Kapsulotaenia beveridgei, Chambrier & Brabec & Scholz, 2020

Chambrier, Alain De, Brabec, Jan & Scholz, Tomáš, 2020, Molecular data reveal unexpected species diversity of tapeworms of Australasian reptiles: revision of Kapsulotaenia (Cestoda: Proteocephalidae), Zootaxa 4869 (4), pp. 529-561 : 547-549

8. Kapsulotaenia beveridgei n. sp.

( Figs. 6 , 10E , 11 E–H)

Syn. Kapsulotaenia sp. 1 of de Chambrier et al. (2015)

Type and only known host. Rosenberg’s monitor, Varanus rosenbergi Mertens, 1957 ( Squamata : Varanidae ).

Site of infection. Intestine.

Type locality. Rocky River , Road to Snake Lagoon , 2 km before Bales Beach, Kangaroo Island, South Australia, Australia .

Additional localities. Cross Road Penneshaw—America River; Stansail, South Road; Playford Highway; all Kangaroo Island , South Australia .

Type material. Holotype from host No. Aus031 (MHNG-PLAT-85989—slide C- 183/57), 1 paratype (hologenophore) from V. rosenbergi (Aus031; MHNG-PLAT-32842—slide C- 183/51), 1 paratype from V. rosenbergi (Aus031, C 183/59, SAM 031.183/59); 1 paratype from V. rosenbergi (Aus031, C- 183/59, NHMUK 2020.4.25.7); 1 paratype from V. rosenbergi ((Aus032; MHNG-PLAT-85990—slides C- 183/61–66); paratype from V. rosenbergi (Aus029, slide C- 121/32; IPCAS C- 831/1).

DNA sequences. lsr DNA: MT 611164 , MT 611165 (Aus028, 029), AJ 583452 — de Chambrier et al. (2015; hologenophore MHNG-PLAT-32842); cox 1: MT 627455 , MT 627460 , MT 627461 (Aus028, 031, 029).

Material studied. All from Varanus rosenbergi, Kangaroo Island, South Australia, Australia, collected by A. de Chambrier on 14.–16.xi.2001: host Aus 028: 12 slides (3 whole-mounts with 1 scolex and 9 slides with cross sections), Cross Road Penneshaw—America River (MHNG-PLAT-36555); Aus 029: 6 slides with several mounted specimens (8 scoleces), Stansail , South Road including one paratype (1 slide IPCAS C-831 /1 and 1 slide NHMUK 2020.4 .25.7), 4 slides (MHNG-PLAT-36552); host Aus 031: 10 slides of whole-mounted specimens including 1 paratype and hologenophore (MHNG-PLAT-32842), holotype and vouchers (5 scoleces), Rocky River, Road to Snake Lagoon, 2 km before Bales Beach (MHNG-PLAT-85989); host Aus032: 1 slide with whole-mounted specimens including paratype and vouchers (2 scoleces) and 5 slides with cross sections (MHNG-PLAT-85990); host Aus033: 5 slides with whole-mounted specimens (2 scoleces; additional scolex used for SEM observations), 18 slides with cross sections and 5 slides with sections of the host’s intestine with attached cestode, Playford Highway (MHNG-PLAT-36305 and 1 slide C 118/53; IPCAS C-831 /1) .

Etymology. The new species is named after Ian Beveridge from the University of Melbourne, Australia, for his great contribution to the knowledge of tapeworms and other helminth parasites as well as for his generous support during the trips of the senior author to Australia in 2001 and 2003.

Morphological description (for measurements—see Table 2 ). Proteocephalidae , Acanthotaeniinae . Cestodes up to 105 mm in total length; maximum width up to 1,305. Strobila acraspedote, anapolytic. Immature proglottids wider than long to longer than wide (length: width ratio 0.43–1.60), mature, pregravid and gravid proglottids longer than wide (ratio 1.51–7.69) ( Fig. 6 B–D). Inner longitudinal musculature present, composed of very few muscle fibres. Ventral osmoregulatory canals slightly sinuous, 12–20 in diameter. Dorsal osmoregulatory canals slightly sinuous, 5–10 in diameter. Canals situated between vitelline follicles and testes ( Fig. 6B ).

Scolex wider than neck ( Figs. 6A , 11E ). Suckers uniloculate, spherical, directed laterally to anterolaterally. Rostellum dome-shaped, 155–185 long to 155–220 wide, containing large apical organ, 60–80 long to 55–80 wide, posteriorly surrounded by numerous circular muscular fibres ( Fig. 6A ). Retractor muscles connecting rostellum with neck present.

Testes medullary, in 1 layer, rounded to elongate, in 2 wide longitudinal bands in both sides of proglottids, with poral band separated by terminal genitalia into preporal and postporal groups ( Fig. 6C, D ); testes and ovary degenerate in gravid proglottids ( Fig. 6F ). Cirrus-sac pyriform, thin-walled, 100–140 long ( Fig. 6E ). Cirrus short, covered by spinitriches, its length representing up to 50% of cirrus-sac length ( Fig. 6E ). Internal sperm duct coiled. External sperm duct (vas deferens) strongly coiled, directed anteriorly, situated between proximal part of cirrus-sac and midline of proglottids, often crossing it ( Fig. 5C, D ). Genital atrium deep ( Fig. 6E ); genital pores alternating irregularly, situated in posterior part of proglottid ( Fig. 6C, D, F ).

