Journal of Parasitology NEW SPECIES OF PARAPHARYNGODON (NEMATODA: PHARYNGODONIDAE) IN RHINELLA MARINA (ANURA: BUFONIDAE) FROM GRENADA, WEST INDIES --Manuscript Draft-Manuscript Number:
GE-3235R1
Full Title:
NEW SPECIES OF PARAPHARYNGODON (NEMATODA: PHARYNGODONIDAE) IN RHINELLA MARINA (ANURA: BUFONIDAE) FROM GRENADA, WEST INDIES
Short Title:
NEW SPECIES OF PARAPAHRYNGODON
Article Type:
Regular Article
Corresponding Author:
Charles R. Bursey Pennsylvania State University Sharon, PA UNITED STATES
Corresponding Author Secondary Information: Corresponding Author's Institution:
Pennsylvania State University
Corresponding Author's Secondary Institution: First Author:
Charles R. Bursey
First Author Secondary Information: Order of Authors:
Charles R. Bursey Michael Drake Rebecca Cole Mauritz Sterner III Rhonda Pinckney Ulrike Zieger
Order of Authors Secondary Information: Abstract:
Parapharyngodon grenadaensis sp. n. (Nematoda: Pharyngodonidae) from the large intestine of the cane toad, Rhinella marina, is described and illustrated. Parapharyngodon grenadaensis sp. n. is the 48th species assigned to the genus and the 16th from the Neotropical region. It differs from other species in the genus by possessing 4 pairs of caudal papillae, an echinate anterior cloacal lip, and a blunt spicule of 67-104 µm. This is only the second report of Rhinella marina harboring a species of Parapharyngodon.
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RH: BURSEY ET AL.--NEW SPECIES OF PARAPHARYNGODON NEW SPECIES OF PARAPHARYNGODON (NEMATODA: PHARYNGODONIDAE) IN RHINELLA MARINA (ANURA: BUFONIDAE) FROM GRENADA, WEST INDIES Charles Bursey, Michael Drake*, Rebecca Cole†, Mauritz Sterner, III†, Rhonda Pinckney‡, and Ulrike Zieger* Department of Biology, Pennsylvania State University, Shenango Campus, Sharon, Pennsylvania 16146. e-mail:
[email protected] ABSTRACT: Parapharyngodon grenadaensis n. sp. (Nematoda: Pharyngodonidae) from the large intestine of the cane toad, Rhinella marina, is described and illustrated. Parapharyngodon grenadaensis n. sp. is the 48th species assigned to the genus and the 16th from the Neotropical region. It differs from other species in the genus by possessing 4 pairs of caudal papillae, an echinate anterior cloacal lip, and a blunt spicule of 67-104 µm. This is only the second report of Rhinella marina harboring a species of Parapharyngodon. During an ecological study of the cane toad, Rhinella marina (Linnaeus, 1758), in Grenada, West Indies, 60 nematodes (5 males, 55 females) of an undescribed species of Parapharyngodon Chatterji, 1933, were collected from the large intestines of 18 toads. The original range of Rhinella marina extended from the lower valley region of southern Texas (USA) and southern Sonora (Mexico) south through tropical lowland Mexico and Central America to the west coast of Ecuador and extreme northwestern Peru, and, east of the Andes throughout Amazonian South America. Subsequently, it has been introduced worldwide, including Antilles, Hawaii, Fiji, Philippines, Taiwan, Ryukyu Islands, New Guinea, Australia and many Pacific islands (Frost, 2011). In the 1800’s, the cane toad was introduced to Grenada to control agricultural pests in sugar cane plantations (Barbour, 1914; Easteal, 1981). Introduced
