Abstract
The wood warbler, Phylloscopus sibilatrix (Aves: Passeriformes), is a well-known model organism for studying bird migration, breeding habitat selection and nest predation. The nest acarofauna of this bird species has not been extensively studied so far. To provide a comprehensive report on mite species inhabiting wood warbler nests and to assess infestation parameters (prevalence, intensity, and abundance) for mite species and orders, we collected 45 nests of this bird species in the Wielkopolska National Park in western Poland. Analyses revealed a huge diversity (198 species) of mites inhabiting wood warbler nests. We found individuals belonging to the Mesostigmata, Trombidiformes and Sarcoptiformes. The Trombidiformes, represented in our study only by the Prostigmata, achieved statistically significantly lower intensity and abundance, compared to representatives of other orders. However, the number of recorded prostigmatid species was high (65). The most common were: Stigmaeus sphagneti (22 nests), Stigmaeus longipilis (16), Eupodes voxencollinus (15), Cunaxa setirostris (14), Stigmaeus pilatus (11), and Linopodes sp. 2 (10). The prevalence of Mesostigmata and Sarcoptiformes was equal, reaching 91.1%. Most of Gamasina (Mesostigmata) species found in this study were more characteristic of the soil environment and forest litter than bird nests, but there was also a typical bird parasite, viz. Ornithonyssus sylviarum. None of the observed species of Uropodina (Mesostigmata) or Oribatida (Sarcoptiformes) was typical for bird nests. Among the Uropodina, the highest parameters of nest infestation were achieved by Oodinychus ovalis, whereas among the Oribatida, they were achieved by Metabelba pulverosa. We discuss the importance of wood warbler nests for mite dispersal, survival and reproduction.
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Introduction
Mites are among the most diverse groups of invertebrate taxa and occupy a wide range of environments. Among many different microhabitats, mites inhabit nests and burrows of vertebrates where they act as ectoparasites, free-living predators, or as edaphic or coprophilous organisms (e.g., Proctor and Owens 2000; Mašán and Stanko 2005; Celebias et al. 2019). The mites common and typical for birds of nests and small mammals are called nidicolous (Napierała and Błoszyk 2013). To date, most attention has been paid to mite fauna inhabiting nests of mammals (e.g., rodents, moles) and birds, such as storks, eagles, owls, pigeons, sea birds, and some passerine species (Kaźmierski 1998a; Gwiazdowicz et al. 1999; Kristofik et al. 2002, 2005; Błoszyk et al. 2005; Pilskog et al. 2014; Napierała et al. 2016; Kaminskienė et al. 2017; Kaźmierski et al. 2018, 2021; Celebias et al. 2019). Those studies showed that the type of nest and the period when the nest is used play an important role in shaping mite assemblage structure. Mites are more abundant in yearly reused nests than in 1-year nests, as the latter are more ephemeral microhabitats, available only for a short time, i.e., during birds’ breeding period (e.g., Mašán et al. 2014).
Bird nests amaze us with a diversity of forms, occupied places, structures and building materials used, and provide various abiotic and biotic conditions for invertebrates. For example, the scrape-nest represents the simplest type of nest built in the ground as a shallow depression for the birds to lay their eggs. Birds that build scrape-nests tend to have precocial chicks that are able to leave the nest quickly after hatching (Campbell and Lack 1985; Reid et al. 2002). In nests of this type, the abundance of mites and the complexity of their communities are rather low (Ambros et al. 1992). In contrast, burrow nests and mound nests provide shelters that allow rapid mite development and reproduction, and in nests of these types, mite densities are usually high (Woodroffe 1953; Ambros et al. 1992; Fend’a 2010). Mound nests are often made from mud, branches, sticks, twigs, and leaves. When organic material of the nest begins to decay, the compost pile heats up and gives off heat to incubate the chicks (Campbell and Lack 1985; Hansell and Overhill 2000; Deeming and Reynolds 2015). Probably such conditions make mound nests attractive and suitable for invertebrates, including mites as has been shown for pigeon nests (Woodroffe 1953).
Mites inhabit also cup nests (Møller 1990; Mašán et al. 2014), platform nests (Gwiazdowicz et al. 1999), natural cavity nests (Pung et al. 2000), and artificial nest boxes (Stamp et al. 2002; Błoszyk et al. 2016) used by cavity nesters when natural cavities cannot be found (Campbell and Lack 1985). Observations carried out in platform nests showed that the abundance of invertebrates in nests yearly reused by birds, with additional building material added to the nest structure, was higher than in one-season nests (Błoszyk et al. 2005, 2009; Gwiazdowicz et al. 2005, 2006).
Thus, the nest characteristics, such as shape, building material (Pilskog et al. 2014; Gwiazdowicz et al. 2022), annual use or reuse (Gwiazdowicz et al. 1999; Błoszyk et al. 2009), and nest location (Ambros et al. 1992) influence the composition and abundance of mite fauna. When birds nest on the ground (Campbell and Lack 1985), they provide an easily available area to be inhabited by mites, especially by mite species associated with litter (Fenďa and Schniererová 2005). Such nests may be colonized by free-living or nidicolous mites but also by ectosymbiotic mite species including parasites, which are, at least seasonally, dependent on the presence of their bird host (Coulson et al. 2009). Other important factors affecting mite community composition in bird nests are the geographical region and climate. For example, in nests of snow buntings [Plectrophenax nivalis (L.)], located in the Arctic region (Spitsbergen, Svalbard), mainly females of the mite Dermanyssus hirundinis (Hermann) occur in large densities, whereas in other regions, nests of this bird species are inhabited by a greater diversity of mite taxa (Gwiazdowicz et al. 2012).
