Oribatid Mites (Oribatida) Associated with Nests of Hollow-Nesting Birds, on the Example of a Model Species, the European Pied Flycatcher (Ficedula hypoleuca), in the Taiga Forests of the European North-East of Russia
Institute of Biology, Komi Science Centre, Ural Branch, Russian Academy of Sciences (IB FRC Komi SC UB RAS), Kommunisticheskaya Str. 28, 167982 Syktyvkar, Russia
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Author to whom correspondence should be addressed.
Diversity 2023, 15(6), 765; https://doi.org/10.3390/d15060765
Submission received: 5 April 2023
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Revised: 28 May 2023
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Accepted: 8 June 2023
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Published: 12 June 2023
(This article belongs to the Special Issue Diversity of Terrestrial Invertebrate Communities)
Abstract
:The authors have obtained original material on the fauna and population structure of oribatid mites inhabiting nests of the European Pied Flycatcher (Ficedula hypoleuca, Passeriformes, hollow-nesting bird) on the territory of the taiga zone of the European North-East of Russia. Long-term research and the collection of nests were carried out in the green zone of Syktyvkar in 2017–2022. Observations were made for artificial nests (hollows) of a box type with a bottom area of 100 cm2. The material of the tray was collected completely. In 135 studied nests of Pied Flycatchers, 1762 specimens were found and identified for 22 species of oribatid mites from 19 genera and 16 families. In the nests of the Pied Flycatcher, a complex of species was found that is known as an arboricolous species for this region; these are Oribatula (Zygoribatula) propinqua, Oribatula (Z.) exilis, Trichoribates (T.) berlesei, and Ameronothrus oblongus. We suggested that arboricolous species, as well as eurytopic species, can actively inhabit bird nests. Highly numerous in our collections were representatives of the Oribatulidae and Scheloribatidae families; they are Oribatula (Z.) propinqua, Oribatula (Z.) exilis, Oribatula (O.) tibialis, and Scheloribates laevigatus. Epigeic species are dominated by the species number. The fauna of oribatid mites mainly included widespread Holarctic species (54.54%).
1. Introduction
The nests of migratory birds are of interest as habitats for soil microarthropods, including oribatid mites [1,2,3,4,5,6,7,8]. There is information about some findings of oribatids in the feathers of migratory birds [9,10,11]; it has been suggested that birds carry microarthropods in their feathers thousands of kilometers away from their wintering to nesting sites, increasing the diversity of some groups of microarthropods in northern latitudes and expanding their ranges [9,12]. The nests of migratory birds in the Arctic are of increasing interest [13]. This paper is an attempt broaden understanding of this phenomenon with the example of the European Pied Flycatcher (Ficedula hypoleuca), a representative of small passerine birds. This species is a common model species for conducting various kinds of population studies.
Being a typical hollow-nesting species easily attracted to artificial nesting sites, the European Pied Flycatcher (Ficedula hypoleuca) can serve as a convenient material to study the fauna and population of microarthropods, including oribatid mites that live in nests. Pied flycatcher nests are relatively protected from the effects of weather conditions, such as precipitation and wind, and it is likely that a special microclimate for arthropods is formed in such microhabitats. Studies on the breeding biology of the Pied Flycatcher aimed at obtaining qualitative and quantitative characteristics of its nesting will provide information that will form the basis for further studying the formation patterns of the fauna and population of oribatid mites living in nests of this bird. Moreover, studies on the seasonal dynamics of microarthropod fauna in the nests of flycatchers are of particular interest as the birds leave their nests for a long time after finishing the nesting season. The main purpose of our research is to analyze the dynamics of the fauna and population of oribatid mites in the nests of the Pied Flycatcher relative to the nesting progress and life cycle of the birds in the taiga zone of the European North-East of Russia.
2. Materials and Methods
2.1. Study Region
The study region is located in the taiga zone of the European North-East of Russia within the Komi Republic, Syktyvkar (61.40° N, 50.48° E). The territory belongs to the Vychegda–Mezen district of spruce, birch, and pine forests of the middle taiga subzone and is situated on the plain. Dark coniferous spruce forests dominate in the drained interfluves. Spacious pine forests alternate with upland peats on the terraces. Significant areas are occupied by spruce-birch forests with some aspen trees [14]. The climate is moderately continental with short and cool summers and snowy and long winters. The annual air temperature amplitude is 33 °C. The warmest year month is July (the average monthly temperature is +17 °C) and the coldest year month is January (−16 °C). The mean annual air temperature is 0 °C. The number of days with a mean daily air temperature above zero is 190. The average annual precipitation is 600 mm. The average height of snow cover is 50 cm, and the duration of its occurrence is 190 days [15,16].
Nests of Pied Flycatchers were observed in the green zones of Syktyvkar, particularly in the mixed poplar–birch stands of the Kirov Park of Culture and Recreation (KP), mixed spruce–birch stands of the Michurin City Park (MP), and mixed spruce–birch forest (in the vicinity of the Radiobiological Complex of the Institute of Biology (RBC)). KP and MP plots are situated in the central city part. RBC belongs to the southwestern outskirts of the city. The total area of the studied plots was 15 hectares.
2.2. Pied Flycatcher, Distribution, Nesting Biology
The European Pied Flycatcher (Ficedula hypoleuca) is a representative of the flycatcher family (Muscicapidae) of the order of passerine birds (Passeriformes). The breeding range of the species covers Northwest Africa and a significant part of Eurasia from the Atlantic coast to the Yenisei River valley. In the north, it occurs up to the 64–70th parallel, in the south, up to the 43–56th parallel, and in Africa, up to the 35th parallel [17]. The Pied Flycatcher makes annual migrations to wintering grounds. Its wintering grounds are located in the Mediterranean and Central and North Africa [18] (Figure 1). For the territory of the European North-East of Russia, the Pied Flycatcher is a common nestling migratory species in the south and middle taiga subzones. It is few in number in the north taiga and is considered to be a rare species in the extremely north taiga subzones [19,20,21,22].
