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Most prostigmatans are monoxenous or narrowly oligoxenous parasites and only 8.7–22.6% of species in various groups are associated with host of one family, 1.7–21.4% - with hosts of one order and only 1.1–3.4% - with hosts of various orders. Many species records, however, are solitary and the level of host specificity could be overestimated for some species. The most strictly specific symbionts are parasitic Cheyletidae and Syringophilidae, 83% and 70% of monoxenous species, respectively; the less specific symbionts are Ereynetidae and Harpirhynchidae – 48.6% and 62%, respectively. It is interesting that some species in the families, represented generally by the highly specific parasites, are associated with wide spectrum of hosts, for example, Bakericheyla chanayi (Cheyletidae).
At the generic level the host specificity of prostigmatan mites is less marked but still significant. In the Cheyletidae, four genera (36%) parasitize birds from one family, the genus Apodicheles is associated exclusively with Apodiformes, and six other genera (54%) are associated with birds of two or even more orders. In the Harpirhynchidae, six genera (50%) are associated with hosts of one family, two (17%) – with hosts of one order, and four (33%) – with hosts of various orders. In Syringophilidae, 39 genera (74%) parasitize birds of one order and only 14 genera (26%) are associated with birds of two or even three various orders. Finally, in the Ereynetidae, seven genera (47%) are associated with one bird family, two (13%) – with birds of one order, and six (40%) – with birds of various orders.
Most prostigmatan families and subfamilies are cosmopolite, excluding Pneumocoptinae (Cloacaridae), which is still known from a single record.
To date, prostigmatans are known from birds from 25 of 34 orders belonging to neognathous as well as to paleognathous (Tinamiformes) birds. These mites are absent on birds of the orders Cariamiformes, Eurypygiformes, Gaviiformes, Mesitornithiformes, Otidiformes, Phaethoniformes, Sphenisciformes, Struthioniformes, and Trogoniformes. Their absence on Struthioniformes and Sphenisciformes is explainable the external morphological modifications of these hosts (especially feathers), whereas birds of the other orders are insufficiently explored (or not explored at all) for the presence of these mites. However, with a high probability they could also be infected by prostigmatans. Prostigmatans are characterized by a relatively low prevalence and many of unexplored hosts are rare and poorly represented in collections. Moreover, most of museum bird specimens are preserved as dry skins and unavailable for examination on prostigmatans because techniques of their collecting can damage the skins.
The number of described prostigmatans represents only a small fraction of their actual biodiversity because their expected number is estimated as 5000 species (instead of 500 presently known species) based on the data about host specificity and number of their potential hosts. At the same time, it could be stated, based on distribution of these mites, that at least 50% of their extant genera are known to date. For example, among 110 extant passerine families, prostigmatans are recorded on hosts from more than 50 families.
Mites of the family Cheyletidae are known from birds of 13 orders, Syringophilidae – from 21 orders, Harpirhynchidae– from 18 orders and Ereynetidae – from 17 orders. Moss and Wojcik (1978) also listed Caprimulgiformes as hosts of harpirhynchids but did not provide the full data; therefore these records were not taken here into account.
As it is expected, representatives of all prostigmatan families, excluding Cloacaridae, are recorded mostly from hosts of species-rich orders, i.e. Apodiformes, Charadriformes, Columbiformes, Coraciiformes, Cuculiformes, Galliformes, Gruiformes, Passeriformes, Pelecaniformes, Piciformes, Psittaciformes, and Strigiformes.
The only mites of the family Syringophilidae are known to date from palaeognathous birds of the order Tinamiformes; whereas other prostigmatans are still recorded exclusively from Neognathae.
Within the Neognathae, hosts of the more archaic Galloanserae clade are parasitized by most prostigmatan families, excluding Cheyletidae and Cloacaridae on Anseriformes, but the absolute majority of mite species are associated with hosts of the clade Neoaves and with passerines within this clade.
Thus, birds were colonized independently by mites of several prostigmatan phylogenetic lines – three groups of cheyletids (Ornithocheyletiini, Metacheyletiini, and Cheletosomatini), Syringophilidae, Harpirhynchidae, Ereynetidae (Speleognathinae), and Cloacaridae (Pneumocoptinae).