One of the bird species that builds nests exclusively on the ground is the wood warbler, Phylloscopus sibilatrix (Bechstein). This passerine, belonging to the family Phylloscopidae, is a small (~ 10 g) insectivorous, migratory songbird, with breeding grounds spanning northern and temperate Europe, as well as Central Asia (Cramp 1992). It is assumed to be a common bird, but in recent years scientists have observed declining trends in some regions, although the reasons of these trends are not sufficiently understood (Mallord et al. 2012a, b; Vickery et al. 2014; Mallord et al. 2016, 2017). The wood warbler is a forest-dwelling species, inhabiting mainly deciduous and mixed forests. Nests are dome-shaped, have a horizontally-oriented entrance, and are concealed usually among low herb vegetation in shady places, often near fallen branches or logs. Nests are constructed each season from plant materials, with the external layer of the nest made of decayed tree leaves or grasses, and mites have an opportunity to inhabit the nests at the beginning of the breeding season (Wesołowski 1985). Mites may colonize the nest directly from the ground but they can also be transported with nest-building material. So far, studies on wood warbler ecology have mainly focused on migration, breeding habitat selection and nest predation (Bellamy et al. 2018; Tøttrup et al. 2018). The nest fauna of this bird species has not been studied extensively. Some studies show that ants are frequently present in wood warbler nests (Maziarz et al. 2018), which can be associated with the thermal activity of the birds warming their nests (Maziarz et al. 2020, 2021). Among mites, only the Uropodina and Crotonioidea inhabiting wood warbler nests have been investigated so far (Napierała et al. 2021).
In this study we expand the knowledge on mite species colonizing wood warbler nests, taking into consideration all mite taxa, belonging to superorders Parasitiformes and Acariformes, found in nests during comprehensive sampling. Such knowledge is crucial to recognize the capability of mites to colonize ephemeral microhabitats that are available only for a few months every year. Such research is an essential foundation for studying intraspecific (mites-mites) and interspecific (mites-mites, mites-birds) interactions that may influence mite presence and abundance, and for explaining the role of 1-year nests as microhabitats for mites. Our aims were to (i) provide a comprehensive report on mite species inhabiting wood warbler nests, and (ii) assess infestation parameters (prevalence, intensity, and abundance) for mite species and higher taxa, to increase faunistic and ecological knowledge regarding these specific microhabitats.
Materials and methods
Study area
The study was conducted in the Wielkopolska National Park (WNP) in western Poland (52°13ʹ39.4ʹʹ–52°19ʹ08.0ʹʹ N, 16°32ʹ00.0ʹʹ–16°46ʹ08.0ʹʹ E). WNP covers an area of 75.84 km2, dominated by forests (61%) and farmland (ca. 30%) with a mosaic of fields, meadows, and wastelands. Forest habitats consist mainly of mixed forests dominated by pedunculate oak, Quercus robur L., sessile oak, Quercus petraea (Matt.) Liebl, or Scots pine, Pinus sylvestris L. In the WNP, wood warblers are found predominantly in mature oak-dominated and mixed oak-pine forests with a closed canopy, intermediate herb-layer cover, and bushes or trees branched in the lower stem area serving as song-posts (Szymkowiak et al. 2016, 2017; Szymkowiak and Kuczyński 2017).
Collection of wood warbler nests
In 2013, territorial wood warblers were monitored in the WPN from mid-April to early July for a different study (see Szymkowiak et al. 2016 for details). After fledging or nest failure, we carefully collected the whole nest, placed it in a plastic string bag, and brought it to the laboratory for further processing. Nests were of sizes typical for this bird species (ca. 15 cm diameter). If the nest structure was damaged by a predator (eight incidents), all material that could be unambiguously assigned as nest remnants was collected. In total, we analyzed 45 wood warbler nests. In the laboratory, the microarthropod fauna was extracted using Berlese funnels with a mesh size of approximately 2 mm, under 40 W light bulbs, into 96% alcohol for 5 days until the nests were completely dry.
Preparation and identification of mite taxa
Samples containing mite specimens stored in alcohol were inspected under stereomicroscopes and specimens belonging to different orders were counted and collected to separate vials. Subsequently, specimens were prepared for taxonomic identification to species by mounting on slides according to methods specific to each taxonomic group. We counted individuals representing the following taxa: superorder, order, suborder, cohort (in the case of Mesostigmata), family and species according to the systematic classification of Lindquist et al. (2009). Both adult and juvenile forms were counted, and juveniles were identified to the species level whenever possible, i.e., for Mesostigmata and Prostigmata.
Mesostigmata
The Sejida and Gamasida were mounted on permanent (Hoyer’s medium) and semipermanent (lactic acid) slides. The specimens were counted and examined under a microscope (Zeiss Axioscop 2), and identified using Ghilarov and Bregetova (1977), Karg (1993) and Gwiazdowicz (2007, 2010). Specimens of the Uropodina were mounted on semipermanent slides (lactic acid and glycerin) under a stereomicroscope (Olympus SZX16) and light microscope (Olympus BX53), and identified with Hirschmann and Zirngiebl-Nicol (1961), Kramer (1882), Karg (1989), Błoszyk (1999) and Mašán (2001).
Trombidiformes
Mite specimens were mounted in Berlese medium on microscope slides and thereafter stored in 70% alcohol. Mounted specimens were examined with phase contrast microscopes (Zeiss Peraval Inter-FAKO and Olympus BX91 Nomarski), and identified with Kuznetzov (1978a, b), Zacharda (1980), Michocka (1987), Smiley (1992), Kaźmierski (1998a, b), Jesionowska (2010), Skvarla et al. (2014), Hernandes et al. (2016), Silva et al. (2016), and Kaźmierski et al. (2021).
Sarcoptiformes
Mite specimens were cleaned for 24 h in lactic acid at room temperature (ca. 25 °C), mounted on temporary cavity slides for identification, and thereafter stored in 70% ethanol in vials. Individuals were identified with a microscope (Olympus BX51), using the key and descriptions in Weigmann (2006). Species nomenclature followed Subías (2004, updated 2022), Weigmann (2006), and Niedbała (2008).
Statistical analysis
We calculated infestation indices for higher taxa (superorders and orders) and for each mite species. The following parameters were used (following Bush et al. 1997; Skoracka and Kuczyński 2012):
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prevalence the percentage of nests infested, interpreted as the probability of finding the mite taxon in a random nest;
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intensity the mean number of mite specimens of a given mite taxon found in an infested nest, interpreted as population density in nests occupied by that taxon; and
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abundance the mean number of mite specimens of a given taxon found in all nests, expressed in the same units as intensity (no. of individuals per nest), but reflecting population density across all potentially available nests.
