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Research Article
A new feather mite species of the genus Proterothrix Gaud, 1968 (Acarina, Proctophyllodidae) from the Large Niltava, Niltava grandis (Passeriformes, Muscicapidae) – an integrative description
expand article infoIoana Cristina Constantinescu, Oana Paula Popa§, Luis Ovidiu Popa§, Ioana Cobzaru|, D. Khlur B. Mukhim, Costică Adam§
‡ “Grigore Antipa” National Museum of Natural History, Bucharest, Romania
§ ”Grigore Antipa” National Museum of Natural History, Bucharest, Romania
| Institute of Biology, Romanian Academy, Bucharest, Romania
¶ Zoology Department, Lady Keane College, Shillong, India
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Abstract

A new species of the feather mite genus Proterothrix (Proctophyllodidae: Pterodectinae) is described from the Large Niltava Niltava grandis (Blyth) (Passeriformes, Muscicapidae) in northeast India (Meghalaya, Jaintia Hills, Shnongrim village). Proterothrix chachulae Constantinescu, sp. n. differs from all known species of the genus by having in males the aedeagus with bilobate tip. The morphological description is supplemented with molecular characterisation of a fragment f near the 5` terminus of the mitochondrial COI gene.

Keywords

Taxonomy, feather mite, new species, Pterodectinae, Proterothrix

Introduction

The bird genus Niltava Hodgson belongs to the family of Old World Flycatchers (Passeriformes: Muscicapidae), currently includes six valid species and is distributed in Indo-Malayan biogeographic region (Clements et al. 2016). Feather mites were previously recorded only in two of these species: Analges sp., Anisodiscus sp., Mesalgoides sp., Proctophyllodes cotyledon Trouessart, 1899, Bicentralges distinctus Orwig, 1968, Proterothrix sp., and Trouessartia sp. ex Niltava grandis (Blyth); Analges sp., Proctophyllodes elegans Atyeo and Braasch, 1966, Proterothrix sp., Therisalges sp., Trouessartia sp., and Xolalges sp. ex Niltava sundara Hodgson (Atyeo 1973; Atyeo and Braasch 1968; Orwig 1968). An unidentified Proterothrix species, reported by Atyeo (1973) from Niltava grandis in Asia is a potentially a new species, but has never been described. In this paper we describe a new species of Proterothrix collected from N. grandis grandis in Meghalaya (Northeast India).

The genus Proterothrix Gaud, 1968 (Proctophyllodidae: Pterodectinae) includes 28 species known exclusively from the Old World (Ethiopian, Oriental and Australasian regions) (Hernandes and Valim 2014). In the Oriental region, the genus appears to be one of the most widespread proctophyllodid genera, with 13 described species (from Malaysia, Taiwan, China, Vietnam and India) and 56 potentially new species recorded by Atyeo (1973), but never described elsewhere.

Species of the genus Proterothrix have been identified to date on birds from the orders Coraciiformes (Alcedinidae) and Passeriformes (Dicruridae, Eurylaimidae, Leiothrichidae, Monarchidae, Muscicapidae, Paradisaeidae, Paradoxornithidae, and Pellorneidae). According to modern concepts, this genus, along with seven more genera belongs to the “Phroterothrix generic group” incorporating archaic pterodectines with setae ps3 anterior to adanal suckers in males (Mironov and Proctor 2009, Hernandes and Valim 2014). Twenty six out of the 28 species were arranged in three species groups: megacaula (3 species), schizothyra (4 species) and wolffi (19 species) (Gaud 1952, 1962, 1968, 1979, Mironov et al. 2008, 2010, 2012, Mironov and Proctor 2009, Mironov and Tolstenkov 2013, Constantinescu et al. 2014). The new species of Proterothrix described herein belongs to the wolffi species group, in having almost closed coxal fields III in males and parallel-sided terminal cleft in females.

