A Review of the Feather Mite Genus Lopharalichus Gaud & Atyeo, 1996 (Acariformes: Pterolichidae), with Descriptions of Three New Species from Brazilian Parrots (Psittaciformes: Psittacidae) ^†

Simple Summary

Understanding the current biodiversity of our planet is an ongoing challenge, as natural habitats are being destroyed at a faster rate than species are described. This is especially true for South America, which harbors over one-third of the parrot species in the world. A diverse yet poorly studied group of mites associated with birds are feather mites, which currently include about 2500 known species, and estimates range from 10,000 to 20,000 species. Herein, three new species of feather mites of the genus Lopharalichus are described from parrots in Brazil.

Abstract

Feather mites of the genus Lopharalichus Gaud & Atyeo, 1996 (Pterolichidae: Pterolichinae), formerly containing three described species, are associated with New World parrots (Psittaciformes: Psittacidae) of the subfamily Arinae. Three new species of this genus are described: Lopharalichus tuim sp. nov. from Forpus xanthopterygius (Spix, 1824), L. spinosus sp. nov. from Ara ararauna (Linnaeus, 1758), and L. chiriri sp. nov. from Brotogeris chiriri (Vieillot, 1818). Type specimens of the previously described Lopharalichus species were examined, and a key to the known species is provided.

1. Introduction

Three groups of feather mite genera from the subfamily Pterolichinae (Acariformes: Pterolichidae) are found on parrots (Psittaciformes): Protolichus, Psittophagus, and Rhytidelasma groups [1,2,3]. The Protolichus generic group, incorporating nearly 100 described species in 24 genera, is the most diverse of these groups, with 11 genera found on parrots of the New World [4]. The genus Lopharalichus Gaud & Atyeo, 1996 belongs to this group and has included, to date, three species [5,6]: Lopharalichus denticulatus (Mégnin & Trouessart, 1884) from Pyrrhura cruentata (Wied-Neuwied, 1820) from Brazil, L. cribiformis (Mégnin & Trouessart, 1884) from Forpus passerinus (Linnaeus, 1758) from Guyana, and L. beckeri Mironov, Dabert & Ehrnsberger, 2005 from Conuropsis carolinensis (Linnaeus, 1758), an extinct parrot of North America. Gaud & Atyeo [5] presented illustrations of two undescribed species from two other New World parrots, Thectocercus acuticaudatus (Vieillot, 1818) (formerly Aratinga acuticaudata) and Forpus modestus sclateri (Gray, 1859) (formerly Forpus sclateri). An undetermined Lopharalichus species was reported from Brotogeris chiriri (Vieillot, 1818) [7] (not confirmed whether it corresponds to the new species described herein form the same parrot species). Pedroso and Hernandes [8] reported three undescribed species of Lopharalichus from Brazil, and these mites are described below.

The most distinctive feature of the genus Lopharalichus is the presence of prominent spiny crests on the femora and genua of legs I and II of both males and females, after which the genus was named (Gr. lophos = crest, mane). Other noticeable features are as follows: in both sexes, the lateral regions of hysterosoma have small cuticular spines, setae c2 are bifid, scapular setae si are subequal to or longer than setae se, setae se are very short (at maximum ½ the distance si:se), the prodorsal shield is entire (unlike species of the genera Aralichus Gaud 1966, Chelomatolichus Gaud & Atyeo 1996, and Pararalichus Atyeo 1989, in which the shield is divided by a transverse band of weakly sclerotized area at level of scapular setae si, se), and setae h1 are absent. Additionally, in males, setae h2 and h3 are flatly expanded with a filamentous tip, setae e2 are bifid with a short basal spine (except in L. denticulatus), setae f2 are expanded (leaf-like), setae ps1 are broad, and in females, setae e2 and ps1 are short, expanded with minute spines.

In this paper, three new species of Lopharalichus are described from parrots of Brazil, and a key to the known species of this genus is presented.

2. Materials and Methods

The new mites studied herein were collected from either wild bird specimens found dead in the field or from taxidermied bird specimens (see below). In the former case, the birds were collected and frozen for a later study; in laboratory, they were washed in a plastic tray with water and detergent to remove the ectoparasites [9], and the water was filtered through a paper filter. The mites were collected from the filters with a fine brush under a dissecting microscope. A few specimens from Ara ararauna (Linnaeus) were also retrieved from dry museum skins deposited at the Museu de História Natural Capão da Imbuia (MHNCI), Curitiba, following the ruffling technique described in Gaud & Atyeo [5]. The mites obtained with both methods were cleared and distended in 30% lactic acid at 50 °C for 24 h, mounted on microscopic slides using Hoyer’s medium [10], and heated and dried at 50 °C for 5 days. Finally, the edges of the coverslips were sealed with transparent varnish and the slides were labeled. The specimens were studied under an Olympus CX31 microscope, and illustrations were prepared from pictures of the mites taken with a digital camera (Omax A35140U 14mpx, Chengdu, China) attached to the ocular lenses and produced on Adobe Illustrator CS5 using a Wacom Bamboo Create tablet. The chaetotaxies of idiosoma and legs follow Griffiths et al. [11] and Atyeo & Gaud [12], respectively, with further corrections for coxal setae [13]. The nomenclature of birds is according to Gill et al. [14].

