Paranybelinia otobothrioides, Dollfus, 1966

Morales-Ávila, José Raúl, Gómez-Gutiérrez, Jaime, Hernandez-Saavedra, Norma Y., Robinson, Carlos J. & Palm, Harry W., 2019, Phylogenetic placement and microthrix pattern of Paranybelinia otobothrioides Dollfus, 1966 (Trypanorhyncha) from krill Nyctiphanes simplex Hansen, 1911, International Journal for Parasitology: Parasites and Wildlife 10, pp. 138-148 : 144-146

4.2. The blastocyst of Pa. otobothrioides and its systematic importance

According to Dollfus (1966) Pa. otobothrioides and Ps. odontacantha showed distinctive morphological characters, i.e., homeoacanth tentacular armature, two bothria with the so called “bothrial pits” and the absence of blastocysts that led to the erection of an own family Paranybeliniidae to include these monotypic species. Shimazu (1982) recovered Ps. odontacantha infecting E. recurva from the East China Sea. This author highlighted that the metacestodes infecting krill lacked a blastocyst supporting findings provided in Dollfus (1966). Nevertheless, Shimazu (2006) pointed out that metacestodes of Ps. odontacantha (published in Shimazu, 1982) could have occurred in a blastocyst, though no evidence was provided. More recently, Palm (2008) described the surface ultrastructure of the scolex of Ps. odontacantha based on the type material deposited in the collection of the Museum National d ʹ Historie Naturelle, Paris, France. However, since these trypanorhynch species had not been recovered after Dollfus (1966) and Shimazu (1982), morphological re-examination of Pa. otobothrioides and the formation of a blastocyst in both species remained to be confirmed.

In the present study, we show that the freshly collected specimens of Pa. otobothrioides occur enclosed in a blastocyst that could only be opened by dissection with acupuncture needles. The single layer tissue blastocyst containing the scolex was found inside the hepetopancreas of the host. This finding demonstrates that Pa. otobothrioides and most likely Ps. odontacantha ( Shimazu, 1999, 2006) develop within a simple blastocyst when infecting their intermediate hosts, the euphausiids N. simplex parasitizing Pa. otobothrioides and E. recurva parasitizing Ps. odontacantha . Four pori in Pa. otobothrioides ’ blastocyst more likely allow direct interaction between the coelomic fluid of the host and the inner part of the blastocyst surrounding the scolex, suggesting a possible feeding and/or excretory function. After opening the blastocyst, the scolex moved freely and resembled the typical plerocercoid stages known from the related tentaculariids. It is interesting to note that Tentacularia coryphaenae , one of the most closely related tentaculariid to Pa. otobothrioides in the present study, was earlier reported in a skinny “translucent host capsule” shown in Fig. 1 in Palm et al. (2007), and also Shimazu (1999) documented that the plerocercoids of N. surmenicola occur in a translucent simple blastocyst inside the temperate euphausiid E. pacifica .

The lack of a blastocyst was considered a plesiomorphic character ( Hoberg et al., 1997; Beveridge et al., 1999). According to Palm (1997), its presence is a convergent development within the superfamilies of trypanorhynchs (absent in the Tentacularioidea and Gymnorhynchoidea, and present in the Otobothrioidea , Lacistorhynchoidea, and Eutetrarhynchoidea ). Therefore, the lack or presence of a blastocyst was used to distinguish the trypanorhynch taxa at the family level only. However, when the species description was based only on adult specimens, the incipient knowledge of their early larval development infecting intermediate/paratenic hosts lead to tentatively assignment of some genera in superfamilies and families despite not knowing if their larvae have a blastocyst. In this context, the systematic position of Pa. otobothrioides has been unstable and widely debated allocating it within the superfamilies Tentacularioidea and the Otobothrioidea . Schmidt (1986), Campbell and Beveridge (1994) and Beveridge et al. (1999) based on a plerocercoid lacking a blastocyst and the presence of a homeoacanthous armature, affiliated (with cladistics) the genera Paranybelinia and Pseudonybelinia close to Kotorella and Nybelinia belonging to the family Tentaculariidae (Tentacularioidea) . Although Shimazu (1999) stated that the tentaculariid N. surmenicola is enclosed in a simple blastocyst or bladder and infects the digestive gland of the krill E. pacifica , it was supposed that the superfamily Tentacularioidea lacks a blastocyst during their ontogeny ( Dollfus, 1929; Palm and Walter, 2000; Palm, 2008). Herewith, a blastocyst has been observed in members of all five superfamilies Otobothrioidea , Lacistorhynchoidea, Gymnorhynchoidea, Eutetrarhynchoidea , and Tentacularioidea ( Shimazu, 1999, 2006, present study).

Additionally, strong hyaline cysts surrounding plerocerci, the latter also complex multilayered or even merocercoids, have been recorded in lacistorhynchoid, otobothriod (e.g. Palm and Overstreet, 2000) and gymnorhynchoid trypanorhynchs ( Palm, 2004). Mattis (1986) demonstrated that Prochristianella hispida (Linton, 1890) (Eutetrarhynchoidea) develops a different type of blastocyst in respect to Poecilancistrum caryophyllum (Diesing, 1850) (Otobothrioidea) . The morphological features observed in the merely simple single-layered blastocyst including the plerocercoid scolex of Pa. otobthrioides are so far unique and can be easily distinguished from any other trypanorhynch. This suggests that in the classification of the trypanorhynchs, the blastocyst morphology and its development instead of the solely presence/absence of the blastocysts will add more taxonomic resolution at the family level. However, further morphological characterizations of blastocysts within families and genera are needed in order to evaluate the level of taxonomic precision and autapomorphies.

Figures

Fig. 1. Paranybelinia otobothrioides parasitizing the subtropical krill Nyctiphanes simplex collected in the Gulf of California, Mexico. (A) Alive Pa. otobothrioides observed in the hemocoel of the host. (B) Histological section showing longitudinal view of Pa. otobothrioides inside the blastocyst. (C,D) Blastocyst containing the plerocercus of the same specimen, note the contraction (C) and expanding (D) movement of the blastocyst. (E) Pa. otobothrioides scolex dissected from the blastocyst. (F) Scanning electron microscope external view of the blastocyst, showing single distinct projectable centrally oriented porous-like terminal end (anterior), and 2 lateral and 1 central cone terminal projection (posterior end). (G,H) Detail of funnel openings at the anterior and posterior end. Scale bars: (A–F) 100 μm, (G) 5 μm, (H) 30 μm.