The flycatcher inhabits forest stands and prefers mixed and deciduous mature and overmature forests [18]. It often inhabits artificial nesting grounds in city parks and squares. The nest is normally arranged in natural hollows of trees, in stumps, and in niches of buildings at a height of up to 15–20 m, usually at a height of 2–4 m from the very ground. The bird uses dry branches, leaves, grass blades, roots, needles, and pine and birch bark as nesting material. The nest tray in some cases does not differ from the material of the rest of the nest, and in other cases, it can be lined with very thin scales of pine bark or birch bark, and also with the hair of large mammals [18]. Adult birds are associated with the nest for about one month; this is the period of the incubation of eggs and the feeding of chicks before they leave the nest. Thus, the nest is inhabited for about 30 days. Egg laying lasts 3–11 days (usually 6–8), incubation—10–17 days (usually 12–13), and the feeding of chicks—13–18 days (usually 15–16). There are 3–11 eggs in a clutch (usually 6–8). There is one reproductive cycle per summer, but birds may re-lay eggs if the first clutches die. The departure of birds to wintering grounds begins after the end of the nesting period in late July to early August and finishes in early September [18]. Flycatchers mainly feed on insects. The birds collect them from the ground, grass, leaves, or branches or catch insects on the wing [23]. More than half of the collected insects are non-flying or poorly mobile [23,24,25].
2.3. Sampling Methods
We observed the nests located in artificial nest boxes with a bottom area of 100 cm2 (Figure 2). About 90 artificial nests were monitored annually in the green zones of Syktyvkar, apart from 2022, when the majority of nest boxes were removed. We observed only 29 nests in 2022. The inspection of the nests was carried out once a week on the territory of the park areas and five times a week on the territory of RBC.
The period when the birds used nests was recorded: the time of nest construction, the beginning and the end of egg laying, the clutch size, the period of chicks’ feeding, the flying-out dates of chicks, and the incubation and feeding progress. We examined the nesting material of 135 nests of the European Pied Flycatcher for the presence of oribatid mites in them.
The date of laying the first egg was calculated based on the fact that incubation began with the last laid egg [18]. The duration of the nesting cycle (or time when the birds live in the nest) was calculated as the difference between the flying-out date of chicks and the first egg-laying date. In the absence of information on the exact date of departure (although we recorded the successful completion of the nesting period), the last date of observation of the active nest was taken as the date of departure. The “period of absence of birds in the nest” was understood as a period between the last chicks’ departure and the removal of the nest from the nest box. The overall success of reproduction was estimated by the ratio of the number of fledglings that flew out to the number of laid eggs. The analysis includes data on 135 collected nests of Pied Flycatchers over a six-year period (2017–11, 2018–30, 2019–31, 2020–29, 2021–29, 2022–5 nests) with a total duration of 4068 nesting days (Appendix A, Table A1). The nests were taken away from the nest boxes after the end of the nesting period, approximately 7 days after the chicks’ departure. Towards the beginning of the nesting season of 2018, we sampled 11 “overwintered” nests which were places of egg laying and the rearing of offspring in 2017. Thus, these nests were collected 9–10 months later after the chicks had flown away. The material of the tray was collected completely.
2.4. Material Treatment
The invertebrates were extracted from nests using the Berlese–Tullgren thermoeclectors under 40 Watt bulbs into 96% alcohol for ten days [26]. Micropreparations were made from oribatid mites using For-Berlese liquid [26]. The oribatids were identified as species by morphological taxonomic characters using the key [27]. The taxonomy and type of global species distribution are given according to the L. Subias’ classification [28]. For the analysis of the geographical distribution of species, literary sources were used [29,30,31,32,33] as well as others.
The classification of life forms of oribatid mites is given according to Krivolutsky [26]. The collections included varying species: inhabitants of the soil surface and upper horizons of the litter (epigeic), inhabitants of the litter layer (hemiedaphic), inhabitants of small soil holes (euedaphic), and eurybiontic and hydrobiontic species.
To compare three samples from three observation sites, these diversity indices were used: the number of taxa, the number of specimens, the Shannon index, the Menhinick index, and the Berger–Parker index. The Kruskal–Wallis test and the Mann-Whitney U test was used to determine the significance of differences. The SIMPER analysis (percentage similarity) was used to identify the species responsible for differences in the abundance of oribatids in different observation periods at different sites. The pairs of samples are compared using the Bray–Curtis measure. The calculations were carried out using the PAST 4.12b program [34]. We calculated indicators such as the number of specimens (N), dominance (D%), and the frequency of occurrence in samples (F%).
3. Results
3.1. Success of Pied Flycatcher Nesting
The start of the flycatcher’s nesting period significantly varied from year to year. The earliest egg laying was recorded on 15 May, and the latest recorded eggs among repeated clutches were laid on 30 June. The duration median of the nesting cycle (distribution differs from the normal distribution) was 33 days for the entire study period. The reproduction of the Pied Flycatchers ended successfully in 101 nests (75%). The breeding success of individual pairs varied from 17 to 100%. The lowest total loss of clutches was observed in the green zone on the outskirts of the city (RBC)—6%—in contrast to the urban parks (KP, MP) where it was 30–33% (Appendix A, Table A1).
3.2. Abundance of Oribatid Mites
In the studied nests of the Pied Flycatcher, 1762 specimens of oribatid mites were found. The abundance of oribatid mites in the nests was generally low and uneven. The majority of nests counted only several specimens of oribatid mites. Only single nest boxes hosted from 60 to 80, and rarely more than 100 oribatid specimens. Some nests did not have them at all.
