Microhabitats on the host body
Prostigmatan mites permanently associated with birds, being represented by both ecto- and endoparasities, occupy wide spectrum of microhabitats on the host body: skin, subcutaneous layers, nasal cavities, feather quills, and even bronchi. Most of these mites belong to morphoecotypes recognized in feather mites.
Skin inhabiting prostigmatans of the families Cheyletidae (Ornithocheyletiini) and Harpirhynchidae (many genera of Harpirhynchinae) correspond to the epidermoptoid morphoecotype, which is analogous to the skin morphoecotype of mammal-associated mites. Prostigmatan mites refrred to this morphoecotype have the terminally situated gnathosoma, which can possess various apophyses used for attaching, the idiosoma is strongly flattened dorso-ventrally, distinctly developed setation of the idiosoma and legs, and the male genital opening located dorsally. Their legs are inserted laterally; ambulacra are well developed, at least, on the anterior legs. Many representatives of cheyletids spin the group (Bakericheyla) or individual (Ornithocheyletia) cobweb covers. Such cobweb cover protects mites and their eggs, stabilises the temperature and humidity regime and prevents elimination from the host body.
Harpirhynchine females of some skin-inhabiting genera, for example, Neharpyrhynchus, are quite different morphologically from other skin-inhabiting mites. Their females are attached at the base of calamus of the body covert feathers on the neck or head of avian host. They are oriented parallel to the length of the shaft, with mouthparts inserted in the host skin; their idiosoma is sacciform and the eggs are laid in a string; the female opisthosoma, thus, serves as the "stalk" or site of attachment for the eggs.
The bird skin almost devoid of glands is not so beneficial substrate as the mammalian skin, therefore, mites of the intracutaneous morphoecotype like Demodicidae and Psorergatidae are absent among bird-associated prostigmatans. Among them, however, are present mites of the skin-burrowing morphoecotype (analogous to the knemidocoptid morphoecotype in feather mites) belonging to the family Harpirhynchidae. In this family, the tendency of transition from the skin surface (ectoparasitism) to intradermal parasitism (endoparasitism) is widely observed and this switches independently happened within several harpirhynchid genera (for example Harpyrhynchoides). Harpirhynchid females accumulate in the feather follicles, where they develop subcutaneous cysts; many of them are strongly morphologically modified. At the same time, harpirhynchid males belonging to skin-burrowing species do not undergo strong morphological modifications. Females of the subfamily Harpypalpinae, forming the subcutaneous cysts, are even less specialized than ectoparasitic mites of the subfamily Harpirhynchinae, because their posterior legs are not reduced, and their opisthosomal setation is more reach than in harpirhynchins. In some genera of Harpirhynchinae, cyst-inhabiting species (Harpirhynchus or Hapyrhynchoides) also do not significantly differ from ectoparasitic (skin-inhabiting) representatives of the family, whereas species of the genera Anharpyrhynchus, Cypsharpirhynchus, Harpyrhynchiella, and Trichorhynchiella are strongly modified being habitually similar with some skin-burrowing mites of the astigmatan subfamily Teinocoptinae (Sarcoptoidea: Sarcoptidae). Their gnathosoma is replaced to the ventral idiosomal surface, the idiosoma is sacciform, the anterior legs are shortened and the posterior legs are strongly reduced or lost; the body and leg setation is very poor.
The parasitic prostigmatans inhabiting quills correspond to the dermoglyphid morphoecotype. Among prostigmatan mites this morphoecotype is represented by mites of the family Syringophilidae and cheyletid mites of the tribe Metacheyletiini. The idiosoma of these mites is strongly elongated (Syringophilidae) or egg-shaped (Metacheyletia) and weakly sclerotized. Legs are relatively short. In contrast to feather mites which take harborage within quills, many idiosomal and some leg setae of these mites are long or ultralong and control, thus, a significant space around the mite. Mites of the subfamily Syringophilinae are mostly associated with the quills of flight feather, whereas the absolute majority of picobiins inhabit quills of the body feathers. Females of the latter subfamily are characterized by the physogastry - an extensive enlargement of the female hysterosoma in the process of feeding - that is unknown for other quill mites.
The predatory mites inhabiting quills belong to the tribe Cheletosomatini (Cheyletidae). These mites do not differ habitually from nidicolous cheyletids. Even mites of the cheletosomatine genus Picocheyletus transferred from a predation to parasitism do not differ morphologically from their predatory relatives. It should be noted, however, that some idiosomal and leg setae of these mites are ultralong, as in parasitic prostigmatans inhabiting quills.
The nasal prostigmatan parasites of birds are represented by mites of the subfamily Speleognathinae (Ereynetidae). These mites belong to the respiratory morphoecotype established by Bochkov (2007) and are not significantly modified in comparison to free-living relatives. Their palps are 1-3-segmented (four-segmented palps in free-living ereynetids), the idiosoma is slightly flattened dorso-ventrally and in some species bears the eyes, the body and leg setae are relatively short, and the legs are well developed, inserted laterally, and bear empodium and paired claws; in males, the aedeagus is absent. An interesting adaptation of parasitic ereynetids is the presence of calyptostatic nymphs. In these mites, the active stages are only larva and adults.
The interstitial bird parasites among prostigmatans are represented by a single species Pneumophagus bubonis (Cloacaridae) from tissues around bronchi of Bubo virginianus (Strigiformes: Strigidae) from USA. This is a typical representative of the interstitial morphoecotype. Among acariform mites permanently associated with vertebrates this morphoecotype is represented by the families Epimyodicidae and Cloacaridae . The body of these mites has a slightly elongated and streamlined form; in females, the gnathosoma is almost completely reduced and represented only by chelicerae (absent in males), the legs are thickened and shortened and their segments are telescopic, almost all body setae are absent, and the leg setation is strongly reduced; the coxal apodemes are hypertrophied. Thus, cloacarid mites are almost ideally adapted for moving in friable interstitial tissues.
Thus, bird-associated prostigmatans are represented by four main morphoecotypes: skin (epidermoptid), skin-burrowing (knemidocoptid), quill (dermoglyphid), and interstitial.
In feather mites and mammal-associated Acariformes, the skin-inhabiting forms belong to the ancestral morphoecotype and most other morphoecotypes are its derivations. In prostigmatans, the colonization of different microhabitats on the bird body has been realized by free-living mites independently, mostly omitting a stage of the skin ectoparasitism. Quill predators and parasites switched to the life in the feather quills originate directly from the nest predation; nasal mites (Speleognathinae) also originated directly from the free-living forms omitting the skin parasitism; interstitial mites (Pneumophaginae) supposedly switched to birds from turtles and the origin of cloacarid parasitism is still not clear; only intracutaneous mites (some Harpirhynchidae) originated from ectoparasitic forms inhabiting the skin surface.
This complicated picture of colonization of the avian body by prostigmatan mites could be explained by the absence of the direct phylogenetic links between these mites. Since all bird-associated prostigmatans are true parasites feeding on the live tissues or predators, they did not colonize the feather vexillums (proctophyllodid morphoecotype) or the down feathers (analgid morphoecotype); nor they did occupy the quill walls inhabited by some feather mites (Laminosioptidae).
References: Mironov 1987; Bochkov 2007; Akimov and Gorgol 1990; Moss et al. 1979; Bochkov and Literak 2011; Fain 1995; Literak et al. 2005; Johnston and Kethley 1973; Skoracki et al. 2001; Skoracki 2011; Andre and Fain 2001; Fain and Smiley 1989; Bochkov et al. 2008; Bochkov and OConnor 2008.
