Kapsulotaenia varia ( Beddard, 1913 ) Freze, 1963

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 : 545-547

7. Kapsulotaenia varia ( Beddard, 1913) Freze, 1963

( Figs. 5 , 10D, F , 11 A–D)

Syns. Ichthyotaenia varia Beddard, 1913 ; Acanthotaenia varia ( Beddard, 1913) Nybelin, 1913 ; Proteocephalus varius ( Beddard, 1913) Baer, 1927 ; Crepidobothrium varia ( Beddard, 1913) Meggitt, 1927 ; Kapsulotaenia sp. 3 and sp. 4 of de Chambrier et al. (2004, 2015)

Type and only known host. Lace monitor, Varanus varius (White, 1790) ( Squamata : Varanidae ).

Site of infection. Intestine.

Type locality. Zoological Gardens (not specified either on slide with types or in the original description).

Additional localities. Rome and Highway Moonie—St. Georges, Queensland, Australia.

Type material. Syntypes—2 slides with fragments of immature & mature proglottids of 1 specimen (without scolex) and gravid proglottids from Varanus varius (White, 1790) , Zoological Garden ( NHMUK 1915.5.14.2) .

DNA sequences. lsr DNA: MT 611159 , MT 611160 , MT 611161 (Aus137c, 137a, 137b), AJ 583451 (Aus019)— Kapsulotaenia sp. 3 of de Chambrier et al. (2004; hologenophore MHNG-PLAT-32840); AJ 583454 (Aus016)— Kapsulotaenia sp. 4 of de Chambrier et al. (2015; hologenophore MHNG-PLAT-32838); cox 1: MT 627448 , MT 627453 , MT 627459 , MT 627463 , MT 627468 (Aus137b, 019, 137c, 016, 137a).

Material studied. Syntype (gravid proglottids); 4 slides with 2 specimens including 2 scoleces and additional scolex for SEM from V. varius (Aus016), Rome, Injune road, Taroom turnoff, Queensland, Australia, collected by A. de Chambrier on 30.iii.2001 (MHNG-PLAT-32838, 85982) (material collected from a frozen host); 29 slides with numerous fragments of several specimens (5 scoleces), 25 slides of longitudinal sections of scolex and cross sections of strobila, and 1 scolex for SEM from V. varius (Aus137), Highway Moonie—St. Georges, km 77, Queensland, Australia, collected by A. de Chambrier on 2.xi.2003 (MHNG-PLAT-36700–36702, 72084, 85999, 86001, 86003, 86006, 86020, 97997–97999). Two slides with fragments of 1 specimen (1 scolex) designated as Kapsulotaenia sp. 3 in de Chambrier et al. (2004) from Varanus sp. (Aus019; host was incorrectly reported as V. gouldii in de Chambrier et al. 2004 ), Culgoa Floodplain National Park, Queensland, collected on 16.ii.1998 (MHNG-PLAT-32840).

Morphological description (see Table 2 for measurements). Strobila moderately long (total length of 65–103 mm). Proglottids usually longer than wide. Scolex small, wider than neck, with a globular rostellum containing apical organ. Retractor muscles connecting rostellum with neck region present. Testes ovoid to oblong, in one or two layers and in two fields converging anteriorly, interrupted porally by cirrus-sac and vagina. Vas deferens convoluted, in anterior median field. Cirrus-sac pyriform; cirrus armed with small spines (spinitriches). Vagina opens more often posteriorly than anteriorly to cirrus-sac. Vaginal sphincter present. Genital pore irregularly alternating, post-equatorial. Vitelline follicles in two lateral bands, not reaching anterior nor posterior margin of proglottids, interrupted at level of cirrus-sac on ventral side. Uterine stem without lateral diverticula, not reaching anterior and posterior margins of proglottids. Uterine stem not reaching anterior, nor posterior margin, without lateral diverticula. Eggs in capsules.

Remarks. This species was described as Ichthyotaenia (Acanthotaenia) varia by Beddard (1913) based on a great number of proglottids, but no complete specimen was found in V. varius . Beddard (1913) found a scolex, but was uncertain whether it belonged to the proglottids of K. varia . The original description was extensive, but contained very limited information about taxonomically important characteristics, the geographic origin of the type host was not indicated and few measurements were provided. No figures of the scolex, mature proglottid or terminal genitalia were provided by Beddard (1913). Moreover, the illustration of a (pre)gravid proglottid lacks any indication of the extent of the uterus and eggs in capsules are only partly developed.

Kapsulotaenia varia was originally differentiated from only two species now placed in two different genera, namely Acanthotaenia gracilis ( Beddard, 1913) and Rostellotaenia nilotica ( Beddard, 1913) , by the presence of eggs in capsules (“perhaps 12–20 in each batch of eggs” versus eggs not forming capsules in the two latter species). Freze (1965) listed three species of monitor lizards as definitive hosts of K. varia , V. varius , V. gouldii and the nonexisting V. bellii , but without any reference to original records from these monitors.

A study of several proglottids of the syntype of K. varia has revealed their close resemblance to specimens found in two V. varius from Queensland (Aus016 and Aus137; 2 of 9 hosts infected, i.e., prevalence of 22%). These tapeworms are considered conspecific and the species diagnosis of K. varia is amended by adding new measurements of the new material ( Table 2 ) and its illustrations ( Fig. 5A, C, D ). Compared to K. tidswelli (see above), K. varia possesses shorter and wide proglottids and a higher number of testes ( Table 2 ).

Kapsulotaenia varia differs from K. frezei and K. saccifera by the absence of banana-shaped egg clusters; from K. pythonis by the number of eggs in cluster (19–22 versus 5–12); from K. sandgroundi by a lower ovary relative width ratio (55–71% versus 42–59%). From K. beveridgei , K. cannoni and K. nybelini , it differs by the ovary surface ratio (5.2% versus 3.0–3.7%, 3.8–4.5% and 2.4–4.2%, respectively). From K. chisholmae , K. varia can be distinguished by a shorter body length (65–103 mm versus 180–315 mm), and by a different position of the vagina in relation to the cirrus-sac (34–66% versus 93% anterior).

Eggs of K. varia from the host No. Aus137 possess narrow, long (finger-like) projections on their surface ( Fig. 10F ), similarly as observed in Australophiotaenia gallardi (Johnston, 1911) from red-bellied black snake, Pseudechis porphyriacus (Shaw) (Serpentes, Elapidae ), in Australia ( de Chambrier & de Chambrier 2010). Interestingly, these projections were not observed in the eggs of apparently conspecific tapeworms from the host No. Aus016 ( Fig. 10D ).

Molecular data hint at a possible existence of a third species of Kapsulotaenia in the lace monitor ( Kapsulotaenia sp. 5) through the relative cox 1 sequence divergence of the specimen from host No. Aus006 ( MT627462 ) from both K. tidswelli and K. varia representatives (see Figs. 1 , 2 ). Unfortunately, no morphological vouchers of this specimen collected in Queensland in December 2000 were available to the authors. A denser sampling of molecular data will be needed to further develop the possibility.

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 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.