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Feather mites (Acariformes, Astigmata) from marine birds of the Barton Peninsula (King George Island, Antarctica), with descriptions of two new species
expand article infoYeong-Deok Han§, Sergey V. Mironov|, Jeong-Hoon Kim, Gi-Sik Min
‡ Inha University, Incheon, Republic of Korea
§ National Institute of Ecology, Yeongyang-gun, Republic of Korea
| Zoological Institute, Russian Academy of Sciences, Saint-Petersburg, Russia
¶ Korea Polar Research Institute, Incheon, Republic of Korea
Open Access

Abstract

We report on the first investigation of feather mites associated with birds living on the Barton Peninsula (King George Island, Antarctica). We found seven feather mite species of the superfamily Analgoidea from four host species. Two new species are described from two charadriiform hosts: Alloptes (Sternalloptes) antarcticus sp. nov. (Alloptidae) from Stercorarius maccormicki Saunders (Stercorariidae), and Ingrassia chionis sp. nov. (Xolalgidae) from Chionis albus (Gmelin) (Chionidae). Additionally, we provide partial sequences of the mitochondrial cytochrome c oxidase subunit I (COI), which was utilized as a DNA barcode, for all seven feather mite species.

Keywords

Alloptes, Analgoidea, Antarctica, feather mites, Ingrassia, systematics

Introduction

Feather mites (Astigmata, Analgoidea and Pterolichoidea) are a vast group of highly specialized parasites or mutualistic ectosymbionts that spend their entire life cycle on their bird hosts (Gaud and Atyeo 1996; Dabert and Mironov 1999; Proctor 2003). Most of these mites occupy various microhabitats in the plumage of birds; however, representatives of a few families are parasites located on the skin and in the respiratory tract of their avian hosts. Owing to their specialization to particular microhabitats on birds and dispersal mainly by a direct contact of host individuals, feather mites usually show a high level of host-specificity (Mironov and Dabert 1999; Proctor and Owens 2000; Dabert 2005).

Antarctica is the fifth largest and most isolated continent on our planet (Peck 2018; Sancho et al. 2019). On this 14 million km2 continent, less than 0.35% of the territory remains seasonally free of ice and snow (Bockheim 2015). Many endemic species inhabit these ice-free terrestrial areas, where birds and marine mammals breed in the coastal zones (Chown and Convey 2007; Hughes 2010). Approximately 400 species of birds have been recorded from the Antarctic continent and oceanic waters north to approximately 40°S (Shirihai 2007). Vanstreels et al. (2020) recently summarized data on the biodiversity of ectoparasites associated with Antarctic and Subantarctic birds and reported 30 feather mite species from 28 bird species in this region.

King George Island is the largest of the South Shetland Islands at the northwest tip of the Antarctic Peninsula (Potapowicz et al. 2020). This island has six areas designated as the Antarctic Specially Protected Areas (ASPA), one of which is ASPA No. 171, located on the southeast coast of the Barton Peninsula. Approximately 5,000 pairs of two penguin species, Pygoscelis antarcticus (Forster) and P. papua (Forster), breed in ASPA No. 171, and 14 other bird species have been observed on the Barton Peninsula: Chionis albus (Gmelin), Larus dominicanus Lichtenstein, Stercorarius antarcticus (Lesson), S. maccormicki Saunders, Sterna paradisaea Pontoppidan, and St. vittata Gmelin (Charadriiformes), Leucocarbo bransfieldensis (Murphy) (Pelecaniformes), Daption capense (Linnaeus), Fregetta tropica (Gould), Fulmarus glacialoides (Smith), Macronectes giganteus (Gmelin), Oceanites oceanicus (Kuhl) (Procellariiformes), Eudyptes chrysolophus (Brandt), Pygoscelis adeliae (Hombron & Jacquinot) (Sphenisciformes) (Kim et al. 2005, 2014).

To date, no studies have been conducted on feather mites associated with birds living on the Barton Peninsula. In the present work, we report seven analgoid feather mites, including descriptions of two new species from the genera Alloptes and Ingrassia, found on four bird species on the Barton Peninsula of King George Island. Additionally, we provide DNA barcodes for the mitochondrial cytochrome c oxidase subunit I (COI) from these seven analgoid feather mite species.

Materials and methods

Material sampling

Mite samples were obtained from the Antarctic Shag (L. bransfieldensis), South Polar Skua (S. maccormicki), Wilson’s Storm Petrel (O. oceanicus), and three Snowy Sheatbills (Ch. albus) in the Barton Peninsula. The birds were captured using a hand net or loop according to ‘SKUAS Manual for Fieldworkers’ (PBEG 2003), and all birds were released after collecting the mites. Feather mites were collected using 3M ScotchMagicTape (3M, St. Paul, Minnesota, USA) from the wing, down, and tail feathers, and then immediately preserved in 70% ethanol for 3 h. The preserved samples were separated from Scotch tape under a dissecting microscope with a dissecting needle and then preserved in 95% ethanol. The collected mite specimens were cleared in 10% lactic acid for 24 h at room temperature and then mounted on microscope slides using PVA mounting medium (BioQuip, Rancho Dominguez, California, USA).

