Oochoristica Piankai Sp. N. (Cestoda: Linstowiidae) and Other Helminths of Moloch Horridus (Sauria: Agamidae) from Australia

J. Helminthol. Soc. Wash. 63(2), 1996, pp. 215-221

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

CHARLES R. BURSEY,' STEPHEN R. GOLDBERG,2 AND DAVID N. WooLERY2 'Department of Biology, Pennsylvania State University, Shenango Campus, Sharon, Pennsylvania 16146 (e- mail: [email protected]), and 2Department of Biology, Whittier College, Whittier, California 90608 (e-mail: [email protected])

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, Mo- loch horridus, lizard, Agamidae, Australia.

Only 3 of 74 species of Oochoristica Luhe, Northern Territory (snout-vent length = 86.1 mm ± 1898, a cosmopolitan genus of cestodes, have 14.5 SD). These specimens had been collected between been reported previously from reptiles of Aus- October 1966 and January 1968 for use in an ecological study (Pianka and Pianka, 1970); collection data will tralia. Taenia trachysauri MacCallum, 1921, was be found in that report. Because the ecological study described from specimens discovered in the in- included stomach analysis, only small and large intes- testine of the Australian lizard Trachydosaurus tines remained with most of the carcasses, but 3 intact rugosus Gray, in the New York Zoological Gar- stomachs and 5 pyloric stomach regions were present. Each organ was searched for helminths using a dis- den. Baer (1927) moved Taenia trachysauri to secting microscope, and the helminths found were the genus Oochoristica. Johnston (1932) reported identified utilizing a glycerol wet mount. Five cestodes O. trachysauri in Trachdoysaurus rugosus. Spas- were stained with Harris' hematoxylin, dehydrated in skii (1951), however, believed substantial differ- an alcohol series, cleared in xylene, whole-mounted in ences existed between the specimens described Canada balsam, and examined by compound micros- copy. Drawings were made with the aid of a micro- by MacCallum (1921) and Johnston (1932) and projector. established Oochoristica australiensis Spasskii, 1951, for Johnston's specimens. Oochoristica Results vacuolata Hickman, 1954, was described from Five nematodes, 4 Parapharyngodon kartana the lizard Egernia whitii (Lacepede). Three ad- (Johnston and Mawson, 1941) Adamson, 1981, ditional species of Oochoristica, namely, O. an- and 1 larva of Abbreviata sp., were found in 5 techini Beveridge, 1977, O. eremophila Bever- lizards; 16 cestodes identifiable only to the genus idge, 1977, and O. nyctophili Hickman, 1954, Oochoristica were found in 8 lizards. One lizard have been described from Australian mammals; (LACM 54223) had a dual infection, namely, 1 but the possession of craspedote proglottids by cestode and 1 male Parapharyngodon kartana. O. antechini and the passage of reproductive ducts All infected lizards were from central Western dorsal to osmoregulatory canals in O. eremophila Australia within the area bounded by 26°14'S- and O. nyctophili suggests to us that these 3 spe- 28°31'S and 121°00'E-123°15'E. Voucher spec- cies should be reassigned to the genus Mathev- imens in vials of alcohol were deposited in the otaenia Akumyan, 1946. The purpose of this pa- U.S. National Parasite Collection (USNPC) per is to describe a new species of Oochoristica (Beltsville, Maryland): Oochoristica piankai, that was found in the small intestines of the thorny 84590; Parapharyngodon kartana, 84591; and devil, Moloch horridus Gray, from Australia and Abbreviata sp. (larva), 84592. Except where not- to list other helminth parasites found in this host. ed, all measurements are in micrometers. Materials and Methods Oochoristica piankai sp. n. One hundred four Moloch horridus from the collec- (Figs. 1^1) tions of the Natural History Museum of Los Angeles County (LACM 54134-54223, 55269-55282) were ex- With characters of the genus: specifically, sco- amined: 102 from Western Australia and 2 from the lex with 4 suckers and without rostellum or ar- 215

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Figures 1-4. Oochoristica piankai sp. n. 1. Anterior portion of cestode, scolex to proglottids with sexual primordia. 2. Mature proglottid. 3. Gravid proglottid. 4. Uterine capsule with onchosphere.

