Six new feather mite species (Acari: Astigmata) from the carolina parakeet Conuropsis carolinensis (Psittaciformes: Psittacidae), an extinct parrot of North America

We describe six new feather mite species collected from museum skins of the carolina parakeet Conuropsis carolinensis Linnaeus, 1758, which lived in North America and became extinct at the beginning of the 20th century: Genoprotolichus simplex sp. n., Lopharalichus beckeri sp. n., Neorhytidelasma conuropsis sp. n. (Pterolichidae: Pterolichinae), Chiasmalges carolinensis sp. n. (Psoroptoididae: Pandalurinae), Fainalges gracilitarsus sp. n., and Protonyssus proctorae sp. n. (Xolalgidae: Ingrassiinae). Brief comments on the current systematic state and host associations of these feather mite genera are provided.


Introduction
Among non-passerine orders of birds, parrots (Psittaciformes) are characterized by a taxonomically and morphologically diverse feather mite fauna. In the past 20 years, the feather mite fauna of New World parrots has been extensively and purposefully explored (Atyeo 1985(Atyeo , 1988(Atyeo , 1989a(Atyeo , 1989b(Atyeo , 1989cAtyeo and Pérez 1988a, 1988bAtyeo et al. , 1988. To a lesser extent, feather mites associated with parrots from Africa (Gaud 1980) and Australia and the Indo-Malaya region (Gaud 1968;Atyeo and Pérez 1982;Gaud 1987, 1991;Mironov and Galloway 2002; have also been investigated. In the course of these studies, it was discovered that the feather mite fauna associated with psittaciforms is extremely rich in diversity of higher-ranking taxa and in richness of mite species inhabiting each parrot species. In total, representatives of 10 feather mite families from two superfamilies have been recorded from the order Psittaciformes (Gaud and Atyeo 1996). Most studies of common and widely distributed parrot species have shown that one host species may harbour more than 15 mite species occupying very specific locations in the plumage Pérez 1995Pérez , 1996. In spite of investigations carried out so far, the diversity of feather mites associated with psittaciforms in both hemispheres has been only superficially explored, and the mite fauna of many parrot species is still completely unknown.
In the course of our current project on biodiversity, systematics and phylogeny of feather mites associated with parrots, we have had the rare opportunity to collect feather mites from the carolina parakeet Conuropsis carolinensis Linnaeus, 1758. This endemic North American parrot species was once widely distributed in the south-eastern USA. Due to persecution in the name of food crop protection and the destruction of the forest habitat of the carolina parakeet, this parrot was rendered extinct by the beginning of the 20th century (Brooks 2000). Although this species has been extinct for less than 100 years, no feather mites have ever been described from it. The present paper gives descriptions of six new feather mite species collected from the carolina parakeet and belonging to six different genera of the families Pterolichidae (Pterolichoidea), Psoroptoididae and Xolalgidae (Analgoidea). These species represent two distinct ecological groups of feather mites in regard to their location in the plumage of the host. Three of the described mite species of the family Pterolichidae represent the ecological group of feather mites specialized for inhabiting feathers with well-developed vanes (flight and tail feathers and wing coverts), while the mites of the families Psoroptoididae and Xolalgidae are commonly located among down feathers and downy parts of body covert feathers.

