Three Feather Mites (Acari: Sarcoptiformes) Isolated from Black-Tailed Godwit, Limosa limosa in Korea

Abstract

Feather mites comprise two superfamilies(Analgoidea and Pterolichoidea) and are highly specialized ectosymbionts of birds. To date, this group contains more than 2,500 species worldwide. Fifty-five feather mite species have been reported in Korea, and only one species of genus Alloptes has been recorded from black-tailed godwit Limosa limosa. Three new records of feather mites from the L. limosa in Korea are added in this study: Avenzoaria punctata Gaud, 1972, Bregetovia limosae (Buchholz, 1869), and Montchadskiana buchholzi (Canestrini, 1878). The genus Bregetovia Dubinin, 1951 is also new report for this country. In this paper, we provide the morphological descriptions and illustrations based on the present specimens. Additionally, we determined partial sequences of the mitochondrial cytochrome c oxidase subunit I(COI) from three feather mites as DNA barcodes.

INTRODUCTION

Feather mites comprise two superfamilies (Acari: Sarcoptiformes: Analgoidea and Pterolichoidea) and are highly specialized ectosymbionts of birds (Mironov, 2003; Proctor, 2003; Oconnor, 2009). To date, this group contains more than 2,500 species worldwide (Mironov, 2003; Stefan et al., 2014). In Korea, 55 species have been reported (Tibbetts, 1955; Santana, 1976; Pérez and Atyeo, 1992; Han and Min, 2019a, 2019b, 2019c).

The family Avenzoariidae Oudemans, 1905 consists of two subfamilies(Avenzoariinae Oudemans, 1905 and Bonnetellinae Atyeo and Gaud, 1981), and is associated with a variety of aquatic birds(Gaud and Atyeo, 1996; Dabert et al., 2001; Oconnor, 2009; Stefan et al., 2014). The genera Avenzoaria Oudemans, 1905 and Bregetovia Dubinin, 1951 belong to the Avenzoariinae subfamily and contain 16 (including A. grallatoris and A. limicolae) and 6 species, respectively (Mironov et al., 1993; Badek and Dabert, 2005).

The family Pterolichidae Trouessart and Mégnin, 1884 contains over 400 species in approximately 120 genera and are found on diverse birds with the exception of those in the order Passeriformes(Gaud and Atyeo, 1996; Mironov and Dabert, 2010). The genus Montchadskiana belongs to the Pterolichidae family and contanis 17 species (Gaud and Atyeo, 1996; Dabert and Ehrnsberger, 1999).

The black-tailed godwit Limosa limosa (Linnaeus, 1758) breeds in grasslands with peat, clay, and sandy soil. These places can be found in blanket bogs and wet moorlands in central Eurasia (Gill et al., 2007). This species migrates to Africa, Southern Europe, India, Southeast Asia, and Australia and is known as a passage migrant bird in Korea (Lee et al., 2014; Park, 2014). Thus far, approximately 13 species of feather mites have been identified from black-tailed godwits worldwide (Bedford, 1936; Dubinin, 1951, 1956; Gaud, 1958, 1972, 1973; Zumpt, 1961; Gaud and Mouchet, 1963; Vasyukova and Mironov, 1991; Dabert and Ehrnsberger, 1999; Dabert, 2003). In Korea, only one species of the genus Alloptes has been recorded (Han and Min, 2019a).

Here, we recovered A. punctata, B. limosae, and M. buchholzi from the black-tailed godwit, and provide descriptions and illustrations of these three feather mites based on morphology. Additionally, we provide the partial sequences of the mitochondrial cytochrome c oxidase subunit I(COI) as DNA barcodes.

