NEW GENUS, NEW SPECIES OF CESTODA (ANOPLOCEPHALIDAE ...

J. Parasitol., 91(4), 2005, pp. 882–889 q American Society of Parasitologists 2005

NEW GENUS, NEW SPECIES OF CESTODA (ANOPLOCEPHALIDAE), NEW SPECIES OF NEMATODA (COSMOCERCIDAE) AND OTHER HELMINTHS IN CYRTODACTYLUS LOUISIADENSIS (SAURIA: GEKKONIDAE) FROM PAPUA NEW GUINEA Charles R. Bursey, Stephen R. Goldberg*, and Fred Kraus† Department of Biology, Pennsylvania State University, Shenango Campus, Sharon, Pennsylvania 16146. e-mail: [email protected] ABSTRACT:

Gekkotaenia novaeguineaensis n. gen., n. sp. (Cestoda: Anoplocephalidae) from the small intestine and Cosmocerca zugi n. sp. (Nematoda: Cosmocercidae) from the large intestine of the ring-tailed gecko, Cyrtodactylus louisiadensis (Sauria: Gekkonidae) are described and illustrated. Gekkotaenia novaeguineaensis n. gen., n. sp. is unique among the acraspedote Linstowiinae in possessing a poral female reproductory system. Cosmocerca zugi n. sp. is the 22nd species to be assigned to the genus and differs from other species in the genus by possessing 4 pairs of rosette papillae on plectanes and having a gubernaculum longer than the spicules. It is the fifth species to be described from the Australian biogeographical region. Eight additional helminth species were found: the digenean, Allopharynx macallisteri; 2 cestodes, cysticercoids of Cyclophyllidea gen. sp. and tetrathyridia of Mesocestoides sp.; 5 nematodes, larvae in cysts of Abbreviata sp., Aplectana macintoshii, Oswaldocruzia bakeri, Parapharyngodon maplestonei, and an undescribed species of Physalopteroides. Cyrtodactylus louisiadensis represents a new host record for each of these helminths.

During a helminthological examination of 7 ring-tailed geckos Cyrtodactylus louisiadensis (de Vis, 1892) from Papua New Guinea, all were found to harbor helminth parasites. Three harbored 9 cestodes not assignable to any known genus and 4 harbored 11 (4 male, 7 female) nematodes of an undescribed species of Cosmocerca Diesing, 1861. Cyrtodactylus louisiadensis occurs in Papua New Guinea and surrounding islands, the Solomon Islands, and northeastern Queensland, Australia (Bauer, 1994). To our knowledge, there are no reports of helminths from C. louisiadensis. Currently 12 genera are assigned to the Linstowiinae, species of which infect reptiles or mammals (Beveridge, 1994), and 21 species are assigned to Cosmocerca, 11 from the Neotropical biogeographical region, 5 from the Palaearctic region, 4 from the Australian region, and 1 from the Oriental region (Table I). The purpose of this paper is to describe a new genus and 2 new species of helminths.

sey, 1998; 3 species of Cestoda represented by tetrathyridia of Mesocestoides sp., cysticercoids of a cyclophyllidean species, and Gekkotaenia novaeguineaensis n. gen. n. sp.; 5 species of Nematoda, Aplectana macintoshii (Stewart, 1914), Cosmocerca zugi n. sp., Oswaldocruzia bakeri Moravec and Sey, 1986, Parapharyngodon maplestonei Chatterji, 1933, and Physalopteroides sp. Prevalence, mean intensity, range of infection, and museum accession numbers for these helminths are given in Table II. DESCRIPTION

Gekkotaenia n. gen.

MATERIALS AND METHODS Seven Cyrtodactylus louisiadensis were collected by hand by FK, Milne Bay Province, Papua New Guinea, 6 from Misima Island (108409S, 1528419E, 11–16 January 2003) and 1 from Normanby Island (108029S, 1508599E) and fixed in neutral buffered 10% formalin. The body cavity was opened by a longitudinal lateral incision and the gastrointestinal tract was removed by cutting across the esophagus and rectum. The esophagus, stomach, small intestine, and large intestine of each gecko were examined separately for parasites. Nematodes were placed in glycerol, allowed to clear, and examined under a light microscope; cestodes were regressively stained in Delafield’s hematoxylin, dehydrated in graded alcohols, cleared in xylene, and mounted in balsam for examination. Drawings were made with the aid of a microprojector. Measurements are given in micrometers (unless otherwise stated) as mean and 1 SD, with range in parentheses. Lizards were deposited in the Bernice P. Bishop Museum (BPBM), Honolulu, Hawaii, as BPBM 16860–16866.