Copyright © 2011, The Helminthological Society of Washington BURSEY ET AL. - OOCHORISTICA PIANKAI SP. N. FROM MOLOCH HORRID US 217 mature; proglottids acraspedote; genital pores ir- R. Pianka, Denton A. Cooley Centennial Pro- regularly alternate; genital ducts lie between os- fessor of Zoology, University of Texas at Austin, moregulatory canals; uterus ephemeral; testes for his pioneering studies on the ecology of Aus- posterior to vitellarium. tralian lizards. Description based on 5 specimens; mean mea- surement and range. Total length 60 (40-70) mm; Remarks maximum width of strobila, 1.15 mm; proglottid Comparisons of selected measurements of number in mature worms 72 (60-80); 16-22 im- Oochoristica piankai sp. n. with 74 species of mature proglottids wider than long (0.615-0.714 cestodes generally accepted as Oochoristica that mm by 0.179-0.255 mm), 18-30 mature pro- infect reptiles are presented in Table 1; data were glottids (0.620-0.750 mm by 0.765-0.893 mm); taken from original papers. Oochoristica piankai 16-28 gravid proglottids longer than wide (0.750- sp. n. belongs to that group of species having 1.147 mm wide by 2.04-6.00 mm long). Scolex circular suckers, 20-40 testes occurring in a sin- 221 (170-256) wide by 189 (170-200) long, with gle cluster, and an ovoid vitellarium, namely, O. 4 circular suckers, 92 (80-103) in diameter. Os- gallica Dollfus, 1954, O. junkea Johri, 1950, O. moregulatory system of 4 longitudinal canals vis- parvula (Stunkard, 1938), O. vacuolata, and O. ible throughout length of strobila. Genital pores vanzolinii Rego and Oliveira-Rodrigues, 1965. irregularly alternating, situated in first third of In O. junkea, O. vacuolata, and O. vanzolinii, proglottid. Cirrus sac length 127 (114-142) long each lobe of the ovary is not lobulate; each lobe by 34 (22-45) wide. The genital ducts pass be- of the ovary of O. piankai sp. n. is subdivided tween the osmoregulatory canals. Ovary bilobed into 6-8 distinct lobules. The strobila of O. pian- and situated in center of proglottid; 247 (142- kai sp. n. is twice the length of O. gallica and O. 285) wide by 93 (68-114) long; each lobe sub- parvula. Of the Australian species, O. piankai sp. divided into 6-8 well-defined secondary lobes. n. has half as many testes as O. australiensis, 24- Oval vitelline gland situated on midline directly 38 compared to 65-80, and lacks the vacuoles behind ovary, 121 (85-143) wide by 66 (45-85) seen in O. vacuolata. Oochoristica trachysauri long. Ootype and Mehlis' gland complex between has testes in 2 clusters as compared to the single ovary and vitelline gland. Testes posterior to cluster in O. piankai sp. n. ovary and vitelline gland in 1 cluster, numbering 31 (24-38) in each proglottid; testes measure 11- Discussion 17 by 17-22. In gravid proglottids, uterine cap- In addition to Oochoristica piankai sp. n., oth- sules, 127 (114-142), each containing a single er helminths found in Moloch horridus are re- egg, fill entire proglottid; eggs 52 (45-57); on- ported for the first time. Two male and 2 female cosphere 38 (34-40); oncosphere hook lengths Parapharyngodon kartana were found in the large (19) 17-20. intestines of 4 lizards. Parapharyngodon kartana was originally described as Thelandros kartana Taxonomic Summary from the skink Hemiergisperonii from Kangaroo TYPE HOST: Moloch horridus Gray, 1841, Island, Australia (Johnston and Mawson, 1941). "Thorny Devil" or "Moloch" (Sauria: Agami- It was also found in the gecko Christinus mar- dae), deposited in the LACM, No. 54199, adult moratus as well as H. peronii by Angel and Maw- female, 90 mm snout-vent length. son (1968) and in the agamid Ctenophorus fionni TYPE LOCALITY: Western Australia (8 km NE and the skink Lerista sp. as well as H. peronii by Dunges Table Hill), 28°05'S, 123°55'E, 250 m Mawson (1971). Thelandros kartana was reas- elevation. signed to the genus Parapharyngodon by Ad- SITE OF INFECTION: Small intestine, adjacent amson (1981) and has since been reported from to pyloric valve. the skinks Emoia nigra and E. samoenses from PREVALENCE: Eight of 104 (8%) lizards were Samoa by Goldberg and Bursey (1991). Moloch infected. horridus is a new host record for P. kartana. MEAN INTENSITY: Sixteen cestodes, range 1- A stomach cyst containing 1 larva of Abbrev- 5, mean 2. iata sp. was also found. Jones (1995) examined TYPE SPECIMENS: Holotype: USNPC No. the stomach contents of 85 Moloch horridus and 84588, 1 slide; Paratype: No. 84589, 1 slide. found 9 (10.6%) to contain larval physalopterids ETYMOLOGY: The specific epithet honors Eric (mean intensity 1.4). Jones (1995) believes that

