Acuaria europaea, Yasen Mutafchiev & Jean Mariaux & Boyko B. Georgiev, 2017

Yasen Mutafchiev, Jean Mariaux & Boyko B. Georgiev, 2017, Description of Acuaria europaea n. sp. (Spirurida: Acuariidae) from Dendrocopos syriacus (Hemprich & Ehrenberg) and Oriolus oriolus (L.) (Aves) in Europe, with results of re-examination of related European species of Acuaria Bremser, 1811, Systematic Parasitology 94, pp. 201-214 : 202-208

Acuaria europaea n. sp.

Type-host: Dendrocopos syriacus (Hemprich & Ehrenberg) ( Piciformes : Picidae ).

Other host: Oriolus oriolus (L.) ( Passeriformes : Oriolidae ).

Type-locality: Plovdiv, Bulgaria (42 11 0 18.59 0 0N, 24 45 0 2.65 0 0E).

Site in host: Under the koilin lining of the gizzard. Intensity: 1 male and 2 females.

Type-material: Holotype: ZMB ‘‘Vermes’’ E.7576 (1 male). Paratypes: ZMB ‘‘Vermes’’ E.7577 (one entire female) and IBER-BAS N001.119 (anterior end and region of the vulva of a single female).

Other material: Ex Oriolus oriolus , IBER-BAS N000.645 (1 female); IBER-BAS N000.978 (1 female); MNHN 135E (1 female).

Representative DNA sequence: GenBank KX353874 (cox 1).

Etymology: The name of the new species reflects its known geographical range.

Description ( Figs. 1 , 2 , 3 )

General. [Based on specimens from Dendrocopos syriacus .] Medium-sized acuariid nematode. Anterior end with 2 triangular pseudolabia, each bearing single amphid and one pair of papillae ( Fig. 1A ). Cordons arise dorsally and ventrally between pseudolabia, extend posteriorly in longitudinal direction just beyond junction of muscular and glandular oesophagus ( Fig. 1A–C ); each cordon consists of 2 rows of cuticular plates, approximately two times wider than long, delimiting longitudinal groove ( Fig. 2B, C ). Deirids small ( Fig. 2A ), c. 1 long, situated at level of nerve-ring ( Fig. 1B ). Buccal cavity elongate, with fine annulations. Excretory pore posterior to nerve-ring. Nerve-ring situated at anterior portion of muscular oesophagus. Phasmids subterminal ( Fig. 1D, H ).

Male. Body length 8.84 mm. Maximum width 154 at level of glandular oesophagus. Tail 210 long. Body width at level of cloaca 76. Cordons 730 long, up to c.10 wide; plates up to 4–5 wide and c. 2 long, reducing their size in posterior quarter of cordons. Deirids and excretory pore at 172 and 277, respectively, from anterior end. Cuticle up to 10 thick; distance between cuticular annulations at mid-body c. 6–7 apart. Buccal cavity 143 long, 11 wide. Muscular oesophagus 438 long, maximum width 50 at posterior portion. Glandular oesophagus 1,407 long, maximum width 92 at level of middle and posterior third. Nerve-ring at 172 from anterior extremity. Testis reflection at 121 posterior to oesophago-intestinal junction. Caudal alae relatively broad, 462 long. Caudal papillae: 4 subventral precloacal pairs and single median papillae near cloaca, postcloacal papillae composed of 5 and 6 papillae on right and left side, respectively ( Fig. 1D, G ). Left spicule 297 long ( Fig. 1F ). Right spicule 155 long ( Fig. 1E ).

Female. Body length 24.64 mm. Maximum body width 242 at level of glandular oesophagus. Body width at level of vulva 227, at level of anus 111. Tail 202 long, strongly curved ventrally. Cordons 1,270 long, up to 17 wide. Plates up to 6–7 wide and c.3 long, reducing their size in posterior quarter of cordons. Deirids and excretory pore at 272 and 315, respectively, from anterior extremity. Cuticle up to 15 thick. Distance between cuticular annulations up to 6–7 apart; along lateral midlines cuticular ornamentation in form of single row of plates, c. 400 long, extending posterior of deirids ( Fig. 2D, E ). Buccal cavity 209 long, 18 wide. Muscular oesophagus 701 long, maximum width 66, at posterior portion. Glandular oesophagus 2,035 long, maximum width at posterior half. Nerve-ring at 237 from anterior extremity. Vulva situated at 11.21 mm from anterior extremity; vulvar region protruding without distinct cuticular ornamentation ( Fig. 1I ). Ovejector posteriorly directed 1,240 long ( Fig. 1J ). Uteri two, with narrow terminal parts c. 900 long, lined with epithelium consisting of tall, narrow cells. Eggs oval, 34–35 9 20–21 (n = 10), containing fully-developed embryo ( Fig. 1K ).

Molecular data

A 646 bp fragment of the COI gene was amplified (GenBank KX353874 ). The nucleotide and translated protein sequences were compared to two other acuariid species available, namely Proyseria petterae Mutafchiev, Mariaux & Georgiev, 2014 (87% nucleotide and 93% protein similarity; GenBank KJ995862 ; Mutafchiev et al., 2014) and Stammerinema hyalinum (von Linstow, 1890) (85% nucleotide and 88% protein similarity; GenBank KP059294 ; Mutafchiev et al., 2015).