The species descriptions are given according to the formats proposed by Mironov et al. [6] and Hernandes [4]. Type specimens of the new species are deposited at the Acari Collection of the Department of Ecology and Zoology of the Universidade Federal de Santa Catarina, Florianópolis (ECZ–UFSC). Additional material examined consisted of types and other specimens of Lopharalichus cribriformis and L. denticulatus determined by W.T. Atyeo and are deposited at the Trouessart collection of the Muséum National d’Histoire Naturelle (MNHN), Paris, France. Photos of non-type specimens of L. beckeri deposited at the Zoology Institute, Russian Academy of Sciences (ZISP), St. Petersburg, were also examined.

3. Results

Systematics

Pterolichidae Trouessart & Mégnin, 1884

Lopharalichus Gaud & Atyeo, 1996

(Lopholichus, Gaud & Atyeo 1996:121, sic)

Type species: Pterolichus (Pterolichus) denticulatus Mégnin & Trouessart, 1884, by original designation.

Lopharalichus denticulatus (Mégnin & Trouessart, 1884)

(Figure 1A, Figure 2A, Figure 3A and Figure 4)

Pterolichus (Pterolichus) denticulatus Mégnin & Trouessart, 1884 [15]: 211.

Pterolichus (Eupterolichus) denticulatus; Canestrini & Kramer, 1899 [16]: 37.

Pterolichus denticulatus; Radford, 1953 [17]: 201; Gaud & Atyeo, 1996 [5]: 128.

Type material examined: Lectotype male ex Pyrrhura cruentata (Wied-Neuwied, 1820) (Psittaciformes: Psittacidae) from BRAZIL, no further data, MNHN#969.236.3 (slide 35-I-6) (the remounted slide also contains a paralectotype male of Neorhytidelasma tritiventris (Trouessart, 1884)).

Additional material examined: One male ex P. cruentata, BRAZIL, Bahia state, Boa Nova, 5 June 1928, E. Kaempfer (AMNH241747, UGA10,450), MNHN#1060.31.2 (slide 65-D-6) (W.T. Atyeo det. 1993); one female ex P. cruentata, BRAZIL, Espírito Santo state, Lagoa Juparanã, 11 November 1929, E. Kaempfer (AMNH317283, UGA10,452), MNHN#1060.31.1 (slide 65-D-5) (W.T. Atyeo det. 1993).

Remarks: Lopharalichus denticulatus stands out from other species in having, in males, setae ps1 roughly triangular, setae e2 simple and not bifurcate basally; in females, the prodorsal setal pair si is well spaced by about three-times the distance si:se (Figure 3A); in both sexes, vertical setae vi are slightly expanded (Figure 2A and Figure 3A), genua I, II have prominent, thick antiaxial crests, and the hysteronotal shield is usually devoid of lacunae; in one non-type male examined, there are a few small, sparse circular lacunae in the center of the shield, about 1–3 μm in diameter. The only examined female is broken, with legs, epigynum, and other structures displaced from their original position.

Lopharalichus cribriformis (Mégnin & Trouessart, 1884)

(Figure 1B, Figure 2B, Figure 3B and Figure 5A–F)

Pterolichus (Pterolichus) denticulatus var. cribriformis Mégnin & Trouessart, 1884 [15]: 213.

Pterolichus (Eupterolichus) cribriformis; Canestrini & Kramer, 1899 [16]: 38.

Pterolichus denticulatus; Radford, 1953 [17]: 201.

Type material examined: Syntypes 15 males and 19 females (in the same original slide, not remounted) ex Forpus passerinus (Linnaeus, 1758) (=Psittaculus passerinus), from GUYANA, MNHN#969.237.1 (slide 35-I-8).

Additional material examined: one male and one female ex Forpus passerinus cyanochlorus (Schlegel, 1864), BRAZIL, Amazonas state, Frechal, Rio Surumu, 6 September 1929, T.D. Carter col. (AMNH236355, UGA12,742) MNHN#1060.30 (slide 65-D-4) (W.T. Atyeo det. 1993).

Remarks: Lopharalichus cribriformis is very similar to L. beckeri Mironov et al. (2005), differing from that species in having, in males, the terminal cleft angular and the paragenital apodemes indistinctly developed, and in females, setae si distinctly longer and more robust than se (at least twice longer and twice thicker) (Figure 3B), and the solenidion on tibia IV as long as half the width of this segment (Figure 5F). In males of L. beckeri, the lobar cleft is nearly semicircular (Figure 1C), and the paragenital apodemes are distinctly formed; and in females, setae se and si are both piliform and similar in structure (Figure 3C), and solenidion φ on tibia IV is about the same length as the width of tibia (Figure 5G).

