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Out of Africa: the mite community (Arachnida: Acariformes) of the common waxbill, Estrilda astrild (Linnaeus, 1758) (Passeriformes: Estrildidae) in Brazil

Background The common waxbill, Estrilda astrild (L., 1758) (Passeriformes: Estrildidae) is a small passerine bird native to Sub-Saharan Africa that has been introduced into several regions of the world. Results In the present paper, eight mite species (Acariformes) are reported from this host from Brazil, including three species new to science: Montesauria caravela n. sp., M. conquistador n. sp. (Proctophyllodidae), Trouessartia transatlantica n. sp., T. minuscula Gaud & Mouchet, 1958, T. estrildae Gaud & Mouchet, 1958 (Trouessartiidae), Onychalges pachyspathus Gaud, 1968 (Pyroglyphidae), Paddacoptes paddae (Fain, 1964) (Dermationidae) and Neocheyletiella megaphallos (Lawrence, 1959) (Cheyletidae). Comparative material from Africa was also studied. Conclusions These mites represent at least three morpho-ecological groups regarding their microhabitats occupied on the bird: (i) vane mites (Montesauria and Trouessartia on the large wing and tail feathers); (ii) down mites (Onychalges); and (iii) skin mites (Paddacoptes and Neocheyletiella). On one bird individual we found representatives of all eight mite species. Although the common waxbill was introduced to the Neotropical region almost two centuries ago, we demonstrate that it still retains its Old World acarofauna and has not yet acquired any representatives of typical Neotropical mite taxa.


Background
The common waxbill, Estrilda astrild (L., 1758) (Passeriformes: Estrildidae) is a small passerine bird native to sub-Saharan Africa that has been introduced into several other regions of the world [1,2]. Along with the helmeted guineafowl, Numida meleagris (Linnaeus, 1858) (Galliformes: Numididae), it is among the very few African birds that have successfully adapted to the Neotropics [1,3]. It is the only member of the large family Estrildidae (c.140 species and subspecies) that occurs in Brazil, the remaining species being restricted to Africa and Australasia [1]. Until now, only a single feather mite species, Onychalges pachyspathus , has been recorded from this host [4]. In this paper, we report eight mite species (Acariformes) from E. astrild from Brazil, including three species new to science.

Methods
The material from Brazil was collected from two freshly dead specimens of Estrilda astrild found in and near the campus of the Universidade Estadual Paulista, Rio Claro, São Paulo state. Comparative material from Africa was recently collected with mistnets by teams from the Field Museum of Natural History, Chicago, USA. Additional specimens, collected from museum skins by the late Dr. W.T. Atyeo, are now housed in the University of Michigan Museum of Zoology. In the Brazilian laboratory, one of us (FAH) examined the host bodies under a stereomicroscope and removed mites from them using a needle. The mites were cleared in 30% lactic acid for 24 h at 50°C, and mounted in Hoyer's medium according to the standard technique for small acariform mites [5]. After 5 days at 50°C, the slides were sealed with varnish. Recently collected African specimens were skeletonized in the field, the feathers and skins placed in individual plastic bags with 95% ethanol and transferred to the laboratory of one of us (BMOC). Mite specimens were collected and processed as above. Drawings and measurements of mites were made with a Leica DM3000 microscope equipped with differential interference contrast (DIC) optics and a camera lucida. Pencil sketches were scanned at 300 dpi grayscale, and line drawings were created with Adobe Illustrator CS6 and a Wacom Bamboo Create tablet. The chaetotaxy of the idiosoma and legs follows Griffiths et al. [6] and Atyeo & Gaud [7], respectively, with corrections of coxal setae proposed by Norton [8].
Specimens are deposited in the following collections:
Femur II with ventral crest, other segments of legs I, II without processes. Solenidion σ1 of genu I short, 7-10 long, situated at midlevel of segment. Solenidion σ of genu III inserted basally. Genual setae cGI, II, mGI, II as in male. Setae f of tarsi I, II slightly longer than corresponding seta d, setae f of tarsi III, IV 2-3 times longer than corresponding setae d. Genu IV dorsally inflated, without crest.