The “overwintered” nests of the 2017 nesting season were selected in May 2018. These nests were found for oribatid mites whose number reached 140 specimens or more per nest. The “overwintered” nests were normally inhabited by species of the Oribatulidae and Scheloribatidae families. For example, 142 specimens of oribatids of one species, Oribatula (Zygoribatula) propinqua, were found in nest box No. 25 (MP) on 16 May 2018; 74 specimens of O. (Z.) propinqua and two specimens of Oribatula (Z.) exilis were found in nest box No. 32 (MP). Nest box No. 21 (KP) was identified for 46 specimens of Scheloribates (S.) laevigatus, as well as for one specimen of O. (Z.) propinqua on 16 May 2018. It can be assumed that these mites successfully survived the winter in the nests of Pied Flycatchers.
The general number of oribatids in June and July of 2018 and other observation years was low compared to that in May. It continued being high in summer only in some nests dominated by the same species. Vice versa, the diversity of species increased in June and July. For example, 79 specimens of oribatid mites of five species were found in nest box No. 19 (KP) on 22 July 2020. Among them, one species, O. (Z.) propinqua, dominated in abundance (57.09%), and the others (S. (S.) laevigatus, O. (Z.) exilis, Tectocepheus velatus, Graptoppia (Apograptoppia) foveolata) were single specimens. The number of oribatids per nest normally ranged from three to ten specimens.
3.3. Taxonomic Composition and Diversity of Oribatid Mites
The examined nests of the Pied Flycatcher were found for 22 species of oribatid mites from 17 families (Table 1). The diversity of species was low. Some nests contained five or six species of oribatids, and the majority contained one or three species. The epigeic species, the so-called inhabitants of the soil surface and upper horizons of the forest litter according to the classification of life forms by D.A. Krivolutsky [21], dominated in species number. Eurybiontic species, representatives of the Oribatulidae and Scheloribatidae families, dominated in abundance. From the first family, the species Oribatula (Zygoribatula) propinqua, Oribatula (Z.) exilis and Oribatula (O.) tibialis were most common, and Scheloribates laevigatus from the second family. The inhabitants of shallow soil wells (euedaphic species) were rare. The greatest diversity of species was noted in nest box No. 8 (KP) on 19 July 2021 (five species), nest box No. 9 (KP) on 23 June 2021 (five species), nest box No. 9 (RBC) on 23 June 2021 (five species), and nest box No. 25 (MP) on 23 June 2021 (five species).
We compared (Kruskal-Wallis test) three observation sites: Kirov Park, Michurin City Park, and RBC in terms of such diversity indices as: the number of taxa, the number of specimens, the Shannon Index, the Menhinick Index, and the Berger–Parker Index; there were no significant differences between the three sites in these indicators revealed, with the exception of the number of specimens indicator (Kruskal-Wallis test, p = 0.038): the abundance of individuals in RBC was statistically significant less than in the Kirov Park (Mann-Whitney test, Z = 2.44, p = 0.016) (Figure 3).
4. Discussion
4.1. Taxonomic Composition
The SIMPER analysis (similarity percentage) revealed two significant species that determined the differences in the number of oribatid mites in different observation periods; these were the species Oribatula (Z.) propinqua and Scheloribates (S.) laevigatus. When comparing the number of oribatid mites at the RBC site, significant differences were revealed in overwintered nests collected before the arrival of birds (in May to early June 2018) not yet inhabited by birds, and nests collected in the summer, when they were already populated by birds. In the overwintered nests that were inhabited by birds in 2017, the number of oribatid mites was significantly higher (Mann-Whitney test, Z = 2.2, p = 0.028) (Figure 4).
The Oribatula (Zygoribatula) propinqua species was earlier found by us in epiphytic lichens of coniferous forests of the European North-East [35]. This species was recorded exclusively in epiphytes. It dominated in abundance in the Hypogimnia physodes thallus in pine forests and was rare in spruce forests. The species was not found in the soil. We included this species in the ecological group of arboreal dominant species [35]. The eurytopic species Scheloribates (S.) laevigatus was often found in both ground and epiphytic lichens [35,36]. The Oribatula (Z.) exilis, Melanozetes mollicomus, and Trichoribates (T.) berlesei species also inhabited epiphytic lichens [36].
Some species rare in Pied Flycatcher nests have also been noted as arboreal species.
Thus, only one specimen of Ameronothrus oblongus was found in nest box No. 26 (MP) on 16 May 2018. We earlier found it in epiphytic lichens, and it was not recorded in any other habitats and was included in the group of a few arboreal species [35].
Representatives of the Ameronothrus genus known as hydrobiontic littoral species have previously been recorded in bird nests. For example, Ameronothrus lineatus (Thorell, 1871) was found in nests of Common Eider, Glaucous Gull, and Black-legged Kittiwake on the Svalbard archipelago [12]. This species (A. lineatus) was identified in the nest of Common Eider in the north of the European part of Russia (the Murmansk region) [37].
Arboricolous species could possibly actively inhabit artificial nests of the Pied Flycatcher. The eurytopic species Scheloribates (S.) laevigatus and Tectocepheus velatus occupy various habitats and also could actively inhabit nest boxes. According to S.V. Shakhab [37], the oribatid species Tectocepheus velatus, Oribatula tibialis, and Scheloribates laevigatus, being eurybiontic species according to the D.A. Krivolutsky system [26], dominated in abundance in bird nests in the European part of Russia.
We believe that oribatid mites can enter the nests of the Pied Flycatcher within the nest-building material the birds collect mainly from the soil surface. This conclusion relies on the fact that the majority of oribatid mite species found in the nests are common to the taiga forests of the European North. These species are predominantly inhabitants of the soil surface and the upper horizons of the forest litter (Damaeus (Epidamaeus) bituberculatus, Carabodes (C.) subarcticus, Chamobates (C.) pusillus, Neoribates (N.) aurantiacus et al.). Therefore, it is very likely to capture them with pieces of litter, bark, or lichens.