Mironov et al. [6] stated that, in males of L. cribriformis, setae e2 are twice as long as f2, and in females, setae f2 are “large and foliform, almost circular, and with a vein”. However, in the examined specimens of this species, setae e2 and f2 have about the same length in males, and setae f2 of females are roughly triangular, like in L. beckeri. The type series of L. cribriformis consists of a single slide containing 34 poorly clarified syntypes, still with the original label by E.L. Trouessart. The illustrations presented here are based on non-type material collected from the type host species and determined by W.T. Atyeo.

Lopharalichus beckeri Mironov, Dabert & Ehrnsberger, 2005

Figure 1C, Figure 2C, Figure 3C and Figure 5G)

Lopharalichus beckeri Mironov, Dabert & Ehrnsberger, 2005 [5]: 2259

Material examined: Photos of 1 male and 1 female (ZISP 6760, 6767) ex Conuropsis carolinensis (MCZ 209911, UNAM 110), USA, Florida, Tampa, no date, coll. W. Brewster.

Remarks: Lopharalichus beckeri was described from Conuropsis carolinensis (Linnaeus, 1758), an extinct parrot from North America. This species is very similar to L. cribriformis (see differential characters in the remarks of the previous species).

Lopharalichus tuim sp. nov.

(Figure 1D, Figure 2D, Figure 3D and Figure 6, Figure 7 and Figure 8)

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Type material. Holotype male, paratypes 10 males, 31 females, and 1 nymph ex Forpus xanthopterygius (Spix, 1824) (Psittaciformes: Psittacidae), BRAZIL, São Paulo State, Pedreira, 22°44′ S, 46°54′ W, June 2012, D.V. Boas-Filho col. (#1074).

Male (holotype, range for five paratypes in parentheses). Idiosoma length (from the level of setae vi to the base of setae h3) 284 (284–297), greatest width at level of humeral shields 162 (163–176). Prodorsal shield shaped as an Erlenmeyer flask (elongated trapezoid), with rounded edges, posterior margin slightly sinuous, surface without ornamentation, 64 (64–72) in length from the level of setae vi to the posterior margin, 69 (69–78) in width at the widest part. Scapular setae si thin spiculiform, 9 (8–11) long, setae se piliform, reduced, distance between bases of scapular setae si:si 29 (25–27), se:se 57 (56–61). Hysterosoma 212 (211–226) in length from sejugal area to the bases of setae h3. Hysteronotal shield: anterior margin straight, length from anterior margin to bases of setae h3 207 (212–227), greatest width at the level of setae d2 138 (144–158), surface with numerous circular lacunae posterior to level of setae c1 (Figure 6A), supranal concavity poorly distinct, anterior to level of setae e1. A bow-shaped transverse fold between levels of setae e1 and ps1. Membranous margin of terminal cleft (=contour of free margin of interlobar membrane) blunt-angular, 28 (30–34) long, opisthosomal lobes with prominent tubercles at bases of setae h3, narrow interlobar membrane between bases of setae ps1. Setae c2 bifid, 12 (12–15) long; setae e2 lanceolate with short basal bifurcation, 45 (42–49) long; setae f2 lanceolate with outer edge minutely serrate, 54 (56–65); setae ps1 roughly parallelogram-shaped, 78 (77–84) long. Distances between hysteronotal setae: c2:d2 72 (84–90), d2:e2 84 (76–82), e2:h3 40 (45–50), d1:d2 10 (8–13), e1:e2 4 (5–13), ps1:ps1 45 (43–51), h3:h3 69 (66–76), h2:h2 82 (82–92), and ps2:ps2 106 (106–117).

Bases of epimerites I and II with inflations and dark sclerotized (Figure 6B). Humeral shields developed ventrally and bearing setae c3, cp. Setae c3 thin piliform, 14 (12–16) long; coxal fields I–II without sclerotized areas. Genital apparatus situated between levels of trochanters III and IV, 24 (24–28) long, 11 (10–13) wide; paragenital apodemes as a pair of longitudinal sclerites lateral to the genital apparatus and bearing the genital acetabula. Distances between setae: g:4a 55 (51–58), g:g 8 (6–9). Cupules ih ventrally at the level of setae ps2. Adanal suckers 13 (13–15) in diameter, distance between centers of suckers 24 (22–26), corolla with 5–7 teeth on anterior half, posterior half without teeth (Figure 1D and Figure 6B).

