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Systematic position of the enigmatic Quentinia mesovitellinica (Rêgo, 1967) (Cestoda, Cyclophyllidea)

   | Dec 26, 2023

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Introduction

Catenotaenia mesovitellinica Rêgo, 1967 (Cestoda, Cyclophyllidea) was described from the hystricomorph rodent Galea spixii (Wagler) (Caviidae) in Brazil. In the same year, Quentin (1967) described Atriotaenia (Ershovia) baltazardi Quentin, 1967 (Linstowiidae) from the same host species (G. spixii) and the same country (Brazil). Spasskii (1969) established a new genus, Quentinia Spasskii, 1969, for A. baltazardi and assigned it to the family Anoplocephalidae. Later, Tenora et al. (1980) proposed the genus Quentinotaenia Tenora, Mas-Coma, Murai & Feliu, 1980 for C. mesovitellinica within the family Catenotaeniidae.

It was later suggested by Quentin (1994) that Quentinia baltazardi (Quentin, 1967) and Quentinotaenia mesovitellinica (Rêgo, 1967) are in fact the same species and that “mesovitellinica” is the valid specific epithet because of an earlier publication date. It followed that Quentinotaenia fell into synonymy with Quentinia, and the valid combination is therefore Quentinia mesovitellinica (Rêgo, 1967). Quentin’s (1967) action of assigning the new species to Atriotaenia Sandground, 1926 is clearly erroneous, because Q. mesovitellinica has a persistent sac-like uterus, rather than an ephemeral uterus with eggs embedded in the parenchyma, the latter type characterizing the family Linstowiidae (see Beveridge, 1994).

Although it was recognized that Q. mesovitellinica has some unusual morphologic features, it has usually been assigned to the family Catenotaeniidae, either within the genus Catenotaenia Janicki, 1904 (see Quentin, 1971, Tenora and Murai, 1975, Tenora, 1977, Genov and Tenora, 1979) or as an independent genus within the Catenotaeniidae (Schmidt, 1986, Georgiev et al., 2006) or within the (non-monophyletic) subfamily Catenotaeniinae (Tenora et al., 1980, Quentin, 1994, Haukisalmi et al., 2010). However, Mariaux et al. (2017) classified Quentinia as a genus incertae sedis.

In addition to the morphologic issues, the host and geographic distributions of Q. mesovitellinica are peculiar. Quentinia mesovitellinica is the only known catenotaeniid species parasitizing hystricomorph rodents and also the only catenotaeniid in South America. Most catenotaeniids parasitize myomorph rodents, with a smaller number in castorimorphs and sciuromorphs, their diversity peaking in cricetid rodents in the Holarctic region and in murid and nesomyid rodents in Africa (Haukisalmi et al., 2018; see also the Global Cestode Database [GCD]; Caira et al., 2023). Catenotaenia peromysci Smith, 1954 from Mexico represents the southernmost verified record of a catenotaeniid cestode in the Americas (Carmona Huerta, 1994), with a description.

Following Spasskii (1969), the association of Q. mesovitellinica with the Anoplocephalidae sensu stricto [s. s.] has not been considered, despite the fact that the anoplocephalid genera Andryoides Haukisalmi, 2023, Monoecocestus Beddard, 1914 and Viscachataenia Denegri, Dophic, Elissondo & Beveridge, 2003 form the most diverse tapeworm group in South American rodents (see the GCD). The purpose of the present study is to reevaluate the systematic position of the “enigmatic” Q. mesovitellinica based on published information, particularly that of Quentin (1967). The syntype specimens of Rêgo (1967), which are in poor condition, are unavailable, and no types were assigned by Quentin (1967).

In the following text, it is assumed that Q. baltazardi is a junior synonym of Q. mesovitellinica, and only the latter name is used; the status of these taxa is discussed in the end of the Results and Discussion section.

Ethical Approval and/or Informed Consent

This study does not contain any studies with human participants or live animals.

