Open Access
Research Article
Issue
Parasite
Volume 29, 2022
Article Number 6
Number of page(s) 24
DOI https://doi.org/10.1051/parasite/2022002
Published online 09 February 2022

© D. Uhrovič et al., published by EDP Sciences, 2022

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Introduction

The members of the genus Archigetes Leuckart, 1878 are extraordinary among tapeworms due to their direct (monoxenic) life cycle, i.e., the lack of an intermediate host, with sexual maturation in the invertebrate host. Since its erection by Leuckart [25], the genus has been the subject of intense speculation about the origin of the tapeworm life cycle [28, 29]. The monoxenic life cycle, with the production of eggs by progenetic plerocercoids in the body cavity of oligochaetes, and excluding fish as a typical caryophyllidean definitive host, was considered by some authors to be an ancestral type of the cestode life cycle, assuming that invertebrates were primary hosts of the most ancient tapeworms [1, 5, 11, 52].

This monoxenic cycle was found in all five species of the genus Archigetes recognised as valid [5, 19]. Accidentally infected freshwater teleosts most likely served as a postcyclic host, which may have resulted in the life cycle being extended to two host, i.e., heteroxenic (indirect) life cycle [11]. An alternative view is that some Archigetes species evolved by progenesis, i.e., early development of the reproductive system leading to sexual maturity (including the production of eggs) in a larval stage [36]. This scenario is supported by some morphological and developmental data [41, 42].

Molecular data have clearly shown that Archigetes is neither the most basal lineage within all cestodes nor within the order Caryophyllidea [36, 50]. This means that sexual maturity in the invertebrate host is unlikely to have an impact on understanding of the protocestode state [36]. In contrast, these molecular phylogenetic studies show that at least three Archigetes species are members of the most recently diverging caryophyllidean lineage, which comprises almost entirely Nearctic caryophyllideans [50]. The available data thus support the hypothesis that the monoxenic life cycle of Archigetes is a secondary abbreviation of the developmental cycle, similar to some spathebothriideans, such as Cyathocephalus truncatus (Pallas, 1781), Diplocotyle olrikii Krabbe, 1874 or Spathebothrium simplex Linton, 1922, whose maturation and egg production may occur in gammarid amphipods as their intermediate host [20, 35, 46].

In addition to controversies over the position of Archigetes and the evolutionary origin of its monoxenic life cycle, there is much confusion about the species composition of the genus. Kennedy [19] considered the following five species as valid: A. sieboldi Leuckart, 1878 (type species); A. brachyurus Mrázek, 1908; A. cryptobothrius Wisniewski, 1928; A. limnodrili (Yamaguti, 1934) Kennedy, 1965; and A. iowensis. However, no taxonomical revision based on properly fixed material and molecular data has been carried out. Moreover, the taxonomic position of some caryophyllideans placed in the genera Biacetabulum Hunter, 1927, Brachyurus Szidat, 1938 and Paraglaridacris Janiszewska, 1950 is also problematic, as they morphologically resemble the species of Archigetes.

The genus Archigetes was first reported from North America by Ward [57] who found unidentified tapeworms resembling those of Archigetes spp. known from Europe in a fish from the Illinois River at Havana. The genus was for a long time represented in North America by only two species, A. iowensis Calentine, 1962, described from non-native common carp (Cyprinus carpio L.) and Limnodrilus hoffmeisteri Claparède [5], and A. sieboldi, reported from the same hosts [4]. Recently, Scholz and Pérez-Ponce de León [49] reported three morphotypes of Archigetes tapeworms, which may represent putative new species, from eastern shiners, Notropis spp. (Cypriniformes: Leuciscidae), and silverside, Chirostoma humboldtianum (Valenciennes) (Atheriniformes: Atherinidae) in the Nearctic part of Mexico. The latter fish is the first representative of the order Atheriniformes that has been reported as the host of caryophyllidean tapeworms [49].

Recent studies on North American caryophyllideans have revealed high diversity of these tapeworms, previously only partly described. Two new genera were erected and nine new species of the genera Biacetabulum Hunter, 1927, Promonobothrium Mackiewicz, 1968 and Isoglaridacris Mackiewicz, 1965 described [37, 39, 40, 49, 5456]. In the present paper, three new species of the enigmatic Archigetes are described from catostomid fishes from the southern United States (USA). In addition, species diversity of the genus is discussed together with the assessment of their phylogenetic relationships. The diagnosis of Archigetes is amended and a key to identification of North American taxa, including A. iowensis transferred to Paraglaridacris, is provided. Taxonomic status of morphologically similar species of the latter genus, which may also mature in oligochaetes, is discussed based on material from North America (USA), Asia (Japan) and Europe (Czech Republic, Russia and Slovakia).

Materials and methods

The specimens studied were newly collected by the present authors and their collaborators in Mississippi (USA), in 2012 and 2019. In addition, specimens from the private collection of the late John S. Mackiewicz (USA) donated to the senior author (T.S.) and vouchers deposited in the Helminthological Collection of the Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, České Budějovice (IPCAS) were examined.

Newly collected tapeworms were obtained from the intestines of freshly killed fish; they were rinsed with saline and fixed in hot, nearly boiling, 4% formaldehyde for morphological studies [38]. Some worms were fixed completely in 96% molecular-grade ethanol or in hot saline and then placed in 80% molecular-grade ethanol for DNA sequencing (see below). For light microscopy, specimens were stained in Mayer’s carmine, dehydrated in an ethanol series, cleared with clove oil (eugenol), and mounted in Canada balsam. Line drawings were made using a Leica DM 5000B light microscope (Leica Microsystems, Wetzlar, Germany). For scanning electron microscopy, selected specimens were examined using a Jeol I AM 6510LV and a Jeol JSEM 7401F electron microscope (Jeol Ltd., Tokyo, Japan) according to the procedure described by Oros et al. [38].

The phylogenetic relationships of the studied tapeworms were assessed based on the partial (D1–D3 region) nuclear ribosomal large subunit rRNA gene (lsrDNA) sequences. A list of sequenced samples and sequences used in the phylogenetic analysis is provided in Table 1. Genomic DNA was isolated using the Monarch Genomic DNA Purification Kit (New England Biolabs, Inc., USA), following the manufacturer’s instructions. A 1420 nucleotide (nt) long fragment of the 28S rRNA gene was amplified following the protocol described by Brabec et al. [3] or Scholz et al. [51]. An ExoSAP-IT PCR Cleanup enzymatic kit from Thermo Fisher Scientific, Inc. (Waltham, MA, USA) was used to purify the PCR products, following the manufacturer’s protocol. PCR amplicons were thereafter sequenced from both strands using the PCR primers and additional internal sequencing primer 300F and ECD2 [26]. Sequences were assembled and edited using Geneious version 11 (Biomatters, Auckland, New Zealand). The new lsrDNA sequences were aligned with the sequences of Archigetes spp. and Biacetabulum spp. available in GenBank using ClustalW implemented in Geneious ver. 11 (Biomatters, Auckland, New Zealand). The length of the final alignment was 1329 nucleotides (nt).

Table 1

Host, geographical origin and GenBank accession data for taxa included in the phylogenetic analysis.

Bayesian inference (BI) and maximum likelihood (ML) methods were used to assess phylogenetic relationships within the dataset. The best-fitting model for the analyses, GTR + I + G, was estimated using jModelTest 2.1.2 [10]. MrBayes software (ver. 3.2.3) [45] was used to perform the BI analysis. Markov chain Monte Carlo analyses were run for 10,000,000 generations, log-likelihood scores were plotted, and only the final 75% of trees were used to build the consensus tree. ML analysis was performed using PhyML version 3.0 [13] with nonparametric bootstrap validation based on 100 pseudoreplicates. FigTree ver. 1.4 software [44] was used to visualise the phylogenetic trees. To calculate genetic distances (uncorrected p-distance), a separate alignment including only sequences of Archigetes spp. (1356 nt) was used in MEGA ver. X [24].

In addition to IPCAS (see above), the studied specimens are deposited in the National Helminthological Collection of Mexico, Instituto de Biología, Universidad Nacional Autónoma de México, Mexico City, Mexico (CNHE), Harold W. Manter Laboratory, University of Nebraska, Lincoln, USA (HWML), and the National Museum of Natural History, Washington, D.C., USA (USNM). The terminology of the scolex morphology follows the proposal of Mackiewicz [30] and Oros et al. [39]. Terminology of microtriches follows Chervy [9]. The scientific and common names of fish hosts follow FishBase [12]. In descriptions, measurements are given in micrometres unless otherwise noted.

Host code numbers correspond to a unique individual fish host examined and small letters specify individual tapeworm(s) found in this host, i.e., correspond to morphological voucher(s). See Table 1.

Results

Molecular phylogeny

Molecular phylogenetic analysis, which included sequences of nine newly recovered isolates of Archigetes and sequences of this genus available in GenBank, revealed a well-supported monophyletic group (Fig. 1). Archigetes spp. were positioned in three clades. Clade I contained isolates of two morphologically distinct species, i.e., the type species of the genus, A. sieboldi, from Europe and Japan and a putative new species from I. bubalus collected in North America. The genetic divergence within this clade was 0–5 nt (0–0.37%). In contrast to conspicuous morphological differences (see below), the interspecific divergence between A. sieboldi and this new species was rather low and ranged between 1 and 5 nt (0.08–0.37%). Clades II and III contained isolates representing two species from Ictiobus spp. in North America that were recognised as species new to science. Sequences of Clade II were identical. The three new species are described below. The nucleotide divergence of sequences of each isolate is summarised in Supplementary Table S1.

thumbnail Figure 1

Bayesian phylogram of lsrDNA for (Cestoda: Caryophyllidea) Nodal support from Bayesian inference (BI) and maximum likelihood (ML) bootstrap support are indicated as BI/ML; values < 0.90 (BI) and < 70 (ML) are not shown. The scale bar indicates the expected number of substitutions per site. The newly generated sequences are highlighted in bold. Coloured rectangles indicate new species of Archigetes identified in this study Abbreviation: MS, Mississippi (country code for host field numbers). Archigetes megacephalus (MW027493 and MW027494) correspond to Archigetes sp. 2, and Archigetes loculotruncatus (MW027502) corresponds to Archigetes sp. 1 in Scholz et al. [50].