Femora I with 1–3 apicoventral spines or crests, femur II with 2–6 apicoventral spines. Acute apicoventral spines on genua, tibiae I, II. Length of tarsi excluding ambulacra: tarsus I 37 (35–38), tarsus II 44 (46–50), tarsus III 49 (49–54), tarsus IV 55 (55–57). Seta kT present on tibia IV. Setae d, e minute spiculiform, inserted close together (Figure 8D). Setae p, q on tarsi I thinner and apically less expanded than on tarsi of other legs. Solenidion σ2 of genu I apparently absent. Length of solenidia: σ2I 10 (9–12), σIII 9 (7–9), φI 50 (50–55), φII 45 (43–47), φIII 33 (30–33), φIV 40 (35–43), ω1I 10 (10–12), ω3I 29 (29–32), and ω1II 19 (17–18).

Female (range for 6 paratypes). Idiosoma length 309–334, greatest width 173–185. Prodorsal shield-shaped as in the male, 73–79 long, 76–79 wide (Figure 7A); scapular setae si spiculiform, 14–17 long, setae se piliform, reduced; distances between scapular setae si:si 21–28, se:se 59–63. Hysteronotal shield 239–247 in length, 162–171 in width at the widest part; surface with numerous circular lacunae posterior to level of setae c1. Setae c2 bifid, setae f2, ps1 flat, spiky leaf-like, setae c1, d1, d2, e1, e2 piliform. Terminal region of opisthosoma shaped as a semicircular concavity between a pair of tubercles bearing setae h2, h3, and with a small external copulatory tube in the center about 5–7 long located between setae ps1. Posterolateral margins of opisthosoma with small spines. Length of setae: c2 12–15, c3 16–31, e2 11–16, and f2 16–22. Distances between dorsal setae: c2:d2 95–101, d2:e2 89–93, d1:d2 11–20, e1:e2 40–46, ps1:ps1 17–21, h3:h3 37–40, h2:h2 52–56.

Epimerites I free. Bases of epimerites I, II inflated, dark-sclerotized (Figure 7B). Epigynum as a low arch, 9–13 in length, 24–35 in width. Distance between ventral setae 1a:3a 36–42, 3a:g 20–30. Legs I, II as in the male, except for a shorter apicoventral spine on genu and tibia I. Length of tarsi excluding ambulacra: tarsus I 35–42, tarsus II 44–50, tarsus III 53–56, tarsus IV 59–65. Length of solenidia: σ2I 10–13, σIII 9–10, φI 61–62, φII 50–55, φIII 35–38, φIV 12–16, ω1I 11–13, ω3I 30–34, and ω1II 18–25.

Differential diagnosis: The new species, L. tuim sp. nov., is very close to L. cribriformis (Mégnin & Trouessart, 1884) described from Forpus passerinus in having a blunt-angular terminal cleft in males. In males of L. denticulatus and L. beckeri, the lobar cleft is concave and semi-circular. The new species most clearly differs from L. cribriformis in the relative length and arrangement of prodorsal setae si: in females of L. tuim sp. nov., si reaches the base of se of the same side (Figure 3D), and in males, si reaches at least halfway to the base of corresponding setae se, si being about twice longer than se (Figure 2D). Also, in males of the new species, setae si are inserted slightly closer to the corresponding se than to the other member of the pair si (distance si:si is about 1 ½ the distance si:se). In L. cribriformis females, setae si only reach about halfway to the bases of corresponding se (Figure 3B), and in males of that species, these setae reach one-third of that distance (si is about the same length as se) (Figure 2B), and in both sexes, the scapular setae si and se are uniformly spaced (distance si:se = si:si).

Etymology: The name of the new species is based on the Brazilian common name of the host (tuim) and is a noun in apposition.

Lopharalichus spinosus sp. nov.

(Figure 1E, Figure 2E, Figure 3E and Figure 9, Figure 10 and Figure 11)

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Type material: holotype male, seven male and six female paratypes ex Ara ararauna (Linnaeus, 1758) (Psittaciformes: Psittacidae), BRAZIL, São Paulo State, Itatiba, 23°00′ S, 46°50′ W, 24 March 2007, U. Kawazoe col. (#152). Paratypes from the same host species: five males and four females, Pernambuco State, 29 September 1953 (MHNCI#1557), mites collected from the bird skin by FAH in November 2016.