RESULTS All 7 geckos were found to harbor helminths: 1 species of Digenea, Allopharynx macallisteri Dailey, Goldberg and BurReceived 18 June 2004; revised 10 November 2004; accepted 10 November 2004. * Department of Biology, Whittier College, Whittier, California 90608. † Bishop Museum, Department of Natural Sciences, 1525 Bernice Street, Honolulu, Hawaii 96817. 882

Diagnosis: Strobila small, acraspedote; mature proglottids longer than wide. Scolex with 4 acetabula, rostellum lacking. Genitalia single, genital pores alternate irregularly, genital ducts lie between osmoregulatory canals. Seminal vesicle absent. Vagina posterior to cirrus sac. Ovary and vitellarium compact, poral. Testes mostly aporal, lateral and posterior to ovary and vitellarium. Uterus ephemeral, forming uterine capsules, each with a single egg. Oncospheres oval.

Gekkotaenia novaeguineaensis n. sp. (Figs. 1–4) Description (based on 4 complete and 5 incomplete specimens): Cestodes of small size, flattened dorsoventrally; strobila acraspedote. Total length 53.8 6 4.8 mm (50–60 mm; unrelaxed strobila, N 5 4); maximum width of strobila 1.1 6 0.1 mm (0.9–1.3 mm; unrelaxed, N 5 9); neck 4.48 6 0.78 mm (3.84–5.76; N 5 6); proglottid number in complete strobila 227 6 38 (179–273; N 5 4). Following measurements from selected relaxed proglottids: immature proglottids wider than long 826 6 64 3 93 6 24 (768–960 3 64–128; N 5 10), mature proglottids wider than long 739 6 85 3 275 6 38 (640–896 3 224–320; N 5 10); gravid proglottids mostly isodiametric 691 6 73 3 711 6 183 (576–800 wide 3 512–1152 long; N 5 10); terminal proglottids longer than wide 1712 6 486 3 525 6 61 (1152–2560 long 3 480–640 wide; N 5 6). Scolex (N 5 7) 137 6 22 (110–171) wide by 120 6 20 (100–140) long, with four oval suckers, 97 6 9 (85–110) 3 70 6 11 (61–92), long axes parallel to that of cestode. Protonephridial system of 4

Palaearctic C. banyulensis Chabaud and Campana Rouget, 1955 C. commuta (Diesing, 1851) 5 C. pulcherrima Ivanitzky, 1940 5 C. skrjabini Ivanitzky, 1940 5 C. kashmirensis Fotedae, 1959 5 C. timofejovoi Skarbilovitch, 1950 C. longitcaudata (Linstow, 1885) 5 C. trispinosa Railliet and Henry, 1916 C. japonica Yamaguti, 1938 C. ornata (Dujardin, 1845) 5 C. indica Nama and Khichi, 1973 5 C. macrogubernaculum Rao, 1979 5 C. miniscula Travassos, 1931 5 Cosmocercella polissensis Maguza, 1972 5 Paracosmocerca mucronata Kung and Wu, 1945 5 Paracosmocerca spinocerca Rao, 1979

Oriental C. ishaqi (Islam, Farooq and Khanum, 1981)

C. paraguayensis Moravec and Kaiser, 1994 5 C. ornata sensu Baker and Vaucher, 1984 C. parva Travassos, 1925 5 C. freitasi Silva, 1954 C. podicipinus Baker and Vaucher, 1984 5 C. panamaensis Martinez and Maggenti, 1989 C. rara Freitas and Vicente, 1966 C. travassosi Rodrigues and Fabio, 1970 C. uruguayensis Lent and Freitas, 1948 C. vrcibradici Bursey and Goldberg, 2004

Neotropical C. brasiliense Travassos, 1925 C. chilensis Lent and Frietas, 1948 C. cruzi Rodrigues and Fabio, 1970 C. longispicula Moravec and Kaiser, 1994

Australian C. archeyi Baker and Green, 1988 C. australis Baker and Green, 1988 C. limnodynastes Johnston and Simpson, 1942 C. novaeguineae Moravec and Sey, 1990 C. zugi n. sp.

Biogeographical region Cosmocerca sp.

