Analgoidea, Analgidae) – a New Species of Feather Mite from the Common Chiffchaff Phylloscopus Collybita (Passeriformes, Sylviidae) from England

Home , Analgidae, Analgoidea, Mosque swallow

DOI: 10.2478/s11686-010-0048-9 © W. Stefan´ski Institute of Parasitology, PAS Acta Parasitologica, 2010, 55(4), 392–398; ISSN 1230-2821 Anhemialges bakeri sp. nov. (Analgoidea, Analgidae) – a new species of feather mite from the Common Chiffchaff Phylloscopus collybita (Passeriformes, Sylviidae) from England

Jacek Dabert1*, Barry Nattress2 and Anna Labrzycka3 1Department of Animal Morphology, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614 Poznań, Poland; 225 West Lea Drive, West Ardsley, Wakefield WF3 1DH, UK; 3Molecular Biology Techniques Laboratory, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614 Poznań, Poland

Abstract A new species of the poorly known feather mite genus Anhemialges Gaud, 1958 is described from the Common Chiffchaff Phyl- loscopus collybita. Anhemialges bakeri sp. nov. differs from all other species of the genus by the shape of setae w and s on tarsi III, which are hair-like and slightly thickened in basal and median parts. In all other described species of Anhemialges, setae w and s on tarsi III are blade-like or shaped as thick spines. The lack of leg III hypertrophy is discussed and interpreted as characteristic feature of the species rather than male homeomorphy. Remarks about the recent and possible species richness of the genus Anhemialges are given.

Keywords Anhemialges, passerine birds, male polymorphism, host-symbiont relationships

Introduction C. senegalensis (L., 1766); and Petit’s Black Saw-wing Psali- doprocne pristoptera petiti Sharpe et Bouvier, 1876 (the re- The feather mite family Analgidae Trouessart et Mégnin, 1884 ports of A. gaudi from this host are probably actually of a comprises 34 genera and over 200 species. All members of different species of Anhemialges, Mironov, pers. com.). this family are commensals or parasites of birds, and occupy 2. A. subinteger (Berlese, 1883) from the Northern House the downy layer of plumage. Especially species-rich analgid Martin Delichon urbicum (L., 1758) and Collared Sand Mar- acarofauna inhabit passeriform birds, of which members of tin Riparia riparia (L., 1758) (the reports of A. subinteger the genus Analges Nitsch, 1818 (Analginae) make up almost from this host are probably actually of a different species of one-third of the analgid species on these birds. The remaining Anhemialges, Mironov, pers. com.). 11 analgine genera associated with Passeriformes are far less 3. A. albidus (Tyrrel, 1882) from the Tree Swallow Tachy- investigated and apparently have more restricted host range. cineta bicolor (Vieillot, 1808). One such understudied genus is undoubtedly the Anhemialges 4. A. gracillimus (Bonnet, 1924) from white eyes (Zos- Gaud, 1958. teropidae): Madagascan White-eye Zosterops m. maderas- After the recent revision by Mironov (2009), the genus An- patanus (L., 1766) (= Z. madagascariensis, type host); hemialges contains four species. Three of these are associated Mascarene White-eye Z. borbonicus (Gmelin, JF, 1789); Sil- with swallows and martins (Hirundinidae): ver-eye Z. lateralis westernensis (Quoy et Gaimard, 1830) (= 1. A. gaudi Mironov, 2009 (type species) from the Barn Z. westernensis); Black-capped White-eye Z. atricapilla Sal- Swallow Hirundo rustica L., 1758 (type host); Wire-tailed vadori, 1879 (= Z. clara); Rennell Island White-eye Z. ren- Swallow H. smithi Leach, 1818; White-throated Blue Swal- nellianus Murphy, 1929; Cape White-eye Z. pallidus Swain- low H. nigrita Gray, GR, 1845; Lesser Striped Swallow Ce- son, 1838; Bare-eyed White-eye Woodfordia superciliosa cropis abyssinica (Guérin-Méneville, 1843); Mosque Swallow North, 1906; and Mountain Black-eye Chlorocharis emiliae

