Beatriz Rodríguez-Ortíz ¹, Luis García-Prieto ², Jonathan Herrera-Vázquez ¹ & Gerardo Pérez-Ponce de León ²

1 Laboratorio de Helmintología, Facultad de Microbiología, Universidad de Costa Rica, San José, Costa Rica, e-mail: brodrigu@cariari.ac.ucr.cr; jonnathan@biologia.ucr.ac.cr

2 Laboratorio de Helmintología, Instituto de Biología, UNAM. Ap. Postal 70-153. C.P. 04510, México D.F., e-mail: ppdleon@servidor.unam.mx; gprieto@ibiologia.unam.mx

Received 22-II-2004. Corrected 01-III-2004. Accepted 01-III-2004.

In this work, we present an addendum to the "Checklist of the helminth parasites of vertebrates in Costa Rica" with a parasite-host list as well as a host-parasite list. This addendum updates the available information on this group of parasites in Costa Rica, since very recently a new input has been made to describe the helminth fauna of vertebrates, particularly at the Área de Conservación de Guanacaste. In this paper, we add 33 records, representing 23 species. This raises the number of helminth species described in vertebrates from Costa Rica to 325, represented by 89 species of digeneans, 23 of monogeneans, 63 of cestodes, 13 of acanthocephalans, and 137 of nematodes. In total, 133 species of vertebrates have been studied for helminths in Costa Rica (31 species of fishes, 7 amphibians, 18 reptiles, 40 birds, and 37 mammals). Currently, 67 species (20.6 %) have been recorded as new species from Costa Rica and most of them are endemic to particular regions. The Colección de Helmintos de Costa Rica, housed at the Universidad de Costa Rica (UCR), San José, is the depositary of only 23% of the species recorded so far; however this situation is changing and people recognizes.

Key Words: Helminths, Costa Rica, Biodiversity, Biological inventories, Parasites, Vertebrates.

The checklist of helminth parasites of vertebrates in Costa Rica, published recently (Rodríguez-Ortiz et al. 2004), updated all the available information about helminth parasites of vertebrates in Costa Rica along the past 50 years. Notwithstanding, the inventory of all eukaryotic parasites of the species of vertebrates living within the Área de Conservación Guanacaste, Costa Rica, started in 1996 by Daniel R. Brooks and co-workers, has produced a great dealt of information in the last two years. For this reason, we present this addendum, in order to compile all this information and some other available records, all of them will be available electronically in 2004 at www.chcr.ucr.ac.cr.

Refer to Rodríguez-Ortiz et al. (2004).

This addendum to the checklist contains records of 23 species included in 17 genera of helminths (9 digeneans, 1 acanthocephalan and 13 nematodes). 14 of them represent new species and 4 new genera. Helminths were reported in 25 species of vertebrates not previously studied in Costa Rica. Likewise, we add some taxonomic remarks made in recent publications on 5 species included in the original checklist. Next, we present the information for each species of helminth.

Symbology: B= bird; M= mammal; R= reptile; NA= information not available; CHCR refers to the Colección de Helmintos de Costa Rica, San José, Costa Rica; HWML to the Harold W. Manter Laboratory of Parasitology, University of Nebraska State Museum, Lincoln, Nebraska, U.S.A.; USNPC to the U.S. National Parasite Collection, Beltsville, Maryland, U.S.A.

1. Bakkeius moragai Zamparo, Brooks and Causey, 2003 Gallbladder, intestine, Gymnopithys leucaspis (B), Estación San Gerardo, Guanacaste, Henicorhina leucosticta, Phaenostictus mcleannani, Thryothorus pleurostictus (B), Maritza and Sendero la Parcela, Guanacaste (Zamparo et al. 2003b). Specimens: CHCR, USNPC.

2. Pojmanskia riosae Zamparo, Brooks and Causey, 2003 Intestine, gallbladder, Thryothorus pleurostictus (B), Cafetal, Guanacaste, Caryothraustes poliogaster, Euphonia hirudinacea, Morococcyx erythropygius, Platyrinchus coronatus, Thryothorus nigricapillus, (B), Estación San Gerardo, Guanacaste (Zamparo et al. 2003b). Specimens: CHCR, USNPC.

Notes: Both genus were not assigned to any of the families within the Brachylaimoidea.

Brachycoeliidae (Looss, 1899)
Johnston, 1912

3. Mesocoelium monas (Rudolphi, 1819) Teixeira de Freitas, 1958 Intestine, Norops limifrons (R), Hacienda La Suerte, Limón (Bursey and Goldberg 2003). Specimens: HWML.

