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Archigetes Leuckart, 1878 (Cestoda, Caryophyllidea): diversity of enigmatic fish tapeworms with monoxenic life cycles - PubMed

Archigetes Leuckart, 1878 (Cestoda, Caryophyllidea): diversity of enigmatic fish tapeworms with monoxenic life cycles

Dalibor Uhrovič et al. Parasite. 2022.

Abstract

The caryophyllidean genus Archigetes Leuckart, 1878 is unique among all tapeworms in that its species can mature in invertebrate hosts (Oligochaeta), i.e., have a monoxenic (direct) life cycle. All five species were described as progenetic plerocercoids in oligochaetes and two of them also as adults from cypriniform fishes. Two species, A. sieboldi Leuckart, 1878 and A. iowensis Calentine, 1962, were found in North America in non-native common carp (Cyprinus carpio). A molecular study of caryophyllideans from the southern United States has revealed the occurrence of three new species in native freshwater fishes (Catostomidae, Ictiobinae): Archigetes loculotruncatus n. sp. from Ictiobus bubalus, I. niger and Carpiodes cyprinus is the largest representative of the genus and differs by a loculotruncate scolex. Archigetes megacephalus n. sp. from Ictiobus niger, I. bubalus and I. cyprinellus is characterised by a prominent, bothrioloculodiscate scolex. Archigetes vadosus n. sp. from I. bubalus is typified by a globular scolex with very shallow loculi; it differs from the closely related A. sieboldi in the shape of the body, with a distinct neck region and a scolex wider than the remaining body. Archigetes iowensis Calentine, 1962 becomes a junior synonym of Paraglaridacris limnodrili (Yamaguti, 1934). The generic diagnosis of Archigetes is amended and a key to identification of North American taxa is provided. Species of Archigetes and Paraglaridacris differ from each other most conspicuously in the structure of the ovary, which is follicular in Archigetes versus compact in Paraglaridacris.

Title: Archigetes Leuckart, 1878 (Cestoda, Caryophyllidea) : diversité de cestodes de poissons énigmatiques à cycle de vie monoxène.

Abstract: Le genre Archigetes Leuckart, 1878 (Caryophyllidea) est unique parmi les cestodes en ce sens que ses espèces peuvent atteindre la maturité chez des hôtes invertébrés (Oligochaeta), c’est-à-dire avoir un cycle de vie monoxénique (direct). Les cinq espèces ont été décrites à partir de plérocercoïdes progénétiques chez des oligochètes et deux d’entre elles aussi à partir d’adultes chez des poissons cypriniformes. Deux espèces, A. sieboldi Leuckart, 1878 et A. iowensis Calentine, 1962, ont été trouvées en Amérique du Nord chez des carpes communes (Cyprinus carpio), non indigènes. Une étude moléculaire des caryophyllidés du sud des États-Unis a révélé la présence de trois nouvelles espèces chez les poissons d’eau douce indigènes (Catostomidae, Ictiobinae). Archigetes loculotruncatus n. sp. d’Ictiobus bubalus, I. niger et Carpiodes cyprinus est le plus grand représentant du genre et est caractérisé par un scolex loculotronqué. Archigetes megacephalus n. sp. d’Ictiobus niger, I. bubalus et I. cyprinellus est caractérisé par un scolex proéminent et bothrioloculodisqué. Archigetes vadosus n. sp. d’I. bubalus est caractérisé par un scolex globulaire avec des loges très peu profondes, et diffère d’A. sieboldi, étroitement apparenté, par la forme du corps, avec une région du cou distincte et un scolex plus large que le reste du corps. Archigetes iowensis Calentine, 1962 devient un synonyme plus récent de Paraglaridacris limnodrili (Yamaguti, 1934). Le diagnostic générique d’Archigetes est modifié et une clé d’identification des taxons nord-américains est fournie. Les espèces d’Archigetes et de Paraglaridacris diffèrent de la manière la plus visible les unes des autres par la structure de l’ovaire, qui est folliculaire chez Archigetes par opposition à compact chez Paraglaridacris.

Keywords: Catostomidae; Comparative morphology; Eucestoda; Fish; Histology; Ictiobinae; Molecular prospecting; Nearctic Region; SEM; Species diversity; lsrDNA.

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

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Figures

Figure 1
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].

Figure 2
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.

Figure 3
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.

Figure 4
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.

Figure 5
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.

Figure 6
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.

Figure 7
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.

Figure 8
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.

Figure 9
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.

Figure 10
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.

Figure 11
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.

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