INTRODUCTION

Varanus spenceri Lucas & Frost, 1903 is a large lizard which grows up 1.2 metres (Cogger, 2014), and is probably the least known of the large Australian varanid lizards (Lemm & Bedford, 2004). It is confined to the black soil country, which is the most fertile soil in Australia, of west Queensland and the Barkly Tablelands of the Northern Territory, Australia, where perennial Mitchell Grass (Astrebla spp.) is the dominant vegetation. Apart from report of the nematode Abbreviata hastaspicula from a road-killed V. spenceri (Wooley, 2010), there have been no reports on the cestodes parasites of this large species. The first author undertook this study to determine whether the helminth fauna differed significantly from that in related species (V. gouldii, V. panoptes), and to investigate whether its restricted and specialized habitat, and hence its diet, exercised a discernible influence on this fauna. A paper concerning the nematode fauna present in V. spenceri has been published recently (Jones, 2013). The cestodes recovered from four V. spenceri are considered to belong to a previously undescribed species, and this is described below.

MATERIALS AND METHODS

The worms came from two different sources. The first worms came from dissected gastro-intestinal tracts of 14 preserved V. spenceri held in the Queensland Museum. Cestodes were prepared using standard methods; they were washed in water to remove alcohol, stained with basic fuchsin or haematoxylin, washed, fixed in 70% ethanol, destained in acid alcohol, dehydrated through an alcohol series, cleared in xylol, and mounted in DPX (distyrene, tricresyl phosphate and xylene). Alternatively, some were stained following the method described in de Chambrier (2001). The second source consists in one specimen without scolex, which was collected in November 2000 in Nelia (Queensland) by I. Beveridge.

Mature proglottides were embedded in paraffin wax, sectioned at 12-15 µm, and stained with haematoxylin and eosin. Several proglottides and the scoleces were cleared in lactophenol. Helminths were examined under a BA series Olympus microscope or with a Leica DMLB, and illustrations made with a drawing tube. Scolices for scanning electron microscopy (SEM) were processed as follows: worms were dehydrated in a graded ethanol series (80, 96, twice 100%), then transferred to a graded amyl acetate series, critical point dried in CO₂, sputter-coated with gold and examined with a Zeiss 940A electron microscope. Type of uterine formation defined according to de Chambrier et al. (2004). Relative ovarian size (ratio of ovarian size in relation to that of entire proglottis) calculated according to de Chambrier et al. (2012).

Museum acronyms used in this text are as follows:

RESULTS

Figs 1–3.

Kapsulotaenia chisholmae n. sp. (1) Total lateral view of a scolex (holotype – QM G235015). (2) Dorsal view of a mature proglottis (paratype MHNG-PLAT-31201). (3) Dorsal view of a pregravid proglottis (paratype MHNG-PLAT-31201). Abbreviations: ao – apical organ; cc – chromophilic cells; ci – cirrus; cm – circular musculature; cs – cirrus-sac; do – dorsal osmoregulatory canal; du – uterine diverticula; mg – Mehlis' glands; ov – ovary; te – testes; us – uterine stem; va – vas deferens; vc – vaginal canal; vi – vitelline follicles; vo – ventral osmoregulatory canal.

Figs 4–7.

Kapsulotaenia chisholmae n. sp. (4) Transversal section of a proglottis at level of its anterior part (paratype MHNG-PLAT-31201). (5) Transversal section of a proglottis at level of cirrus-sac (paratype MHNG-PLAT-31201). (6) Transversal section of a proglottis at level of the ovary (paratype QM G235018). (7) Egg cluster. Abbreviations: ci – cirrus; cs – cirrus-sac; do – dorsal osmoregulatory canal; em – tri-layered embryophore; lm – internal longitudinal musculature; oe – outer envelope; on – oncosphere; ov – ovary; st – subtegumental muscle fibres; su – subtegumental cells; te – testes; tg – tegument; ud – uteroduct; ut – uterus; va – vas deferens; vc – vaginal canal; vd – vitelloduct; vi – vitelline follicles; vo – ventral osmoregulatory canal.

