Helminths of Two Species of Frogs, Lithobates taylori and Lithobates vaillanti (Ranidae), From Costa Rica
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1 Caribbean Journal of Science, Vol. 43, No. 1, 65-72, 2007 Copyright 2007 College of Arts and Sciences University of Puerto Rico, Mayagüez Helminths of Two Species of Frogs, Lithobates taylori and Lithobates vaillanti (Ranidae), From Costa Rica STEPHEN R. GOLDBERG 1 AND CHARLES R. BURSEY 2 1 Department of Biology, Whittier College, Whittier, California sgoldberg@whittier.edu 2 Department of Biology, Pennsylvania State University, Shenango Campus, Sharon, Pennsylvania cxb@psu.edu ABSTRACT. Two species of ranid frogs, Lithobates taylori and Lithobates vaillanti, from Costa Rica were examined for helminth parasites. Three species of Digenea, Gorgoderina megacetabularis, Gorgoderina parvicava, Haematoloechus meridionalis and three species of Nematoda, Oswaldocruzia costaricensis, Subulascaris falcaustriformis, Porrocaecum sp. (larvae) were found in Lithobates taylori. All represent new host records. Five species of Digenea, Glypthelmins facioi, Gorgoderina megacetabularis, Haematoloechus meridionalis, Langeronia macrocirra, Loxogenes arcanum, four species of Nematoda, Contracaecum sp. (larvae), Foleyellides striatus, Physaloptera sp. (larvae), Subulascaris falcaustriformis, and two species of Acanthocephala (centrorhynchid and oligacanthorhynchid cystacanths) were found in Lithobates vaillanti. Loxogenes arcanum, Contracaecum sp., Physaloptera sp., oligacanthorhynchid cystacanths represent new host records. KEYWORDS. Lithobates taylori, Lithobates vaillanti, Ranidae, Digenea, Cestoda, Nematoda, Acanthocephala, Costa Rica INTRODUCTION The Peralta frog, Lithobates taylori, (Smith, 1959) is found at scattered localities in humid Atlantic lowlands from eastern Nicaragua to southeastern Costa Rica and in humid premontane and lower montane areas of Costa Rica; Vaillant s frog, Lithobates vaillanti (Brocchi, 1877), is known from the lowlands of the Atlantic versant from southern Veracruz, Mexico to northern Colombia and on the Pacific slope from Ecuador to western Panama with disjunct populations in southern Mexico, western Nicaragua, and northwestern Costa Rica (Savage 2002). To our knowledge, there are no reports of helminths in Li. taylori and 12 reports of helminths in Li. vaillanti (9 from Mexico: Guillén 1992; Léon-Règagnon et al. 1999; Razo-Mendivil et al. 1999; Guillén- Hernández et al. 2000; Pérez-Ponce de León et al. 2000; Goldberg et al. 2002; León- Règagnon and Paredes-Calderon 2002; Paredes-Calderón et al. 2004; Zelmer et al. 2004; 3 from Costa Rica: Zelmer and Brooks 2000; León-Règagnon et al. 2001; Mata- López et al. 2005). The purpose of this paper is to report results of a helminthological 65 survey of Li. taylori and Li. vaillanti from Costa Rica. MATERIALS AND METHODS Ten Li. taylori (mean snout-vent length, SVL = 65.3 mm ± 7.4 SD, range: mm) and five Li. vaillanti (SVL = 84.8 mm ± 12 SD, range: mm) collected in Costa Rica ( ) were borrowed from the herpetology collection of the Natural History Museum of Los Angeles County (LACM), Los Angeles, California and examined for helminths (Appendix 1). These frogs, all from the Costa Rica Expeditions Collection, were originally fixed in 10% formalin, and then stored in 70% ethanol. The body cavity was opened by a longitudinal incision from throat to vent and the digestive tract was excised by cutting across the esophagus and rectum. The esophagus, stomach, small and large intestines were opened longitudinally and examined with a dissection microscope. The liver, lungs, urinary bladder, and body cavity were also searched. Helminths were placed in vials of 70% ethanol for later examination. Nematodes and acanthocephalans were identi-