Results and Discussion

Neither Rêgo (1967) nor Tenora et al. (1980) specified the reasons for assigning Q. mesovitellinica to the Catenotaeniidae, but it may be assumed that the action was based on apparent morphological similarities between the former species and Catenotaenia sensu lato [s. l.], particularly the shape of the mature proglottids (more or less elongate) and uterus (with lateral diverticula or sacculations) and the position of testes (posterior to the female glands). However, Q. mesovitellinica differs fundamentally from Catenotaenia s. l. and other catenotaeniids with respect to several morphologic features, particularly the shape of the ovary, the position of the vitellarium, the position of the vagina with respect to the cirrus sac, the structure of the fully developed uterus, the prominence of the genital atrium and ability to form a distinct genital papilla, the alternation of genital pores and the structure of the osmoregulatory system (Table 1, Figs. 1, 2). Instead, Q. mesovitellinica shares all these features with Monoecocestus sensu Beveridge (1994), a genus in the family Anoplocephalidae s. s. Therefore, Q. mesovitellinica is evidently a species of Monoecocestus, which may have more elongated proglottids than the congeneric species, but does not otherwise differ from them with respect to the main morphologic features.

Main morphologic features that separate Quentinia Spasskii, 1969 from Catenotaenia sensu lato (Catenotaeniidae) and associate it with Monoecocestus Beddard, 1914 sensu Beveridge (1994) (Anoplocephalidae sensu stricto).

Quentinia Monoecocestus Catenotaenia sensu lato
Dorsal longitudinal osmoregulatory canals, position lateral to ventral canals lateral to ventral canals medial to ventral canals, pass between arches of transverse connecting canals
Genital atrium, size prominent, capable of forming genital papilla prominent, capable of forming genital papilla inconspicuous, not capable of forming genital papilla
Genital pores, alternation irregularly in very short series regularly or irregularly in very short series irregularly in relatively long series
Vagina, position runs anterior to cirrus sac distally, opens anterior to male pore runs (partly) anterior to cirrus sac, opens anterior to male pore runs posterior to cirrus sac, opens posterior or postero-ventral to male pore
Ovary, shape symmetrical, arched symmetrical; arched, transversely elongated or ovoid asymmetrical, extensive
Vitellarium, position median median or slightly poral poral
Fully developed uterus, shape sparsely lobulated/sacculated without distinct trunk, secondary ramifications absent sparsely lobulated/sacculated without distinct trunk, secondary ramifications absent deeply lobulated with distinct trunk, secondary ramifications usually present (“dendritic”)
Pyriform apparatus in eggs, presence present in Q. eljefe, undefined in Q. mesovitellinica present absent

Fig. 1.

A–D, Quentinia mesovitellinica (Rêgo, 1967), redrawn from Quentin (1967). A, scolex. B, early mature proglottid. C, late mature proglottid. D, gravid proglottid. E, Monoecocestus petiso Haverkost & Gardner, 2010, mature proglottid. F, G, Quentinia eljefe (Haverkost & Gardner, 2010) n. comb. F, mature proglottid. G, gravid proglottid (scale-bar not available). E–G redrawn from Haverkost & Gardner (2010). Scale-bars in micrometers. T, testes; CS, cirrus sac; O, ovary; Va, vagina; Vi, vitellarium; SR, seminal receptacle; U, uterus; VO, ventral longitudinal osmoregulatory canal; DO, dorsal longitudinal osmoregulatory canal.

Fig. 2.

Catenotaenia matovi Genov, 1971. A, mature proglottid, redrawn from Tenora et al. (1980). Longitudinal osmoregulatory canals ventral to terminal genital ducts; dorso-ventral position with respect to other organs undefined. B, pregravid proglottid, redrawn from Genov (1971). Scale-bars in micrometers. For symbols, see Fig. 1.

According to the GCD, the genus Monoecocestus sensu Beveridge (1994), which is endemic to the Americas, comprises 27 valid species parasitizing mainly rodents, with one species in artiodactyls and one in birds. Sixteen species occur in hystricomorph rodents in South, Central and North America, with highest diversity in South American caviids (eight species), including two species in Galea musteloides Meyen in Bolivia (Haverkost and Gardner, 2010).

