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Acariformes: TROMBIDIFORMES) Permanently Associated with Birds M Acarina 20 (2): 67–107 © Acarina 2012 A REVIEW OF PROSTIGMATA (ACARIFORMES: TROMBIDIFORMES) PERMANENTLY associated WITH BIRDS M. Skoracki1, S. A. Zabludovskaya2 and A. V. Bochkov3, 4 * 1Department of Animal Morphology, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61–614 Poznan, Poland 2Schmalghausen Institute of Zoology, National Academy of Ukraine, B. Khmelnitzky str. 15, Kiev, Ukraine 3Zoological Institute of the Russian Academy of Sciences, Universitetskaya Emb. 1, 199034 Saint Pe- tersburg, Russia; e-mail: [email protected] 4Museum of Zoology, University of Michigan, 1109 Geddes Ave., Ann Arbor, Michigan 48109, USA *Corresponding author ABSTRACT: Prostigmatan mites (Acariformes: Prostigmata) permanently parasitizing birds are reviewed at the familial level. Keys to all genera and lists of included species along with verified host records are provided. This ecological group includes about 500 species in 5 families: Cheyletidae (Cheletosomatini, Ornithocheyletiini, and Metacheyletiini), Syringophilidae, Harpirhynchidae (Harpirhynchinae and Harpypalpinae), Cloacaridae (Pneumophaginae), and Ereynetidae (Speleognathinae). The original and reference data on the external morphology, phylogeny, systematics and the host-parasite relationships of these mites are sum- marized. KEY WORDS: Prostigmata, birds, mites, symbionts, systematics, host-parasite relationships INTRODUCTION Prostigmatic mites (Acari: Acariformes: Pros- tion of host phylogeny and in deciphering of the tigmata) permanently associated with birds are po- host biogeography. Such investigations were un- tentially very species-rich groups supposedly in- dertaken on various groups of symbionts, includ- cluding about 5000 species (Kethley and Johnston ing acariform mites, and often showed a high level 1975; Moss 1979), but nearly 10 % (about 500 of phylogenetic congruence between hosts and species) of these mites are recognized to date. symbionts (Klassen 1992). Although some investi- These mites occupy a great diversity of microhab- gations conducted on astigmatan mites did not re- itats on the host body: skin, quills, intracutaneous veal phylogenetically congruent pattern, they pro- layers, and respiratory tract, and are very interest- vided valuable results for the host biogeography ing in the global evolutionary sense as well as in (Bochkov and OConnor 2005). At the same time, several parasitological aspects, including host- as a taxonomically poorly studied group, the pros- parasite relationships. tigmatans permanently associated with birds have This ecological group includes mites of five never been involved in this kind of investigations. families belonging to three phylogenetically dis- The data concerning systematics, phylogeny tant superfamilies: Cheyletidae, Harpirhynchidae, and host-parasite relationships of acariform mites and Syringophilidae of the superfamily Cheyle- permanently associated with mammals and birds toidea, Cloacaridae (Cloacaroidea), and Ereyneti- were recently revised (Proctor 2003; Bochkov dae (Tydeoidea) (Mironov and Bochkov 2009). 2009, 2010), but bird-associated prostigmatans The absence of taxonomic revisions and identifi- were not considered in these works. cation keys for most bird-associated prostigmatans In this paper we provide the family level re- seriously impedes their phylogenetic and ecologi- view of bird-associated prostigmatans, keys to all cal investigations. genera, and check-lists of their species along with Most prostigmatic inhabitants of bird are true verified host records. The data on phylogeny, biol- parasites feeding on live host tissues, but the ma- ogy and host-parasite associations of these mites jority of cheyletids living in feather quills are are briefly discussed. predators feeding on other quill-inhabiting mites and thus should be considered as commensals or MATERIAL AND METHODS even mutualists. The materials used in this work were obtained Taking into consideration the high specificity from acarological collections housed in various of permanently parasitizing prostigmatans to avian museums. Data on bird-associated prostigmatan hosts and their non-random distribution on host families including numbers of recognized species taxa (Fain 1994a; Bochkov 2009; Skoracki 2011), and genera, hosts, microhabitats, and distribution data about these mites could be used for the valida- are summarized in Table 1. Idiosomal and leg seta- 67 M. Skoracki, S.A. Zabludovskaya, A.V. Bochkov A B Fig. 1. Scheme of eleutherengone gnathosoma: A — in dorsal view; B — in ventral view (from Bochkov 2009, with minor modifications). tion of these families is represented in Tables 2–5. Prostigmata includes parasitic forms. Most of the examined materials are deposited Parasites