species will often harbor parasites found in the original native range, as well as newly encountered parasites, which they acquire after introduction (Barton, 1996). The validity of Parapharyngodon has been in question almost since its proposal by Chatterji (1933). Baylis (1936) considered it to be a synonym of Thelandros Wedl, 1862. Karve (1938), García-Calvente (1948), and Skrjabin et al. (1951) maintained the synonymy. Freitas (1957) reinstated the genus. Yamaguti (1961) reduced Parapharyngodon to a subgenus of Thelandros; later, Chabaud (1965) returned it to synonymy with Thelandros. Sharpilo (1976) reinstated Parapharyngodon, while Petter and Quentin (1976) again synonymized Parapharyngodon with Thelandros. Adamson (1981) reestablished Parapharyngodon based on dietary habits of the host, male genital cone morphology (well developed in Thelandros, reduced or absent in Parapharyngodon), egg morphology (operculum polar in position, embryonated at deposition in Thelandros; subpolar operculum early cleavage in Parapharyngodon), and morphology of the tail of females (variable in Thelandros; short, stiff spike in Parapharyngodon). Castaño-Fernandez et al. (1987) retained the 2 genera, but restricted separation of the genera to morphological characters, not dietary habits of the hosts. Gupta et al. (2009) reinstated subgenus status for Parapharyngodon; however, Pereira et al. (2011) retained both genera. We consider the most significant character for separation of Parapharyngodon and Thelandros to be egg morphology. The eggs of Parapharyngodon spp. have a subterminal operculum and are in the early stages of cleavage when released; the eggs of Thelandros spp. have a terminal operculum and are fully embryonated at deposition. Other distinguishing differences: males of Parapharyngodon spp. lack a genital cone, papillae surround the cloaca, accessory piece is absent, and the tail is subterminal and curved dorsally, whereas males of
Thelandros spp. have a narrow, elongated genital cone (occasionally with an accessory piece), papillae are outside the genital cone, and the tail is terminal. Females of Parapharyngodon spp. have a conical tail ending in a short spike, while females of Thelandros spp. have various caudal morphologies (in some species the tail is conical, tapering evenly from the anus; in others, it is rounded and supports a short filiform appendage). Based on egg morphology, the specimens taken from Rhinella marina collected in Grenada are assigned to Parapharyngodon. MATERIALS AND METHODS Specimens of Rhinella marina were collected by hand (n = 100) in Grenada from 3 locations in St. George’s Parish, i.e., True Blue Peninsula (12°00.289'N, 61°46.033'W), Lance Aux Epines Peninsula (12°00.236'N, 61°45.506'W), and Fort Jeudy/Woburn area (12°00.754'N, 61°43.989'W). They were killed by applying 20% benzocaine gel (Anbesol®) to their dorsal surface, followed by pithing (St. George University IACUC 10012-R). At necropsy, the body was opened by a longitudinal incision from vent to throat, and the gastrointestinal tract was removed by transection of esophagus and rectum. The esophagus, stomach, and small and large intestines of each toad were examined separately for helminths. Nematodes were heat fixed in 10% neutral buffered formalin for 15 min, then preserved in a 70% ethanol/5% glycerol solution. They were later transferred to lactophenol, allowed to clear, and examined using a compound microscope. Drawings were made with the aid of a microprojector. Measurements are in micrometers with mean ± 1 SD and range in parenthesis, unless otherwise stated. DESCRIPTION Parapharyngodon grenadaensis n. sp. (Figs. 1-11)
