A N N A L E S Z O O L O G I C I (Warszawa), 2008, 58(2): 397-402
A NEW SPECIES OF THE GENUS PROCTOPHYLLODES (ANALGOIDEA: PROCTOPHYLLODIDAE) FROM CETTI’S WARBLER CETTIA CETTI (PASSERIFORMES: SYLVIIDAE) WITH DNA BARCODE DATA AGNIESZKA BADEK1*, MIROSLAWA DABERT2, SERGE V. MIRONOV3 and JACEK DABERT4 1
Department of Animal Morphology, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614 Poznan, Poland; e-mail:
[email protected] *Corresponding author 2 Molecular Biology Techniques Laboratory, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614 Poznań, Poland; e-mail:
[email protected] 3 Zoological Institute, Russian Academy of Sciences, Universitetskaya quay 1, 199034, Saint Petersburg, Russia; e-mail:
[email protected] 4 Department of Animal Morphology, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614 Poznan, Poland; e-mail:
[email protected]
Abstract.— A new feather mites species, Proctophyllodes cetti sp. nov., is described from Cetti’s warbler, Cettia cetti (Temminck, 1820) (Sylviidae) from Kazakhstan. The standard morphological description is supplemented by cytochrome subunit oxidase I sequence data (DNA barcode). ± Key words.— Feather mites, Astigmata, COI.
INTRODUCTION The feather mite genus Proctophyllodes Robin, 1877 is the most species-rich genus in the analgoid family Proctophyllodidae. It currently includes over than 150 species, arranged in 12 species groups (Atyeo and Braasch 1966, Gaud and Fain 1990, Mironov and Kopij 1996, Mironov and Galloway 2002). Systematics of Proctophyllodes, including subdivision into species groups and species identification, are based mainly on the structure of the body terminus and genital region in males, while females of this genus are rather monotonous morphologically. Intrageneric relationships between species groups are still unclear. PL ISSN 0003-4541 © Fundacja Natura optima dux doi: 10.3161/000345408X326735
Most known species of the genus Proctophyllodes are commensals of various passeriform birds with only a few confirmed associations with Charadriiformes, Apodiformes, and Piciformes (Mironov and Galloway 2002). The present paper gives the description of one new species from the plumage of Cetti’s warbler Cettia cetti (Temminck, 1820) (Passeriformes, Sylvidae) in the course of the investigation of the feather mite fauna of passerines in Kazakhstan (by SVM). The description is prepared in a new standard of feather mite species description introduced by us, in which the typical morphological diagnosis is accompanied with DNA barcode data.
A. BADEK, M. DABERT, S. V. MIRONOV and J. DABERT
398
MATERIALS
AND METHODS
The material used in the present study was collected from the flight feathers of a living Cetti’s warbler, captured in the course of bird-banding carried out by the Institute of Zoology (Almaty, Kazakhstan Republic) in southern Kazakhstan in October 2007, with the respective permission for parasitological collecting given by the named institute. Total genomic DNA was extracted from mites preserved in 96% ethanol using a non-destructive method as described by Dabert et al. (2008). After DNA extraction the exoskeletons were mounted on microscopic slides. Vouchers, including type material (specimens and corresponding DNA samples) are deposited in the collection of the Faculty of Biology, Adam Mickiewicz University in Poznań, Poland. (AMU), and some paratypes are deposited in the collection of the Zoological Institute, Russian Academy of Sciences. (ZISP), holotype, 2 male and 10 female paratypes – AMU, 2 male and 5 female paratypes – ZISP. Specimens mounted in Faure medium (Evans 1992) were investigated under the light microscope Olympus BX50 with differential interference contrast (DIC) illumination. Drawings were made using a camera lucida drawing attachment. The morphological description follows the descriptive scheme proposed by Atyeo and Braasch (1966). All measurements are given in micrometres. Length of gnathosoma was measured from the distal tips of palpi to the basal margin of subcapitulum. Width of gnathosoma was measured at the widest section of subcapitulum. Idiosoma length was measured from the anterior margin of prodorsum to the posterior end of body excluding terminal hyaline appendages (females) or excluding opisthosomal lamellae (males). Width of idiosoma was measured at the level of setae c2. Chaetotactic nomenclature follows that of Gaud and Atyeo (1996). Latin and English names of birds as well as the higherlevel classification of birds are those of Sibley and Monroe (1990). Genetic analysis of the DNA barcode region was performed as described by Dabert et al. (2008).