Materials and methods

The material used in the present paper was collected in Shnongrim (Meghalaya, India) in January 2014. The birds were captured using mist–nets, identified and visually checked for the presence and collection of mites and released back to the wild. Mite specimens were collected manually with a needle and placed in tubes with 96% ethanol. Later, in laboratory conditions, mite specimens were cleared in 90% lactic acid for 24 hours, and mounted on microscope slides in Hoyer’s medium. Drawings were made using an Olympus CX21 microscope, with a camera lucida drawing device. The bird specimens were identified according to Rasmussen and Anderton (2012) and Grimmett et al. (2011), and the taxonomy of birds follows Clements et al. (2016). The body setation of mites follows that of Griffiths et al. (1990) with the modifications by Norton (1998) concerning coxal setae, while the setation of legs follows Gaud and Atyeo (1996). The description of the new species of Proterothrix is given according to the current format used for species of pterodectine mites (Mironov and Fain 2003, Mironov 2006, Valim and Hernandes 2006, Mironov et al. 2008) and the measuring techniques of particular structures used were described by Mironov and Proctor (2009).

The full set of measurements is given for a holotype (male) and a range of measurements for corresponding paratypes. All measurements are in micrometers (μm). The holotype and paratypes of the new species are deposited in the Acarological Collection of the “Grigore Antipa” National Museum of Natural History, Bucharest, Romania (inventory numbers are given in brackets for all type specimens).

Three paratype specimens of Proterothrix chachulae sp. n. (two males ANA747, ANA748 and one female ANA749) were used to isolate DNA using DNAeasy Tissue Kit (Qiagen). All three specimens used for molecular analyses were mounted and kept as reference vouchers for morphological examination. The specimens preserved in ethanol 96% were transferred in 180μl ATL Buffer with 20 μl of Proteinase K and incubated overnight at 56ºC on a shaking thermoblock. After 24h, 5μl of Proteinase K were added and incubation was continued until 72h. For the rest of the protocol we followed the manufacturer specifications and the modification suggested by Dabert et al. (2008).

The 663bp fragment near the 5` terminus of the COI gene was used as DNA barcode region, amplified by PCR with the degenerate primers bcdF05 (5`- TTTTCTACHAAYCATAAAGATATTGC-3`) and bcdR04 (5`- TATAAACYTCDGGATGNCCAAAAAA-3`), according to Dabert et al. (2008). The PCRgenotyping reaction was performed in a 50 μL total volume containing DNA template, 1X Green GoTaq® Flexi Buffer, 2.5 mM MgCl2, each dNTP at 0.1 mM, each primer at 0.5 μM (the primers were M13 tailed) and 1.5 units of GoTaq® DNA polymerase (5U/μl) (Promega, Madison, USA). The PCR products were isolated from samples containing visible bands and sent for sequencing to Macrogen (Seoul, Korea).

Sequence chromatograms were edited and assembled with CodonCode Aligner version 3.7.1. Pairwise distances between sequences were computed with MEGA version 6 (Tamura et al. 2013) using K2P distance model (Kimura 1980). DnaSP v5 was used to obtain data about the genetic polymorphism in the studied specimens (Librado and Rozas 2009).

Results

Family Proctophyllodidae Trouessart et Mégnin, 1884

Subfamily Pterodectinae Park et Atyeo, 1971

Genus Proterothrix Gaud, 1968

Proterothrix chachulae Constantinescu, sp. n.

Figs 1, 2, 3, 4, 5, 6

Type material

Male holotype (ANA672), 6 male (ANA671, ANA673, ANA674, ANA675, ANA747(P2♂), ANA748(P1♂)) and 6 female (ANA676, ANA677, ANA678, ANA679, ANA680, ANA749(P1♀) paratypes, 27.01.2014, from the Large Niltava Niltava grandis grandis (Blyth) (Passeriformes, Muscicapidae); INDIA: Meghalaya, Jaintia Hills, Shnongrim village, (25°21'12.36"N, 92°31'3.06"E); 1151 m; subtropical forest; collector D. K. B. Mukhim.