Confidence intervals (95% CI) for prevalence were calculated using the profile likelihood method. Confidence intervals for abundance and intensity were calculated using a bias-corrected and accelerated bootstrap (Efron and Tibshirani 1993). All computations were made in R v.4.1 (R Foundation for Statistical Computing, Vienna, Austria, 2022).
Results
The probability (P) of finding members of the Acariformes (represented by the Trombidiformes and Sarcoptiformes) as well as the intensity of nest infestation (I) and abundance (A) were similar to those of the Parasitiformes (represented by the Mesostigmata): P: 93.3% (95% CI 83.6–98.3%) vs. 91.1% (80.5–97.1%); I: 190.1 (153.5–226.8) vs. 110.0 (51.5–382.6); A: 177.4 (140.8–216.0) vs. 100.3 (46.5–312.3). Mites belonging to the orders Mesostigmata, Sarcoptiformes, and Trombidiformes had similar prevalence, whereas intensity and abundance of the Trombidiformes were much lower compared to the other two orders (for details see Fig. 1).
Parameters of infestation by mite species belonging to the Mesostigmata, Trombidiformes, and Sarcoptiformes are presented in Tables 1, 2 and 3. Among Mesostigmata, representatives of suborders Sejida and Monogynaspida were observed. The Sejida were represented solely by Sejus togatus C.L. Koch, whereas the Monogynaspida were represented by two cohorts: Uropodina (five species belonging to four families) and Gamasina (52 species belonging to 15 families) (Table 1).
The Trombidiformes were represented only by the suborder Prostigmata, which was characterized by high overall richness (65 species belonging to 14 families). The highest prevalence (> 20% up to almost 50%) was observed for Stigmaeus sphagneti (Hull) (22 nests), Stigmaeus longipilis (Canestrini) (16), Eupodes voxencollinus Thor (15), Cunaxa setirostris (Hermann) (14), Stigmaeus pilatus Kuznetsov (11), and Linopodes sp. 2 (10) (Table 2).
Within the Sarcoptiformes, 73 species belonging to 35 families of the suborder Oribatida and two species belonging to two families of the suborder Endeostigmata were recorded (Table 3).
Discussion
Our extensive investigation of wood warbler nests resulted in the identification of a huge diversity of mites (198 species) occurring in this ephemeral, single-season microhabitat. Representatives of both mites’ phylogenetic lineages—the Parasitiformes and Acariformes—were present in the nests. Considering the order level, the probability of finding representatives belonging to the Mesostigmata, Sarcoptiformes, and Trombidiformes was high (prevalence ≥ 80%). However, the Trombidiformes, represented in our study only by the Prostigmata, achieved significantly lower levels of intensity and density, as compared to members of the other orders. This suggests that although the Prostigmata can easily and frequently enter wood warbler nests, their survival or reproduction may be restricted, e.g., due to unsuitable abiotic conditions or competition with representatives of other mite orders, which attain much higher densities. Another scenario is that the Prostigmata generally are less abundant than representatives of other taxa in the soil, from which they can move to the nests. For example, Dziuba (1966) showed that in Poland, regardless of the cultivated plant and soil structure, the Trombidiformes (including Prostigmata) were the least numerous group of soil mites, whereas the Mesostigmata dominated in soils with inferior (compact) structure and the Sarcoptiformes dominated in soils with better (granular) structure. The monitoring of soil mites in various agroecosystems and forest ecosystems in Kenya revealed that Prostigmata mites were less abundant than the Oribatida and Mesostigmata (Maribie et al. 2011). Similarly, in natural soil of Argentina the Oribatida and Mesostigmata were more numerous than the Prostigmata (Bedano et al. 2005). Hasegawa et al. (2013) analysed the soil communities of Mesostigmata, Prostigmata, and Oribatida in broad-leaved regeneration forests and conifer plantations in Japan, and demonstrated that oribatid mites dominated in terms of densities and species richness for both forest types.
Among mites belonging to the Mesostigmata we found representatives of the suborders Sejida and Monogynaspida. From the suborder Sejida, only S. togatus was recorded. It inhabits various microhabitats, such as forest litter, rotting wood, ant nests, and bark beetle feeding grounds (Gwiazdowicz 2010). Although it was previously found in nests of white-tailed eagle, Haliaeetus albicilla (L.), it is not considered to be closely associated with microhabitats of nest birds (Gwiazdowicz et al. 2005). Low nest infestation parameters of S. togatus in our study support the suggestion that this species is not typical for bird nests.
From the suborder Monogynaspida, representatives of the cohorts Uropodina and Gamasina were identified in the wood warbler nests. More than 50 species of Gamasina were recorded, most of which usually inhabit forest litter and rotting wood. Only a few species indicated in the analyzed material were previously found in bird nests. In this context, it is worth mentioning that the parasite Ornithonyssus sylviarum (Canestrini et Fanzago) has been found in nests of many bird species, e.g., barn swallow (Hirundo rustica L.), greenfinch (Chloris chloris L.), rook (Corvus frugilegus L.), or song thrush (Turdus philomelos Brehm) (Micherdziński 1980). This blood-sucking mite also affects various domestic birds, including chickens, ducks, pigeons, parrots, and canaries, and is increasingly found to cause problems in aviaries and the poultry industry (Knee and Proctor 2007; Murillo and Mullens 2017). In the material we analyzed, O. sylviarum occurred in 11 nests, so the probability of finding this species in wood warbler nests was > 24%. In addition, several species known from the nests of other bird species were also found in this study, but their numbers were low. For example, Alliphis halleri (G. et R. Canestrini) and Parasitus fimetorum (Berlese), occurring in huge numbers in the nests of Haliaeetus albicilla L. (Gwiazdowicz et al. 2006), were found sporadically in the analyzed material. Although the probability of finding A. halleri in wood warbler nests was > 35%, the intensity of infestation and density were very low. Therefore, most Gamasina found in this study are more characteristic for the soil environment and forest litter than for bird nests.
