Parassitologia 49: 97-100, 2007
A new pronocephalid, Pleurogonius tortugueroi n. sp. (Digenea), from the intestine of green sea turtles (Chelonia mydas) in Costa Rica M. Santoro 1, E.C. Greiner 2, J.A. Morales 1, B. Rodríguez-Ortíz 3 1 Departamento de Patología, Escuela de Medicina Veterinaria, Universidad Nacional, Heredia, Costa Rica; 2 Department of Infectious Diseases and Pathology, College of Veterinary Medicine, University of Florida, Gainesville, FL, USA; 3 Laboratorio de Helminthología, Facultad de Microbiología, Universidad de Costa Rica, San Pedro, Costa Rica.
Abstract. A new species of trematode, Pleurogonius tortugueroi n. sp. (Digenea: Pronocephalidae) is described from the lower intestine of green sea turtles (Chelonia mydas) from Tortuguero National Park, Costa Rica. The new species differs from all other species of Pleurogonius by having a short oesophagus and oval testes close to lateral posterior limit of the body. It differs from all other species, except P. malaclemys Hunter 1961, by having an ovary between the testes; moreover the latter species is a parasite of freshwater turtles. All others members of the genus have a long oesophagus, testes placed to some distance from the posterior end, and the ovary is pretesticular. The new species appears most closely related to P. linearis Looss, 1901 but differs from it by having a different body shape, lappets of the head collar close at the cecal bifurcation level, a longer vitellarian field, different testis shape and position, ovary intertesticular, and different egg size. Key words: Pleurogonius tortugueroi, Digenea, Pronocephalidae, Chelonia mydas, green turtle, Costa Rica.
The green sea turtle (Chelonia mydas) is a herbivorous species widely distributed in the Caribbean Sea where nest sites occur and extensive pastures of Thalassia testudinum provide their forage. Data regarding the helminth fauna of Caribbean green turtles are scarce. Because sea turtles are endangered the collection of endoparasites may occur only when the chelonian is found dead. Previous reports indicate that digenetic trematodes have been obtained from free-ranging green turtles in Jamaica (Stephens, 1911), Trinidad (Gupta, 1961), an unnamed Caribbean site (Gupta, 1962), Cuba (Groschaft, 1977; Groschaft et al., 1977; Groschaft and Tenora, 1978), and Puerto Rico (Dyer et al., 1991; Williams et al., 1994; Dyer et al., 1995a). Digenetic trematodes collected during a parasitological survey performed on green turtles at Tortuguero National Park, Costa Rica by Santoro et al. (2006), included an undescribed species of the family Pronocephalidae Looss, 1902. Herein, we describe Pleurogonius tortugueroi n. sp. from the lower intestine of Chelonia mydas.
Materials and methods Forty female green turtles (curved carapace length ranging from 92 to 111 cm) collected between June and September of 2003 and 2004, from Tortuguero National Park, Costa Rica (10º 32’ 27’’ N, 83º 29’ 59’’ W - 10º 21’ 17’’ N, 83º 23 ’29’’ W), were necropsied following the methods of Wolke and Correspondence: Dr Mario Santoro, Departamento de Patología, Escuela de Medicina Veterinaria, Universidad Nacional, PO Box 86, Heredia 3000, Costa Rica. Tel/Fax +506 2600849, e-mail:
[email protected]
George (1981). Turtles were obtained freshly dead along 26 km of the park’s beach. Organs were carefully examined for parasites following the methods described by Greiner et al. (1980). Trematodes were placed in tap water, refrigerated overnight, then fixed in AFA (alcohol-formalin-acetic acid solution) or 70% ethanol, stained with Mayer’s acid carmine, mounted in Canada balsam, and examined by light microscopy. Measurements are reported in micrometers (unless otherwise stated) with the mean followed by the range in parentheses. Figures were drawn with the aid of a camera lucida. Specimens were deposited in the Colección Helmintológica de Costa Rica (CHCR), Universidad de Costa Rica, San José, Costa Rica, and the Harold W. Manter Laboratory of Parasitology (HWML), Nebraska State Museum, Lincoln, Nebraska.