200 167 155 177

Toad Frog Toad Lizard

Frog Frog

Salamander

Frog Toad

104 rudimentary

92

10 180

100

94

Frog

Toad

90–110

83–108

170 80 74 300

95 99–123 50–75 60 79–116

Spicule length (mm)

Frog

Toad Toad Frog Frog Frog

Frog Frog Frog Frog Lizard

Type host

TABLE I. Selected characteristics of male individuals of species of Cosmocerca.

84 110–120

190

80 186–213

absent

206 130 133 95

134

85–108

106–122

145 84 85 138

87 82–88 110 111 92–122

Gubernaculum length (mm)

5 5

6

5–6 7

11

6 5 7 7

5

5–7

4–5

8–11 6 5 7

4 3–4 4 5 4

Plectane number pairs

Yamaguti, 1938 Skrjabin et al., 1961

Skrjabin et al., 1961

Chaubaud and Campana-Rouget, 1955 Moravec and Vojtkova´, 1974

Islam et al. 1979

Freitas and Vicente, 1966 Rodrigues and Fabio, 1970b Lent and Freitas, 1948 Bursey and Goldberg, 2004b

Baker and Vaucher, 1984

Mordeglia and Digiani (1998)

Baker and Vaucher (1984)

Dyer and Altig (1976) Lent and Freitas (1948) Rodrigues and Fabio (1970a) Moravec and Kaiser (1994)

Baker and Green (1988) Baker and Green (1988) Johnston and Simpson (1942) Moravec and Sey (1990) This article

Reference

BURSEY ET AL.—TWO NEW HELMINTH SPECIES 883

884

THE JOURNAL OF PARASITOLOGY, VOL. 91, NO. 4, AUGUST 2005

TABLE II. Site of infection, number of helminths, prevalence, mean intensity, and range of infection for 10 helminth species in Cyrtodactylus louisiadensis. Prevalence

Site of infection

Number

(%)

Trematoda Allopharynx macallisteri

Small intestine

4

14

Cestoda Cyclophyllidea gen. sp. (cystciercoids) Mesocestoides sp. (tetrathyridia) Gekkotaenia novaequineaensis n. sp.

Coelom Coelom Small intestine

44 4 9

28 14 43

Nematoda Abbreviata sp. (larvae in cysts) Aplectana macintoshii Cosmocerca zugi n. sp. Oswaldocruzia bakeri Parapharyngodon maplestonei Physalopteroides sp. (immature female)

Coelom Large intestine Large intestine Large intestine Large intestine Large intestine

33 92 11 2 22 1

57 86 57 14 86 14

8.3 15.3 2.8 2 3.7 1

Helminth species

longitudinal ducts visible throughout length of strobila. Genital pores irregularly alternating, situated in anterior quarter of proglottid. Remaining measurements, N 5 10. Cirrus sac length 81 6 6 (73–91), width 34 6 3 (30–37); vagina opening into genital atrium posterior to cirrus sac, extending posteriolaterally to Mehlis’ gland. Vas deferens and vagina pass between osmoregulatory ducts. Ovary bilobed, in poral half of proglottid; each lobe subdivided into numerous secondary lobules; ovary width 114 6 13 (92–134), length 46 6 7 (37–55); ovoid vitelline gland situated behind ovary, 49 6 7 3 64 6 7 (37–58 3 49–73); ootype and Mehlis’ gland complex between ovary and vitelline gland. Testes number 18–26 in each proglottid, oval in shape 32 6 4 3 22 6 5 (24–37 3 16–31) and lying posterior and primarily aporal to ovary; 2–4 poral to vitelline gland and remainder aporal to vitelline gland. Uterus ephemeral, uterine capsules 52 6 7 (43–64) in diameter, each containing a single egg, fill entire proglottid; egg oval in shape 41 6 3 3 22 6 3 (34–43 3 18–27); oncosphere oval in shape 35 6 3 3 17 6 2 (31–37 3 15–20); oncosphere hook 11 6 1 (10–12) in length. Vagina, vas deferens, and cirrus pouch are visible in gravid proglottids. On average, 200–225 ova in terminal proglottid, eggs not occurring lateral of excretory ducts.