Representatives of the Uropodina can be found at all latitudes, except polar regions. They occur wherever organic matter accumulates, and inhabit diverse habitats from coastal and inland dunes to rocky grasslands at the highest elevations. Although they clearly prefer the litter and soil of different types of forest ecosystems, they are just as likely to inhabit ephemeral microhabitats (merocenoses), such as cavities, dead wood, anthills, bird and mammal nests, and feces (Błoszyk 1999). Some members of the Uropodina colonize both annual bird nests and perennial nests of birds of prey and storks (Błoszyk and Olszanowski 1985; Błoszyk et al. 2005, 2006, 2009, 2016). Among the nearly 150 species of the Uropodina in Poland, 28 were found to be closely associated with bird nests (Napierała and Błoszyk 2013). In this study, only five Uropodina species were found in wood warbler nests in the Wielkopolska National Park: four of them were relatively frequent (prevalence 31–73%), and two of them had quite high intensity of infestation and density, compared to other Mesostigmata species and species belonging to two other orders. However, none of these species was a typical nidicole; instead, all were representatives of soil fauna. A similar outcome has been reported by Napierała et al. (2021), who studied wood warbler nests in Białowieża Forest. Akin to Napierała et al. (2021), in our study Oodinychus ovalis (CL Koch) achieved the highest parameters of infestation, compared to other species found in wood warbler nests. This is probably due to the fact that it is a highly genetically polymorphic species and the most numerous representative of the Uropodina in Poland. It occurs as often in the soil as in deadwood merocenoses (Błoszyk et al. 2019). Additionally, the fauna of the Uropodina in our study was notably less diverse than the Uropodina fauna found in wood warbler nests in Białowieża Forest, which included 14 species (Napierała et al. 2021).
The order Trombidiformes (represented by the Prostigmata) is an ecologically heterogeneous group of mites. They are cosmopolitan and occur in a myriad of microhabitats, including nests of vertebrates. The mites also remarkably vary in food preference, feeding behavior, and biotic associations. Some of them are predators, others are scavengers (saprophagous), and others are phytophagous or parasitic. In our study the suborder Prostigmata was characterized by high prevalence and overall richness, but very low density and intensity of infestation. The highest probability of finding prostigmatid species in wood warbler nests was for Stigmaeus sphagneti, S. longipilis, S. pilatus, Eupodes voxencollinus, Cunaxa setirostris, and Linopodes sp. 2. These common species are known from various environments, but they prefer mosses and lichens, which are used by the wood warbler to build its nest. This may explain their high prevalence in nests – they were simply brought along with the building material. Their low density and intensity of infestation may result from unsuitable abiotic conditions or negative biotic interactions, e.g., competition. The other species were recorded from a few or even single nests, which may suggest that they were accidental. Among these accidental species, we found representatives of a new genus, which indicates that the Prostigmata fauna in the soil, litter or vegetation surrounding warbler nests still hides undescribed species.
The Oribatida (Sarcoptiformes) are an extremely diverse and dominant group of mites, mainly in the soil organic layer in temperate forest. They can be found wherever dead organic matter occurs, specifically in mosses, lichens, rock cavities, tree crowns, on herbaceous plants, in rotting wood, and in bird and mammal nests. Most of them are saprophagous and fungivorous (Walter and Proctor 2013). In our study we found 73 species of oribatids, some with relatively medium or high infestation parameters. Wood warbler nests are built directly on the ground from organic debris, grass, moss, and dry branches. Therefore, the presence of all these oribatid species was, most likely, accidental and associated with materials gathered by the birds for nest building. We found no species typical of bird nests nor any species which could have symbiotic relationships with birds. All the species we found are common in Poland, and most of them have a Palearctic distribution. Interestingly, the diversity of ptyctimous oribatids in wood warbler nests in our study (11 species) was much lower than that found in wood warbler nests in Białowieża Forest (20 species) (Wojciech Niedbała, unpubl. data)—an outcome similar to that of uropodine mites. We did not find the following species that were present in nests investigated in Białowieża Forest: Mesoplophora pulchra Sellnick, Phthiracarus boresetosus Jacot, Phthiracarus clavatus Parry, Phthiracarus compressus Jacot, Phthiracarus globosus C.L. Koch, Steganacarus applicatus (Sellnick), Steganacarus magnus (Nicolet), Steganacarus spinosus (Sellnick). This difference likely results from higher species richness of mites and more diverse habitats in Białowieża Forest, compared to Wielkopolska National Park.
The presence of invertebrates in nests may lead to the evolution of different relationships (e.g., commensal or mutualistic) between birds and invertebrate nest inhabitants. For example, ants are attracted to wood warbler nests by the heat generated by the host (Maziarz et al. 2020). The occurrence of mites in nests may also be the first step to parasitism on birds. For example, the prostigmatid Speleognathinae (Ereynetidae, Tydeoidea), which live as parasites in bird nostrils, likely originated from free-living ancestors inhabiting the nests (Kaźmierski et al. 2018). In another ereynetid subfamily, Ereynetinae, a tendency to parasitism is also observed: Ricardoella limacum (Schrank) lives in the mantle cavity of pulmonary snails (Turk and Phillips 1946; Karbarz-Wiktorowicz 1973), whereas Hydranetes tropisternus Kethley infects water beetles (Kethley 1971). Undoubtedly, the cohabitation of birds and nest-dwelling invertebrates may stimulate the evolution of interspecific interactions (Maziarz et al. 2020). Such relationships are poorly studied. A quantitative report, such as the present one, can be an important first step for such investigations, by indicating which mite species are accidental and which potentially interact with the bird host or benefit from the nesting conditions.
One such benefit may be an increase of mite dispersal potential. During nest building, by collecting and bringing various kinds of material (mosses, lichens, grass, etc.), wood warblers may play an important role in mite dispersal. Mites themselves cannot actively travel long distances because of their small size and lack of wings. With building material, however, they can be transferred over a distance of several dozen meters or so, and in this way wood warblers collecting nest material from various places may increase the possibility of contact between individuals from different, often isolated, mite populations. Dispersal, both active and passive, has important consequences for the structuring of genetic variation within species (Waters et al. 2020). Thus, unintentional movement of mites with nest material may influence genetic variation and population structure of species as well as their ability to spread and increase local ranges.
