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Data Paper (Biosciences)
A comprehensive survey of Rhinonyssid mites (Mesostigmata: Rhinonyssidae) in Northwest Russia: New mite-host associations and prevalence data
expand article infoManuel De Rojas, Jorge Doña§, Ivan Dimov|
‡ University of Seville, Seville, Spain
§ Illinois Natural History Survey, Champaign, United States of America
| State Pediatric Medical University, St. Petersburg, Russia
Open Access

Abstract

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.

Keywords

birds, checklist, ectoparasites, parasites, symbionts

Introduction

Nasal mites of the family Rhinonyssidae 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 (Rhinonyssidosis avium disease) (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 Dermanyssidae (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 Rhinonyssidae 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).

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)

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: 

60.05; 31.75.

Taxonomic coverage

Description: 

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 Passeriformes (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 Charadriiformes and Anseriformes (with 4 and 3 new host-mite associations, respectively). Only a single new host-mite association was detected in Caprimulgiformes and Cuculiformes. Lastly, no new association was found in Columbiformes, Galliformes or Piciformes.

Taxa included:
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

Usage rights

Use license: 
Creative Commons Public Domain Waiver (CC-Zero)

Data resources

Data package title: 
Host-mite associations of rhinonyssid mites (Mesostigmata: Rhinonyssidae) in Northwest Russia.
Number of data sets: 
1
Data set name: 
Table S2
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 Rhinonyssidae 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).

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

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 Passeriformes) 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 Sternostoma, Mesonyssus, Rhinonyssus and Ptilonyssus. 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 Rhinonyssidae 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. Mesonyssus hirsutus from Columba livia; Ptilonyssus nudus from Fringilla coelebs; Ptilonyssus pari from Parus ater; Parus caeruleus or Parus europea; Rhinonyssus vanellus from Vanellus vanellus). 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).

Acknowledgements

The authors are very grateful to the head of the laboratory of parasitology ZIN RAS Medvedev DSc. and employees of the laboratory of parasitology: Mironov DSc., Shatrov DSc., Bochkov DSc. and Leonovich DSc. for the comprehensive assistance and support provided in the process of carrying out the research. We thank Centro Municipal Zoosanitario de Sevilla and especially Mr. Francisco Peña Fernández and Mr. Rafael Cuadrado Nieto for their technical support. Our thanks to Geoffrey Giddings for proof-reading the manuscript.

Author contributions

MDR, JD, and ID conceived the study. ID collected the samples. MR and ID made the morphobiometric assessments. JD analysed the data. JD wrote the last version of the article with the help of all authors.

References

Supplementary materials

Suppl. material 1: Figure S1 
Authors:  de Rojas M, Doña J, Dimov I
Data type:  Figure
Brief description: 

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

Suppl. material 2: Table S1 
Authors:  de Rojas M, Doña J, Dimov I
Data type:  Table
Brief description: 

Comparison of species of the family Rhinonyssidae 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 *

Suppl. material 3: Table S2 
Authors:  de Rojas, M., Doña, J., Dimov, I
Data type:  Table
Brief description: 

Rhinonyssid mites from Russian birds