Mean intensity 6 SD

4

Accession number Range

USNPC

—

95174

22.0 6 19.8 4 3.0 6 1.0

8–36 — 2–4

95175 95176

6 13.2 6 10.1 6 1.3

1–28 1–29 1–4 — 1–11 —

95177 95178

6 3.7

BPBM

— F221 F224 See text

H94 H92 See text 95179 H95 95180 H93 95181 —

Remarks The presence of a scolex with 4 acetabulate suckers and a compact vitellarium posterior to the ovary allows the assignment of the new species to the Cyclophyllidea Van Beneden in Braun, 1900. The presence of marginal genital pores, absence of rostellum, and an ephemeral uterus replaced by uterine capsules containing a single egg allows placement in the Linstowiinae Fuhrmann, 1907, of the Anoplocephalidae Cholodkovsky, 1902. The new genus is most similar to the Oochoristica Lu¨he, 1898, differing in the placement of ovary and vitellarium (poral vs. central), location of testes (primarily aporal to vitellarium vs. posterior to vitellarium), and shape of oncospheres (oval vs. spherical). It should be noted that, in illustrations of the type species of Oochoristica, O. tuberculata (Rudolphi, 1819), the ovary is on the poral side of the midline (see Beveridge, 1994); however, one character in Beveridge’s (1994) key for the separation of Oochoristica from the other genera of the Anoplocephalidae is ‘‘testes posterior to vitellarium.’’ DESCRIPTION

Cosmocerca zugi n. sp. (Figs. 5–13)

Taxonomic summary Type host: Cyrtodactylus louisiadensis (de Vis, 1892), ringtailed gecko; symbiotype, BPBM 16862; collection date, 13 January 2003. Type locality: Misima Island, Milne Bay Province, Papua New Guinea (108409S, 1528419E). Site of infection: Small intestine. Prevalence: Three (43%) of 7 geckos were infected. Mean intensity: 3.0 6 1.0 (2–4). Type specimens: Holotype, U.S. National Parasite Collection (USNPC) 95169; paratypes, USNPC 95170; voucher specimens, BPBM F222, BPBM F223. Etymology: The new genus is named for its host; the new species is named for the country of collection.

General: Small, stout nematodes. Prominent sexual dimorphism, males one-half length of females. Lateral alae present in both males and females. Cuticle transversely striated. Mouth with 3 small V-shaped lips, dorsal lip with 2 sessile papillae, each ventrolateral lip with 1 ventral sessile papilla, 1 lateral amphid. Esophagus with indistinct buccal cavity, short pharynx, cylindrical corpus and posterior bulb containing valves. Excretory pore anterior to esophageal bulb. Male: Based on 4 mature specimens. Length 1.72 6 0.09 mm (1.63–1.84 mm), width at midbody 154 6 11 (140–166). Pharynx 17 6 2 (15–18) long, esophageal corpus 282 6 14 (265–299) long, esophageal bulb 60 6 5 (55–67) long, 61 6 6 (52–67) wide. Nerve ring 92 6 10 (79–104) and excretory pore 294 6 25 (262–323) from anterior end, respectively. Lateral

BURSEY ET AL.—TWO NEW HELMINTH SPECIES

FIGURES 1–4.

885

Gekkotaenia novaeguineaensis n. gen., n. sp. 1. Scolex. 2. Mature proglottid. 3. Egg. 4. Terminal proglottid.

alae beginning at level of nerve ring and terminating at level of fourth plectane. Four rows of somatic papillae, 2 dorsolateral in position, 2 ventrolateral, becoming more pronounced posteriorly. Tail flexed ventrally, 166 6 13 (153–183) in length. Gu-

bernaculum tridentate, central arm more massive, 104 6 13 (92–122) long, heavily sclerotized, distal end sharply pointed. Spicules equal 96 6 15 (79–116), lightly sclerotized. In addition to somatic papillae, 1 median precloacal papilla and 15

