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NEW SPECIES OF ALLOPHARYNX (DIGENEA: PLAGIORCHIIDAE) ANDOTHER HELMINTHS IN URANOSCODON SUPERCILIOSUS (SQUAMATA:TROPIDURIDAE) FROM AMAZONIAN BRAZILAuthor(s): Charles R. Bursey, Stephen R. Goldberg, Laurie J. VittSource: Journal of Parasitology, 91(6):1395-1398. 2005.Published By: American Society of ParasitologistsDOI: http://dx.doi.org/10.1645/GE-3478.1URL: http://www.bioone.org/doi/full/10.1645/GE-3478.1

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1395

J. Parasitol., 91(6), 2005, pp. 1395–1398q American Society of Parasitologists 2005

NEW SPECIES OF ALLOPHARYNX (DIGENEA: PLAGIORCHIIDAE) AND OTHERHELMINTHS IN URANOSCODON SUPERCILIOSUS (SQUAMATA: TROPIDURIDAE)FROM AMAZONIAN BRAZIL

Charles R. Bursey, Stephen R. Goldberg*, and Laurie J. Vitt†Department of Biology, Pennsylvania State University, Shenango Campus, Sharon, Pennsylvania 16146. e-mail: cxb13@psu.edu

ABSTRACT: Allopharynx daileyi n. sp. (Digenea: Plagiorchiidae) from the small intestine of the tropidurid lizard Uranoscodonsuperciliosus from Amazonian Brazil is described and illustrated. Of the 11 currently recognized species of Allopharynx, weconsider Allopharynx megorchis Simha, 1961 a synonym of Allopharynx mehrai (Gogate, 1935) Price 1938 and Allopharynxpuertoricensis Acholonu, 1976 a synonym of Allopharynx riopedrensis Garcia-Diaz; thus, A. daileyi becomes the 10th speciesassigned to the genus. The trematode species Mesocoelium monas and 2 species of Nematoda, Africana chabaudi and Cosmocercavrcibradici, were also present.

Thirty-five Uranoscodon superciliosus (Linnaeus, 1758)were collected between July 1993 and April 1998 in Para, Ron-donia, or Roraima states, Brazil by 1 of us (L.J.V.), used in alife history study, and subsequently deposited in the herpetol-ogy collection of the Sam Noble Oklahoma Museum of NaturalHistory (OMNH). The specimens were originally fixed in 10%formalin and stored in 70% ethanol. Twenty-five lizards wereborrowed from OMNH, examined for helminths, and found toharbor an undescribed trematode species as well as 1 othertrematode species and 2 nematode species.

Uranoscodon superciliosus (Tropiduridae) occurs in northernSouth America east of the Andes (Avila-Pires, 1995). It is anarboreal lizard, living in vegetation along streams, rivers, andmarshes and feeding largely on insects and other invertebrateswashed up on shores or deposited in rift piles just above thewater line (Howland et al., 1990). It is the sister taxon to allother tropidurids (Frost, 1992). To our knowledge, 1 report ofhelminths in U. supercilious exists, i.e., Baker (1981) describedAfricana chabaudi in specimens collected in Belem, Para, Bra-zil. The purpose of this paper is to describe a new trematodespecies and to list helminth species known to infect U. super-ciliosus.

MATERIALS AND METHODS

Twenty-five lizards were borrowed from OMNH (10 male, 15 female,mean snout–vent length 5 104 mm 6 35 mm, range 48–168 mm;OMNH 36544, 36545, 36551–36558, 36631, 36636, 36638, 37182,37506–37520) and examined for helminths. The abdominal cavity ofeach lizard had been opened and the stomach previously removed. Forthis study, the intestines were removed, opened longitudinally, andsearched for helminths using a dissecting microscope. The coelom wasalso searched. Each helminth was cleared in glycerol on a glass slideand nematodes were identified from these preparations with a light mi-croscope. Selected trematodes were rinsed in distilled water, regressive-ly stained in Delafield’s hematoxylin, dehydrated in a series of gradedethanol, and mounted in Canada balsam. Illustrations were made withthe aid of a microprojector. Measurements were taken from 8 gravidspecimens and are given in micrometers (mm) unless otherwise indi-cated as holotype measurements with mean and range in parentheses.