However, it is also possible that some species could have been transferred by birds in feathers from the southern regions where they winter, as well as from stopping places (for feeding and resting) during the migration period, since some of the oribatid mites species (Pergalumna (P.) willmanni, Diapterobates oblongus), found in the nests of the Pied Flycatcher, are rare in the taiga zone. It is known that arthropods, including oribatid mites, have been found in the feathers of migratory birds [9,10,11].
Some species found in nests of the Pied Flycatcher including eurybiontic species, populated nests of small mammals. They are Heminothrus (P.) peltifer (as Platynothrus peltifer), Dissorhina ornata (as Oppia ornata), Suctobelbella (S.) acutidens sarekensis (as Suctobelbella sarekensis), T. velatus, Oribatula tribialis, Scheloribates laevigatus, and Chamobates (C.) pusillus (as Chamobates borealis) [38]. Dissorhina (Oppia) ornata, Oribatula tibialis, and Tectocepheus velatus inhabited nests of waterfowl and semiaquatic birds in the water ecosystems of the Sea of Azov; T. velatus was among the two dominants [39].
Some species found in the nests of the European Pied Flycatcher were previously identified in the nests of passerine birds (Passeriformes). For example, the eurytopic species of Tectocepheus velatus, Oribatula (Z.) exilis, and Scheloribates (S.) laevigatus were found in the nests of Lapland Bunting on the Vaigach island [6]. Five species from the Crotonioidea superfamily, including two species of the Heminothrus genus as H. peltifer and H. longisetosus (Crotoniidae family) were identified in the nests of the ground-nesting Wood Warbler Phylloscopus sibilatrix in Poland [7]. Some oribatid specimens could possibly have been brought to the nests by birds in feathers from the places of migration stops (for feeding and rest) during the flight back home in the spring.
4.2. Zoogeographic Structure of Fauna and Distribution of Species
The zoogeographic structure of fauna was dominated by widespread Holarctic species (12 species, 54.54%). Cosmopolitans and semi-cosmopolitans were also present (four species, 18.18%). Palearctic species accounted for 27.27% (six species). The majority of oribatid species found in nests are common representatives of taiga forests of the European North. They are Carabodes (C.) subarcticus, Neoribates (N.) aurantiacus, Oribatula (O.) tibialis, and other species widely distributed in the Arctic–Boreal zone [29,32,33,35,40].
Some species we found are rare for northern latitudes. For example, Subias [28] characterizes the species Pergalumna (P.) willmanni (Zachvatkin, 1953) as a Palearctic (European: less common in the north, and southwest of Siberia) species. In the European part of Russia, the species is known to inhabit coniferous–deciduous forests, forest-steppe, and steppe [26,29,30]. In the taiga zone of the northeastern part of European Russia, the Ameronothrus oblongus species was previously noted only in epiphytic lichens as a single specimens [35,36]. The Oribatula (Zygoribatula) propinqua species was highly abundant in our samples and was previously among the dominating species in epiphytes of spruce and pine forests [35]. It also is not widely distributed in the North.
5. Conclusions
In total, 135 nests of the European Pied Flycatcher were identified for 1762 specimens of oribatid mites of 22 species. Highly common and numerous in our collections were the Oribatula (Zygoribatula) propinqua (family Oribatulidae) and Scheloribates (S.) laevigatus (Scheloribatidae) species. Rare were the Heminothrus (P.) peltifer, Ameronothrus oblongus, Sphaerozetes piriformis, and Diapterobates oblongus species. They were only found as single specimens.
In the nests of Pied Flycatchers, a complex of species that were previously known as arboricolous for the study region, such as Oribatula (Zygoribatula) propinqua, Oribatula (Zygoribatula) exilis, Trichoribates (T.) berlesei, and Ameronothrus oblongus, was found. We assume that arboricolous, as well as eurytopic, species (Scheloribates (S.) laevigatus, Oribatula (O.) tibialis), can actively populate bird nests. It is also possible that some species of oribatids that are rare in the taiga zone (such as Pergalumna (P.) willmanni, Diapterobates oblongus) could have been brought by birds in their plumage from more southern regions. The findings of numerous oribatid specimens in the “overwintered” nests suggest that they can last over winter in a nest without a nest owner.
Author Contributions
Conceptualization, E.N.M. and N.P.S.; methodology, E.N.M., N.P.S. and A.N.K.; validation, E.N.M. and N.P.S.; formal analysis, A.N.K.; investigation, E.N.M. and N.P.S.; data curation, N.P.S.; writing—original draft preparation, E.N.M., N.P.S. and A.N.K.; writing—review and editing, E.N.M., N.P.S., and A.N.K.; visualization, E.N.M., N.P.S. and A.N.K.; supervision, E.N.M.; project administration, E.N.M. All authors have read and agreed to the published version of the manuscript.
Funding
This research was carried out on the theme of the State Assignment of the Institute of Biology of the Komi Scientific Center of the Ural Branch of the Russian Academy of Sciences “Fauna diversity and spatial and ecological structure of the animal population of the European North-East of Russia and adjacent territories under conditions of environmental change and economic development”, registration No. 122040600025-2.
Institutional Review Board Statement
Not applicable.
Data Availability Statement
Not applicable.
Acknowledgments
The authors are deeply grateful to the student of the Pitirim Sorokin Syktyvkar State University Nikolay Belykh for help in field work and the collection of bio-material.
Conflicts of Interest
The authors declare no conflict of interest.
Appendix A
Table A1.
Life cycle phases and nesting progress of the European Pied Flycatcher in the green zones of Syktyvkar for 2017–2022 (MP—the Michurin Park, KP—the Kirov Park, RBC—the Radiobiological Complex.
Table A1.