To conclude, our study has increased faunistic and ecological knowledge of the mite fauna of wood warbler nests. We have shown that wood warbler nests provide a space for survival of numerous mite species. We found several mesostigmatid species that are characteristic of nests, but most of the recorded species are not typical for bird nests and seem to be accidental. We pointed out the potential importance of wood warbler nests for mite dispersal and for the evolution of interspecific interactions.
References
Ambros M, Krištofík J, Šustek Z (1992) The mites (Acari, Mesostigmata) in the birds’ nests in Slovakia. Biológia 47:369–381
Bedano JC, Cantú MP, Doucet ME (2005) Abundance of soil mites (Arachnida: Acari) in a natural soil of central Argentina. Zool Stud 44(4):505–512
Bellamy PE, Burgess MD, Mallord JW, Cristinacce A, Orsman CJ, Davis T, Grice PV, Charman EC (2018) Nest predation and the influence of habitat structure on nest predation of Wood Warbler Phylloscopus sibilatrix, a ground-nesting forest passerine. J Ornithol 159:493–506. https://doi.org/10.1007/s10336-017-1527-7
Błoszyk J (1999) Geograficzne i ekologiczne zróżnicowanie zgrupowań roztoczy z kohorty Uropodina (Acari: Mesostigmata) w Polsce. I. Uropodina lasów grądowych (Carpinion betuli). Dissertation, Adam Mickiewicz University, Poznań
Błoszyk J, Olszanowski Z (1985) Materiały do znajomości roztoczy gniazd i budek lęgowych ptaków. I: Uropodina i Nothroidea (Acari: Mesostigmata i Oribatida). Prz Zool 29:69–74
Błoszyk J, Gwiazdowicz DJ, Bajerlein D, Halliday RB (2005) Nests of the white stork Ciconia ciconia (L.) as a habitat for mesostigmatic mites (Acari, Mesostigmata). Acta Parasitol 50:171–175
Błoszyk J, Bajerlein D, Gwiazdowicz DJ, Halliday RB, Dylewska M (2006) Uropodine mite communities (Acari: Mesostigmata) in birds’ nests in Poland. Belgian J Zool 136:145–153
Błoszyk J, Gwiazdowicz DJ, Halliday RB, Dolata PT, Gołdyn B (2009) Nests of the black stork Ciconia nigra as a habitat for mesostigmatid mites (Acari: Mesostigmata). Biologia (bratisl) 64:962–968. https://doi.org/10.2478/s11756-009-0146-z
Błoszyk J, Gwiazdowicz DJ, Kupczyk M, Książkiewicz-Parulska Z (2016) Parasitic mesostigmatid mites (Acari)—common inhabitants of the nest boxes of starlings (Sturnus vulgaris) in a Polish urban habitat. Biologia 71:1034–1037. https://doi.org/10.1515/biolog-2016-0124
Błoszyk J, Buczkowska K, Bobowicz MA, Bączkiewicz A, Adamski Z, Napierała A (2019) Are polymorphic species of Uropodina (Acari: Mesostigmata) more successful evolutionarily? A case study of closely related species from the genus Oodinychus Berlese, 1917 based on DNA sequences. Syst Appl Acarol 24:866–881
Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583
Campbell B, Lack E (1985) A Dictionary of birds. Published for the British Ornithologists’ Union by Poyser, London
Celebias P, Melke A, Gwiazdowicz DJ, Przewoźny M, Komosiński K, Baraniak E, Winnicka K, Melosik I, Ziomek J (2019) Species composition, diversity, and the abundance of arthropods inhabiting burrows of the common hamster (Cricetus cricetus L). Bull Entomol Res 109:781–793. https://doi.org/10.1017/S0007485319000087
Coulson SJ, Moe B, Monson F, Gabrielsen GW (2009) The invertebrate fauna of high Arctic seabird nests: the microarthropod community inhabiting nests on Spitsbergen, Svalbard. Polar Biol 32:1041–1046. https://doi.org/10.1007/s00300-009-0603-8
Cramp S (ed) (1992) vol 6. Oxford Univ Press, Oxford
Deeming DC, Reynolds SJ (eds) (2015). Oxford University Press, Oxford
Dziuba S (1966) Quantitative ratio between Mesostigmata, Trombidiformes and Sarcoptiformes in soil of cultivated fields [Ilościowy udział Mesostigmata, Trombidiformes i Sarcoptiformesw glebie pól uprawnych]. Zesz Probl Post Nauk Roln 65
Efron B, Tibshirani RJ (1993) An introduction to the bootstrap. Chapman and Hall, New York
Fend’a P, (2010) Mites (Mesostigmata) inhabiting bird nests in Slovakia (Western Carpathians). Trends in acarology. Springer, Dordrecht, pp 199–205
Fenďa P, Schniererová E (2005) Mites (Acarina, Gamasida) in littoral zone of Jakubov fishponds (Slovakia). In: Tajovský K, Schlaghamerský J, Pižl V (eds) Contributions to soil zoology in Central Europe I. ISB AS CR, České Budějovice, pp 9–14
Ghilarov MS, Bregetova NG (eds) (1977). Nauka, Moscow (In Russian)
Gwiazdowicz DJ (2007) Ascid mites (Acari, Mesostigmata) from selected forest ecosystems and microhabitats in Poland. Wydawnictwo Akademii Rolniczej, Poznań
Gwiazdowicz DJ (2010) Sejoidea, Antennophoroidea, Celaenopsoidea, Microgynioidea (Acari, Mesostigmata) of Poland. Bogucki Wydawnictwo Naukowe, Poznań
Gwiazdowicz DJ, Mizera T, Skorupski M (1999) Mites in greater spotted eagle nests. J Raptor Res 33:257–260
Gwiazdowicz DJ, Błoszyk J, Mizera T, Tryjanowski P (2005) Mesostigmatic mites (Acari: Mesostigmata) in white-tailed sea eagle nests (Haliaeetus albicilla). J Raptor Res 39:60–65
Gwiazdowicz DJ, Błoszyk J, Bajerlein D, Halliday RB, Mizera T (2006) Mites (Acari: Mesostigmata) inhabiting nests of the while-tailed sea eagle Haliaeetus albicilla (L.) in Poland. Entomol Fennica 8:366–372. https://doi.org/10.33338/ef.84359