*Corresponding author: [email protected] Anhemialges bakeri sp. nov. from Phylloscopus collybita 393

Sharpe, 1888. Two other host species reported for A. gracil- All measurements are given in micrometers (µm). Length limus, Golden Whistler Pachycephala pectoralis (Latham, of gnathosoma was measured from the distal tips of palpi to 1802) (Pachycephalidae) and Hook-billed Vanga Vanga curvi- the basal margin of the subcapitulum. Idiosoma length was rostris (L., 1766) (Vangidae, represent either accidental con- measured from the anterior margin of prodorsum to the tips tamination or (an-) other Anhemialges species. of the opisthosomal lobes (male) or the posterior end of the The former designation of type species of the genus An- body (females). The sejugal furrow delimited the anterior mar- hemialges made by Gaud (1958), Megninia longipes Troues- gin of hysterosoma. Width of idiosoma was measured at the sart, 1899, turned out to be a misinterpretation repeated by level of setae c2, width of hysteronotal shield was measured subsequent authors several times during last 60 years. This at anterior margin. Distance between different pairs of idioso- species was originally described by Trouessart from another mal setae is the shortest distance between corresponding trans- host, the Horned Screamer Anhima cornuta (L., 1766) (An- verse setal rows. The nomenclature of morphological features himidae) from South America. When this misidentification and chaetotaxy of body and legs follows that of Gaud and was found out (Mironov 2009), it formally appeared that the Atyeo (1996) and Mironov (2009). English and Latin names mite species from swallows used as the type of Anhemialges of birds are those in Dickinson (2003). does not have a name. Therefore it was formally described as a new species A. gaudi Mironov, 2009 with the Barn Swal- low Hirundo rustica as the type host. The species from the Taxonomy Horned Screamer retained its original name in the recent taxonomic form Anhimomegninia longipes (Trouessart, 1899) Anhemialges bakeri sp. nov. (Figs 1–4) as a type species of the new genus Anhimomegninia Miro- nov, 2009. Type material There are also numerous reports about collecting speci- mens of Anhemialges from other passeriform birds (Gaud 1964, From the Common Chiffchaff Phylloscopus collybita (type McClure and Ratanaworabhan 1973, Mironov 1983, Bishop host): 1 male holotype, 2 female paratypes, Linton, near and Heath 1998, Kolarova and Mitov 2008). Unfortunately, Wetherby, West Yorkshire, England on 03 April, 2005, all these records are without species identification, mostly be- leg. B. Nattress, #AMU01750. The mites were found on the cause of incomplete material (no males present). Undoubted- neck and back coverts, including upper tail coverts. Types ly these data and also some reports regarding undescribed are deposited in the Department of Animal Morphology, species from passerine birds (e.g. from Locustella luscinioides Faculty of Biology, A. Mickiewicz University, Poznań, (Savi, 1824), Mironov, pers. com.) show that the species rich- Poland. ness of the Anhemialges is undoubtedly much greater than recent data suggests. Differential diagnosis In the present study we describe a new Anhemialges species from an Old World warbler, the Common Chiffchaff The comparison to other species of the genus is difficult since, Phylloscopus collybita (Vieillot, 1817). In his paper, Černý with the exception of Anhemialges gaudi, all remaining named (1965) recorded finding of Anhemialges females on the Wil- species are incompletely described and badly illustrated and low Warbler Phylloscopus trochilus (L., 1758) in southern need thorough taxonomic redescription. Males of Anhemial- Sweden. However, because species determination in this ge- ges bakeri sp. nov. are most similar to those of A. subinteger nus is not reliable on the basis of females alone, this species in having setae ps1 that are not longer than 1.5 times the dis- was not formally described due to the lack of males in the tance between them and short opisthosomal lobes that, meas- Černý sample. It is highly possible that the new species de- ured together with membrane on lobar apices, are as long as scribed here is conspecific with the one found on P. trochilus wide at the base; in the remaining named species setae ps1 are by Černý (1965). 3–4 times longer than the distance between them or the opisthosomal lobes with membrane are twice as long as they are wide at the base. The new species differs from A. subinteger Materials and methods in lacking paragenital apodemes and having setae d2 much shorter than the distance between them; in A. subinteger a pair The material used in the present study was collected (by BN) of longitudinal paragenital apodemes is present and setae d2 from a Common Chiffchaff Phylloscopus collybita from Lin- are much longer than the distance between them. ton, near Wetherby, West Yorkshire, England, 53º55΄N, In addition, A. bakeri sp. nov. differs from all other named 1º24΄W. The bird was a road casualty. The mites were moun- species of the genus by the shape of setae w and s on tarsi III, ted on slides using a polyvinyl lactoglycerol medium and ex- which are hair-like with thickened basal and median parts; in amined under Olympus BX51 light microscope with No- all remaining species setae w and s on tarsi III are blade-like marsky differential interference contrast (DIC). Drawings or shaped as thick spines. Also, the new species have macrose- were made using a camera lucida drawing device. tae h3 simple, setiform, while in species from swallows 394 Jacek Dabert et al.