886



pairs of caudal papillae: 9 pairs precloacal, anterior-most 2 pairs simple, followed by 4 pairs of rosette papillae containing 12 digitiform projections on plectanes, 1 pair rosette papillae, 2 pairs simple papillae; 6 pairs postcloacal, 4 pairs ventral in position, first pair rosette, 1 pair lateral, terminal pair dorsolateral in location. Female: Based on 7 gravid specimens. Length 3.126 0.14 (2.94–3.33), width 298 6 29 (262–336) at level of esophagointestinal junction. Pharynx 21 6 3 (18–24) long, esophageal corpus 393 6 27 (354–421) long, esophageal bulb 94 6 7 (85– 104) long, 106 6 15 (85–122) wide. Nerve ring 204 6 20 (183– 232), excretory pore 364 6 19 (342–390), and slightly salient vulva 1.72 6 0.13 mm (1.60–1.98 mm) from anterior end, respectively. Lateral alae beginning at level of nerve ring and terminating at base of tail. Tail straight, 394 6 41 (357–459) long, including flexible awl-shaped terminal process. Vagina directed anterodorsally then posteriorly; uteri prodelphic. Eggs 82 6 4 (76–88) long; 57 6 5 (49–61) wide; thin shelled and in all stages of development. Hatched larvae present in uterus, apparently no eggs released to environment. Taxonomic summary Type host: Cyrtodactylus louisiadensis (de Vis, 1892), ringtailed gecko; symbiotype, BPBM 16860; collection date, 11 January 2003. Type locality: Misima Island, Milne Bay Province, Papua New Guinea (108409S, 1528419E). Site of infection: Large intestine. Prevalence: Four (57%) of 7 geckos were infected. Mean intensity: 2.8 6 1.3 (1–4). Type specimens: Holotype male, U.S. National Parasite Collection: USNPC 95171; allotype female, USNPC 95172; paratypes, USNPC 95173. Etymology: The new species is named for George R. Zug, Division of Amphibians and Reptiles, Smithsonian Institution, Washington, D.C., for his contributions to the herpetology of Oceania. Remarks Cosmocerca zugi is the fifth species from the Australian biogeographical region to be assigned to the genus. With the exception of the recently described Cosmocerca vrcibradici, all species of Cosmocerca are parasites of anurans. Although Baker (1987) reported Cosmocerca ornata (Dujardin, 1845), a common parasite of European frogs, from 2 reptile hosts, namely, the slowworm, Anguis fragilis, and the grass snake, Natrix natrix, neither A. fragilis nor N. natrix is considered to be a definitive host of C. ornata. Records for A. fragilis are apparently based on misidentifications of the somewhat similar Oxysomatium brevicaudatum (Zeder, 1800) and are not included in recent host lists by Lewin (1990). Natrix natrix serves only as a facultative host for C. ornata, i.e., it acquires C. ornata by feeding on infected frogs (Bozkov, 1975). Cosmocerca zugi is

887

the second species of Cosmocerca reported to have a reptilian definitive host. Cosmocerca zugi is easily separated from the other Australian species (Table I). Rosettes of Cosmocerca archeyi and Cosmocerca australis are formed from 2 concentric circles of punctations, that of Cosmocerca limnodynastes is formed from single circle of punctations, Cosmocerca novaeguineaensis has posteriorly directed plectanes surrounded by semicircles of punctations, and C. zugi has 2 parallel rows of digitiform punctations at the terminus of a plectane. DISCUSSION With the exception of G. novaeguineaensis and Cosmocerca zugi, none of the parasites found in this study was unique to C. louisiadensis. However, C. louisiadensis is a newly recognized host for each of the parasite species reported here. Allopharynx macallisteri was originally described from specimens removed from the small intestines of Lepidodactylus lugubris collected from central Guam (Dailey et al., 1998). It was reported from the same host collected from Guam and Rota by Goldberg et al. (1998). Cyrtodactylus louisiadensis represents the second host record and Papua New Guinea is a new locality for A. macallisteri. The strobilar stage of species assigned to Cyclophyllidea occur in amphibians, reptiles, birds, and mammals (Jones et al., 1994). To our knowledge, cysticercoids have not previously been reported from the coelom of lizards from the Australian biogeographical region, but they are known from African lizards (Goldberg 2002a, 2002b). It is not known whether the cysticercoids found in this study represent an accidental infection or if C. louisiadensis is a paratenic host. The strobilar stage of species of Mesocestoides occur in mammals; tetrathyridia are frequently found in amphibians and reptiles (Rausch, 1994). Goldberg et al. (2004) summarized world occurrences. To that list should be added Callulops humicola from Papua New Guinea (Moravec, 1990) and Platymantis pelewensis (Bursey and Goldberg, 2004a). Attempts to elucidate the life cycle of Mesocestoides have proven unsuccessful; however, a second intermediate, but yet unknown, host may be necessary to complete the life cycle (Padgett and Boyce, 2004). Aplectana macintoshii originally described by Stewart (1914) from Rana tigerina (currently Hoplobatrachus tigerinus) and Bufo stomaticus from India is the most cosmopolitan species of Aplectana and occurs in Africa, China, Europe, Japan, India, South America, and Malaysia, where it is known from 37 species of frogs and toads, 3 species of lizards, and 1 species of snake (Baker, 1987; Goldberg et al., 1993). Cyrtodactylus louisiadensis represents the fourth lizard species reported as host for A. macintoshii; Papua New Guinea is a new locality. Oswaldocruzia bakeri was originally described from specimens taken from Phrynomantis stictogaster (currently, Callulops stictogaster) collected in the Eastern Highlands Province of Papua New Guinea (Moravec and Sey, 1986). It is also known from Cal-