MATERIALS AND METHODS

Two black-tailed godwits (CNWARC no. CN17-265 and CN12-402) were initially rescued from Asan and Seosan-si by the Chungnam Wild Animal Rescue Center (CNWARC) but later died and were stored in a -20°C freezer at this center. Mite samples were collected from flight feathers of wings using a vacuum machine. The collected mites were preserved directly in 95% ethyl alcohol. The mite specimens were cleared by lactic acid for 24 h and then mounted on micro slides using PVA mounting medium(Downs, 1943). The specimens were photographed using a microscopic digital camera (Leica, Wetzlar, Germany). The terms and measurements follow Gaud and Atyeo (1996) and Norton (1998). All examined specimens were deposited in the National Institute of Biological Resources(NIBR) and Inha University, Korea.

DNA sequencing

DNA was extracted from a leg of each specimen using a Tissue DNA Purification Kit (Cosmogenetech Inc., Seoul, Korea), according to the manufacturer’s instructions. Partial sequences of the mitochondrial COI gene were amplified with two primers: bcdF05 5ʹ-TTTTCTACHAAYCATAAAGATA TTGC-3ʹ and bcdR04 5ʹ-TATAAACYTCDGGATGNCCAA AAAA-3ʹ (Dabert et al., 2008). PCR condition, purification and sequencing were performed according to the methods described by Han et al.(2016).

SYSTEMATIC ACCOUNTS

Order Sarcoptiformes Canestrini, 1891

Family Avenzoariidae Oudemans, 1905

Genus Avenzoaria Oudemans, 1905

Avenzoaria punctata Gaud, 1972 (Figs. 1, 2)

Avenzoaria punctata: Gaud, 1972: 37-42, figs. 16-17, 19; Vasyukova and Mironov, 1991: 23, 30, fig. 4.

Fig. 1. Avenzoaria punctata, male. A, Dorsal view; B, Ventral view. gp, genital papillae. Scale bars: A, B=0.1 mm.

Fig. 2. Avenzoaria punctata, female. A, Dorsal view; B, Ventral view. eg, epigynum, gp, genital papillae. Scale bars: A, B=0.1 mm.

Material examined. 1♂, 1♀, Korea, Chungcheongnam-do, Asan-si, Tangjeong-myeon, 36°48ʹ58ʺN, 126°2ʹ45ʺE, 18 May 2017, collected using vacuum machine from flight feathers on the wings of black-tailed godwit L. limosa by Han YD

Description. Male: Length 415 μm of idiosoma from anterior end to bases of setae h3, width 170 μm at level of humeral shields (Fig. 1A). Prodorsal shield (Fig. 1A): posterior margin with medial convex, posterior angles acute, with small round lacunae, length 98 μm along midline, width 75 μm at posterior part. Hysteronotal shield (Fig. 1A): Anterior part straight, with irregularly round lacunae, length 350 μm from anterior margin to bases of setae h3, width 113 μm at level of setae d1. Interlobar cleft transversal oval-shaped, with anterior part concave. Interlobar membrane expanded at the distal edges of the lobes. Incision in interlobar membrane elongated oval. Postlobar membranes with one rounded and four acute teeth. Sternum (Fig. 1B): epimerites I not fused. Genital apparatus l situated between levels of trochanters III and IV. Genital papillae located anterior to base of genital apparatus(Fig. 1B).

Female: Idiosoma size 420×180 μm (length×width)(Fig. 2A). Prodorsal shield (Fig. 2A): Mostly shaped as in male, length along middle line 92 μm, width 82 μm at posterior part. Hysteronotal shield (Fig. 2A): Shaped as in male, posterior part with stronger sclerotization, length 310 μm, width 125 μm. Opisthosoma terminus round-shape. Terminal cleft small semicircular. Sternum (Fig. 2B): epimerites I shaped as in male. Epigynum horseshoe-shaped, with each side by slightly concavity at level of setae 4b, length 53 μm, width 73 μm at posterior margins. ends of epigynum extending to level of genital papillae.

Remarks. Avenzoaria punctata was originally described by Gaud (1972) based on specimens collected from L. limosa in Morocco. Thereafter, this species was reported by Vasyukova and Mironov (1991) from Limosa lappoinca in the Sakha Republic (=Yakutia Republic) of Russia.