Results One and 10 mature specimens of Pleurogonius tortugueroi n. sp. were collected from the lower intestine of 2 out of 40 (5%) green turtles examined for parasites. Pleurogonius tortugueroi n. sp. (Fig. 1) Description based on 10 mature specimens. Body small and elongate, anterior extremity narrow to point and posterior rounded. Tegument aspinose. Body 2.1 (1.5-2.4) mm long by 0.7 (0.5-0.8) mm wide. Lappets of the head collar close at cecal bifurcation level. Oral sucker sub-terminal, small, round to slightly oval, 107 (72-123) long by 116 (93-124) wide. Oesophagus short and narrow, 168 (121-214) long. Ceca long reaching posterior end of body, slightly sinuous, with
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M. Santoro et al. - A new pronocephalid from Chelonia mydas
Fig. 1. Pleurogonius tortugueroi n. sp. A: Ventral view of holotype. B: Terminal genitalia.
small diverticula throughout entire length. Testes 2, oval irregularly lobed, opposite, extracecal, close to lateral posterior limit of body. Left testis 285 (206360) long by 179 (154-206) wide. Right testis 275 (175-337) long by 192 (113-227) wide. Cirrus sac tubular, robust with thick walls, intercecal, 394 (340463) long by 111 (84-124) wide, placed longitudinally with genital pore sinistral to midline of body. External seminal vesicle coiled, posterior to base of cirrus sac. Ovary round irregularly lobed, intertesticular, dextral to mid line of body, 158 (133-195) long by 164 (124-206) wide. Mehlis’ gland round, postovarian on midline of body, 133 (93-184) long by 117 (93154) wide. Laurer’s canal not seen. Vitellaria composed of lateral longitudinal row of large extracecal oval follicles overlapping anterior margin of testis, occupy 1/4 of total body length. Left vitelline follicles (n = 20) 43 (30-81) long by 66 (49-106) wide. Right vitelline follicles (n = 20) 44 (24-86) long by 61 (3286) wide. Vitelline ducts form small reservoir ventral to Mehlis’ gland, overlapping anterior margin of testis. Excretory vesicle small. Uterus preovarian, mainly extracecal, with sinuous transverse coils filled by eggs extending from anterior limit of ovary to posterior limit of cirrus sac, occupies 1/3 of body, ending in a tubular metraterm parallel to cirrus pouch. Eggs numerous (n = 30) 27 (24-30) long by 14 (12-17) wide, with single polar filament (n = 5) 247 (230270) long on each end.
Taxonomic summary Type host: Chelonia mydas Linnaeus, 1758 (Testudines: Cheloniidae). Site of infection: Lower intestine. Type locality and collection date: Tortuguero National Park (10º 32’ 27’’ N, 83º 29’ 59’’ W - 10º 21’ 17’’ N, 83º 23’ 29’’ W), Limón Province, north east Caribbean coast of Costa Rica; July and August 2004. Specimens deposited: Holotype, CHCR 168; paratypes, CHCR 173/175 (5 specimens), and HWML 48205-48234 (2 specimens). Prevalence and intensity of infection: 5% (2 infected/40 examined); Intensity 1-10. Etymology: The new species is named after the Tortuguero National Park.