Life cycle phases and nesting progress of the European Pied Flycatcher in the green zones of Syktyvkar for 2017–2022 (MP—the Michurin Park, KP—the Kirov Park, RBC—the Radiobiological Complex.
| Nest-Box Number | Nest-Box Location Place | Nesting Start (Date) | Nesting End (Date) | Period the Birds Are in Nest, Days | Period the Birds Are Out of Nest, Days | Breeding Progress (%) | Sampling (Date) |
|---|---|---|---|---|---|---|---|
| 5 | MP | 13 June 2017 | 13 July 2017 | 30 | 307 | 100 | 16 May 2018 |
| 18 | MP | 27 June 2017 | 4 August 2017 | 38 | 285 | 100 | 16 May 2018 |
| 25 | MP | 11 June 2017 | 13 July 2017 | 32 | 307 | 100 | 16 May 2018 |
| 26 | MP | 10 June 2017 | 26 June 2017 | 16 | 324 | 0 | 16 May 2018 |
| 32 | MP | 10 June 2017 | 13 July 2017 | 33 | 307 | 50 | 16 May 2018 |
| 5 | KP | 30 June 2017 | 4 August 2017 | 35 | 285 | 43 | 16 May 2018 |
| 9 | KP | 11 June 2017 | 23 June 2017 | 12 | 285 | 0 | 16 May 2018 |
| 17 | KP | 12 June 2017 | 20 July 2017 | 38 | 300 | 100 | 16 May 2018 |
| 29 | KP | 11 June 2017 | 23 June 2017 | 12 | 327 | 0 | 16 May 2018 |
| 31 | KП | 10 June 2017 | 13 July 2017 | 33 | 307 | 57 | 16 May 2018 |
| б/н | KP | 27 June 2017 | 4 August 2017 | 38 | 285 | 100 | 16 May 2018 |
| 3 | MP | 13 June 2018 | 13 July 2018 | 30 | 7 | 100 | 13 July 2018 |
| 4 | MP | 21 May 2018 | 23 June 2018 | 33 | 13 | 86 | 6 July 2018 |
| 7 | MP | 3 June 2018 | 6 July 2018 | 33 | 7 | 100 | 13 July 2018 |
| 11 | MP | 26 May 2018 | 29 June 2018 | 34 | 7 | 86 | 6 July 2018 |
| 12 | MP | 25 May 2018 | 15 June 2018 | 21 | 21 | 0 | 6 July 2018 |
| 15 | MP | 13 June 2018 | 13 July 2018 | 30 | 7 | 83 | 13 July 2018 |
| 19 | MP | 25 May 2018 | 29 June 2018 | 35 | 13 | 71 | 6 July 2018 |
| 22 | MP | 25 May 2018 | 29 June 2018 | 35 | 13 | 43 | 6 July 2018 |
| 26 | MP | 25 May 2018 | 15 June 2018 | 21 | 21 | 0 | 6 July 2018 |
| 30 | MP | 12 June 2018 | 22 June 2018 | 10 | 14 | 0 | 6 July 2018 |
| 32 | MP | 31 May 2018 | 06 July 2018 | 36 | 7 | 100 | 13 July 2018 |
| 3 | KP | 22 June 2018 | 13 July 2018 | 21 | 19 | 0 | 1 August 2018 |
| 5 | KP | 20 May 2018 | 13 June 2018 | 24 | 7 | 0 | 20 July 2018 |
| 9 | KP | 11 June 2018 | 12 July 2018 | 31 | 7 | 83 | 20 July 2018 |
| 17 | KP | 25 May 2018 | 29 June 2018 | 35 | 7 | 43 | 6 July 2018 |
| 18 | KP | 29 June 2018 | 6 July 2018 | 7 | 14 | 0 | 20 July 2018 |
| 19 | KP | 21 June 2018 | 29 June 2018 | 8 | 21 | 0 | 20 July 2018 |
| 23 | KP | 18 June 2018 | 20 July 2018 | 32 | 7 | 100 | 20 July 2018 |
| 24 | KP | 1 June 2018 | 6 July 2018 | 35 | 13 | 100 | 6 July 2018 |
| 28 | KP | 24 May 2018 | 29 June 2018 | 36 | 7 | 100 | 6 July 2018 |
| 29 | KP | 5 June 2018 | 6 July 2018 | 31 | 7 | 100 | 20 July 2018 |
| 30 | KP | 26 May 2018 | 29 June 2018 | 34 | 13 | 57 | 6 July 2018 |
| 38 | KP | 31 May 2018 | 29 June 2018 | 29 | 7 | 86 | 6 July 2018 |
| 41 | KP | 13 June 2018 | 22 June 2018 | 9 | 6 | 0 | 1 August 2018 |
| 45 | KP | 25 May 2018 | 29 June 2018 | 35 | 7 | 86 | 6 July 2018 |
| 8 | RBC | 8 June 2018 | 12 July 2018 | 34 | 1 | 86 | 13 July 2018 |
| 10 | RBC | 20 May 2018 | 29 June 2018 | 40 | 0 | 71 | 2 July 2018 |
| 11 | RBC | 4 June 2018 | 12 July 2018 | 38 | 0 | 100 | 12 July 2018 |
| 13 | RBC | 29 May 2018 | 6 July 2018 | 38 | 0 | 83 | 6 July 2018 |
| 15 | RBC | 21 May 2018 | 2 July 2018 | 42 | 0 | 100 | 3 July 2018 |
| 2 | MP | 31 May 2019 | 4 July 2019 | 34 | 7 | 43 | 11 July 2019 |
| 4 | MP | 16 May 2019 | 21 June 2019 | 36 | 7 | 86 | 28 June 2019 |
| 9 | MP | 30 May 2019 | 4 July 2019 | 35 | 8 | 88 | 11 July 2019 |
| 14 | MP | 1 June 2019 | 4 July 2019 | 33 | 13 | 17 | 11 July 2019 |
| 19 | MP | 22 May 2019 | 6 June 2019 | 15 | 7 | 0 | 13 June 2019 |
| 29 | MP | 20 May 2019 | 22 June 2019 | 33 | 7 | 50 | 28 June 2019 |