Male (holotype, range for two paratypes in parentheses). Idiosoma length from the level of setae vi to the base of setae h3 345 (338–350), greatest width at level of humeral shields 190 (190–193). Prodorsal shield shaped roughly as an isosceles trapezoid, with sinuous lateral margins and rounded edges, 78 (76–78) in length from the level of setae vi to the posterior margin, 96 (93–96) in width at the posterior margin. Scapular setae si as a short spike, about as long as the distance between their bases, 13 (11–13) long, distance between scapular setae si:si 25 (24–25), se:se 75 (73–77). Hysterosomal region 263 (256–265) in length from sejugal area to the bases of setae h3. Hysteronotal shield: anterior margin straight, length from anterior margin to bases of setae h3 260 (254–256), greatest width around the level of setae d2 165 (167–176), surface with numerous circular lacunae from the level of setae c1 to genua IV (Figure 9A). A bow-shaped transverse fold between levels of setae e1 and ps1. Membranous margin of terminal cleft blunt-angular, 30 (30–30) long, opisthosomal lobes with prominent tubercles at bases of setae h3, narrow interlobar membrane between bases of setae ps1. Setae c2 bifid, 21 (17–21) long; setae e2 lanceolate with short basal bifurcation, greatest length 43 (40–43); setae f2 lanceolate with external margin minutely serrate, 66 (64–66); setae ps1 roughly parallelogram-shaped with sharp posterior edges, 89 (88–90) long. Distances between hysteronotal setae: c2:d2 111 (106–111), d2:e2 101 (95–98), e2:h3 52 (50–52), d1:d2 11 (13–14), e1:e2 11 (9–11), ps1:ps1 49 (45–52), h3:h3 78 (75–78), h2:h2 96 (92–96), and ps2:ps2 126 (116–126).

Bases of epimerites I, II inflated, dark-sclerotized (Figure 9B). Humeral shields bearing setae c3, cp ventrally. Setae c3 thin piliform, 19 (17–19) long, coxal fields I, II without sclerotized areas. Genital apparatus situated between levels of trochanters III, IV, 30 (27–30) long, 12 (12–14) wide; paragenital apodemes as a pair of longitudinal sclerites roughly parallel to the arms of genital arch and bearing genital acetabula. Distances between setae: g:4a 66 (61–67), g:g 9 (7–9). Cupules ih ventrally at the level of setae ps2. Adanal suckers 15 (14–17) in diameter, distance between centers of suckers 27 (25–27), corolla with 5–7 teeth on anterior half, posterior half without teeth.

Femora I, II with 3–5 apicoventral spines or crests. Acute apicoventral spines on genua, tibiae I, II. Length of tarsi excluding ambulacra: tarsus I 44 (40–42), tarsus II 55 (53–55), tarsus III 57 (58–60), tarsus IV 67 (62–65). Seta kT present on tibia IV. Setae d, e minute spiculiform inserted together (Figure 11D). Genual solenidion σ1 on genu I present, minute, about 5 in length. Length of solenidia: σ2I 10 (10–11), σIII 10 (8–10), φI 49 (46–50), φII 43 (42–44), φIII 47 (39–42), φIV 45 (37–42), ω1I 11 (10–11), ω3I 30 (26–30), and ω1II 20 (17–20).

Female (range for six paratypes). Idiosoma length 367–399, greatest width 197–212. Prodorsal shield shaped as in the male, 82–90 long, 94–106 wide (Figure 10A); scapular setae si spiculiform, 17–20 long, setae se piliform; distances between scapular setae si:si 29–39, se:se 78–88. Hysteronotal shield 278–307 in length, 179–190 in width at the widest part at the level of setae d1; surface with numerous circular lacunae from the level between setae c1 to e2. Lateral hysterosomal setae c2 bifid, c1, d1, d2, e1, e2 thin piliform, setae f2, ps1 flat, spiky leaf-like. Terminal region of opisthosoma shaped as a semicircular concavity flanked by a pair of tubercles bearing setae h2 and h3. Posterolateral margins of opisthosoma with small spines. Terminal margin of opisthosoma between setae ps1 with small copulatory extension about 5–7 long. Length of setae: c2 14–20, e2 10–14, c3 20–29, and f2 23–32. Distances between dorsal setae: c2:d2 113–124, d2:e2 110–121, d1:d2 7–13, e1:e2 39–48, ps1:ps1 21–26, h3:h3 42–49, and h2:h2 59–65.

Epimerites I free, bases of epimerites I, II inflated, dark-sclerotized (Figure 10B). Epigynum as a low arch, 12–18 in length, 34–46 in width. Distance between ventral setae 1a:3a 46–55, 3a:g 14–24. Legs I, II as in the male. Length of tarsi excluding ambulacra: tarsus I 39–47, tarsus II 56–61, tarsus III 61–66, tarsus IV 70–76. Solenidion σ1I present, minute, about 5 in length. Length of solenidia: σ2I 10–13, σIII 11–13, φI 56–64, φII 51–60, φIII 41–58, φIV 13–18, ω1I 10–14, ω3I 27–34, ω1II 19–21.