Description

MALE (Figs 1; 2; 3; holotype, range for 6 paratypes in parentheses): Pseudorutellar lobes with long and acute lateral extensions. Length of idiosoma 284 (284–288), width 104 (104–109), length of hysterosoma 184 (190–192). Prodorsal shield entire, anterolateral extensions short and with acute tips, lateral margins without incisions, posterior margin with wide blunt-angular extension, posterior angles well expressed, length 96 (94–96), width 82 (82–88), surface with ovate lacunae (Fig. 1). Scapular setae se separated by 36 (35–42). Scapular shields narrow. Humeral shields narrow, separated from outer sclerotized areas of epimerites III. Setae cp situated ventrally, setae c2 filiform, situated dorsally, both pairs on striated tegument. Subhumeral setae c3 lanceolate, 18 (18–20) × 6 (6–8). Hysteronotal shield with anterior margin concave, anterior angles rounded, distance from anterior margin to bases of setae h3 174 (180–186), greatest width in anterior part 74 (72–80), surface with small circular lacunae. Opisthosomal lobes roughly trapezoidal, short, each with angular median expansion on posterior margin, setae h3 situated slightly posterior to setae h2. Terminal cleft V–shaped, 16 (16–20) in length; margins of terminal cleft without membranes. Supranal concavity clearly outlined, triangular. Setae f2 slightly posterior to bases of setae ps2. Setae h1 near lateral margins of opisthosoma. Setae ps1 filiform, length 6 (5–8), situated near lateral margins of opisthosomal lobes, anterior to bases of setae h3. Setae c1 present, setae h3 flattened and enlarged in basal part, shorter than h2. Dorsal measurements: c2d2 68 (64–68), d2e2 70 (72–78), e2h3 42 (40–46), d1d2 33 (31–34), e1e2 24 (20–26), h1ps2 10 (7–11), h2h2 36 (34–36), h3h3 20 (20–22), ps2ps2 44 (46–48).

Figure 1.

Proterothrix chachulae sp. n., male holotype: dorsal view of idiosoma.

Epimerites I fused into a V, posterior end connected with epimerites II by transverse sclerotized bands. Epimerites II long, with posterior ends free. Coxal field I closed, coxal field II open, coxal fields III almost closed, coxal fields IV with narrow sclerotized areas at bases of trochanters IV. Epimerites IVa present, well developed, their anterior tips bearing bases of setae 4a (Fig. 2). Genital arch 12 (8–10) long, 18 (14–18) wide, basal sclerite of genital apparatus rounded posteriorly; aedeagus with bilobate tip 64 (64–69) long, extending to level of setae ps3. Genital papillae situated at level of genital arch. A pair of small ovoid sclerites located near tips of genital arch. Two pairs of adanal shields (median and anterolateral) represented by small triangular plates, setae ps3 situated on median pairs. Anal suckers 12 (11–12) in diameter, corolla indented, with 8 small teeth. Ventral measurements: 3a4b 20 (18–22), 4b4a 30 (28–30), 4ag 30 (27–32), gps3 36 (37–40), ps3ps3 17 (16–18), ps3h3 36 (36–40).

Figure 2.

Proterothrix chachulae sp. n., male holotype: ventral view of idiosoma.

Legs I longer than legs II, femora I and II with ventral crest (Fig. 3A, B). Seta e of tarsus I filiform. Setae mGII thickened basally, with filiform apex, setae d of tarsi II, III much shorter than corresponding setae f. Tarsus IV 23 (22–24) long, with apical claw-like process, setae d, e button-like, seta d bigger in diameter than e, situated in basal and apical parts of segment, respectively (Fig. 3D). Length of solenidia: ω1I 10 (10–14), ω1II 9 (8–10), φI 56 (54–60), φII 46 (42–44), φIII 25 (22–26), φIV 22 (18–20).

Figure 3.

Proterothrix chachulae sp. n., A–D details of male legs, dorsal view: A leg I B leg II C leg III D leg IV E opisthosoma of male, ventral view.