Observations on females from Oriolus oriolus

Main metrical data for these specimens are presented in Table 1 ; see also Fig. 3 . The general morphology of these females corresponds to that of the specimens from Dendrocopos syriacus in the shape of the pseudolabia, the opening of the excretory pore, the position of the nerve-ring, the length and structure of the cordons, the position and the shape of the deirids and the morphology of the buccal cavity and the muscular and glandular oesophagus ( Fig. 3A ). They have also a similar single row of plates, 500–600 long, along the lateral midlines and beginning just posterior to the deirids; the vulvar region is protruding, without distinct cuticular ornamentation and the tail is strongly curved ventrally ( Fig. 3C ). Uteri are full with unfertilized eggs only ( Fig. 3B ).

Remarks

The relative length of the cordons and their detailed structure i.e. shape and size of the plates have been shown to be species specific and to be of importance for the taxonomy of the genus Acuaria (see Williams, 1929; Baruš & Garrido, 1968; Mawson, 1972; Mutafchiev et al., 2012, 2013).

Acuaria parorioli Chabaud & Petter, 1961 was described on the basis of one male and one female designated as holotype and allotype, respectively, collected from a single Oriolus oriolus L. in France ( Chabaud & Petter, 1961). The male and the female were described with markedly different cordon lengths, 220 and 1,200 lm, respectively. Our reexamination of the type-specimens confirms the recorded differences between the lengths of the cordons of the male and the female. In addition, the plates of the cordons of the male are irregular in shape, while those of the female are rectangular. These differences of the length and structure of the cordons and the absence of fertilized eggs in the uterus of the female suggest that the male and the female in the type-series of A. parorioli are not conspecific.

The comparison of the female nematode reported as Acuaria anthuris ( Rudolphi, 1819) from Oriolus oriolus by Petrova (1974), the female paratype (‘‘allotype’’) of A. parorioli and the newly reported female from the same host in Bulgaria demonstrates that they exhibit similar morphology, which also corresponds well to the female of A. europaea n. sp. from Dendrocopos syriacus . Therefore, we identified them as A. europaea n. sp.

Smogorzhevskaya (1990) identified A. parorioli from two females collected from O. oriolus in the Ukraine, which were characterised by short cordons, 315 lm long.

Gendre (1912) described Acuaria gracilis ( Gendre, 1912) from Dicrurus adsimilis (Bechstein) (= Buchanga atra adsimilis ) ( Passeriformes : Dicruridae ) and Oriolus auratus Vieillot in Benin. The species, in its original description, was characterised by males having cordons 220 lm long and left and right spicules 150 and 120 lm long, respectively, as well as females possessing cordons 380 lm long and a tail curved dorsally. Gendre (1912) specified that the male from O. auratus had the same morphology as that from D. adsimilis except for the number of postcloacal papillae (7 vs 6 pairs). Chabaud & Petter (1961) considered that difference significant and described Acuaria orioli Chabaud & Petter, 1961 from O. auratus based on the description provided by Gendre (1912). Acuaria europaea n. sp. can be distinguished from A. orioli by the lengths of its cordons and spicules.

Acuaria europaea n. sp., similarly to A. subula ( Dujardin, 1845) as redescribed by Mutafchiev et al. (2013), possesses cordons extending slightly beyond the junction of the muscular and glandular oesophagus. However, the cordons of these two species differ by their detailed structure, i.e. A. subula is characterised by plates overlapping the anterior part of the adjacent posterior plate, while in the new species the plates do not overlap. Females of A. subula have specific mosaic ornamentation on the lateral and ventral side of the region close to vulva, the vulvar opening is surrounded by circular folds and the tail is bent dorsally, while in the new species the cuticle surrounding the vulva is smooth and the tail is strongly bent ventrally. The male of the new species differs from males of A. subula by having longer right (155 vs 110–134 lm) and left (297 vs 180–227 lm) spicules. The new species can be distinguished from the other species known in Europe by the length of its cordons ( Chabaud & Petter, 1961; Smogorzhevskaya, 1990; Mutafchiev et al., 2013; present study).

Acuaria europaea n. sp. is characterised by cordons extending slightly beyond the level of anterior end of the glandular oesophagus, a relatively long left spicule ([250 lm), which is almost twice as long as the right spicule as well as a strongly ventrally curved female tail. These morphological characters make the new species comparable to several species of the genus Acuaria known from India and China, i.e. Acuaria turdi ( Wang, 1966) from Turdus mandarinus Bonaparte (= Turdus merula mandarinus Bonaparte ) ( Passeriformes : Turdidae ); Acuaria lucknowensis Gupta & Jehan, 1972 from Cissa chinensis (Boddaert) ( Passeriformes : Corvidae ) (type-host) and Turnix suscitator (Gmelin) ( Charadriiformes : Turnicidae ); Acuaria copsychusi Gupta & Jehan, 1972 from Copsychus saularis (L.) ( Passeriformes : Muscicapidae ); Acuaria magpii Gupta & Jehan, 1972 from Urocissa erythrorhyncha (Boddaert) ( Passeriformes : Corvidae ); and Acuaria cissae Wang, 1976 from U. erythrorhyncha (see Wang, 1966, 1976; Gupta & Jehan, 1972; Gupta & Kumar, 1977). The new species differs from A. copsychusi and A. magpii , which have been described with longer cordons extending to the posterior end of the glandular oesophagus, vulva situated at mid-body and posteriorly, respectively, and different lengths of the right spicule (120 and 170 lm, respectively). Acuaria europaea n. sp., similarly to A.