Descriptions of two new species are given according to standard formats used for the corresponding feather mite taxa (Mironov and Palma 2006; Mironov and Proctor 2008; Stefan et al. 2013; Hernandes et al. 2017). Terminology, idiosomal, and leg chaetotaxy follow Gaud and Atyeo (1996), with minor corrections for the coxal chaetotaxy by Norton (1998). All measurements are in micrometers (μm). All examined specimens are deposited at the National Institute of Biological Resources (NIBR), Korea. The classification and scientific names of birds follow Gill et al. (2021).

DNA sequencing

Before preparing the microscopic slides, genomic DNA was extracted from one leg of each specimen using a Tissue DNA Purification Kit (Cosmogenetech Inc., Seoul, Korea) according to the manufacturer’s instructions. The COI barcode fragment was amplified using two universal primers: bcdF05 (5′-TTTTCTACHAAYCATAAAGATATTGC-3′) and bcdR04 (5′- TATAAACYTCDGGATGNCCAAAAAA-3′) under the following conditions: 2 min at 94 °C; 40 cycles at 98 °C for 15 s, 50 °C for 30 s, and 68 °C for 60 s; and a final extension at 68 °C for 5 min (Dabert et al. 2008). The amplified products were sequenced using an ABI3100 automated sequencer (Perkin Elmer, Foster City, California, USA). Sequence assembly, alignment, and trimming were performed using Geneious 8.1.9 software (Kearse et al. 2012). We obtained a 654 bp fragment sequence of the COI gene from two individuals per mite species.

Systematic account

Superfamily Analgoidea Trouessart & Mégnin, 1884

Family Alloptidae Gaud, 1957

Alloptes Canestrini, 1879

Notes

Alloptes is one of the most specious genera of the family Alloptidae and currently includes about 50 described species (Gaud 1972; Vasyukova and Mironov 1991; Kivganov and Mironov 1992; Mironov and Palma 2006). All representatives of this genus are associated with birds of the order Charadriiformes, with exception of a questionable host association of Alloptes tubinarii Dubinin, 1949 reported from several procellariiform hosts (Dubinin 1949). Gaud (1972) subdivided the genus into the three subgenera, Alloptes s. str., Apodalloptes Gaud, 1972, and Conuralloptes Gaud, 1972. Further, nearly a half of species of the subgenus Conuralloptes was arranged into a fourth subgenus, Sternalloptes Mironov, 1992 (in Kivganov and Mironov 1992). Three Alloptes species found on marine birds of the Barton Peninsular belong to three different dubgenera. Below we provide descimination features for these subgenera.

Alloptes Canestrini, 1879

Notes

The subgenus Alloptes s. str. currently includes three species and is characterized by the following features (Gaud 1952, 1972; Mironov 1996): in both sexes, seta mG of genu II is spiculiform; in males, the opisthosoma is roughly shaped as an equilateral triangle with terminal part strongly enlarged, setae h3 are present, setae ps2 are well developed (half as long as f2); in females, the opisthosoma is rounded, the opisthosomal lobes are not developed, idiosomal setae ps1 and f2 are present. Representatives of the subgenus are known from birds of the families Scolopacidae and Chionidae (Gaud 1952, 1957, 1972; Vasyukova and Mironov 1991). Five Alloptes species described by Dubinin (1952) from auks (Alcidae) could also belong to this subgenus, because these mites have filiform genual setae mGII and females have the opisthosoma rounded or with strongly abbreviated lobes, but all these species need re-investigation.

Alloptes (Alloptes) aschizurus Gaud, 1952

Alloptes aschizurus Gaud, 1952: 163–164, fig. 2; Atyeo and Peterson 1967: 98; 1970: 129.

Alloptes (Alloptes) aschizurus: Gaud 1972: 59.

Material examined

3 males and 3 females (NIBR No. NIBRIV0000887146–NIBRIV0000887151) from Chionis albus (Gmelin) (Charadriiformes, Chionidae), Antarctica, King George Island, Barton Peninsula, 62°14'16"S, 58°46'13"W, 8 January 2016, coll. Han Y.-D.

