Acuaria europaea Yasen Mutafchiev &amp; Jean Mariaux &amp; Boyko B. Georgiev 2017, n. sp.
Creators: name: Mutafchiev, Yasen
name: Mariaux, Jean
name: Georgiev, Boyko B.
Publisher: name: Zenodo
Year: 2017
Subjects: Biodiversity
Taxonomy
Animalia
Nematoda
Secernentea
Spirurida
Acuariidae
Acuaria
Acuaria europaea

description: <i>Acuaria europaea</i> n. sp. <i>Type-host</i>: <i>Dendrocopos syriacus</i> (Hemprich &amp; Ehrenberg) (Piciformes: Picidae). <i>Other host</i>: <i>Oriolus oriolus</i> (L.) (Passeriformes: Oriolidae). <i>Type-locality</i>: Plovdiv, Bulgaria (42 11 0 18.59 0 0N, 24 45 0 2.65 0 0E). <i>Site in host</i>: Under the koilin lining of the gizzard. <i>Intensity</i>: 1 male and 2 females. <i>Type-material</i>: 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). <i>Other material</i>: Ex <i>Oriolus oriolus,</i> IBER-BAS N000.645 (1 female); IBER-BAS N000.978 (1 female); MNHN 135E (1 female). <i>Representative DNA sequence</i>: GenBank KX353874 (<i>cox</i> 1). <i>Etymology</i>: The name of the new species reflects its known geographical range. Description (Figs. 1, 2, 3) <i>General</i>. [Based on specimens from <i>Dendrocopos syriacus.</i>] 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), <i>c.</i> 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). <i>Male</i>. 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 <i>c</i>.10 wide; plates up to 4–5 wide and <i>c.</i> 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 <i>c.</i> 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). <i>Female</i>. 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 <i>c</i>.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, <i>c.</i> 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 <i>c.</i> 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 <i>Proyseria petterae</i> Mutafchiev, Mariaux &amp; Georgiev, 2014 (87% nucleotide and 93% protein similarity; GenBank KJ995862; Mutafchiev et al., 2014) and <i>Stammerinema hyalinum</i> (von Linstow, 1890) (85% nucleotide and 88% protein similarity; GenBank KP059294; Mutafchiev et al., 2015). Observations on females from <i>Oriolus oriolus</i> 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 <i>Dendrocopos syriacus</i> 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 <i>Acuaria</i> (see Williams, 1929; Baruš &amp; Garrido, 1968; Mawson, 1972; Mutafchiev et al., 2012, 2013). <i>Acuaria parorioli</i> Chabaud &amp; Petter, 1961 was described on the basis of one male and one female designated as holotype and allotype, respectively, collected from a single <i>Oriolus oriolus</i> L. in France (Chabaud &amp; 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 <i>A. parorioli</i> are not conspecific. The comparison of the female nematode reported as <i>Acuaria anthuris</i> (Rudolphi, 1819) from <i>Oriolus oriolus</i> by Petrova (1974), the female paratype (‘‘allotype’’) of <i>A. parorioli</i> 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 <i>A. europaea</i> n. sp. from <i>Dendrocopos syriacus.