Species diversity of Archigetes Leuckart, 1878

Several taxa have been placed in Archigetes, but only the four following species were recently recognised as valid [48]: A. sieboldi Leuckart, 1878 (type species); A. brachyurus Mrázek, 1908 (both species found in oligochaetes and fish [43]); A. cryptobothrius Wisniewski, 1928 (known only from oligochaetes); and A. iowensis (species reported from oligochaetes and fish). Scholz and Oros [48] erroneously listed Paraglaridacris limnodrili (Yamaguti, 1934) Mackiewicz, 1994 also among valid species of Archigetes. The validity of two species, namely A. brachyurus and A. cryptobothrius, which have been reported only from Europe [19, 43], could not be critically assessed because of the lack of properly fixed material and molecular data.

Archigetes sieboldi and A. iowensis also occur in North America and their taxonomic status and biogeography are briefly discussed below. In addition to the three unidentified morphotypes of Archigetes recently reported from Mexico [49], another three new species found in catostomids from the southern USA are described below based on morphological and molecular data.

Archigetes loculotruncatus n. sp. (Figs. 25; Table 2)

Syn.: Archigetes sp. 1 of Scholz et al. [50]

thumbnail Figure 2

Line drawings of Archigetes loculotruncatus n. sp. from Ictiobus bubalus (Rafinesque), Chotard Lake near Vicksburg, Mississippi, USA (host field code US 260d, IPCAS C-903/1, PBI-464). A total view (testes and vitelline follicles are not illustrated in the middle portion of the body), B anterior part with scolex, C posterior part. Abbreviations: cga – common genital atrium, cs – cirrus-sac, esv – external seminal vesicle, Mg – Mehlis’ gland, ov – ovary, povf – postovarian vitelline follicles, sr – receptaculum seminis, te testes, ut – uterus, va – vagina, vd – vas deferens, vf vitelline follicles.

Table 2

Comparative measurements of new species of Archigetes from ictiobine fish (Catostomidae) in Mississipppi, USA.

urn:lsid:zoobank.org:act:1C1DE51D-7DC2-41A6-9CCB-9AC1BC31089F

Type host: Ictiobus bubalus (Rafinesque), Smallmouth buffalo.

Other host: Ictiobus niger (Rafinesque), Black buffalo; Carpiodes cyprinus (Lesueur), Quillback (all Cypriniformes: Catostomidae, Ictiobinae).

Site in host: Anterior intestine.

Type locality: Chotard Lake near Vicksburg, Mississippi, USA (32.587867; −91.021317).

Additional localities: Pascagoula River, Benndale; Sunflower River, Indianola (all Mississippi, USA); Reelfoot Lake, Tennessee, USA.

Type material: Holotype from I. bubalus (host code No. US 260d) collected on 24 March 2012 (IPCAS C-903/1); three paratypes from I. bubalus (US 260d, US 257a) (IPCAS C-903/1); four paratypes from I. niger (US 244b) (HWML 216781; IPCAS C-903/2); two paratypes from I. bubalus (US 257a) (USNM 1661733).

Material studied: Four slides with eight whole-mounted specimens and five slides with sagittal and cross sections of another specimen from I. bubalus (US 257a and 260b – PBI464); five slides with nine specimens (one incomplete) and five slides with longitudinal and cross sections of another specimen from I. niger (US 244b); one slide with one whole-mounted specimen from C. cyprinus (host code No. US 262b), all specimens from Chotard Lake near Vicksburg, collected by the authors (R.K. and M.O.) on 23 and 24 March 2012; one slide with whole-mounted specimen from C. cyprinus (host code No. US 171a) from Pascagoula River, near Benndale, coll. by the same authors on 18 March 2012; one slide with whole-mounted specimen from I. bubalus (host code No. RF3/490), Reelfoot Lake, donated by J.S. Mackiewicz to T.S.; two slides with two immature specimens from I. niger (FR19_765), Sunflower River coll. by F. Reyda on 17 August 2019.

Representative DNA sequences and phylogenetic relationships: Sequences of one individual from I. bubalus (US 260d/PBI-464) in Mississippi were provided by Scholz et al. [50]: ssr DNA (GenBank Accession Nos. MW027441), lsr DNA (MW027502) and rrnL (MW027379); Scholz et al. [50]). This species differs most conspicuously from all other sequenced species in lsrDNA sequences by 16–20 nt (1.18–1.48%) (Supplementary Table S1).

Etymology: The species name loculotruncatus refers to the loculotruncate scolex, which is a unique characteristic of this new species among other members of the genus Archigetes.

Description (based on whole mounts of 21 specimens; for measurements – see Table 2): Caryophyllidea, Capingentidae sensu Scholz et al. [50]. Body elongate, with maximum width from mid-length to level of ovary, slightly tapering towards neck region anteriorly and sharply narrowing posterior to ovary towards pointed posterior end (Figs. 2A, 3A, 4A). Body covered with acicular fillitriches. Scolex loculotruncate (corresponding to scolex type illustrated in Fig. 5.3 by Mackiewicz [30]), wider than distinct, relatively long neck (Figs. 2A, 2B; 3A, 3B). Scolex with one median pair of ovoid acetabulum-like loculi, two pairs of shallower lateral loculi, and widely conical apical disc (Figs. 2B; 3B, 3C; 4A–4E; 5A–5C). Internal and external longitudinal musculature well-developed. Osmoregulatory canals in cortex, forming 12–14 pairs of narrow canals (Fig. 5D).

thumbnail Figure 3

Line drawings of Archigetes loculotruncatus n. sp. from Carpiodes cyprinus (Lesueur), Chotard Lake near Vicksburg, Mississippi, USA (US 262b, IPCAS C-903/3). A total view (testes and vitelline follicles are not illustrated in the middle portion of the body), B anterior part with scolex, C posterior part.

thumbnail Figure 4

Scanning electron micrographs of Archigetes loculotruncatus n. sp. A, B, C, F – from Ictiobus bubalus (Rafinesque) (US 257a and US 260d, IPCAS C-903/1, PBI-464); D – from I. niger (Rafinesque, 1818) (US 244b, IPCAS C-903/2), Chotard Lake near Vicksburg, Mississippi, USA; E – from I. niger (Rafinesque, 1818) (FR19_765, IPCAS C-903/2), Sunflower River in Indianola, Mississippi, USA. A – total view, B–E – variability in scolex shape, F – posterior part with common genital atrium.

thumbnail Figure 5

Histological section of Archigetes loculotruncatus n. sp. from Ictiobus niger (Rafinesque) (US 244b, IPCAS C-903/3), Chotard Lake near Vicksburg, Mississippi, USA. A – sagittal section of scolex; B, C – longitudinal sections of scolex; D – cross section of middle portion of body; E – sagittal section of genital pores. Abbreviations: cga – common genital atrium, cs – cirrus-sac, esv – external seminal vesicle, fgp – female gonopore, ilm – inner longitudinal muscles, mgp – male gonopore, orc – osmoregulatory canals, te testes, ut – uterus, vd – vas deferens, vf vitelline follicles.

Testes medullary, subspherical to widely oval (Figs. 2B, 2C; 3B, 3C; 5D). Anterior-most testes begin posterior to anterior-most vitelline follicles. Posteriorly, testes reach to level of external seminal vesicle, rarely up to cirrus-sac (Figs. 2C, 3C). Cirrus-sac subspherical to spherical, thick-walled, situated anterior to ovary. External seminal vesicle ovoid, thick-walled (Figs. 2C, 3C). Male genital pore opens anterior to female gonopore to common genital atrium (Fig. 5E).

Ovary butterfly-shaped, with follicular lateral wings (Figs. 2C, 3C). Vagina tubular, sinuous, widened to form elongate, narrow seminal receptacle anterodorsal to ovarian isthmus, joins uterus to form uterovaginal canal opening close to but separate from male gonopore at bottom of distinct genital atrium (corresponding to Fig. 5.24 of Mackiewicz [30]) (Figs. 2C, 3C, 4F, 5E). Preovarian vitelline follicles numerous, in medullary parenchyma (Figs. 2B, 2C; 3B, 3C; 5D). Preovarian vitelline follicles may be partially connected with postovarian vitelline follicles by a few follicles situated irregularly alongside (laterodorsal to) ovarian wings (Fig. 2C). Postovarian vitelline follicles relatively numerous, forming V-shaped field (Fig. 2C; Table 2).

Uterus forms several loops, with single loop extending slightly anterior to cirrus-sac (Figs. 2C, 3C); uterine glands well-developed, absent only in distal and proximal parts of uterus. Eggs operculate, without fully formed oncosphere in utero.

Differential diagnosis

The new species is the largest member of the genus with a total body length of 6.0–8.3 mm vs 1.1–3.5 mm in the other five valid species. It also differs from all valid species of Archigetes, including the other two new species described below, in possessing a loculotruncate (Figs. 2B; 3B, 3C; 4A–4E; 5A–5C), rather than a bothrioloculodiscate or bulboloculate scolex as reported in other species (for types of scoleces – see Mackiewicz [30]).

The new species is also distinguished from the five previously known species by (i) a relatively long neck, whose length represents 10–15% of the total body length and which is absent or indistinct in the other species; (ii) a butterfly-shaped ovary in the new species vs dumb-bell-shaped ovary; (iii) an elongate seminal vesicle, which is longer than the diameter of the cirrus-sac in the new species vs spherical and smaller than the cirrus-sac in the other valid species.

Remarks

The new species is placed in the genus Archigetes based on morphological and molecular data (see Fig. 1 in Scholz et al. [50]), but differs from nominal species in having a distinct, long neck and a butterfly-shaped ovary. Archigetes loculotruncatus has been found in two species of Ictiobus and in Carpiodes cyprinus, i.e., suckers of the subfamily Ictiobinae. Most specimens were found in Chotard Lake, a former branch of the Mississippi River on the Mississippi-Louisiana state line. However, some specimens have also been found in the quillback from the Pascagoula River near Benndale, in southeastern Mississippi, in black buffalo from the Sunflower River in Indianola, east of the Mississippi River in central Mississippi, and smallmouth buffalo from Reelfoot Lake in Tennessee. This indicates a relatively large range for the new species in the southern USA.

Archigetes megacephalus n. sp. (Figs. 68; Table 2)

Syn.: Archigetes sp. 2 of Scholz et al. [50]

thumbnail Figure 6

Line drawings of Archigetes megacephalus n. sp. from Ictiobus niger (Rafinesque), Chotard Lake near Vicksburg, Mississippi, USA (US 244b, IPCAS C-904/3, PBI-417). A total view (testes and vitelline follicles are not illustrated in the middle portion of the body), B anterior part with scolex, C posterior part.

urn:lsid:zoobank.org:act:66185BB1-AF2D-456C-BA5E-7A83385207CE

Type host: Ictiobus niger (Rafinesque), Black buffalo.

