Checklist of the helminth parasites of vertebrates in Costa Rica

Helminth parasites of vertebrates have been studied in Costa Rica for more than 50 years. Survey work on this group of parasites is far from complete. We assembled a database with all the records of helminth parasites of wild and domestic vertebrates in Costa Rica. Information was obtained from different sources such as literature search (all published accounts) and parasite collections. Here we present a checklist with a parasitehost list as well as a host-parasite list. Up to now, 303 species have been recorded, including 81 species of digeneans, 23 monogeneans, 63 cestodes, 12 acanthocephalans, and 124 nematodes. In total, 108 species of vertebrates have been studied for helminths in Costa Rica (31 species of fishes, 7 amphibians, 14 reptiles, 20 birds, and 36 mammals). This represents only 3.8% of the vertebrate fauna of Costa Rica since about 2,855 species of vertebrates occur in the country. Interestingly, 58 species (19.1 %) were recorded as new species from Costa Rica and most of them are endemic to particular regions. Considering the valuable information that parasites provide because it is synergistic with all the information about the natural history of the hosts, helminth parasites of vertebrates in Costa Rica should be considered within any initiatives to accomplish the national inventory of biological resources. Starting with this compilation work, the Colección de Helmintos de Costa Rica (CHCR), hosted at the Facultad de Microbiología, Universidad de Costa Rica, has re-emerged and it is our hope that it will have the standards of quality to assure that it will become the national depository of helminths in the country.

Costa Rica possesses a strong tradition in the study of parasites of domestic and wildlife vertebrates.For more than 50 years the helminth fauna of these hosts has been studied by national parasitologists and microbiologists (see for example Jiménez-Quirós and Brenes-Madrigal 1957, Brenes-Madrigal and Jiménez-Quirós 1959, Brenes-Madrigal et al. 1959a, Brenes-Madrigal et al. 1960a, Brenes-Madrigal and Arroyo-Sancho 1962a y b, Brenes-Madrigal et al. 1966).Since the very beginning in his career, Dr. Rodrigo Brenes-Madrigal, from the Facultad de Microbiología, Universidad de Costa Rica, established a close collaboration with Dr. Eduardo Caballero and his research group from the Instituto de Biología, Universidad Nacional Autónoma de México (UNAM) to contribute to the understanding of the Costa Rican helminth parasite biodiversity and as a result, several papers were published between the late 50´s and early 80´s (see Caballero et al. 1957, Caballero and Brenes-Madrigal 1958, Brenes-Madrigal and Bravo-Hollis 1959, Lamothe-Argumedo and Brenes-Madrigal 1983).A first attempt to compile the information of the helminth parasites of Costa Rica was made by Brenes-Madrigal (1961) who presented up to that year a checklist of about 150 species described as helminth parasites of wild and domestic vertebrates as well as human beings.
However, the extraordinary biological richness of Costa Rica has attracted the attention of several foreign parasitologists who have contributed, more recently, to increase the amount of information about the helminths of vertebrates in Costa Rica and in fact, a group of parasitologists leaded by Dr. Daniel Brooks have developed a research program to inventory the parasites of particular regions of the country, i.e. the Área de Conservación de Guanacaste (ACG), in the province of Guanacaste (further information about the data base of parasites of vertebrates in the ACG can be obtained at: http://brooksweb.zoo.utoronto.ca)(see for example Marques et al. 1996, Pérez-Ponce de León et al. 1998, Brooks et al. 1999, Platt 2000, Zelmer and Brooks 2000, Carreño et al. 2001, León-Régagnon et al. 2001, Choudhury et al. 2002).