Strobila Scolex Sucker Testes Ovary No. Maximum Mean Vitellaria Realm prog- length Neck width Size Arrange- Lobules/ Oochoristica sp. lottids (mm) (mm) (/im) (/im) Shape Number ment lobe Shape

Australian realm O O. australiensis Spasskii, 1951 * 220 0.4 335 120 Circular 65-80 1 Cluster 3-7 Ovoid aH O. novaezealandae Schmidt and Allison, 1985 20 20 None 250 90 Circular 12-15 1 Cluster None Spheroid tn Circular 1 a O. piankai sp. n. 82 70 0.6 213 92 24-38 Cluster 5-7 Ovoid m O. trachysauri (MacCallum, 1921) — 50 — 330 150 Circular 60 2 Clusters None Ovoid g O. vacuolata Hickman, 1954 53 53 0.8 300 130 Circular 19-45 1 Cluster None Ovoid hU Z Ethiopian realm H O. chavenoni Capron, Brygoo, and Broussert, 1962 150 50 2.0 370 120 x 154 Oval 22-31 1 Cluster 3-6 Ovoid Or O. courduieri Capron, Brygoo, and Broussert, 1962 130 110 1.5 780 180-208 Oval 35-1 6 1 Cluster 7-9 Ovoid 0 O O. crassiceps Baylis, 1 920 100 30 2.5 1,050 250 x 300 Oval 20-30 1 Cluster None Ovoid O. danielae Capron, Brygoo, and Broussert, 1962 100 60 0.8 840 104 x 130 Oval 30-42 1 Cluster 2-3 Triangular r> O. najdei Magzoub, Kasim, and Shawa, 1980 — 75 Present 320 95 Circular 16-24 2 Clusters 1-3 Triangular on O. nupta Kugi and Mohammad, 1988 - 50 None 250 53 ± 82 Oval 28-30 2 Clusters None Ovoid O. theileri Fuhrmann, 1924 28 8 None 350 130 Circular 26-35 2 Clusters None Round 8 O. truncata (Krabbe, 1879) >48 115 None 550 180 Circular 27-48 1 Cluster 6-9 Triangular H O. ubelakeri Bursey, McAllister, Freed, and Freed, 1994 65 25 None 388 150 x 200 Oval 22-30 2 Clusters 3-5 Ovoid

O. americana Harwood, 1932 — 40 3 500 160 Circular 35-40 1 Cluster 6-8 Triangular o^n O. anniellae Stunkard and Lynch, 1 944 45 15 None 385 112 x 163 Oval 60-70 1 Cluster None Triangular a O. anolis Harwood, 1932 — 70 2 350 160 x 300 Oval 20-35 1 Cluster 5-6 Triangular o O. bezyi Bursey and Goldberg, 1992 30 8 0.57 250 119 x 150 Oval 22-32 2 Clusters 6-8 Triangular H O. bivitellobata Loewen, 1 940 21 150 0.43 413 147 Circular 48-106 1 Cluster None Bilobed § O. crotaphyti McAllister, Trauth, and Ubelaker, 1985 52 27 None 373 105 x 126 Oval 23-37 1 Cluster 3 Ovoid o O. elaphis Harwood, 1932 75 5.5 350 145 Circular 30-53 1 Cluster None Kidney shape u> - "K> O. eumecis Harwood, 1932 — 103 2 500 220 x 260 Oval 40-55 1 Cluster 3-5 Triangular O. gracewileyae Loewen, 1 940 >200 >850 2.4 426 145 x 152 Oval 70-140 1 Cluster Numerous Triangular ^G O. islandensis Bursey and Goldberg, 1 992 69 24 None 318 120 x 170 Oval 38-1 6 2 Clusters 8-10 Triangular r *0 O. natricis Harwood, 1932 — 130 1-2 550 190 x 260 Oval 50-70 1 Cluster None Triangular O. osheroffi Meggitt, 1934 >200 205 0.95 385 136 Circular 59-76 1 Cluster 4-8 Ovoid O. scelopori Voge and Fox, 1950 171 120 3 365 115 Circular 22-43 1 Cluster Numerous Triangular O. whitentoni Stellman, 1939 >211 275 3.3 400 165 Circular 100-150 1 Cluster 10-12 Ovoid Neotropical realm O. ameivae (Beddard, 1914) — 120 Short 550 175 Circular 39-50 1 Cluster 5-8 Irregular O. bresslaui Fuhrmann, 1927 — 40 2 140 54 Circular 60 1 Cluster 5-6 Irregular

I JOURNA Tabl e 1. Continued.