Other host: Ictiobus bubalus (Rafinesque), Smallmouth buffalo; Ictiobus cyprinellus (Valenciennes), Bigmouth buffalo (all Cypriniformes: Catostomidae, Ictiobinae).

Site in host: Anterior intestine.

Type locality: Chotard Lake near Vicksburg, Mississippi, USA (32.587867; −91.021317).

Additional localities: Pascagoula River, Wilkerson’s Ferry launch (all Mississippi, USA), Reelfoot Lake, Tennessee, USA.

Type material: Holotype from I. niger collected on 23 March 2012 (host code No. US 244b) (IPCAS C-904/3); two paratypes from I. niger (US 244b) (IPCAS C-904/3; USNM 1661735); seven paratypes from I. cyprinellus (US 242a) (HWML 216782; IPCAS C-904/1; USNM 1661734); one paratype from I. bubalus (IPCAS C-904/2).

Material studied: One slide with one whole-mounted specimen from I. bubalus (US 257b), collected by the present authors (R.K. and M.O.) on 24 March 2012; two slides with two specimens from I. bubalus (DNA-02-267D), coll. by R.M. Overstreet and S.S. Curran in 2002; five slides with eight whole-mounted specimens and one slide with longitudinal sections of another specimen from I. cyprinellus (host code No. US 242a – PBI-462); three slides with four specimens from I. niger (US 244b – PBI-417), coll. authors (R.K. and M.O.) on 23 March 2012; all specimens from Chotard Lake near Vicksburg; two slides with five whole-mounted specimens from I. bubalus (host code No. RF3/490), Reelfoot Lake, donated by J.S. Mackiewicz to T.S.

Representative DNA sequences and phylogenetic relationships: The lsrDNA sequences of one individual from I. bubalus (US 260b – OM103265), one from I. cyprinellus (US 242a/PBI-462 – MW027493), and three from I. niger (US 244b/PBI-417 – MW027494; OM103263; OM103264), all from Chotard Lake. Three novel sequences and two sequences retrieved from GenBank were identical. They differed from the sequence of Archigetes loculotruncatus n. sp. by 16 nt (1.18%) (Supplementary Table S1).

Etymology: The species name, mega – very big; cephalus – head or scolex, refers to a conspicuously large scolex, the width of which considerably exceeds that of the neck.

Description (based on whole mounts of 16 specimens; for measurements – see Table 2): Caryophyllidea, Capingentidae sensu Scholz et al. [50]). Body elongate, with maximum width near mid-length of body or at level of cirrus-sac, slightly and gradually tapering towards neck region anteriorly, with posterior part of body tapering from ovarian level (Figs. 6A, 7A, 8A). Body covered with acicular fillitriches. Scolex bothrioloculodiscate (see Fig. 5.4 in Mackiewicz [30]), spherical, robust, conspicuously (at least two times) wider than neck and body, with one pair of deep, ovoid acetabulum-like median loculi, two pairs of slightly shallower, but distinct lateral loculi, and widely convex apical disc (Figs. 6A, 6B; 7A–7D; 8A, 8B). Neck distinct, narrow, relatively short. Internal and external longitudinal muscles well-developed. Osmoregulatory canals narrow, numerous, in cortex.

thumbnail Figure 7

Scanning electron micrographs of Archigetes megacephalus n. sp. A, B – from Ictiobus bubalus (Rafinesque) (US 257a and US 260b, IPCAS C-904/2); C – from I. cyprinellus (Valenciennes, 1844) (US 242a, IPCAS C-904/1, PBI-462); D – from I. niger (Rafinesque) (US 244b, IPCAS C-904/3, PBI-417), Chotard Lake near Vicksburg, Mississippi, USA. A – total view, B – detail of scolex, C, E – variability in scolex shape.

thumbnail Figure 8

Histological section of Archigetes megacephalus n. sp. from Ictiobus cyprinellus (Valenciennes) (US 242a, IPCAS C-904/1, PBI-462), Chotard Lake near Vicksburg, Mississippi, USA. A – longitudinal section of body (total view); B – longitudinal section of scolex; D – longitudinal section of posterior part of body. Abbreviations: dlvf – dorsolateral vitelline follicles, cs – cirrus-sac, esv – external seminal vesicle, ilm – inner longitudinal muscles, ov – ovary, povf – postovarian vitelline follicles, te testes, ut – uterus, vf vitelline follicles.

Testes medullary, subspherical to widely oval (Figs. 6B, 6C). Anterior-most testes begin posterior to anterior-most vitelline follicles. Posteriorly, testes reach to level of external seminal vesicle (Fig. 6C), rarely to cirrus-sac level. Cirrus-sac spherical, thick-walled, anterior to ovary. External seminal vesicle elongate, thick-walled (Fig. 6C). Male genital pore anterior to female gonopore, opens separately to common genital atrium.

Ovary butterfly-shaped, follicular (Figs. 6C, 8C). Vagina tubular, sinuous, widened to form elongate, narrow seminal receptacle anterodorsal to ovarian isthmus, joins uterus to form uterovaginal canal, opening close to but separate from male gonopore at bottom of distinct genital atrium (see Fig. 5.24 of Mackiewicz [30]) (Fig. 6C).

Preovarian vitelline follicles numerous, in medullary parenchyma (Figs. 6B, 6C; 8A), almost always connected with postovarian group of vitelline follicles by continuous row of follicles situated alongside, laterodorsal to ovarian wings (Figs. 6C; 8A, 8C). Postovarian vitelline follicles relatively numerous, forming V-shaped field (Fig. 6C; Table 2).

Uterus forms several loops, one loop extending slightly anterior to cirrus-sac (Fig. 6C, 8C); uterine glands well-developed, absent only in distal and proximal parts of uterus. Eggs operculate, without fully formed oncosphere in utero.

Differential diagnosis

The new species differs from other congeneric species, including Archigetes loculotruncatus n. sp., by the shape and relative size of the scolex, which is bothrioloculodiscate and conspicuously (> 2×) wider than the body (Figs. 6A, 6B; 7A–7D; 8A, 8B). The new species can also be distinguished from A. loculotruncatus n. sp. by the presence of vitelline follicles nearly always present alongside the ovarian wings, whereas only some specimens of A. loculotruncatus n. sp. have a few follicles laterodorsal to the ovary and they never form a continuous row as in A. megacephalus n. sp. (compare Figs. 2C, 3C and 6C). In addition, the new species can be distinguished by some subtle biometrical differences (see also Table 2).

Remarks

Archigetes megacephalus n. sp. was found in all three species of buffalo (Ictiobus spp.) examined from Chotard Lake (western part of Mississippi State), and in smallmouth buffalo from Reelfoot Lake, Tennessee. The new species was found sympatric with A. loculotruncatus n. sp. in the anterior part of the intestine in three fish individuals, one black buffalo (US 244) and two smallmouth buffalo (US 257; RF3/490). These new species can be distinguished from each other mainly by the shape and size of the scolex and body length, but live cestodes are highly mobile and change shape, including the scolex. For this reason, identification of live specimens with the naked eye can be difficult in mixed infections. Specimens should be fixed with hot fixative so that they retain their natural shape and do not shrink unnaturally, as is typical for specimens fixed with unheated fixative.

Archigetes vadosus n. sp. (Figs. 9, 10; Table 2)

urn:lsid:zoobank.org:act:21724C2F-6202-4E5D-A514-D9D832598A12

thumbnail Figure 9

Line drawings of Archigetes vadosus n. sp. from Ictiobus bubalus (Rafinesque), Bluff Creek, Pascagoula River, Mississippi, USA (host field codes US 862d, IPCAS C-905/1). A total view (testes and vitelline follicles are not illustrated in the middle portion of the body), B anterior part with scolex, C posterior part.

thumbnail Figure 10

Scanning electron micrographs of Archigetes vadosus n. sp. from Ictiobus bubalus (Rafinesque) A, C – specimens from host field codes US 831d, Oxbow south of Cumbest Bridge landing, Pascagoula River, Mississippi, USA; B – specimen from host code FR19_765, Sunflower River in Indianola, Mississippi, USA; D – specimen from host code US 862d (all specimens IPCAS C-905/1), Bluff Creek, Pascagoula River, Mississippi, USA. A – total view, B – detail of scolex, C, D – variability in scolex shape.

Type host: Ictiobus bubalus (Rafinesque), Smallmouth buffalo (Cypriniformes: Catostomidae, Ictiobinae).

Site in host: Anterior intestine.

Type locality: Bluff Creek, Mississippi, USA (30.4568653; −88.6180754).

Additional localities: Pascagoula River and Sunflower River, Indianola (all Mississippi, USA), Reelfoot Lake (Tennessee, USA).

Type material: Holotype from I. bubalus (host code No. US 862d) collected on 23 June 2019 (IPCAS C-905/1); two paratypes (hologenophores) from I. bubalus (US 862b, c) (IPCAS C-905/1); one paratype from I. bubalus (US 831d-3), one paratype from I. bubalus (US 863c) (USNM 1661736); two paratypes from I. bubalus (US 869b) (HWML 216783; 216784; IPCAS C-905/1); one paratype from I. bubalus (US 871a) (USNM 1661737).

Material studied: Fifteen slides with 16 whole-mounted specimens from I. bubalus (US 827c, 831c, d, 862b–d, 863c, 866b, 869b and 871a) from Oxbow south of Cumbest Bridge landing on the Pascagoula River and Bluff Creek, collected by the present authors (R.K., M.O. and T.S.) on 19 and 23 June 2019; one slide with two whole-mounted specimens from I. bubalus (FR19_655), Oxbow on the Pascagoula River, Vancleave, coll. by F. Reyda on 12 August 2019; two slides with two whole-mounted specimens (one slide together with A. iowensis – see below) from I. bubalus (FR19_767) from Sunflower River, coll. by F. Reyda on 17 August 2019; four slides with eight whole-mounted specimens from I. bubalus (host code No. RF3/490), Reelfoot Lake, donated by J.S. Mackiewicz to T.S.

Representative DNA sequences and phylogenetic relationships: The lsrDNA sequences of six individuals from I. bubalus (US 828a, 3× 831d, 862b and 862c – OM103266OM103271). Sequence divergence among individual isolates of A. vadosus n. sp. was 0–4 nt (0–0.30%). They differed from sequence of A. loculotruncatus n. sp. by 17–20 nt (1.33–1.41%), from sequences of A. megacephalus n. sp. by 4–5 nt (0.30–0.37%), and from sequences of A. sieboldi by 1–5 nt (0.08–0.37%).