Diagnosis: Robust nematodes with prominent annulations beginning just behind cephalic extremity and continuing to anus. Evident sexual dimorphism; males one-third length of females. Triangular oral opening surrounded by 3 bilobed lips, each lobe with 1 small papilla. One small, pedunculate amphid laterally situated on each ventrolateral lip. Lateral alae present in males, absent in females. Males without caudal alae; caudal filament directed dorsally. Females with conical tail. Male (holotype and 4 paratypes): Length 2.01 ± 0.32 mm (1.54-2.27 mm), width at level of excretory pore 261 ± 59 (204-344). Esophagus 383 ± 98 (306-510): vestibule 15 ± 3 (12-18), corpus 324 ± 44 (300-390), isthmus 20 ± 3 (18-24), bulb 89 ± 14 (67-106) long, 92 ± 15 (67106) wide. Nerve ring 116 ± 5 (110-122) and excretory pore 644 ± 90 (535-740) from anterior end, respectively. Lateral alae beginning at level of nerve ring, gradually increasing in width to 20, ending at level of precloacal papillae. Annulations about 12 apart. Testis at midbody, flexing posteriorly immediately behind excretory pore. Vas deferens separated from testis by narrow tube. Tail 91 ± 11 (79-104) inserted dorsally, reduced to slender appendage 29 ± 2 (2731) from insertion. Spicule 87 ± 17 (67-104) long, terminating in a blunt tip. Eight caudal papillae, 1 pair ventral, precloacal; 1 pair lateral, post cloacal, 1 pair median, post cloacal, 1 pair on caudal appendage 28 ± 2 (26-30). Anterior cloacal lip echinate. Female: (allotype and 9 paratypes): Length 5.54 ± 0.56 mm (4.29-6.16 mm), width at vulva 478 ± 26 (434-50). Esophagus 1,106 ± 49 (995-1,148), vestibule 15 ± 3 (12-18), corpus 888 ± 35 (816-918), isthmus 36 ± 6 (25-47), bulb, 172 ± 14 (148-195) long, 205 ± 12 (189-226) wide. Nerve ring 205 ± 13 (191-230), excretory pore 1,392, ± 101 (1, 216-1,536), and nonsalient vulva 3,046 ± 269 (2,624-3,328) from anterior end, respectively. Proximal half of vagina muscular. Vagina directed dorsally, then posteriorly to join divergent uteri. Anterior uterus
forming several loops in midbody region, posterior uterus extending to posterior end of body cavity, then flexing anteriorly. Both uteri join oviducts in midbody region; distinct spermatheca present at junction. Ovaries originating in region of esophageal bulb. In older gravid individuals, the ovaries extend into corporal region and wrap around esophageal corpus. Eggs subovate, slightly flattened on 1 side, flattened side obvious in optical cross section, 70 ± 3 (67-73) long, 35 ± 2 (31-37) wide, early stages of cleavage at deposition. Egg shell thick; surface covered with tiny punctuations. Anus slit like, 488 ± 32 (434-536) from end of tail. Posterior end of body conical; body cavity terminates 243 ± 23 (217-281) from posterior end of tail and this last portion, especially in very gravid females, becomes slightly set off from the body. Taxonomic summary Type host: Rhinella marina (Linnaeus, 1758) Anura, Bufonidae; cane toad. (Class exercise: toads discarded). Type locality: Grenada, St. George’s Parish. Site of infection: Large intestine. Prevalence and intensity of infection: 18% (18/100); mean intensity 3.2. Type specimens: Holotype: male, USNPC 105770; allotype: female, USNPC 105771; paratypes: 3 males, 9 females, USPC 105772; voucher specimens, female, USNPC 105773. Etymology: The species is named after the collection site of the hosts: Grenada, West Indies. Remarks Forty-seven nominal species of Parapharyngodon are recognized by Pereira et al. (2011) and with the exception of P. anomalus Hobbs, 1996, P. duniae Bursey and Brooks, 2004, P. garciae Schmidt and Whitaker, 1975, P. japonicus Bursey and Goldberg, 2000, and P. verrucosus Freitas and Dobbin, 1959, all are parasites of lizards. Currently, 3 species are found