Remarks

Alloptes (Alloptes) aschizurus was initially described from specimens collected from the Black-faced Sheathbill, Chionis minor (Hartlaub) on Kerguelen Island (Gaud 1952). Later, this mite species was found on the same host on Heard Island and on the Snowy Sheathbill, Ch. albus, on Greenwich Island and Gaston Islands (Atyeo and Peterson 1967). As for all members of the subgenus Alloptes s. str., this mite species is characterized by the following features: in both sexes, genual setae mGII are spiculiform; in males, the opisthosoma is shaped as an equilateral triangle with a strongly enlarged posterior end; in females, the posterior end of the opisthosoma is rounded, and the opisthosomal lobes are not developed (Gaud 1972; Vasyukova and Mironov 1991; Mironov and Hernandes 2020). Alloptes (A.) aschizurus is distinguished from the closest species of the subgenus, A. (A.) tringae (Grube, 1859) [widely known under the junior synonym A. (A.) crassipes (Canestrini, 1878)] in having the following features. In both sexes, the length of the idiosoma is approximately 500 long (vs approximately 450 in A. tringae), and trochanteral setae sRIII are equal to or slightly longer than the trochanters III (vs distinctly shorter than the trochanters) (Gaud 1952; Atyeo and Peterson 1967; Vasyukova and Mironov 1991; Mironov and Hernandes 2020).

Molecular data

The COI sequences were obtained from two individuals and deposited in GenBank with accession numbers MZ489637 and MZ489638.

Conuralloptes Gaud, 1972

Notes

The subgenus Conurlloptes currently includes 23 species and is characterized by the following features (Gaud 1972; Vasyukova and Mironov 1991): in both sexes, seta mG of genu II is short spine-like with widely rounded apex; in males, the opisthosoma is triangular, gradually narrowed posteriorly and without posterior enlargement, idiosomal setae h3 are absent, setae ps2 are strongly reduced (barely distinct); in females, opisthosoma with well-developed opisthosomal lobes, setae ps1 and f2 are present. This subgenus is known from birds of the families Chionidae, Pedionomidae, Recurvirostridae, and Scolopacidae in the order Charadriiformes (Gaud 1972; Vasyukova and Mironov 1991; Mironov and Palma 2006).

Alloptes (Conuralloptes) chionis Atyeo & Peterson, 1967

Alloptes chionis Atyeo & Person, 1967: 98, figs 1–4; 1970: 129–130, figs 15–17.

Alloptes (Conuralloptes) chionis: Mironov 2007: 619.

Material examined

3 males and 3 females (NIBR No. NIBRIV0000887152–NIBRIV0000887157) from Chionis albus (Gmelin) (Charadriiformes, Chionidae), Antarctica, King George Island, Barton Peninsula, 62°14'3"S, 58°46'56"W, 13 January 2016, coll. Han Y.-D.

Remarks

Alloptes (Conuralloptes) chionis was described from specimens collected from Ch. minor (type host) on Heard Island and was also found on Ch. albus from the Gaston Islands (Atyeo and Person 1967). When this mite was described, the genus Alloptes had not yet been subdivided into subgenera. Gaud (1972) established three subgenera in this genus but did not consider the taxonomic position of this species. Mironov (2007) placed this mite in the subgenus Conuralloptes based on the following characters: in both sexes, genual setae mGII are shaped as short and thick spines with bluntly rounded apices; in males, the opisthosoma is not enlarged apically, and idiosomal setae h3 are absent; in females, the idiosomal setae ps1 and f2 are present. The males of A. (C.) chionis can be distinguished from other species of the subgenus Conuralloptes by the following combination of features: the anterior margin of the hysteronotal shield is slightly convex, the pregenital sclerites are free from each other and almost parallel, the adanal shields are C-shaped, and macrosetae h2 are flattened and slightly widened in the medial part (Atyeo and Peterson 1967, 1970).

Molecular data

The COI sequences were obtained from two individuals and deposited in GenBank with accession numbers MZ489639 and MZ489640.

Sternalloptes Mironov, 1992

Notes

The subgenus Sternalloptes includes about 20 species and is characterized by the following features (Kivganov and Mironov 1992; Mironov 1996): in both sexes, seta mG of genu II is shortspine-like with widely rounded apex; in males, the opisthosoma is triangular, gradually narrowed posteriorly and with noticeable terminal enlargement, idiosomal setae h3 are present or absent, setae ps2 are strongly reduced; in females, the opisthosoma with well-developed opisthosomal lobes, idiosomal setae ps1 and f2 are absent. Common hosts of the subgenus Sternalloptes are birds of the families Laridae and Stercorariidae in the order Charadriiformes (Gaud 1976; Vasyukova and Mironov 1991; Kivganov and Mironov 1992; Mironov and Kivganov 1993).

Alloptes (Sternalloptes) antarcticussp. nov.