Received 25 August 2004; revised 1 February 2005; 12 April 2005;accepted 12 April 2005.

* Department of Biology, Whittier College, Whittier, California 90608.† Curator of Reptiles, Division of Herpetology, Sam Noble Oklahoma

Museum of Natural History, and Zoology Department, University ofOklahoma, Norman, Oklahoma 73072.

RESULTS

Two species of Digenea, comprising a new species of Allo-pharynx (Strom, 1928) and Mesocoelium monas (Rudolphi,1819), and 2 species of Nematoda, Africana chabaudi Baker,1981 and Cosmocerca vrcibradici Bursey and Goldberg, 2004,were found. Eleven of 25 (44%) lizards were infected. Preva-lence, mean intensity, and range for these helminth species aregiven in Table I. Selected helminths were deposited in the U.S.National Parasite Collection (USNPC), Beltsville, Maryland:Allopharynx daileyi, USNPC 95013–95016, 95018; Mesocoe-lium monas, USNPC 95017; Africana chabaudi, USNPC95019, Cosmocerca vrcibradici, USNPC 95020. A descriptionof the new species follows.

DESCRIPTION

Allopharynx daileyi n. sp.(Figs. 1–4)

General: Based upon holotype and 7 paratypes. Plagiorchiidae (Luhe,1901) Ward, 1917; Astriotrematinae Baer, 1924. Generic diagnosisbased on Acholonu (1976) with 1 emendation: testes diagonal, parallel,or tandem.

Description: Body large, spinose, elongate, 13 mm (9.4 mm 6 3.7mm, 4–15 mm) long; 2.1 mm (1.6 6 0.5 mm, 0.8–2.1 mm) wide atlevel of posterior testis. Spines at anterior end of body approximately6 in length and retaining length until end of vitellarian field, then be-coming 2 or less in length. Oral sucker terminal, ventrally directed, 230in diameter (199 6 18, 179–230). Prepharynx lacking. Pharynx 230(214 6 19, 182–230) long, 153 (129 6 16, 110–153) wide; esophagus204 (185 6 18, 153–204) long; ceca slender, straight, extend to nearposterior end. Acetabulum slightly larger than oral sucker, 255 (234 627, 204–281) in diameter. Cirrus pouch dorsal to acetabulum, elongate,969 (857 6 136, 650–1020) long, 204 (160 6 50, 100–230) wide,enclosing a coiled seminal vesicle which fills posterior third of cirrussac, a pars prostatica which occupies the middle third, and a smallcirrus, and opens to the exterior midway between the intestinal bifur-cation and the anterior edge of the acetabulum. Ovary at end of firstquarter of body, transversely oval, 191 (143 6 55, 96–230) long, 548(372 6 167, 183–561) wide. Seminal receptacle 150 (131 6 10) long,100 (78 6 9) wide, immediately posterior to ovary. Testes tandem,transversely oval, posterior to ovary; posterior testis near end of secondquarter of body. Anterior testis 306 (193 6 97, 102–357) long, 842(504 6 252, 254–842) wide; posterior testis 306 (185 6 90, 105–332)long, 893 (540 6 252, 272–893) wide. Vasa efferentia join just anteriorto the anterior testes. Vitellaria bunchlike, extracecal, 16–22 in 2 lateralrows beginning at the level of posterior end of cirrus sac and ending atend of third quarter of body. Uterus extensive, intercecal, highly con-voluted, passing posteriorly from Mehlis’ gland on right side of bodyto extend near posterior end of body then turning anteriorly to passforward on left side of body, passing ventral to posterior and anteriortestes. Metraterm approximately one-third length of cirrus sac, with thin

1396 THE JOURNAL OF PARASITOLOGY, VOL. 91, NO. 6, DECEMBER 2005

TABLE I. Site of infection, number of helminths, prevalence, mean intensity, and range of infection for 4 helminth species in Uranoscodonsuperciliosus.