Figs 8–10.

Kapsulotaenia chisholmae n. sp. Figs. 8-10, QM G235019. Scanning electron micrographs. (8) Dorsoventral view. (9) Lateral view. (10) Apical view.

Fig 11.

Kapsulotaenia chisholmae n. sp. Schematic view of the scoleces, showing the different shape of contraction, with rostellum extended, partially and fully retracted.

REMARKS

Due to the fact that the majority of cestodes were recovered from preserved lizards, most specimens of K. chisholmae were not in optimal condition: longitudinal excretory canals were sometimes difficult to distinguish, the uterine lateral diverticula in gravid proglottides were unclear, and the irregular shape and size of the testes may have been an artifact of poor preservation. The specimen collected from a living host in Nelia is better preserved, but does not have the scolex. Nonetheless, several constant features could be identified which readily differentiate this species from the other species of Kapsulotaenia (Table 1).

de Chambrier (2006) recognized five species which have been formally described, viz. Kapsulotaenia tidswelli (Johnston, 1909) from Varanus varius in eastern Australia (Johnston, 1909), K. sandgroundi (Carter, 1943) from the Komodo dragon, V. komodoensis (Carter, 1943), K. frezei Schmidt & Kuntz, 1974 from V. salvator (= V. palawanensis Koch, Gaulke & Böhme, 2010) in Palawan, Philippines (see Koch et al., 2010; Schmidt & Kuntz, 1974), K. saccifera (Ratz, 1900), from Varanus sp. in New Guinea (Ratz, 1900a, b), and K. varia (Beddard, 1913) from V. varius in Australia (Beddard, 1913). Yamaguti (1959) however considered K. varia to be a synonym of K. sandgroundi, an opinion that the present authors do not share. Johnston (1909) commented that the scolex in K. saccifera is very similar to that in K. tidswelli.

The cestodes recovered from five out of fourteen V. spenceri in the present study resemble K. sandgroundi, as described by Carter (1943) and redescribed by de Chambrier (2006). However, Kapsulotaenia chisholmae n. sp. differs from this species and from K. varia and K. tidswelli by the anterior position of the vagina to cirrus-sac. It also differs from K. varia, K. frezei and K. saccifera by a different egg number in each cluster (8-13 in K. chisholmae versus 12-20, 90-100 and more than 100, respectively), from K. frezei and K. saccifera by a different cluster shape (spherical to oval versus banana-shaped in the two latter), from K. sandgroundi and K. tidswelli by a greater diameter of the embryophore (37-45 µm versus respectively 25-30 µm and 19-32 µm); from K. sandgroundi and K. varia (sensu Nybelin, 1917 – see below), by the absence of a vaginal sphincter. Finally, K. chisholmae differs from K. varia, K. tidswelli, K. frezei and K. saccifera by a larger length of the strobila (up to 315 mm versus 30 mm, 27-30 mm, 40 mm, and 10-40 mm, respectively) (Table 1).