2 66 S. R. GOLDBERG AND C. R. BURSEY fied after clearing in a drop of undiluted glycerol on a glass slide. Cestodes and trematodes were regressively stained in hematoxylin, dehydrated in graded ethanol and mounted in balsam for study with a compound microscope. Voucher helminths were deposited in the United States National Parasite Collection (USNPC), Beltsville, Maryland (Appendix II). RESULTS Lithobates taylori harbored three species of Digenea, Gorgoderina megacetabularis Mata-López, León-Règagnon and Brooks, 2004, Gorgoderina parvicava Travassos, 1922 and Haematoloechus meridionalis León- Règagnon, Brooks and Zelmer, 2001 and three species of Nematoda, Oswaldocruzia costaricensis Bursey and Goldberg, 2005, Subulascaris falcaustriformis Freitas and Dobbin, 1977 and larvae in cysts of a species of Porrocaecum Railliet and Henry, 1912 (Table 1). Lithobates vaillanti harbored five species of Digenea, Glypthelmins facioi, Brenes, Arroyo, Jiménez-Quirós and Flores, 1959, Go. megacetabularis, H. meridionalis, Langeronia macrocirra Caballero and Bravo Hollis, 1949, Loxogenes arcanum (Nickerson, 1900), four species of Nematoda, Foleyellides striatus (Ochtoterena and Caballero, 1932), S. falcaustriformis, larvae of Contracaecum Railliet and Henry, 1912 and Physaloptera Rudolphi, 1819 and two species of Acanthocephala, cystacanths of the Centrorhynchidae and Oligacanthorhynchidae (Table 1). DISCUSSION Seven species of Digenea limited to anurans were found in this study. Glypthelmins facioi was originally described by Brenes et al. (1959) from a Costa Rican frog identified as Lithobates pipiens, a species now known not to occur in Costa Rica. It was subsequently reported from the Mexican frogs, Leptodactylus melanonotus, Lithobates berlandieri and Li. vaillanti (Razo- Mendivil et al. 1999; Goldberg et al. 2002). Gorgoderina megacetabularis was recently described in Li. vaillanti from Costa Rica by Mata-López et al. (2005) and has been reported in Lithobates vibaricarius by Bursey and Goldberg (2006). Lithobates taylori represents a new host record. Gorgoderina parvicava is widely distributed in Central and South American anurans and is known TABLE 1. Infection site (IS), number (N), prevalence as percentage (P), and mean intensity ±1SD(M±SD)for Lithobates taylori and Lithobates vaillanti from Coast Rica. Host IS N P M ± SD Lithobates taylori (N = 10) Gorgoderina megacetabularis Urinary bladder ± 0.6 Gorgoderina parvicava Urinary bladder ± 6.4 Haematoloechus meridionalis Lungs ± 0.6 Oswaldocruzia costaricensis Small intestine Subulascaris falcaustriformis Small intestine Porrocaecum sp. Coelom Lithobates vaillanti (N = 5) Glypthelmins facioi Small intestine ± 1.4 Gorgoderina megacetabularis Urinary bladder ± 1.4 Haematoloechus meridionalis Lung Langeronia macrocirra Small intestine Loxogenes arcanum Small intestine Foleyellides striatus Coelom ± 0.3 Subulascaris falcaustriformis Stomach ± 0.7 Contracaecum sp. Coelom ± 15.9 Physaloptera sp. Stomach ± 45.9 centrorhynchid cystacanth Coelom oligacanthorhynchid cystacanth Coelom
3 HELMINTHS OF COSTA RICAN FROGS 67 from Chaunus crucifer, Chaunus marinus, Chaunus schneideri, Leptodactylus ocellatus, Leptodactylus pentadactylus, Li. berlandieri, Lithobates palmipes, Li. vaillanti and Pseudis paradoxa (see Prudhoe and Bray 1982; Guillén-Hernández et al. 2000). Lithobates taylori represents a new host record for G. parvicava. Haematoloechus meridionalis was described from Li. vaillanti collected in Costa Rica by León-Règagnon et al. (2001). Lithobates taylori is the second host reported to harbor H. meridionalis. Langeronia macrocirra was originally described by Caballero and Bravo Hollis (1949) from a Mexican frog identified as Li. pipiens, a species now known not to occur in Mexico. It has been reported from the Central American anurans C. marinus, Li. berlandieri, Li. tarahumarae, Li. vaillanti and Lithobates warszewitschii (Guillén 1992; Goldberg et al. 2002) as well as the North American frogs, Lithobates catesbeianus, Li. pipiens and Lithobates sphenocephalus (Babero and Golling 1974). León-Règagnon et al. (2005) reported