Helminths of Freshwater Fishes from the Metztitlán Canyon Reserve of the Biosphere, Hidalgo, Mexico

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<ul><li><p>BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofitpublishers, academic institutions, research libraries, and research funders in the common goal of maximizing access tocritical research.</p><p>Helminths of Freshwater Fishes from the Metztitln CanyonReserve of the Biosphere, Hidalgo, MexicoAuthor(s): Scott Monks , Vctor Rafael Zrate-Ramrez , Griselda Pulido-FloresSource: Comparative Parasitology, 72(2):212-219. 2005.Published By: The Helminthological Society of WashingtonDOI: http://dx.doi.org/10.1654/4139URL: http://www.bioone.org/doi/full/10.1654/4139</p><p>BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in thebiological, ecological, and environmental sciences. BioOne provides a sustainable onlineplatform for over 170 journals and books published by nonprofit societies, associations,museums, institutions, and presses.</p><p>Your use of this PDF, the BioOne Web site, and all posted and associated contentindicates your acceptance of BioOnes Terms of Use, available at www.bioone.org/page/terms_of_use.</p><p>Usage of BioOne content is strictly limited to personal, educational, and non-commercialuse. Commercial inquiries or rights and permissions requests should be directed to theindividual publisher as copyright holder.</p><p>http://dx.doi.org/10.1654/4139http://www.bioone.org/doi/full/10.1654/4139http://www.bioone.orghttp://www.bioone.org/page/terms_of_usehttp://www.bioone.org/page/terms_of_use</p></li><li><p>Helminths of Freshwater Fishes from the Metztitlan Canyon Reserveof the Biosphere, Hidalgo, Mexico</p><p>SCOTT MONKS,1,3 VICTOR RAFAEL ZARATE-RAMIREZ,2 AND GRISELDA PULIDO-FLORES1</p><p>1 Universidad Autonoma del Estado de Hidalgo, Centro de Investigaciones Biologicas, Ciudad Universitaria,</p><p>Apdo. Postal 1-69, Pachuca, CP 42001, Hidalgo, Mexico (e-mail: smonks@uaeh.edu.mx; gpulido@uaeh.edu.mx) and2 El Colegio de la Frontera Sur-Unidad Chetumal, Avenida Centario Km. 5.5,</p><p>CP 77001, Chetumal, Quintana Roo, Mexico</p><p>ABSTRACT: The occurrence of 6 species of helminth parasites (Clinostomum complanatum, Diplostomidae gen. sp.,</p><p>Posthodiplostomum minimum, Bothriocephalus acheilognathi, Glossocercus sp., Contracaecum sp.) is reported from</p><p>7 species of freshwater fishes (Chirostoma jordani, Astyanax mexicanus, Herichthys labridens, Oreochromis niloticusniloticus, Abramis brama, Cyprinus carpio carpio, and Poeciliopsis gracilis) in Metztitlan Lake (Laguna de Metztitlan),</p><p>Reserva de la Biosfera Barranca de Metztitlan, Hidalgo, Mexico. Fish were collected between July 2002 and June 2003. The</p><p>helminth fauna of H. labridens, an endangered species of Cichlidae, is described for the first time. Migratory birds of the</p><p>families Ardeidae and Phalacrocoracidae appear to play an important role in the helminth species composition of fishes from</p><p>Metztitlan Lake. All helminth species represent new records for this federally protected area of Hidalgo.</p><p>KEY WORDS: Digenea, Cestoda, Nematoda, Poeciliidae, Cyprinidae, Cichlidae, Characidae, Atherinidae, Clinostomum</p><p>complanatum, Posthodiplostomum minimum, Bothriocephalus acheilognathi, Glossocercus, Contracaecum, Chirostoma</p><p>jordani, Astyanax mexicanus, Herichthys labridens, Oreochromis niloticus niloticus, Abramis brama, Cyprinus carpiocarpio, Poeciliopsis gracilis, zoonosis, Hidalgo, Mexico.