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Helminth Records from Eleven of (Sauria: Scincidae) from Oceania1

Stephen R. Goldberg,2 Charles R. Bursey,3 and Robert N. Fisher4

Abstract: As part of an ongoing study of the biogeography of helminth parasites of from Oceania, 53 specimens of Emoia (11 species) were examined, as follows: E. atrocostata, E. boettgeri, E. caerulocauda, E. cyanogaster, E. cyanura, E. impar, E. nigra, E. nigromarginata, E. ponapea, E. sanfordi, E. trossula. One species of Digenea, Paradistomoides gregarium, and six species of Nematoda, Hedruris hanleyae, Maxvachonia chabaudi, Parapharyngodon maplestoni, Physalopteroides ar- noensis, Spauligodon gehyrae, and Moaciria sp. indet., were found. These hel- minths have been reported previously from other species. Seventeen new host records and eight new locality records are reported.

As part of an ongoing investigation of the materials and methods biogeography of helminth parasites of lizards Eleven species of ( ¼ 53) from Oce- in Oceania, we identified helminths from a Emoia n ania were examined, as follows: E. atrocostata collection of (Emoia spp.) from Belau, ( ¼ 1, Kobasang Island, Belau, 7 30 0 N, Federated States of , Fiji, Tonga, n 134 30 0 N); E. boettgeri (n ¼ 1, Pohnpei Is- and . The Emoia consists of at land, Federated States of Micronesia, 9 00 least 72 species that range from Southeast N, 150 00 E); E. caerulocauda (n ¼ 8, Efate Asia through the Indo-Australian Archipelago 0 0 and Oceania (Brown 1991). To our knowl- Island, Vanuatu, 15 0 S, 168 0 E); E. cya- nogaster (n ¼ 2, Efate Island, Vanuatu); E. cy- edge, only , E. nigra, and E. anura (n ¼ 9; 4 from the Kingdom of Tonga, samoensis have previously been reported to 0 0 harbor helminths (Goldberg and Bursey 19 50 S, 174 30 W; 1 from Pohnpei Island, Federated States of Micronesia; 4 from Na- 1991, Goldberg et al. 2000). The purpose of nuku Island, Fiji, 16 35 0 S, 179 08 0 E); this paper is to add helminths from 11 species E. impar (n ¼ 5; 4 from Efate Island, Vanuatu; of Emoia to the checklist of endoparasites for 1 from Ugaga Island, Fiji, 18 22 0 S, 178 13 0 lizards from Oceania and to ascertain their E); ( ¼ 11, Kingdom of Tonga); distribution on the islands of Oceania. The E. nigra n ( ¼ 10, Efate Island, Van- checklist of endoparasites for lizards from E. nigromarginata n uatu); ( ¼ 1, Pohnpei Island, Oceania began with the summaries of hel- E. ponapea n Federated States of Micronesia); minthological data on geckonid and scincid E. sanfordi ( ¼ 1, Efate Island, Vanuatu); lizards by Goldberg et al. (1998, 2000) and n E. trossula ¼ Goldberg and Bursey (2002). (n 4, Kingdom of Tonga). Lizards from the Kingdom of Tonga were collected in 1972 and are deposited in the Museum of the South Pacific, Suva, Fiji. , 1 Manuscript accepted 12 November 2004. E. boettgeri, and E. ponapea were collected 2 Department of Biology, Whittier College, Whittier, in 1991 and are deposited in the California California 90608. 3 Department of Biology, Pennsylvania State Univer- Academy of Sciences, San Francisco. All sity, Shenango Campus, Sharon, Pennsylvania 16146. other Emoia were collected in 1993 and are 4 U.S. Geological Survey, 5745 Kearny Villa Road, deposited in the United States National Mu- Suite M, San Diego, California 92123. seum, Washington, D.C. Lizards were dissected shortly after cap- Pacific Science (2005), vol. 59, no. 4:609–614 ture; helminths were removed and placed in : 2005 by University of Hawai‘i Press vials of 70% ethanol; the carcasses were then All rights reserved preserved in 10% formalin and subsequently