Etymology: The species name vadosus (= shallow in Latin) refers to the unusually shallow pair of median loculi.

Description (based on whole mounts of 16 specimens; for measurements – see Table 2): Caryophyllidea, Capingentidae sensu Scholz et al. [50]). Body elongate, with maximum width at middle of body, slightly tapering towards neck region anteriorly and narrowing gradually towards posterior end (Figs. 9A, 10A). Body covered with acicular fillitriches. Scolex bulboloculate, i.e., bulbous, wider than neck, with three pairs of loculi, one pair of shallow median ovoid loculi, two pairs of indistinct lateral loculi and indistinct apical disc forming small apical cone (Figs. 9A, 9B; 10B–10D). Neck short. Internal and external longitudinal muscles well-developed. Osmoregulatory canals numerous, narrow, in cortex.

Testes medullary, subspherical to widely oval (Fig. 9B, 9C). Anterior-most testes begin posterior to anterior-most vitelline follicles. Posteriorly, testes reach to level of external seminal vesicle or to anterior margin of cirrus-sac (Fig. 9C). Cirrus-sac subspherical to spherical, thick-walled. External seminal vesicle elongate, thick-walled. Male genital pore opens anterior to female gonopore to common genital atrium.

Ovary butterfly-shaped, follicular (Fig. 9C). Vagina tubular, sinuous, widened to form elongate, narrow seminal receptacle anterodorsal to ovarian isthmus, joins with uterus to form uterovaginal canal, opening close to but separate from male gonopore (Fig. 9C) at bottom of distinct genital atrium (see Fig. 5.24 of Mackiewicz [30]). Preovarian vitelline follicles numerous, in medullary parenchyma, reaching posteriorly to ovary, but always absent alongside ovary (Fig. 9C). Postovarian vitelline follicles relatively numerous, reaching ovary, forming V-shaped field (Fig. 9C).

Uterus forms several loops, one loop extending anterior to cirrus-sac (Fig. 9C); uterine glands well-developed, absent only in distal and proximal parts of uterus. Eggs operculate, without fully formed oncosphere in utero.

Differential diagnosis

The new species differs from the five previously known species of Archigetes by having an elongate body with a distinct neck, and from the two new species by possessing a bulboloculate scolex with shallow median loculi, almost indistinct lateral loculi and indistinct apical disc (Figs. 9A, 9B; 10B–10D). Archigetes vadosus n. sp. can also be distinguished from most congeners by the complete absence of vitelline follicles alongside the ovarian wings (present in other species). Other biometrical differences from A. loculotruncatus n. sp. and A. megacephalus n. sp. are obvious in Table 2. The new species is closely related to A. sieboldi (Fig. 1), but differs considerably by body shape, especially the presence of a distinct neck region which separates the scolex from the remaining body, a butterfly-, rather than dumb-bell-shaped ovary, and the external seminal vesicle longer than the diameter of the cirrus-sac.

Remarks

Archigetes vadosus n. sp. was found in only one species of buffalo, I. bubalus, in the Pascagoula River, neighbouring Bluff Creek, Mississippi, and Reelfoot Lake, Tennessee. One smallmouth buffalo from Reelfoot Lake harboured all three new species, one A. loculotruncatus, five A. megacephalus, and eight A. vadosus. Interestingly, A. vadosus n. sp. was not found in Chotard Lake, where two other new species commonly occurred in two smallmouth buffaloes examined.

Paraglaridacris limnodrili (Yamaguti, 1934) Mackiewicz, 1994 (Fig. 11)

Syns.: Glaridacris limnodrili Yamaguti, 1934; Archigetes limnodrili (Yamaguti, 1934) Kennedy, 1965; Archigetes iowensis Calentine, 1962 (new synonym)

thumbnail Figure 11

Line drawing of Paraglaridacris limnodrili (Yamaguti, 1934) Mackiewicz, 1994 (synonym Archigetes iowensis Calentine, 1962). from Ictiobus bubalus (Rafinesque) (FR19_767, IPCAS C-588/3), Sunflower River in Indianola, Mississippi, USA. Abbreviations: cga – common genital atrium, cs – cirrus-sac, esv – external seminal vesicle, Mg – Mehlis’ gland, ov – ovary, povf – postovarian vitelline follicles, te testes, ut – uterus, vd vas deferens, vf vitelline follicles.

Type host: Cyprinus carpio Linnaeus, Common carp (Cypriniformes: Cyprinidae).

Other hosts: Ictiobus bubalus (Rafinesque), Smallmouth buffalo (Cypriniformes: Catostomidae, Ictiobinae) (new host record); Limnodrilus hoffmeisteri Claparède, Red worm (Clitellata: Naididae) (progenetic plerocercoids).

Site in host: Anterior intestine (fish) and body cavity (naidids).

Type locality: Iowa River, Hardin County, Iowa, USA.

Distribution: Whole USA (Iowa, Mississippi – new geographical record, Wisconsin).

Type specimens: Holotype from C. carpio (USNM 1355440); paratype from L. hoffmeisteri (USNM 1355441).

Material studied: One specimen from the intestine of I. bubalus (host code No. FR-19_767; IPCAS C-588/3), Sunflower River, Indianola, Mississippi, collected by F. Reyda on 17 August 2019; one specimen from the body cavity of L. hoffmeisteri, locality unspecified, donated by J.S. Mackiewicz to T.S. (IPCAS C-588/1); four whole-mounted specimens and two slides with longitudinal sections of another specimen from Cyprinus carpio (BN C-78), Wisconsin, USA, coll. by R.L. Calentine in 1966 and donated by J.S. Mackiewicz to T.S. (IPCAS C-588/2).

Representative DNA sequences: Not available.

Redescription (based on six specimens; for measurements – see Table 3): Caryophyllidea, Capingentidae sensu Scholz et al. [50]). Body narrowly ovoid, with maximum width at level of cirrus-sac or external seminal vesicle, slightly tapering towards neck region (Fig. 11). Scolex bothrioloculodiscate (see Fig. 5.4 in Mackiewicz [30]), slightly wider than neck, with one pair of shallow acetabulum-like loculi, two pairs of indistinct lateral loculi, and well-developed apical disc (Fig. 11). Neck short, but distinct, slightly narrower than body width. Internal and external longitudinal muscles well-developed. Osmoregulatory canals narrow, numerous, in cortex.

Table 3

Comparative measurements of Paraglaridacris limnodrili (Yamaguti, 1934) Mackiewicz, 1994 (synonym Archigetes iowensis Calentine, 1962).

Testes medullary, subspherical to widely oval (Fig. 11), with first testes anterior to anterior-most vitelline follicles. Posteriorly, testes reach to cirrus-sac (Fig. 11). Cirrus-sac subspherical, thick-walled. External seminal vesicle ovoid, thick-walled, shorter than cirrus-sac. Male genital pore anterior to female gonopore, opens to common genital atrium.

Ovary compact (non-follicular), dumb-bell-shaped (Fig. 11). Vagina tubular, slightly sinuous, widened to form elongate, narrow seminal receptacle anterodorsal to ovarian isthmus, joins uterus to form uterovaginal canal that opens separately from male gonopore into small, but distinct genital atrium (corresponding to Fig. 5.24 of Mackiewicz [30]; Fig. 11). Preovarian vitelline follicles numerous, in medullary parenchyma. Postovarian vitelline follicles relatively numerous, forming U-shaped field (Fig. 11; Table 3). Fields of preovarian and postovarian vitelline follicles continuous, connected by follicles dorsolateral to lateral ovarian wings.

Uterus forms several loops, with distal part of uterus not extending farther anteriorly than cirrus-sac (Fig. 11). Uterine glands well-developed, absent only in distal and proximal parts of uterus. Eggs operculate, without fully formed oncospheres in utero.

Remarks

Calentine [5] described A. iowensis based on adults found in common carp and progenetic plerocercoids in the naidid L. hoffmeisteri from the Iowa River. The same author [6] studied the life cycle of this species in laboratory conditions. Thereafter, the species was found in common carp from the Red Cedar River in Wisconsin by D.R. Sutherland in 1979 (voucher deposited as USNM 1397329), but this record does not seem to have been published. Williams [58] also found A. iowensis in L. hoffmeisteri in Wisconsin (USNM 1370351, 1370352), but designated his specimens as “Archigetes limnocesti”, which is a non-existing name (nomen nudum).

Comparison of North American specimens of A. iowensis from cypriniforms and oligochaete host with those of Paraglaridacris limnodrili from the Palearctic region has revealed that these species can be distinguished from each other neither by their morphology nor measurements [18, 43, 61].

Both species are typified by (i) a compact, dumb-bell-shaped ovary; (ii) a small body separated by a short, but distinct neck, which is slightly narrower than the scolex, anterior-most testes being always anterior to anterior-most vitelline follicles; (iii) largely lateral preovarian vitelline follicles, with a very few median folllicles (Calentine [5] originally the preovarian vitelline follicles were reported as exclusively lateral, but Mackiewicz [30] corrected this characteristic); (iv) vitelline follicles uninterrupted alongside (dorsolateral) the ovarian wings, thus making bands of pre- and postovarian follicles continuous; (v) the uterus reaching anteriorly only to the anterior margin of the cirrus-sac; and (vi) external seminal vesicle shorter than the diameter of the cirrus-sac. Archigetes iowensis and P. limnodrili have been found as adults in cypriniforms and as progenetic plerocercoids in oligochaetes [5, 61]. Based on the rule of priority, A. iowensis becomes a junior synonym of P. limnodrili and the number of valid species of Archigetes is reduced to six (three new species, A. sieboldi, A. brachyurus and A. cryptobothrius).

Archigetes sieboldi Leuckart, 1878

Syns.: Archigetes appendiculatus Mrázek, 1898; Biacetabulum sieboldi Szidat, 1937; Archigetes sp. 3 of Scholz and Pérez-Ponce de León [49] (new synonym)

Type host: Limnodrilus hoffmeisteri Claparède, Red worm (Clitellata: Naididae).

Other hosts (in North America only; all hosts see in Protasova et al. [43]): Common carp, Cyprinus carpio (Cypriniformes: Cyprinidae); shortfin silverside, Chirostoma humboldtianum (Valenciennes) (Atheriniformes: Atherinidae) (new host record).