Differential diagnosis
Montesauria caravela n. sp. belongs to the emberizae group, a group characterized by having dorsal setae c2 inserted on anterolateral margins of hysteronotal shield, setae f2 present, and coxal fields I-II without large sclerotized areas [13]. The new species most closely resembles M. zosteropis in having lanceolate setae h3 in males, but is distinguished from this and from all previously known species of the emberizae group by the following features: in both sexes, humeral shields present dorsally; in males, a pair of adanal shields present anterior to adanal suckers, seta h3 is much wider than in male M. zosteropis; in females, anterior hysteronotal and lobar shields fused (these shields separated from each other in all previous species of the emberizae group).
Femora I, II with ventral crests (Fig. 4b), other segments of legs I-IV without processes. Ambulacra with pointed median axis. Solenidion σ1 of genu I 8 (7)(8) long, situated at basal half of segment; solenidion σ of genu III inserted at midlevel of segment. Genual setae cGI, II and mGI, II filiform. Seta f of tarsi II about twice the length of corresponding seta d (Fig. 6b); seta f of tarsi III three times longer than corresponding seta d (Fig. 6c). Solenidion φ of tibia IV extending to midlevel of apex of ambulacral disc. Tarsus IV 25 (24)(25)(26) long, with small claw-like apical process; setae d and e buttonlike, seta d situated at basal half of segment (Fig. 6d).
Coxal apodemes I fused into a Y, sternum about half of the total length of these apodemes, anterior arms connected with sclerotized parts of coxal fields I (Fig. 5b).
Femur II with ventral crest, other segments of legs I, II without processes. Solenidion σ1 of genu I short, [8][9] long, situated at midlevel of segment. Solenidion σ of genu III inserted basally. Genual setae cGI, II, mGI, II as in male. Seta f of tarsi I, II slightly longer than corresponding seta d, setae f of tarsi III, IV 2-3 times longer than corresponding setae d. Genu IV dorsally inflated, without crest.

Differential diagnosis
Montesauria conquistador n. sp. belongs to the heterocaula species group, which is so far restricted to the Estrildidae and is characterized by having dorsal setae c2 off the hysteronotal shield, setae f2 present, and coxal fields I-II with large sclerotized areas [13]. Seven species are currently recognized in this group: M. bacillus  (Gaud, 1953), and M. synosterna (Gaud & Mouchet, 1957). Montesauria conquistador n. sp. most closely resembles M. heterocaula in the overall body shape of females (body length about three times body width). It is readily distinguished from M. heterocaula in the following features: in females, setae ps2 button-like (normal, setiform in M. heterocaula); in males, sclerotization between arms of coxal apodemes I is absent (present in M. heterocaula).

Differential diagnosis
Trouessartia transatlantica n. sp. belongs to the estrildae species group [20] and is very close to T. decorata Gaud & Mouchet, 1958, in having, in males, well-separated lobes, postgenital plaque absent, and translobar apodeme absent. It can be distinguished from the latter species by the following features: in males, hysterosomal shield smooth; in females, small elongate lacunae between setae d1 and d2, and two distinct rows of 3-4 elongate lacunae between setae e1 and e2. In T. decorata, males have numerous circular lacunae on the hysteronotal shield, and females have large circular lacunae between d1 and d2 and two distinct rows of 7-8 elongate lacunae between e1 and e2.

Remarks
Described from Estrilda nonnula Hartlaub (Estrildidae) from Cameroon [29], this species is readily recognized by the conspicuous dark edges of the dorsal shields in both sexes, and by the bifurcate seta g of males (Figs. 9 and 10). Santana [20] expressed doubts concerning the association between the only male from the type-host and the few females from E. melpoda (Vieillot, 1817). Here, in addition to the aforementioned material deposited at the MRAC, we analysed specimens from E. astrild from South Africa and Brazil, with males and females from this latter locality, and can confirm the association between both sexes of this species. The female of T. minuscula is herein illustrated for the first time, and Estrilda astrild represents a new host for this mite species. The recent discovery of horizontal transfer of Allopsoroptoides galli from wild Guira cuckoos, Guira guira (Gmelin, 1788), Cuculiformes, to laying hens, Gallus gallus domesticus (Linnaeus, 1758) (Galliformes), in Brazil demonstrates that feather mites may occasionally colonize phylogenetically distant hosts, especially in captivity [42]. In the case of the mites from Estrilda astrild, we suspect that this would be a highly improbable event, given the fact that most feather mites are highly host specific, and the common waxbill remains the only representative of the family Estrildidae introduced in the Neotropics.

Conclusion
In this study, eight mites belonging to five families and two orders are reported for the first time from Estrilda astrild from its introduced range in Brazil, all of which are recorded for the first time in the Neotropics. We conclude that the mite community reported from this bird species contains only typical Old World taxa, despite this bird having been present in the new environment for almost two centuries. No representatives of Neotropical acarine taxa were found associated with this bird. We suspect that the horizontal transfer between these distinct acarofaunas would be quite an unlikely event, since most feather mites are highly host specific, and the common waxbill remains the only estrildid introduced in the Neotropics.