609 610 PACIFIC SCIENCE . October 2005 stored in 70% ethanol. For lizards from the discussion Kingdom of Tonga, the esophagus, stomach, and small and large intestines were opened Paradistomoides gregarium was originally de- and separately searched for helminths under scribed as Paradistomum magnum from speci- a dissecting microscope. From the other lo- mens taken from the gall bladder of a , calities, only stomachs were examined. The Hemidactylus frenatus, collected in the Philip- helminths were examined in 2001, at which pines by Tubangui (1928). However, Paradi- time the nematodes were identified after stomum magnum was preoccupied, and clearing in a drop of glycerol under a cover- Tubangui (1929) changed the name to Para- slip on a microscope slide, and the digeneans distomum gregarium, which was assigned to were stained with hematoxylin and studied as its current genus by Travassos (1944). Syno- whole mounts. nyms include Paradistomum brevis, P. gecko- num, P. laruei, P. magnum, P. medicus, P. results oroterminosus, and P. paloensis. Additional hosts include the agamid lizards Calotes versicolor, We found one species of Digenea, Paradi- Hydrosaurus pustulatus; the gekkonids Cosym- stomoides gregarium (Dicrocoeliidae), and six botus platyurus, mutilata, G. oceanica, species of Nematoda: Hedruris hanleyae Gekko gecko, Hemidactylus frenatus, H. brookii, (Hedruridae), Maxvachonia chabaudi (Cosmo- Lepidodactylus guppyi, Nactus pelagicus; the la- cercidae), Moaciria sp. indet. (Heterakidae), certid Takydromus sexlineatus; and the scincids Parapharyngodon maplestoni (Pharyngodoni- Emoia cyanurum, Lipinia noctua, Prasinohaema dae), Physalopteroides arnoensis (Physalopteri- virens, Sphenomorphus solomonis (Tubangui dae), and Spauligodon gehyrae (Pharyngodo- 1933, Fischthal and Kuntz 1967, Killick and nidae). Prevalence (percentage of host Beverley-Burton 1982). Emoia atrocostata rep- species infected by a helminth species) and resents a new host record, and Belau is a new mean intensity G 1 SD (number of individ- locality record. uals of a helminth species divided by num- Hedruris hanleyae was described from the ber of infected hosts) are given in Table 1. stomach of a gecko, Hemidactylus garnotii, col- Voucher specimens of the helminths were de- lected in the Cook Islands (Bursey and Gold- posited in the United States National Parasite berg 2000). Additional hosts include Gehyra Collection (USNPC), Beltsville, Maryland: mutilata, G. oceanica, Hemidactylus frenatus, Emoia atrocostata (Paradistomoides gregarium, Lepidodactylus lugubris, L. moestus, and L. paur- USNPC 93732); Emoia boettgeri (Hedruris olepis. Emoia boettgeri, E. caerulocauda, E. cya- hanleyae, USNPC 93733; Moaciria sp. indet., nogaster, E. cyanura, E. impar, E. nigra, E. USNPC 93734); Emoia caerulocauda (Hedruris nigromarginata, E. sanfordi, and E. trossula rep- hanleyae, USNPC 93735); Emoia cyanogaster resent new host records. Vanuatu and Feder- (Hedruris hanleyae, USNPC 93736); Emoia cy- ated States of Micronesia are new locality anura (Hedruris hanleyae, USNPC 93737); records. (Hedruris hanleyae, USNPC Maxvachonia chabaudi was described from 93738, 93739); (Hedruris hanleyae, individuals pooled from nine species of lizards USNPC 93709; Maxvachonia chabaudi, and one species of snake collected in USNPC 93715; Parapharyngodon maplestoni, by Mawson (1972): the gekkonid Phyllurus USNPC 93710; Physalopteroides arnoensis, milii; the scincids australis, C. labillar- USNPC 93712); Emoia nigromarginata (He- dieri, C. leae, Egernia whitii, Eulamprus koscius- druris hanleyae, USNPC 93740); Emoia pona- koi, Hemiergis peronii, Lerista bougainvillii, pea (Moaciria sp. indet., USNPC 93741); Morethia lineoocellata; and the elapid Pseudo- Emoia sanfordi (Hedruris hanleyae, USNPC naja affinis. Additional Australian hosts 93742); Emoia trossula (Hedruris hanleyae, include the scincids Ctenotus brooksi, C. leon- USNPC 93727; Physalopteroides arnoensis, hardii, C. pantherinus, C. quattuordecimlineatus, USNPC 93731; Spauligodon gehyrae, USNPC C. regius, and Egernia inornata and the varanid 93728). Varanus tristis ( Jones 1988, Goldberg and TABLE 1 Prevalence as Percentage (P) and Mean Intensity G 1 SD (M) for Each Helminth Species Infecting 11 Species of Skinks from Oceania

Paradistomoides Maxvachonia Parapharyngodon Physalopteroides Spauligodon gregarium Hedruris hanleyae chabaudi Moaciria sp. maplestoni arnoensis gehyrae

Emoia sp. P M P M P M P M P M P M P M

E. atrocostata 1/1 (100) 22 — — — — — — — — — — — — E. boettgeri — — 1/1 (100) 1 — — 1/1 (100) 1 — — — — — — E. caerulocauda — — 8/8 (100) 2.3 G 1.5—————————— E. cyanogaster — — 2/2 (100) 1 G 0— — ———— — — —— E. cyanura — — 5/9 (56) 6.6 G 2.9 1/9 (11) 1 — — — — — — — — E. impar — — 5/5 (100) 1.8 G 1.1—————————— E. nigra — — 11/11 (100) 7.7 G 3.7 3/11 (27) 7.0 G 5.0 — — 3/11 (27) 1.0 G 0 5/11 (45) 3.2 G 3.5 — — E. nigromarginata — — 10/10 (100) 2.7 G 0.9—————————— E. ponapea — — — — — — 1/1 (100) 6 — — — — — — E. sanfordi — — 1/1 (100) 1 — — — — — — — — — — E. trossula — — 3/4 (75) 8.0 G 5.6 — — — — — — 2/4 (50) 2.5 G 2.1 1/4 (25) 3 612 PACIFIC SCIENCE . October 2005