Of all the helminth specimens collected from Costa Rican hosts, only a few were saved in the collection of the Facultad de Microbiología, University of Costa Rica and most of them have been deposited in foreign parasite collections, i.e. the Colección Nacional de Helmintos, Mexico City, Mexico, the U.S. National Parasite Collection, Beltsville, Maryland, U.S.A., and in the Harold W. Manter Laboratory of Parasitology, Lincoln, Nebraska, U.S.A., since there was not a national parasite collection in Costa Rica.However, this is changing.Recently, the University of Costa Rica has issued an initiative to support biological collections, among other kind of collections.This interest is completely congruent with the initiative developed by Costa Rica to establish an inventory of the biological diversity within its territory, and to facilitate their efforts to preserve biodiversity.The starting point for planning the conservation and use of biodiversity is the compilation of information through biological surveys and inventories.Biological collections are one of the most important components of this inventory work, considering both the specimens preserved with high standards of quality and the information associated with each specimen (database) (Reaka-Kudla et al. 1997).So the objective of this paper is two-fold, to update all the available information about helminth parasites of vertebrates in Costa Rica, and to set the basis for the re-establishment of the Colección Helmintológica de la Facultad de Microbiología as the Colección de Helmintos de Costa Rica which should have the status of National Collection, and will become the depository of the helminth parasites of vertebrates and invertebrates in the near future, calling the attention to all national and foreign parasitologists, that some of the specimens collected in the country, and their published accounts should be deposited in this re-emerged collection.

MATERIALS AND METHODS
To accomplish the goals of this paper, we conducted a search in two kinds of sources: Parasite collections and bibliographic references.Information from the Colección Nacional de Helmintos in Mexico City, from the U.S. National Parasite Collection, and the Parasitological Collection of the Harold W. Manter Laboratory of Parasitology, University of Nebraska-Lincoln, both in the U.S.A., was obtained with permission of their curators.All records from Costa Rican hosts were then extracted and entered in a database built on Microsoft Access 2000.At the same time, a bibliographical search was conducted in sources such as Helminthological Abstracts and Biological Abstracts.We did put special attention to all published accounts done in Costa Rican journals where some records have also been published.These records were also entered in the database.The database will be available upon request to B.R.O., curator of the Colección de Helmintos de Costa Rica.
The checklist is divided in two parts.First we present a parasite-host list.It is presented in phylogenetic order starting with Platyhelminthes (Digenea, Monogenea and Cestoda), and following with Acanthocephala and Nematoda.Within each phylum and class, families are presented alphabetically and within family, species are also presented in alphabetical order.To allocate species in families we followed taxonomical treatments such as Yamaguti (1963Yamaguti ( , 1971)), Amin (1985Amin ( , 1992)), Schmidt (1986), Khalil et al. (1994), and Anderson et al. (1973-1984).Each record contains the information about the species name, authority and year, habitat, host(s) with the group to which it belongs in parentheses (see symbology section), locality (particular locality when possible and province), and bibliographical reference.In those cases where specimens were deposited in some parasite collection, the collection acronym is mentioned.Finally, in most cases we present notes to point out possible taxonomical changes, synonyms, and new combinations of names.In all cases, we tried to consider the inclusion of the most well accepted taxonomical name following authorities.Most records are made from adults, but when larval forms were recorded, it is pointed out after the parasite name in parentheses.
The second part is the host-parasite list.This list is ordered following a traditional classification of vertebrates (Pisces, Amphibia, Reptilia, Aves, and Mammalia).Within each vertebrate group, host species are presented in alphabetical order, with the list of helminths parasitizing each of them ordered in the same way, indicating the group to which each helminth parasite belongs (see symbology).We used the name of the host as described in the original papers, however we recognize that some of them may have changed after taxonomical revisions or more accurate determinations.
Intestine, Capra hircus (M), NA (Velázquez and Solís 1983).Notes: This species was found in a goat, which had been imported into Costa Rica from the U.S.A. 70.Trypanoxyuris sp.

DISCUSSION
In this checklist we present information of 303 species of helminths parasitizing 108 species of vertebrates in Costa Rica.Helminth species are represented by 81 species of digeneans, 23 of monogeneans, 63 of cestodes, 12 of acanthocephalans, and 124 of nematodes.Strikingly, almost all the records we present herein correspond to adult forms infecting mostly the intestine of their hosts, or habitats such as the liver or lungs.Vertebrates infected with helminths are included in all major groups, such as fishes (including elasmobranchs and teleosts, with 31 species), amphibians (7 species), reptiles (14 species), birds (20 species), and mammals (36 species), including both wildlife and domestic.The largest number of helminth species has been described from Mammals, however this might be an artifact of the sampling since this is the group on which more species have been analyzed for helminths in Costa Rica.Characteristically, most records of helminths are presented as isolated reports describing one species in a particular host, and only a few surveys of the helminth fauna of a particular host have been conducted (see for example Carreño et al. 2001).However, in this checklist we present a comprehensive list of the helminth fauna of each host species when it is available, considering all the published accounts, e.g. the toad Bufo marinus possess a helminthological record of 12 species of helminths, recorded in 12 reports (papers) from 10 localities along its distributional range in Costa Rica.In contrast, the shark Carcharhinus leucas is parasitized with 14 species of helminths in one single locality (Watson and Thorson 1976).