As it was the above mentioned, the superfamily Cheyletoidea, including most bird permanent symbionts, is represented by two main phylogenetic lineages: Cheyletidae–Syringophilidae (I), and Harpirhynchidae (Demodicidae–Psorergatidae) (II) .
The ancestor of lineage I undoubtedly was a predator preying on other arthropods. Most part of the apomorphic modifications of these mites concerns the gnathosomal structures and, probably, serves for more effective preying. At the same time, the idiosoma and legs in these mites are relatively archaic and weakly modified, like those in the other predatory family Raphignathidae. The family Syringophilidae originated from the common ancestor with Cheyletidae, which preyed in bird nests. Syringophilids developed some adaptations to the parasitic mode of life in feather quills (the stylophore surrounded by the idiosoma and the elongate body); they have also lost some structures, which serve for preying and are useless for permanent parasites: the thumb-claw complex, cupules, and the strong sclerotization of the shields. In these mites, some idiosomal setae (4a and ps3) have undergone a reduction in parallel to parasitic cheyletoids of lineage II. In Cheyletidae, the parasitism on birds originated independently in three phylogenetic lineages (tribes) .
Family Cheyletidae. This family is represented by the predators and permanent parasites of the terrestrial vertebrates, birds and small mammals. To date, it includes more 380 species in 72 genera and is the most species-rich grouping comparing to other families of the superfamily Cheyletoidea . Cheyletids have a worldwide distribution and are known from a wide spectrum of biotopes. They occur in a soil, vegetable debris, in nests of insects, mammals and birds. This family includes almost all intermediate stages between free-living predation to highly specialized permanent parasites of vertebrates, birds and mammals. The obligatory phoresy on certain insects is typical for some predatory cheyletids. There are several general directions in the cheyletid evolution: predator-dendrophils, predator-entomophils, forms being phoretic on insects and living in their nests, nidicolous predators in vertebrate nests, parasites of birds and mammals.
Among bird-associated cheyletids, mites of the tribe Cheletosomatini (six genera) include predators inhabiting the feather quills and prey there on parasitic astigmatic mites and mites of the family Syringophilidae. All representatives of this tribe are morphologically similar to Acaropsellina-like mites and probably originated from the common ancestor inhabited bird nests. The monotypic genus Picocheyletus was recently described from quills of Tricholaema hirsuta flavipunctata from Gabon. These mites were collected from quills of the primary and secondary wing feathers. In each infested feather, the rachis was naturally split ventrally in its basal part, exposing the hollow interior. The mites occupied spaces between septae, one mite per inter-septal space. In addition, from one to four eggs were present in some inter-septal spaces. It should be noted that no other mites or remains of mites were observed inside the quills that might serve as a prey. Some examined specimens contained dark inclusions, similar to hematite inclusions, which usually are visible in blood-feeding cheyletids of the genus Bakericheyla (Ornilhocheyletiini). Therefore, it can be concluded that these mites are true parasites on the avian host. In this case we see transition to parasitism happened literally in “our presence”. Among other representatives of the tribe, species of the genus Cheletoides are associated with galliform birds (Galliformes). A single species of the genus Eucheletopsis is recorded from tree swifts of the genus Hemiprocne (Apodiformes: Hemiprocnidae), and two species of the genus Cheletosoma are associated with hosts of the orders Gruiformes and Cuculiformes. The genus Metacheyletoides includes species from galliform (Galliformes) and cuculiform (Cuculiformes) birds. Mites of the genus Cheletopsis are associated exclusively with charadriiform birds (Charadriiformes). Its representatives show variable specificity to their hosts; some species are limited to hosts of one genus, whereas others occur on birds of several charadriiform families.