Material and methods
The material was collected by the authors from a dry museum skin of the carolina parakeet Conuropsis carolinensis (access number 1440), deposited in the Ü bersee Museum (Bremen, Germany). Mites were extracted from the sample according to the scratching method of Gaud and Atyeo (1996) and preserved in 70% ethanol. For light microscope study mites were mounted on slides in Faure medium (Evans 1992). Before mounting, mites were softened and cleared in 10% lactic acid at +60uC for 2-3 days.
The descriptions of new taxa follow the standard schemes used for respective taxa of feather mites (Gaud and Atyeo 1996;. The nomenclature of idiosomal chaetotaxy follows Griffiths et al. (1990) and leg chaetotaxy is that of Atyeo and Gaud (1966). Measurements in the descriptions are given in micrometres (mm); measurements of a distance between idiosomal setae of different pairs imply a distance between transverse rows formed by setal pairs. The taxonomic system, Latin and common names of hosts in the present study follow those of del Hoyo et al. (1997).
PTEROLICHOIDEA Gaud and Atyeo, 1978PTEROLICHIDAE Trouessart and Mégnin, 1884PTEROLICHINAE Trouessart and Mégnin, 1884 Lopharalichus Gaud and Atyeo, 1996 The genus Lopharalichus belongs to the Protolichus generic group (Pterolichinae). With 21 genera, the Protolichus group is the most diverse of three pterolichid groups associated exclusively with parrots. Within this generic group, the genus Lopharalichus and four closely related genera, Aralichus Gaud, 1966, Chelomatolichus Gaud and Atyeo, 1996, Tanyaralichus Gaud and Atyeo, 1996, Scolaralichus Gaud and Atyeo, 1996, constitute the Aralichus generic complex (Gaud and Atyeo 1996). Mites of this complex are restricted to New World parrots (Psittacinae: Arini). The Aralichus complex is characterized as follows. In both sexes, the scapular setae se, si are setiform, very short and subequal in length; the hysteronotal shield is commonly covered with a pattern of numerous pit-like lacunae; apicoventral apophyses on tibiae, genua and femora of legs I, II are commonly well-developed. In males, legs I, II are not hypertrophied; the adanal apodemes are welldeveloped; genital apodemes are greatly reduced or absent. By 1990, over 30 species had been recognized within this complex (Atyeo 1985(Atyeo , 1989a(Atyeo , 1989bPérez and Atyeo 1986;Atyeo and Pérez 1990), but all were treated as members of a single genus Aralichus. Later on, in the world revision of feather mite supraspecific taxa (Gaud and Atyeo 1996), representatives of the genus Aralichus were rearranged into five separate genera; two species were included in the new genus Lopharalichus. Although two formerly known Lopharalichus species have been recorded only from the parrot genera Forpus Boie, 1858 and Pyrrhura Bonaparte, 1856, according to the data of the mentioned experts, this genus is widely distributed on New World parrots. The scheme of description used below follows the most expanded format proposed by Atyeo (1989b).
Tarsi I, II expanded ventrally; apicoventral apophyses of tibiae and genua I, II acute; blade-like ventral apophyses of femora I, II with three to five acute teeth. Tarsus IV 58 in length, setae d, e thin thorn-shaped, adjacent to each other ( Figure 1C).

Differential diagnosis
Among the two species previously described (Mégnin and Trouessart 1884;Gaud and Atyeo 1996), the new species is more similar to Lopharalichus cribriformis (Mégnin and Trouessart, 1884) described from the green-rumped parrotlet Forpus passerinus Linnaeus, 1758 in Guyana by having simple spine-shaped ventral apophyses on genua I, II and by pronounced pit-like lacunae on hysteronotal shield. Males of L. beckeri sp. n. differ from L. cribriformis by having parallelogram-shaped setae ps1 with slightly rounded apex, and setae e2 subequal in length to setae f2; females are distinguished by having triangle-shaped setae f2. In males of L. cribriformis, the apices of setae ps1 are acute, setae e2 are twice as long as f2; in females, the setae f2 are large and foliform, almost circular, and with a vein.

Etymology
This species is named in honour of Dr Peter-René Becker, the head of the Natural History Department in the Ü bersee Museum (Bremen, Germany).

Remark on chaetotaxy
The assignation of chaetotaxy nomenclature for the ventral coxo-genital setae 3a, 4a and g in males given in the present paper (Figures 1, 2) differs from that applied for the genera of the Aralichus complex by Atyeo and Pérez (Atyeo 1988(Atyeo , 1989a(Atyeo , 1989b(Atyeo , 1989cAtyeo and Pérez 1990). Comparison of the male ventral chaetome in various representatives of the Protolichus group genera and in other representatives of Pterolichidae (Mironov 2003; gives clear evidence that the setae disposed slightly mesal to the inner tips of epimerites IIIa should be referred to the coxal setae 3a, but not 4a as Atyeo and Pérez suggested, while two median pairs situated anterior and posterior to the genital apparatus should be treated, respectively, as g and 4a. Genoprotolichus Gaud and Atyeo, 1996 This genus, as the previous one, belongs to the Protolichus generic group and currently includes three described species (Favette and Trouessart 1904;Gaud and Atyeo 1996). Mites of the genus Genoprotolichus are associated exclusively with New World parrots. Gaud and Atyeo (1996) reported a great number of undescribed species, which they had collected from 50 species of 14 parrot genera. According to these authors, the genus Genoprotolichus represents an archaic form of the Protolichus group and probably is very close to the common ancestor of the Protolichus group.

Differential diagnosis
Among three previously described species, the males of the new species are most similar to those of Genoprotolichus major (Favette and Trouessart, 1904) described from the austral parakeet Enicognathus ferrugineus (Mü ller, 1776) in Patagonia by lacking ornamentation on the hysteronotal shield. The males of G. simplex sp. n. differ from that species by having completely sclerotized prodorsum without any striation, and much smaller idiosomal size, 506-510; females are distinguished by weakly expressed narrow longitudinal lacunae in posterior half of the hysteronotal shield and also by idiosomal size less than 510. In the males of G. major, the prodorsal shield is rectangular, extending slightly beyond the row of scapular setae, while the remaining part of prodorsum is striated and weakly sclerotized, the length of idiosoma is 630-650; the females have clear longitudinal striation in lateral parts of hysteronotal shields, and their idiosomal length is 610-630.