Site in host: Body cavity (progenetic plerocercoids in oligochaetes); intestine (adults in fish).

Type locality: Ponds and puddles around Leipzig, Germany.

Distribution: Kinnickinnic River, River Falls, Wisconsin, USA [4]; Lago de Zacapu, Michoacán, Mexico [49] (for record out of North America see in Protasova et al. [43]).

Morphological description: Mrázek [32], Kennedy [19], Calentine and DeLong [4], Protasova et al. [43].

Material studied: seven plerocercoids from L. hoffmeisteri and L. udekemianus Claparède; two adults from C. carpio, both from several fishponds in South Bohemia, Czech Republic, collected by F. Moravec and T.S. between 1984 and 1988 (IPCAS C-45/1, C-45/5, and C-45/2, respectively) [31]; 13 adults from C. carpio, Tisa River near Velké Trakany, Slovakia, coll. by M.O. and V. Hanzelová in June 2006 and 2007, and April 2008 (host code Nos. 263/06, 155/07, 159/07, 17/08 and 20/8); one adult from Blicca bjoerkna (L.), Latorica River, Slovakia, coll. by R. Ergens in 1964 (IPCAS C-45/3); two adults from Abramis brama (L.), two fishponds in Průhonice park near Prague and České Budějovice, respectively, coll. by T.S. in 1983 and 1990 (IPCAS C-45/4); two adults from Pseudorasbora parva (Temminck & Schlegel), and two adults from Rhynchocypris lagowskii (Dybowski), Lake Suwa, Japan, coll. by T. Shimazu in 1992 (IPCAS C-45/6 and C-45/8, respectively); six adults from Gnathopogon elongatus (Temminck & Schlegel), Kawashima, Japan, coll. by M. Urabe in 2002, 2003 and 2012 (IPCAS C-45/7); six plerocercoids from Limnodrilus udekemianus, Latka River near Borok, Yaroslavl Region, Russia, coll. by L.G. Poddubnaya in 2000 (IPCAS C-368/1); one specimen from Chirostoma humboldtianum, Lago de Zacapu, Michoacán, collected by Berenit Mendoza-Garfias in November 2008 (CNHE 6801; identified as Archigetes sp. 3 by Scholz and Pérez-Ponce de León [49]).

Representative DNA sequences and phylogenetic relationships: Olson et al. [36] sequenced adult A. sieboldi from the fish host Gnathopogon elongatus (Temminck & Schlegel, 1846) in Japan and progenetic plerocercoid from the coelom of oligochaete L. hoffmeisteri in Russia: EU343744, EU343745 (ssr DNA; both sequences identical) and EU343736 (lsrDNA). Scholz et al. [50] sequenced adult A. sieboldi from gudgeon, Gobio gobio L. (Cyprinidae) from the Czech Republic: MW027431 (ssr DNA) and MW027492 (lsr DNA). The lsr DNA sequences of this species from both studies differed by 3 nt (0.24%).

Remarks

Calentine and DeLong [4] and Calentine [7] studied the life history of A. sieboldi from the Kinnickinnic River in Wisconsin. The authors concluded that gravid stages occur in oligochaetes and occasionally in fish because a high prevalence of infection with A. sieboldi in oligochaetes compared to its rare occurrence in fish indicates that A. sieboldi is primarily a parasite of oligochaetes. Wiśniewski [60] and Nybelin [34] in Europe failed to infect cyprinids, but Kulakovskaya [23] successfully infected cyprinids (tench – Tinca tinca (L.)) with A. sieboldi from oligochaetes.

The specimen from Chirostoma humboldtianum in Mexico, designated as Archigetes sp. 3 by Scholz and Pérez-Ponce de León [49] (CNHE 6801), corresponds in its morphology to A. sieboldi found by Calentine and DeLong [4] in the USA, including overall shape of the body, with the scolex of a similar width as the remaining body, a more anterior position of vitelline follicles compared to that of the anterior-most testes, follicular, dumb-bell-shaped ovary, preovarian vitelline follicles lateral and median, with follicles lacking at the ovarian level, thus making pre- and postovarian vitelline follicles separated. Therefore, this specimen is considered to belong to A. sieboldi from C. humboldtianum in Mexico and represents a new definitive host and new geographical area, but this fish species should be confirmed as a true host of A. sieboldi.

Unidentified species of Archigetes

Scholz and Pérez-Ponce de León [49] reported three morphotypes of Archigetes from two species of shiners, Notropis spp., and Chirostoma humboldtianum in the Nearctic part of Mexico. These specimens differ conspicuously from the newly described species from the USA in their much smaller size (total length up to 2.50 mm), dumb-bell-shaped ovary, uterine loops reaching far anterior to the cirrus-sac, and the external seminal vesicle smaller than the cirrus-sac.

All the three morphotypes can be distinguished from Paraglaridacris limnodrili (syn. A. iowensis) by the lateral and median position of preovarian vitelline follicles (follicles form two lateral bands only, with only very few median follicles in A. iowensis), and by much shallower loculi on the scolex in Mexican specimens (conspicuous, deep loculi in A. iowensis). The third morphotype from C. humboldtianum (Archigetes sp. 3) resembles in its morphology A. sieboldi found by Calentine and DeLong [4] in North America and is considered conspecific (see above).

Camp [8] found two caryophyllideans identified as Archigetes sp. in creek chub, Semotilus atromaculatus Mitchill (Cypriniformes: Leuciscidae), Sugar Creek, Normal, Illinois, USA. Voucher specimens were not available to the present authors.

Key to the identification of species of Archigetes Leuckart, 1878 and Paraglaridacris Janiszewska, 1950 in North America

Because of the lack of newly collected or museum material of A. brachyurus and A. cryptobothrius, the identification key includes only five species of both morphologically similar genera that occur in North America. Morphotypes Archigetes sp. 1 and sp. 2 from Mexico are not included (see above).

  • 1a. Ovary compact; anterior-most testes anterior to anterior-most vitelline follicles; median vitelline follicles almost completely absent (a few follicles may be present medially) ........................................................................................................................... P. limnodrili (synonym A. iowensis)

  • 1b. Ovary follicular; anterior-most testes posterior to anterior-most vitelline follicles; median vitelline follicles present ...... 2

  • 2a. Ovary butterfly-shaped; neck distinct, narrower than the body .............................................................................. 3

  • 2b. Ovary dumb-bell-shaped; neck indistinct, wider than the scolex ............................................................ A. sieboldi

  • 3a. Body short (length < 5 mm), scolex bothrioloculodiscate or bulboloculate .............................................................. 4

  • 3b. Body long (length > 5 mm), scolex loculotruncate ........................................................... A. loculotruncatus n. sp.

  • 4a. Scolex bothrioloculodiscate, conspicuously (> 2×) wider than the body .............................. A. megacephalus n. sp.

  • 4b. Scolex bulboloculate, only slightly wider than the body ............................................................... A. vadosus n. sp.

Discussion

Previously, only two nominal taxa of Archigetes have been reported in North America [47, 58]. New data greatly expand the known spectrum of definitive hosts for Archigetes species that now include also catostomids (suckers). Three new species were found in the southern part of the USA, whereas Paraglaridacris limnodrili (new syn. A. iowensis) and A. sieboldi were previously known only from the Midwest (Iowa and Wisconsin). The present study, together with previous studies by the present authors, clearly demonstrates that the Nearctic fauna of freshwater fish tapeworms is still severely underexplored and insufficiently known [21, 47].

All new North American species of Archigetes have an elongate body with a distinct, relatively long neck (usually absent or indistinct in species described in Europe), butterfly-shaped ovary, and a conical to globular scolex wider than the neck. The new species also share the presence of a small, shallow genital atrium to which the male and female (uterovaginal canal) gonopores open separately, thus not forming a single hermaphroditic duct. The presence of a single common gonopore or two separate gonopores has been considered taxonomically important at the genus-level. Mackiewicz [30] distinguished four types, but some of them are difficult to differentiate from each other, depending in part on the contraction or relaxation of the worm.

Species of Archigetes and the closely related genus Biacetabulum Hunter, 1927 should have a single gonopore according to Mackiewicz [30]. However, recent studies of Biacetabulum spp. have shown that the male and female gonopores are separate and do not form a hermaphroditic duct, but open into a shallow genital atrium (see [54, 55]). Thus, using the terminology of Mackiewicz [30] and his key to the genera of the Caryophyllidea, all species of these two genera would be classified as having separate gonopores, but in fact have a single pore – a mouth of the common genital atrium. This situation is consistent with observations of Yamaguti [61] and Protasova et al. [43].

Johnston and Muirhead [17] described, based on a single specimen, Biacetabulum tandani Johnston and Muirhead, 1950 from the plotosid catfish Tandanus tandanus (Mitchell) in Australia. The authors placed the species in Biacetabulum because of the anterior extent of the uterus far anterior to the cirrus-sac and the presence of two acetabulum-like loculi on the scolex. Scholz and Oros [48] recognised this species as valid, but Uhrovič et al. [56] questioned its generic assignment. However, B. tandani is provisionally retained in Biacetabulum until new material is available. The most intriguing features of this poorly known species are its occurrence in a very distant zoogeographical distribution from that of species of both genera, which occur in the Palaearctic and Nearctic zoogeographical regions, and the presence of an external seminal vesicle, which is a morphological characteristic present only in most species of the Capingentidae, including Archigetes and Biacetabulum (see [50]). A feasible explanation of the occurrence of B. tandani in Australia could be possible introduction of this species with imported common carp to Australia and subsequent host switch to local plotosid catfish which may represent an accidental host. However, there is no supporting evidence for this assumption because no data are available on the occurrence of caryophyllidean tapeworms in introduced common carp in Australia.

One of the interesting results of molecular analysis is that both European isolates of A. sieboldi fall within the same clade as A. vadosus n. sp. However, these tapeworms are not considered conspecific because they differ considerably from each other in their morphology, including shape of the ovary (butterfly-shaped in the new species versus dumb-bell-shaped in A. sieboldi), different spectrum of fish hosts (Catostomidae versus Cyprinidae) and partly zoogeographical distribution (southern USA versus Holarctic, with most records in Europe). Comparison of sequence data from A. sieboldi from North America with A. vadosus could be quite instructive, but no ethanol-fixed material of A. sieboldi from North America is available. Another obstacle to better understand relationships between caryophyllidean tapeworms is the existence of multiple mt haplotypes that most likely represent paralogs (i.e. numts), which were detected by Brabec et al. [3] in two mitochondrial genes (cox1 and nad3).