La. macrocirra in Li. berlandieri from Nuevo León, Mexico. Loxogenes arcanum was originally described as Distomum arcanum by Nickerson (1900) from an undetermined North American frog species (but not Li. catesbeianus) used for laboratory dissections and was later placed in the genus Loxogenes by Stafford (1905). It is known from the North American frogs Li. catesbeianus, Lithobates clamitans and Li. pipiens (McAlpine and Burt 1998). Lithobates vaillanti represents a new host record and Costa Rica is a new locality record for Lo. arcanum. Mesocoelium was established by Odhner (1911) with Mesocoelium sociale (Lühe, 1901) as the type species. Freitas (1958) reassigned Distoma monas Rudolphi, 1819 to Mesocoelium and later (Freitas 1963) revised the genus recognizing 7 valid species with M. monas as the type species. Goldberg et al. (2005) provided a list of hosts for M. monas. Four species of Nematoda reaching maturity in anurans were found. Foleyellides striatus was originally described as Chandlerella striata by Ochoterena and Caballero (1932) from Li. berlandieri and Lithobates montezumae collected in Mexico; it was moved to Foleyellides by Caballero (1935). Foleyellides striatus has been reported from Lithobates forreri, Lithobates magnaocularis, and Li. tarahumarae, all collected in Mexico (Bursey and Goldberg 2001; Goldberg and Bursey 2002). Lithobates vaillanti represents a new host record; Costa Rica is a new locality record for F. striatus. Oswaldocruzia costaricensis was recently described from specimens taken from the intestines of Lithobates cf. forreri collected in Costa Rica (Bursey and Goldberg 2005). Lithobates taylori represents the second reported host for O. costaricensis. Subulascaris falcaustriformis was described by Freitas and Dobbin (1957) from Li. palmipes collected in Brazil and has been reported from Le. melanonotus, Li. magnaocularis and Li. tarahumarae collected in Mexico (Bursey and Goldberg 2001; Goldberg and Bursey 2002; Goldberg et al. 2002). Lithobates taylori and Li. vaillanti represent new host records. Costa Rica is a new locality record for S. falcaustriformis. Four species of helminths, one cestode species and three nematode species, all of these being incapable of completing their life cycles in anurans, were found: proteocephalid plerocercoids in cysts; Contracaecum sp. and Porrocaecum sp. as larvae in cysts; Physaloptera sp. as larvae within the lumen of the digestive system. Species assigned to the Proteocephalidea are primarily parasites of freshwater fishes (Schmidt 1986). García-Altamirano et al. (1993) reported proteocephalid plerocercoids in Lithobates dunni from Mexico. The definitive hosts of species of Contracaecum are piscivorous birds and mammals; larvae hatch in water and are ingested by invertebrate hosts; fish serve as vertebrate intermediate hosts (Anderson 2000). Paredes-Calderón et al. (2004) reported larvae of Contracaecum sp. in Li. vaillanti collected in Mexico. Species of Porrocaecum are parasites of birds, earthworms are the typical intermediate host but small mammals that consume earthworms may serve as paratenic hosts (Anderson 2000). Goldberg et al. (2002) reported larvae of Porrocaecum sp. in Craugastor rhodopis and Le. melanonotus collected in Mexico. Because these larvae were found in cysts, we believe frogs can serve as paratenic hosts for species of Contracaecum