Ovary bilobed, butterfly-shaped ( Fig. 6 B–D). Mehlis’ gland small, 40–55 wide. Vaginal canal straight in proximal part, enlarged to form small seminal receptacle anterior to or overlapping ovarian isthmus ( Fig. 6B ). Terminal (distal) part of vaginal canal (pars copulatrix vaginae) surrounded by few chromophilic cells ( Fig. 6E ), vaginal sphincter absent. Vagina anterior (11%) or posterior (89%, n = 314) to cirrus-sac ( Fig. 6 B–D). Vitelline follicles arranged in 2 longitudinal bands near lateral margins of proglottids (1–3 rows of follicles) interrupted at level of cirrus-sac and vagina ( Fig. 6 B–D).

Primordium of uterine stem ventral, present in immature proglottids ( Fig. 6C ). Development of uterus of type 1 according to de Chambrier et al. (2004, 2015). In pregravid proglottids, uterus occupies up to 66–69% of proglottid length, with 17–20 lateral diverticula on each side, not overlapping ovary. In gravid proglottids, uterus occupies up to 85% of proglottid length ( Fig. 6F ). Uteroduct enters uterus anterior to ovarian isthmus. Intrauterine eggs oval to subspherical, grouped in clusters of 7–10 (x = 8, n = 42) eggs ( Fig. 10E ). Outer envelope thin, embryophore trilayered, oncosphere spherical, six embryonic hooks, 6–8 long.

Differential diagnosis. Kapsulotaenia beveridgei n. sp. differs from all but two species of Kapsulotaenia by a lower number of the testes. It differs from K. frezei and K. saccifera by the presence of a lower number of eggs in spherical clusters versus banana-shaped clusters containing more than 90 eggs.

Remarks. Tapeworms from 5 individual Rosenberg’s monitors (5 of 6 hosts examined were infected, i.e., prevalence of 83%) in the Kangaroo Island, South Australia (Aus028, 029, 031–033) are indistinguishable in their morphology from each other and are considered conspecific. In addition, cox 1 sequences of specimens from 3 host individuals show very low nucleotide variability (maximum of 9 nt out of 1,608 bp cox 1) thus supporting their conspecificity ( Figs. 1 , 2 ). The new species seems to be a specific parasite of this monitor lizard and it is so far known only from South Australia. Varanus rosenbergi , the definitive host of K. beveridgei , is found in southern regions of the continent ( Pianka et al. 2004).

Figures

FIGURE 1. Phylogenetic relationships of tapeworms of the subfamily Acanthotaeniinae (Cestoda: Proteocephalidae) based on a maximum likelihood analysis of concatenated (lsrDNA +cox1) data. Nodal values depict standard bootstrap supports (1,000 resamples) over 50, dashed lines are used for nodes with bootstrap values below 50. Branch length scale bar indicates number of substitutions per site. GenBank accession numbers can be found in Table 1.

FIGURE 2. Maximum likelihood single-gene phylogenies of Kapsulotaenia based on cox1 (above) and lsrDNA (below) data. Nodal values depict standard bootstrap supports (1,000 resamples) over 50, dashed lines are used for nodes with bootstrap values below 50. Branch length scale bar indicates number of substitutions per site. GenBank accession numbers can be found in Table 1.

FIGURE 5. Kapsulotaenia varia (Beddard, 1913) from Varanus varius, Australia (new material Aus137—A, C; Aus016—D; syntype NHMUK 1915.5.14.2—B). A—scolex; B—immature proglottid, ventrally; C, D—pregravid proglottids, ventrally.

FIGURE 6. Kapsulotaenia beveridgei n. sp. from Varanus rosenbergi, Australia. A—scolex (Aus031b/85989); B—posterior part of mature proglottid, dorsally (Aus033; MHNG-PLAT-36305); C—pregravid proglottid, dorsally (Aus031; MHNG-PLAT- 85989); D—mature proglottid, ventrally (Aus031b; MHNG-PLAT-85989); E—terminal genitalia, dorsally (Aus028; MHNG- PLAT-36555); F—gravid proglottid, ventrally (Aus031; MHNG-PLAT-85989).

FIGURE 10. Egg capsules of species of Kapsulotaenia (eggs from unmounted proglottids drawn in distilled water). A—K. pythonis from Morelia viridis (syntype); B—Kapsulotaenia sp. 6 from Varanus varius (host AUS005); C—K. tidswelli from Varanus varius (host Aus135); D, F—K. varia from V. varius (hosts Aus016 and Aus137); E—K. beveridgei n. sp. from V. rosenbergi (host Aus028); G, H—K. cannoni n. sp. from V. gouldii (host Aus140).

FIGURE 11. Scanning electron micrographs of Kapsulotaenia spp. A–D. Kapsulotaenia varia from Varanus varius (Aus137; MHNG-PLAT-72084). A. Subapical view of the scolex. B. Coniform spinitriches and capilliform filitriches on the rostellum (apex of the scolex). C. Capilliform filitriches with sparse gladiate spinitriches on the outer rim of suckers. D. Gladiate spinitriches on the strobila. E–H. K. beveridgei n. sp. from V. rosenbergi (Aus029—MHNG-PLAT-36552). E. Frontal view of the scolex. F. Coniform spinitriches interspersed with capilliform filitriches on the rostellum (apex of the scolex). G. Gladiate spinitriches in-between the suckers. H. Gladiate spinitriches on the strobila. I–P. K. cannoni n. sp. from V. gouldii (Aus140; MHNG- PLAT-36703). I. Frontal view of the scolex. J.Apical view of the scolex. K. Subapical view of the partly withdrawn rostellum. L. Detail of the sucker rim with capilliform filitriches and coniform spinitriches. M. Coniform spinitriches of the rostellum (apex of the scolex). N. Capilliform filitriches of the outer rim of the suckers, with coniform spinitriches in the lower part (sucker cavity). O. Coniform spinitriches interspersed with papilliform filitriches in the sucker cavity. P. Gladiate spinitriches on the neck. Small letters within figures mark position of detailed pictures of microtriches.