Differential diagnosis: Lopharalichus spinosus sp. nov. is close to L. beckeri and L. cribriformis in having, in males, well-formed cuticular spines in the lateral part of idiosomal anterior to setae e2. In both sexes of L. spinosus, however, those spines are much more numerous and occupy a larger area, from the level of setae cp to that of setae e2; in addition, in males of the new species, scapular setae si are spiculiform, noticeably more robust than se (Figure 2E). In both sexes of L. beckeri and L. cribriformis, the lateral spines are present only from the level of trochanter IV to the level of setae e2. In males of L. cribriformis and L. beckeri, and in females of the latter species, both scapular setae si and se are thin piliform (Figure 2B,C and Figure 3C); in females of L. cribriformis, setae si are more robust than se, but they only reach halfway to the distance between those setae (Figure 3B), whereas in L. spinosus sp. nov. females, si reaches the bases of corresponding setae se (Figure 3E).

Etymology: the specific name is an adjective (masculine) referring to the numerous cuticular spines on the lateral margins of hysterosoma, more pronounced and numerous than in other known species.

Lopharalichus chiriri sp. nov.

(Figure 1F, Figure 2F, Figure 3F and Figure 12, Figure 13 and Figure 14)

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Type material: holotype male, 15 male and 8 female paratypes ex Brotogeris chiriri

(Vieillot, 1818) (Psittaciformes: Psittacidae), BRAZIL, São Paulo State, Pedreira, 22°44′ S, 46°54′ W, October 2013, D.V. Boas Filho col. (#1113); paratypes 4 females and 1 nymph, same host species, Pará State, Santana do Araguaia, Fazenda Fartura, 09°40′ S/50°23′ W, 07 September 2011, D.V. Boas-Filho coll. (#1006).

Male (holotype, range for six paratypes in parentheses). Idiosoma length from the level of setae vi to the base of setae h3 285 (294–308), greatest width at level of humeral shields 160 (160–167). Prodorsal shield roughly as an isosceles trapezoid with rounded posterior corners, 76 (67–74) in length from the level of setae vi to the posterior margin, 74 (76–79) in width at the widest part. Scapular setae si piliform, 7 (6–7) long, distance between si:si 23 (23–26), se:se 59 (57–62), si:se 17 (17–19). Hysterosomal region 224 (213–219) in length from sejugal area to the bases of setae h3. Hysteronotal shield: anterior margin straight, length from anterior margin to bases of setae h3 207 (213–219), greatest width around the level of setae d2 150 (140–155), surface with sparse circular lacunae from the level of setae c1 to genua IV (Figure 12A). A bow-shaped transverse fold between levels of setae e1 and ps1. Membranous margins of terminal cleft blunt-angular, 30 (28–31) long, opisthosomal lobes with prominent tubercles at bases of setae h3, and narrow interlobar membranes between bases of setae ps1. Setae c2 bifid, 12 (11–15) long; setae e2 lanceolate with short basal bifurcation, greatest length 35 (35–44); setae f2 lanceolate with outer margin minutely serrate, 54 (59–68); setae ps1 roughly parallelogram-shaped, 73 (73–82) long. Distances between hysteronotal setae: c2:d2 95 (94–100), d2:e2 81 (71–81), e2:h3 42 (41–50), d1:d2 16 (9–16), e1:e2 9 (8–14), ps1:ps1 42 (42–47), h3:h3 66 (67–72), h2:h2 82 (85–92), ps2:ps2 106 (107–115).

Bases of epimerites I, II inflated, dark-sclerotized (Figure 12B). Humeral shields bearing setae c3, cp ventrally. Setae c3 thin piliform, 17 (12–15) long, coxal fields I–II without sclerotized areas. Genital apparatus situated between levels of trochanters III and IV, 13 (10–13) long, 11 (10–11) wide; paragenital apodemes as a pair of thin longitudinal sclerites roughly parallel to the arms of genital arch and bearing genital acetabula. Distances between setae: g:4a 51 (47–53), g:g 9 (7–13). Cupules ih ventrally at the level of setae ps2. Adanal suckers 13 (13–15) in diameter, distance between centers of suckers 24 (22–27), corolla with 5–7 teeth on anterior half, posterior half without teeth.

Femora I, II with 1–4 apical spines on. Acute apicoventral spines on genua, tibiae I, II (slightly more developed on legs II than in legs I). Length of tarsi excluding ambulacra: tarsus I 33 (31–36), tarsus II 43 (40–45), tarsus III 46 (42–49), tarsus IV 48 (48–50). Seta kT present on tibia IV. Setae d, e minute spiculiform inserted close together. Solenidion σ2 of genu I apparently absent. Length of solenidia: σ2I 7 (7–9), σIII 9 (7–10), φI 50 (48–55), φII 43 (39–48), φIII 41 (34–45), φIV 40 (33–40), ω1I 12 (10–11), ω3I 26 (25–28), ω1II 19 (18–20).