TAXONOMY Proctophyllodes cetti Badek, Mironov et J. Dabert sp. nov. (Figs 1–2) Type material. Male holotype, 4 male and 15 female paratypes ex Cettia cetti (Temminck, 1820) (Sylviidae), Kazakhstan, Kyzylkol’ Lake, 43°44’35.1”N, 69°30’06.6”E, 335 m h, SVM-07-1009-11(1), 9 October 2007, leg. S. V. Mironov; voucher AMUFM906-909, DNAbarcode FM909 (Acc. EU371933). Differential diagnosis. The new species belongs to the pinnatus species group, the largest and most
homogenous species group in the genus Proctophyllodes, consisting of about 30 species (Atyeo and Braasch 1966). This group is characterized by the following combination of features: (1) the base of genital organ with heavily sclerotized ring, (2) the genital organ relatively short, directed backward from the base and not extending beyond anal suckers, (3) the genital sheath is strongly thickened basally and attenuate to apex, wedge-shaped or ampulliform, (4) the opisthogastric shield is entire (one pieced), H-shaped, (5) the setae g and ps3 are in trapezoid arrangement and situated on posterior margin of opisthogastric shield, (6) the corolla of anal suckers circular, not notched, (7) the pair of dark-colored sclerites in area of anal suckers (“accessory glands” of Atyeo and Braasch 1966) are absent, (8) paragenital apodemes absent. Within this group, Proctophyllodes cetti sp. nov. belongs to the clavatus species complex characterized by the ampuliform genital sheath and is most closely related to P. clavatus Fritsch, 1961 by having terminal lamellae shorter than 60, posterior ends of opisthogastric shields not extending past the apices of anal suckers and distance from the apex of the genital arch to the level of setae ps1 less than 95 µm. The new species is also close by several mensurative characteristics of genital structures in males to P. occidentalis Atyeo et Braasch, 1966 and P. calamospizae Atyeo et Braasch, 1966 (Tab. 1). The males of Proctophyllodes cetti most clearly differ by having shorter distance g–g and ps3–ps3 (9 and 20 versus 15 and 30, respectively, in P. clavatus), and the genital organ extending beyond the level of setae ps3. Females of the new species and P. clavatus share the following characters: setae h3 long, almost reaching the top of the terminal appendages, and of terminal cleft is doubly concave, hourglass-shaped. The females of Proctophyllodes cetti sp. nov. differ from those of P. clavatus by having a wider terminal cleft (22, versus 17 in P. clavatus) and strongly convex lateral margins of this cleft. The females of the new species differ from two other closely related species, P. occidentalis and P. calamospizae, by having longer setae h3, which are about 3/ of the length of terminal appendages; in the two lat4 ter species, these setae are much shorter, approximately 1/2 the length of terminal appendages, and the terminal cleft has different proportions and form of lateral margins (Table 1). Description. Male (Figs 1A, B) (holotype, measurements for 3 paratypes in brackets): Gnathosoma length 48 (50–52), greatest width 35 (33–35), length/ width 1.4 (1.5), subcapitulum shaped as a transverse rectangle. Idiosoma length 295 (287–288), width 138 (115–120), length/width 2.1 (2.4–2.5). Prodorsal shield: posterior margin almost straight, posterior angles rounded, lateral margins entire with short angular anteriorlateral extensions, length 78 (75–78), greatest width 78
PROCTOPHYLLODES CETTI, A NEW FEATHER MITE SPECIES FROM CETTIA CETTI
399
100
Figure 1. Proctophyllodes cetti sp. nov., male. (A) Ventral view; (B) dorsal view. Designations of setae after Gaud and Atyeo (1996).
(73–75); surface of shield monotonously punctured. Distances between scapular setae: se–se 52 (48–50), si–si 37 (33). Scapular shields narrow. Humeral shield narrow, separated from epimerites III. Hysteronotal shield: anterior margin slightly concave, anterior angles acute, length 162 (158–163), width at anterior margin 83 (78), surface of shield without lacunae. Supranal concavity opened terminally, anterior end reaching level of setae e2. Posterior margin of opisthosoma truncate, slightly convex; terminal lamellae ovate, with pennate venation, not overlapping and separated by a narrow slit; length of the lamellae 53 (50), maximal width 37(37). Subhumeral setae c3 lanceolate, 15 (15–17) long, 5 (3–5) wide. Dorsal setae c2 short, situated on anterior ends of humeral shields. Setae ps1 as long as distance between them. Distances between setae: c1–c1 60 (57–60), c1–d1 33 (32–35), d1–d2 33 (37–38), e1–e1 40 (38–42), h1–h1 42 (42–43), d2–e1 48 (45–47), c2–d2 58 (57), d2–e2 72 (67–70), e1–h1 40 (37–40), e2–h2 30 (28–30).