Gwiazdowicz DJ, Coulson SJ, Grytnes J-A, Pilskog HE (2012) The bird ectoparasite Dermanyssus hirundinis (Acari, Mesostigmata) in the High Arctic; a new parasitic mite to Spitsbergen, Svalbard. Acta Parasitol 57:378–384. https://doi.org/10.2478/s11686-012-0050-5
Gwiazdowicz DJ, Niedbała W, Skarżyński D, Zawieja B (2022) Occurrence of mites (Acari) and springtails (Collembola) in bird nests on King George Island (South Shetland Islands, Antarctica). Polar Biol 45:1035–1044. https://doi.org/10.1007/s00300-022-03052-1
Hansell M, Overhill R (2000) Bird nests and construction behaviour. Cambridge University Press, Cambridge
Hasegawa M, Okabe K, Fukuyama K, Makino S, Okochi I, Tanaka H, Goto H, Mizoguchi T, Sakata T (2013) Community structures of Mesostigmata, Prostigmata and Oribatida in broad-leaved regeneration forests and conifer plantations of various ages. Exp Appl Acarol 59(4):391–408. https://doi.org/10.1007/s10493-012-9618-x
Hernandes FA, Skvarla MJ, Fisher JR, Dowling APG, Ochoa R, Ueckermann EA, Bauchan GR (2016) Catalogue of snout mites (Acariformes: Bdellidae) of the world. Zootaxa 4152:1–83. https://doi.org/10.11646/ZOOTAXA.4152.1.1
Hirschmann W, Zirngiebl-Nicol I (1961) Gangsystematic der Parasitiformes. Teil. 4. Acarologie Schriftenreihe Für Vergleichende Milbenkunde 4:1–41
Jesionowska K (2010) Cocceupodidae, a new family of eupodoid mites, with description of a new genus and two new species from Poland. Part I. (Acari: Prostigmata: Eupodoidea). Genus 21:637–658
Kaminskienė E, Radzijevskaja J, Balčiauskas L, Gedminas V, Paulauskas A (2017) Laelapidae mites (Acari: Mesostigmata) infesting small rodents in the Curonian Spit Lithuania. Biologija. https://doi.org/10.6001/biologija.v63i2.3528
Karbarz-Wiktorowicz H (1973) Badania nad morfologią Riccardoella limacum (Schrank) (Acari, Ereynetidae). Pol Pismo Entomol 43:767–788
Karg W (1989) Acari (Acarina) Milben, Unterordnung Parasitiformes (Anactinochaeta). Uropodina Kramer. Schildkrötenmilben Tierwelt Deutschlands 67:1–203
Karg W (1993) Acari (Acarina), Milben Parasitiformes (Anactinochaeta), Cohors Gamasina Leach. Raubmilben. Die Tierwelt Deutschlands, VEB Gustav Fischer Verlag (Jena). Teil 59:1–523
Kaźmierski A (1998a) A review of the genus Proctotydaeus Berlese (Actinedida: Tydeidae: Pronematinae). Acarologia 39:33–47
Kaźmierski A (1998b) Tydeinae of the world: generic relationships, new and redescribed taxa and keys to all species. A revision of the subfamilies Pretydeinae and Tydeinae (Acari: Actinedida: Tydeidae)—part IV. Acta Zool Cracoviensia 41:283–455
Kaźmierski A, Marciniak M, Sikora B (2018) Tydeinae mites (Acariformes: Prostigmata: Tydeidae) from bird nests with description of three new species. Syst Appl Acarol 23:803–823. https://doi.org/10.11158/saa.23.5.3
Kaźmierski A, Laniecka I, Laniecki R (2021) A review of the genus Primotydeus (Acariformes: Tydeoidea: Iolinidae). Syst Appl Acarol 26:2320–2337. https://doi.org/10.11158/saa.26.12.11
Kethley JB (1971) Hydranetes, a new genus of Ereynetidae from hydrophilid beetles (Prostigmata: Ereynetidae). J Georgia Entomol Soc 6:176–184
Knee W, Proctor H (2007) Host records for Ornithonyssus sylviarum (Mesostigmata: Macronyssidae) from birds of North America (Canada, United States, and Mexico). J Med Entomol 44:709–713. https://doi.org/10.1093/jmedent/44.4.709
Kramer P (1882) Ueber Gamasiden. Arch Naturgesch 48:406–407
Kristofik J, Masan P, Sustek Z (2005) Arthropods in the nests of marsh warblers (Acrocephalus palustris). Biologia 60:171–177
Kristofik J, Sustek Z, Masan P (2002) Arthropods (Pseudoscorpionida, Acari, Coleoptera, Siphonaptera) in the nests of red-backed shrike (Lanius collurio) and lesser grey shrike (Lanius minor). Biologia 57:603–613
Kuznetzov NN (1978a) Revision of the genus Stigmaeus (Acariformes, Stigmaeidae). ZoolZhl 57:682–694
Kuznetzov NN (1978b) A guide to the soil mites—Trombidiformes. Moskva, Science (In Russian)
Lindquist EE, Krantz GW, Walter DE (2009) Classification. In: Krantz GW, Walter DE (eds) A Manual of Acarology, 3rd edn. Texas Tech University Press, Texas, pp 97–103
Mallord JW, Charman EC, Cristinacce A, Orsman CJ (2012a) Habitat associations of Wood Warblers Phylloscopus sibilatrix breeding in Welsh oakwoods. Bird Study 59:403-415S. https://doi.org/10.1080/00063657.2012.727780
Mallord JW, Orsman CJ, Cristinacce A, Butcher N, Stowe TJ, Charman EC (2012b) Mortality of Wood Warbler Phylloscopus sibilatrix nests in Welsh Oakwoods: predation rates and the identification of nest predators using miniature nest cameras. Bird Study 59:286–295. https://doi.org/10.1080/00063657.2012.669359
Mallord JW, Orsman CJ, Roberts JT, Skeen R, Sheehan DK, Vickery JA (2016) Habitat use and tree selection of a declining Afro-Palaearctic migrant at sub-Saharan staging and wintering sites. Bird Study 63:459–469. https://doi.org/10.1080/00063657.2016.1214813
