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Helminth Parasites in Freshwater Fish from the Papaloapan River Basin

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Helminth Parasites in Freshwater Fish from the Papaloapan River Basin Parasitol Res (2005) 96: 69–89 DOI 10.1007/s00436-005-1315-9 ORIGINAL PAPER Guillermo Salgado-Maldonado Æ Rogelio Aguilar-Aguilar Guillermina Caban˜as-Carranza Æ Eduardo Soto-Galera Carlos Mendoza-Palmero Helminth parasites in freshwater fish from the Papaloapan river basin, Mexico Received: 8 October 2004 / Accepted: 26 January 2005 / Published online: 6 April 2005 Ó Springer-Verlag 2005 Abstract A checklist based on previously published re- Introduction cords and original data is presented for the helminth parasites reported in 35 fish species from nine families Recent research on the helminth parasites of freshwater from the Rı´o Papaloapan basin, east Mexico. The fish in Mexico’s hydrological basins has increased checklist contains 85 taxa from 39 helminth families. knowledge of the helminth fauna in these areas. To date, Trematodes and nematodes were the most abundant helminth parasite inventories have been published for taxonomic groups. The helminth fauna in the fish of the the freshwater bodies of the Yucata´n Penı´nsula (Mora- Papaloapan River basin predominantly consists of vec et al. 1995a, b; Scholz et al. 1995a, b, 1996b; Sal- Neotropical species that are largely autogenic. The gado-Maldonado et al. 1997; Mendoza-Franco et al. introduced species Centrocestus formosanus was the 1999; Kritsky et al. 2000), the Balsas (Salgado-Maldo- most widely distributed helminth, infecting 16 host nado et al. 2001a), Lerma and Santiago (Salgado- species. Ten of the recorded helminth species have only Maldonado et al. 2001b)andPa´nuco river basins been found in fish from the Papaloapan. This inventory (Salgado-Maldonado et al. 2004a), the Ayuquila River contributes 157 new host records, and reports the pres- in the Sierra de Manantla´n, Jalisco (Salgado-Maldona- ence of 30 helminth species in the Papaloapan for the do et al. 2004b), water bodies in the Sierra Madre Or- first time . This inventory shows the richness of helminth iental (Aguilar-Aguilar et al. 2004), and the lowlands in parasite species in the fish of the Papaloapan River basin the state of Tabasco drained by the Grijalva–Usumac- in comparison with the other hydrological basins in inta system (Salgado-Maldonado et al. 2005). Helminth Mexico. It also demonstrates that this fauna is typically inventories have also been published for some fish Neotropical and quite similar to that from the neigh- families, particularly for the cichlids (Salgado-Maldo- boring basins of the Grijalva–Usumacinta system and nado et al. 1997; Vidal-Martı´nez et al. 2001a), poecilids the Yucatan Peninsula. The data also suggest highly and goodeids (Pineda-Lo´pez et al. 2005). Information effective transmission between environments within the on the nematodes of freshwater fish in the Neotropics same basin and that the regional parasite fauna is has been addressed by Moravec (1998). Two zoogeo- strongly influenced by fish community composition. graphic treatments aid in systematizing the knowledge generated on the distribution, richness and endemic areas of helminths in freshwater fish in Mexico (Vidal- Martı´nez and Kennedy 2000; Aguilar-Aguilar et al. 2003b). Notwithstanding, the helminth fauna data for G. Salgado-Maldonado (&) Æ R. Aguilar-Aguilar fish from the Papaloapan River, one of the largest and G. Caban˜ as-Carranza Æ C. Mendoza-Palmero most important watercourses in Mexico, are still scat- Instituto de Biologı´a, tered, mostly in taxonomic publications. Universidad Nacional Auto´noma de Me´xico, The Papaloapan River basin is the second largest Apartado Postal 70-153, 04510 Me´xico, Mexico E-mail: [email protected] hydrological basin in Mexico and is considered the northern limit of the Neotropical Region. It includes a E. Soto-Galera 46,517 km2 area in the states of Veracruz, Oaxaca and Laboratorio de Ictiologı´a y Limnologı´a, Escuela Nacional de Ciencias Biolo´gicas, Puebla (17°N–19°N; 95°W–97°40¢W) (Revel-Mouroz Instituto Polite´cnico Nacional, Carpio y Plan de Ayala, 1980). The rivers feeding the Papaloapan generally flow Santo Toma´s, 11340 Me´xico, Mexico to the east. These tributaries include the Rı´o Cajones, 70 Rı´o de la Lana, Rı´o Grande–Santo Domingo, Rı´o San ertsoni (Cichlidae, 3); C. urophthalmus (Cichlidae, 10); Juan, Rı´o Tesechoaca´n, Rı´o Tonto, Rı´o Valle Nacional Cichlasoma sp. (Cichlidae, 27); Oreochromis sp. (Cichli- and Rı´o Jaltepec. The Papaloapan flows into the Gulf of dae, 3); Petenia splendida (Cichlidae, 1); Eleotris sp. Mexico at the Laguna de Alvarado in the state of (Eleotridae, 6); Dormitator maculatus (Eleotridae, 47); Veracruz. The Papaloapan basin can be divided into two Gobiomorus dormitor (Eleotrididae, 50); Dorosoma anale sections: the Upper Papaloapan, which includes waters (Clupeidae, 2), D. petenense (Clupeidae, 16); Heterandria above 1,000 m asl, and the Lower Papaloapan. Los bimaculata (Poeciliidae, 70); *Poecilia catemaconis Tuxtlas area in Veracruz, forms part of the Lower (Poeciliidae, 25); P. mexicana (Poeciliidae, 