in the Australian Realm, 8 in the Ethiopian Realm, 3 in the Nearctic Realm, 15 in the Neotropical Realm, 7 in the Oriental Realm, and 11 in the Palearctic Realm. Morphological characters used to separate species of Parapharyngodon include the pattern and number of caudal papillae, lateral alae, cloacal lip and spicule morphologies of the male as well as ovary location, and egg and tail morphologies in the female. Of the 47 nominal species, as in P. grenadaensis n. sp., males of 19 species possess 4 pairs of caudal papillae (Table I), namely, P. adamsoni Crusz and Daundasekera, 1988, P. adramitana Adamson and Nasher, 1984, P. almorensis Karve, 1949, P. anomalus, P. awokoyai Babero and Okpala, 1962, P. baueri Bursey and Goldberg, 2007, P. bulbosus (Linstow, 1899), P. californiensis (Read and Amrein, 1952), P. colonensis Bursey, Goldberg and Telford, 2007, P. dogieli Markov and Bogdanov, 1965, P. echinatus Rudolphi, 1819, P. fitzroyi Jones, 1992, P. garciae, P. margaritiferi Hering-Hagenbeck, 2001, P. meridionalis Chabaud and Brygoo, 1962, P. micipsae Seurat, 1917, P. osteopili Adamson, 1981, P. rousseti Tcheprakoff, 1966, and P. skrjabini Vakaker, 1969. Males of 6 of the 19 species possess a smooth anterior cloacal lip in contrast to the echinate lip of P. grenadaensis n. sp., namely, P. adamsoni, P. baueri, P. bulbosus, P. californiensis, P. garciae, and P. skrjabini. Females of remaining species listed above possess smooth egg shells in contrast to the punctate shell of P. grenadaensis n. sp., namely, P. adramitana, P. almorensis, P. anomalus, P. awokoyai, P. brevicaudatus, P. colonensis, P. dogieli, P. echinatus, P. fitzroyi, P. margaritiferi, P. meridionalis, P. micipsae, and P. rousseti. To our knowledge, only specimens of Rhinella marina collected in American Samoa have been reported to harbor species of Parapharyngodon, namely, P. kartana (Goldberg and Bursey, 1992), a nematode species common in the Samoan skinks, Emoia nigra and E. samoense (Goldberg and Bursey, 1991). Parapharyngodon grenadaensis differs from P. kartana in that
the anterior cloacal lip of males of P. kartana is smooth. Also, to our knowledge, only 4 species of anurans, in addition to R. manina, occur on Grenada, i.e., Eleutherodactylus johnstonei Barbour, 1914, E. planirostris (Cope, 1862), Leptodactylus validus Garman, 1888, and Pristimantis euphronides (Schwatz, 1967) (Frost, 2011). Both Goldberg et al. (1995) and Linzey (1998) reported P. garciae from E. johnstonei collected in Bermuda. In the only examination of E. planirostris, Coy Otero, and Vetosa (1984) reported Batracholandros bassi (Walton, 1940) from frogs collected in Cuba. Leptodactylus validus and P. euphronides apparently have not been subjects of helminthology studies. Thus, we cannot say with any certainty whether P. grenadaensis was transported or acquired. However, males of Parapharyngodon grenadaensis differ from P. garciae in that the anterior cloacal lip of P. garciae is smooth. ACKNOWLEDGMENTS The authors thank various veterinary students at St. George University, St. George, Grenada for assistance in capture and necropsies of toads. Partial funding of work was supplied by College of Veterinary Medicine, MSc Wildlife Conservation Medicine Program and Pathobiology Department, St. George’s University, St. George, Grenada and U.S. Geological Survey, National Wildlife Health Center, Madison, Wisconsin. Use of trade or product names does not imply endorsement by the U.S. Government. LITERATURE CITED Adamson, M. L. 1981. Parapharyngodon osteopili n. sp. (Pharyngodonidae: Oxyuroidea) and a revision of Parapharyngodon and Thelandros. Systematic Parasitology 3: 105-117. ________, and A. K. Nasher. 1984. Pharyngodonids (Oxyuroidea; Nematoda) of Agama adramitana in Saudi Arabia with notes on Parapharyngodon. Canadian Journal of Zoology 62: 2600-2609.