Type material

Male holotype (NIBR No. NIBRIV0000887158), 3 males and 4 females paratypes (NIBR No. NIBRIV0000887159–NIBRIV0000887164) from Stercorarius maccormicki Saunders (Charadriiformes, Stercorariidae), Antarctica, King George Island, Barton Peninsula, 62°14'2"S, 58°46'20"W, 2 January 2016, coll. Han Y.-D.

Description

Male (Figs 1, 3A–E, 4A, B; holotype, range for 3 paratypes in parentheses): idiosoma, length × width, 370 (340–365) × 200 (175–205). Length of hysterosoma 228 (213–243). Prodorsal shield (Figs 1A, 4A): length 80 (78–80), width at posterior margin 114 (102–118), posterolateral corners truncate, posterior margin slightly concave. External scapular setae se situated on posterolateral extensions of prodorsal shield near their anterior margins. Hysteronotal shield: greatest length 255 (235–258), width at anterior margin 100 (98–108), anterior margin slightly concave, lateral margins without incisions at bases of setae d2 and fused ventrally with bases of epimerites IV. Length between prodorsal and hysteronotal shields along midline 31 (18–22). Dorsal setae c2 32 (33–36) long, shorter than trochanters III (Fig. 4C). Subhumeral setae c3 narrowly lanceolate, 23 (19–23) × 2 (3). Posterior part of opisthosoma gradually expanded at posterior end, width at level of setae h2 50 (46–53). Length of interlobar septum 82 (80–86). Terminal lamella with three pairs of festoons; incision between inner pair narrow slit-like or inner festoons slightly overlapping. Setae h3 present, setae ps2 distinct. Setae h2 cylindrical, not expanded in medial part. Dorsal measurements: se:se 118 (96–106), c2:d2 55 (50–57), d2:ps1 165 (158–168). Bases of trochanters I, II flanked by narrow sclerotized bands connecting bases of corresponding epimerites (Fig. 1B). Pregenital sclerites fused as a Y, their anterior ends connected to inner ends of epimerites IIIa, posterior end fused with paragenital arch. Coxal fields III and IV closed. Length of genital-anal field 163 (158–168). Genital arch: 17 (15–17) × 20 (19–20). Coxal setae 4b situated anterior to level of setae 3a. Setae 4a surrounded by sclerites of irregular form. Ventral measurements: 3a:4b 10 (9–13), 4b:g 45 (43–43), 4b:4a 63 (60–65), g:ps3 30 (31–35), ps3:ps1 110 (109–117), 4a:4a 120 (110–112). Setae mG of genua I thin spine-like with acute apex, setae mGII shaped as thick spine with bluntly rounded apex. Legs IV 203 (193–203) long. Distal margin of tibia IV with small spine. Tarsus IV 54 (49–55) long, with claw-like apex; setae d and e small spine-like, seta e situated near tarsal apex, seta d at level of seta f, setae r and w in basal one-third of the segment (Fig. 3A–C).

Figure 1. 

Alloptes (Sternalloptes) antarcticus sp. nov., male A dorsal view B ventral view.

Female (Figs 2, 4F, G, 4C; range for 4 paratypes): idiosoma, length × width, 350–360 × 148–153 (Fig. 2A). Hysterosoma 238–250 long. Prodorsal shield: shaped as in male, 80–83 × 85–90. Setae c2 10–14 long, shorter than trochanters III. Setae c3 lanceolate, 13–15 × 2–3. Hysteronotal shield: 233–238 × 60–62, anterior margin straight or slightly concave, surface without ornamentation. Setae h1 and e2 situated at same transverse level. Setae f2 and ps1 absent. Distance between prodorsal and hysteronotal shields along midline 23–33. Supranal concavity ovate, opened posteriorly, delimited from terminal cleft by short extensions. Opisthosomal lobes well developed, approximately as long as wide at base, terminal cleft as an inverted U, 24–30 long, 12–20 wide (Fig. 4C). Anterior end of supranal concavity extending slightly beyond level of setae h2. Dorsal measurements: se:se 83–89, c2:d2 64–67, d2:e2 104–106, e2:h2 39–43, h2:h3 19–20, h2:h2 55–60, h3:h3 25–31. Bases of trochanters I, II flanked by narrow sclerotized bands connecting bases of corresponding epimerites (Fig. 2B). Epimerites IVa barely distinct. Epigynum bow-shaped, 24–27 × 55–59. Legs IV with ambulacral discs reaching level of insertions of setae h2 (Figs 2, 3F, G).

Figure 2. 

Alloptes (Sternalloptes) antarcticus sp. nov., female A dorsal view B ventral view.

Figure 3. 

Alloptes (Sternalloptes) antarcticus sp. nov., details A opisthosoma of male, dorsal view B leg I of male C leg II of male D leg III of male E leg IV of male F leg III of female G leg IV of female.