| 32 | MP | 17 May 2019 | 7 June 2019 | 21 | 7 | 0 | 13 June 2019 |
| 1 | KP | 1 June 2019 | 4 July 2019 | 33 | 7 | 71 | 11 July 2019 |
| 3 | KP | 24 June 2019 | 25 July 2019 | 31 | 7 | 20 | 25 July 2019 |
| 6 | KP | 16 May 2019 | 22 June 2019 | 37 | 7 | 67 | 28 June 2019 |
| 9 | KP | 28 June 2019 | 25 July 2019 | 27 | 4 | 25 | 29 July 2019 |
| 18 | KP | 16 May 2019 | 22 June 2019 | 37 | 7 | 70 | 28 June 2019 |
| 19 | KP | 6 June 2019 | 13 July 2019 | 37 | 7 | 89 | 19 July 2019 |
| 20 | KP | 24 May 2019 | 1 June 2019 | 8 | 7 | 0 | 6 June 2019 |
| 23 | KP | 27 May 2019 | 28 June 2019 | 32 | 7 | 63 | 4 July 2019 |
| 24 | KP | 27 May 2019 | 28 June 2019 | 32 | 7 | 0 | 4 July 2019 |
| 28 | KP | 16 May 2019 | 31 May 2019 | 15 | 13 | 0 | 13 June 2019 |
| 29 | KP | 15 May 2019 | 22 June 2019 | 38 | 7 | 88 | 28 June 2019 |
| 37 | KP | 5 June 2019 | 4 July 2019 | 29 | 7 | 43 | 4 July 2019 |
| 38 | KP | 6 June 2019 | 11 July 2019 | 35 | 7 | 100 | 11 July 2019 |
| 45 | KP | 16 May 2019 | 20 June 2019 | 35 | 8 | 100 | 28 June 2019 |
| 2 | RBC | 30 May 2019 | 8 July 2019 | 39 | 0 | 86 | 8 July 2019 |
| 4 | RBC | 3 June 2019 | 8 July 2019 | 35 | 0 | 71 | 8 July 2019 |
| 8 | RBC | 14 June 2019 | 17 July 2019 | 33 | 12 | 100 | 29 July 2019 |
| 9 | RBC | 16 June 2019 | 4 July 2019 | 18 | 4 | 56 | 8 July 2019 |
| 11 | RBC | 15 May 2019 | 28 May 2019 | 13 | 5 | 0 | 5 June 2019 |
| 12 | RBC | 16 June 2019 | 20 June 2019 | 4 | 11 | 0 | 1 July 2019 |
| 13 | RBC | 30 May 2019 | 1 July 2019 | 32 | 8 | 83 | 9 July 2019 |
| 14 | RBC | 30 May 2019 | 4 July 2019 | 35 | 1 | 67 | 9 July 2019 |
| 15 | RBC | 9 June 2019 | 14 July 2019 | 35 | 15 | 83 | 29 July 2019 |
| 2 | MP | 19 May 2020 | 23 June 2020 | 35 | 7 | 71 | 23 June 2020 |
| 4 | MP | 31 May 2020 | 30 June 2020 | 30 | 7 | 86 | 7 July 2020 |
| 12 | MP | 20 May 2020 | 23 June 2020 | 34 | 7 | 71 | 30 June 2020 |
| 17 | MP | 12 June 2020 | 14 July 2020 | 32 | 7 | 60 | 22 July 2020 |
| 18 | MP | 29 June 2020 | 30 June 2020 | 1 | 7 | 0 | 30 June 2020 |
| 19 | MP | 20 May 2020 | 23 June 2020 | 34 | 7 | 71 | 30 June 2020 |
| 25 | MP | 20 May 2020 | 23 June 2020 | 34 | 7 | 63 | 30 June 2020 |
| 28 | MP | 24 May 2020 | 23 June 2020 | 30 | 7 | 0 | 23 June 2020 |
| 31 | MP | 11 June 2020 | 14 July 2020 | 33 | 7 | 67 | 14 July 2020 |
| 33 | MP | 29 May 2020 | 17 June 2020 | 19 | 7 | 0 | 23 June 2020 |
| 1 | KP | 19 May 2020 | 23 June 2020 | 35 | 7 | 71 | 30 June 2020 |
| 3 | KP | 22 May 2020 | 23 June 2020 | 32 | 7 | 0 | 23 June 2020 |
| 8 | KP | 21 May 2020 | 23 June 2020 | 33 | 7 | 0 | 23 June 2020 |
| 9 | KP | 27 May 2020 | 23 June 2020 | 27 | 7 | 29 | 7 July 2020 |
| 14 | KP | 21 May 2020 | 30 June 2020 | 40 | 7 | 0 | 30 June 2020 |
| 19 | KP | 9 June 2020 | 7 July 2020 | 28 | 15 | 20 | 22 July 2020 |
| 23 | KP | 29 May 2020 | 14 July 2020 | 46 | 8 | 0 | 22 July 2020 |
| 24 | KP | 23 May 2020 | 23 June 2020 | 31 | 7 | 0 | 23 June 2020 |
| 28 | KP | 6 June 2020 | 8 July 2020 | 32 | 7 | 33 | 14 July 2020 |
| 29 | KP | 18 May 2020 | 23 June 2020 | 36 | 7 | 100 | 23 June 2020 |
| 41 | KP | 13 June 2020 | 22 July 2020 | 39 | 7 | 0 | 28 July 2020 |
| 43 | KP | 28 May 2020 | 1 July 2020 | 34 | 7 | 100 | 7 July 2020 |
| 2 | RBC | 23 May 2020 | 29 June 2020 | 37 | 7 | 86 | 30 June 2020 |
| 5 | RBC | 27 May 2020 | 30 June 2020 | 34 | 0 | 86 | 30 June 2020 |
| 6 | RBC | 28 May 2020 | 30 June 2020 | 33 | 3 | 71 | 3 July 2020 |
| 8 | RBC | 24 May 2020 | 29 June 2020 | 36 | 1 | 75 | 30 June 2020 |
| 10 | RBC | 28 May 2020 | 30 June 2020 | 33 | 3 | 83 | 3 July 2020 |
| 12 | RBC | 15 May 2020 | 22 June 2020 | 38 | 0 | 100 | 22 June 2020 |
| 13 | RBC | 23 May 2020 | 26 June 2020 | 34 | 0 | 100 | 26 June 2020 |
| 15 | RBC | 9 June 2020 | 14 July 2020 | 35 | 0 | 83 | 14 July 2020 |
