Glanitaenia de Chambrier, Zehnder, Vaucher & Mariaux, 2004

Alain de Chambrier & Tomáš Scholz, 2016, An emendation of the generic diagnosis of the monotypic Glanitaenia (Cestoda: Proteocephalidae), with notes on the geographical distribution of G. osculata, a parasite of invasive wels catfish, Revue suisse de Zoologie 123 (1), pp. 1-9 : 6-8

Glanitaenia de Chambrier, Zehnder, Vaucher & Mariaux, 2004 – amended diagnosis

Diagnosis: Proteocephalidea , Proteocephalidae . Large tapeworms with numerous slightly craspedote proglottids, wider than long including for pregravid and gravid proglottids. Inner longitudinal musculature well developed, formed by highly anastomosed, numerous bundles of muscle fibres. Scolex unarmed, with four uniloculate suckers, with convoluted osmoregulatory canals in its posterior part. Apical sucker well developed, strongly muscular, with deep cavity; apical part lined with numerous gland cells. Neck region (proliferation zone) long, containing extensively developed, convoluted osmoregulatory canals with numerous anastomoses in its anterior part. Immature proglottids numerous, begin at considerable distance posterior to scolex. Testes numerous, medullary, in one continuous field and in one layer, exceptionally with a few testes in second incomplete layer. Ovary medullary, numerous, bilobed, relatively large in relation to surface of proglottids.Vagina opening to common genital atrium anterior to cirrus-sac; vaginal canal with circular vaginal sphincter situated ventral to ventrolateral to vitelline follicles; terminal (distal) part of vaginal canal encircled by separated bundles of muscle fibres. Genital pore slightly preequatorial. Vitelline follicles lateral, occupying almost entire proglottid length. Uterus medullary, ventral, with ramified lateral diverticula. Development of uterus of type 2. Parasites of siluriform fish in Palaearctic Region. Type and only species: Glanitaenia osculata (Goeze, 1782) de Chambrier, Zehnder, Vaucher & Mariaux, 2004 [synonyms Taenia osculata Goeze, 1782 ; Proteocephalus osculatus (Goeze, 1782) La Rue, 1911 ; Ichthyotaenia skorikowi von Linstow, 1904; Proteocephalus skorikowi (von Linstow, 1904) La Rue, 1911; Gangesia osculata (Goeze, 1782) Reichenbach-Klinke, 1962 ].

DISCUSSION

In the present study, generic diagnosis of one of the earliest diverging taxon of the subfamily Proteocephalinae (see de Chambrier et al., 2015) is amended, based on the examination of newly collected and museum material of its type and only species, Glanitaenia osculata . This species was poorly known since its description as Taenia osculata by Goeze (1782) and La Rue (1911, 1914) placed it (as Proteocephalus osculatus ) among species inquirendae, partly because it was confused with another specific parasite of wels catfish, Silurotaenia siluri (Batsch, 1786) ( Proteocephalidea : Gangesiinae ). Nybelin (1942) was the first who confirmed the validity of P. osculatus and provided a most detailed description of its morphology at a given time.

Freze (1965), who studied extensive material of P. osculatus (= Glanitaenia osculata ) from the former Soviet Union, stated that “Nybelin’s description of P. osculatus [= G. osculata ] insufficiently reflects the boundaries of its morphological variations, although Freze’s material in general corresponds to this description and pertains to the same species.” Scholz et al. (1998) provided detailed data on the scolex morphology of G. osculata (as P. osculatus ) including SEM micrographs, and Scholz & Hanzelová (1998) redescribed the species based on newly collected specimens from the Czech Republic.

In the present study, some morphological and biometrical data are provided for the first time, which made it possible to amend the generic diagnosis of Glanitaenia . de Chambrier et al. (2004) have demonstrated potential importance of the uterine development as one of very few morphological characteristics that may reflect the evolutionary history of the order (see also de Chambrier et al., 2015). The former authors classified the development of the uterus of G. osculata as type 2 (see fig. 1 in de Chambrier et al., 2004), but did not provide any details. Surprisingly, the shape of the developed uterus of G. osculata with ramified lateral diverticula is most similar to that of Ageneiella brevifilis de Chambrier & Vaucher, 1999, a parasite of the auchenipterid catfish Ageneiosus inermis (Linnaeus) in the Neotropical Region (see fig. 31 in de Chambrier & Vaucher, 1999), which belongs to a most derived clade of proteocephalidean cestodes (de Chambrier et al., 2015).