4 68 S. R. GOLDBERG AND C. R. BURSEY TABLE 2. Helminths (reference in parenthesis) reported for Costa Rican species of Lithobates. Helminth L. cf forreri L. taylori L. vaillanti L. vibaricarius L. warszewitschii Digenea Glypthelmins facioi (1) Gorgoderina diaster (2) (2) Gorgoderina megacetabularis (1) (1),(2) (3) Gorgoderina parvicava (1) (2) Haematoloechus meridionalis (1) (1),(4) Haematoloechus parcivitellarius (5) Halipegus eschi (6) Langeronia macrocirra (1) (7) Loxogenes arcanum (1) Megalodiscus temperatus (5) Cestoda Ophiotaenia magna (3) Nematoda Aplectana incerta (5) Aplectana itzocanensis (5) (3) Brevimulticaecum sp. (larvae in cysts) (5) Cosmocerca podicipinus (5) (3) Contracecum sp. (larvae in cysts) (1) Falcaustra costaricae (3) Foleyellides striatus (5) (1) Oswaldocruzia costaricensis (5) (1) Physaloptera sp. (larvae) (1) Porrocaecum sp. (larvae in cysts) (1) Raillietnema lynchi (3) Rhabdias savagei (5) (3) Subulascaris falcaustriformis (5) (1) (1) Acanthocephala Centrorhynchidae gen. sp. (1) (3) Oligacanthorhynchidae gen. sp. (1) 1. This paper; 2. Mata-Lopez et al. 2005; 3. Bursey and Goldberg 2006; 4. Leon-Regagnon et al. 2001; 5. Bursey and Goldberg 2005; 6. Zelmer and Brooks 2000; 7. Brenes et al and Porrocaecum. Larvae of species of Physaloptera (but not adults) are commonly found in anurans. Goldberg et al. (1993) provided an initial list of larvae of Physaloptera sp. in anurans. To that list should be added Anaxyrus kelloggi, C. marinus, Ollotis marmorea, Ollotis mazatlanensis, Dendropsophus microcephalus, Pseudacris regilla, Pachymedusa dacnicolor, Li. forreri, Li. magnaocularis, Li. tarahumarae, and Smilisca baudinii, all from Mexico (Galicia-Guerrero et al. 2000; Goldberg and Bursey 2002; Goldberg et al. 2002). No further development occurs beyond the larval stage and the larvae pass from the digestive tract with the feces. Insects serve as intermediate hosts for species of Physaloptera (Anderson 2000), and any insectivore might therefore at times harbor larvae which we consider an artifact of diet. Two species of acanthocephalans, cystacanths assigned to the Centrorhynchidae and the Oligacanthorhynchidae, were found. Acanthocephalans require at least two hosts in the life cycle; arthropods are the usual intermediate hosts in which the infective stage, the cystacanth develops (Nickol 1985). When eaten by an appropriate final host, the cystacanth excysts and develops to maturity in the digestive tract; in an inappropriate host cystacanths migrate from the digestive tract into the body cavity and again encyst. Centrorhynchid and oligacanthorhynchid cystacanths were previously found in L. vaillanti from Mexico (Goldberg et al. 2002, Paredes-Calderón et al. 2004). Savage (2002) reported 5 species of Lithobates to occur in Costa Rica, namely, Li. for-
5 HELMINTHS OF COSTA RICAN FROGS 69 reri, Li. taylori, Li. vaillanti, Li. vibaricarius, and Li. warszewitschii. More recent work (Zaldívar-Riverón et al. 2004) indicates that the name Li. forreri should be applied only to those populations that occur from southern Sonora south to northern Jalisco, Mexico and that frogs in Costa Rica considered to be Li. forreri represent an undescribed species. We will identify the Costa Rican frog as Li. cf. forreri to separate it from other undescribed Mesoamerican ranids (see Zaldívar-Riverón et al. 2004). Holmes and Price (1986) define a compound helminth community as all species of helminths within a community of host species. The compound helminth community for Costa Rican species of Lithobates is given in Table 2 and currently is composed of 26 species. Further examination of ranid frogs from Cost Rica will no doubt add new helminths to the community list and will indicate more commonality among the hosts. Acknowledgments. We thank David A. Kizirian (Natural History Museum of Los Angeles County) for permission to examine frogs and Amanda Woolsey for assistance with dissections. Ranids are from the CRE collection donated to LACM in 1998 by Jay M. Savage. LITERATURE CITED Anderson, R. C Nematode Parasites of Vertebrates: Their Development and Transmission. 2 nd Edit., Oxon, UK. CABI Publishing Babero, B. B., and K. Golling Some helminth parasites of Nevada bullfrogs, Rana catesbiana Shaw. Rev. Biol. Trop. 21: Brenes, R. R., G.A. Sancho, O. Jiménez-Quirós, and E. D. Flores Helmintos de la República de Costa Rica XIII. Algunos tremátodos de Rana pipiens. Descripción deglypthelmins facioi n. sp. Rev. Biol. Trop. 7: Bursey, C. R., and S. R. Goldberg Falcaustra lowei n.sp. and other helminths from the Tarahumara frog, Rana tarahumarae (Anura: Ranidae), from Sonora, Mexico. J. Parasitol. 