(Hirundinidae) setae h3 have membranous enlargement in narrowing considerably in opisthosomal part, length 329, central part. width 148, length/width 2.2. Propodosomal and hysterosomal lengths 100 and 229 respectively, propodosoma/hysterosoma Description 0.4. Pronotal shield trapezoidal with wider posterior end, length 73, maximal width 60, length/width 1.2; posterior mar- Male, holotype (Figs 1 and 3). Gnathosoma with oblong sub- gin concave with two small triangular extensions 6 in length. capitulum and with convex lateral margins, length 41, width The shield has thicker and more pronounced punctation in 34, length/width 1.2. Idiosoma elongated, parallel-sided and postero-medial part and more heavily sclerotized lateral mar-

Fig. 1. Male of Anhemialges bakeri sp. nov.: A – dorsal view, B – ventral view Anhemialges bakeri sp. nov. from Phylloscopus collybita 395

gins. Scapular shields large, roughly triangular, developed on ceeding terminally lobar apices by rounded ends; membrane dorsal side only with flat suprategumental extension in pos- reaching laterally bases of setae h3. Incision in interlobar tero-mesal angle. Hysteronotal shield with concave lateral and membrane triangular, length 26, maximal width 39. All dorsal anterior margins, length 202, width 88; shield uniformly and and lateral setae piliform. Setae vi 6 long, ve represented by finely punctate with some longitudinal striae in posterior part hollow alveolae. Setae se and si inserted on posterior angles of and two longitudinal lateral bands of thicker dots between pronotal shield; se 180 long, si 14 long, distance between setae opisthonotal gland openings gl and setae e1. Posterior end of se:se 50, si:si 40. Dorsal setae c1 absent. Setae c2 inserted on opisthosoma with narrow opisthosomal lobes, length 43, width striated tegument, shaped as macrosetae, 140 long. Setae cp 31 (at the level of setae f2), separated by trapezoidal terminal and c3 inserted on humeral shields, cp 76 long, finer c3 50 cleft (excluding supranal concavity). Anterior margin of ter- long. Setae d2 relatively short, 43 in length, about half the minal cleft concave and fused to longitudinal poorly outlined length of e2, 100 long. Setae d1 and e1 present, shaped as mi- supranal concavity. Interlobar membrane wide and slightly ex- crosetae. Setae e1 set on the level of cupules im and posterior

Fig. 2. Legs I–IV of the male Anhemialges bakeri sp. nov. 396 Jacek Dabert et al.