FEMALE (Figs 4; 5; 6A–E; range for 6 paratypes): Pseudorutellar lobes with long and acute lateral extensions as in males. Length of idiosoma 392–396, width 125–132, and length of hysterosoma 270–280. Prodorsal shield entire, anterolateral extensions with rounded tips, lateral margins without deep incisions, posterior margin almost straight, length 117–121, width 107–110, surface with small circular lacunae in anterior part and bigger ovate and circular lacunae in posterior part (Fig. 4). Scapular setae se separated by 43–46. Scapular shields narrow. Humeral shields narrow, separated from epimerites III. Setae c2 filiform, situated dorsally on striated tegument. Subhumeral setae c3 lanceolate, 18–22 × 6–8. Anterior hysteronotal shield roughly rectangular, anterior and posterior margins concave, greatest length 189–190, greatest width in anterior part 99–101, surface with sparsely disposed circular lacunae. Length of lobar region 74–79, width at level of setae h2 63– 65. Terminal cleft parallel-sided, narrow, with almost touching margins posterior to level of setae ps1, length 45–52. Supranal concavity well developed, ovoid. Setae h1 on lobar shield, at midlevel of supranal concavity; surface of lobar shield without ornamentation. Setae h2 spindle-shaped, with terminal filament, 73–81 × 6–8. Setae ps1 closer to inner margin of opisthosomal lobes, setae h3 17–18 long, about 1/3 from the length of terminal appendages. Dorsal measurements: c2d2 83–84, d2e2 99–105, e2h2 44–47, h2h3 32–35, d1d2 34–47, e1e2 40–42, h1h2 28–32, h2ps1 26–30, h1h1 29–31, h2h2 49–51.

Figure 4.

Proterothrix chachulae sp. n., female paratype: dorsal view of idiosoma.

Epimerites I fused as a V, with short lateral extensions. Coxal fields I, II with small sclerotized areas, epimerites IVa absent (Fig. 5). Translobar apodemes of opisthosomal lobes present, fused to each other anterior to terminal cleft. Epigynum horseshoe-shaped, greatest width 49–53. Secondary spermaducts short, about 10 long (Fig. 6E). Distance between pseudanal setae: ps2ps2 20–23, ps3ps3 16–18, ps2ps3 16–20.

Figure 5.

Proterothrix chachulae sp. n., female paratype: ventral view of idiosoma.

Legs I slightly longer than legs II; femora I, II with wide ventral crest; setae mGII thickened basally, with filiform apex. Length of solenidia: ω1I 9–11, ω1II 6–9, φI 59–67, φII 46–48, φIII 30–35, φIV 5–7 (Fig. 6A–D).

Figure 6.

Proterothrix chachulae sp. n., A–D details of female legs, dorsal view: A leg I B leg II C leg III D leg IV E spermatheca and spermaducts of female. Abbreviations: hs–head of spermatheca; pd–primary spermaduct; sd–secondary spermaduct.

Etymology

This species is named in honor of Oana Mirela Chachula (a biologist, the National Museum of Romanian History, Romania), for her support of our research of ectoparasites of birds from Meghalaya (India).

Remarks

Proterothrix chachulae sp. n. belongs to the wolffi species group by having almost closed coxal fields III in males and parallel-sided terminal cleft in females. Males of the new species differ from all known males of the genus by having the aedeagus with bilobate tip. Among all species of the genus, P. chachulae is closely related to P. cyornis Mironov and Tolstenkov, 2013 from Cyornis tickelliae Blyth (Passeriformes: Muscicapidae) by having the pseudorutelar lobes with acute lateral extensions in both sexes. Males of both species have the opisthosomal lobes roughly trapezoidal and short, setae h3 flattened and enlarged in basal part, a similar general proportions of aedeagus and epimerites IVa well developed, their anterior tips bearing bases of setae 4a. Proterothrix chachulae differs from that species by the following features: in males, the prodorsal shield has posterior margin with wide blunt-angular extension, the opisthosomal lobes have angular median expansion on posterior margin, a pair of small ovoid shields is located at the tips of the genital arch, seta d is bigger in diameter then e on tarsus IV; in females, the prodorsal shield bears in anterior part a few small circular lacunae, the lobar shield is without ornamentation, and the setae h3 have about 1/3 from the length of terminal appendages. In males of P. cyornis, the prodorsal shield has posterior margin slightly convex, the opisthosomal lobes have posterior margin with a small median invagination, small sclerites near the tips of genital arch are absent, seta d and e on tarsus IV are subequal in diameter; in females, the prodorsal shield bears big ovate lacunae in anterior part, the lobar shield bears few circular lacunae in anterior part, and the setae h3 have about 1/5 from the length of terminal appendages.