| 4 | MP | 11 June 2021 | 12 July 2021 | 31 | 7 | 100 | 12 July 2021 |
| 5 | MP | 22 May 2021 | 1 June 2021 | 10 | 7 | 0 | 7 June 2021 |
| 10 | MP | 20 May 2021 | 14 June 2021 | 25 | 15 | 100 | 29 June 2021 |
| 14 | MP | 21 May 2021 | 23 June 2021 | 33 | 6 | 63 | 29 June 2021 |
| 18 | MP | 9 June 2021 | 12 July 2021 | 33 | 7 | 100 | 12 July 2021 |
| 21 | MP | 25 May 2021 | 29 June 2021 | 35 | 6 | 89 | 5 July 2021 |
| 25 | MP | 2 June 2021 | 14 June 2021 | 12 | 9 | 0 | 23 June 2021 |
| 28 | MP | 25 May 2021 | 29 June 2021 | 35 | 7 | 86 | 29 June 2021 |
| 30 | MP | 6 June 2021 | 29 June 2021 | 23 | 7 | 0 | 5 July 2021 |
| 32 | MP | 17 May 2021 | 17 May 2021 | 0 | 20 | 0 | 23 June 2021 |
| 3 | KP | 19 May 2021 | 23 June 2021 | 35 | 7 | 100 | 23 June 2021 |
| 8 | KP | 11 June 2021 | 12 July 2021 | 31 | 7 | 80 | 19 July 2021 |
| 9 | KP | 19 May 2021 | 23 June 2021 | 35 | 9 | 100 | 23 June 2021 |
| 14 | KP | 17 May 2021 | 23 June 2021 | 37 | 9 | 86 | 23 June 2021 |
| 19 | KP | 25 May 2021 | 29 June 2021 | 35 | 6 | 83 | 29 June 2021 |
| 20 | KP | 10 June 2021 | 12 July 2021 | 32 | 7 | 100 | 12 July 2021 |
| 23 | KP | 20 May 2021 | 23 June 2021 | 34 | 9 | 100 | 29 June 2021 |
| 28 | KP | 28 May 2021 | 29 June 2021 | 32 | 6 | 100 | 5 July 2021 |
| 29 | KP | 19 May 2021 | 23 June 2021 | 35 | 9 | 100 | 23 June 2021 |
| 31 | KP | 30 May 2021 | 1 July 2021 | 32 | 6 | 0 | 7 June 2021 |
| 43 | KP | 17 May 2021 | 17 May 2021 | 0 | 29 | 0 | 14 June 2021 |
| 45 | KP | 21 May 2021 | 1 July 2021 | 41 | 6 | 0 | 7 June 2021 |
| 1 | RBC | 18 May 2021 | 23 June 2021 | 36 | 1 | 86 | 24 June 2021 |
| 4 | RBC | 17 May 2021 | 24 June 2021 | 38 | 0 | 100 | 24 June 2021 |
| 8 | RBC | 1 June 2021 | 30 June 2021 | 29 | 4 | 83 | 2 July 2021 |
| 9 | RBC | 18 May 2021 | 24 June 2021 | 37 | 0 | 100 | 24 June 2021 |
| 11 | RBC | 10 June 2021 | 12 July 2021 | 32 | 3 | 75 | 14 July 2021 |
| 12 | RBC | 17 May 2021 | 21 June 2021 | 35 | 0 | 86 | 21 June 2021 |
| 15 | RBC | 18 May 2021 | 21 June 2021 | 34 | 3 | 67 | 21 June 2021 |
| 2 | RBC | 4 June 2022 | 7 July 2022 | 33 | 0 | 100 | 8 July 2022 |
| 8 | RBC | 29 May 2022 | 30 June 2021 | 32 | 3 | 83 | 4 July 2022 |
| 11 | RBC | 2 June 2022 | 5 July 2022 | 33 | 2 | 86 | 7 July 2022 |
| 12 | RBC | 5 June 2022 | 7 July 2022 | 32 | 1 | 100 | 11 July 2022 |
| 14 | RBC | 30 May 2022 | 4 July 2022 | 35 | 4 | 100 | 4 July 2022 |
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Figure 1.
Distribution map of the European Pied Flycatcher according to the Red List data (https://www.iucnredlist.org, accessed: 25 January 2023).
Figure 1.
Distribution map of the European Pied Flycatcher according to the Red List data (https://www.iucnredlist.org, accessed: 25 January 2023).
Figure 2.
The nests of the European Pied Flycatcher at different nesting stages: (a) eggs, (b) chicks, (c) fledglings.
Figure 2.
The nests of the European Pied Flycatcher at different nesting stages: (a) eggs, (b) chicks, (c) fledglings.
Figure 3.
Comparison of three sites samples (KP—Kirov Park, MP—Michurin City Park, RBC—the Radiobiological Complex) by diversity indices, based on the results of 2018-2022 (excluding overwintered nests 2017).
Figure 3.
Comparison of three sites samples (KP—Kirov Park, MP—Michurin City Park, RBC—the Radiobiological Complex) by diversity indices, based on the results of 2018-2022 (excluding overwintered nests 2017).
Figure 4.
The number of oribatid mites in the RBC site in different months of observation in 2018 (2017—overwintered nests, 2018—nests collected in summer).
Figure 4.
The number of oribatid mites in the RBC site in different months of observation in 2018 (2017—overwintered nests, 2018—nests collected in summer).
Table 1.