Notes: Bursey and Goldberg (2003) refers the record of Mesocoelium travassosi realized by Caballero and Brenes-Madrigal (1958) in toads from Costa Rica to the species M. monas. Both species were synonymyzed by Teixeira de Freitas (1963).

4. Tinamutrema canoae Zamparo, Brooks and Causey, 2003 Cloaca, Crypturellus cinnamomeus (B), Finca Jenny, Guanacaste (Zamparo et al. 2003a). Specimens: CHCR, USNPC.

Cyclocoeliidae
Kossack, 1911

5. Neohaematotrephus arayae Zamparo, Brooks, Causey and Rodríguez, 2003 Body cavity, Jacana spinosa (B), Laguna Los Jícaros, Guanacaste (Zamparo et al. 2003d). Specimens: CHCR, USNPC.

Macroderoididae
McMullen, 1937

6. Parallopharynx gonzalezi Brenes-Madrigal, Arroyo-Sancho and Montero- Gei, 1960 Intestine, Ctenosaura quinquecarinata (R), Cuajiniquil, Guanacaste (Zamparo et al. 2004b). Specimens: CHCR, USNPC.

7. P. matternae Zamparo, Brooks, Tkach and Rodríguez, 2004 Intestine, Basiliscus basiliscus (R), Río Tempisquito, Guanacaste (Zamparo et al. 2004b). Specimens: CHCR, USNPC.

Prosthogonimidae (Lühe, 1909) ]]> Lahille, 1922

8. Whallwachsia illuminata Zamparo, Brooks and Causey, 2003 Bile duct, intestine, Amazilia saucerrottei (B), Cafetal, Guanacaste, Tolomomyias sulphurescens (B), main entrance to Santa Rosa, Parcela Principe, Estación San Gerardo, Guanacaste (Zamparo et al. 2003c). Specimens: CHCR, USNPC.

Urotrematidae
Poche, 1926

9. Urotrema shirleyae Zamparo, Brooks, and Tkach, 2004 Intestine, Norops oxylophus (R), Santa Rosa, Guanacaste (Zamaparo et al., 2004a). Specimens: CHCR, USNPC.

1. Acanthocephalus saurius Bursey and Goldberg, 2003 Intestino, Norops limifrons (R), Hacienda La Suerte, Limón (Bursey and Goldberg 2003). Specimens: HWML.

Acuariidae Seurat, 1913

1. Acuariidae gen. sp. (larvae) Stomach wall, Norops limifrons (R), Hacienda La Suerte, Limón (Bursey and Goldberg 2003). Specimens: HWML.

2. Acuaria mayori Lent, Teixeira de Freitas and Proenca, 1945 Gizzard, Myiarchus nuttingi (B), Cafetal and Quebrada Costa Rica, Guanacaste (Zhang et al. 2003a). Specimens: USNPC.

3. A. wangi Zhang, Brooks and Causey, 2003 Gizzard, Gymnipithys leucaspis and Hylophylax naevioides (B), Estación San Gerardo, Guanacaste (Zhang et al. 2003a). Specimens: USNPC.

4. Syncuaria mycteriae Zhang, Brooks and Causey, 2003 Gizzard, Mycteria americana (A), Santa Rosa, Guanacaste (Zhang et al. 2003b). Specimens: USNPC.

5. Synhimantus (Dispharynx) nasuta Zhang, Brooks and Causey, 2004. Craw, Thraupis episcopus (B), Estación San Gerardo, Guanacaste (Zhang et al. 2004a). Specimens: CHRC, USNPC.

Habronematidae (Chitwood y Wehr, 1932)
Ivaschkin, 1961

6. Procyrnea mawsonae Zhang, Brooks and Causey, 2004 Craw, Buteo magnirostris (B), Cafetal, Guanacaste (Zhang et al. 2004b). Specimens: CHCR, USNPC.

Hetarkidae
Railliet and Henry, 1912

8. Strongyluris panamensis Bursey, Goldberg and Telford, 2003 Intestine, Norops limifrons (R), Hacienda La Suerte, Limón (Bursey and Goldberg 2003). Specimens: HWML. Onchocercidae (Leiper, 1911)

9. Litomosoides sp. ND, Artibeus jamaicensis (M), NA (Bain et al. 2002).

10. L. brasiliensis Almeida, 1936 Body cavity, Carollia perspicillata azteca (M), Santa Ana, San José (Bain et al. 2003). Specimens: CHCR.

