Oochoristica piankai sp. n. (Cestoda: Linstowiidae) and Other Helminths of Moloch horridus (Sauria: Agamidae) from Australia

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1 J. Helminthol. Soc. Wash. 63(), 1996, pp. 151 Oochoristica piankai sp. n. (Cestoda: Linstowiidae) and Other Helminths of Moloch horridus (Sauria: Agamidae) from Australia CHARLES R. BURSEY,' STEPHEN R. GOLDBERG, AND DAVID N. WooLERY 'Department of Biology, Pennsylvania State University, Shenango Campus, Sharon, Pennsylvania ( and Department of Biology, Whittier College, Whittier, California 608 ( ABSTRACT: Oochoristica piankai sp. n., a new linstowiid cestode, discovered in the small intestine of the thorny devil, Moloch horridus, is described and illustrated. Sixteen specimens of Oochoristica piankai sp. n. were found in 8 of 104 (8%) Moloch horridus from Australia. Oochoristica piankai sp. n. differs from 3 other Australian species of Oochoristica from lizards in the number of testes and the shape of the ovary. The presence of the nematode Parapharyngodon kartana and an encysted larva of Abbreviata sp. are also reported. Moloch horridus represents a new host record for P. kartana. KEY WORDS: Oochoristica piankai sp. n., cestode, Parapharyngodon kartana, Abbreviata sp., nematode, Moloch horridus, lizard, Agamidae, Australia. Only 3 of 74 species of Oochoristica Luhe, 1898, a cosmopolitan genus of cestodes, have been reported previously from reptiles of Australia. Taenia trachysauri MacCallum, 191, was described from specimens discovered in the intestine of the Australian lizard Trachydosaurus rugosus Gray, in the New York Zoological Garden. Baer (197) moved Taenia trachysauri to the genus Oochoristica. Johnston (193) reported O. trachysauri in Trachdoysaurus rugosus. Spasskii (1951), however, believed substantial differences existed between the specimens described by MacCallum (191) and Johnston (193) and established Oochoristica australiensis Spasskii, 1951, for Johnston's specimens. Oochoristica vacuolata Hickman, 1954, was described from the lizard Egernia whitii (Lacepede). Three additional species of Oochoristica, namely, O. antechini Beveridge, 1977, O. eremophila Beveridge, 1977, and O. nyctophili Hickman, 1954, have been described from Australian mammals; but the possession of craspedote proglottids by O. antechini and the passage of reproductive ducts dorsal to osmoregulatory canals in O. eremophila and O. nyctophili suggests to us that these 3 species should be reassigned to the genus Mathevotaenia Akumyan, The purpose of this paper is to describe a new species of Oochoristica that was found in the small intestines of the thorny devil, Moloch horridus Gray, from Australia and to list other helminth parasites found in this host. Materials and Methods One hundred four Moloch horridus from the collections of the Natural History Museum of Los Angeles County (LACM , ) were examined: 10 from Western Australia and from the 15 Northern Territory (snoutvent length = 86.1 mm ± 14.5 SD). These specimens had been collected between October 1966 and January 1968 for use in an ecological study (Pianka and Pianka, 1970); collection data will be found in that report. Because the ecological study included stomach analysis, only small and large intestines remained with most of the carcasses, but 3 intact stomachs and 5 pyloric stomach regions were present. Each organ was searched for helminths using a dissecting microscope, and the helminths found were identified utilizing a glycerol wet mount. Five cestodes were stained with Harris' hematoxylin, dehydrated in an alcohol series, cleared in xylene, wholemounted in Canada balsam, and examined by compound microscopy. Drawings were made with the aid of a microprojector. Results Five nematodes, 4 Parapharyngodon kartana (Johnston and Mawson, 1941) Adamson, 1981, and 1 larva of Abbreviata sp., were found in 5 lizards; 16 cestodes identifiable only to the genus Oochoristica were found in 8 lizards. One lizard (LACM 543) had a dual infection, namely, 1 cestode and 1 male Parapharyngodon kartana. All infected lizards were from central Western Australia within the area bounded by 6 14'S 8 31'S and 11 00'E13 15'E. Voucher specimens in vials of alcohol were deposited in the U.S. National Parasite Collection (USNPC) (Beltsville, Maryland): Oochoristica piankai, 845; Parapharyngodon kartana, 84591; and Abbreviata sp. (larva), Except where noted, all measurements are in micrometers. Oochoristica piankai sp. n. (Figs. 1^1) With characters of the genus: specifically, scolex with 4 suckers and without rostellum or ar

2 16 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, 63(), JUL 1996 O O in 1 ; >JH»wi? % QO9&9 '= * V «<5^( r eok LO CO Figures 14. Oochoristica piankai sp. n. 1. Anterior portion of cestode, scolex to proglottids with sexual primordia.. Mature proglottid. 3. Gravid proglottid. 4. Uterine capsule with onchosphere.