← FIGURES 5–13. Cosmocerca zugi n. sp. 5. Female, entire, lateral view. 6. Female, en face view. 7. First plectane, lateral view. 8. Larvated egg. 9. First plectane, ventral view. 10. Male, entire, lateral view. 11. Gubernaculum and spicule, lateral view. 12. Male, posterior end, lateral view. 13. Male, posterior end ventral view. Scale bar values are given in micrometers.

888


lulops humicola and Phrynomantis wilhelmana from Papua New Guinea (Moravec, 1990). Cyrtodactylus louisiadensis represents a new host record and is the first lizard species reported as a host for Oswaldocruzia bakeri. Parapharyngodon maplestonei was originally described from specimens taken from the intestine of the common Burmese lizard, Calotes versicolor, collected in Rangoon, Burma (Chatterji, 1933). It has also been reported in Calotes cristatellus, Hemidactylus flavoviridis, Hemidactylus frenatus, Ophisaurus apodus, and Sphenomorphus emigrans (Baker, 1987). Papua New Guinea is a new locality. Encysted larvae assigned to Abbreviata and Physaloptera as well as encysted larvae assigned to Physalopteridae have been reported from Australian gekkonids: Christinus marmoratus, Diplodactylus ciliaris, Diplodactylus conspicillatus, Diplodactylus elderi, Diplodactylus stenodactylus, Diplodactylus strophurus, Gehyra variegata, Nephrurus laevissimus, Nephrurus levis, Oedura robusta, Rhynchoedura ornata (Jones, 1992, 1995a, 1995b; Bursey and Goldberg, 1999). Mature individuals of 15 species of Abbreviata have been found in Australian reptiles (Pichelin et al., 1999). Roca (1993) suggested that prevalence of encysted larval nematodes in a lizard population indicates their degree of importance as prey because lizards can serve as intermediate hosts. Species of Abbreviata require an insect intermediate host (Anderson, 2000). The immature female specimen of Physalopteroides apparently represents a new species. The dental pattern is unique, 3 central teeth on the right lip, 2 truncate lateral teeth on the left lip, when compared with other species assigned to the genus. Its description must await the collection of mature specimens. ACKNOWLEDGMENTS We thank Peggy Firth for the preparation of the illustrations constituting Figures 1–13; Ezra Theodoro and Amanda Woolsey for dissection assistance; David Mitchell and Conservation International for logistical and field assistance; the Papua New Guinea (PNG) National Museum and Art Gallery for providing in-country collaborative assistance; and the PNG Department of Environment and Conservation, PNG National Research Institute, and Milne Bay Provincial Government for permission to work in Milne Bay Province. This research was supported by National Science Foundation grant DEB 0103794.

LITERATURE CITED ANDERSON, R. C. 2000. Nematode parasites of vertebrates: Their development and transmission. CABI Publishing, Wallingford, U.K., 650 p. BAKER, M. R. 1987. Synopsis of the Nematoda parasitic in amphibians and reptiles. Memorial University of Newfoundland Occasional Papers in Biology 11: 1–325. ———, AND D. M. GREEN. 1988. Helminth parasites of native frogs (Leiopelmatidae) from New Zealand. Canadian Journal of Zoology 66: 707–713. ———, AND C. VAUCHER. 1984. Parasitic helminths from Paraguay VI: Cosmocerca Diesing, 1861 (Nematoda: Cosmocercoidea) from frogs. Revue Suisse de Zoologie 91: 925–934. BAUER, A. M. 1994. Familia Gekkonidae (Reptilia, Sauria), Part I. Australia and Oceania. Walter de Gruyter, Berlin, Germany, 306 p. BEVERIDGE, I. 1994. Family Anoplocephalidae Cholodkovsky, 1902. In L. F. Khalil, A. Jones, and R. A. Bray (eds.). Keys to the cestode parasites of vertebrates, CAB International, Wallingford, Oxon, U.K., p. 315–366. BOZKOV, D. 1975. Invasion paths of post cyclic hosts by sexually mature helminths. Scripta Facultatis Scientiarum Naturalium Universitatis Purkynianae Brunensis 5: 77–80. BURSEY, C. R., AND S. R. GOLDBERG. 1999. Skrjabinodon piankai sp. n.