Molecular phylogenetic analysis also revealed that four North American species of Archigetes form a monophyletic group nested within the clade composed of Biacetabulum spp. (Fig. 1), which is consistent with the results in Scholz et al. [50]. The species of Archigetes form a sister lineage to the clade composed of the three so-called long-necked, recently described species of Biacetabulum from redhorses and spotted suckers [54].

The close relationship between the species of Archigetes and Biacetabulum is not surprising, and some species have been placed in both genera, such as Caryophyllaeus appendiculatus Ratzel, 1868 (probably larva of Caryophyllaeus laticeps (Pallas, 1781)) in Archigetes and Biacetabulum [19]. Hunter [14] mentioned close morphological similarity between these genera when he erected Biacetabulum and differentiated them only by exclusive egg production of progenetic plerocercoids in oligochaetes for species of Archigetes versus full maturation exclusively in teleosts for species of Biacetabulum.

Based on the ICZN [15] priority rule, Archigetes has priority and all species of Biacetabulum would be transferred to this genus, provided that both genera are considered synonymous. Unfortunately, no molecular data are available for the type species of B. infrequens Hunter, 1927. Therefore, the synonymy of the two genera is not yet proposed. However, these two genera could be distinguished from each other by a somewhat smaller body in Archigetes (less than 8 mm, usually less than 5 mm in Archigetes vs 4–16 mm in Biacetabulum), an H-shaped ovary in Biacetabulum vs dumb-bell-shaped ovary in Archigetes, the extent of vitelline follicles, which may be present alongside the ovary in Archigetes but are absent in Biacetabulum, and uterine loops extending slightly anterior to the cirrus-sac in Archigetes vs uterine loops extending far anterior to the cirrus-sac in Biacetabulum. The addition of three new species with a larger body and a butterfly-shaped ovary implies that the generic diagnosis of the genus should be amended:

Archigetes Leuckart, 1878

Amended generic diagnosis: Caryophyllidea: Capingentidae sensu Scholz et al. [50]. Body small (less than 10 mm, usually only a few mm), with maximum width most commonly at middle part of body. Inner longitudinal musculature well developed. Scolex bothrioloculodiscate, globulate or loculotruncate. Neck present or indistinct. Testes medullary. Cirrus-sac thick-walled, subspherical to spherical, anterior to ovary. External seminal vesicle present, thick-walled. Ovary follicular, dumb-bell- or butterfly-shaped, with short, wide lateral lobes and wide ovarian isthmus. Preovarian vitelline follicles medullary, lateral and median. Postovarian follicles present, may be continuous with preovarian follicles. Uterus forms several loops, with at least one loop extending anterior to cirrus-sac; uterine glands present. Male and female gonopores separate, not forming a hermaphroditic duct, but open into distinct common genital atrium. Eggs operculate, without fully formed oncosphere in utero. Parasites of cyprinids (Cyprinidae) and catostomids (Catostomidae, both Cypriniformes) in Holarctic Region. Progenetic plerocercoids in coelom of naidid oligochaetes.

Type species: Archigetes sieboldi Leuckart, 1878.

Additional species: Archigetes brachyurus Mrázek, 1908; Archigetes cryptobothrius Wiśniewski, 1928; Archigetes loculotruncatus n. sp.; Archigetes megacephalus n. sp.; Archigetes vadosus n. sp.

The taxonomy of the genus Archigetes is still insufficiently clear because European taxa were described superficially, without any type or voucher specimens deposited in collections. Archigetes brachyurus and A. cryptobothrius were described in the first third of the 20th century from oligochaetes L. hoffmeisteri from the Czech Republic and Poland, respectively [33, 59]. Both species seem to differ from each other especially in the shape of the scolex, with A. brachyurus having a hexagonal scolex with deep loculi and a distinct, narrow neck (see [33]), whereas A. cryptobothrius has a short scolex, only slightly wider than a wide, almost indistinct neck, and bears shallow median loculi (see [59]).

Kennedy [19] differentiated both species only by the number of testes, which in fact overlaps: 120–159 in several rows of 30–40 each in A. brachyurus, versus 154 in several rows of 18–26 each, in A. cryptobothrius. In addition, this differential criterion is questionable because of difficulties in reliably counting numerous testes and their aggregation in rows. Nevertheless, both species are considered valid by most authors [19, 43, 48]. Protasova et al. [43] reported several cyprinids as hosts of A. brachyurus, namely Abramis brama (L.), Barbus barbus (L.), Barbus petenyi Heckel, Gobio gobio, and Vimba vimba (L.). However, no details on geographical origin (Dniester, Prut or Northern Doniets basins) and morphology of these specimens were provided. Protasova et al. [43] illustrated only progenetic plerocercoids from L. hoffmeisteri but these larvae identified as A. brachyurus differ from each other considerably in the shape of the body and scolex, and in the number of testes. Archigetes cryptobothrius has been reported only once since its original description, in L. hoffmeisteri from the Susaa River at Møllebro and Nymøllebro in Denmark [2].

Mackiewicz [30] proposed Paraglaridacris Janiszewska, 1950 as the first available name for Brachyurus Szidat, 1938, which was preoccupied by Brachyurus Fischer-Waldheim, 1813 (a genus of rodents). Szidat [53] erected Brachyurus, apparently unaware that this generic name was preoccupied, to accommodate B. gobii Szidat, 1938, which he found in G. gobio from small fishpond around the former Prussian town of Rossitten (now Rybachy in the Kaliningrad enclave of Russia) in Curonian Spit. Kennedy [19] synonymised this species with Yamaguti’s [61] Glaridacris limnodrili as A. limnodrili. Mackiewicz [30] did not question conspecificity of both taxa, but considered G. limnodrili to belong to Brachyurus Szidat, 1938, nec Fischer-Waldheim, 1813 (= Paraglaridacris sensu Mackiewicz, 1994). Comparison of A. iowensis specimens with Paraglaridacris limnodrili did not reveal any difference in their morphology and measurements in the present study (Table 3). As a result, both taxa are considered conspecific, with A. iowensis becoming a new junior synonym of P. limnodrili.

The second species, Paraglaridacris silesiacus Janiszewska, 1950, was described based on a single decomposed specimen from common bream, A. brama, in Poland [16]. The author even considered the new species description as provisional (“Comprenant qu’il s’agit d’une espèce, probablement assez rare, je résolus d’en donner une description provisoire.”). Morphological description of this species was not detailed and Janiszewska [16] did not recognise the presence of postovarian vitelline follicles, which was later corrected by Mackiewicz [27], who studied the holotype of P. silesiacus.

The validity of Paraglaridacris sensu Mackiewicz, 1994 could not be confirmed using molecular data, because no ethanol-fixed material was available. However, validity of the genus is supported by the following morphological characteristics, in which this genus differs from Archigetes: (i) compact ovary (versus follicular in Archigetes); (ii) largely lateral preovarian vitelline follicles, with only very few follicles median (median follicles are common in Archigetes); (iii) more anterior position of the first testes compared to vitelline follicles (versus the testes usually posterior or at same level as the anterior-most vitelline follicles). The difference in the structure of the ovary is conspicuous and enables easy differentiation between the specimens of both genera. Therefore, Paraglaridacris is provisionally considered a valid genus. It should also be mentioned here that two of the present authors contributed to the existing confusion as to nomenclature of these tapeworms [48].

The host specificity of most species of Archigetes and P. limnodrili was previously considered narrow, especially in North America. Calentine [6] examined 975 fishes representing 20 species from the same locality and only the common carp was infected, as in experimental infections. He also examined four species of oligochaetes but only L. hoffmeisteri was infected, with the same results of experimental infections of oligochaetes. A similarly narrow host range was reported for A. sieboldi in North America [4, 7], but a presumably conspecific tapeworm was found in Chirostoma humboldtianum from Mexico by Scholz and Pérez-Ponce de León [49]. The present record of A. iowensis in smallmouth buffalo, i.e., fish of a different family (Catostomidae), also challenges the above-mentioned assumption about strict host specificity of these species at the level of fish definitive host. Indeed, a broader host spectrum has been reported for A. sieboldi and P. limnodrili in the Palaearctic region ([43, 21], present study) and for two of the three new species of Archigetes described herein, because they occur in three species of fish hosts.

Acknowledgments

We thank the two reviewers who provided helpful suggestions. Florian Reyda, Oneonta College, SUNY, New York State, kindly provided several specimens of Archigetes spp. from Mississippi to the present authors. Stephen S. Curran and Robin M. Overstreet, Gulf Coast Research Laboratory, Ocean Springs, Mississippi, supported stays of the present authors in Mississippi in 2012 and 2019; they also provided caryophyllideans from Chotard Lake and the Pascagoula River. Steve Curran and Eric Pulis helped the present authors considerably in capturing fish for parasitological examination. This study was partly supported by the Grant Agency VEGA (No. 2/0126/20), Ministry of Education, Sports and Youth of the Czech Republic (project LTAUSA18010; Czech-BioImaging LM2015062), and the Institute of Parasitology (RVO: 60077344). MO and TS also acknowledge the Fulbright Commission who supported their research stays in the USA.