to opisthonotal gland openings gl. Macrosetae h2 and h3 sube- Epimerites I Y-shaped, sternum over 2/3 of total length of qual (about 320 each), inserted on opisthosomal lobes, h2 epimerites I. Coxal fields not sclerotized, at most with narrow slightly posterior to level of setae ps1, h3 on terminal tips of sclerotized areas along epimerites. Epimerites IV rudimentary lobes; h3 setiform, without flattened enlargement in medial with setae 4a on anterior ends. Genital arch wide, 16 × 31, part. Distances between dorsal hysterosomal setae and pores: aedeagus minute, several times shorter than the branches of c2:d2 61, d1:d2 24, e1:e2 12, d2:e2 77, e2:h2 57, h2:h3 20, genital arch. Epiandrum thin, arranged as shallow arch, 8 long, ps1:h3 27, h2:h2 68, h3:h3 57, e1:gl 19. 36 wide. Genital papillae located at tips of epiandrum. Para-

Fig. 3. Female of Anhemialges bakeri sp. nov.: A – dorsal view, B – ventral view Anhemialges bakeri sp. nov. from Phylloscopus collybita 397

Fig. 4. Tibiae and tarsi III–IV of the female Anhemialges bakeri sp. nov. genital apodemes absent. Gastral shield consists of two longi- cGI on genu setiform, cGII with membraneous basal exten- tudinal pieces, length 50, width of each 19 (Fig. 1B). Adanal sion. Setae w and s on tarsus III hair-like, slightly widened shield paired, represented by two small irregular sclerites car- basally. Setae d and e on tarsi IV reduced, e shaped as small rying setae ps3. Each piece is fused anteriorly with posterior spine, d as transparent button. margin of corresponding part of the gastral shield. Adanal Female (Figs 2 and 4, range of measurements for 2 para- membranes narrow stretching from posterior ends of gastral types). Gnathosoma shaped as in male, length 50–51, width shield to the bases of setae ps2. Adanal apodemes running 43, length/width 1.25. Idiosoma parallel-sided with rounded along base of adanal membranes, poorly sclerotized, espe- posterior margin, length 485–496, width 185–198, length/ cially in posterior part. Anal suckers shaped as short cylinders width 2.4–2.7. Propodosoma and hysterosoma lengths 116– with smooth corollas, diameter 12. Distinct cupules ih set pos- 127 and 369–373 respectively, propodosoma/hysterosoma 0.3. tero-lateral to anal suckers. Anal field flanked by narrow lat- Pronotal shield shaped as in male, length 92–93, maximal eral adanal membranes reaching posteriorly the level of cu- width 82–89, length/width 1.0–1.1. Scapular shields shaped pulae ih only. Distances between ventral hysterosomal setae: similarly to males but extended to the ventral side, hys- 3a:4a 26, 3a:g 32, g:ps3 81, ps2:ps2 76. teronotal shield absent. Setae vi length 10–14, ve as empty Legs I, II, and IV of similar size (Fig. 2). Legs III signifi- alveolae. Setae se and si inserted within the shield; se 174– cantly longer and thinner than legs IV, extending slightly be- 194 long, si 20–23 long, distance between setae se:se 65–67, yond the posterior extremity of the lobar apices. Femur I with si:si 54–56. Setae c2 set at the level of setae cp, about 4 times large retrograde ventral apophysis; apophysis on femur II longer than setae d2 and e2. Setae d2 and e2 subequal, shorter minute. Tibiae I and II with small poorly sclerotized ventral than half of idiosoma width; d2 not reaching the bases of e2. triangular protuberances; tibiae II with apicodorsal sharp Minute setae d1 and e1 present; d1 set anterior to the level of spine. Tarsi I and II with apical spines and ventral well-devel- setae d2, e1 at the level of e2. Distances between dorsal hys- oped membraneous collars bearing the base of setae s. Tarsi III terosomal setae and pores: c2:d2 80–84, d1:d2 20–23, e1:e2 narrow and elongated (54) with single apical spine, tarsi IV 2–4, d2:e2 107–112, e2:h2 136–138, h2:h3 7, ps1:h3 2–3, conical and slightly curved, with bidentate apex. Ambulacral h2:h2 104, h3:h3 85–87, e1:gl 5–9. Copulatory opening sub- stalks with two dorsal spines triangular protuberances. Setae terminal, set on small protuberance. 398 Jacek Dabert et al.