(Nematoda: Pharyngodonidae) and other helminths of geckos (Sauria: Gekkonidae: Nephrurus spp.) from Australia. Journal of the Helminthological Society of Washington 66: 175–179. ——— AND ———. 2004a. A new species of Spinicauda (Nematoda: Heterakidae) and other endoparasites in Platymantis pelewensis (Anura: Ranidae) from the Palau Islands, Republic of Belau, Oceanica. Journal of Parasitology (in press). ——— AND ———. 2004b. Cosmocerca vrcibradici n. sp. (Ascaridida: Cosmocercidae), Oswaldocruzia vitti n. sp. (Strongylida: Molineidae), and other helminths from Prionodactylus eigenmanni and Prionodactylus oshaughnessyi (Sauria: Gymnophthalmidae) from Brazil and Ecuador. Journal of Parasitology 90: 140–145. CHABAUD, A.-G., AND Y. CAMPANA-ROUGET. 1955. He´lminthes de la re´gion de Banyule I. Ne´matodes parasites d’amphibiens. Vie et Milieu 6: 83–92. CHATTERJI, R. C. 1933. On a new nematode, Parapharyngodon maplestonei gen. nov., sp. nov., from a Burmese lizard. Annals of Tropical Medicine and Parasitology 27: 131–134. DAILEY, M. D., S. R. GOLDBERG, AND C. R. BURSEY. 1998. Allopharynx macallisteri sp. n. (Trematoda: Plagiorchiidae) from the mourning gecko, Lepidodactylus lugubris, from Guam, Mariana Islands, Micronesia, with a key to the species of the genus Allopharynx. Journal of the Helminthological Society of Washington 65: 16–20. DYER, W. G., AND R. ALTIG. 1976. Redescription of Cosmocerca brasiliensis Travassos 1925 (Nematoda: Cosmocercidae) from Ecuadorian frogs. Journal of Parasitology 62: 262–264. FREITAS, J. F. T., AND J. J. VICENTE. 1966. Noˆvo nemato´deo do geˆnero Cosmocerca Diesing, 1861, parasito de anfisbaendeo. Atas Sociedade de Biologia do Rio de Janeiro 10: 109–111. GOLDBERG, S. R., AND C. R. BURSEY. 2002a. Helminths of four species of gekkonid lizards from southern Africa. African Zoology 37: 43– 46. ———, AND ———. 2002b. Helminths of seven species of lacertid lizards from southern Africa. African Zoology 37: 159–164. ———, ———, AND H. CHEAM. 1998. Gastrointestinal helminths of four gekkonid lizards, Gehyra mutilata, Gehyra oceanica, Hemidactylus frenatus and Lepidodactylus lugubris from the Mariana Islands, Micronesia. Journal of Parasitology 84: 1295–1298. ———, ———, AND R. TAWIL. 1993. Aplectana macintoshii (Nematoda: Cosmocercidae) in Eumeces latiscutatus (Sauria: Scincidae), from Japan. Journal of the Helminthological Society of Washington 60: 283–284. ———, ———, AND S. R. TELFORD, JR. 2004. Helminths of six species of snakes from Honshu Island, Japan. Comparative Parasitology 71: 49–60. ISLAM, A., M. FAROOQ, AND Z. KHANUM. 1979. Two new genera of nematode parasites (Oxyuridae: Oxysomatiinae) from toad Bufo andersoni of Pakistan. Pakistan Journal of Zoology 11: 69–73. JOHNSTON, T. H., AND E. R. SIMPSON. 1942. Some nematodes from Australian frogs. Transactions of the Royal Society of South Australia 66: 172–179. JONES, A., R. A. BRAY, AND L. F. KHALIL. 1994. Order Cyclophyllidea van Beneden in Braun, 1900. In L. F. Khalil, A. Jones, and R. A. Bray (eds.). Keys to the cestode parasites of vertebrates. CAB International, Wallingford, Oxon, U.K., p. 305–307. JONES, H. I. 1992. Gastrointestinal nematodes in the lizard genera Tiliqua and Cyclodomorphus (Scincidae) in Western Australia. Australian Journal of Zoology 40: 115–126. ———. 1995a. Gastric nematode communities in lizards from the Great Victoria Desert, and an hypothesis for their evolution. Australian Journal of Zoology 43: 141–164. ———. 1995b. Pathology associated with physalopterid larvae (Nematoda: Spirurida) in the gastric tissues of Australian reptiles. Journal of Wildlife Diseases 31: 299–306. LENT, H. AND J. F. T. FREITAS. 1948. Uma coleçaõ de Nemato´deos, parasitos de vertebrados, do Museu de Historia Natural de Montevideo. Memo´rias do Instituto Oswaldo Cruz 46: 1–71. LEWIN, J. 1990. Parasitic worms in a slowworm (Anguis fragilis L.) population from the Bieszczady Mountains (Poland). Acta Parasitologica Polonica 35: 207–215. MORAVEC, F. 1990. Additional records of nematode parasites from Papua New Guinea amphibians with a list of recorded endohelminths by amphibian hosts. Folia Parasitologica 37: 43–58.