</i> Therefore, we identified them as <i>A. europaea</i> n. sp. Smogorzhevskaya (1990) identified <i>A. parorioli</i> from two females collected from <i>O. oriolus</i> in the Ukraine, which were characterised by short cordons, 315 lm long. Gendre (1912) described <i>Acuaria gracilis (Gendre, 1912)</i> from <i>Dicrurus adsimilis (Bechstein)</i> (= <i>Buchanga atra adsimilis</i>) (Passeriformes: Dicruridae) and <i>Oriolus auratus</i> 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 <i>O. auratus</i> had the same morphology as that from <i>D. adsimilis</i> except for the number of postcloacal papillae (7 <i>vs</i> 6 pairs). Chabaud &amp; Petter (1961) considered that difference significant and described <i>Acuaria orioli Chabaud &amp; Petter, 1961</i> from <i>O. auratus</i> based on the description provided by Gendre (1912). <i>Acuaria europaea</i> n. sp. can be distinguished from <i>A. orioli</i> by the lengths of its cordons and spicules. *Measurement is affected by the highly contracted anterior end <i>Acuaria europaea</i> n. sp., similarly to <i>A. subula (Dujardin, 1845)</i> 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. <i>A. subula</i> 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 <i>A. subula</i> 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 <i>A. subula</i> by having longer right (155 <i>vs</i> 110–134 lm) and left (297 <i>vs</i> 180–227 lm) spicules. The new species can be distinguished from the other species known in Europe by the length of its cordons (Chabaud &amp; Petter, 1961; Smogorzhevskaya, 1990; Mutafchiev et al., 2013; present study). <i>Acuaria europaea</i> 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 <i>Acuaria</i> known from India and China, i.e. <i>Acuaria turdi</i> (Wang, 1966) from <i>Turdus mandarinus</i> Bonaparte (= <i>Turdus merula mandarinus</i> Bonaparte) (Passeriformes: Turdidae); <i>Acuaria lucknowensis</i> Gupta &amp; Jehan, 1972 from <i>Cissa chinensis</i> (Boddaert) (Passeriformes: Corvidae) (type-host) and <i>Turnix suscitator</i> (Gmelin) (Charadriiformes: Turnicidae); <i>Acuaria copsychusi</i> Gupta &amp; Jehan, 1972 from <i>Copsychus saularis</i> (L.) (Passeriformes: Muscicapidae); <i>Acuaria magpii</i> Gupta &amp; Jehan, 1972 from <i>Urocissa erythrorhyncha</i> (Boddaert) (Passeriformes: Corvidae); and <i>Acuaria cissae</i> Wang, 1976 from <i>U. erythrorhyncha</i> (see Wang, 1966, 1976; Gupta &amp; Jehan, 1972; Gupta &amp; Kumar, 1977). The new species differs from <i>A. copsychusi</i> and <i>A. magpii</i>, 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). <i>Acuaria europaea</i> n. sp., similarly to <i>A.</i> <i>lucknowensis</i>, <i>A. cissae</i> and <i>A. turdi</i>, has cordons extending to the region of the anterior part of the glandular oesophagus (Gupta &amp; Jehan, 1972, 1977; Wang, 1966). However, females of <i>A. lucknowensis</i> are characterised by a vulva situated posterior to the mid-body and shorter tail, 75–130 lm. Males of <i>A. lucknowensis</i> 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 &amp; Jehan, 1972). According to Gupta &amp; Kumar (1977), <i>A. lucknowensis</i> 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 <i>A. lucknowensis</i>, 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 <i>A. lucknowensis</i> are characterised by a shorter left and right spicule compared to those of the new species. The female of <i>A. turdi</i> differs from <i>A. europaea</i> n. sp. by its shorter body (10.2 mm long) and longer cordons (1,440 lm long). The male of <i>A. turdi</i> 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). <i>Acuaria europaea</i> n. sp. differs from <i>A. cissae</i>, 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 <i>Acuaria cyanocitta</i> (Boyd, 1956) from <i>Cyanocitta cristata</i> (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, <i>A. cyanocitta</i> 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).