Ashour, A. A., M. Q. Wanas, M. M. I. Salama, and N. A. Gafarr. 1994. Scanning electron microscope observations on Parapharyngodon bulbosus (Linstow, 1899) (Nematoda: Pharyngodonidae) from Egyptian Chalcides ocellatus. Journal of the Egyptian Society of Parasitology 24: 585-590. Babero, B. B., and I. Okpala. 1962. Parasites of the lizard, Agama colonarum, in Nigeria with description of a new species. Transactions of the American Microscopical Society 81: 228-237. Barbour, T. 1914. A contribution to the zoogeography of the West Indies, with especial reference to amphibians and reptiles. Memoires of the Museum of Comparative Zoology at Harvard College 44: 209-346. Barton, D. P. 1996. The cane toad: A new host for helminth parasites in Australia. Australian Journal of Ecology 21: 114-117. Baylis, H. A. 1936. Nematoda. I. Ascaridoidea and Strongyloidea. The fauna of British India. Taylor and Francis, London, U.K., 408 p. Bursey, C. R., and S. R. Goldberg. 2007. New species of Parapharyngodon (Nematoda: Pharyngodonidae) and other helminths in Petrosaurus repens and P. thalassinus (Squamata: Phrynosomatidae) from Baja California del Sur, Mexico. The Southwestern Naturalist 52: 243250. Castaño-Fernandez, C., L. M. Zapatero-Ramos, and M. A. Solera-Puertas. 1987. Revisión de los géneros Parapharyngodon Chatterji, 1933 y Thelandros Wedl, 1862 (Oxyuroidea, Pharyngodonidae). Revista Ibérica de Parasitología 47: 271-274. Chabaud, A. G. 1965. Ordre des Ascaridida. In Traité de zoologie. Systematique de nematodes, P. P. Grassé (ed.). Masson et Cie, Paris, France, p. 932-1180.
_________, and E.-R. Brygoo. 1962. Nematodes parasites de cameleons malgaches. Annales de Parasitologie Humaine et Camparée 37: 569-602. Chatterji, R. C. 1933. On a new nematode, Parapharyngodon maplestoni gen. nov., sp. nov. from a Burmese lizard. Annals of Tropical Medicine and Parasitology 27: 131-134. Crusz, H., and D. M. A. K. Daundasekera. 1988. Parasites of the relic fauna of Ceylon. IX. Helminths from burrowing scincine lizards. Annales de Parasitologie Humaine et Comparée 63: 439-447. Easteal, S. 1981. The history of introductions of Bufo marinus (Amphibia: Anura): A natural experiment in evolution. Biological Journal of Linnaean Society 16: 93-113. Freitas, J. F. T. 1957. Sôbre os gêneros Thelandros Wedl, 1862 e Parapharyngodon Chatterji, com descrição de Parapharyngodon alvarengai n. sp. (Nematoda, Oxyuroidea). Memórias do Instituto Oswaldo Cruz 55: 21-45. Frost, D. R. 2011. Amphibian species of the world: An online reference. Version 5.5 (31 January, 2011). Electronic Database accessible at http://research.amnh.org/vz/herpetology/amphibia/
American Museum of Natural History, New York, USA. García-Calvente, I. 1948. Revisión del género Pharyngodon y descripción de nuevas especies. Revista Ibérica de Parasitología 8: 367-410. Goldberg, S. R., and C. R. Bursey. 1991. Parapharyngodon kartana in two skinks, Emoia nigra and Emoia samoense (Sauria: Scincidae), from Samoa. Journal of the Helminthological Society of Washington 58: 265-266.
_________, and _________. 1992. Helminths of the marine toad, Bufo marinus (Anura: Bufonidae), from American Samoa. Journal of the Helminthological Society of Washington 59: 131-133. _________, _________, and S. R. Telford, Jr. 2007. Gastrointestinal helminths of 14 species of lizards from Panama with descriptions of five new species. Comparative Parasitology 74: 108140. Gupta, N., M. Bhaskar, and D. K. Gupta. 2009. Gastro-intestinal invasion of Hemidactylus flaviviridis with a new species of Parapharyngodon (Oxyuroidea: Pharyngodonidae). Zootaxa 2165: 39-51. Hering-Hagenbeck, S. F. B. N., A. J. Petter, and J. Boomker. 2002. Redescription of some Spauligodon spp. and Parapharyngodon spp. and of Skrjabinodon mabuyae (Sandground, 1936) Inglis, 1968 (Pharyngodonidae: Oxyuroidea) from insectivorous South African lizards. Onderstepoort Journal of Veterinary Research 69: 7-29. Hobbs, R. P. 1996. Parapharyngodon anomalus sp. n. (Oxyurida, Pharyngodonidae) from the Australian echidna Tachyglossus aculeatus, with notes on the Thelandroinae. Journal of the Helminthological Society of Washington 63: 56-61. Jones, H. I. 1992. Gastrointestinal nematodes in the lizard genera Tiliqua and Cyclodomorphus (Scincidae) in Western Australia. Australian Journal of Zoology 40: 115-126. Karve, J. N. 1938. Some nematode parasites of lizards. In Livro Jubilar do Prof. Lauro Travassos, Editado para commemorar o 25 anniversario de suas actividades scientificas (19131938), B. Silva (ed.). Insituto Oswaldo Cruz, Rio de Janeiro, Brazil, p. 251-258. _________. 1949. Parasitic nematodes from an agamid lizard, Agama tuberculata Gray. Journal of the University of Bombay 18: 1-16.