</p><p>The Biosphere Reserve projects combine conser-</p><p>vation with human development in a context of</p><p>sustainable development and scientific investigation.</p><p>The Metztitlan Canyon (Barranca de Metztitlan)</p><p>Reserve of the Biosphere, in the northern part of the</p><p>centrally located state of Hidalgo, Mexico, has a high</p><p>level of endemism in plants and animals (SEMAR-</p><p>NAP, 1999) because of its geomorphologic origin.</p><p>No extensive survey of fish parasites has been con-</p><p>ducted in Hidalgo.</p><p>Metztitlan Lake (Laguna de Metztitlan; Lugar de</p><p>la Luna) is located in the northwest end of an</p><p>enclosed basin or endorreic and has a surface area of</p><p>3,230 km2. The lake was formed naturally when</p><p>a prehistoric rockslide closed off the exit for the</p><p>outflow of Metztitlan River, which today still feeds</p><p>the lake. The local fishery has an ancient history, and</p><p>the catch of native species of fishes has had a large</p><p>economic and nutritional impact on indigenous</p><p>people. Water level in the lake fluctuates greatly</p><p>depending on the season and rainfall within the</p><p>watershed, and the lake has been known to</p><p>completely dry up at least twice in recent times. In</p><p>the past, native species from rivers and streams that</p><p>feed the lake have repopulated the lake after its</p><p>return. In the past decade, the Mexican government</p><p>began extensive introductions of exotic Cichlidae,</p><p>tilapia, and Cyprinidae carpas (Ibanes-Aguirre</p><p>et al., 2002) before efforts were successful in getting</p><p>the area recognized as a reserve. The full consequen-</p><p>ces of these introductions of exotic species on the</p><p>survival of native fauna are not known, although it is</p><p>expected that the cointroduced helminths will have</p><p>negative effects (Osorio-Sarabia et al., 1986; Sal-</p><p>gado-Maldonado et al., 1986). Also, Metztitlan Lake</p><p>is visited by migratory birds (mainly Ardeidae and</p><p>Phalacrocoracidae), and the potential is high for the</p><p>spread of introduced helminths, mainly digeneans</p><p>and nematodes, to other Mexican localities (Lamothe-</p><p>Argumedo and Perez-Ponce de Leon, 1986; Ramos-</p><p>Ramos, 1995). This article represents the first report</p><p>of helminth parasites of freshwater fish from this</p><p>protected area of Hidalgo, Mexico, many of which</p><p>are new reports for fishes from the Panuco River</p><p>Basin.</p><p>MATERIALS AND METHODS</p><p>This study focused on fish from Metztitlan Lake (locatedbetween 988239000 and 988579080W and between 208149150and 208459260 N), municipio of Metztitlan, Hidalgo,Mexico. Monthly collections were made from July 2002 toJune 2003, and 366 fishes were obtained, mostly with thehelp of a local fisherman. All species of fish that are knownto inhabit the lake were collected. The majority of fish weretransported live to the laboratory in containers of lake water,but when the number of fish was large, some fish were keptin plastic bags and chilled on ice; fish were examined within48 hr of capture. Fish were identified using the study of3 Corresponding author.