Abstract
Species diversity and interrelationships of tapeworms of the genus Kapsulotaenia Freze, 1963 (Proteocephalidae: Acanthotaeniinae), parasites of lizards, especially monitors (Varanus spp.) in the Australasian region, were re-assessed using an interdisciplinary approach. Molecular phylogenetic analyses of newly characterized lsrDNA and cox1 sequences confirmed monophyly of the genus, which is typified by the presence of eggs in capsules, and also indicated a strict (oioxenous) level of host specificity of its species thus revealing unexpected species diversity. Diagnoses of insufficiently described species were amended based on a study of the types and freshly collected specimens and, in addition, three new species were described. A list of ten species of the genus recognized as valid is provided, including illustrations of taxonomically important structures of poorly known taxa. Kapsulotaenia beveridgei n. sp. from V. rosenbergi in Australia differs from all other species of Kapsulotaenia but K. frezei and K. saccifera by having a lower number of testes and an absence of banana-shaped clusters of eggs. Kapsulotaenia cannoni n. sp. from V. gouldii can be distinguished from all species but K. chisholmae by a smaller scolex diameter and from all remaining species by its bigger cirrus-sac ratio and a bigger Mehlis’ gland/proglottid width ratio. Kapsulotaenia cannoni n. sp. differs from K. chisholmae, by the presence of an armed cirrus and a lower number of eggs in cluster (3–7 versus 8–13). Kapsulotaenia nybelini n. sp., which also occurs in V. gouldii, differs from K. tidswelli, K. frezei and K. beveridgei by having a greater number of testes, and it differs from K. varia by having a smaller relative size of the ovary. It differs from K. saccifera by the absence of banana-shaped cluster, and from K. pythonis by the number of eggs in clusters. Identification keys for all species of Kapsulotaenia and genera of the Acanthotaeniinae are also provided, together with SEM micrographs of three species, including two newly described species.
References
Baylis, H.A. (1929) On a larval forms of Acanthotaenia. Annals and Magazine of Natural History, Series 10, 4 (20), 224–229.
https://doi.org/10.1080/00222932908673042
Beddard, F.E. (1913) Contributions to the anatomy and systematic arrangement of the Cestoidea. VII. On six species of tapeworms from reptiles, belonging to the genus Ichthyotaenia (s.l.). Proceedings of the Zoological Society of London, Part 1, 4–36.
https://doi.org/10.1111/j.1096-3642.1913.tb01980.x
Carter, W.J. (1943) Proteocephalus sandgroundi, a new tetraphyllidean cestode from an East Indian monitor lizard. Transactions of the American Microscopical Society, 62, 301–305.
https://doi.org/10.2307/3223035
de Chambrier, A. (1989a) Révision du genre Crepidobothrium Monticelli, 1900 (Cestoda: Proteocephalidae) parasite d’Ophidiens néotropicaux. I. C. gerrardii (Baird, 1860) et C. viperis (Beddard, 1913). Revue Suisse de Zoologie, 96, 191–217.
https://doi.org/10.5962/bhl.part.117763
de Chambrier, A. (1989b) Révision du genre Crepidobothrium Monticelli, 1900 (Cestoda: Proteocephalidae) parasite d’Ophidiens néotropicaux. II. C. dollfusi Freze, 1965, C. lachesidis (MacCallum, 1921) et conclusions. Revue Suisse de Zoologie, 96, 345–380.
https://doi.org/10.5962/bhl.part.117769
de Chambrier, A. (2001) A new tapeworm from the Amazon, Amazotaenia yvettae n. gen., n. sp. (Eucestoda: Proteocephalidea) from the siluriform fishes Brachyplatystoma filamentosum and B. vaillanti (Pimelodidae). Revue Suisse de Zoologie, 108, 303–316.
https://doi.org/10.5962/bhl.part.79632
de Chambrier, A. (2006) Redescription of Kapsulotaenia sandgroundi (Carter, 1943) (Eucestoda: Proteocephalidae: Acanthotaeniinae), a parasite of Varanus komodoensis (Varanoidea: Varanidae) from Indonesia. Systematic Parasitology, 63, 83–93.
https://doi.org/10.1007/s11230-005-9001-y
de Chambrier, A., Beveridge, I. & Scholz, T. (2018) Tapeworms (Cestoda: Proteocephalidae) of Australian reptiles: hidden diversity of strictly host-specific parasites. Zootaxa, 4461, 477–498.