Taxonomic composition of oribatid mites in the nests of the European Pied Flycatcher.
| Title 1 | Life Forms | Distribution | N | D% | F% |
|---|---|---|---|---|---|
| Trhypochthoniidae Willmann, 1931 Trhypochthonius tectorum s. str. (Berlese, 1896) | |||||
| hemiedaphic | Semi-cosmopolitan | 4 | 0.23 | 1.54 | |
| Crotoniidae Thorell, 1876 Heminothrus (Platynothrus) peltifer s. str. (Koch, 1839) | |||||
| hemiedaphic | Semi-cosmopolitan | 2 | 0.11 | 1.54 | |
| Damaeidae (Berlese, 1896) | |||||
| Damaeus (Epidamaeus) bituberculatus (Kulczynski, 1902) | epigeic | Palearctic | 30 | 1.7 | 9.23 |
| Liacaridae Sellnick, 1928 | |||||
| Adoristes (A.) ovatus (Koch, 1839) | epigeic | Holarctic | 3 | 0.17 | 1.54 |
| Oppiidae (Sellnick, 1937) | |||||
| Dissorhina ornata s. str. (Oudemans, 1900) | euedaphic | Holarctic | 31 | 1.77 | 6.15 |
| Graptoppia (Apograptoppia) foveolata (Paoli, 1908) | euedaphic | Holarctic | 17 | 0.96 | 4.61 |
| Suctobelbidae Jacot, 1938 | |||||
| Suctobelbella (S.) acutidens sarekensis (Forsslund, 1941) | euedaphic | Holarctic | 2 | 0.11 | 1.54 |
| Carabodidae Koch, 1843 | |||||
| Carabodes (C.) subarcticus Trägårdh, 1902 | epigeic | Palearctic | 8 | 0.45 | 3.08 |
| Tectocepheidae (Grandjean, 1954) | |||||
| Tectocepheus velatus (Michael, 1880) | eurybiontic | Cosmopolitan | 13 | 0.74 | 3.08 |
| Ameronothridae Vitzthum, 1943 | |||||
| Ameronothrus oblongus Sitnikova, 1975 | hydrobiontic | Holarctic | 1 | 0.06 | 1.54 |
| Ceratozetidae Jacot, 1925 | |||||
| Melanozetes mollicomus (Koch, 1839) | epigeic | Holarctic | 9 | 0.51 | 3.08 |
| Sphaerozetes piriformis (Nicolet, 1855) | epigeic | Palearctic | 3 | 0.17 | 1.54 |
| Trichoribates (T.) berlesei (Jacot, 1929) | epigeic | Holarctic | 4 | 0.23 | 4.61 |
| Chamobatidae Thor, 1937 | |||||
| Chamobates (C.) pusillus (Berlese, 1895) | epigeic | Holarctic | 7 | 0.40 | 4.61 |
| Humerobatidae Grandjean, 1971 | |||||
| Diapterobates oblongus (L. Koch, 1879) | epigeic | Palearctic | 9 | 0.51 | 6.15 |
| Diapterobates humeralis (Hermann, 1804) | epigeic | Holarctic | 7 | 0.40 | 3.08 |
| Oribatulidae Thor, 1929 | |||||
| Oribatula (Oribatula) tibialis (Nicolet, 1855) | eurybiontic | Holarctic | 21 | 1.19 | 7.69 |
| Oribatula (Zygoribatula) exilis (Nicolet, 1855) | eurybiontic | Holarctic | 76 | 4.31 | 9.23 |
| Oribatula (Z.) propinqua (Oudemans, 1902) | eurybiontic | Palearctic | 1006 | 57.09 | 41.53 |
| Scheloribatidae Grandjean, 1933 | |||||
| Scheloribates (S.) laevigatus (Koch, 1835) | eurybiontic | Semi-cosmopolitan | 487 | 27.64 | 30.77 |
| Parakalummidae Grandjean, 1936 | |||||
| Neoribates (N.) aurantiacus (Oudemans, 1914) | epigeic | Holarctic | 15 | 0.85 | 3.08 |
| Galumnidae Jacot, 1925 | |||||
| Pergalumna (P.) willmanni (Zachvatkin, 1953) | epigeic | Palearctic | 7 | 0.40 | 4.61 |
| Total | 1762 | 100 | |||
Note. N number of specimens; D% dominance; F% frequency of occurrence in samples.
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Melekhina, E.N.; Korolev, A.N.; Selivanova, N.P. Oribatid Mites (Oribatida) Associated with Nests of Hollow-Nesting Birds, on the Example of a Model Species, the European Pied Flycatcher (Ficedula hypoleuca), in the Taiga Forests of the European North-East of Russia. Diversity 2023, 15, 765. https://doi.org/10.3390/d15060765
AMA Style
Melekhina EN, Korolev AN, Selivanova NP. Oribatid Mites (Oribatida) Associated with Nests of Hollow-Nesting Birds, on the Example of a Model Species, the European Pied Flycatcher (Ficedula hypoleuca), in the Taiga Forests of the European North-East of Russia. Diversity. 2023; 15(6):765. https://doi.org/10.3390/d15060765
Chicago/Turabian StyleMelekhina, Elena N., Andrey N. Korolev, and Natalia P. Selivanova. 2023. "Oribatid Mites (Oribatida) Associated with Nests of Hollow-Nesting Birds, on the Example of a Model Species, the European Pied Flycatcher (Ficedula hypoleuca), in the Taiga Forests of the European North-East of Russia" Diversity 15, no. 6: 765. https://doi.org/10.3390/d15060765
APA StyleMelekhina, E. N., Korolev, A. N., & Selivanova, N. P. (2023). Oribatid Mites (Oribatida) Associated with Nests of Hollow-Nesting Birds, on the Example of a Model Species, the European Pied Flycatcher (Ficedula hypoleuca), in the Taiga Forests of the European North-East of Russia. Diversity, 15(6), 765. https://doi.org/10.3390/d15060765
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