Morphologically, Monoecocestus spp. are characterized by a single set of genitalia per proglottid, a finely reticulate early uterus confined in the median field, a posterior distribution of testes (forming a transverse band in species with transversely elongated proglottids), and a vagina that runs (partly) anterior to the cirrus sac and opens anterior to the male pore (Fig. 1E). The latter feature is of high diagnostic value, because the vagina is posterior or postero-ventral to the cirrus sac in other anoplocephalids (s. s.) and catenotaeniids. The vagina of Q. mesovitellinica, as illustrated in Quentin (1967), is distally anterior to the cirrus sac and opens anterior to the male pore. The arched (“horse-shoe shaped”), symmetric ovary has been regarded as one of the main diagnostic features of the genus Quentinia (see Tenora, 1977). However, in Monoecocestus there are several species in which the ovary is symmetrically arched, including M. eljefe Haverkost & Gardner, 2010 and M. petiso Haverkost & Gardner, 2010 from G. musteloides, greatly resembling the corresponding organ in Q. mesovitellinica (Fig.1; see also the GCD and Haverkost and Gardner, 2010). The pronounced curvature of the ovary in the type material of Q. mesovitellinica, compared with Monoecocestus spp., may be related to the excessive elongation of its proglottids.

Compared with other South American anoplocephalids (s. s.), Q. mesovitellinica differs from Viscachataenia with respect to the same features that differentiate the former species from Monoecocestus (Table 1) and also with respect to the number of genitalia per proglottid (double in Viscachataenia), and from Andryoides with respect to the position of female glands and genital pores in the antero-posterior plane, position of the vagina with respect to the cirrus sac, shape of the ovary and vitellarium and distribution of testes (Denegri et al., 2003, Haukisalmi, 2023; see also the GCD). All anoplocephalid (s. s.) cestodes, with a few exceptions, have a pyriform apparatus in the eggs. However, neither of the descriptions of Q. mesovitellinica mentions a pyriform apparatus. In the material of Quentin (1967), the eggs were “not fully embryonated”, and the failure of Rêgo (1967) to observe a pyriform apparatus could also have been due to the absence of fully developed eggs or technical issues. In M. eljefe, assigned here to Quentinia (below), a pyriform apparatus is present (Haverkost and Gardner, 2010).

The structure of the early uterus, an important feature in the genus-level classification of anoplocephalids, has not been described for Q. mesovitellinica. This may be due to the facts that the finely reticulated early uterus is sometimes poorly visible, especially in poor-quality specimens, and/or that the presence of such a structure was not specifically examined, because it does not occur in catenotaeniids or in linstowiids. However, the sparsely sacculated pregravid/gravid uterus of Q. mesovitellinica (see Quentin, 1967) is similar to the corresponding structure of Monoecocestus and other anoplocephalids, and differs distinctly from the “dendritic” uterus of catenotaeniids (Figs. 1, 2).

Although the morphology of eggs and early uterus of Q. mesovitellinica is unknown, the facts presented above and in Table 1 show unambiguously that this species is not a catenotaeniid cestode, but belongs to the family Anoplocephalidae s. s. within the genus Monoecocestus sensu Beveridge (1994). However, the genus Monoecocestus is a morphologically heterogeneous assemblage (see the GCD and Rêgo, 1961), and will probably be split when enough morphologic and phylogenetic information becomes available for a comprehensive taxonomic revision. Therefore, instead of transferring Q. mesovitellinica to Monoecocestus, Quentinia is considered here a valid genus within the Anoplocephalidae s. s.

Besides Monoecocestus (for Taenia decrescens Diesing, 1856) and Quentinia, other available names for Monoecocestus-like species are Lentiella Rêgo, 1964 (for L. machadoi Rêgo, 1964) and Perutaenia Parra, 1953 (for Paranoplocephala threlkeldi Parra, 1952), both synonymized with Monoecocestus by Beveridge (1994). Schizotaenia Janicki, 1904 (for M. decrescens) is preoccupied and Pecarezia Spasskii, 1999, which has the same type species as Monoecocestus (M. decrescens), is a junior synonym of the latter genus. The genus Lentiella was revalidated by Haverkost and Gardner (2008) on the grounds that the uterus of the type species L machadoi and that of Lentiella lamothei Haverkost & Gardner, 2008 is tubular, thus differing from the reticular early uterus of Monoecocestus. However, the illustrations of mature proglottids by Rêgo (1964) and Haverkost and Gardner (2008) fail to show a tubular early uterus, but instead appear to show a finely reticulated uterus, particularly in the type species. Therefore, Lentiella should remain a junior synonym of Monoecocestus until the morphology of L machadoi and the features differentiating the former genus from Monoecocestus have been adequately described.