87: Bursey, C. R., and S. R. Goldberg New species of Oswaldocruzia (Nematoda: Molineoidae), new species of Rhabdias (Nematoda: Rhabdiasidae) and other helminths in Rana cf. forreri (Anura: Ranidae) from Costa Rica. J. Parasitol. 91: Bursey, C. R., and S. R. Goldberg New Species of Raillietnema (Nematoda: Cosmocercidae) and other helminths in Rana vibicaria (Ranidae) from Costa Rica. Comp. Parasitol. 73: Caballero, E Nemátodos parásitos de los batracios de México. III Cuarta contribución al conocimiento de la parasitología derana montezumae. An. Inst. Biol. Univ. Nac. Autón. México. 6: Caballero, E., and M. Bravo Hollis Description d un nouveau genre de Pleurogeninae (Trematoda: Lecithodendriidae) de grenouilles du Mexique Langeronia macrocirra n. g. n. sp. An. Parasit. Hum. Comp. 24: Freitas, J. F. T Breve nota sôbre o Distoma monas Rudolphi, 1819 (Trematoda). Rev. Brasil. Biol. 18: Freitas, J.F. T Revisão dafamília Mesocoeliidae Dollfus, 1933 (Trematoda). Mem. Instit. Oswaldo Cruz 61: Freitas, J. F. T., and J. E. Dobbin Novo nematódo parasito de Rana palmipes Spix: Subulascaris falcaustriformis g.n. sp. n. (Nematoda, Ascaridoidea). Rev. Brasil. Biol. 17: Galicia-Guerrero, S., C. R. Bursey, S. R. Goldberg, and G. Salgado-Maldonado Helminths of two sympatric toad species, Bufo marinus (Linnaeus) and Bufo marmoreus Wiegmann, 1833 (Anura: Bufonidae) from Chamela, Jalisco, Mexico. Comp. Parasitol. 67: García-Altamirano, I., G. Pérez-Ponce de León, and L. García-Prieto Contribución al conocimiento de la comunidad de helminthos de dos especies de anfibios endémicos del lago de Pátzcuaro, Michoacán: Rana dunni y Ambystoma dumerilii. Cuad. Mex. Zool. 1: Goldberg, S. R., and C. R. Bursey Helminth parasites of seven anuran species from northwestern Mexico. West. N. Amer. Nat. 62: Goldberg, S. R., C. R. Bursey, G. Salgado-Maldonado, R. Báez, and C. Cañeda, Helminth parasites of six species of anurans from Los Tuxtlas and Catemaco Lake, Veracruz, Mexico. Southwest. Nat. 47: Goldberg, S.R., C.R. Bursey, and R. Tawil Gastrointestinal helminths of the western brush lizard, Urosaurus graciosus graciosus (Phrynosomatidae). Bull. Southern Calif. Acad. Sci. 92: Goldberg, S. R., C. R. Bursey, and S. R. Telford, Jr Metazoan endoparasites of four species of lizards, Gehyra mutilata, Hemidactylus frenatus (Gekkonidae), Mabuya cumingi, Mabuya multifasciata (Scincidae), and one species of snake, Ramphotyphlops braminus (Typhlopidae), from the Philippine Islands. Comp. Parasitol. 72: Guillén, H. S Comunidades de helmintos de algunos
6 70 S. R. GOLDBERG AND C. R. BURSEY anuros de Los Tuxtlas, Veracruz. M.Sc. Thesis, Fac. Sci., Univ. Nac, Aut. México, D.F. Guillén-Hernandez, S., G. Salgado-Maldonado, and R. Lamothe-Argumedo Digeneans (Plathelminthes: Trematoda) of seven sympatric species of anurans from Los Tuxtlas, Veracruz, Mexico. Studies of the Neotropical Fauna and Environment 35: Holmes, J. G., and P. W. Price Communities of parasites. In Community Ecology: Pattern and Process. eds. J. Kikkawa and D. J. Anderson, pp Blackwell Scientific Publications, Oxford, U.K. León-Règagnon, V., and E. L. Paredes-Calderón Haematoloechus danbrooksi n. sp. (Digenea: Plagiorchioidea) from Rana vaillanti from Los Tuxtlas, Veracruz, Mexico. J. Parasitol. 88: León-Règagnon, V., D. R. Brooks, and G. Pérez-Ponce de Léon Differentiation of Mexican species of Haematoloechus Looss, 1899 (Digenea: Plagiorchiformes): molecular and morphological evidence. J. Parasitol. 85: León-Règagnon, V., D. R. Brooks, and D. A. Zelmer Morphological and molecular description of Haematoloechus meridionalis n. sp. (Digenea: Plagiorchioidea: Haematoloechidae) from Rana vaillanti Brocchi of Guanacaste, Costa Rica. J. Parasitol. 