References

  1. Bazitov AA. 1981. Caryophyllidea, their origin and position in the phylum of Platyhelminthes. Zhurnal Obshchei Biologii, 42, 920–927 (in Russian). [Google Scholar]
  2. Berg K. 1948. Biological studies on the River Susaa. Folia Limnologica Scandinavica, 4, 40–54. [Google Scholar]
  3. Brabec J, Scholz T, Králová-Hromadová I, Bazsalovicsová E, Olson PD. 2012. Substitution saturation and nuclear paralogs of commonly employed phylogenetic markers in the Caryophyllidea, an unusual group of nonsegmented tapeworms (Platyhelminthes). International Journal for Parasitology, 42, 259–267. [CrossRef] [PubMed] [Google Scholar]
  4. Calentine RL, DeLong BL. 1966. Archigetes sieboldi (Cestoda: Caryophyllaeidae) in North America. Journal of Parasitology, 52, 428–431. [CrossRef] [Google Scholar]
  5. Calentine RL. 1962. Archigetes iowensis sp. n. (Cestoda: Caryophyllaeidae) from Cyprinus carpio L. and Limnodrilus hoffmeisteri Claparède. Journal of Parasitology, 48, 513–524. [CrossRef] [Google Scholar]
  6. Calentine RL. 1964. The life cycle of Archigetes iowensis (Cestoda: Caryophyllaeidae). Journal of Parasitology, 50, 454–458. [CrossRef] [Google Scholar]
  7. Calentine RL. 1984. Biology of Archigetes (Caryophyllaeidae) in Limnodrilus hoffmeisteri (Tubificidae). Proceedings of the Helminthological Society of Washington, 51, 109–112. [Google Scholar]
  8. Camp JW. 1990. Helminths of Semotilus atromaculatus from Sugar Creek, McLean County, Illinois. Journal of the Helminthological Society of Washington, 57, 162–164. [Google Scholar]
  9. Chervy L. 2009. Unified terminology for cestode microtriches: a proposal from the International Workshops on Cestode Systematics in 2002–2008. Folia Parasitologica, 56, 199–230. [CrossRef] [PubMed] [Google Scholar]
  10. Darriba D, Taboada GL, Doallo R, Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772. [Google Scholar]
  11. Freeman R. 1973. Ontogeny of cestodes and its bearing on their phylogeny and systematics. Advances in Parasitology, 11, 481–557. [CrossRef] [PubMed] [Google Scholar]
  12. Froese R, Pauly D, Editors. 2021. FishBase. World Wide Web electronic publication. www.fishbase.org (accessed January 2021). [Google Scholar]
  13. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59, 307–321. [CrossRef] [PubMed] [Google Scholar]
  14. Hunter GW. 1927. Notes on the Caryophyllaeidae of North America. Journal of Parasitology, 14, 16–26. [CrossRef] [Google Scholar]
  15. International Code of Zoological Nomenclature. 1999. International Commission for Zoological Nomenclature. https://www.iczn.org/the-code/the-code-online/. [Google Scholar]
  16. Janiszewska J. 1950. Biacetabulum sieboldi Szidat est-elle la forme adulte d’Archigetes sieboldi Leuck? Zoologica Poloniae, 5, 57–65. [Google Scholar]
  17. Johnston TH, Muirhead NG. 1950. Some Australian caryophyllaeid cestodes. Records of the South Australian Museum, 9, 339–348. [Google Scholar]
  18. Kennedy CR. 1965. The life-history of Archigetes limnodrili (Yamaguti) (Cestoda: Caryophyllaeidae) and its development in the invertebrate host. Parasitology, 55, 427–437. [CrossRef] [Google Scholar]
  19. Kennedy CR. 1965. Taxonomic studies on Archigetes Leuckart, 1878 (Cestoda, Caryophyllidea). Parasitology, 55, 439–451. [CrossRef] [Google Scholar]
  20. Kuchta R, Pearson R, Scholz T, Ditrich O, Olson PD. 2014. Spathebothriidea: survey of species, scolex and egg morphology, and interrelationships of a non-segmented, relictual tapeworm group (Platyhelminthes: Cestoda). Folia Parasitologica, 61, 331–346. [CrossRef] [PubMed] [Google Scholar]
  21. Kuchta R, Řehulková E, Francová K, Scholz T, Morand S, Šimková A. 2020. What do we know about parasites of cypriniform fishes? Diversity of monogeneans and tapeworms across two continents. International Journal for Parasitology, 50, 771–786. [CrossRef] [PubMed] [Google Scholar]
  22. Kulakovskaya OP. 1961. On the fauna of the Caryophyllaeidae (Cestoda, Pseudophyllidea) of the USSR. Parazitologicheskij Sbornik, 20, 339–354 (in Russian). [Google Scholar]
  23. Kulakovskaya OP. 1962. Data on the progenetic cestodes in the body of Oligochaeta. Dopovidi Akademii Nauk Ukrainian SSR, 6, 825–829 (in Russian). [Google Scholar]
  24. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35, 1547–1549. [CrossRef] [PubMed] [Google Scholar]
  25. Leuckart R. 1878. Archigetes sieboldi, eine geschlechtsreife Cestodenamme. Zeitschrift für Wissenschaftliche Zoologie, 30(Suppl.), 593–606. [Google Scholar]
  26. Littlewood DTJ, Curini-Galletti M, Herniou EA. 2000. The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Molecular Phylogenetics and Evolution, 16, 449–466. [CrossRef] [PubMed] [Google Scholar]
  27. Mackiewicz JS. 1965. Isoglaridacris bulbocirrus gen. et sp. n. (Cestoidea: Caryophyllaeidae) from Catostomus commersoni in North America. Journal of Parasitology, 51, 377–381. [CrossRef] [Google Scholar]
  28. Mackiewicz JS. 1972. Caryophyllidea (Cestoidea): A review. Experimental Parasitology, 31, 417–512. [CrossRef] [PubMed] [Google Scholar]
  29. Mackiewicz JS. 1981. Caryophyllidea (Cestoidea): Evolution and classification. Advances in Parasitology, 19, 139–206. [CrossRef] [Google Scholar]
  30. Mackiewicz JS. 1994. Order Caryophyllidea van Beneden in Carus, 1863, in Keys to the cestode parasites of vertebrates. Khalil LF, Jones A, Bray RA, Editors. CAB International: Wallingford. p. 21–43. [Google Scholar]
  31. Moravec F. 1986. The finding of the caryophyllaeid cestode Archigetes sieboldi Leuckart, 1878 in carp in Czechoslovakia. Folia Parasitologica, 33, 69–70. [Google Scholar]
  32. Mrázek A. 1898. Archigetes appendiculatus Ratz. Věstník Královské České Společnosti Náuk, 32, 1–47. [Google Scholar]
  33. Mrázek A. 1908. Ueber eine neue Art der Gattung Archigetes. Zentralblatt für Bakteriologie und Parasitenkunde., 46, 719–723. [Google Scholar]
  34. Nybelin O. 1962. Zur Archigetes-Frage. Zoologiska Bidrag från Uppsala, 35, 292–306. [Google Scholar]
  35. Okaka CE. 2000. Maturity of the procercoid of Cyathocephalus truncatus (Eucestoda: Spathebothriidae) in Gammarus pulex (Crustacea: Amphipoda) and the tapeworm life cycle using the amphipod as the sole host. Helminthologia, 37, 153–157. [Google Scholar]
  36. Olson PD, Scholz T, Poddubnaya LG, Littlewood DTJ. 2008. On the derived position of Archigetes and the early evolution of the tapeworms (Platyhelminthes: Cestoda). Journal of Parasitology, 94, 898–904. [CrossRef] [PubMed] [Google Scholar]
  37. Oros M, Brabec J, Kuchta R, Choudhury A, Scholz T. 2016. A synoptic review of Promonobothrium Mackiewicz, 1968 (Cestoda: Caryophyllidea), parasites of suckers (Catostomidae) in North America, with description of two new species. Folia Parasitologica, 63, 008. [CrossRef] [Google Scholar]
  38. Oros M, Scholz T, Hanzelová V, Mackiewicz JS. 2010. Scolex morphology of monozoic cestodes (Caryophyllidea) from the Palaearctic Region: a useful tool for species identification. Folia Parasitologica, 57, 37–46. [CrossRef] [PubMed] [Google Scholar]
  39. Oros M, Uhrovič D, Choudhury A, Mackiewicz JS, Scholz T. 2020. Scolex morphology of monozoic tapeworms (Caryophyllidea) from the Nearctic Region: taxonomic and evolutionary implications. Folia Parasitologica, 67, 003. [CrossRef] [Google Scholar]
  40. Oros M, Uhrovič D, Scholz T. 2018. A new classification of Glaridacris Cooper, 1920 (Cestoda: Caryophyllidea), parasites of suckers (Catostomidae) in North America, including erection of Pseudoglaridacris n. gen. Journal of Parasitology, 104, 60–69. [CrossRef] [PubMed] [Google Scholar]
  41. Poddubnaya LG, Davydov VG, Kuperman BI. 1984. A morpho-functional study of Archigetes sieboldi Leuckart (1878) (Cestoda: Caryophyllidea) concerning the peculiarities of its life cycle. Doklady AN SSSR, 276, 1010–1013 (in Russian). [Google Scholar]
  42. Poddubnaya LG, Mackiewicz JS, Kuperman BI. 2003. Ultrastructure of Archigetes sieboldi (Cestoda: Caryophyllidea): relationship between progenesis, development and evolution. Folia Parasitologica, 50, 275–292. [CrossRef] [PubMed] [Google Scholar]
  43. Protasova EP, Kuperman BI, Roitman VA, Poddubnaya LG. 1990. Caryophyllid tapeworms of the Fauna of USSR. Nauka: Moscow, 237 pp. (in Russian). [Google Scholar]
  44. Rambaut A. 2012. FigTree v1. 4. Molecular evolution, phylogenetics and epidemiology. Institute of Evolutionary Biology, University of Edinburgh: Edinburgh, UK. Retrieved from http://tree.bio.ed.ac.uk/software/figtree [Google Scholar]
  45. Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Huelsenbeck JP. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542. [CrossRef] [PubMed] [Google Scholar]
  46. Sandeman IM, Burt MDB. 1972. The biology of Bothrimonus (= Diplocotyle) (Pseudophyllidea: Cestoda): ecology, life cycle, and evolution; a review and synthesis. Journal of the Fisheries Research Board of Canada, 29, 1381–1395. [CrossRef] [Google Scholar]
  47. Scholz T, Choudhury A. 2014. Parasites of freshwater fishes in North America: Why so neglected? Journal of Parasitology, 100, 26–45. [CrossRef] [PubMed] [Google Scholar]
  48. Scholz T, Oros M. 2017. Caryophyllidea van Beneden in Carus, 1863, in Planetary Biodiversity Inventory (2008–2017): Tapeworms from vertebrate bowels of the Earth. Caira JN, Jensen K, Editors. University of Kansas, Natural History Museum, Special Publication No. 25: Lawrence, Kansas. p. 47–64. [Google Scholar]
  49. Scholz T, Pérez-Ponce de León G., de León G. 2021. Caryophyllidean tapeworms (Cestoda), Nearctic parasites of fish in Mexico, including description of a new species of Isoglaridacris and the first report of Khawia japonensis, an invasive parasite of common carp (Cyprinus carpio). International Journal for Parasitology: Parasites and Wildlife, 15, 70–78. [CrossRef] [Google Scholar]
  50. Scholz T, Waeschenbach A, Oros A, Brabec J, Littlewood DTJ. 2021. Phylogenetic reconstruction of early diverging tapeworms (Cestoda: Caryophyllidea) reveals ancient radiations in vertebrate hosts and biogeographic regions. International Journal for Parasitology, 51, 263–277. [CrossRef] [PubMed] [Google Scholar]
  51. Scholz T, de Chambrier A, Kuchta R, Littlewood DT, Waeschenbach A. 2013. Macrobothriotaenia ficta (Cestoda: Proteocephalidea), a parasite of sunbeam snake (Xenopeltis unicolor): example of convergent evolution. Zootaxa, 3640, 485–499. https://doi.org/10.11646/zootaxa.3640.3.12. [CrossRef] [PubMed] [Google Scholar]
  52. Stunkard HW. 1975. Life-histories and systematics of parasitic flatworms. Systematic Zoology, 24, 378–385. [CrossRef] [Google Scholar]
  53. Szidat L. 1938. Brachyurus gobii n. g. n. sp., eine neue Caryophyllaeiden-Art aus dem Grundling, Gobio fluviatilis Cuv. Zoologischer Anzeiger, 124, 249–258. [Google Scholar]
  54. Uhrovič D, Oros M, Kudlai O, Choudhury A, Scholz T. 2021. Molecular evidence of three closely related species of Biacetabulum Hunter, 1927 (Cestoda: Caryophyllidea): A case of recent speciation in different fish hosts (Catostomidae)? Parasitology, 148, 1040–1056. [CrossRef] [PubMed] [Google Scholar]
  55. Uhrovič D, Oros M, Reyda F, Kudlai O, Scholz T. 2021. Redescription of Biacetabulum giganteum Hunter, 1929 (Cestoda, Caryophyllidea) and description of two new, closely related species from suckers (Catostomidae) in North America. Systematics and Biodiversity, 19, 1062–1079. [CrossRef] [Google Scholar]
  56. Uhrovič D, Scholz T, Kudlai O, Oros M. 2021. Disentangling taxonomy of Biacetabulum (Cestoda, Caryophyllidea), parasites of catostomid fishes in North America: proposal of Megancestus gen. n. to accommodate B. carpiodi. Parasitology Research, 120, 1993–2001. [CrossRef] [PubMed] [Google Scholar]
  57. Ward HB. 1911. The discovery of Archigetes in America, with a discussion of its structure and affinities. Science, 33, 272–273. [Google Scholar]
  58. Williams DD. 1979. Archigetes iowensis (Cestoda: Caryophyllidea) from Limnodrilus hoffmeisteri (Annelida: Tubificidae) in Wisconsin. Proceedings of the Helminthological Society of Washington, 46, 272–274. [Google Scholar]
  59. Wiśniewski LW. 1928. Archigetes cryptobothrius n. sp. nebst Angaben die Entwicklung im Genus Archigetes, R. Leuck. Zoologischer Anzeiger, 77, 113–124. [Google Scholar]
  60. Wiśniewski LW. 1930. Das Genus Archigetes. Eine Studie zur Anatomie, Histogenese, Systematik und Biologie. Mémoires de l’Académie Polonaise des Sciences et Lettres, Classe des Sciences Mathématiques et Naturelles, Serie B, Sciences Naturelles, 2, 1–160. [Google Scholar]
  61. Yamaguti S. 1934. Studies on the helminth fauna of Japan. Part 4. Cestodes of fishes. Japanese Journal of Zoology, 6, 1–112. [Google Scholar]