The tribe Ornithocheyletiini (four genera) is represented by ectoparasites inhabiting the skin surface of birds. Mites of the genus Neocheyletiella are mono- or oligoxenous parasites associated with birds of four orders: Passeriformes, Pelecaniformes, Columbiformes, and Strigiformes. Species of the genus Bakericheyla are known from birds if three orders, Apodiformes, Coraciiformes, and Passeriformes. Most of these species are highly specific to their hosts and distributed in Africa, but Bakericheyla chanayi, however, is known from birds of various families and orders and has a cosmopolitan distribution. The genus Ornitocheyletia is represented by parasites of six bird orders: Columbiformes, Cuculiformes, Galliformes, Passeriformes, Piciformes, and Psittaciformes. Ornitocheyletia species are mostly mono- or oligoxenous parasites. Three species known in the genus Apodicheles are restricted to swifts from South-East Asia and Africa (Apodiformes: Apodidae). Thus, mites of the tribe Ornithocheyletiini are known from representatives of several bird orders, belonging to the two major phyletic lines, Galloanserae (excluding Anseriformes) and Neoaves. It can be hypothesized that the ancestor of this tribe parasitized on a common ancestor of these superorders.
The tribe Metacheyletiini includes the only genus Metacheyletia with five species inhabiting the feather quills. Three of these species parasitize parrots from the Old and New Worlds, and two species were recorded from quills of passeriform and cuculiform birds in the Tropical Africa. The biology of Metacheyletia species is still unknown. Atyeo et al. (1984) believed that these mites are predators because their chelicerae are too short to pierce the quill wall. Moreover, in all cases, these cheyletids were collected together with other mites in those quills. Bochkov and Fain (2001), however, had another opinion and suggested that these mites are parasites. According to these authors, the morphological characters of Metacheyletia species are similar to those of other parasitic cheyletids: legs I-III are short, legs IV are reduced, setae of the palpal tarsi are short and smooth, the gnathosoma is relatively small. It is suggested that these mites use for feeding the openings pierced by the adult syringophilids. This hypothesis is supported by the presence of syringophilids in all cases where these mites were found.
Family Syringophilidae. The syringophilid ancestors were, probably, initially predators on other mites inhabiting feather quills. According to the estimation based on the “molecular clock”, the divergence between cheyletids and syringophilids could take place approximately 180–185 million years ago in the Early Jurassic. Thus, syringophilids were, probably, associated even with the bird ancestors – theropod dinosaurs, many of which possessed feathers.
The host-parasite relationships of syringophilid were analyzed by Kethley and Johnston (1975). According to data of these authors the phylogenetic pattern of these mites and birds are strongly incongruent at the level of mite genera and bird orders. This incongruence could also be explained by the horizontal syringophilid switches on phylogenetically distant hosts. Kethley and Johnston (1975) considered host switches as the main modus in the evolution of this family and even proposed a new term for it – resource tracking. According to their hypothesis, host distribution of syringophilid species is determined by thickness of the quill walls and mite capability to pierce it.
The second important evolution aspect in syringophilid evolution on their hosts is a distribution of these mites on various types of quills. The wing-feathers, i.e. primaries and secondaries, are probably the ancestral type of the syringophilid habitat. The majority of representatives of the family, including the most archaic ones, were associated with quills of these feathers. The subfamily Picobiinae represented mostly by the dwellers of the body covert feathers was probably originated in wing quills, because representatives of the archaic genus Calamincola occupy these microhabitats. In comparison to syringophilines, picobiines are much more morphologically specialized and possess some advantages, ror instance heterosomy, which, probably, allowed them to use more effectively small quills of the body coverts. Thus, picobiines avoided competitions with other syringophilids and formed the second line distributed in parallel with syringophilines on the same hosts. Unfortunately, the biodiversity of this group is yet poorly studied in comparison to Syringophilinae.
Among 48 genera of the subfamily Syringophilinae, 38 genera are restricted to particular avian orders, whereas most of reamining mite genera occur on birds of several orders.
The phylogenetic lineage II of Cheyletoidea is exclusively represented by permanent parasites of vertebrates which can be characterized by the unique palpal structure. All three families of this lineage demonstrate a tendency towards intracutaneous parasitism (a part of Harpirhynchidae, Demodicidae and Psorergatidae). Skin-inhabiting Harpirhynchidae are relatively slow-moving ectoparasites, which are very often embedded in the host epidermis. By this reason, the reduction tendencies prevailed in the evolution of this mite lineage.