Avenzoaria punctata has very similar external traits to A. arenarii Dubinin, 1951 and A. tringae (Oudemans, 1904). However, A. punctata can be clearly distinguished from A. arenarii and A. tringae by the following characteristics: hysteronotal shield has small round ornamentation; in male, postlobar membranes consist of single-rounded and four pointed teeth; in female, posterior ends of epigynum are extend to level of genital papillae (Gaud, 1972; Vasyukova and Mironov, 1991). The Korean specimens were morphologically consistent with the original descriptions and illustrations provided by Gaud (1972).

Host. This species was found on wings feathers of the blacktailed godwit L. limosa.

Distribution. Morocco (Gaud, 1972), Russia (Vasyukova and Mironov, 1991), Korea (this study).

Deposition. NIBR No. NIBRIV0000835097-0000835098.

Molecular characteristics. The COI sequences were obtained from single individual and deposited in GenBank with accession numbers of MK085955.

Genus Bregetovia Dubinin, 1951

Bregetovia limosae (Buchholz, 1869)(Figs. 3-5)

Dermaleichus limosae: Buchholz, 1869: 26, figs. 12-13

Pterolichus limosae: Mégnin and Trouessart, 1884: 337; Oudemans, 1904: 194.

Bregetovia limosae: Dubinin, 1951: 178-180, fig. 38, 1956: 415-419, figs. 199-200; Zumpt, 1961: 269, fig. 165; Vasyukova and Mironov, 1991: 37-40, figs. 22, 25; Mironov, 1992: 128-144, figs. 1, 4, 6.

Fig. 3. Bregetovia limosae, homeomorphic male. A, Dorsal view; B, Ventral view. gp, genital papillae. Scale bars: A, B=0.1 mm

Fig. 4. Bregetovia limosae, meosomorphic male. A, Dorsal view; B, Ventral view. gp, genital papillae. Scale bars: A, B=0.1 mm.​​​​​​​

Fig. 5. Bregetovia limosae, female. A, Dorsal view; B, Ventral view. eg, epigynum, gp, genital papillae. Scale bars: A, B=0.1 mm.​​​​​​​

Material examined. 2♂♂(Homeomorphic type), 2♂♂ (Mesomorphic type), 3♀♀, Korea, Chungcheongnam-do, Asan-si, Tangjeong-myeon, 36°48ʹ58ʺN, 126°2ʹ45ʺE, 18 May 2017, collected using vacuum machine from flight feathers on the wings of black-tailed godwit L. limosa by Han Y.-D. Description. Homeomorphic male: Length 470-475 μm of idiosoma from anterior end to base of the setae h3, width 205-210 μm at level of humeral shields(Fig. 3A). Prodorsal shield (Fig. 3A): Triangle-shaped, with small protrusions at anterior to bases of setae se, length 108 μm along midline, width 113 μm at posterior margin, without seta vi. Hysteronotal shield (Fig. 3A): Anterior margin straight, lateral margins with small rounded extensions, length 350 μm from anterior margins to base of setae h3, width 150-155 μm at level of small rounded extensions. Opisthosomal lobes almost straight-shaped and blunt at the cleft apex, with irregular longitudinal wavy striation between setae e2 and cleft apex. Interlobar membrane expanded at the entire edges of the terminal cleft and not narrowing to bases of setae h2. Sternum(Fig. 3B): Epimerites I fused in to a Y-shape, with transversal sclerite on the posterior end. Setae c3 located outside ventral margins of the humeral shield. Epiandrium extended anteriorly by long T-shaped sclerite and posterior parts inverted Y-shaped, with genital papillae on stem of Y.