Differential diagnosis

Among 18 previously known species in the subgenus Sternalloptes (Kivganov and Mironov 1992; Mironov and Kivganov 1993; Kivganov 1996; Hernandes et al. 2017), the new species Alloptes (S.) antarcticus sp. nov. is most similar to A. (S.) catharacti Mironov, 1991 found on the same host, S. maccormicki from Mirny station (Queen Mary Land, Antarctica), in having setae c3 lanceolate and short (shorter that trochanters III), the pregenital sclerite fused into a Y connecting the tips of epimerites IIIa and the apex of the paragenital arch, and setae h2 not expanded (Mironov 1991). Alloptes (S.) antarcticus sp. nov. differs from A. (S.) catharacti in having the following characteristics: in both sexes, the external scapular setae se are situated on the posterolateral extensions of the prodorsal shield; in males, the dorsal setae c2 (32–36) are approximately 1.5 times longer than setae c3 (19–23) and shorter than trochanters III (Fig. 4A, B); in females, the terminal cleft is shorter (24–30 long), and the supranal concavity is open posteriorly into the terminal cleft (Fig. 4C). In both sexes of A. (S.) catharacti, setae se are situated on the soft tegument near the anterior margin of the posterolateral extensions of the prodorsal shield; in males, the dorsal setae c2 (63–93) are 2–3 times longer than setae c3 (24–29) and exceed the length of trochanters III (Fig. 4D, E); in females, the terminal cleft is longer (38–48), and the supranal concavity is separated from the terminal cleft (Mironov 1991) (Fig. 4F).

Figure 4. 

Alloptes species A–C Alloptes (Sternalloptes) antarcticus sp. nov. D–F A. (S.) catharacti A, D prodorsal shield of males B, E humeral shield of males C, F opisthosomal lobes of females.

Remark

The comparative material of A. (S.) catharacti used here to illustrate morphological differences was collected from the same host species, S. maccormicki, at Jangbogo station, Terra Nova Bay, Antarctica, in 2016, by Ji-Yong Lee.

Molecular data

The COI sequences were obtained from two individuals and deposited in GenBank with accession numbers MZ489641 and MZ489642.

Etymology

The specific name refers to the geographical range of the type host.

Family Avenzoariidae Oudemans, 1905

Subfamily Bonnetellinae Atyeo & Gaud, 1981

Genus Scutomegninia Dubinin, 1951

Subgenus Scutomegninia Dubinin, 1951

Scutomegninia (Scutomegninia) subantarctica Mironov, 2000

Scutomegninia phalacrocoracis: Atyeo & Peterson 1967: 100, figs 5–8; 1970: 150, figs 68–70.

Scutomegninia subantarctica Mironov, 1990: 53, nom. nudum.

Scutomegninia (Scutomegninia) subantarctica: Mironov 2000: 14–18, fig. 5.

Material examined

1 male and 3 females (NIBR No. NIBRIV0000887165–NIBRIV0000887168) from Leucocarbo bransfieldensis (Murphy) (Suliformes, Phalacrocoracidae), Antarctica, King George Island, Barton Peninsula, 62°14'4"S, 58°46'52"W), 8 January 2016, coll. Han Y.-D.

Remarks

Mites of the genus Scutomegninia, collected from the Imperial Shag, Leucocarbo atriceps (King) (= Phalacrocorax atriceps) in Maipo Island (Buls Bay on Brabant Island, Palmer Archipelago, Antarctica) by Atyeo and Peterson (1967), were originally identified as S. phalacrocoracis (Dubinin and Dubinina, 1940). Furthermore, Atyeo and Peterson (1970) reported S. (S.) phalacrocoracis from Leucocarbo georgianus (Lönnberg) (= P. atriceps georgianus) from Bird Island, South Georgia. Later, Mironov (1990, 2000) described specimens from the Palmer Archipelago as a separate species, S. (S.) subantarctica. According to the present taxonomic view, Phalacrocorax atriceps belongs to the genus Leucocarbo and is split into several separate species restricted to particular areas of the Antarctic and subantarctic regions (Gill et al. 2021). Taking into consideration this concept, S. (S.) subantarctica reported by previous researchers (Atyeo and Peterson 1967, 1970) were collected from the Antarctic Shag, L. bransfieldensis (Antarctic Peninsula and Palmer Archipelago), and the South Georgia Shag, L. georgianus (South Georgia).

Scutomegninia (S.) subantarctica belongs to the phalacrocoracis group (species associated with Phalacrocoracidae and Anhingidae), and it is most similar to S. (S.) pygmaea Mironov, 1990. It differs from S. (S.) pygmaea and other species of the phalacrocoracis group by the following combination of characters in males: the terminal ends of the interlobar membrane have a small spine-like process; the lateral adanal shields have acute posterior ends, while the medial adanal shields have the posterior ends bluntly rounded; the anteromedial ends of adanal apodemes are rounded; setae s of tarsus III are spine-like, strongly attenuate apically, and bear two small denticles; the terminal cleft is 1.8–2 times longer than wide; and the incision in the interlobar membrane extends to the level of setae h2 (Mironov 1990, 2000).