DISCUSSION

Within the cestode order Proteocephalidea, Freze (1963) erected the subfamily Acanthotaeniinae, with three genera Acanthotaenia Linstow, 1903, Rostellotaenia Freze, 1963 and Kapsulotaenia Freze, 1963, all of which occur in monitors (Varanus spp.) (Freze, 1965). de Chambrier & de Chambrier (2010) described another acanthotaenine genus, Vandiermenia, a parasite of the red-bellied snake Pseudechis porphyriacus from Australia. Kapsulotaenia is characterized principally by the presence of eggs in clusters in the gravid proglottides. Based on molecular data, de Chambrier et al. (2004) separated four species in this genus in Australia, with one species in V. varius (White, 1790), two in V. gouldii (Gray, 1838) and one in V. rosenbergi Mertens, 1957. There is also one species in V. indicus (Daudin, 1802) (A. de Chambrier, unpublished). Species of Kapsulotaenia are believed to exhibit oioxenous specificity for their host (sensu Euzet & Combes, 1980). The main problem in the study of the Kapsulotaenia species is that most descriptions are incomplete. Ratz (1900a, b) gave an identical, very poor description of Ichthyotaenia saccifera (= K. saccifera) in two different publications, one in French and the other in German. Schwarz (1908) redescribed this taxon, but both descriptions are incomplete (missing a description of the scolex, number of testes, cirrus-sac ratio, testis field, uterine branches number, etc.) and no illustration was presented. Furthermore, the host was not identified to species. But Schwarz (1908) described for K. saccifera egg clusters elongated, bag-shaped (banana-shaped), each proglottis containing 2 to 11 clusters, which allows us to differentiate this taxa from our new species. Pending a revision of the genus, we consider K. saccifera as a species inquirenda.

Beddard (1913) described Acanthotaenia varia (= Kapsulotaenia varia) from Varanus varius in a “Zoological Garden”. Nybelin (1917) collected some cestode specimens from Varanus gouldii that he identified as Acanthotaenia varia Beddard, 1913. However, the description of these worms differs from the ones incompletely described by Beddard (1913) in the position of the vagina relative to the cirrus-sac (posterior in Beddard's description and anterior/ posterior in Nybelin's) and in the absence of a vaginal sphincter in the former specimens but present in the latter (Table 1). Therefore, the specimens identified as Kapsulotaenia varia (Beddard, 1913) described by Nybelin (1917) are considered as Kapsulotaenia sp. Furthermore, de Chambrier et al. (2004, 2015) observed a strict (oioxenous) specificity for the members of the monophyletic Kapsulotaenia and described differences between Kapsulotaenia sp. 2 from Varanus gouldii and Kapsulotaenia sp. 4 from V. varius. Johnston (1909) described K. tidswelli (as Acanthotaenia tidswelli) from Varanus varius, but the same author (Johnston, 1912) listed this species also as parasite of Varanus gouldii. However, this host record should be confirmed (voucher specimens are not available). It is obvious that the genus Kapsulotaenia is pending taxonomic revision.

The ecology and distribution of Varanus komodoensis (host of K. sandgroundi) and V. spenceri (host of K. chisholmae) differ. V. komodoensis only occurs in the Lesser Sunda islands, Indonesia, principally Komodo and Flores, where it inhabits deciduous monsoon rain forest, savannah and mangrove (Ciofi, 2004). As well as feeding on invertebrates and smaller vertebrates, adult V. komodoensis can kill and consume large vertebrates such as deer, wild boar and goats; decomposing carcasses form a significant part of its diet (Auffenberg, 1981). In contrast, V. spenceri is a burrowing species confined to relatively treeless grasslands with Astrebla spp. in central Queensland and the adjacent Northern Territory, and feeds on other smaller reptiles, small mammals such as Rattus villosisimus, and invertebrates such as orthopterans including plague locust species (Pengilley, 1981; Valentic & Turner, 1997; Wooley, 2010). It is interesting to note that no cestodes were recovered from 12 V. gouldii and 10 V. panoptes in Queensland (H.I. Jones, unpublished).

Table 1.

Summary of diagnostic traits in Kapsulotaenia species.

Measurements in micrometres (µm) unless otherwise stated. PC = proportion of the length of cirrus-sac to the width of the proglottis; PP = position of the genital pore (cirrus pore) as % of the proglottis length; OV = percentage of the width of the ovary in relation to the width of the proglottis; SL = supplementary layer within the embryophore (see de Chambrier, 2006, p. 91);* see de Chambrier et al. (2012); D = taken from the original drawings; B = measurements taken from cotypes of Beddard (BMNH 1915.5.14.2); R = measurements taken from type specimens of Ratz (MHNG-PLAT-36037).