species are known in this group (de Rojas et al. 2018).

Figure S1

Data type: Figure

Brief description: Map of sampling localities. Note that specific locations, as well as their coordinates, can be found in Table 2.

File: oo_365465.png

Table S1

Data type: Table

Brief description: Comparison of species of the family located in Northwest Russia, the European part of Russia and Western Europe; plus and minus signs indicate presence and absence, respectively. Mite species found in this study are marked with *

File: oo_365467.tsv

Table S2

Data type: Table

Brief description: Rhinonyssid mites from Russian birds

File: oo_365526.tsv

Rank	Scientific Name	Common Name
kingdom	Animalia	Animals
subkingdom	Eumetazoa
phylum	Chordata
subphylum	Vertebrata
class	Aves	Birds
subclass	Galloanserae
subclass	Passerae
superorder	Anserimorphae
superorder	Columbimorphae
superorder	Cuculimorphae
superorder	Gallomorphae
superorder	Passerimorphae
order	Accipitriformes
order	Anseriformes
order	Caprimulgiformes
order	Charadriiformes
order	Columbiformes
order	Cuculiformes
order	Galliformes
order	Gruiformes
order	Passeriformes
suborder	Accipitri
suborder	Anseri
suborder	Caprimulgi
suborder	Charadrii
suborder	Columbi
suborder	Cuculi
suborder	Passeri
suborder	Phasiani
suborder	Ralli
superfamily	Accipitroidea
superfamily	Aegithaloidea
superfamily	Alaudoidea
superfamily	Anatoidea
superfamily	Bombycilloidea
superfamily	Caprimulgoidea
superfamily	Charadrioidea
superfamily	Columboidea
superfamily	Corvoidea
superfamily	Cuculoidea
superfamily	Fringilloidea
superfamily	Gruoidea
superfamily	Hirundinoidea
superfamily	Laroidea
superfamily	Muscicapoidea
superfamily	Passeroidea
superfamily	Phasianoidea
superfamily	Ralloidea
superfamily	Reguloidea
superfamily	Scolopacoidea
superfamily	Sittoidea
superfamily	Sturnoidea
superfamily	Sylvioidea
family	Accipitridae
family	Anatidae
family	Caprimulgidae
family	Charadriidae
family	Columbidae
family	Corvidae
family	Cuculidae
family	Emberizidae
family	Fringillidae
family	Laridae
family	Motacillidae
family	Muscicapidae
family	Paridae
family	Ploceidae
family	Rallidae
family	Regulidae
family	Scolopacidae
family	Sturnidae
family	Sylviidae
family	Turdidae
species	Acanthis canabina
species	Acanthis flammea
species	Aegithalos caudatus
species	Accipiter nisus
species	Alauda arvensis
species	Anas crecca
species	Anas platyrhynchos
species	Anthus pratensis
species	Anthus trivialis
species	Aythya nyroca
species	Bombycilla garrulus
species	Buteo buteo
species	Caprimulgus europeus
species	Carduelis carduelis
species	Carpodacus erythrinus
species	Charadrius dubius
species	Chloris chloris
species	Columba livia
species	Corvus cornix
species	Coturnix coturnix
species	Cuculus canorus
species	Delichon urbica
species	Dendrocopos major
species	Emberiza citrinella
species	Emberiza hortulana
species	Emberiza rustica
species	Emberiza schoeniclus
species	Ficedula hypoleuca
species	Fringilla coelebs
species	Fringilla montifringilla
species	Fulica atra
species	Gallinula chloropus
species	Garrulus glandarius
species	Hirundo rustica
species	Larus ridibundus
species	Loxia curvirostra
species	Luscinia luscinia
species	Motacilla alba
species	Motacilla flava
species	Muscicapa striata
species	Oenanthe oenanthe
species	Parus ater
species	Parus caeruleus
species	Parus cristatus
species	Parus major
species	Parus montanus
species	Parus palustris
species	Passer domesticus
species	Passer montanus