Helminth species Site of infection Number Prevalence (%) Mean intensity 6 SD Range

Trematoda

Allopharynx daileyi n. sp.Mesocoelium monas

small intestinelarge intestine

895

244

14.8 6 19.35

1–50—

Nematoda

Africana chabaudiCosmocerca vrcibradici

large intestinelarge intestine

394

408

3.9 6 3.11.5 6 0.7

1–101–2

musculature, lying left of cirrus sac. Eggs, operculate, thick-shelled, 196 3 (15–24) 3 13 6 2 (10–15). Excretory vesicle Y-shaped, long me-dian stem; short, broad rami near ovary; excretory pore terminal (seenonly in nongravid individuals).

Taxonomic summary

Type host: Uranoscodon superciliosus (Linnaeus, 1758) (Squamata:Tropiduridae) common name Calangu Cego (blind lizard, derived fromthe fact that these lizards often allow extremely close approach, relyingon crypsis to escape detection, thus giving the impression that they areblind); symbiotype, OMNH 37508; collection date, 29 January 1988.

Type locality: Rio Formoso, Parque Estadual Guajara-Mirim, Ron-donia state, Brazil 108199S, 648349W.

Type specimens: Holotype, USNPC 95013; Paratypes, USNPC95014. Voucher specimens (immature), USNPC 95015, 95016, and95018.

Etymology: The new species is named in honor of Murray D. Dailey(The Marine Mammal Center, Sausilito, California) in recognition ofhis work on the Trematoda.

Remarks

Acholonu (1976) remarked that species of Allopharynx were of rareoccurrence and that species descriptions were based on one to a fewworms. Indeed, Acholonu (1976) described A. puertoricensis from thesingle specimen found in the 234 Anolis cristatellus (Polychrotidae) thathe examined. Garcıa-Dıaz (1966) described A. riopedrensis from 2specimens taken from an unspecified number of A. cristatellus collectedover an 18-yr period. Simha (1965) described Allopharynx leiperi from8 specimens collected from several hundreds of Indian snakes dissectedover a 2-yr period. Gogate (1935) described Allopharynx mehrai from13 specimens taken from 2 of 19 snakes dissected, 10 specimens fromPtyas korros and 3 specimens from Ptyas mucosus collected in Burma.Allopharynx parorchis was described by Wang (1980) from a singlespecimen taken from a single individual of the snake Dinodon rufozon-atum collected in South China. Allopharynx macallisteri was describedby Dailey et al. (1998) from 7 trematodes taken from 3 of 21 individualsof the gekkonid lizard Lepidodactylus lugubris collected in Guam. Sev-eral species of Allopharynx differ only in body size and given the var-iation seen in our specimens (gravid individuals ranging from 4 to 15mm), we believe some synonymy is necessary. Allopharynx megorchisSimha, 1961 is a synonym of A. mehrai (Gogate, 1935) Price 1938; thestated differences between the 2 species are that A. megorchis has testesof larger diameter and the uterus is greatly distended, otherwise similarmeasurements and the same snake species as host. Allopharynx puer-toricensis Acholonu, 1976 is a synonym of A. riopedrensis Garcia-Diaz,1966; the stated difference between the 2 species is length of body, A.puertoricensis measures 3.5 mm (n 5 1) compared to 5.8 mm for A.riopedrensis (n 5 2). Otherwise they have similar organ arrangementand they were taken from the same lizard host species collected inPuerto Rico.

Allopharynx daileyi n. sp. is most similar to A. macallisteri in thatthe testes are tandem in placement. With the exception of A. parorchis,which has parallel testes, all other species of Allopharynx have diagonaltestes. Differences between A. daileyi and A. macallisteri include theposition of the cirrus sac, parallel to the long axis of the body in A.daileyi but perpendicular to the long axis of the body in A. macallisteri,

and the morphology of the vitellaria, grapelike clusters in A. daileyi butsolid fields of follicles with gaps between fields in A. macallisteri.

Key to species of Allopharynx

1A. Testes parallel . . . . . . . . . . . . . . . . . . A. parorchis Wang, 1980B. Testes otherwise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

2A. Testes tandem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3B. Testes diagonal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4

3A. Cirrus pouch elongate, parallel to long axis of body . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . A. daileyi n. sp.