Notes: Bain et al. (2003) identified this species based on fragments of females includes among type specimens of L. peñai.

11. Piratuba digiticauda Lent and Teixeira de Freitas, 1941 Body cavity, Norops limifrons (R), Hacienda La Suerte, Limón (Bursey and Goldberg 2003). Specimens: HWML. Seuratidae (Hall, 1916) Railliet, 1906

12. Skrjabinura mesamericana Zhang and Brooks, 2004. Intestine, Calocitta formosa (B), Estación San Gerardo, Guanacaste (Zhang and Brooks, 2004). Specimens: CHCR, USNPC.

13. S. vali (Guerrero, 1971) Caecum, Myiarchus tyrannulus, Piaya cayana (B), Cafetal, Guanacaste (Zhang and Brooks, 2004). Specimens: CHCR, USNPC.

Taxonomic remarks on the status
of some of the species of helminths
from Costa Rica vertebrates

Digenea (Van Beneden, 1858)
Cyclocoeliidae
Kossack, 1911

1. Uvitellina facioi (Brenes-Madrigal and Arroyo- Sancho 1962) Aerial sacs, Jacana spinosa (B), Aranjuez, Puntarenas (Brenes-Madrigal and Arroyo- Sancho 1962). Specimens: CHCR.

Notes: this species was originally described as Cyclocoelum facioi Brenes-Madrigal and Arroyo- Sancho 1962, included in the genus Haematotrephus Stossich, 1902 by Yamaguti (1971) and finally transferred to Uvitellina Witenberg, 1923 by Zamparo et al. (2003d).

2. Langeronia macrocirra Caballero and Bravo-Hollis, 1949 Intestine, Bufo marinus and Rana warche-witschii (N), Corís, Cartago (Brenes-Madrigal et al. 1959). Specimens: CHCR.

Notes: specimens originally determined as L. macrocirra, were transferred to L. provitellaria by Christian (1970) and later re-established as L. macrocirra by Martínez-Salazar (2004) who re-examined voucher specimens deposited in CHCR.

3. Mathevotaenia didelphidis (Rudolphi, 1819) Spasskii, 1951 Intestine, Marmosa sp. (M), Río Grande de Atenas, Alajuela (Flores-Barroeta et al. 1961).

Notes: this species was originally recorded as Oochoristica didelphidis (Rudolphi, 1819). Campbell et al. (2003) pointed out that these specimens differ from the original description of M. didelphidis and probably represent a distinct species.

4. M. pennsylvanica (Chandler and Melvin, 1951) Yamaguti, 1959 Intestine, Didelphis marsupialis etensis (M), Bello Horizonte, Escazú, San José (Flores-Barroeta et al. 1958). Specimens: CNHE.

Notes: originally recorded as Oochoristica pennsylvanica Chandler and Melvin, 1951. Campbell et al. (2003) pointed out that description of specimens from Costa Rica differ from the original description of M. pennsylvanica in several traits.

Nematoda (Rudolphi, 1808)
Onchocercidae (Leiper, 1911)

5. Litomosoides hamletti peñai (Jiménez-Quirós and Arroyo-Sancho, 1960) Body cavity, Carollia perspicillata azteca (=Hemiderma perspicillata) (M), Santa Ana, San José (Jiménez-Quirós and Arroyo-Sancho 1960). Specimens: CHCR.

Notes: Bain et al. (2003) analyzed the type material of Litomosoides peñai and proposed the subspecific status for this species.

After June, 2002, when we finished the compilation of the original "Checklist of the helminth parasites of vertebrates in Costa Rica" (Rodríguez-Ortíz et al. 2004), 14 papers have been published with new records on the helminth fauna of Costa Rican vertebrates (particularly in the Área de Conservación de Guanacaste). In these studies, 23 additional species of helminths parasitizing 25 species of vertebrates have been described. About 76% of these new material was deposited in the CHCR. This fact establish a new era for the Colección de Helmintos de Costa Rica, since this collection will become a primary repository for parasite biodiversity in the country. To summarize, up to date 325 helminth species have been described in vertebrates from Costa Rica, represented by 89 species of digeneans, 23 of monogeneans, 63 of cestodes, 13 of acanthocephalans, and 137 of nematodes. We encourage people describing helminth parasites of this country to send specimens to be deposited and saved in this re-emerged collection.

To Daniel R. Brooks for providing information form their databases. Funds to complete this paper were provided by the agreement between the Universidad de Costa Rica and the Instituto Mexicano de Cooperación Internacional through the project: "Support to catalog and maintain the Helminthological collection of the University of Costa Rica".