Masova, S., V. Barus, I. Hodova, I Matejusova, P. Koubek, and B. Koubkova. 2008. Morphometric and molecular characterization of Parapharyngodon echinatus (Nematoda, Pharyngodonidae) from the Senegal gecko (Tarentola parvicarinata). Acta Parasitologica 53: 274-283. Pereira, F. B., B. M. Sousa, and S. de Souza Lima. 2011. A new species of Pharyngodonidae (Nematoda) of Tropidurus torquatus (Squamata: Tropiduridae) from Brazil. Journal of Parasitology 97: 311-317. Petter, A. J., and J. C. Quentin. 1976. CIH Keys to the nematode parasites of vertebrates. No. V. Keys to the genera of the Oxyuroidea. Commonwealth Agricultural Bureaux, Farnham Royal, U.K., 30 p. Read, C. P., and Y. U. Amrein. 1952. Some new oxyurid nematodes from southern California. Journal of Parasitology 38: 379-384. Seurat, L. G. 1917. Sur les oxyures des sauriens du Nord-africain. Archives de Zoologie Expérimentale et Générale 56: 401-444. Sharpilo, C. P. 1976. Parasitic worms of the reptilian fauna of the USSR: Systematics, chorology, biology. Naukova Dumka, Moscow. Russia, 287 p. Skrjabin, K. I., N. P. Shikhobalova, and A. A. Mozgovoi. 1951. Key to parasitic nematodes. Vol. 2. Oxyurata and Ascaridata. Izdatel’stvo Akademii Nauk S.S.S.R., Moscow. (English translation by Amerind Publishing Co. Pvt. Ltd., New Delhi, India, 1982, 703 p.) Schmidt, G. D., and F. H. Whittaker. 1975. Nematode parasites of Puerto Rican tree frogs, Eleutherodactylus spp: Two new species and a proposal of Poekilostrongylus gen. nov. (Trichostrongylidae). Parasitology 70: 287-294.
Tcheprakoff, R. 1965. Description de Thelandros roussesti n. sp., parasite d’Agame au Sahara. Bulletin du Museum National d’Histoire Naturelle 37: 861-864. Yamaguti, S. 1961. Systema helminthum, Vol. III (Parts I and II) Nematodes of vertebrates. Interscience Publishers, Inc., New York, New York, 1261 p.
Figures 1-11. Parapharyngodon grenadaensis n. sp. (1) Female, entire, lateral view. (2) Female, anterior end, en face view. (3). Female, anterior end, dorsal view. (4). Male, entire, lateral view (5) Male, entire, lateral view. (6) Male, posterior end, lateral view. (7) Male, posterior end, ventral view (8) Egg, early cleavage, optical cross-section (9) Egg, early cleavage, optical longitudinal-section (10) Egg, operculate surface. (11) Male, spicule. Measurements are in µm.
*Department of PreClinical Studies, St. George’s University, School of Veterinary Medicine, St. George’s, Grenada. †USGS, National Wildlife Health Research, 6006 Schroeder Road, Madison, Wisconsin 53711-6223. ‡Department of Pathobiology, St. George’s University, School of Veterinary Medicine, St. George’s, Grenada.