319); Papaloapan, even though it does have areas higher than P. reticulata (Poeciliidae, 34); *Poeciliopsis catemaco 1,000 m asl. (Poeciliidae, 24); Poeciliopsis gracilis (Poeciliidae, 35); A total of 44 fish species are known in the lotic and Poeciliopsis sp. (Poeciliidae, 13); Xiphophorus helleri lentic waters of the Papaloapan River basin of which ten (Poeciliidae, 68); Ophisternon aenigmaticum (Synbran- are endemic to it (Sevilla 1977; Miller 1986; Miller and chidae, 42); Rhamdia guatemalensis (Pimelodidae, 48); Smith 1986; Espinosa-Pe´rez et al. 1998). It is an ich- Sycidium gymnogaster (Gobiidae, 11). Fish sample size thyologic fauna characteristic of lowland tropical Mex- per site are given in Table 2. We sampled localities in the ico, and towards the east, it mixes with the ichthyologic Upper Papaloapan; including irrigation channels, fauna of the Usumacinta River. streams and secondary rivers, and localities in the main Studies of the parasites of the fish in the Papaloapan Rı´o Grande and Rı´o Valle Nacional. Sampling localities basin began in 1954 and are largely taxonomic treat- of the Lower Papaloapan include streams and large ments concentrating mostly on fish in the Los Tuxtlas rivers’ tributaries to the main Papaloapan course. The area and particularly Catemaco Lake, Veracruz (Cabal- principal trend of the Rı´o Papaloapan was sampled near lero and Winter 1954; Lamothe-Argumedo 1974, 1977; the Tlacotalpan village. Several streams and lakes at Los Lamothe-Argumedo and Ponciano-Rodrı´guez 1986; Tuxtlas region were also sampled (Table 1, Fig. 1). Caballero-Deloya 1977; Salgado-Maldonado 1978; Sal- Fish at each site were captured using a DC Backpack gado-Maldonado et al. 1992, 1998; Garcı´a-Prieto 1990; Electrofishing device, using gill nets, or by angling. Garcı´a-Prieto et al. 1996;Pe´rez et al. 1992; Jime´nez- Captured fish were taken alive to the laboratory and Garcı´a 1993; Moravec 1998; Moravec et al. 1998, 2000, were examined within 24 h using standard procedures. A 2002a, b; Caspeta-Mandujano et al. 1999, 2000a, b; complete examination for helminth parasites was done Scholz and Salgado-Maldonado 2000, 2001; Scholz et al. of each specimen. External surfaces including scales, 2001b;Pa´ez-Rodrı´guez et al. 2002; Aguilar-Aguilar et al. skin, and fins were examined for ectoparasites using a 2003a; Mendoza-Franco et al. 2003b). More recent stereomicroscope. Gills arches were examined individu- studies addressing the role of freshwater fishes as trans- ally. Examination for monogeneans was done immedi- mitters of the human gnathostomiasis have been done in ately after the fish were taken out of water. The buccal the Temascal Reservoir, Oaxaca (Almeyda-Artigas 1991; cavity, opercula, and eyes were examined separately. Almeyda-Artigas et al. 1995; Lamothe-Argumedo 1977; The external surfaces of the internal organs (heart, liver, Lamothe-Argumedo et al. 1989). No other water bodies spleen, gall bladder, digestive tract, gonads, swim blad- in this basin have been studied. In response, the present der and kidney, as well as the entire body cavity and study brings together previously published information mesentery) were inspected for free or encapsulated par- and provides new data derived from our own research to asites, and then separated and examined individually. update the knowledge of the helminth parasites of the The intestine was opened longitudinally. The liver, fish of the Papaloapan River basin. spleen, kidney, and heart were compressed between glass plates and were examined for parasites. The body mus- culature was removed from the vertebral column, the Materials and methods skin removed from the fillets, and the fillets compressed between glass plates and inspected for helminths using a A review of the literature dealing with freshwater fish stereomicroscope. All collected helminths were sorted by helminth parasites in the Papaloapan River basin was taxon, cleaned and counted by organ. Trematodes (adult made. In addition, a total of 1,088 fish was collected and metacercariae), monogeneans, cestodes (adults and from 25 sites (Table 1, Fig. 1) in the Papaloapan River metacestodes), and nematodes were fixed in hot 4% basin between March 1999 and July 2002. The following formalin. Acanthocephalans were placed in distilled fish species were examined (family and sample size, n, water, refrigerated overnight (6–12 h) to evert the pro- follow each taxon parenthetically, taxa marked * are boscis, and then fixed in hot 4% formalin. Trematodes, endemic to the Rı´o Papaloapan basin as stated by Miller monogeneans, cestodes, and acanthocephalans were 1986; Miller and Smith 1986; Espinosa-Pe´rez et al. stained with Mayer’s paracarmine or Ehrlich’s haemat- 1993): Agonostomus monticola (Mugilidae, 17); Astyanax oxylin, dehydrated using a graded alcohol series, cleared aeneus (Characidae, 125); *Bramocharax caballeroi in methyl salicylate, and mounted whole. To study (Characidae, 10); *Atherinella ammophila (Atherinidae, sclerotized parts, several specimens of each species of 9); *Cichlasoma ellioti (Cichlidae, 2); *C. fenestratum monogenean were fixed following Malmberg’s semiper- (Cichlidae, 67); C.
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