En este trabajo presentamos una addenda al "Listado de helmintos parásitos de vertebrados de Costa Rica". Esta addenda actualiza la información disponible acerca de este grupo de parásitos en dicho país, cuyo estudio recientemente ha tomado un nuevo impulso. En este trabajo, se adicionan 33 registros, representando 23 especies. Lo anterior eleva el número de especies de helmintos parásitos de vertebrados de Costa Rica registrado hasta ahora a 325: 89 especies de digéneos, 23 de monogéneos, 63 de céstodos, 13 de acantocéfalos, y 137 de nemátodos. En total, 133 especies de vertebrados han sido estudiadas en busca de helmintos en Costa Rica (31 especies de peces, 7 de anfibios, 18 de reptiles, 40 de aves, y 37 de mamíferos). Hasta la fecha, 67 especies (20.6 %) fueron descritas como nuevas en Costa Rica y muchas de ellas son endémicas a una región particular. La Colección de Helmintos de Costa Rica, localizada en la Universidad de Costa Rica (UCR) en San José, resguarda material de únicamente el 23% de las especies registradas para el país, pero afortunadamente esto está cambiando actualmente.

Bain, O., S. Babayan, J. Gomes, G. Rojas & R. Guerrero. 2002. First account on the larval biology of a Litomosoides filaria, from a bat. Parassitol. 44: 89-92.        [ Links ]

Bain, O., R. Guerrero, B. Rodríguez, S. Babayan & N. Jouvenet. 2003. Examination of type material of two species of Litomosoides (Filaroidea: Onchocercidae), parasites from bats; taxonomic consequences. Parasite. 10: 211-218.        [ Links ]

Brenes-Madrigal, R. & G. Arroyo-Sancho. 1962. Helmintos de la República de Costa Rica XX. Algunos tremátodos de aves silvestres. Rev. Biol. Trop. 10: 205-227.        [ Links ]

Brenes-Madrigal, R., G. Arroyo-Sancho & E. Delgado-Flores. 1959. Helmintos de la República de Costa Rica XI. Sobre la validez del género Langeronia Caballero y Bravo, 1949 (Trematoda: Lecithodendriidae) y hallazgo de Ochetosoma miladelarocai Caballero y Vogelsang, 1947. Rev. Biol. Trop. 7: 81-87.        [ Links ]

Bursey, C.R. & S.R. Goldberg. 2003. Acanthocephalus saurius n. sp., (Acanthocephala: Echinorhynchidae) and other helminths from the lizard Norops limifrons (Sauria: Polychrotidae) from Costa Rica. J. Parasitol. 89: 573-576.        [ Links ]

Caballero, C.E. & R. Brenes-Madrigal. 1958. Helmintos de la República de Costa Rica VII. Tremátodos de algunos vertebrados salvajes, con descripción de una nueva especie de Acanthostomum Looss, 1899. An. Inst. Biol. Univ. Nac. Autón. Méx. 29: 165-179.        [ Links ]

Campbell, M.L., S.L. Gardner & G.T. Navone. 2003. A new species of Mathevotaenia (Cestoda: Anoplocep-halidae) and other tapeworms from marsupials in Argentina. J. Parasitol. 89: 1181-1185.        [ Links ]

Christian, A.F. 1970. Langeronia parva sp. n. (Trematoda: Lecithodendriidae) with revision of the genus Langeronia Caballero and Bravo-Hollis, 1949. J. Parasitol. 56: 321-324.        [ Links ]

Flores-Barroeta, L., E. Hidalgo-Escalante & R. Brenes-Madrigal. 1958. Céstodos de Vertebrados IV. Rev. Biol. Trop. 6: 55-78.        [ Links ]

Flores-Barroeta, L., E. Hidalgo-Escalante & F. Montero-Gei. 1961. Céstodos de vertebrados. VIII. Rev. Biol. Trop. 9: 187-207.        [ Links ]

Jiménez-Quirós, O. & G. Arroyo-Sancho. 1960. Helmintos de la República de Costa Rica. XV. Nematoda 3. Presencia de Litomosoides peñai n. sp. en Hemiderma perspicillata aztecum (Saussure, 1860). Rev. Biol. Trop. 8: 63- 67.        [ Links ]

Martínez-Salazar, E.A. 2004. Estudio taxonómico de algunas poblaciones del género Langeronia Caballero y Bravo-Hollis, 1949 (Trematoda: Lecithodendriidae) en México. Tesis de Maestría, Universidad Nacional Autónoma de México, México D.F., México.         [ Links ]