3 BURSEY ET AL. OOCHORISTICA PIANKAI SP. N. FROM MOLOCH HORRID US 17 mature; proglottids acraspedote; genital pores irregularly alternate; genital ducts lie between osmoregulatory canals; uterus ephemeral; testes posterior to vitellarium. Description based on 5 specimens; mean measurement and range. Total length 60 (70) mm; maximum width of strobila, 1.15 mm; proglottid number in mature worms 7 (6080); 16 immature proglottids wider than long ( mm by mm), 18 mature proglottids ( mm by mm); 168 gravid proglottids longer than wide ( mm wide by mm long). Scolex 1 (17056) wide by 189 (17000) long, with 4 circular suckers, 9 (80103) in diameter. Osmoregulatory system of 4 longitudinal canals visible throughout length of strobila. Genital pores irregularly alternating, situated in first third of proglottid. Cirrus sac length 17 (11414) long by 34 (45) wide. The genital ducts pass between the osmoregulatory canals. Ovary bilobed and situated in center of proglottid; 47 (14 85) wide by 93 (68114) long; each lobe subdivided into 68 welldefined secondary lobes. vitelline gland situated on midline directly behind ovary, 11 (85143) wide by 66 (4585) long. Ootype and Mehlis' gland complex between ovary and vitelline gland. Testes posterior to ovary and vitelline gland in 1 cluster, numbering 31 (438) in each proglottid; testes measure by 17. In gravid proglottids, uterine capsules, 17 (11414), each containing a single egg, fill entire proglottid; eggs 5 (4557); oncosphere 38 (34); oncosphere hook lengths (19) 170. Taxonomic Summary TYPE HOST: Moloch horridus Gray, 1841, "Thorny Devil" or "Moloch" (Sauria: Agamidae), deposited in the LACM, No , adult female, mm snoutvent length. TYPE LOCALITY: Western Australia (8 km NE Dunges Table Hill), 8 05'S, 13 55'E, m elevation. SITE OF INFECTION: Small intestine, adjacent to pyloric valve. PREVALENCE: Eight of 104 (8%) lizards were infected. MEAN INTENSITY: Sixteen cestodes, range 1 5, mean. TYPE SPECIMENS: Holotype: USNPC No , 1 slide; Paratype: No , 1 slide. ETYMOLOGY: The specific epithet honors Eric R. Pianka, Denton A. Cooley Centennial Professor of Zoology, University of Texas at Austin, for his pioneering studies on the ecology of Australian lizards. Remarks Comparisons of selected measurements of Oochoristica piankai sp. n. with 74 species of cestodes generally accepted as Oochoristica that infect reptiles are presented in Table 1; data were taken from original papers. Oochoristica piankai sp. n. belongs to that group of species having circular suckers, 0 testes occurring in a single cluster, and an ovoid vitellarium, namely, O. gallica Dollfus, 1954, O. junkea Johri, 19, O. parvula (Stunkard, 1938), O. vacuolata, and O. vanzolinii Rego and OliveiraRodrigues, In O. junkea, O. vacuolata, and O. vanzolinii, each lobe of the ovary is not lobulate; each lobe of the ovary of O. piankai sp. n. is subdivided into 68 distinct lobules. The strobila of O. piankai sp. n. is twice the length of O. gallica and O. parvula. Of the Australian species, O. piankai sp. n. has half as many testes as O. australiensis, 4 38 compared to 6580, and lacks the vacuoles seen in O. vacuolata. Oochoristica trachysauri has testes in clusters as compared to the single cluster in O. piankai sp. n. Discussion In addition to Oochoristica piankai sp. n., other helminths found in Moloch horridus are reported for the first time. Two male and female Parapharyngodon kartana were found in the large intestines of 4 lizards. Parapharyngodon kartana was originally described as Thelandros kartana from the skink Hemiergisperonii from Kangaroo Island, Australia (Johnston and Mawson, 1941). It was also found in the gecko Christinus marmoratus as well as H. peronii by Angel and Mawson (1968) and in the agamid Ctenophorus fionni and the skink Lerista sp. as well as H. peronii by Mawson (1971). Thelandros kartana was reassigned to the genus Parapharyngodon by Adamson (1981) and has since been reported from the skinks Emoia nigra and E. samoenses from Samoa by Goldberg and Bursey (1991). Moloch horridus is a new host record for P. kartana. A stomach cyst containing 1 larva of Abbreviata sp. was also found. Jones (1995) examined the stomach contents of 85 Moloch horridus and found 9 (10.6%) to contain larval physalopterids (mean intensity 1.4). Jones (1995) believes that