https://doi.org/10.11646/zootaxa.4461.4.2
de Chambrier, A., Binh, T.T. & Scholz, T. (2012) Ophiotaenia bungari n. sp. (Cestoda), a parasite of Bungarus fasciatus (Schneider) (Ophidia: Elapidae) from Vietnam, with comments on relative ovarian size as a new and potentially useful diagnostic character for proteocephalidean tapeworms. Systematic Parasitology, 81, 39–50.
https://doi.org/10.1007/s11230-011-9320-0
de Chambrier, A., Brabec, J., Tran, B.T. & Scholz, T. (2019) A morphological and molecular study of Acanthotaenia von Linstow, 1903 (Cestoda: Proteocephalidae), parasites of monitors (Varanus spp.): redescription of the type species, description of a new species from Vietnam and phylogenetic interrelationships. Parasitology Research, 118, 1761–1783.
https://doi.org/10.1007/s00436-019-06326-6
de Chambrier, A. & Scholz, T. (2012) A new species of Australotaenia (Cestoda: Proteocephalidea), from a snake in Cambodia: host switching or postcyclic parasitism in a distant region? Folia Parasitologica, 59, 279–286.
https://doi.org/10.1007/s11230-011-9320-0
de Chambrier, A., Scholz, T., Mariaux, J. & Kuchta, R. (2017) Onchoproteocephalidea I Caira, Jensen, Waeschenbach, Olson & Littlewood, 2014. In: Caira, J.N. & Jensen, K. (Eds.), Planetary Biodiversity Inventory (2008–2016): Tapeworms from vertebrate bowels of the Earth. Special Publication No. 25. University of Kansas, Natural History Museum, Lawrence, Kansas, pp. 251–277.
de Chambrier, A., Waeschenbach, A., Fisseha, M., Scholz, T. & Mariaux, J. (2015) A large 28S rDNA-based phylogeny confirms the limitations of established morphological characters for classification of proteocephalidean tapeworms (Platyhelminthes, Cestoda). ZooKeys, 500, 25–59.
https://doi.org/10.3897/zookeys.500.9360
de Chambrier, A., Zehnder, M.P., Vaucher, C. & Mariaux, J. (2004) The evolution of the Proteocephalidea (Platyhelminthes, Eucestoda) based on an enlarged molecular phylogeny, with comments on their uterine development. Systematic Parasitology, 57, 159–171.
https://doi.org/10.1023/B:SYPA.0000019083.26876.34
de Chambrier, S. & de Chambrier, A. (2010) Two new genera and two new species of proteocephalidean tapeworms (Eucestoda) from reptiles and amphibians in Australia. Folia Parasitologica, 57, 263–279.
https://doi.org/10.14411/fp.2010.033
Chernomor, O., von Haeseler, A. & Minh, B.Q. (2016) Terrace aware data structure for phylogenomic inference from supermatrices. Systematic Biology, 65, 997–1008.
https://doi.org/10.1093/sysbio/syw037
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.
https://doi.org/10.14411/fp.2009.025
Freze, V.I. (1963) On convergent formation of the rostellum in two lineages of proteocephalans and a revision of the subfamilies Gangesiinae Mola, 1929 and Acanthotaeniinae Frese, 1963 (Cestoda, Proteocephalata). In: Gelminty cheloveka, zhivotnykh i selskokhozyaistvennykh rastenii (k 85-letiyu Akademika K.I. Skryabina). Izdatel’stvo Akademii Nauk, Moscow, pp. 150–155. [in Russian]
Freze, V.I. (1965) [Proteocephalata in Fish, Amphibians and Reptiles]. Essentials of Cestodology. Vol. V. Nauka, Moscow, 538 pp. [in Russian, English translation, Israel Program of Scientific Translation, 1969, Cat. No. 1853, v + 597 pp.]
Gomez-Puerta, L.A. (2011) Primer registro de Crepidobothrium gerrardii (Cestoda: Proteocephalidae) en el Perù. Revista Peruana de Biologia, 18, 387–888.
https://doi.org/10.15381/rpb.v18i3.459
Hallinger, M.J., Taubert, A. & Hermosilla, C. (2020) Occurrence of Kalicephalus, Strongyloides, and Rhabdias nematodes as most common gastrointestinal parasites in captive snakes of German households and zoological gardens. Parasitology Research, 119, 947–956.
https://doi.org/10.1007/s00436-019-06526-0
Jones, H.I. & de Chambrier, A. (2016) Kapsulotaenia chisholmae n. sp. (Cestoda: Proteocephalidae), from Varanus spenceri (Reptilia: Varanidae) in Australia. Revue Suisse de Zoologie, 123, 209–217.
https://doi.org/10.5281/zenodo.155139
Johnston, T.H. (1909) On a new reptilian cestode. Journal and Proceedings of the Royal Society of New South Wales, 43, 103–116 & 1 Plate.
Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587–589.
https://doi.org/10.1038/nmeth.4285
Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780.
https://doi.org/10.1093/molbev/mst010
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Mentjies, P. & Drummond, A. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649.
https://doi.org/10.1093/bioinformatics/bts199
Nguyen, L.T., Schmidt H.A., von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution, 32, 268–274.
https://doi.org/10.1093/molbev/msu300
Nybelin, O. (1917) Australischen Cestoden. Results of D.E. Mjoberg’s Swedish scientific expeditions to Australia 1910–1913. Kungliga Svenska Vetenskapsakademiens Handlingar, 52 (14), 1–48.
Pianka, E.R., King, D.R. & King, R.A. (2004) Varanoid Lizards of the World. Indiana University Press, Bloomington, Indiana, 587 pp.
https://doi.org/10.2307/j.ctt2005wjp
von Rátz, S. (1900) Drei neue Cestoden aus Neu-Guinea. Zentralblatt für Bakteriologie und Parasitenkunde, Infektionskranheiten und Hygiene, 28, 657–660.
Rego, A.A. (1967) Sobres alguns cestodeos parasitos de repteis. Revista Brasileira de Biologia, 27, 181–187.
Rego, A.A. (1994) Order Proteocephalidea Mola, 1928. In: Khalil, L.F., Jones, A. & Bray, R.A. (Eds.), Keys to the Cestode Parasites of Vertebrates. CAB International, Wallingford, pp. 257–293.
Schmidt, G.D. (1986) CRC Handbook of Tapeworm Identification. CRC Press, Boca Raton, Florida, 675 pp.
Schmidt, G.D. & Kuntz, R.E. (1974) Tapeworms from Philippine reptiles, with two new species of Proteocephalata. Proceedings of the Helminthological Society Washington, 41, 195–199.
Scholz, T. & de Chambrier, A. (2019) Amendment of Rostellotaenia Freze, 1963 (Cestoda: Proteocephalidae) from African monitors (Varanus spp.) and a redescription of its type species, R. nilotica (Beddard, 1913). Systematic Parasitology, 96, 659–672.
https://doi.org/10.1007/s11230-019-09876-6
Thompson, G. (2004) 7.10. Varanus gouldii. In: Pianka, E.R., King, D.R. & King, R.A. (Eds.), Varanoid Lizards of the World. Indiana University Press, Bloomington, Indiana, pp. 380–405.
Thompson, R.C.A., Hayton, A.R. & Jue Sue, L.P. (1980) An ultrastructural study of the microtriches of adult Proteocephalus tidswelli (Cestoda: Proteocephalidea). Zeitschrift für Parasitenkunde, 64, 95–111.
https://doi.org/10.1007/BF00927060
Tran, B.T., Nguyen, S.T., Nguyen, T.T., Luc, P.V., Mafie, E., Rupa, F.H. & Sato, H. (2016) Endoparasites of Vietnamese lizards recorded in the last 50 years (1966–2015). Japanese Journal of Veterinary Parasitology, 15, 34–58.
Uetz, P., Freed, P. & Hošek, J. (Eds.) (2019) The Reptile Database. Online publication. Available from: http://www.reptile-database.org (accessed 30 December 2019)
Waeschenbach, A., Webster, B.L., Bray, R.A. & Littlewood, D.T.J. (2007) Added resolution among ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with complete small and large subunit nuclear ribosomal RNA genes. Molecular Phylogenetics and Evolution, 45, 311–325.
https://doi.org/10.1016/j.ympev.2007.03.019
Wahid, S. (1968) A new species of the genus Acanthotaenia, with a note on Anonchotaenia trochili from a new host. Pakistan Journal of Sciences and Industrial Research, 11, 81–84.
Weawers, B. (2004) 7.24. Varanus varius. In: Pianka, E.R., King, D.R. & King, R.A. (Eds.), Varanoid Lizards of the World. Indiana University Press, Bloomington, Indiana, pp. 488–502.
Welton, L.J., Travers, S.L., Siler, C.D. & Brown, R.M. (2014) Integrative taxonomy and phylogeny-based species delimitation of Philippine water monitor lizards (Varanus salvator complex) with descriptions of two new cryptic species. Zootaxa, 3881 (3), 201–227.
https://doi.org/10.11646/zootaxa.3881.3.1
Wolf, D., Vrhovec, M.G., Failing, K., Rossier, C., Hermosilla, C. & Pantchev, N. (2014) Diagnosis of gastrointestinal parasites in reptiles: comparison of the coprological methods. Acta Veterinaria Scandinavica, 56, 44.
https://doi.org/10.1186/s13028-014-0044-4