The new material of G. osculata also enabled us to provide data on the relative size of the ovary (see de Chambrier et al., 2012). The surface of the ovary of G. osculata represents 7.5-8.7% of the total surface of proglottids (and 10.6-10.7% in specimens illustrated by Scholz & Hanzelová, 1998), which well corresponds to the values in other species of proteocephalideans from teleost fishes and it is markedly larger than those in most species of Ophiotaenia La Rue, 1911 from reptiles (see table 1 in de Chambrier et al., 2015).

A novelty of the present study is a detailed description of a vaginal sphincter in G. osculata and its peculiar position and morphology. Indeed, Nybelin (1942) also described a small vaginal sphincter and illustrated it in his fig. 3, but he did not provide any details. In contrast, Scholz & Hanzelová (1998) did not report this structure at all. They illustrated a thick layer of cells lining the terminal (distal) part of the vaginal canal in their fig. 9G (cross section at the level of the vagina), but these cells were not interpreted as a vaginal sphincter. Similarly, no sphincter was illustrated in the terminal part of the vaginal canal (fig. 16I in that paper).

One of the reasons why Scholz & Hanzelová (1998) did not report the vaginal sphincter, which is actually present in the specimens studied by these authors, could be its unusual position. It is situated at the level of vitelline follicles, i.e. much more medially than in related taxa such as Proteocephalus longicollis (Zeder, 1800) and P. percae (Müller, 1780) , in which the sphincter is close to the genital atrium (see figs 14G, 18E, F and 20 H, I in Scholz & Hanzelová, 1998).

The terminal part of the vaginal canal of G. osculata , which is surrounded by a medially situated circular vaginal sphincter of a typical shape (ring-like sphincter) and a few separated bundles of muscle fibres situated more distally, somewhat resembles that of phylogenetically distant species from Neotropical catfish, Mariauxiella piscatorum de Chambrier & Vaucher, 1999 (see fig. 87 in de Chambrier & Vaucher, 1999).

The eggs of G. osculata are described and illustrated for the first time in the present paper, even though Scholz (1999) studied early phases of the developmental cycle of the species. However, he provided only data on metacestodes (plerocercoids) from experimentally infected copepods 12 and 21 days post infection. In fact, the eggs of G. osculata resemble those typical of most species of the Proteocephalus aggregate (see Scholz, 1999).

The anterior part of the body of G. osculata , specifically the posterior part of its scolex and the anterior part of a very long proliferative zone (neck region), contains strongly convoluted osmoregulatory canals that form a dense network of anastomosed canals. Scholz et al. (1998) observed similar networks in the scolex of most Palaearctic species of the Proteocephalus aggregate, but they did not focus on the presence of these canals in the proliferative zone. In addition, the canals seem to be much more developed in G. osculata compared to those in species of the Proteocephalus aggregate (see figs 1K, 3G, I, J, 5E, Q in Scholz et al., 1998). A dense network of osmoregulatory canals situated in the posterior part of the scolex and the anterior part of the neck region was also observed in phylogenetically distant Proteocephalus regoi de Chambrier, Scholz & Vaucher, 1996, a parasite of Hoplias malabaricus (Bloch) ( Characiformes : Erythrinidae ) in the Neotropical Region (see figs 1 and 3 in de Chambrier et al., 1996), and in Sandonella sandoni (Lynsdale, 1960) from Heterotis niloticus (Cuvier) ( Osteoglossiformes : Arapaimidae ) in the Ethiopian Region (see fig. 2 in de Chambrier et al., 2008). Function of these canals and the reason of their concentration in the scolex or in the proliferative zone are not known. Cestodes seem to be osmoconformers whose excretory system plays little or no role in osmoregulation and is largely excretory (Smyth & McManus, 1989).