permanently associated with birds in the following collections: Adam Mickiewicz belong to two phylogenetically distant parvorders, University (Poznan, Poland); Royal Belgian Insti- Eupodina (Ereynetidae) and Eleutherengona tute of Natural Sciences (Brussels, Belgium); (Cheyletidae, Cloacaridae, Harpirhynchidae, and Royal Museum for Central Africa (Tervuren, Bel- Syringophilidae). gium); Zoological Institute, Russian Academy of The only possible paleontological record of Sciences (Saint-Petersburg, Russia). these bird-associated mites is the finding of eggs In the taxonomic part, the gnathosomal seta- on a feather from the Lower Cretaceous period tion follows Grandjean (1946), the leg and idio- (northeast Brazil) (Martill and Davis 1998). Au- somal setation follows Grandjean (1939, 1944). thors believed that these eggs were laid by feather The universal setal nomenclature of idiosoma pro- mites (Astigmata: Psoroptidia). These spherical posed by Grandjean (1939) was adopted for Pros- eggs are more similar to those of Cheyletoidea, tigmata by Kethley (1990). Schemes of external than to the strongly elongated eggs of feather mites mite morphology are provided in Figs. 1 and 2. (Bochkov 2008). Proctor (2003), however, sup- The bird systematics follows Clements et al. posed that this feather dropped to water and these (2011). Data about all described species of bird- eggs were laid by Ostracoda. associated prostigmatans are summarized in the Appendix (deposited at Acarina web-site: http:// Key to families of Prostigmata — permanent parasites of birds insects.ummz.lsa.umich.edu/acarina/). 1. Subcapitulum of gnathosoma distinctly devel- SYSTEMATICS AND PHYLOGENY oped (Fig. 1). Palps present. At least some of idio- Suborder Trombidiformes Reuter, 1909 somal and leg setae filiform .............................. 2 Infraorder Prostigmata Kramer, 1887 — Subcapitulum of gnathosoma strongly reduced According to the system of acariform mites or absent. Palps absent. Idiosomal and leg setae proposed by Mironov and Bochkov (2008), the represented by alveoli or fleshy-like projections ... suborder Trombidiformes is separated into four Cloacaridae Camin, Moss, Oliver et Singer, 1967 infraorders, Sphaerolichida, Bimichaelida, Oeh- (Pneumophagus Fain et Smiley, 1989) (Fig. 10) serichestida, and Prostigmata. Only the infraorder 2. Propodonotal setae si represented by unmodi- 68 A review of Prostigmata permanently associated with birds A B C D Fig. 2. Scheme of eleutherengone mite: A — idiosoma in dorsal view; B — same in ventral view; C — setation of legs I–IV; D — tarsus I (from Bochkov 2009, with minor modifications). 69 M. Skoracki, S.A. Zabludovskaya, A.V. Bochkov fied simple setae. Genital papillae absent. Tibia of is located on the ventral side of the trochanter-fe- legs I with or without solenidion φ .................... 3 mur-genu, the absence of the eupathidia on the — Propodonotal setae si represented by bothridia palpal tarsus, the absence of the separate hyster- (Fig. 11A). Genital papillae present. Tibia of legs I onotal shield, the completely fused genital and with complicate ereynetal organ (sensory complex, anal openings in females, the absence of the Fig. 12A) ............ Ereynetidae (Speleognathinae) aggenital setae in both sexes, the absence of setae 3. Distal part of hypostome fused with subcapitu- ft, vsI, solenidion φI, σI, coxal setae 1b (reversed lum. Peritremes situated on subcapitulum, not lin- in Ophioptinae), 3b, and 4c (reversed in Harpypal- ear. Palpal trochanter, femur and genu not fused. pinae). Setae scx very small, covered by lateral extensions Family Cheyletidae Leach, 1815 of propodonotum. Tibia and genu I with 1 solen- idion each .......................................................... 4 Figs. 3–5 — Distal part of hypostome not fused with subca- Type genus: Cheyletus Latreille, 1796 pitulum. Peritremes situated at base of subcapitu- Diagnosis. Gnathosoma moderately or dis- lum, linear. Palpal trochanter, femur and genu tinctly developed (1/5–1/3 of idisosomal length). fused to each other. Setae scx distinctly developed, Subcapitulum bearing setae elc. p, n, ao1 and ao2. situated dorsally. Tibia and genu I without solen- Peritremes situated on rostral part of stylophore, idion ......................................... Harpirhynchidae distinctly segmented, generally M-shaped. Distal Dubinin, 1957 (Figs. 8, 9) part of hypostome fused with stylophore. Hypos- 4. Subcapitulum not deeply submerged in idioso- tomal lips present. Palps linear, consisting of 5 ma, subcapitular apodeme absent. Claw of palpal segments, with various projections in some para- tibia present. Palpal tibia and tarsus separated. Se- sitic forms. Palpal tibia with distinct claw. Palpal tae 4a present. Setae a’I absent ............................. tarsus strongly
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