Cite this article as: Uhrovič D, Oros M, Kudlai O, Kuchta R & Scholz T. 2022. Archigetes Leuckart, 1878 (Cestoda, Caryophyllidea): diversity of enigmatic fish tapeworms with monoxenic life cycles. Parasite 29, 6.

Supplementary Material

Table S1: Nucleotide comparison of the partial 28S rDNA sequences of Archigetes spp. based on 1,356 long alignment. P-distance (%) is given above diagonal and the number of variable nucleotides below diagonal. (Access here)

All Tables

Table 1

Host, geographical origin and GenBank accession data for taxa included in the phylogenetic analysis.

Table 2

Comparative measurements of new species of Archigetes from ictiobine fish (Catostomidae) in Mississipppi, USA.

Table 3

Comparative measurements of Paraglaridacris limnodrili (Yamaguti, 1934) Mackiewicz, 1994 (synonym Archigetes iowensis Calentine, 1962).

All Figures

thumbnail Figure 1

Bayesian phylogram of lsrDNA for (Cestoda: Caryophyllidea) Nodal support from Bayesian inference (BI) and maximum likelihood (ML) bootstrap support are indicated as BI/ML; values < 0.90 (BI) and < 70 (ML) are not shown. The scale bar indicates the expected number of substitutions per site. The newly generated sequences are highlighted in bold. Coloured rectangles indicate new species of Archigetes identified in this study Abbreviation: MS, Mississippi (country code for host field numbers). Archigetes megacephalus (MW027493 and MW027494) correspond to Archigetes sp. 2, and Archigetes loculotruncatus (MW027502) corresponds to Archigetes sp. 1 in Scholz et al. [50].

In the text
thumbnail Figure 2

Line drawings of Archigetes loculotruncatus n. sp. from Ictiobus bubalus (Rafinesque), Chotard Lake near Vicksburg, Mississippi, USA (host field code US 260d, IPCAS C-903/1, PBI-464). A total view (testes and vitelline follicles are not illustrated in the middle portion of the body), B anterior part with scolex, C posterior part. Abbreviations: cga – common genital atrium, cs – cirrus-sac, esv – external seminal vesicle, Mg – Mehlis’ gland, ov – ovary, povf – postovarian vitelline follicles, sr – receptaculum seminis, te testes, ut – uterus, va – vagina, vd – vas deferens, vf vitelline follicles.

In the text
thumbnail Figure 3

Line drawings of Archigetes loculotruncatus n. sp. from Carpiodes cyprinus (Lesueur), Chotard Lake near Vicksburg, Mississippi, USA (US 262b, IPCAS C-903/3). A total view (testes and vitelline follicles are not illustrated in the middle portion of the body), B anterior part with scolex, C posterior part.

In the text
thumbnail Figure 4

Scanning electron micrographs of Archigetes loculotruncatus n. sp. A, B, C, F – from Ictiobus bubalus (Rafinesque) (US 257a and US 260d, IPCAS C-903/1, PBI-464); D – from I. niger (Rafinesque, 1818) (US 244b, IPCAS C-903/2), Chotard Lake near Vicksburg, Mississippi, USA; E – from I. niger (Rafinesque, 1818) (FR19_765, IPCAS C-903/2), Sunflower River in Indianola, Mississippi, USA. A – total view, B–E – variability in scolex shape, F – posterior part with common genital atrium.

In the text
thumbnail Figure 5

Histological section of Archigetes loculotruncatus n. sp. from Ictiobus niger (Rafinesque) (US 244b, IPCAS C-903/3), Chotard Lake near Vicksburg, Mississippi, USA. A – sagittal section of scolex; B, C – longitudinal sections of scolex; D – cross section of middle portion of body; E – sagittal section of genital pores. Abbreviations: cga – common genital atrium, cs – cirrus-sac, esv – external seminal vesicle, fgp – female gonopore, ilm – inner longitudinal muscles, mgp – male gonopore, orc – osmoregulatory canals, te testes, ut – uterus, vd – vas deferens, vf vitelline follicles.

In the text
thumbnail Figure 6

Line drawings of Archigetes megacephalus n. sp. from Ictiobus niger (Rafinesque), Chotard Lake near Vicksburg, Mississippi, USA (US 244b, IPCAS C-904/3, PBI-417). A total view (testes and vitelline follicles are not illustrated in the middle portion of the body), B anterior part with scolex, C posterior part.

In the text
thumbnail Figure 7

Scanning electron micrographs of Archigetes megacephalus n. sp. A, B – from Ictiobus bubalus (Rafinesque) (US 257a and US 260b, IPCAS C-904/2); C – from I. cyprinellus (Valenciennes, 1844) (US 242a, IPCAS C-904/1, PBI-462); D – from I. niger (Rafinesque) (US 244b, IPCAS C-904/3, PBI-417), Chotard Lake near Vicksburg, Mississippi, USA. A – total view, B – detail of scolex, C, E – variability in scolex shape.

In the text
thumbnail Figure 8

Histological section of Archigetes megacephalus n. sp. from Ictiobus cyprinellus (Valenciennes) (US 242a, IPCAS C-904/1, PBI-462), Chotard Lake near Vicksburg, Mississippi, USA. A – longitudinal section of body (total view); B – longitudinal section of scolex; D – longitudinal section of posterior part of body. Abbreviations: dlvf – dorsolateral vitelline follicles, cs – cirrus-sac, esv – external seminal vesicle, ilm – inner longitudinal muscles, ov – ovary, povf – postovarian vitelline follicles, te testes, ut – uterus, vf vitelline follicles.

In the text
thumbnail Figure 9

Line drawings of Archigetes vadosus n. sp. from Ictiobus bubalus (Rafinesque), Bluff Creek, Pascagoula River, Mississippi, USA (host field codes US 862d, IPCAS C-905/1). A total view (testes and vitelline follicles are not illustrated in the middle portion of the body), B anterior part with scolex, C posterior part.

In the text
thumbnail Figure 10

Scanning electron micrographs of Archigetes vadosus n. sp. from Ictiobus bubalus (Rafinesque) A, C – specimens from host field codes US 831d, Oxbow south of Cumbest Bridge landing, Pascagoula River, Mississippi, USA; B – specimen from host code FR19_765, Sunflower River in Indianola, Mississippi, USA; D – specimen from host code US 862d (all specimens IPCAS C-905/1), Bluff Creek, Pascagoula River, Mississippi, USA. A – total view, B – detail of scolex, C, D – variability in scolex shape.

In the text
thumbnail Figure 11

Line drawing of Paraglaridacris limnodrili (Yamaguti, 1934) Mackiewicz, 1994 (synonym Archigetes iowensis Calentine, 1962). from Ictiobus bubalus (Rafinesque) (FR19_767, IPCAS C-588/3), Sunflower River in Indianola, Mississippi, USA. Abbreviations: cga – common genital atrium, cs – cirrus-sac, esv – external seminal vesicle, Mg – Mehlis’ gland, ov – ovary, povf – postovarian vitelline follicles, te testes, ut – uterus, vd vas deferens, vf vitelline follicles.

In the text

Current usage metrics show cumulative count of Article Views (full-text article views including HTML views, PDF and ePub downloads, according to the available data) and Abstracts Views on Vision4Press platform.

Data correspond to usage on the plateform after 2015. The current usage metrics is available 48-96 hours after online publication and is updated daily on week days.

Initial download of the metrics may take a while.