species	Phylloscopus sibilatrix
species	Phylloscopus trochilus
species	Pica pica
species	Pinicola enucleator
species	Pyrrhula pyrrhula
species	Regulus regulus
species	Riparia riparia
species	Saxicola rubetra
species	Scolopax rusticola
species	Serinus canaria
species	Serinus serinus
species	Sitta europea
species	Somateria mollissima
species	Spinus spinus
species	Sterna hirundo
species	Sturnus vulgaris
species	Sylvia atricapilla
species	Sylvia borin
species	Sylvia curruca
species	Turdus iliacus
species	Turdus merula
species	Turdus philomelos
species	Turdus pilaris
species	Vanellus vanellus
kingdom	Animalia	Animals
subkingdom	Eumetazoa
phylum	Chordata
phylum	Arthropoda	Arthropods
subphylum	Vertebrata
subphylum	Chelicerata
class	Aves	Birds
class	Arachnida
subclass	Galloanserae
subclass	Passerae
subclass	Acari	Mites
superorder	Anserimorphae
superorder	Columbimorphae
superorder	Cuculimorphae
superorder	Gallomorphae
superorder	Passerimorphae
superorder	Parasitiformes
order	Accipitriformes
order	Anseriformes
order	Caprimulgiformes
order	Charadriiformes
order	Columbiformes
order	Cuculiformes
order	Galliformes
order	Gruiformes
order	Passeriformes
order	Mesostigmata
suborder	Accipitri
suborder	Anseri
suborder	Caprimulgi
suborder	Charadrii
suborder	Columbi
suborder	Cuculi
suborder	Passeri
suborder	Phasiani
suborder	Ralli
suborder	Monogynaspida
infraorder	Gamasina
superfamily	Accipitroidea
superfamily	Aegithaloidea
superfamily	Alaudoidea
superfamily	Anatoidea
superfamily	Bombycilloidea
superfamily	Caprimulgoidea
superfamily	Charadrioidea
superfamily	Columboidea
superfamily	Corvoidea
superfamily	Cuculoidea
superfamily	Fringilloidea
superfamily	Gruoidea
superfamily	Hirundinoidea
superfamily	Laroidea
superfamily	Muscicapoidea
superfamily	Passeroidea
superfamily	Phasianoidea
superfamily	Ralloidea
superfamily	Reguloidea
superfamily	Scolopacoidea
superfamily	Sittoidea
superfamily	Sturnoidea
superfamily	Sylvioidea
superfamily	Dermanyssoidea
family	Accipitridae
family	Anatidae
family	Caprimulgidae
family	Charadriidae
family	Columbidae
family	Corvidae
family	Cuculidae
family	Emberizidae
family	Fringillidae
family	Laridae
family	Motacillidae
family	Muscicapidae
family	Paridae
family	Ploceidae
family	Rallidae
family	Regulidae
family	Scolopacidae
family	Sturnidae
family	Sylviidae
family	Turdidae
family	Rhinonyssidae	Rhinonyssids
species	Larinyssus iohanssenae
species	Larinyssus orbicularis
species	Mesonyssus columbae
species	Mesonyssus melloi
species	Ptilonyssus degtiarevae
species	Ptilonyssus euroturdi
species	Ptilonyssus hirsti
species	Ptilonyssus lovottiae
species	Ptilonyssus mironovi
species	Ptilonyssus motacillae
species	Ptilonyssus pari
species	Ptilonyssus sairae
species	Ptilonyssus schumili
species	Rallinyssus caudistigmus
species	Rhinonyssus bregetovae
species	Rhinonyssus dobromiri
species	Rhinonyssus kadrae
species	Rhinonyssus levinsini
species	Rhinonyssus neglectus
species	Rhinonyssus nyrocae
species	Rhinonyssus polystictae
species	Rhinonyssus subrhinolethrum
species	Sternostoma dureni
species	Sternostoma marchae
species	Sternostoma turdi
species	Sternostoma zini
species	Vitznyssus tsachevi

Data set 1.

Column label	Column description
Bird taxa	Scientific name and authority of bird taxa
Mite species	Scientific name and authority of mite taxa
Locality (this study)	Sampling localities
Coordinates	Coordinates in degrees minutes and seconds
Date	Collection date