Glanitaenia osculata belongs to the largest cestodes of teleost fishes, with a total length reaching up to 1 m (Lühe, 1910); the longest specimen found in the present study was 74 cm long (a tapeworm from Switzerland). The body of G. osculata consists of numerous, rather large proglottids that contain many testes. Even though these are mostly in a single layer, their counting is difficult due to their high number and a well-developed longitudinal musculature. Nybelin (1942) reported 276- 291 testes per proglottid, Freze (1965) 180-424 testes (usually about 250), but Scholz & Hanzelová (1998) only 105 - 171 testes. In the present study, 222-281 testes (x = 249, n = 10) were counted based on illustrations of individual proglottids, which is the most precise method of counting the testes.

This species forms, together with Paraproteocephalus parasiluri (Yamaguti, 1934) , type and single species of Paraproteocephalus Chen in Dubinina, 1962 (see de Chambrier et al., 2004, 2015; Scholz et al., 2007). Species of both monotypic genera differ from each other in their scolex and strobilar morphology, especially in the presence/absence of a metascolex (absent in the former species versus well-developed in P. parasiluri , which was even placed in the subfamily Corallobothriinae – Freze, 1965), the position of bands of vitelline follicles (‘typically’ vertical alongside margins of proglottids in G. osculata versus L-shaped, with most follicles forming a transverse band lateral to the ovary in the latter species – see figs 6 & 7 in Shimazu, 1993), and uterine diverticula (lateral in the former species as in a majority of proteocephalideans versus forming anterior and posterior branches from the transversely situated uterine stem in P. parasiluri – figs 6 & 7 in Shimazu, 1993).

Glanitaenia osculata resembles species of the Proteocephalus aggregate in the morphology of its scolex, which is devoid of any metascolex, and shape of the strobila and its proglottids, which are only slightly wider than long. It can be distinguished from species of the Proteocephalus aggregate by a much more developed apical sucker (versus vestigial or absent in species of the latter group – see Scholz et al., 1998) and by the anterior position of the vaginal canal in relation to the cirrus-sac (ventral to the terminal part of the sac in most species of the Proteocephalus aggregate). In addition, G. osculata is much bigger and more robust than the species of the Proteocephalus aggregate and its proglottids contain much more proglottids, especially immature ones, and more testes (Scholz & Hanzelová, 1998; present study). This tapeworm has been reported from the following countries of Europe and Palaearctic Asia: Bulgaria, Czech Republic, Germany, Hungary, Latvia, Lithuania, Poland, Russia, Slovakia, Sweden, Ukraine, United Kingdom, former Yugoslavia, Azerbaidzhan, Georgia, Iraq and Turkey ( Fig. 16 ; see also Scholz & Hanzelová, 1998 and Gibson et al., 2005 [but misidentification of Postgangesia inarmata de Chambrier, Al-Kallak & Mariaux, 2003 and Postgangesia hemispherous (Rahemo & Al-Niaeemi, 2001) in Iraq cannot be excluded].

Glanitaenia osculata is a specific parasite of wels catfish, which is currently considered to be an invasive species and has recently been introduced to the western and southwestern Europe including northern Italy, Spain, France, Germany and England (Copp et al., 2009; Fig. 16 ). Therefore, it is possible that new geographical records from two of these countries (the River Po in Italy and the River Rhine basin in Germany – River Aare is a tributary of the Rhine joining it in Koblenz, at the Swiss- German border) are a result of this recent expansion of the wels catfish throughout Europe ( Fig. 16 ).

Figures

Fig 16. Geographical distribution of Glanitaenia osculata (Goeze, 1782) in Europe. Countries with previous records indicated by triangles; new geographical records (Italy, Romania and Switzerland) highlighted by asterisk); the original distribution area of wels catfish (grey silhouette; bordered by dashed line) and newly colonized regions of Europe (white silhouette; bordered by dotted line; modified from Copp et al., 2009).