It is presumed from the wide distribution of these mites on birds (Harpirhynchidae) and mammals (Psorergatidae–Demodicidae), that the common ancestor of this branch could occur on the common ancestor of birds and mammals. Transitions from birds, which are hosts of the most archaic representatives of line II (Harpypalpinae), onto mammals, however, can not be excluded during the early phase of mammal evolution. A possible reason for the absence of cheyletoids on recent reptiles (excluding snakes) may be explained by the peculiarities of their skin structure and molting. Squamata lose the entire external dermal layer or large pieces of it during the molt; moreover, they have a multi-layer keratinized epithelium, and skin glands are absent. The high probability of loss of mites during reptile molting seems to have prevented the primary settling of cheyletoid parasites on these hosts. These mites are absent also on crocodilians probably because of their aquatic mode of life. In birds, the skin has undergone significant evolutionary changes comparable to that in of mammals. This probably allowed some cheyletoid mites of the family Harpirhynchidae to transfer to the intradermal parasitism in capsules that is similar to that developed by representatives of Psorergatidae.
Family Harpirhynchidae. This family includes three subfamilies, two subfamilies, Harpirhynchinae and Harpypalpinae are represented by bird parasites and the subfamily Ophioptinae – by ectoparasites of snakes from the superfamily Colubroidea. The monophyly of this family is strongly approved, and hypothesis about the independent origin of the subfamilies Harpirhynchinae and Harpypalpinae from cheyletoid-like ancestors, proposed by by Moss (1979), is groundless.
Mites of the subfamily Harpirhynchinae are known exclusively from Neognathae (Galloanserae and Neoaves). Mites of the most archaic genus Harpirhynchoides are known from 13 bird orders (Fain 1994b). Mites of the genera Neharpirhynchus and Metharpirhynchus parasitize passerines. In addition, the first genus is associated with humming birds (Apodiformes: Trochilidae), and the second genus – with Picidae (Piciformes) (Fain 1995). Another seven genera are represented by a few species which are associated with hosts of one order. Mites of three genera, Harpirhynchus, Anharpirhynchus and Trichorhynchiella are associated with passerines; mites of the genera Cypsharpirhynchus and Harpyrhynchiella are known from Apodidae (Apodiformes); the genus Perharpirhynchus is associated with hosts of the order Charadriiformes;the mites of the genus Ralliharpirhynchus are known only from Rallidae (Gruiformes) (Fain 1995).
Mites of the subfamily Harpypalpinae are known from hosts of 11 families, all of them belong to higher passerines.
It looks like a paradox that mites of the more archaic subfamily are associated with the highly evolved hosts. On the contrary, the immature instars of the Harpypalpinae are highly derived in their morphology, because they have lost legs and are characterized by a quite specialized idiosomal setation. Apparently in this case we have two principally different pathways of the morphological evolution in these two subfamilies. In the Harpirhynchinae the progressive characters are represented in adults, whilst in Harpypalpinae they are developed in immatures. Relationships of Passeriformes with other higher Neoaves are not clear. It is possible that this order represents some earlier separated branch. Certain parasitological data support the hypothesis of the early origin of Passeriformes. Thus, the rather archaic representatives of the families Rhinonyssidae (Mesostigmata) and Ereynetidae (Prostigmata) are associated with Passeriformes. The feather mite family Proctophyllodidae, mostly restricted to the passerines, is one of most evolved feather mite families but is also characterized by certain archaic features. If one admits the hypothesis of earlier origin of Passeriformes the separate phylogenetic position of the Harpypalpinae could be easily explained by their coevolution with the passerines.
The subfamily Ophioptinae is a sister lineage to the Harpypalpinae. It was hypothesized that harpypalpine-like ancestor of Ophioptinae switched to parasitism on snakes from passerines. The possibility of this host shift was originally proposed by Kethley. Certain snakes feed on nestlings and adult birds. Most of this prey is small passerine birds. The subfamily Ophioptinae is associated exclusively with Colubridae and Elapidae. These two snake families are closely related and represent a group of higher snakes.