Mallord JW, Orsman CJ, Cristinacce A, Stowe TJ, Charman EC, Gregory RD (2017) Diet flexibility in a declining long-distance migrant may allow it to escape the consequences of phenological mismatch with its caterpillar food supply. Ibis 159:76–90. https://doi.org/10.1111/ibi.12437
Maribie CW, Nyamasyo G, Ndegwa P, Mung’atu J, Lagerlӧf J, Gikungu M (2011) Abundance and diversity of soil mites (Acari) along a gradient of land use types in Taita Taveta, Kenya. Trop Subtrop Agroecosyst 13:11–26
Mašán P (2001) Mites of the cohort Uropodina (Acarina, Mesostigmata) in Slovakia. First ed. Annot Zool Bot, Bratislava
Mašán P, Stanko M (2005) Mesostigmatic mites (Acari) and fleas (Siphonaptera) associated with nests of mound-building mouse, Mus spicilegus Petényi, 1882 (Mammalia, Rodentia). Acta Parasitol 50:228–234
Mašán P, Fenɱa P, Krištofík J, Halliday B (2014) A review of the ectoparasitic mites (Acari: Dermanyssoidea) associated with birds and their nests in Slovakia, with notes on identification of some species. Zootaxa 3893:77–100. https://doi.org/10.11646/zootaxa.3893.1.3
Maziarz M, Broughton RK, Hebda G, Wesołowski T (2018) Occupation of wood warbler Phylloscopus sibilatrix nests by Myrmica and Lasius ants. Insectes Soc 65:351–355. https://doi.org/10.1007/s00040-018-0613-z
Maziarz M, Broughton RK, Casacci LP, Luca P, Dubiec A, Maák I, Witek M (2020) Thermal ecosystem engineering by songbirds promotes a symbiotic relationship with ants. Sci Rep 10:1–10. https://doi.org/10.1038/s41598-020-77360-z
Maziarz M, Broughton RK, Casacci LP, Luca P, Hebda G, Maák I, Trigos-Peral G, Witek M (2021) Interspecific attraction between ground-nesting songbirds and ants: the role of nest-site selection. Front Zool 18:1–14. https://doi.org/10.1186/s12983-021-00429-6
Micherdziński W (1980) Eine taxonomische Analyse der Familie Macronyssidae Oudemans, 1936, I. Subfamilie Omithonyssinae Lange, 1958 (Acarina, Mesostigmata). Polska Akademia Nauk. Zakład Zoologii Systematycznej i Doświadczalnej, Warszawa
Michocka, S. (1987) Polskie roztocze (Acari) z rodzin Bdellidae i Cunaxidae. Monografie Fauny Polski, PWN, Kraków (In Polish with English Summary)
Møller AP (1990) Effects of parasitism by a haematophagous mite on reproduction in the Barn Swallow. Ecology 71:2345–2357
Murillo AC, Mullens BA (2017) A review of the biology, ecology, and control of the northern fowl mite, Ornithonyssus sylviarum (Acari: Macronyssidae). Vet Parasitol 246:30–37. https://doi.org/10.1016/j.vetpar.2017.09.002
Napierała A, Błoszyk J (2013) Unstable microhabitats (merocenoses) as specific habitats of Uropodina mites (Acari: Mesostigmata). Exp Appl Acarol 60:163–180
Napierała A, Mądra A, Leszczyńska-Deja K, Gwazdowicz DJ, Gołdyn B, Błoszyk J (2016) Community structure variability of Uropodina mites (Acari: Mesostigmata) in nests of the common mole, Talpa europaea, in Central Europe. Exp Appl Acarol 68:429–440. https://doi.org/10.1007/s10493-016-0017-6
Napierała A, Maziarz M, Hebda G, Broughton RK, Rutkowski T, Zacharyasiewicz M, Błoszyk J (2021) Lack of specialist nidicoles as a characteristic of mite assemblages inhabiting nests of the ground-nesting wood warbler, Phylloscopus sibilatrix (Aves: Passeriformes). Exp Appl Acarol 84:149–170
Niedbała W (2008) Ptyctimous mites (Acari, Oribatida) of Poland. Fauna Poloniae, Museum and Institute of Zoology of the Polish Academy of Sciences and Natura optima dux Foundation, Warszawa
Pilskog HE, Solhøy T, Gwiazdowicz DJ, Grytnes J-A, Coulson SJ (2014) Invertebrate communities inhabiting nests of migrating passerine, wild fowl and sea birds breeding in the High Arctic, Svalbard. Polar Biol 37:981–998. https://doi.org/10.1007/s00300-014-1495-9
Proctor H, Owens I (2000) Mites and birds: diversity, parasitism and coevolution. Trends Ecol Evol 15:358–364. https://doi.org/10.1016/S0169-5347(00)01924-8
Pung OJ, Carlile LD, Whitlock J, Vives SP, Durden LA, Spadgenske E (2000) Survey and host fitness effects of red-cockaded woodpecker blood parasites and nest cavity arthropods. J Parasitol 86:506–510. https://doi.org/10.1645/0022-3395(2000)086[0506:SAHFEO]2.0.CO;2
Reid JM, Cresswell W, Holt S, Mellanby RJ, Whitfield DP, Ruxton GD (2002) Nest scrape design and clutch heat loss in Pectoral Sandpipers (Calidris melanotos). Funct Ecol 16:305–312. https://doi.org/10.1046/j.1365-2435.2002.00632.x
Silva GL, Metzelthin MH, Silva O, Ferl NJ (2016) Catalogue of the mite family Tydeidae (Acari: Prostigmata) with the world key to the species. Zootaxa 4135:1–68. https://doi.org/10.11646/ZOOTAXA.4135.1.1
Skoracka A, Kuczyński L (2012) Measuring the host specificity of plant-feeding mites based on field data: a case study of the Aceria species. Biologia 67:546–560. https://doi.org/10.2478/s11756
Skvarla MJ, Fisher JR, Dowling APG (2014) A review of Cunaxidae (Acariformes, Trombidiformes): histories and diagnoses of subfamilies and genera, keys to world species, and some new locality records. ZooKeys 418:1–103. https://doi.org/10.3897/zookeys.418.7629
Smiley RL (1992) The predatory mite family Cunaxidae (Acari) of the world with a new classification. Indira Publishing House, West Bloomfield