DNA barcode

Representative DNA sequences. GenBank accession numbers for molecular voucher: ANA747 P2 male KY594726; ANA748 P1 male KY594724; ANA749 P1 female KY594725.

We sequenced a 660-pb fragment of the mitochondrial cytochrome c oxidase subunit I (COI) gene for two male and one female paratypes. In the resulted alignment we identified 8 variable sites. Two haplotypes were identified: H1 (ANA_748_P1_M and ANA_749_P1_F) and H2 (ANA_747_P2_M).

Intraspecific genetic distance between the analyzed specimens using K2P model is 0.8% (SE 0.3). All observed nucleotide substitutions were synonymous and did not change the amino acid sequence.

This reported genetic distance in the nucleotide sequence of the DNA barcode is comparable with genetic distances found for other Analgoidea species like Proctophyllodes cetti (0.87%) (Badek et al. 2008).

Acknowledgments

We are grateful to the Additional Principal Chief Conservator of Forests, Wildlife & Chief Wildlife Warden from Shillong (Meghalaya, India) for the permission to catch birds (permission No. FWC.G/173/Pt.). We would like to thank Dr. Laura Mihaela Ștefan for her valuable advice regarding the DNA isolation and to our proofreader, D Ana Wetzl (Assistant Professor of English, Kent State University at Trumbull, USA). Ioana Cobzaru was supported by the Institute of Biology Bucharest of Romanian Academy (project no. RO1567–IBB04/2016).