Mesomorphic male: Length 445-455 μm of idiosoma from anterior end to base of the setae h3, width 185-200 μm at level of humeral shields(Fig. 4A). Prodorsal shield (Fig. 4A): Shaped as in homeomorphic male, entire surface with transversal wavy striation, length 100-110 μm along midline, width 115-117 μm at posterior margin. Hysteronotal shield (Fig. 4A): Anterior part straight, with transversal wavy striation excluding lobar part, length 325 μm from anterior margin to base of setae h3, width 77-80 μm. Opisthosomal lobes short and round-shaped at the apex. Setae h3 long and hairlike shaped. Sternum (Fig. 4B): Shaped as in homeomorphic male, posterior end of epimerites I not connected epimerites II. pretarsi of legs I with acuminate processes. The femurs of leg II with narrow and blunt ventral process.

Female: Idiosoma size 455-465×210-230 μm (length× width) (Fig. 5A). Prodorsal shield (Fig. 5A): Shaped as in male. Length 102-107 μm, width 120-123 μm at posterior part. Hysteronotal shield (Fig. 5A): Anterior part straight, length 330-350 μm, width 175-180 μm. Setae c3 situated outside ventral margins of the humeral shield. The posterior part of opisthosoma round-shaped, with medial incision. Sternum (Fig. 5B): Epimerites I fused, posterior end with lateral protuberances. Epigynum thick and semicircular, length 50- 55 μm, width 63-75 μm. Ambulacral disks of legs IV extending posterior of the body margin.

Remarks. Bregetovia limosae was originally described by Buchholz (1869) based on specimens collected from L. limosa in Europe.

Bregetovia limosae possesses similar to external traits B. mucronata (Mégnin and Trouessart, 1884) and B. selenura (Mégnin and Trouessart, 1884). However, B. limosae can be clearly distinguished from B. mucronata and B. selenura by the following characteristics: in males, setae c3 are located outside the ventral margin of the humeral shields; in mesomorphic males, apex of opisthosomal lobes are comparatively thick and rounded; in female, ambulacral disc of leg IV is extends to posterior part of idiosoma (Mironov, 1992). Korean specimens were morphologically consistent with the description and illustrations provided in the literature (Dabert and Ehrnsberger, 1999).

Host. This species was found on wing feathers of the blacktailed godwit L. limosa.

Distribution. Ethiopia (Zumpt, 1961), Europe (Buchholz, 1869), France, Germany, Italy, Russia (Dubinin, 1951; Vasyukova and Mironov, 1991; Mironov, 1992), Korea (this study).

Deposition. NIBR No. NIBRIV0000849808-0000849814.

Molecular characteristics. The COI sequences were obtained from three individuals and deposited in GenBank with accession numbers of MK085956-MK085958.

Family Pterolichidae Trouessart and Mégnin, 1884

Genus Montchadskiana Dubinin, 1951

Montchadskiana buchholzi(Canestrini, 1878) (Figs. 6, 7)

Dermaleichus Buchholzi: Canestrini, 1878: 64.

Proctophyllodes Buchholzi: Canestrini, 1879: 37, Pl. I-III, fig. 12.

Montchadskiana buchholzi: Dubinin, 1951: 168, fig. 31, 1956: 466-469, fig. 226; Gaud, 1972: 76-77; Vasyukova & Mironov, 1991: 127; Dabert, 1997: 244; Dabert and Ehrnsberger, 1999: 234-235, figs. 17, 22.

Fig. 6. Montchadskiana buchholzi, male. A, Dorsal veiw; B, Dorsal idisosoma; C, Ventral idisosoma; D, Genital area. ats, additional transversal sclerites, gp, genital papillae. Scale bars: A=0.2 mm, B, C=0.1 mm, D=0.05 mm.​​​​​​​

Fig. 7. Montchadskiana buchholzi, female. A, Dorsal veiw; B, Dorsal idisosoma; C, Ventral opisthosoma; D, Dorsal opisthosoma; E, Genital area. gp, genital papillae, sc, supranal concavity. Scale bars: A=0.2 mm, B-D=0.1 mm, E=0.05 mm.​​​​​​​

Material examined. 3♂♂, 3♀♀, Korea, Chungcheongnamdo, Seosan-si, Taesoan-eup, 37°0ʹ12ʺN, 126°24ʹ5ʺE, 6 Jul 2012, collected using vacuum machine from flight feathers on the wings of black-tailed godwit L. limosa by Han YD.