Female (range for six paratypes). Idiosoma length 296–338, greatest width 171–189. Prodorsal shield shaped as an Erlenmeyer flask (elongated trapezoid), 68–80 long, 74–83 wide (Figure 13A); scapular setae si short spiculiform, 9–11 long, setae se piliform; distances between scapular setae si:si 21–28, se:se 59–65, si:se 16:21. Hysteronotal shield 233–254 in length, 163–174 in width at the widest part around level of setae d1; surface with numerous circular lacunae from the level between setae c1 to supranal concavity. Lateral hysterosomal setae c2 bifid, c1, d1, d2, e1, e2 thin piliform, setae f2, ps1 flat, spiky leaf-like. Terminal region of opisthosoma shaped as a semicircular concavity flanked by a pair of tubercles bearing setae h2, h3, and a small external copulatory tube around 5–7 in length between bases of setae ps1. Lateral margins of opisthosoma with few small spines. Length of setae: c2 9–13, e2 8–12, c3 14–17, f2 22–25. Distances between dorsal setae: c2:d2 99–112, d2:e2 85–101, d1:d2 10–20, e1:e2 31–46, ps1:ps1 16–20, h3:h3 35–41, h2:h2 53–57.

Epimerites I free, bases of epimerites I, II inflated, dark-sclerotized (Figure 13B). Epigynum as a low arch, 9–12 in length, 27–29 in width. Distance between ventral setae 1a:3a 37–54, 3a:g 17–21. Length of tarsi excluding ambulacra: tarsus I 30–37, tarsus II 40–46, tarsus III 42–48, tarsus IV 51–58. Length of solenidia: σ2I 8–11, σIII 7–11, φI 54–64, φII 48–58, φIII 38–47, φIV 10–14, ω1I 10–13, ω3I 24–29, ω1II 18–24.

Differential diagnosis: Lopharalichus chiriri sp. nov. is very similar to L. cribriformis due to the blunt-angular shape of terminal cleft in males but can be distinguished by the relatively longer distance between prodorsal setae si-si. In males of the new species, this distance is about 3.5-times the length of setae si, against 2.5-times that length in L. cribriformis. Also, the new species has smaller dorsal lacunae and relatively shorter solenidion on tibia IV in males, reaching only about half of the length of tarsus (it reaches at least ¾ of tarsus length in L. cribriformis). The new species is also distinguished from all previously known species in having, in both sexes, considerably longer solenidion on tibia III, roughly longer than the length of genu and tibia III combined. In females of L. chiriri, setae si are relatively shorter, their tips not touching each other (Figure 3F), while in L. cribriformis females, these setae do touch each other. Additionally, in both sexes of L. chiriri, tibial solenidion φIII is equal to the length of genu + tibia III (Figure 14C,H), while in other known species of Lopharalichus, solenidion φIII is shorter than the length of corresponding genu and tibia.

Etymology: the specific name is a noun in apposition referring to the species name of the type host.

Key to species of Lopharalichus Gaud & Atyeo, 1996

1. Both sexes: wide apicoventral spines on genua I, II around base of seta mG, much wider than spines on corresponding tibiae I, II; setae vi dilated; cuticular spines absent; males with setae ps1 roughly triangular with rounded edges (gradually narrowed toward distal end, width of basal part about 4-times wider than distal part); setae e2 not bifid basally……. L. denticulatus (Mégnin & Trouessart, 1884)

1’. Both sexes: spines on genua I, II about as wide as those on tibiae I, II; setae vi not dilated; cuticular spines present on posterolateral margins of opisthosoma; males with setae ps1 parallelogram-shaped (width of base subequal to that of distal end); setae e2 bifid basally ……. 2

2. In both sexes, setae si and se piliform, subequal in length (Figure 2C and Figure 3C) ….. L. beckeri Mironov et al., 2005

2’ In females, setae si always spiculiform; in males, setae si either spiculiform or piliform… 3

3. In both sexes, lateral margins of hysterosoma with pronounced spines from level of setae cp to e2 (Figure 9A and Figure 10A); in males, setae si spiculiform, noticeably more robust than se (Figure 2E) … L. spinosus sp. nov.

3’: In both sexes, spines on the lateral margins of hysterosoma limited to the levels between setae d1 to e2 (in males), and d1 to f2 (in females) …. 4

4. In both sexes, solenidion φIII longer or equal to the length of genu + tibia III (Figure 14C,H); in females, tips setae si not reaching each other …. L. chiriri sp. nov.

4’. In both sexes, solenidion φIII shorter than the length of genu + tibia III; in females, setae si relatively longer, their tips touching each other … 5

5. In both sexes, distance si:si about 1.5 longer than distances between si:se (Figure 2D and Figure 3D); in males, si about twice longer than se; in females, setae si equal to distance si:se ….. L. tuim sp. nov.