B. Cirrus pouch elongate, curved such that distal half perpen-dicular to long axis of body . . . . . . . . . . . . . . . . . .. . . . . . A. macallisteri Dailey, Goldberg and Bursey, 1998

4A. Cirrus pouch entirely anterior to acetabulum . . . . . . . . . . . . 5B. Cirrus pouch extending posteriorly beyond acetabulum . . 6

5A Cuticle spinose throughout . . . . . . . . . A. mehrai (Gogate, 1935)B. Spines preacetubular only . . . . . . . . . A. leiperi Simha, 1965

6A. Pharynx adjacent to cecal bifurcation . . . . . . . . . . . . . . . . . 7B. Pharynx adjacent to oral sucker . . . . . . . . . . . . . . . . . . . 8

7A. Aspinose . . . . . . . . . . . . . . . A. riopedrensis Garcia-Diaz, 1966B. Spinose . . . . . . . . . . . . . . . .A. multispinosa (Bennett, 1935)

8A. Cirrus pouch left of metraterm . . A. amudariensis (Strom, 1928)B. Cirrus pouch right of metraterm . . . . . . . . . . . . . . . . . . 9

9A. Vitellaria beginning at intestinal bifurcation . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . A. japonica Tamura, 1941

B. Vitellaria beginning at level of acetabulum . . . . . . . . .. . . . . . . . . . . . . . . . . . A. tropidonoti (MacCallum, 1919)

DISCUSSION

Mesocoelium was established by Odhner (1911) with Meso-coelium sociale (Luhe, 1901) as the type species. Freitas (1958)reassigned Distoma monas Rudolphi, 1819 to Mesocoelium andlater (1963) revised the genus recognizing 7 valid species withMesocoelium monas as the type species and reducing 18 spe-cies, including M. sociale, to synonymy with M. monas. Nasirand Diaz (1971) reviewed the genus and recognized only 4valid species, namely Mesocoelium brevicaecum Ochi, 1930,Mesocoelium geomydae Ozaki, 1936, Mesocoelium megaloonJohnston, 1912 and M. monas. Goldberg et al. (2005) provideda list of hosts for M. monas; U. superciliosus should be addedto that list.

Africana chabaudi was originally described from U. super-ciliosus collected in Belem, Brazil by Baker (1981). This is thesecond report of A. chabaudi in U. superciliosus.

Cosmocerca vrcibradici was originally described fromPrionodactylus eigenmanni and Prionodactylus oshaughnessyifrom Brazil and Ecuador, respectively (Bursey and Goldberg,2004). This is the second report for C. vrcibradici, and U. su-perciliosus represents the third host for C. vrcibradici.

BURSEY ET AL.—NEW SPECIES OF ALLOPHARYNX 1397

FIGURES 1–4. Allopharynx daileyi n. sp. (1) Mature, entire, ventral view. (2) Immature, entire, ventral view. (3) Terminal genitalia, ventralview. (4) Egg.

1398 THE JOURNAL OF PARASITOLOGY, VOL. 91, NO. 6, DECEMBER 2005

ACKNOWLEDGMENTS

Peggy Firth prepared the illustrations constituting Figs. 1–4. Wethank T. C. S. Avila-Pires, J. P. Caldwell, Shawn S. Sartorius, and PeterA. Zani for helping to collect the lizards and Amanda Woosley forassistance with dissection. Lizards were treated in accordance with fed-eral, state, and university regulations (Animal Care Assurance 73-R-100, approved 8 November 1994, University of Oklahoma). Lizardswere collected under permits issued by the Conselho Nacional de De-senvolvimento Cientıfico e Tecnologico (CNPq, Portaria MCT 170, de28 September 1994) and the Instituto Brasileiro do Meio Ambiente edos Recursos Naturais Renovaveis (IBAMA, permit 073/94-DIFAS).NSF grants DEB-9200779 and DEB-9505518 to L.J.V. and J. P. Cald-well supported collection of lizards.

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AVILA-PIRES, T. C. S. 1995. Lizards of Brazilian Amazonia (Reptilia: Squa-mata). Zoologische Verhandelingen, Leiden, Netherlands, 706 p.

BAKER, M. R. 1981. Africana chabaudi n. sp. (Nematoda, Heterakidae)in a Brazilian iguana. Bulletin du Museum National d’Histoire Na-turelle Paris 3: 783–787.

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