Description. Male: Idiosoma (Fig. 6A): length 530-540 μm of idiosoma from anterior end to base of the setae h3, width 195-230 μm at level of humeral shields, length to width ratio 2.3-2.7. Prodorsal shield (Fig. 6B): Covers the entire prodorsum, length 137-140 and width 153-162 μm, with two vi setae. Hysteronotal shield (Fig. 6B): Anterior margin slightly concave, with transversal striation between setae c1 and d1, length 360-365 μm from anterior margin to base of setae h3, width 185-195 μm at anterior part. Sternum (Fig. 6C): Epimerites I fused. Genital apparatus long and massive. Adanal shields consist of one horizontal sclerite located posterior to the genital apparatus and two triangular sclerites carrying setae ps3. Additional transversal sclerites located posterior to adanal discs. Setae ps3 lanceolate, with extension at the base and bidentate apex (Fig. 6D).

Female: Length 510-525 μm of idiosoma from anterior end to bases of setae h3, width 195-230 μm at level of humeral shields, length to width ratio 2.2-2.6 (Fig. 7A). Prodorsal shield (Fig. 7B): Shaped as in male. Length 145-148 μm at based of setae vi, width 165-175 μm at posterior part. Hysteronotal shield (Fig. 7B, C): Anterior part slightly concave, with horizontal striation at the base from setae c1 to setae d1, lateral margins with horizontal incisions at bases of setae h1, length 365-380 μm, width 375-400 μm at based of setae c2. Setae h1 lanceolate. Supranal concavity circular-shaped, divided from terminal terminus, flanked with a pair of tongueshaped crests(Fig. 7D). Epigynum absent(Fig. 7E).

Remarks. Montchadskiana buchholzi was originally described by Buchholz (1869) based on specimens collected from L. limosa (=Limosa melanura) in Europe. Thereafter, this species was reported from L. limosa and L. lappoinca by several mite taxonomists (Canestrini, 1878; Dubinin, 1951, 1956; Gaud, 1972; Vasyukova and Mironov, 1991; Dabert and Ehrnsberger, 1999).

Montchadskiana buchholzi is very similar to M. calidridis Dubinin, 1956 and M. glareolae Dabert & Ehrnsberger, 1999 with regard to external traits. However, M. buchholzi can be clearly distinguished from M. calidridis and M. glareolae by the following characteristics: in males, adanal shield is comprised of single transversal and two triangular sclerites, and additional two transversal sclerites are located posterior to adanal discs; in female, lateral margins of hysteronotal shield have transversal incisions at bases of setae h1, and one pair of tongue-shaped crests are situated on both sides of the supranal concavity (Dabert and Ehrnsberger, 1999). Korean specimens well agreed with the description and illustrations that described by Dabert and Ehrnsberger(1999).

However, setae ps3 of all observed males have a basal extension and a slightly bidentate apex. We consider this difference to be and geographical or population variability.

Host. Specimens were collected from the surface of flight feathers on the wings of the black-tailed godwit L. limosa.

Distribution. Europe (Canestrini, 1878), France, Morocco (Gaud, 1972), Poland (Dabert and Ehrnsberger, 1999), Russia (Dubinin, 1951, 1956; Vasyukova and Mironov, 1991), and Korea (this study).

Deposition. NIBR No. NIBRIV0000835099, NIBRIV0000 843277-0000843281.

Molecular characteristics. The COI sequences were obtained from single individual and deposited in GenBank with accession numbers of MK791137.