Epimerites I fused into a narrow U, without lateral extensions. Median tips of epimerites IIIa extending beyond level of setae 3a. Genital arch situated at level of trochanters IV, apex of arch not extending to level of setae 4a, 27 (25–27) in length, 30 (32–37) in width. Genital organ with heavily sclerotized ring at base, directed backward. Genital sheath ampulliform, 38 (38–40) long, 12 (10–12) wide at base, tip of genital sheath reaching to or slightly extending beyond level of setae ps3. Paragenital apodemes absent, genital papillae not connected. Opisthogastric shield H-shaped with anterior ends adjoining tips of genital arch; posterior triangular ends almost reaching by tips the corolla of anal suckers; posterior margin of transverse branch with little circular incision. Bases of setae g and ps3 in trapezoid arrangement and situated on posterior margin of opisthogastric shield, distance g–g 10 (8–10), g–ps3 8 (8), ps3–ps3 20 (18–22), distance from genital arch apex to level of setae ps1 88 (92). Anal suckers cylindrical, 20 (20–22) in length, 7 (8) in width, corolla
400
A. BADEK, M. DABERT, S. V. MIRONOV and J. DABERT
100
Figure 2. Proctophyllodes cetti sp. nov., female. (A) Ventral view; (B) dorsal view.
with 18 (18–19) small teeth. Setae ps2 thickened, 37 (37–38) in length. Female (Figs 2A, B) (15 paratypes): Gnathosoma shaped as in males, length 63–70, width 45–48, length/width 1.4. Length of idiosoma 433–463, width 138–150, length/width 3.1–3.2. Prodorsal shield shaped as in males, length 90–97, width 93–107. Distances between scapular setae: se–se 62–68, si–si 43–48. Scapular shields moderately developed. Humeral shield separated from epimerites III, carrying setae c2 in anterior end. Anterior hysteronotal shield roughly rectangular, with anterior margin concave, length 212–225, width at anterior margin 82–88. Lobar region of opisthosoma distinctly separated by transverse furrow from rest part of hysterosoma, greatest distance between hysteronotal and lobar shields 5–8; length of lobar shield 58–68, width at level of setae h2 78–88. Opisthosomal lobes straight, longer than wide, well
separated from each other by terminal cleft, which is approximately equal in width to the width of one lobe. Lateral margins of terminal cleft strongly convex, anterior margin slightly convex, length 45–50, width at level of setae ps1 17–27. Subhumeral setae c3 lanceolate, 20 long, 3–5 wide. Setae h1 set on soft tegument between anterior hysteronotal and lobal shields. Setae h2 lanceolate with filiform distal part, setae h3 60–73 long, about 3/4 of terminal appendages. Distances between setae: c1–c1 63–68, c1–d1 50–58, d1–d2 40–42, e1–e1 57–60, h1–h1 23–25, d2–e1 67–78, c2–d2 75–80, d2–e2 110–115, e2–h2 47–53, h2–h3 28–38. Epimerites shaped as in males. Epigynum semicircular, with acute tips, not extending to level of genital papillae, width 55–62, length 33–47. Opisthosomal lobes with ventral translobar apodemes. Genital setae g anterior level of setae 3b.
PROCTOPHYLLODES CETTI, A NEW FEATHER MITE SPECIES FROM CETTIA CETTI
401
Table 1. Main differential characters between Proctophyllodes cetti sp. nov. and most similar species of the pinnatus species group. Data for P. clavatus, P. occidentalis and P. calamospizae derived from Atyeo and Braasch (1966).