Clearly, the inventory of the helminth parasites of vertebrates in Costa Rica is in its first steps and a large number of species will be described in the next years.So far, only 108 species of vertebrates have been studied for helminths (most of them representing isolated reports and not complete surveys of each host species along its distributional range), and from them, 303 helminth species were recorded.However, only 3.8% of the vertebrate fauna of the country has been studied, considering that there are about 2,855 species of vertebrates in Costa Rica (Janzen 1983, Stiles and Skutch 1989, Bussing 1998).Interestingly, 58 species were recorded as new species from Costa Rica and most of them are endemic to particular regions.This represents approximately 19.1% of endemic species of helminths in vertebrates of Costa Rica.In comparison, after more than 70 years of survey work of helminth parasites of vertebrates in Mexico, approximately 1,632 species of helminths hosted in 947 species of vertebrates have been recorded.Approximately, 20% of the helminth fauna of vertebrates from Mexico has been described so far, according with estimates presented by Pérez-Ponce de León and García-Prieto (2001b).
Considering that every species of vertebrate supports a diverse biota of symbiotic organisms, and that parasites are integral components of biodiversity, we have learned that documenting the diversity of helminth parasites inhabiting vertebrate hosts in Costa Rica (and in any other part of the world) is very important by several reasons.They can act as agents to control and regulate host populations and they can also act as agents of disease representing a threat for domestic and wildlife vertebrates and also a threat for the conservation programs, especially those directed to preserve endangered species and ecosystems.The ecology and evolutionary history of these parasites is tied to that of their hosts, so they can be used as key indicators of ecosystem health, and also as indicators to monitor global change.At the same time, they provide valuable information to the understanding of the biogeographical and coevolutionary history of the association (Gardner and Campbell 1992, Hoberg 1997a, 1997b, Marcogliese and Cone 1997, Overstreet 1997, Brooks and Hoberg 2000, Brooks et al. 2001, Pérez-Ponce de León and García-Prieto 2001a).
There is no doubt about the importance of the helminth parasites as part of the inventory of natural resources in Costa Rica and we would like also to emphasize the important role that these parasites may play as agent of diseases in human beings.Several of the helminths mentioned in the checklist are the cause of some disease that directly causes health problems, or at least the potential exists for some of them to become emerging pathogens (see Morera and Céspedes 1971, Brenes-Madrigal et al. 1974, and Brenes-Madrigal et al. 1983) for cases of human infections with Angiostrongylus costaricensis, Wuchereria bancrofti, and Raillietina sp., respectively).
To summarize, helminth parasites of vertebrates in Costa Rica need to be considered within any initiatives to accomplish the national inventory of biological resources.The information provided by them is synergistic with all the information about the natural history of the hosts that is being assembled from field data and, in addition to that, the risk of emerging diseases will be assessed and probably all the information will be used when decisions to handle and protect biodiversity are taken.In this sense, to build up and preserve a national depository of the specimens (and the information associated to each of them) is a necessary step.Universities and government agencies have to be convinced to support now, and in the future, the establishment of biological collections where all specimens will be saved, so infrastructure and personnel have to be provided to guarantee the quality of the specimens within collections, as well as to provide a service to the society and the scientific community to make sure that the knowledge and the information contained in collections is available for all of them.At this point, the Colección de Helmintos de Costa Rica (CNCR) has re-emerged and we will try to hold the promise that it will have the standards of quality to assure that it will become the national depository of helminths in the country.
Brenes provided some information about localities in Costa Rica.Funds to complete this paper were partially 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".LGP thanks finantial support provided by Fernando Alvarez, Department of Zoology, University of Mexico.
to the genus Urocleidoides Mizelle and Price, 1964 byMolnar et al.