———, AND H. KAISER. 1994. Description of Cosmocerca longispicula sp. nov. (Nematoda: Cosmocercidae), a parasite of a dendrobatid frog from Martinique, French Antilles. Parasitology Research 80: 29–32 ———, AND O. SEY. 1986. Three new nematode species from Phrynomantis spp. (Amphibia: Microhylidae) from Papua New Guinea. Folia Parasitologica 33: 343–351. ———, AND ———. 1990. Some nematode parasites of frogs from Papua New Guinea and Australia. Acta Societatis Zoologicae Bohemslovacae 54: 268–286. ———, AND L. VOJTKOVA´. 1974. Zur kenntnis der nematoden der gattung Cosmocerca Diesing, 1861 in den amphibien der CSSR. Folia Facultatis Scientiarum Naturalium Universitatis Purkynianae Brunensis 15: 53–66. MORDEGLIA, C., AND M. C. DIGIANI. 1998. Cosmocerca parva Travassos, 1925 (Nematoda: Cosmocercidae) in toads from Argentina. Memo´rias do Instituto Oswaldo Cruz 93: 737–738. PADGETT, K. A., AND W. M. BOYCE. 2004. Life-history studies on two molecular strains of Mesocestoides (Cestoda: Mesocestoididae): Identification of sylvatic hosts and infectivity of immature life stages. Journal of Parasitology 90: 108–113. PICHELIN, S., P. M. THOMAS, AND M. N. HUTCHINSON. 1999. A checklist of helminth parasites of Australian reptiles. Records of the South Australian Museum Monograph Series No. 5, Adelaide, South Australia, 61 p.

889

RAUSCH, R. L. 1994. Family Mesocestoididae Fuhrmann, 1907. In L. F. Khalil, A. Jones, and R. A. Bray (eds.). Keys to the cestode parasites of vertebrates. CAB International, Wallingford, Oxon, U.K., p. 309–314 ROCA, V. 1993. Methods and aims in parasitology of Mediterranean reptiles, mainly lizards. In E. D. Valakos, W. Bo¨hme, V. Pe´rezMellado, P. Maragou (eds.). Lacertids of the Mediterranean Region, a biological approach. Hellenic Zoological Society, Athens, Greece, p. 253–262. RODRIGUES, H. O., AND S. P. FABIO. 1970a. Nova espećie do geńero Cosmocerca Diesing, 1861 (Nematoda, Oxyuroidea). Atas da Sociedade de Biologia do Rio de Janeiro 13: 179–180. ———, AND ———. 1970b. Contribuiçaõ ao estudo do geˆnero Cosmocerca Diesing, 1861 (Nematoda, Oxyuroidea). Atas da Sociedade de Biologia do Rio de Janeiro 14: 5–6. SKRJABIN, K. I., N. P. SHIKHOBALOVA, AND E. A. LAGODOVSKAYA. 1961. Oxyurata of animals and man. Part Two. Translated from Russian, Israel Program for Scientific Translations, Jerusalem, Israel, 1974, 460 p. STEWART, F. H. 1914. Studies in Indian helminthology, No. I. Records of the Indian Museum. 10: 165–193. YAMAGUTI, S. 1938. Studies on the helminth fauna of Japan Part 23. Two new species of amphibian nematodes. Japanese Journal of Zoology 7: 603–607.