Family Cloacaridae (Pneumophaginae). The record of Pneumophagus bubonis from the lungs of a single specimen of Bubo virginianus by Fain and Smiley (1989) is still enigmatic. As discussed above, these mites exhibiting general cloacarid morphology are clearly distinguished from the Cloacarinae, and their placement into a separate subfamily has a strong morphological support. The distinctions between pneumophagines and cloacarines are stronger than these between cloacarines parasitizing two chelonian orders Pleurodyra and Cryptodyra. Such morphological distinctions suggest a long history of pneumaphagine parasitism on non-turtle hosts. We believe therefore, that this record is not likely to be the result of a host switch from some as yet unexamined turtle species that happened within the lifespan of that individual bird. On the other hand, the knowledge of the diversity and host distribution of pneumophagines is so far limited to this single record. Therefore we can not hypothesize whether this parasitism has an ancient origin, and birds have inherited cloacarids from their common ancestor with turtles or, that seems much more probable, it was the result of an ancient host shift caused by predation by some birds on live or dead turtles.
Family Ereynetidae (Speleognathinae). This family is represented by three subfamilies. Mites of the subfamily Ereynetidae are predators inhabiting humid microhabitats or facultative parasites of mollusc lungs (snails). Mites of the subfamily Lawrencarinae are endoparasites of amphibian nasal cavities. The subfamily Speleognathinae consists of nasal endoparasites of mammals and birds. It could be suggested that ereynetine-like ancestor of the subfamily Lawrencarinae switched to parasitism on amphibians from their prey - snails or directly from the soil. In the absence of phylogenetic hypothesis for speleognathine mites, two hypotheses of their host relationships could be proposed. According to the first hypothesis, amniotic vertebrates received these mites from amphibians or directly from the soil. Monophyly of the subfamily Speleognathinae is well grounded, therefore, such transition should have happened on one of these two groups. These host switches must be very ancient because of the wide distribution of these mites on avian and mammal orders. An alternative hypothesis suggests the initial parasitism of these mites on a common ancestor of Anamnia and Amniota and extinction of these mites on modern reptiles.
The subfamily Speleognathinae is separated into five tribes, two of them are associated with birds and other three – with mammals.
Two genera of the tribe Boydaiini, Boydaia and Coboydaia are mostly associated with passerines. Among 39 species of the first genus, only four species are, probably, secondary associated with non passerine hosts – Caprimulgiformes, Galliformes, Psittaciformes and Falconiformes. Among six Coboydaia spp, only one is associated with humming birds.
The tribe Trispeleognathini includes the remaining 13 genera of bird-associated speleognathines. All of them parasitize non passerine birds. Most genera are associated with hosts of a single order: the genus Trispeleognathus is associated with Columbiformes, Aureliania – with Strigiformes, Ophthalmognathus – with Pelecaniformes, Psittaboydaia – with Psittaciformes, Neastrida – with Gruiformes, Neoboydaia – mostly with Charadriiformes and one species is recorded from Podicipediformes, Pterniboydaia – with Galliformes, Metaboydaia – with Coraciiformes and Picinyssus – with Piciformes. Four genera are, however, associated with hosts of various orders: Astrida – with Caprimulgiformes, Coraciiformes, and Strigiformes, Ralliboydaia – Gruiformes and Cuculiformes, Phoenicopteriella – with Anseriformes and Phoenicopteriformes, and Speleognathopsis – with Acipitriformes, Galliformes and Charadriiformes.
Reference: Akimov and Gorgol 1990; Fain and Smiley 1989; Kethley and Johnston 1975; Moss et al. 1979; Bochkov 2004, 2008, 2009; Bochkov and Fain 2001; Volgin 1969; Summers and Price 1970; Klimov et al. 2006; Bochkov and OConnor 2003, 2008; Bochkov et al. 1999, 2002; Bochkov and Skoracki 2011; Mayr et al. 2005; Dabert et al. 2011; Casto 1977; Literak et al. 2005; Landmann 1986; Lombert and Moss 1983; Kurochkin 1993; Moss 1979; Mironov 1998; Rieppel 1988; Fain 1985; Andre and Fain 2000.