Etymology
Specific name (Latin simplex, simple) points out a monotonously punctured surface of the hysteronotal shields.
Neorhytidelasma Mironov and Pérez, 2003 The genus Neorhytidelasma belongs to the Rhytidelasma generic group, which with 33 species, nine genera takes second place in number of known taxa among three pterolichine generic groups associated with parrots (Gaud and Atyeo 1996;Mironov and Pérez 2003;. As for the two previous genera, representatives of Neorhytidelasma are restricted to New World parrots. Based mainly on morphological features of males, Atyeo and co-authors Pérez 1988a, 1988b;Atyeo et al. 1988) recognized five species groups (cornigera, forficiventris, mesomexicana, tritiventris, ulocerca) among eight primarily described species and numerous collected but undescribed species of Neorhytidelasma. These studies have also shown that representatives from different species groups may coinhabit the same host species, occupying different locations in the flight feathers. A review and key to all previously known species were provided by Mironov and Pérez (2003).
Epimerites I fused as in the male. Epigynium semicircular, 27651, almost completely anterior to level of setae c2 ( Figure 5D). Ambulacral discs as in the male.

Differential diagnosis
Neorhytidelasma conuropsis sp. n. belongs to the mesomexicana species group, which is characterized by the following combination of characters: in both sexes, the anterior end of prodorsal shield lacking spine-shaped projections; in males, opisthosoma with lateral bluntangular extension, the terminal lamellae with widely separated bases, obliquely directed by apices to midline and bearing transverse crests, setae h1 are close to bases of macrochaetae h2 Mironov and Pérez 2003). Among two species previously referred to this group, the new species is most similar to N. mesomexicana  described from the green parakeet Aratinga holochlora (Sclater, 1859) in Mexico by having the prodorsal shield completely fused with the scapular shields. In N. bicostata (Atyeo and Pérez, 1988) known from the subspecies of orange-fronted parakeet A. canicularis clarae Moore, 1937 in Mexico, these shields are independent from each other. Males of the new species differ from N. mesomexicana by having setae g situated posterior to tips of epimerites IIIa and distant to each other ( Figure 4B); females are distinguished by the position of epigynium, which is almost completely anterior to the level of setae c2, and well-expressed supranal concavity. In the males of N. mesomexicana, the genital setae g are situated at the level of epimerites IIIa and the distance between them is twice shorter than between setae 4a situated on inner margins of genital apodemes; in the females of this species, the anterior margin of epigynium is approximately at the level of setae c2, and the supranal concavity is not expressed.

Etymology
Specific name is directly derived from the generic name of the host. ANALGOIDEA Trouessart and Mégnin, 1884PSOROPTOIDIDAE Gaud, 1958PANDALURINAE Gaud and Atyeo, 1982 Chiasmalges Gaud and Atyeo, 1967 The taxon Chiasmalges was originally established as a genus (Gaud and Atyeo 1967), but subsequently these authors (Gaud and Atyeo 1996) proposed to treat it as a subgenus of the genus Mesalgoides Atyeo, 1967. However, Pérez andRamirez (1996) continued to consider Chiasmalges as a genus. According to recent partial generic revision of the subfamily Pandalurinae (Mironov 2004), the generic rank of Chiasmalges is strongly supported. The genus Chiasmalges is restricted to parrots and has included up to now only three described species: Chiasmalges annahofmannae Ramirez, 1996, Ch. hirsutus (Trouessart, 1899) and Ch. polyplectrus Gaud and Atyeo, 1967.
Female. Female unknown.

Differential diagnosis
The new species is most closely related to Chiasmalges polyplectrus described from Aratinga holochlora (Sclater, 1859) in Mexico (Gaud and Atyeo 1967). The male of Ch. carolinensis sp. n. differs from that species by the following characters: legs III extends beyond the apices of terminal lamellae by distal three-quarters of tarsus and the aedeagus extends only to the genital setae g (Figure 6A, B). In males of Ch. polyplectrus, the legs III extend beyond the terminal lamella apices by whole tarsus III, and the aedeagus is much longer and extends to the anterior tips of adanal apodemes.

Etymology
The specific epithet derives from the specific name of the type host.

Remark on chaetotaxy
Among publications of authors dealing with descriptions of pandalurine mites, there is discordance in the chaetotaxy nomenclature for three pairs of setae situated on the lateral margins of opisthosomal lobes in males, f2, h2, ps2, because their homology to those in other representatives of Analgoidea is not completely clear (Gaud and Atyeo 1967;Č erny 1974;Faccini et al. 1976;Pérez and Ramirez 1996;Mironov 1997Mironov , 2004Mironov and Pérez 2002). In the present paper, we follow the assignation of setal nomenclature originally used by Faccini et al. (1976). XOLALGIDAE Dubinin, 1953INGRASSIINAE Gaud and Atyeo, 1981Protonyssus Trouessart, 1916 The genus is specific to parrots and currently includes only three described species, two of which are known from South America and one from the Philippines (Trouessart 1885(Trouessart , 1916Gaud and Atyeo 1981). Mites of the genus Protonyssus represent large-sized forms of the family Xolalgidae distributed on parrots.