Strobila Scolex Sucker Testes Ovary No. Maximum Mean Vitellaria Realm prog- length Neck width Size Arrange- Lobules/ Oochoristica sp. lottids (mm) (mm) G*m) (Mm) Shape Number ment lobe Shape

O. insulaemargaritae Lopez-Neyra and Diaz-Ungria, 1957 78 115 None 1,025 260 x 358 Oval 67-83 1 Cluster Numerous Irregular O. parvula (Stunkard, 1938) 65 25 4 245 78 Circular 20-30 1 Cluster 3-5 Ovoid O. travassosi Rego and Ibanez, 1965 12 0.75 600 158 x 165 Oval 26-32 1 Cluster 6-10 Irregular — O. vanzolinii Rego and Oliveira-Rodrigues, 1965 180 90 1.9 172 95 Circular 20-28 1 Cluster None Ovoid Oriental realm _ O. aulicus Johri, 1961 172 2.00 325 115 Circular 25-30 1 Cluster Several Triangular O. bailea Singal, 1961 128 None 182 78 Circular 42^ 6 2 Clusters Several Irregular — O. calotes Nama and Khichi, 1974 176 100 None 210 92 Circular 45-55 1 Cluster 10-20 Ovoid O. celebesensis Yamaguti, 1954 140 40 0.52 700 225 Circular 22-31 1 Cluster 5-7 Irregular O. chinensis Jensen, Schmidt, and Kuntz, 1983 128 71 1 225 84 x 108 Oval 12-25 1 Cluster 5-7 Irregular O. cryptobothrium (Linstow, 1 906) 130 0.23 600 140 x 250 Oval 80-90 1 Cluster None Spheroid — O. excelsa Tubangui and Masilungan, 1936 26 Short 250 82 Circular 23-29 1 Cluster None 2 Lobes — O. fibrata Meggitt, 1927 90 None 338 126 x 170 Oval 35-36 2 Clusters 7-10 2 Lobes — O. hainanaensis Hsu, 1935 202 134 1.94 352 150 Circular 40-50 1 Cluster 5-8 Ovoid O. hemidactyli Johri, 1955 49 Short 200 80 Circular 19-30 2 Clusters 5-8 Irregular — O. indica Misra, 1 945 >91 200 6.0 350 180 Circular 30-36 1 Cluster 13-18 Irregular O. javaensis Kennedy, Killick, and Beverley-Burton, 1982 100 44 1.35 177 48 Circular 25-31 1 Cluster 5-7 Spheroid O. jodhpurensis Nama, 1977 91 50 1, 18 205 105 Circular 24-26 2 Clusters Several Irregular Copyright © HelminthologicalThe 2011,of SocietyCopyright© Washingto O. junkea Johri, 1950 53 None 225 125 Circular 23 1 Cluster None Ovoid — O. langrangei Joyeux and Houdemer, 1 927 — 60 2.24 400 180 Circular 50-60 1 Cluster Numerous Ovoid O. lygosomae Burt, 1933 45 15 Short 280 140 Circular 17-18 1 Cluster 5-7 Ovoid O. lygosomatis Skinker, 1935 45 11 2 230 110 Circular 14-18 1 Cluster Several Crescent O. mandapamensis Johri, 1958 14 5.0 160 90 Circular 30-3 4 2 Clusters None Irregular — O. microscolex Delia Santa, 1956 — >35 None 236 95 Circular 50-6 0 1 Cluster None Triangular O. ophia Capoor, Srivastava, and Chauhan, 1974 — 140 4.20 540 160 Circular 38-70 2 Clusters 4-14 Triangular O. pauriensis Malhotra and Gapoor, 1984 174 0.23 197 50 x 105 Oval 31-55 1 Cluster 3-5 Crescent O. tandani Singh, 1957 —40 90 Short 270 115 Circular 37^*5 1 Cluster 4-5 Spheroid O. thapari Johri, 1934 21 None 305 — 48-62 1 Cluster None Ovoid — O. varani Nama and Khichi, 1972 -— 30 Short 370 152 x 287 Oval 40-55 1 Cluster Several Globular Palaearctic realm O. brachysoma Dupouy and Kechemir, 1973 63 40 1.0 1,000 185 Circular 20 2 Clusters None Ovoid O. chabaudi Dollfus, 1954 65 53 430 145 x 155 Oval 36-3 8 1 Cluster 4-6 Ovoid — O. darensis Dollfus, 1957 — 72 Present 485 145 Circular 52-70 2 Clusters 5-7 Irregular O. elongata Dupouy and Kechemir, 1973 >50 Present 315 80 Circular 20-25 1 Cluster None Spheroid — O. gallica Dollfus, 1954 - 30 Present 278 117 Circular 39-40 1 Cluster 5-7 Ovoid n 220 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, 63(2), JUL 1996