Molecular data

The COI sequences were obtained from two individuals and deposited in GenBank with accession numbers MZ489643 and MZ489644.

Genus Zachvatkinia Dubinin, 1949

Zachvatkinia hydrobatidii Dubinin, 1949

Zachvatkinia hydrobatidii Dubinin, 1949: 219, figs 9b, 10b; 1952, 256; Atyeo and Peterson 1967: 101, figs 9–12; 1970: 146, figs 61–63; Mironov 1989: 110–115, figs 5, 7, 8.

Material examined

3 males and 3 females (NIBR No. NIBRIV0000887169–NIBRIV0000887174) from Oceanites oceanicus (Kuhl) (Procellariiformes, Oceanitidae), Antarctica, King George Island, Barton Peninsula, 62°14'15'S, 58°46'28"W, 9 January 2016, coll. Han Y.-D.

Remarks

Zachvatkinia hydrobatidii was described by Dubinin (1949) based on specimens collected from the Wilson’s Storm Petrel, O. oceanicus in Massachusetts (USA), and also from 10 other storm petrels of the genera Fregetta, Garrodia, Pelagodroma (Oceanitidae), and Oceanodroma (Hydrobatidae) from various parts of the world. Mironov (1989) re-examined most of this material and referred to this mite species only the specimens from the oceanitids O. oceanicus and F. tropica. In Antarctica, Z. hydrobatidii was previously reported from O. oceanicus, F. tropica, and Pagodroma nivea (Forster) (Procellariidae) (Atyeo and Peterson 1967, 1970). The record from the procellariid host seems to be questionable. Zachvatkinia hydrobatidii is very close to Z. oceanodromae Mironov, 1989 associated with storm petrels of the genus Oceanodroma, and differs in having the following features: in males, the genital arch is shaped as a completely closed ring, and the distance between setae ps1 and h3 is less than 40; in females, the posterior margin of the opisthosoma between the terminal extensions is not sclerotized, and setae e1 are situated on the inner margins of the lateral hysteronotal shields (Mironov 1989).

Molecular data

The COI sequences were obtained from two individuals and deposited in GenBank with accession numbers MZ489645 and MZ489646.

Zachvatkinia stercorarii Dubinin, 1952

Zachvatkinia stercorarii Dubinin, 1949: 227, fig. 12, nom. nudum, 1952: 255, figs 1, 2; Atyeo and Peterson 1967: 103, 1970: 147; Mironov 1989: 100–111, figs 3, 7, 8.

Material examined

3 males and 3 females (NIBR No. NIBRIV0000887175–NIBRIV0000887180) from Stercorarius maccormicki Saunders (Charadriiformes, Stercorariidae), Antarctica, King George Island, King Sejong station, Barton Peninsula, 62°14'2"S, 58°46'20"W, 21 January 2016, coll. Han Y.-D.

Remarks

Zachvatkinia stercorarii was described by Dubinin (1952) based on specimens collected from three species of skuas or jaegers, Stercorarius pomarinus (Temminck) (type host), S. parasiticus (Linnaeus), and S. longicaudus Vieillot, from Wrangel Island, Russia. Furthermore, it was shown that mites from S. parasiticus and S. longicaudus belong to a separate species, Z. isolata Mironov, 1989 (Mironov 1989; Dabert et al. 2015). In Antarctica, Z. stercorarii was previously reported from S. antarcticus (Lesson) from Adelaide Island and the Palmer Archipelago and from S. maccormicki from Cape Hallett, Haswell Islands, Ross Island, and Victoria Land (Atyeo and Peterson 1967, 1970).

Although Z. stercorarii and Z. isolata are associated with birds in the order Charadriiformes, these mite species belong to the puffini species group, which is characterized by a single dorsobasal spine on tarsus IV in males and setae d1 situated off the lateral hysteronotal shields in females (Mironov 1989). All remaining species of the puffini group are associated with Procellariiformes, while other representatives of the genus Zachvatkinia associated with Charadriiformes belong to the sternae species group. It was hypothesized that the common ancestors of Z. stercorarii and Z. isolata were probably transferred from some procellariiform hosts to the ancestor of the family Stercorariidae (Dabert and Mironov 1999).

Zachvatkinia stercorarii can be clearly distinguished from Z. isolata in having the following features: in males, the bases of genital setae g are adjacent (vs distant from each other); in females, the posterior margin of the prodorsal shield is just slightly convex (vs strongly convex), and the lateral margins of this shield have small incisions posterior to the bases of setae se (vs smooth and without incisions) (Mironov 1989).