Differential diagnosis
The new species seems to be most closely related to Protonyssus larva (Trouessart, 1885) described from the scarlet macaw Ara macao (Linnaeus, 1758) in Guyana by having lanceolate setae cp in both sexes and median sclerotized ridge in females. Males of P. proctorae sp. n. differ from that species by having the terminal cleft with a narrow median extension originated from its bottom, slit-shaped incision in interlobar membrane, and by the absence of terminal extensions of lobar membrane; females are distinguished by smooth and straight median sclerotized dorsal ridges on dorsal idiosomal shield, indentations on inner margin of setae cp and setiform setae e2. In males of P. larva, the terminal cleft is almost semicircular, the incision in interlobar membrane is absent, while the posterior ends of this membrane form two acute extensions projecting beyond the lobar apices; in females, the median ridge of the hysteronotal shield has seven to eight additional transverse ribs on each side, the margins of setae cp are smooth, and setae e2 are enlarged, sickle-shaped.

Etymology
Species is named in a honour of Dr Heather C. Proctor, University of Alberta, Canada, well-known expert of aquatic and feather mites.
Fainalges Gaud and Berla, 1964 This genus currently includes 13 species known exclusively from New World parrots (Gaud and Berla 1964;Gaud and Atyeo 1981;Mejía-Gonzalez and Pérez 1988;Pérez 1996). In contrast to the previous genus, Fainalges represents small-sized forms of ingrassiine mites living on parrots. This genus demonstrates impressive cases of multiple speciations where several closely related Fainalges species are specialized for inhabiting different locations in the plumage of one host species Pérez 1995Pérez , 1996.

Description
Male (holotype). Idiosoma length excluding terminal membrane extensions 263, greatest width 195. Prodorsal shield: greatest length 69, width at posterior margin 53, posterior margin with weakly expressed median extension, setae se on most posterior margin of the shield, separated by 42. Hysteronotal shield completely fused with scapular shields, anterior margin weakly convex, greatest length of the shield (from anterior end to level of setae h3) 174, surface with a pair of longitudinally striated patches mesal to setae cp ( Figure 9A). Setae c2 slightly anterior to margin of hysteronotal shield. Terminal cleft ovate, length (from anterior end to bases of h3) 26, greatest width (distance between ps1) 40. Median longitudinal sclerotization originating from the anterior end of terminal cleft long, extending to level of setae e2. Interlobar membrane well-developed, incision in the membrane triangular, 38 in length, terminal extensions short and rounded. Setae d2 extending to apices of opisthosomal lobes. Distances between dorsal hysteronotal setal rows: c2-d2 41, d2-e2 62, e2-h3 66. Sternum long and narrow, remnants of epimerites IIa present. Coxal fields IV closed. Genital arch 2167, epiandrium and shortened genital apodemes fused into semicircular arch, 19 long, 22 wide, genital shield rectangular, adanal shield bow-shaped, bearing setae ps3 ( Figure 9B). Setae 3a and 3b situated at the same transverse level, setae 3b extending to lobar apices. Distance between ventral setal rows: 3a-g 28, g-ps3 31. Tarsus I with all ventral setae setiform ( Figure 10A), solenidion s1 of femorogenu I 42. Tarsus II with seta s lanceolate at base, with seta wa sickle-shaped ( Figure 10B); femorogenu II with seta mG twice as long as vF. Legs III extending beyond lobar apices by tarsus and distal half of tibia; measurements of segments: femorogenu 56, tibia 83, tarsus 96. Tarsus III with setae w about half and setae f about three-quarters of the tarsus ( Figure 10C); setae kT of tibia III long, extending to mid-level of tarsus III. Tarsus IV curved, with bidentate apical extension ( Figure 10D).
Female. Female unknown.

Differential diagnosis
Male of the new species is most similar to Fainalges apicosetiger Mejía-Gonzalez and Pérez, 1988 described from Aratinga canicularis clarae Moore, 1937 in Mexico by having spine-shaped setae s of tarsi II, very thin and long tarsus III, and by similar form of prodorsal shield (Figure 9). The male of Fainalges gracilitarsus sp. n. is distinguished from this species by having longer dorsal setae d2 and coxal setae 3b, both extending to lobar apices, and setae w of tarsus III reaching about half length of the tarsus. In F. apicosetiger, sete d2 and 3b do not extend to bases of opisthosomal lobes, and seta w are only about one-third of tarsus III.