4 Table 1. Geographic distribution and selected characters of species of Oochoristica from reptiles. Realm Oochoristica sp. No. proglottids Strobila Maximum length Neck Scolex Mean width (/im) Size (/im) Sucker Shape Australian realm O. australiensis Spasskii, 1951 O. novaezealandae Schmidt and Allison, 1985 O. piankai sp. n. O. trachysauri (MacCallum, 191) O. vacuolata Hickman, 1954 Ethiopian realm O. chavenoni Capron, Brygoo, and Broussert, 196 O. courduieri Capron, Brygoo, and Broussert, 196 O. crassiceps Baylis, 1 90 O. danielae Capron, Brygoo, and Broussert, 196 O. najdei Magzoub, Kasim, and Shawa, 1980 O. nupta Kugi and Mohammad, 1988 O. theileri Fuhrmann, 194 O. truncata (Krabbe, 1879) O. ubelakeri Bursey, McAllister, Freed, and Freed, 1994 Nearctic realm O. americana Harwood, 193 O. anniellae Stunkard and Lynch, O. anolis Harwood, 193 O. bezyi Bursey and Goldberg, 199 O. bivitellobata Loewen, 1 9 O. crotaphyti McAllister, Trauth, and Ubelaker, 1985 O. elaphis Harwood, 193 O. eumecis Harwood, 193 O. gracewileyae Loewen, 1 9 O. islandensis Bursey and Goldberg, 1 99 O. natricis Harwood, 193 O. osheroffi Meggitt, 1934 O. scelopori Voge and Fox, 19 O. whitentoni Stellman, 1939 Neotropical realm O. ameivae (Beddard, 1914) O. bresslaui Fuhrmann, 197 * > >00 69 > > > , x x x 95 ± x x x x x x x x x la la la la la la la la la la la la la la la la JOURNAI

5 Table 1. Continued. Realm Oochoristica sp. No. proglottids Strobila Maximum length Neck Scolex Mean width G*m) Size (Mm) Sucker Shap O. insulaemargaritae LopezNeyra and DiazUngria, 1957 O. parvula (Stunkard, 1938) O. travassosi Rego and Ibanez, 1965 O. vanzolinii Rego and OliveiraRodrigues, 1965 Oriental realm O. aulicus Johri, 1961 O. bailea Singal, 1961 O. calotes Nama and Khichi, 1974 O. celebesensis Yamaguti, 1954 O. chinensis Jensen, Schmidt, and Kuntz, 1983 O. cryptobothrium (Linstow, 1 6) O. excelsa Tubangui and Masilungan, 1936 O. fibrata Meggitt, 197 O. hainanaensis Hsu, 1935 O. hemidactyli Johri, 1955 O. indica Misra, O. javaensis Kennedy, Killick, and BeverleyBurton, 198 O. jodhpurensis Nama, 1977 O. junkea Johri, 19 O. langrangei Joyeux and Houdemer, 1 97 O. lygosomae Burt, 1933 O. lygosomatis Skinker, 1935 O. mandapamensis Johri, 1958 O. microscolex Delia Santa, 1956 O. ophia Capoor, Srivastava, and Chauhan, 1974 O. pauriensis Malhotra and Gapoor, 1984 O. tandani Singh, 1957 O. thapari Johri, 1934 O. varani Nama and Khichi, 197 Palaearctic realm O. brachysoma Dupouy and Kechemir, 1973 O. chabaudi Dollfus, 1954 O. darensis Dollfus, 1957 O. elongata Dupouy and Kechemir, 1973 O. gallica Dollfus, _ > > > , , , x x x x 8 16 x x x x