Molecular data

The COI sequences were obtained from two individuals and deposited in GenBank with accession numbers MZ489647 and MZ489648.

Family Xolalgidae Dubinin, 1953

Subfamily Ingrassiinae Gaud & Atyeo, 1981

Ingrassia Oudemans, 1905

Notes

The genus Ingrassia is the most specious genus within the subfamily Ingrassiinae, including 28 species up to now (Gaud 1972; Vasyukova and Mironov 1991; Mironov and Proctor 2008; Stefan et al. 2013). Representatives of the genus have been recorded on hosts from six orders of aquatic birds: Anseriformes, Charadriiformes, Pelecaniformes, Podicipediformes, Procellariiformes, and Sphenisciformes. Identification keys to species of Ingrassia are available only for those associated with birds in the order Charadriiformes in Africa (Gaud 1972) and northern Eurasia (Vasyukova and Mironov 1991). To date, only six species of the genus Ingrassia have been recorded from procellariiform birds (Stefan et al. 2013).

Ingrassia chionis sp. nov.

Type material

Male holotype (NIBR No. NIBRIV0000887181), 2 males and 3 females paratypes (NIBR No. NIBRIV0000887182–NIBRIV0000887186) from Chionis albus (Gmelin) (Charadriiformes, Chionidae), Antarctica, King George Island, Barton Peninsula, 62°14'13"S, 58°46'33"W, 11 January 2016, coll. by Han Y.-D.

Description

Male (Figs 5, 7A–D; holotype, range for 2 paratypes in parentheses): length of idiosoma from anterior end to bases of setae h3 350 (350–355), greatest width 220 (230–240), length of hysterosoma 175 (173–175). Prodorsal shield: narrow longitudinal plate with almost parallel lateral margins and acute posterior end extending beyond level of scapular setae se; length along midline 113 (118), greatest width 28 (27–29); anterior end with short longitudinal ridge about 1/8th the length of shield (Fig. 5A). Setae se and si at same transverse level, bases of setae se situated on teardrop-shaped sclerites and separated by 69 (73–77). Scapular shields wide, inner margins slightly convex, without suprategumental extensions. Hysteronotal shield: anterior margin convex, length of shield from anterior end to bases of setae h3 213 (205–210). Setae c2 and d2 represented by macrosetae, 150 (150–150) and 110 (95–110) long, respectively; both pairs approximately 1.5 time shorter than humeral macrosetae cp. Opisthosomal lobes slightly longer than wide at base. Supranal concavity ovate, poorly outlined, separated from terminal cleft. Terminal cleft semi-ovate in shape, slightly narrowed anteriorly; length of terminal cleft from anterior end to bases of setae h3 63 (58–62), greatest width 40 (41–42). Terminal membranous extensions on lobar apices short and widely rounded, length from bases of setae h3 to apices of terminal extensions 20 (18–19), width of extensions at base 32 (27–28), length of incision between extensions 22 (19–20). Setae ps1 situated approximately at level of setae h2. Distance between dorsal setae: c2:c2 183 (180–188), c2:d2 33 (37–38), d2:e2 52 (50–53), e2:h3 88 (83–84), h3:h3 59 (55–57), ps1:ps1 39 (36–37).

Figure 5. 

Ingrassia chionis sp. nov., male A dorsal view B ventral view.

Sternum about half as long as total length of epimerites I (Fig. 5B). Anterior ends of epimerites IIIa free, widely separated from each other. Setae 4b situated on anterior ends of epimerites IIIa and almost extending to mid-length of opisthosomal lobes. Pregenital apodeme (epiandrum) small bow-shaped, 10 (7–9) long, 35 (32–38) wide. Genital apparatus 13 (10–12) long and 27 (27–28) wide. Setae g situated on small genital shields. Adanal shields triangular, situated anterolateral to setae ps3. Epimerites IVa long, almost completely enclosing coxal fields IV. Central part of coxal fields IV not sclerotized. Diameter of adanal suckers 19 (19–20). Distance between ventral setae: 4b:4b 33 (35–36), 4b:3a 24 (27–29), 4b:g 41 (42–43), g:ps3 29 (32–33), ps3:h3 97 (93–95).

Tarsi I, II each with short apicodorsal extension. Tibiae I, II with well-developed ventral spine-like processes (Fig. 7A, B). Seta s of tibia II spiculiform. Femorogenu II with thick spine-like retrograde apophysis. Tibia III with small angular apical extension bearing base of solenidion φ. Length of tarsus III 81 (78–79). Tarsus IV with finger-like apical extension; modified setae d, e short spiculiform, seta e situated on tarsal apex, seta d subapical (Fig. 7C). Legs IV excluding pretarsus 55 (51–58) long, with tarsus and distal half of genu extending beyond level of lobar apices (bases of setae h3) (Figs 5, 7D).