Bursey 1995, 2000, Goldberg et al. 1999). Nematotaeniidae), Maxvachonia chabaudi, and Other reported hosts include Emoia cyanura, larvae of Skrjabinoptera sp. (Seuratidae) from Gehyra mutilata, G. oceanica, Lepidodactylus lu- E. cyanura (Goldberg and Bursey 1991, Gold- gubris, and L. paurolepis (Goldberg and Bursey berg et al. 2000). Parapharyngodon kartana was 2002). Emoia nigra represents a new host rec- described from the scincid Hemiergis peronii ord. The Kingdom of Tonga is a new locality by Johnston and Mawson (1941) and is also record. known from the agamid Ctenophorus fionni; Moaciria is represented in Australia and the gekkonid Christinus marmoratus; and a Oceania by five species (Gibbons 1979, Jones scincid, Lerista sp. (Goldberg and Bursey 1979), four species described from snakes, 1991). Cylindrotaenia decidua was described namely M. butleri, M. chondropythonis, M. et- from the scincid Oligosoma nigriplantare by nae, M. komodoensis, and one species from a Ainsworth (1985) and is also known from lizard, M. sphenomorphi. Species identification the scincid Cryptoblepharus poecilopleurus for Moaciria is based upon male caudal mor- and the gekkonid Gehyra oceanica (Goldberg phology. Only females were found in this et al. 2000). Larvae of Skrjabinoptera were study; thus identification to species was not also reported from Cryptoblepharus poecilopleu- attempted. Emoia boettgeri and E. ponapea rep- rus and Lepidodactylus lugubris (Goldberg et al. resent new host records for Moaciria. Feder- 2000). ated States of Micronesia is a new locality The 10 species of helminths harbored by record. species of Emoia are generalists (species capa- Parapharyngodon maplestoni was originally ble of infecting more than one species of liz- described from the intestine of an agamid liz- ard). For infection by these species, ecological ard, Calotes versicolor, collected in Burma by factors related to egg survival may be more Chatterji (1933). Additional hosts include the important than physiological (host) factors. agamid Bronchocela cristatellus; the anguid Species of Hedruris, Moaciria, Parapharyngo- Ophisaurus apodus; the gekkonids Hemidactylus don, and Spauligodon have monoxenous life flavoviridis, H. frenatus; and the scincid Gla- cycles and require the ingestion of an egg be- phyromorphus emigrans (Goldberg and Bursey fore infection can occur; species of Physalop- 2002). Emoia nigra is a new host record. The teroides and Skrjabinoptera have heteroxenous Kingdom of Tonga is a new locality record. life cycles that require the ingestion of the in- Physalopteroides arnoensis was described termediate host; the life cycles of species of from the intestinal tract of the gecko Lepido- Maxvachonia are unknown, although other dactylus lugubris, collected in the Republic of cosmocercoids produce larvae that utilize skin the Marshall Islands (Bursey and Goldberg penetration as a route of infection (Anderson 2001). Additional hosts include the gekkonids 2000). Trematodes and cestodes have hetero- Lepidodactylus moestus and L. paurolepis (Gold- xenous life cycles (Roberts and Janovy 2005). berg and Bursey 2002). Emoia nigra and Examination of ecological aspects of the nat- Emoia trossula represent new host records. ural history of species of Emoia may give a The Kingdom of Tonga is a new locality clue to the differential infection rates by the record. helminths reported here. Spauligodon gehyrae was described from the Helminthological examinations of ad- large intestine of the gecko Gehyra oceanica, ditional species are required before the collected in Guam (Bursey and Goldberg helminth diversity of lizard species from Oce- 1996). It has also been reported from Lepido- ania can be known and the distribution of dactylus lugubris. Emoia trossula represents a helminths among the Pacific islands can be new host record. The Kingdom of Tonga is ascertained. a new locality record. Previous reports of helminths in species acknowledgment of Emoia include Parapharyngodon kartana (Pharyngodonidae) from E. nigra and E. sa- We thank Murray D. Dailey (Marine moensis and Cylindrotaenia decidua (Cestoda: Mammal Center, Sausalito, California) for Helminth Records from Emoia Species from Oceania . Goldberg et al. 613 the nematode samples from the Kingdom of nigra and Emoia samoense (Sauria: Scinci- Tonga. dae), from Samoa. J. Helminthol. Soc. 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