Among Monoecocestus spp., Q. mesovitellinica most resembles M. eljefe from G. musteloides, particularly with respect to the position of genital pores (anterior), the transverse and longitudinal position of female glands (median and anterior, respectively), the shape of the ovary (arched, symmetric), the shape and size of the vitellarium (globular, small) and the characteristics of the cirrus sac (slender and relatively short) (Fig. 1). The shared combination of features concerning the position of genital pores and female glands distinguishes Q. mesovitellinica and M. eljefe among Monoecocestus spp. (see the GCD). Monoecocestus eljefe seems to be differentiated from Q. mesovitellinica mainly by its massive ventral longitudinal osmoregulatory canals (Fig. 1), although this feature is highly variable in the former species (Haverkost and Gardner, 2010). Because of the morphologic similarity and distinctiveness of Q. mesovitellinica and M. eljefe among Monoecocestus-like species, the latter is assigned here to Quentinia as Q. eljefe (Haverkost & Gardner, 2010) n. comb.

Although Quentin (1994) placed Q. baltazardi in synonymy with Q. mesovitellinica, no grounds for this action were given. These taxa appear to differ somewhat with respect to the shape of the proglottids and fully developed uterus, but the morphology and relationships of other organs are qualitatively similar (Fig. 1). The comparison of these taxa is hindered by the fact that the material of Q. mesovitellinica is in poor condition, which is evident in the original description and also mentioned by the author (Rêgo, 1967). However, Q. mesovitellinica and Q. baltazardi share the main morphologic features that separate them from Catenotaenia s. l. and other catenotaeniids and associate with Monoecocestus sensu Beveridge (1994), i.e. the structure and position of the osmoregulatory canals, vagina, ovary and vitellarium, and the structure of the genital atrium and fully developed uterus (Table 1). Even if these taxa turn out to be different species, they should both be placed either in Monoecocestus or, as proposed here, in Quentinia, in the family Anoplocephalidae s. s. However, the conspecificity of Q. mesovitellinica and Q. baltazardi and the taxonomic position Q. eljefe with respect to the former species probably cannot be solved definitively without new morphologic and molecular data based on good-quality specimens.

Quentinia Spasskii, 1969 (Anoplocephalidae sensu stricto)

Syn. Quentinotaenia Tenora, Mas-Coma, Murai & Feliu, 1980

Type species: Q. mesovitellinica (Rêgo, 1967) Quentin, 1994, syns. Catenotaenia mesovitellinica Rêgo, 1967, Atriotaenia (Ershovia) baltazardi Quentin, 1967, Quentinia baltazardi (Quentin, 1967) Spasskii, 1969, Quentinotaenia mesovitellinica (Rêgo, 1967) Tenora, Mas-Coma, Murai & Feliu, 1980. The syntypes of Q. mesovitellinica are deposited in the Helminthological Collection of the Oswaldo Cruz Institute, Brazil; accession numbers were not given (Rêgo, 1967).

Other species: Q. eljefe (Haverkost & Gardner, 2010) n. comb., syn. Monoecocestus eljefe Haverkost & Gardner, 2010.

Diagnosis: Strobila slender, of intermediate length. Scolex small. Suckers large relative to size of scolex. Neck short and relatively wide with respect to scolex. Proglottids craspedote, shape from slightly wider than long to elongate. Genitalia single. Genital atrium usually prominent, capable of forming genital papilla. Genital pores opening in anterior third or fourth of proglottid margin; pores alternate irregularly in very short series. Two pairs of longitudinal osmoregulatory canals present, narrower dorsal canals lateral to ventral canals. Genital ducts pass ventral and dorsal osmoregulatory canals dorsally. Cirrus sac slender and relatively short; everted cirrus slender, armed with minute spines; elongate internal seminal vesicle present. External seminal vesicle slightly convoluted or sacculated. Testes largely posterior to female glands, confined by ventral longitudinal canals; few testes may be positioned lateral to vitellarium. Vagina as long as cirrus sac, widening distally, positioned ventral and anterior to cirrus sac and opening anterior to male pore. Seminal receptacle spherical or ovoid, overlapping ovary or lying posterior to it. Female glands median. Ovary arched, sparsely lobulated, antero-median. Vitellarium small, globular, positioned posterior to ovary. Structure of early uterus unknown. Fully developed uterus sparsely sacculated, confined by ventral longitudinal canals. Morphology of eggs in type species unknown; pyriform apparatus present in Q. eljefe. In Galea spp. (Caviidae, Hystricomorpha) in South America.

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