Characters
P. cetti sp. nov.
P. clavatus
P. occidentalis
P. calamospizae
Male Relation of aedeagus of tip and the transverse level of setae ps3
extending posteriorly
reaching
reaching
extending posteriorly
Posterior tips of opisthogastric shields and anal suckers
not reaching the apex of suckers
reaching the apex of suckers
extending past the apex of suckers
extending past the apex of suckers
Opisthosomal lamellae
separated
overlapping
separated
separated
Length of opisthosomal lamellae
51 µm
43 µm
59 µm
60 µm
Length of anal suckers
21 µm
18 µm
24 µm
29 µm
Width of anal suckers
8 µm
8 µm
9 µm
7 µm
2.6
2.3
2.7
4.1
Distance between setae g-g
9 µm
15 µm
14 µm
12 µm
Distance between setae ps3–ps3
20 µm
30 µm
32 µm
24 µm
Distance from apex of genital arch to setae ps1
90 µm
92 µm
102 µm
100 µm
Aedeagus length
50 µm
46 µm
54 µm
55 µm
3/4
3/4
1/2
1/2
Terminal cleft length
47 µm
45 µm
52 µm
50 µm
Terminal cleft width
22 µm
17 µm
38 µm
21 µm
2.1
2.6
1.4
2.4
Strongly convex
Slightly convex
Straight, divergent posterior
Slightly convex
L/W ratio of anal suckers
Female Ratio of length of setae h3 to terminal appendages
Ratio of terminal cleft length to width Lateral margin of terminal cleft
DNA barcode. We amplified and sequenced a 644 bp fragment of the cytochrome oxidase subunit I (COI) gene (DNA barcode region chosen by the Consortium for the Barcode of Life, http://barcoding.si.edu) for 1 male holotype, 4 male and 13 female paratypes (Acc. EU371933). Intraspecific K2P divergence in Proctophyllodes cetti sp. nov. was 0.87%. All observed nucleotide substitutions were synonymous and did not change the amino acid sequence. This observed genetic distance in the nucleotide sequence of the DNA barcode is comparable to the majority of currently recognized species (Hebert et al. 2003). Etymology. The specific epithet is derived from the specific name of host, and is a noun in opposition. Remark. In is necessary to notice that Dubinina and Kulakova (1960) mentioned Proctophyllodes cettioides Dubinin (in litt.) from the Cetti’s warbler in
the delta of the Volga river. It is quite probably that these authors recorded on this host the same mite species as described above; however P. cettioides actually retained undescribed, and this name is a nomen nudum.
ACKNOWLEDGEMENTS The new species is dedicated to Prof. Czesław Błaszak, an outstanding Polish acarologist. The present study was supported (for AB) by the grant of the Faculty of Biology, Adam Mickiewicz University in Poznan (PBWB 704/2006) and in part (for SVM) by the Russian Foundation for Basic Research (07-04-00426).
402
A. BADEK, M. DABERT, S. V. MIRONOV and J. DABERT
REFERENCES Atyeo, W. T. and N. L. Braasch. 1966. The feather mite genus Proctophyllodes (Sarcoptiformes: Proctophyllodidae). Bulletin of the University of Nebraska State Museum, 5: 1–354. Dabert, J., Ehrnsberger, R. and M. Dabert. 2008. Glaucalges tytonis sp. nov. (Analgoidea: Xolalgidae) from the barn owl Tyto alba (Strigiformes: Tytonidae): compiling morphology with DNA barcode data for taxa descriptions in mites (Acari). Zootaxa, 1719: 41–52. Dubinina, M. N. and A. P. Kulakova. 1960. Materials of parasitofauna of Passeriformes in the delta of the Volga river. Parazitologicheskii Sbornik, 19: 344–372. (In Russian). Evans, G. O. 1992. Principles of acarology. CAB International, Wallingford. Gaud, J. and W. T. Atyeo. 1996. Feather mites of the world (Acarina, Astigmata): The supraspecific taxa. Annales du Musée royale de l’Afrique centrale, Série in-80, Sciences zoologiques 277: (Part I, Text) 1–193, (Part II, Illustrations of feather mite taxa): 1–436.
Gaud, J. and A. Fain. 1990. Deux espèces nouvelles d’Acariens plumicoles du genre Proctophyllodes (Analgoidea, Proctophyllodidae) parasites de Passériformes africains de la famille Pycnonotidae. Bulletin de l’Institut royal des Sciences naturelles de Belgique, Entomologie, 60: 133–138. Hebert, P. D., Cywinska, A., Ball, S. L. and J. R. de Waard. 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society of London, Series B–Biological Sciences, 270: 313–321 Mironov, S. V. and T. D. Galloway. 2002. New feather mite taxa (Acari: Analgoidea) and mites collected from native and introduced birds of New Zealand. Acarologia, 42: 185–201. Mironov, S. V. and G. Kopij. 1996. Three new species of the feather mite family Proctophyllodidae (Acarina: Analgoidea) from some South African passerines (Aves: Passeriformes). Acarina, 4(1/2): 27–33. Sibley, C. G. and B. L. Jr. Monroe. 1990. Distribution and taxonomy of birds of the world. New Haven, USA: Yale University Press.
Received: January 15, 2008 Accepted: February 25, 2008