Stamp RK, Brunton DH, Walter B (2002) Artificial nest box use by the North Island Saddleback: effects of nest box design and mite infestations on nest site selection and reproductive success. N Z J Zool 29:285–292. https://doi.org/10.1080/03014223.2002.9518312
Subías LS (2004) Listado sistemático, sinonímico y biogeográfico de los Ácaros Oribátidos (Acariformes, Oribatida) del mundo (1758–2002). Graellsia, 60 (número extraordinario), 3–305 (Actualizado en junio de 2006, en abril de 2007, en mayo de 2008, en abril de 2009, en julio de 2010, en febrero de 2011, en abril de 2012, en mayo de 2013, en febrero de 2014, en marzo de 2015, en febrero 2016, en febrero de 2017, en enero de 2018, en marzo de 2019, en enero de 2020 y en marzo de 2021 y en marzo de 2022. Internet). https://www.bba.bioucm.es/cont/docs/RO_1.pdf (accessed June 2022)
Szymkowiak J, Kuczyński L (2017) Song rate as a signal of male aggressiveness during territorial contests in the wood warbler. J Avian Biol 48:275–283. https://doi.org/10.1111/jav.00969
Szymkowiak J, Thomson RL, Kuczyński L (2016) Wood warblers copy settlement decisions of poor quality conspecifics: support for the tradeoff between the benefit of social information use and competition avoidance. Oikos 125:1561–1569
Szymkowiak J, Thomson RL, Kuczyński L (2017) Interspecific social information use in habitat selection decisions among migrant songbirds. Behav Ecol 28:767–775
Tøttrup AP, Pedersen L, Thorup K (2018) Autumn migration and wintering site of a wood warbler Phylloscopus sibilatrix breeding in Denmark identified using geolocation. Anim Biotelem 6:15. https://doi.org/10.1186/s40317-018-0159-x
Turk FA, Phillips SM (1946) A monograph of the slug mite Riccardoella limacum (Schrank). Proc Zool Soc Lond 115:415–488
Vickery JA, Ewing SR, Smith KW, Pain DJ, Bairlein F, Škorpilová J, Gregory RD (2014) The decline of Afro-Palaearctic migrants and an assessment of potential causes. Ibis 156:1–22. https://doi.org/10.1111/ibi.12118rr
Walter DE, Proctor HC (2013) Mites: ecology, evolution & behaviour: life at a microscale, 2nd edn. Springer, Dordrecht Heidelberg, New York, London
Waters JM, Emerson BC, Arribas P, McCulloch GA (2020) Dispersal reduction: causes, genomic mechanisms, and evolutionary consequences. Trends Ecol Evol 35:512–522. https://doi.org/10.1016/j.tree.2020.01.012
Weigmann G (2006) Acari, Actinochaetida. Hornmilben (Oribatida). (Unter Mitarbeit von L. Miko). In: Dahl F (ed) Die Tierwelt Deutschlands u. der angrenzenden Meeresteile nach ihren Merkmalen u. nach ihrer Lebensweise. 76. Teil. Goecke & Evers, Keltern
Wesołowski T (1985) The breeding ecology of the wood warbler Phylloscopus sibilatrix in primaeval forest. Ornis Scand 16:49–60. https://doi.org/10.2307/3676575
Woodroffe GE (1953) An ecological study of the insects and mites in the nests of certain birds in Britain. Bull Entomol Res 44:739–772. https://doi.org/10.1017/S0007485300024706
Zacharda M (1978) (1980) Soil mites of the family Rhagidiidae (Actinedida: Eupodoidea): Morphology, systematics, ecology. Acta Univ Carol 5–6:489–785
Acknowledgements
The authors thank Maciej Bronikowski for help in segregation of extracted invertebrates, Justyna Pińkowska for help in mounting mite specimens on slides, prof. Jacek Dabert for the loan of the microscope, and Roland Łaniecki for consultation regarding mite systematics. The authors are also grateful for valuable comments of two anonymous reviewers, which significantly improved the manuscript. The study was conducted in accordance with Polish law and thanks to permission no. 2B/2012 given by the Director of the Wielkopolska National Park.
Funding
This work was supported by the National Science Centre in Poland (NSC, grant number 2012/07/N/NZ8/00129, received by JS); JS was also supported by the Foundation for Polish Science (FNP) scholarship ‘Start’. AL’s scholarships were funded by the NSC (PhD scholarship no. 2019/32/T/NZ8/00151) and Adam Mickiewicz University Foundation (awarded in 2019/2020). Besides, AL and MM were supported by European Social Funds (POWR.03.02.00–00–I006/17).
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Conceptualization and design of the study: LK, JS, AS; methodology: LK, JS, AS; field data collection: JS, NH, AS; segregation of mite material: AL, DJG, AK, MM; taxonomic identification: DJG, AK, WN, JB, ZO, MM, AL; data processing: AL, MM, LK, EP; formal analysis: AL, LK; resources: JS, LK; concept of the manuscript: AL, EP, AS; writing—original draft: AL, EP, AS, DJG, JS; writing—review and editing: AL, EP, AS, MM, DJG, AK, WN, JB, LK; final approval for publication: AL, EP, AS, MM, DJG, AK, WN, JB, JS, NH, LK, AS.
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Laska, A., Puchalska, E., Mikołajczyk, M. et al. Mites inhabiting nests of wood warbler, Phylloscopus sibilatrix (Aves: Passeriformes), in the Wielkopolska National Park in western Poland. Exp Appl Acarol 89, 393–416 (2023). https://doi.org/10.1007/s10493-023-00792-5
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DOI: https://doi.org/10.1007/s10493-023-00792-5