5’ In both sexes, distance si:si approximately equal to the distance si:se (Figure 2B and Figure 3B); in males, si and se subequal in length; in females, setae si shorter than the distance between setae si and se ….. L. cribriformis (Mégnin & Trouessart, 1884)

4. Discussion

By the time Gaud & Atyeo [5] established the genus Lopharalichus, they mentioned that it occurred solely on parrots of the subfamily Aratinginae (sensu Wolters [18]). However, they also referred to this genus as having two undescribed species [5] from parrots then considered in the subfamily Forpinae (sensu Wolters): Forpus passerinus and F. sclateri (the latter is currently regarded as a subspecies of Forpus modestus (Cabanis, 1849)). Herein, a new species is described from the genus Brotogeris, previosuly considered in yet another subfamily of Wolters, Brotogerinae. In the current classification of parrots [19], the hosts of Lopharalichus are parrots of the family Psittacidae, subfamily Arinae, tribes Arini, Forpini, and Androglossini—it remains to be discovered whether Lopharalichus is also present on the tribe Amoropsittacini. Those three tribes account for nearly 140 parrot species (~93% of the arine species), and Lopharalichus spp. has been reported from only eight of those hosts so far, including two undescribed species illustrated by Gaud & Atyeo [5].

According to Wright et al. [20], the Arinae—the New World parrots—diverged from the African Psittacinae around the K-T boundary (~66 mya) and diversified approximately 55 mya. Lopharalichus, being found only in New World parrots, probably originating between those dates, and given its seemingly uneven distribution on three out of four arine tribes (see above), it probably independently colonized those hosts horizontally rather than vertically. Recent studies have demonstrated that horizontal transfer is an important means of colonizing new hosts e.g., [21,22]. An alternative but less likely scenario would be Lopharalichus being present on the arine ancestor and having independently become extinct from several hosts of the tribe Arini (e.g., Anodorhynchus Spix, Cyanopsitta Bonaparte, Deroptyus Wagler, Diopsittaca Ridgway, Enicognathus Gray, Leptosittaca Berlepsch & Stolzmann, Pionites Heine, and Pyrrhura Bonaparte) and Androglossini (most genera excepting Brotogeris, see [19]). In a series of papers, W.T. Atyeo and co-workers investigated the pterolichine feather mites from several of those Arini hosts and did not retrieve any mites that would be later classified in the genus Lopharalichus [23,24,25,26,27,28]. Valdebenito et al. [29] examined feather mites from the two species of Enicognathus from Chile (also belonging to the Arini) and did not retrieve Lopharalichus. As for the tribe Androglossini, only one Lopharalichus is known, L. chiriri sp. nov. from Brotogeris chiriri; the latter tribe contains 10 genera and at least 66 species [14]. Since many of those hosts have not been thoroughly investigated for feather mites, it is reasonable to anticipate that other Lopharalichus species may be present in some of those hosts. In the past decade, only a few studies have examined feather mites associated with psittaciform birds in Brazil e.g., [4,30,31,32,33,34]. It is clear, however, that several species remain to be discovered, as nearly 90 parrot species (Psittacidae: Arinae) are found in the country [35].

As in other genera of the Protolichus group, the solenidion σ1 of genu I in Lopharalichus is highly reduced, vestigial, and depending on the position of the specimen on the slide, barely visible. Although the presence of this solenidion was confirmed for some Lopharalichus species (e.g., L. cribriformis, L. beckeri, and L. spinosus sp. nov.), it was not possible to confirm its presence in the remaining species studied.

Despite the presence of cuticular spines in the adults, the two examined immature specimens belonging to the species described herein lack such spines. The retention of small cuticular spines on the posterolateral margins of opisthosoma in most adults of Lopharalichus species (except in L. denticulatus) is not unique to this genus. In other pterolichines belonging to the Protolichus generic group, like Aralichus Gaud, 1966 and Distigmesikya Atyeo, Gaud et Pérez, 1984, the immatures have numerous such spines—in Aralichus, they are mostly located caudally, and in Distigmesikya, they abundantly cover most of the dorsum) [5,25]. As these mites undergo their final moult to adulthood, those spines disappear in most species. In some of them, however, spines are present in adults, like in both sexes of Aralichus glaucogularis Atyeo et Pérez, 1990, and in females of Scolaralichus vazquezae Pérez et Atyeo, 1986, Aralichus menchacai Pérez et Atyeo, 1989, and Tanyaralichus elongatus Pérez et Atyeo, 1989. However, the immatures of the latter two species were not illustrated with cuticular spines [23,24,28].

5. Conclusions

With the description of three new species, Lopharalichus has effectively doubled its known species count, now encompassing six species: L. denticulatus (Mégnin & Trouessart, 1884) (type species), L. cribriformis (Mégnin & Trouessart, 1884), L. beckeri Mironov et al. 2005, L. tuim sp. nov., L. spinosus sp. nov., and L. chiriri sp. nov. However, since most neotropical parrots remain uninvestigated for their feather mites, it is safe to assume that many other Lopharalichus species may exist and will eventually be discovered.