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Table Click here to download Table: GR-3235 Parapharyngodon Table .doc
Table I. Selected characters of species possessing 4 pair of caudal papillae assigned to Parapharyngodon. Biogeographical area
Species
Male
Female
Spicule (µm)
Spicule tip
Cloacal lip Location of lateral alae
Tail terminus
Ovary
Lip structure
P. anomalus
63
Blunt
Echinate
P. fitzroyi
80-92
Blunt
Echinate
1,100 from ant end to 100 from post end Eso bulb to cloaca
Stout spike
Prebulblar
6 simple
Stout spike
Prebulblar
6 simple
P. adramitana
80-86
Sharp
Echinate
Mid-eso to 70 from post end Present, not described
Stout spike
Prebulblar
6 lips
P. awakoyai
590-650
Sharp
Echinate
Stout spike
Prebulblar
Not described
P. baueri
79-98
Sharp
Smooth
Post border eso bulb to 255-383 from post end 370 from ant end to 410 from post end Eso bulb to 500 µm from post end Excretory pore to cloaca
Stout spike
Prebulblar
P. margaritiferi
80
Sharp
Echinate
Stout spike
P. meridionalis
80
Sharp
Echinate
P. rousseti
110
Blunt
Echinate
53-76
Sharp
Smooth
Absent
References
Egg
Australian Analate; shell smooth Analate; shell smooth
Hobbs,1996
Analate; shell smooth Analate; shell smooth
Adamson and Nasher,1984 Babero and Okpala,1962
3 simple
Analate; shell smooth
Bursey and Goldberg, 2007
Prebulblar
6 simple
Stout spike
Prebulblar
3 bilobed
Stout spike
Prebulblar
Male 3 Female 6
Analate; shell smooth Analate; shell smooth Analate; shell smooth
Hering-Hagenbeck et al.2002 Chabaud and Brygoo,1962 Tcheprakoff,1966
Stout spike
Prebulblar
Not described
Analate; shell smooth
Read and Amrein,1952
Jones, 1992
Ethiopian
Nearctic P. californiensis
Neotropical
P. colonensis
61-67
Blunt
Echinate
202-244 from ant end to ant pr papillae
Conical, no spike
Prebulblar
6 simple
Analate; shell punctate
Bursey et al.2007
P. garciae
30-45
Sharp
Smooth
Present, not described
Stout spike
Prebulblar
6 simple
P. grenadaensis n. sp.
67-104
Blunt
Echinate
Prebulbar
6 simple
53-61
Blunt
Echinate
Conical, no spike Conical, no spike
Schmidt and Whittaker, 1975 This paper
P. osteopili
Nerve ring to precloacal papillae Absent
Prebulblar
6 simple
Analate; shell smooth Analate, Shell punctate Alate; shell smooth
P. adamsoni
62-120
Blunt
smooth
Stout spike
Prebulbar
6 simple
P. almoriensis
85-105
Blunt
Echinate
Level of esophagus to 164-267 ant anus 620-720 from ant end to 60-90 from post end
Thin spike
Postbulbar
Not described
Analate; shell smooth Analate; shell smooth
Crusz and Daundasekera, 1988 Karve,1949
P. bulbosus
55
Sharp
Smooth
Stout spike
Postbulbar
6 simlpe
Not described
Ashour et al., 1994
P. dogieli
93-110
Sharp
Echinate
Eso-intest junct to 200 from post end 350 µm from lip to 230 from post end
Conical, no spike
Prebulblar
3 simple
Analate; shell smooth
Sharpilo,1976
P. echinatus
74-112
Blunt
Echinate
Stout spike
Postbubar
3 bilobed
88
Blunt
Echinate
Stout spike
Prebulblar
3 bilobed
Analate; shell smooth Analate; shell smooth
Masova et al., 2008
P. micipsae
P. skrjabini
139-176
Sharp
Smooth
Mid-body to 89-162 from post end 456 from ant end to 400-530 from post end 563 from ant end to cloaca
Thin spike
Prebulblar
Not described
Analate; shell smooth
Sharpilo,1976
Adamson,1981
Oriental
Palaearctic
Seurat,1917
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