6 0 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, 63(), JUL 1996 Si D "jf.s B E 'ti e oo c 5 Sa o go C* * 1 3 ;o 3 uuuuuuuuuuuu a a ^ Quo UU >.5 > QUO O OJ 0).is > > U O O XOOOXO^X'OX X. <! o o o 1 I i. a ISS <u u VI CA U S PH OH I I I u u M M OOOOOOOOOOOO termites, perhaps beetles and cockroaches as well, act as intermediate hosts for larvae of species of Abbreviata. These hosts are consumed by many species of small lizards that act as paratenic hosts and no further development of the nematode occurs until these paratenic hosts are consumed by one of the larger lizards (i.e., species of Varanus or Pogond). Pianka (1994) reported Moloch horridus and other species of small lizards to be regular items of the diet of species of Varanus. Of the 58 species of Abbreviata known to infect reptiles (see Baker, 1987), 15 species (6%) are known from Australian lizards including Varanus spp. Because these definitive hosts do not feed directly on termites, paratenic hosts are an essential link in Abbreviata life cycles (Jones, 1995). Pianka and Pianka (1970) examined the stomachs of 103 Moloch horridus and found only ants (at least 3 species) and a few tiny objects such as stones, sticks, flowers, and insect eggs, which they believed the ants to be carrying at the time of ingestion. These observations raise a question as to the mode of infection of M. horridus by the helminths reported in this paper. Although the life history of Parapharyngodon kartana has not been studied, it would be predicted to have a direct life cycle similar to that of other oxyurids (Anderson, 199), with infection occurring by ingestion of eggs from a fecally contaminated substratum. Such substrata could be ingested at the time ants are taken. Physalopterids require an insect intermediate host in which development to thirdstage larvae occurs (Anderson, 199). Ants carrying dismembered but infected insect parts could be the source of infections. The biology of Oochoristica piankai has not been examined, but Hickman (1963) studied the life history of O. vacuolata in some detail. The adult cestode is estimated to live for 4 yr and shed at least 13 proglottids; the tenebrionid beetle, Cestrinus punctatissimus Pascoe, serves as a natural intermediate host and, experimentally, the cockroach Platyzosteria melanaria Erichson, the dermestid beetle Anthrenocerus australis Hope, and the carabid bettles Gnathaphanus adelaidae Castelnau, Hypharpax moestus Dejean, Mecyclothorax ambiguus Erichson, Promecoderus gibbosus Gray, and Homothes guttifer Germar are capable of serving as intermediate hosts. The paucity of these helminths in M. horridus suggests an "accidental" route of infection. Further study will be required to determine whether or not other desert reptiles share these helminths.

7 BURSEY ET AL.OOCHORISTICA PIANKAI SP. N. FROM MOLOCH HORRIDUS 1 Key to Species of Australian Oochoristica 1. Testes in 1 cluster Testes in clusters O. trachysauri MacCallum, 191. Fewer than testes 3 More than 60 testes O. australiensis Spasskii, Ovarian lobes not subdivided O. vacuolata Hickman, 1954 Ovarian lobes subdivided into 68 lobules O. piankai sp. n. Acknowledgments We thank Peggy Firth for the preparation of the illustrations constituting Figures 14 and Robert L. Bezy, Natural History Museum of Los Angeles County, for allowing us to examine the lizards. Literature Cited Adamson, M. L Parapharyngodon osteopili n. sp. (Pharyngodonidae: Oxyuroidea) and a revision of Parapharyngodon and Thelandros. Systematic Parasitology 3: Anderson, R. C Nematode Parasites of Vertebrates. Their Development and Transmission. C.A.B. International, Wallingford, Oxon, U.K. 578 PP Angel, L. M., and P. M. Mawson Helminths from some lizards mostly from South Australia. Transactions of the Royal Society of South Australia 9:597. Baer, J. G Monographic des Cestodes de la famille des Anoplocephalidae. Bulletin Biologique de France et de Belgique, Paris, Supplement 10: 141. Baker, M. R Synopsis of the Nematoda parasitic in amphibians and reptiles. Memorial University of Newfoundland, Occasional Papers in Biology 11:135. Goldberg, S. R., and C. R. Bursey Parapharyngodon kartana in two skinks, Emoia nigra and Emoiasamoense (Sauria: Scincidae), from Samoa. Journal of the Helminthological Society of Washington 58:6566. Hickman, J. L The biology of Oochoristica vacuolata Hickman (Cestoda). Papers and Proceedings of the Royal Society of Tasmania 97: Johnston, T. H The parasites of the "stumpytail" lizard, Trachysaurus rugosus. Transactions and Proceedings of the Royal Society of South Australia 56:670., and P. M. Mawson Some nematodes from Kangaroo Island, South Australia. Records of the South Australian Museum 7: Jones, H. I Gastric nematode communities in lizards from the Great Victoria Desert, and an hypothesis for their evolution. Australian Journal of Zoology 43: MacCallum, G. A Studies in helminthology. Zoopathologica 1: Mawson, P. M Pearson Island Expedition Helminths. Transactions of the Royal Society of South Australia 95: Pianka, E. R Comparative ecology of Varanus in the Great Victoria Desert. Australian Journal of Ecology 19:395^*08., and H. D. Pianka The ecology of Moloch horridus (Lacertilia: Agamidae) in Western Australia. Copeia 1970:103. Spasskii, A. A Essentials of Cestodology. Vol. 1. Anoplocephalate Tapeworms of Domestic and Wild Animals. The Israel Program for Scientific Translations, Jerusalem, 1961, 783 pp.