Epimerites I as in males. Epigynum well-developed, References arched, length 18–19, width 47–52. Setae 3a set on the tips of the epigynum. Setae ps2 inserted posterior to setae ps3, ps3 Bishop D.M., Heath A.C.G. 1998. Checklist of ectoparasites of birds twice as long as ps2. Distances between ventral hysterosomal in New Zealand. Surveillance, 25, 31. setae: 3a:4a 82–83, 3a:g 20–23, 4a:ps3 208–214, ps2:ps2 Černý V. 1965. Feather mites (Analgesoidea) from birds trapped at the Falsterbo Bird Station, southern Sweden. Acta Universi- 90–92. tatis Lundensis, 8, 3–8. Shape and setation of legs I, II as in male. Tarsi III 47–50 Dickinson E.C. (Ed.) 2003. The Howard & Moore complete check- long, tarsi IV 60–63 (Fig. 4). Solenidion φIII slightly shorter list of the birds of the world. 3rd Edition. Christopher Helm, than corresponding tarsus, φIV about half the length of the London, 1039 pp. corresponding tarsus. Legs IV are relatively short with refer- Gaud J. 1958. Acariens plumicoles (Analgesoidea) parasites des oiseaux du Maroc. II. Analgesidae. Bulletin de la Société de ence to opisthosoma and their ambulacral tips do not extend to Sciences Naturelles et Physiques du Maroc, 38, 27–49. the level of the anterior end of anal slit (Fig. 2B). Gaud J. 1964. Mission de Zoologie médicale au Maniema (Congo, Léopoldville) (P.L.G. Benoit, 1959). 8. Acariens plumicoles Etymology (Analgesoidea). Musée Royal de l’Afrique Centrale, Tervuren, Annales Sciences Zoologiques, 132, 119–130. Gaud J., Atyeo W.T. 1996. Feather mites of the World (Acarina, The specific epithet bakeri is dedicated to Dr Richard A. Astigmata): the supraspecific taxa. Musée Royal de l’Afrique Baker, an authority on the Unionicolidae, a teacher of many Centrale, Tervuren, Annales Sciences Zoologiques, 277, Part generations of British acarologists and guide and mentor to 1, 193 pp., Part 2, 436 pp. the junior author (BN). Kolarova N., Mitov P. 2008. Feather mites of the Superfamily Anal- goidea (Acari: Astigmata) from Passerines (Aves: Passeri- formes) in South Dobrudzha, Bulgaria. Acta Zoologica Bul- Remarks garica, Suppl. 2, 91–102. McClure H.E., Ratanaworabhan N. 1973. Some ectoparasites of the The small body size and lack of thickening of legs III in the birds of Asia. Jintana Printing Ltd, Bangkok, 219 pp. only male known for A. bakeri could be interpreted as home- Mironov S.V. 1983. Feather mites (Sarcoptiformes, Analgoidea) of omorphy, if male polymorphism exists in this species. How- Passeriformes of the Nizhnyesvirsk Preserve. In: (Ed. L.A. Bibikova) Parasitological research in nature reserves. Sbor- ever, Mironov (2009) has shown a strong intraspecific nik Nauchnykh Trudov TsNIL Glavokhoty RSFSR, Moscow, variability in size but no discrete polymorphism in Anhemial- 82–94 (In Russian). ges males, and specifically no evidence for lack of hypertro- Mironov S.V. 2009. On the identity of the feather mite genus An- phy of legs III. Therefore we assume that the thin legs III are hemialges Gaud, 1958 (Astigmata: Analgidae), with the de- a characteristic feature of the new species, not related to male scription of a new genus of the analgid subfamily Megni- niinae. Acarina, 17, 89–100. polymorphism.

(Accepted August 05, 2010)