termites, perhaps beetles and cockroaches as well, act as intermediate hosts for larvae of species of 3 8 1* 3 ;o 3 1 1 1 Abbreviata. These hosts are consumed by many species of small lizards that act as paratenic hosts and no further development of the nematode oc- curs until these paratenic hosts are consumed by •Si 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 uuuuuuuuuuuu reptiles (see Baker, 1987), 15 species (26%) are known from Australian lizards including Var- anus spp. Because these definitive hosts do not feed directly on termites, paratenic hosts are an essential link in Abbreviata life cycles (Jones, 1995).

O OJ 0) Pianka and Pianka (1970) examined the stom- a a ^ > .5 > .is > > Quo UU QUO U O O achs of 103 Moloch horridus and found only ants (at least 3 species) and a few tiny objects such as

D "jf stones, sticks, flowers, and insect eggs, which they .S B XOOOXO^X-'OX X 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

Key to Species of Australian Oochoristica Baker, M. R. 1987. Synopsis of the Nematoda par- asitic in amphibians and reptiles. Memorial Uni- 1. Testes in 1 cluster 2 versity of Newfoundland, Occasional Papers in Testes in 2 clusters Biology 11:1-325. O. trachysauri MacCallum, 1921 Goldberg, S. R., and C. R. Bursey. 1991. Paraphar- 2. Fewer than 50 testes 3 yngodon kartana in two skinks, Emoia nigra and More than 60 testes Emoiasamoense (Sauria: Scincidae), from Samoa. O. australiensis Spasskii, 1951 Journal of the Helminthological Society of Wash- 3. Ovarian lobes not subdivided ington 58:265-266. O. vacuolata Hickman, 1954 Hickman, J. L. 1963. The biology of Oochoristica Ovarian lobes subdivided into 6-8 lobules vacuolata Hickman (Cestoda). Papers and Pro- O. piankai sp. n. ceedings of the Royal Society of Tasmania 97:81- 104. Acknowledgments Johnston, T. H. 1932. The parasites of the "stumpy- We thank Peggy Firth for the preparation of tail" lizard, Trachysaurus rugosus. Transactions and Proceedings of the Royal Society of South the illustrations constituting Figures 1-4 and Australia 56:62-70. Robert L. Bezy, Natural History Museum of Los , and P. M. Mawson. 1941. Some nematodes Angeles County, for allowing us to examine the from Kangaroo Island, South Australia. Records lizards. of the South Australian Museum 7:145-148. Jones, H. I. 1995. Gastric nematode communities in Literature Cited lizards from the Great Victoria Desert, and an hypothesis for their evolution. Australian Journal Adamson, M. L. 1981. Parapharyngodon osteopili n. of Zoology 43:141-164. sp. (Pharyngodonidae: Oxyuroidea) and a revision MacCallum, G. A. 1921. Studies in helminthology. of Parapharyngodon and Thelandros. Systematic Zoopathologica 1:135-284. Parasitology 3:105-117. Mawson, P. M. 1971. Pearson Island Expedition Anderson, R. C. 1992. Nematode Parasites of Ver- 1969. —8. Helminths. Transactions of the Royal tebrates. Their Development and Transmission. Society of South Australia 95:169-183. C.A.B. International, Wallingford, Oxon, U.K. 578 Pianka, E. R. 1994. Comparative ecology of Varanus PP- in the Great Victoria Desert. Australian Journal Angel, L. M., and P. M. Mawson. 1968. Helminths of Ecology 19:395^*08. from some lizards mostly from South Australia. , and H. D. Pianka. 1970. The ecology of Mo- Transactions of the Royal Society of South Aus- loch horridus (Lacertilia: Agamidae) in Western tralia 92:59-72. Australia. Copeia 1970:90-103. Baer, J. G. 1927. Monographic des Cestodes de la Spasskii, A. A. 1951. Essentials of Cestodology. Vol. famille des Anoplocephalidae. Bulletin Biologique 1. Anoplocephalate Tapeworms of Domestic and de France et de Belgique, Paris, Supplement 10: Wild Animals. The Israel Program for Scientific 1-241. Translations, Jerusalem, 1961, 783 pp.