87: León-Règagnon, V., E. A. Martínez-Salazar, D. Lazcano-Villareal, and R. Rosas-Valdez Helminth parasites of four species of anurans from Nuevo Leon, Mexico. Southwest. Nat. 50: Mata-López, R., V. León-Règagnon, and D. R., Brooks Species of Gorgoderina (Digenea: Gorgoderidae) in Rana vaillanti and Rana cf. forreri (Anura: Ranidae) from Guanacaste, Costa Rica, including a description of a new species. J. Parasitol. 91: McAlpine, D. F. and M. D. B. Burt Taxonomic status of Halipegus spp. (Digenea: Derogenidae) parasitic in the mouth and eustachian tubes of North American and Mexican amphibians. J. Helm. Soc. Wash. 65: Nickerson, W. S Note on Distomum arcanum (n. sp.) in American frogs. Amer. Nat. 34: Nickol, B. B Epizootiology. In Biology of the Acanthocephala. Ed. D. W. T. Crompton, and B. B. Nickol pp Cambridge University Press, Cambridge, UK. Ochoterena, I., and E. Caballero Una nueva filaria parásita de las ranas. An. Inst. Biol. Univ. Nac. Auton. México 3: Odhner, T Nordostafrikanische Trematoden, grössenteils von Weissen Nil. 1. Fascioliden (von der Schweidischen Zoologischen Expedition gesammelt). Results of the Swedish Zoological Expedition to Egypt and the White Nile 1901 under the direction of L. A. Jagerskiöld. No. 23A. Uppsala, Sweden. Paredes-Calderón, L., V. León-Règagnon, and L. García-Prieto Helminth infracommunities of Rana vaillanti Brocchi (Anura: Ranidae) in Los Tuxtlas, Veracruz, Mexico. J. Parasitol. 90: Pérez-Ponce de León, G., V. León-Règagnon, L. García-Prieto, U. Razo-Mendivil and A. Sánchez- Alvarez Digenean fauna of amphibians from central Mexico: Nearctic and Neotropical influences. Comp. Parasitol. 67: Prudhoe, S., and Bray, R.A Platyhelminth Parasites of the Amphibia. British Museum (Natural History), Oxford: Oxford University Press, Oxford, U.K. Razo-Mendivil, U., J.P. Lacelete, and G. Pérez-Ponce de Léon New host and locality records for three species of Glypthelmins (Digenea: Macroderoididae) in anurans of Mexico. J. Helminthol. Soc. Wash. 66: Savage, J. M The amphibians and reptiles of Costa Rica: A herpetofauna between two continents, between two seas. University of Chicago Press, Chicago, Il. Schmidt, G. D Handbook of tapeworm identification. CRC Press, Inc., Boca Raton, FL. Stafford, J Trematodes from Canadian vertebrates. Zool. Anz. 28: Zaldívar-Riverón, A. V. León-Règagnon, and A. Nieto-Montes de Oca Phylogeny of the Mexican coastal leopard frogs of the Rana berlandieri group based on mitdna sequences. Molec. Phylog. Evol. 30: Zelmer, D. A., and D.R. Brooks Halipegus eschi n. sp. (Digenea: Hemiuridae) in Rana vaillanti from Guanacaste Province, Costa Rica. J. Parasitol. 86: Zelmer, D. A., L. Paredes-Calderón, V. León- Règagnon, and L. García-Prieto Nestedness in colonization-dominated systems: Helminth infracommunities of Rana vaillanti Brocchi (Anura: Ranidae) in Los Tuxtlas, Veracruz, Mexico. J. Parasitol. 90: APPENDIX I. Lithobates taylori and Li. vaillanti from Costa Rica, listed by province, borrowed from the Natural History Museum of Los Angeles County (LACM), Los Angeles, California. Lithobates taylori (n = 10). Alajuela: LACM ; Cartago: LACM , , ; San José: LACM Lithobates vaillanti (n = 5). Cartago: LACM ; Guanacaste: LACM ; Heredia: LACM ; Limón: LACM ; San José: LACM APPENDIX II. Helminths from Lithobates taylori and Li. vaillanti deposited in the United States National Parasite Collection (USNPC).
7 HELMINTHS OF COSTA RICAN FROGS 71 Lithobates taylori: Gorgoderina megacetabularis (95185), Gorgoderina parvicava (95186), Haematoloechus meridionalis (95187), Oswaldocruzia costaricensis (95188), Porrocaecum sp. (95189), Subulascaris falcaustriformis (95190). Lithobates vaillanti: Glypthelmins facioi (95191), Gorgoderina megacetabularis (95192), Haematoloechus meridionalis (95193), Langeronia macrocirra (95194), Loxogenes arcanum (95195), Contracaecum sp. (95196), Foleyellides striatus (95197), Physaloptera sp. (95198), Subulascaris falcaustriformis (95199), centrorhynchid cystacanth (95200), oligacanthorhynchid cystacanth (95201).
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