Rodríguez-Ortiz, B., L. García-Prieto & G. Pérez-Ponce de León. 2004. Checklist of the helminth parasites of vertebrates in Costa Rica. Rev. Biol.Trop. 52 (Supl.1): 1-41.        [ Links ]

Teixeira de Freitas, J. F. 1963. Revisao de Familia Mesocoelidae Dollfus, 1933. Mem. Inst. Oswaldo Cruz. 61: 177-311.        [ Links ]

Zamparo, D., D.R. Brooks & D. Causey. 2003a. Tinamutrema canoae n. gen. n. sp. (Trematoda: Digenea: Strigeiformes: Brachylaimidae) in Crypturellus cinnamomeus (Aves, Passeriformes, Tinamidae) from the Area de Conservación Guanacaste, Costa Rica. J. Parasitol. 89: 819-822.        [ Links ]

Zamparo, D., D.R. Brooks & D. Causey. 2003b. Bakkeius moragai n. gen. n. sp. and Pojmanskia riosae n. gen. n. sp. (Trematoda: Digenea: Brachylaimoidea) in birds from the Area de Conservación Guanacaste, Costa Rica. J. Parasitol. 89: 823-828.        [ Links ]

Zamparo, D., D.R. Brooks & D. Causey. 2003c. Wallwachsia illuminata n. gen., n. sp. (Trematoda: Digenea: Plagiorchiformes: Prosthogonimidae) in the steely-vented hummingbird Amazilia saucerrottei (Aves: Apodiformes: Trochilidae) and the yellow-olive fly-catcher Tolmomyias sulphurescens (Aves: Passeriformes: Tyraninidae) from the Area de Conservación Guanacaste, Guanacaste, Costa Rica. J. Parasitol. 89: 814-818.        [ Links ]

Zamparo, D., D.R. Brooks, D. Causey & B. Rodríguez. 2003d. Neohaematotrephus arayae n. sp. (Digenea: Echinostomiformes: Cyclocoelidae) in Jacana spinosa (Aves: Charadriiformes: Jacanidae) from the Area de Conservación Guanacaste, Costa Rica. J. Parasitol. 89: 829- 831.        [ Links ]

Zamparo, D., D.R. Brooks & V. Tkach. 2004a. A new species of Urotrema (Digenea: Plagiorchiformes: Urotrematidae) in Norops oxylophus (Squamata) from the Area de Conservación Guanacaste, Costa Rica. J. Parasitol. 90: in press.         [ Links ]

Zamparo, D., D.R. Brooks, V. Tkach & B. Rodriguez. 2004b. Parallopharynx matternae n. sp. (Trematoda: Digenea: Plagiorchiidae) in Basiliscus basiliscus (Squamata: Iguania: Corytophanidae) from the Area de Conservación Guanacaste, Guanacaste, Costa Rica. J. Parasitol. 90: in press.        [ Links ]

Zhang, L. & D.R. Brooks. 2004. Skrjabinura mesoamericana n. sp. (Nematoda: Seuratoidea: Seuratidae) in birds from the Area de Conservación Guanacaste, Costa Rica. J. Parasitol. 90: in press.        [ Links ]

Zhang, L., D.R. Brooks & D. Causey. 2003a. Two species of Acuaria Bremser, 1811 (Nematoda: Acuarioidea: Acuariidae) in Passerine birds from the Area de Conservación Guanacaste, Costa Rica. J. Parasitol. 89: 1039- 1043.        [ Links ]

Zhang, L., D.R. Brooks & D. Causey. 2003b. A new species of Syncuaria Gilbert, 1927 (Nematoda: Acuarioidea: Acuariidae) in the wood stork, Mycteria americana L. (Aves: Ciconiiformes: Ciconiidae) from the Area de Conservación Guanacaste, Costa Rica. J. Parasitol. 89: 1034-1038.        [ Links ]

Zhang, L., D.R. Brooks & D. Causey. 2004a. Two species of Synhimantus (Dispharynx ) Railliet, Henry and Sisoff, 1912 (Nematoda: Acuarioidea: Acuariidae) in passerine birds from the Area de Conservación Guanacaste, Costa Rica. J. Parasitol. 90: in press.         [ Links ]

Zhang, L., D.R. Brooks & D. Causey. 2004b. Procyrnea Chabaud, 1958 (Nematoda: Habronematoidea: Habronematidae) in birds from the Area de Conservación Guanacaste, Costa Rica. J. Parasitol. 90: in press.        [ Links ]

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