description: Published as part of <i>Yasen Mutafchiev, Jean Mariaux &amp; Boyko B. Georgiev, 2017, Description of Acuaria europaea n. sp. (Spirurida: Acuariidae) from Dendrocopos syriacus (Hemprich &amp; Ehrenberg) and Oriolus oriolus (L.) (Aves) in Europe, with results of re-examination of related European species of Acuaria Bremser, 1811, pp. 201-214 in Systematic Parasitology 94</i> on pages 202-208, DOI: 10.1007/s11230-016-9695-z, http://zenodo.org/record/1039390
description: {"references": ["Mutafchiev, Y., Mariaux, J., &amp; Georgiev, B. B. (2014). Description of Proyseria petterae n. sp., with an amended generic diagnosis and a review of the species of Proyseria Petter, 1959 and Stegophorus Wehr, 1934 (Nematoda: Acuariidae). Systematic Parasitology, 89, 3 - 14.", "Bain, O., Mutafchiev, Y., &amp; Junker, K. (2014). Order Spirurida. In A. Schmidt-Rhaesa (Ed.), Handbook of Zoology: Gastrotricha, Cycloneuralia and Gnathifera. Volume 2. Nematoda. Berlin: De Gruyter, pp. 661 - 732.", "Mutafchiev, Y., Mariaux, J., &amp; Georgiev, B. B. (2015). Stammerinema hyalinum n. comb. for Filaria hyalina von Linstow, 1890 and its recognition as a senior synonym of Stammerinema rhopalocephalum (Soltys, 1952) (Spirurida: Acuariidae), a parasite of shrews. Systematic Parasitology, 90, 105 - 111.", "Williams, O. L. (1929). A critical analysis of the specific characters of the genus Acuaria nematodes of birds, with description of new American species. University of California Publication in Zooology, 33, 69 - 107.", "Barus, V., &amp; Garrido, O. H. (1968). Nematodes parasitic in birds of the order Passeriformes in Cuba. Folia Parasitologica, 15, 147 - 160.", "Mawson, P. M. (1972). The genus Acuaria Bremser (Nematoda: Spirurida) in Australia. Transactions of the Royal Society of South Australia, 96, 139 - 147.", "Mutafchiev, Y., Mariaux, J., &amp; Georgiev, B. B. (2012). Acuaria paraguayensis n. sp. from Sirystes sibilator (Aves: Tyrannidae) in Paraguay and a redescription of A. mamillaris (Molin, 1860) from Cyanocorax cayanus (Corvidae) in Brazil, with a key to the species of Acuaria Bremser, 1811 (Nematoda: Acuariidae) in the New World. Systematic Parasitology, 81, 51 - 64.", "Mutafchiev, Y., Kontrimavichus, V. L., &amp; Georgiev, B. B. (2013). Redescriptions and comments on the validity of Acuaria subula and A. skrjabini (Nematoda, Spirurida, Acuariidae), parasites of passerine birds. Acta Parasitologica, 53, 284 - 296.", "Chabaud, A. G., &amp; Petter, A. (1961). Nematodes du genre Acuaria de la Faune de France. Annales de Parasitologie Humaine et Comparee, 36, 409 - 424.", "Rudolphi, C. A. (1819). Entozoorum synopsis cui accedunt mantissa duplex et indices locupletissimi. Berlin: Sumtibus Augusti Rucker, 811 pp.", "Petrova, K. (1974). On the helminth fauna (Nematoda and Acanthocephala) from wild birds from central and eastern Stara Planina Mountain. Izvestiya na Zoologicheskiya Institut s Muzey, 12, 319 - 328 (in Bulgarian).", "Smogorzhevskaya, L. A. (1990). [Nematodes. Part 3. Acuarioidea]. In: Sharpilo, V. P. (Ed.) Fauna Ukrainy. Vol. 32. Kiev: Naukova Dumka, 189 pp (In Russian).", "Gendre, E. (1912). Sur quelques especes de Dispharages du Dahomey. Actes de la Societe Linneenne de Bordeaux, 66, 23 - 31.", "Dujardin, F. (1845). Histoire naturelle des helminthes ou vers intestinaux. Paris: Librairie Encyclopedique de Roret, 654 pp.", "Wang, P. Q. (1966). Notes on Acuarioidea of birds from Fukien, China. Acta Parasitologica Sinica, 3, 15 - 29 (In Chinese, with English Summary).", "Gupta, S. P., &amp; Jehan, M. (1972). On some species of the genus Acuaria Bremser, 1811 from avian hosts from Lucknow. Japanese Journal of Parasitology, 21, 365 - 373.", "Wang, P. Q. (1976). Notes on some new nematodes of the suborder Spirurata from Fujian, China. Acta Zoologica Sinica, 22, 393 - 402 (In Chinese, with English Summary).", "Gupta, S. P., &amp; Kumar, P. (1977). On some species of the genus Acuaria Bremser, 1811 from avian hosts from Uttar Pradesh. Indian Journal of Helminthology, 29, 120 - 136.", "Boyd, E. M. (1956). Two new species of stomach worms (Nematoda: Spiruroidea) from the blue jay, Cyanocitta cristata L. Proceedings of the Helminthological Society of Washington, 23, 70 - 74."]}