lucknowensis , A. cissae and A. turdi , has cordons extending to the region of the anterior part of the glandular oesophagus ( Gupta & Jehan, 1972, 1977; Wang, 1966). However, females of A. lucknowensis are characterised by a vulva situated posterior to the mid-body and shorter tail, 75–130 lm. Males of A. lucknowensis were originally described with a slen- der right spicule, 235–275 lm long, and a broad left spicule, 95–130 lm long, although one of the two drawings showed the opposite (plate 3, figure 3 in Gupta & Jehan, 1972). According to Gupta & Kumar (1977), A. lucknowensis had a left spicule 220–280 lm long and a right spicule 100–120 lm long, although the drawing demonstrated the opposite. Despite these discrepancies in the descriptions of A. lucknowensis , we presume that the species is characterised by a long left spicule and a short right spicule, which are typical for the members of the family Acuariidae ( Bain et al., 2014) . Thus, males of A. lucknowensis are characterised by a shorter left and right spicule compared to those of the new species. The female of A. turdi differs from A. europaea n. sp. by its shorter body (10.2 mm long) and longer cordons (1,440 lm long). The male of A. turdi can be distinguished from the new species by its longer cordons (1,120 lm) and shorter right and left spicules (105 and 262 lm, respectively). Acuaria europaea n. sp. differs from A. cissae , which was described with longer cordons (800–880 lm and 1,680 lm long in males and the female, respectively), shorter right spicule (98–112 lm long), shorter female tail (105 lm long) and vulva situated slightly posterior to the mid-body.

The new species also resembles Acuaria cyanocitta ( Boyd, 1956) from Cyanocitta cristata (L.) ( Corvidae ) in the USA, as described by Boyd (1956), by the length of cordons and the general morphology of the spicules. Compared to the new species, A. cyanocitta has markedly longer left and right spicules (315–370 lm and 220–230 lm, respectively) and a straight and longer female tail (275–380 lm long).

Figures

Fig. 2 Acuaria europaea n. sp., type-material from Dendrocopos syriacus, light microscopy. A, Detail of cordons at level of deirid (arrow), male, lateral view; B, Detail of cordons near their posterior end and lateral field, male; C, Detail of cordon structure at level of deirid, female; D, Detail of lateral field in form of single row of plates, female; E, Detail of lateral field posterior to region forming row of plates, female

b Fig. 1 Acuaria europaea n. sp., type-material from Dendrocopos syriacus. A, Head region, female, lateral view; B, Anterior end, male, lateral view, note deirid (arrow); C, Anterior end, female, lateral view; D, Posterior end, male, ventral view, note phasmids (arrows); E, Right spicule, dextral view; F, Left spicule, sinistral view; G, Distal end of left spicule, note ventral precloacal papilla (arrow); H, Posterior end, female, lateral view, note phasmids (arrows); I, Region of vulva, lateral view; J, Terminal part of female genital system, ventral view; K, Egg

b Fig. 3 Acuaria europaea n. sp., females from Oriolus oriolus. A, Anterior end, lateral view, from Kalimok, Bulgaria; B, Terminal part of genital system, lateral view, specimens from Kalimok, Bulgaria (B 1) and from Indre-et-Loire, France, eggs not depicted (B 2); C, Posterior end, lateral view, specimens from Kalimok, Bulgaria (C 1) and from Indre-et-Loire, France (C 2), note phasmids (arrows)

Tables

Table 1 Metrical data of females of Acuaria europaea n. sp. from various hosts and localities

Host	Dendrocopos syriacus (Hemprich & Ehrenberg)	Oriolus oriolus	(L.)
Locality	Plovdiv (Bulgaria) n = 1	Indre-et-Loire (France) n = 1	Kalimok (Bulgaria) n = 1	Elena (Bulgaria) n = 1
Body length (mm)	24.6	16.2	17.8	13.7
Maximum body width	242	201	161	204
Tail length	202	157	214	161
Deirids, distance from anterior extremity	272	250	246	215*
Excretory pore, distance from anterior extremity	315	337	393	270*
Nerve-ring, distance from anterior extremity	237	245	246	215*
Buccal cavity length	209	192	205	156*
Muscular oesophagus length	701	670	665	222*
Glandular oesophagus length	2,035	1,527	1,892	1,443
Cordons length	1,270	1,219	1,261	929*
Vulva, distance from anterior extremity	11.2	7.9	8.6	6.1
Ovejector length	1,240	948	984	–

*Measurement is affected by the highly contracted anterior end