Female (Figs 6, 7E, F; range for 3 paratypes): length of idiosoma 400–435, greatest width 225–250, length of hysterosoma 220–238. Prodorsal shield: shaped approximately as in male, length 118–123, greatest width 30–33, anterior end with short longitudinal ridge about 1/8th the length of shield (Fig. 6A). Setae se and si at same transverse level; bases of setae se situated on teardrop-shaped sclerites and separated by 75–82. Scapular shields wide, with smooth inner margin. Humeral shields well developed, without anteromesal extensions. Setae c3 short, slightly longer than trochanters III. Hysteronotal shield: large longitudinal plate occupying median part of hysterosoma; anterior part slightly widened; anterior margin right-angular, extending to or beyond level of setae c2; lateral margins unevenly sinuous; posterior margin truncate or slightly concave, extending to level of setae e2; greatest length 158–168, greatest width 85–93. Setae c2, d2, and e2 represented by macrosetae, 139–151, 112–131 and 81–93 long, respectively. Setae d1, d2, and e1 situated on hysteronotal shield, setae c2, e2 situated on striated tegument. Distance between dorsal setae: c2:d2 63–73, d2:e2 84–87, e2:h3 82 87, h3:h3 52–70.

Figure 6. 

Ingrassia chionis sp. nov., female A dorsal view B ventral view.

Sternum about half as long as epimerites I. Epigynum thick and is bow-shaped, 13–22 long, 58–64 wide, with tips bearing bases of setae 4b. Apodemes of oviporus long, their posterior ends long and narrow, encompassing bases of setae 4a (Fig. 6B). Setae 4b, g, 3a, and 4a short, not exceeding length of femorogenua III, IV. Setae h3 approximately two-thirds the length of setae h2.

Legs I, II as in the male. Legs IV with tarsus extending beyond posterior end of opisthosoma. Tarsi III, IV without apical spines, length of tarsi III, IV 60–61 and 72–74, respectively. Setae sRIII subequal to combined length of corresponding femur, genu, and tibia. Seta w of tarsus III and setae r, w of tarsus IV spiculiform (Figs 6, 7).

Figure 7. 

Ingrassia chionis sp. nov., legs A tibia and tarsus I of male B tibia and tarsus II of male C tibia and tarsus III of male D tibia and tarsus IV of male E tibia and tarsus III of female F tibia and tarsus IV of female.

Differential diagnosis

The new species Ingrassia chionis sp. nov. belongs to a group of species associated with the Charadriiformes and is characterized by a retrograde spine-like apophysis on femorogenu II in both sexes (Gaud 1972; Vasyukova and Mironov 1991). Among this species grouping, the new species is most similar to I. tringae Vitzthum, 1922 (= I. minuta Gaud, 1972) described from Calidris minuta (Leisler) (Scolopacidae) in having the following features: in males of both species, the opisthosomal lobes are relatively short, equal to or slightly longer than wide at the bases, and the supranal concavity is completely separated from the terminal cleft; in females, the hysteronotal shield is shaped as a large longitudinal plate occupying the median area of the hysterosoma. Ingrassia chionis is distinguished from I. tringae by the following features: in both sexes, the prodorsal shield is narrow, parallel-sided, with the width about one-third the distance between setae se, and the posterior end of this shield is tapering; in males, the terminal cleft is semi-ovate, narrowed only in the anterior end, and tibia III bears a small apical spine of rectangular shape; in females, the anterior margin of the hysteronotal shield is right-angled and extends to the level of setae c2, and the posterior margin of this shield is truncate and extends to the level of setae e2. In both sexes of I. tringae, the prodorsal shield is a longitudinal plate widened posteriorly, with its greatest width equal to or larger than the halfway between setae se, and the posterior margin is widely rounded; in males, the anterior half of the terminal cleft is strongly narrowed, and tibia III bears a pointed apical spine; in females, the anterior margin of the hysteronotal shield is semi-ovate and does not extend to the level of setae c2, and the posterior margin of this shield is concave and extends beyond the level of setae e2.

Molecular data

The COI sequences were obtained from two individuals and deposited in GenBank with accession numbers MZ489649 and MZ489650.

Etymology

The specific name is taken from the generic name of the type host and is a noun in apposition.

Acknowledgements

This study was supported by Korea Polar Research Institute’s projects on the “Ecophysiology of Antarctic terrestrial organisms to reveal mechanisms of adaptation to changing environment” (PE21130). The authors wish to thank Ji-Young Lee (Chonnam National University, Korea) for sample collection. The permit for catching birds was officially approved the Korean Ministry of Foreign Affairs and Trade through the Korea Polar Research Institute.

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