References

  • Atyeo WT (1973) Feather mites. Pp. 54–78. In: McClure HE and Ratanaworabhan N (Eds), Some ectoparasites of the birds of Asia. Jintana Printing Ltd. , Bangkok, Thailand, 219 pp.
  • Atyeo WT, Braasch L (1966) The feather mite genus Proctophyllodes (Sarcoptiformes: Proctophyllodidae). Bulletin of the University of Nebraska State Museum 5: 1–354.
  • Badek A, Dabert M, Mironov SV, Dabert J (2008) A new species of the genus Proctophyllodes (Analgoidea: Proctophyllodidae) from Cetti’s Warbler Cettia cetti (Passeriformes: Sylviidae) with DNA barcode data. Annales Zoologici 58(2): 397–402. https://doi.org/10.3161/000345408X326735
  • Constantinescu IC, Chişamera G, Mukhim DKB, Adam C (2014) Three new species of feather mite of the genus Proterothrix Gaud, 1968 (Analgoidea: Proctophyllodidae: Pterodectinae) from passerines in Meghalaya, North East India. Systematic Parasitology 89: 45–58. https://doi.org/10.1007/s11230-014-9508-1
  • Dabert J, Ehrnsberger R, Dabert M (2008) Glaucalges tytonis sp. n. (Analgoidea, Xolalgidae) from the barn owl Tyto alba (Strigiformes, Tytonidae): compiling morphology with DNA barcode data for taxon descriptions in mites (Acari). Zootaxa 1719: 41–52.
  • Gaud J (1952) Sarcoptides plumicoles des oiseaux de Madagascar. Mémoires de L'Institut scientifique de Madagascar 7(1): 81–107.
  • Gaud J (1962) Sarcoptiformes plumicoles (Analgesoidea) parasites d'oiseaux de I'Ile Rennell. The Natural History of Rennell Island, British Solomon Islands 4: 31–51.
  • Gaud J (1968) Sarcoptiformes plumicoles (Analgoidea) parasites d'oiseaux de I'Ile Rennell. The Natural History of Rennell Island, British Solomon Islands 5: 121–151.
  • Gaud J (1979) Sarcoptiformes plumicoles des oiseaux Coraciiformes d'Afrique. II. Parasites des Alcedinidae. Revue de Zoologie Africaines 93: 245–266.
  • Gaud J, Atyeo WT (1996) Feather mites of the world (Acarina, Astigmata): the supraspecific taxa. Annalen Zoologische Wetenschappen, Musée Royal de L'Afrique Centrale, Annales Sciences Zoologiques 277: 1–191.
  • Grimmett R, Inskipp C, Inskipp T (2011) Helm Field Guides: Birds of the Indian Subcontinent. Christopher Helm, London, 528 pp.
  • Hernandes FA, Valim MP (2014) On the identity of two species of Proctophyllodidae (Acari: Astigmata: Analgoidea) described by Herbert F. Berla in Brazil, with a description of Lamellodectes gen. nov. and a new species. Zootaxa 3794(1): 179–200. https://doi.org/10.11646/zootaxa.3794.1.8
  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111–120. https://doi.org/10.1007/BF01731581
  • Mironov SV (2006) Feather mites of the genus Montesauria Oudemans (Astigmata: Proctophyllodidae) associated with starlings (Passeriformes: Sturnidae) in the Indo- Malayan region, with notes on systematic of the genus. Acarina 14(1): 21–40.
  • Mironov SV, Diao W, Zhang Y, Zhang C, Yan Z (2008) A new mite species of the genus Proterothrix Gaud (Astigmata, Proctophyllodidae) from Ficedula zanthopygia (Hay) (Passeriformes: Muscicapidae) in China. Acarina 16: 31–38.
  • Mironov SV, Fain A (2003) New species of feather mite subfamily Pterodectinae (Astigmata: Proctophyllodidae) from African passerines (Aves: Passeriformes). Bulletin et Annales de la Societe Royale Belge d'Entomologie 139: 75–91.
  • Mironov SV, Proctor HC (2009) Feather mites of the genus Proterothrix Gaud (Astigmata: Proctophyllodidae) from parrotbills (Passeriformes: Paradoxornithidae) in China. Journal of Parasitology 95: 1093–1107. http://dx.doi.org/10.1645/GE-1961.1
  • Mironov SV, Tolstenkov OO (2013) Three new feather mites of the subfamily Pterodectinae (Acari: Proctophyllodidae) from passerines (Aves: Passeriformes) in Vietnam. Proceedings of Zoological Institute of Russian Academy of Sciences 317(1): 11–29.
  • Mironov SV, Literak I, Čapek M (2008) New feather mites of the subfamily Pterodectinae (Acari: Astigmata: Proctophyllodidae) from passerines (Aves: Passeriformes) in Mato Grosso do Sul, Brazil. Zootaxa 1947: 1–38.
  • Mironov SV, Literak I, Čapek M, Koubek P (2010) New species of the feather mite subfamily Pterodectinae (Astigmata, Proctophyllodidae) from passerines in Senegal. Acta Parasitologica 55(4): 399–413. https://doi.org/10.2478/s11686-010-0051-1
  • Mironov SV, Literak I, Hung MN, Čapek M (2012) New feather mites of the subfamily Pterodectinae (Acari: Proctophyllodidae) from passerines and woodpeckers (Aves: Passeriformes and Piciformes) in Vietnam. Zootaxa 3440: 1–49.
  • Orwig KR (1968) The genera and species of the feather mite subfamily Trouessartiinae except Trouessartia (Acarina: Proctophyllodidae). Bulletin of the University of Nebraska State Museum 8: 1–187.
  • Park CK, Atyeo WT (1971) A generic revision of the Pterodectinae, a new subfamily of feather mites (Sarcoptiformes: Analgoidea). Bulletin of the University of Nebraska State Museum 9(3): 40–88.
  • Rasmussen PC, Anderton JC (2012) Birds of South Asia. The Ripley Guide. Volumes 1 and 2. Second Edition. National Museum of Natural History – Smithsonian Institution, Michigan State University and Lynx Edicions, Washington, D.C., Michigan and Barcelona, vol. 1: 684 pp., vol. 2: 378 pp.
  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729. https://doi.org/10.1093/molbev/mst197
  • Valim MP, Hernandes FA (2006) Redescription of four species of the feather mite genus Pterodectes Robin, 1877 (Acari: Proctophyllodidae: Pterodectinae) described by Herbert F. Berla. Acarina 14: 41–55.