Discussion Pronocephalidae was erected by Looss (1902) for digenetic monostomes from sea turtles characterized by a head collar. Pleurogonius was created for P. longiusculus (Looss, 1901). Glyphicephalus was erected by Looss (1901) for G. solidus and G. lobatus recovered from green turtles. Linton (1910) described 2 new genera, Barisomum with B. erubescens and Himasomum with H. candidulum from marine fishes. Oguro (1936) created Medio-
M. Santoro et al. - A new pronocephalid from Chelonia mydas porus for M. macrophallus and M. cheloniae from Chelonia japonica. Looss (1901), Mehra (1939), and Caballero et al. (1955) synonymized Glyphicephalus and Pleurogonius. Ruiz (1946) in his review of Pronocephalidae family transferred Barisomum, Glyphicephalus, and Medioporus to Pleurogonius. Skrjabin (1964) and Yamaguti (1971) considered again Glyphicephalus, Barisomum (syn. Himasomum), Medioporus, and Pleurogonius as 4 separate genera. Yamaguti (1971) listed 15 valid species of the genus Pleurogonius: P. americanus Caballero et al., 1955, P. bilobus Looss, 1901, P. chelonii Mehra, 1939, P. grocotti Caballero et al., 1954, P. karachii Mehra, 1939, P. keamarii Mehra, 1939, P. linearis Looss, 1901, P. longibursatus Pérez-Vigueras, 1955, P. longiusculus Looss, 1901, P. malaclemys Hunter, 1961, P. minutissimus Looss, 1901, P. ozakii Oguro, 1936, P. sindhii Mehra, 1939, P. trigonocephalus (Rudolphi, 1809) Looss, 1901, and P. truncatus Prudhoe, 1944. To his list should be added P. carettae from loggerheads (Caretta caretta) and P. mandapamensis from Eretmochelys squamosa, both described by Chattopadhyaya (1972), and P. laterouterus and P. puertoricensis described from hawksbills (Eretmochelys imbricata) by Fischthal and Acholonu (1976). In addition, Pérez-Ponce De León and Brooks (1995) in their phylogenetic analysis on Pronocephalidae transferred Medioporus and Glyphicephalus solidus to Pleurogonius. With our new species, 23 species of Pleurogonius have been described. Of the 22 species of Pleurogonius previously described, only 9 have been reported from the Caribbean Sea. P. chelonii (Gupta, 1961; Greiner et al., 1980), P. longiusculus, P. linearis, P. sindhii, and P. solidus (Santoro et al., 2006) from green turtles, P. longibursatus, P. solidus, and P. trigonocephalus from hawksbills of Cuba (Pérez-Vigueras, 1955), and P. laterouteus, P. linearis, P. puertoricensis, and P. trigonocephalus from hawksbills of Puerto Rico (Fischthal and Acholonu, 1976; Dyer et al., 1995b). Pleurogonius tortugueroi n. sp. differs from all other species of Pleurogonius by having a short oesophagus and oval testes close to lateral posterior limit of the body. It also differs from other Pleurogonius, except P. malaclemys described by Hunter (1961) from the freshwater diamondback terrapin Malaclemys terrapin centrata, by having an ovary between the testes. All other members of the genus have a long oesophagus (more than twice as long as the diameter of the oral sucker), testes placed to some distance from the posterior end, and ovary pretesticular (Blair, 2005). Compared to the other species of Pleurogonius, the new species appears most closely related to P. linearis but differs by body shape, the lappets of head collar close at the cecal bifurcation level, a longer vitelline field, different testis shape and position, ovary intertesticular, and different egg size. Pleurogonius linearis has been collected in Chelonia mydas from Egypt (Looss, 1901), Japan (Oguro,
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1936), Brazil (Ruiz, 1946), and Costa Rica (Santoro et al., 2006). The body size of P. tortugueroi n. sp. (2.1 [1.5-2.4] mm by 0.7 [0.5-0.8] mm) is larger than the P. linearis specimens of Looss (1901), (1.31.4 mm by 0.25-0.3 mm); similar to Oguro (1936), (2.1-2.3 mm by 0.57-0.66 mm); but it is much smaller than specimens reported by Ruiz (1946), (3.65-4.66 mm by 0.93-2.20 mm). The eggs of the new species were 27 (24-30) by 14 (12-17); eggs of Looss (1901) specimens 32×16; Oguro (1936) 3233 ×14-16; Ruiz (1946) 32 (28-36)×18 (15-22). The morphometric data for specimens of P. linearis collected by Santoro et al. (2006) from Chelonia mydas in Costa Rica were not reported by the authors, but are as follows; the body and egg size of those specimens were 1.6 (1.5-1.6) mm by 0.3 mm, and 24×11 (9-12), respectively. Acknowledgments We thank Tortuguero Conservation Area and the Park Rangers for logistic support and facilitating the fieldwork. The manuscript was improved by comments and advices from Mr. Garry Foster, University of Florida. Research activities at the Tortuguero National Park were conducted, under permission 091-2003/2004-OFAU from the Ministry of Environment and Energy, and from the National System of Conservation Areas of Costa Rica.
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