</p><p>Comp. Parasitol.72(2), 2005, pp. 212219</p><p>212</p></li><li><p>Alvarez (1950) and by comparison with previouslyidentified voucher specimens. Voucher specimens of eachspecies are deposited in the Coleccion de Helmintos, Centrode Investigacion Biologicas, Universidad Autonoma delEstado de Hidalgo, Hidalgo, Mexico. External surface,internal visceral organs, eyes, and gills of each fish wereexamined using a dissecting microscope and standardparasitological techniques (Pritchard and Kruse, 1982).Live parasites were held briefly in saline, cleaned, andkilled by rapid immersion in hot water, warm Alchohol-Formalin-Acetic acid (AFA), or Berland solution (forNematoda). Platyhelminths were flattened under slightcoverslip pressure and fixed with AFA, subsequentlytransferred to 70% ethanol, stained with Gomori trichrome,Mayer carmalum, or Ehrlich hematoxylin, dehydrated in analcohol series, cleared in methyl salicilate, and mounted inCanada balsam. Nematodes were stored in 70% ethanol,cleared in a mixture of glycerin and ethanol by evaporation,and examined in temporary glycerin mounts. Voucherspecimens of helminths were deposited in the ColeccionNacional de Helmintos (CNHE), Universidad Autonoma deMexico, D. F., Mexico; the Harold W. Manter Laboratory ofParasitology, University of Nebraska Lincoln, Lincoln,Nebraska, U.S.A.; and the Coleccion de Helmintos,(CHE), Hidalgo, Mexico. Infection parameters follow thestudy of Margolis et al. (1982).</p><p>RESULTS</p><p>During the 12-mo study period, 366 fish were</p><p>necropsied as follows: Atherinidae, Chirostomajordani Woolman, 1894 (n 87); Characidae,Astyanax mexicanus (De Filippi, 1853) (n 64);Cichlidae, Herichthys labridens (Pellegrin, 1903) (n 47) and Oreochromis niloticus niloticus Linnaeus,1758 (n 48); Cyprinidae, Abramis brama Linnaeus,1758 (n 10) and Cyprinus carpio carpio Linnaeus,1758 (n 46); and Poecilidae, Poeciliopsis gracilisHeckel, 1848 (n 64). Members of Cyprinidae andCichlidae were the most abundant, with 2 species</p><p>from each family. Three native species were collected</p><p>(Ast. mexicanus, H. labridens, and P. gracilis), 3exotic species (O. n. niloticus, Abr. brama, and C. c.carpio), and 1 species probably translocated fromanother Mexican state (Ch. jordani). Six parasitichelminth taxa (Clinostomum complanatum [Rudol-phi, 1814], Diplostomidae gen. sp., Posthodiplosto-mum minimum [MacCallum, 1921], Bothriocephalusacheilognathi [Yamaguti, 1934], Glossocercus sp.,and Contracaecum sp., Figs. 18) were collectedfrom the 7 species of fish.</p><p>Larval forms</p><p>DigeneaDiplostomidae gen. sp.</p><p>Metacercariae that could only be identified as</p><p>being a member of the Diplostomidae were collected</p><p>from Ast. mexicanus, Ch. jordani, O. n. niloticus, andP. gracilis. These specimens resemble those collectedby Vidal-Martnez et al. (2001) from native cichlids</p><p>of Southeastern Mexico in general characteristics, but</p><p>these specimens have the cecum surrounding the</p><p>tribocytic organ (Fig. 1). The specimens collected</p><p>most resemble a species of Austradiplostomum Szidatand Nani, 1951, but have a well-developed muscular</p><p>acetabulum, almost equal in size to that of the oral</p><p>sucker, in contrast to members of Austradiplosto-mum, which lack the acetabulum. They also some-what resemble Diplostomum compactum (Lutz,1928), a parasite of cichlids from various localities</p><p>of Mexico (Vidal-Martnez et al., 2001), but our</p><p>specimens have a more conspicuous muscular</p><p>acetabulum. In the same manner, our specimens are</p><p>somewhat similar to members of the genus Bursa-tintinnabulus Tehrany, Dronen and Wardle, 1999,and Bursacetabulus Dronen, Tehrany and Wardle,1999 (Diplostomidae), but members of both genera</p><p>lack an acetabulum (Gibson et al., 2002). The biology</p><p>of this species remains unknown, but similar to other</p><p>members of the family Diplostomidae, a bird serves</p><p>as the definitive host (Yamaguti, 1971).</p><p>Hosts in Laguna de Metztitlan: Astyanax mexicanus,Ch. jordani, O. n. niloticus, P. gracilis.</p><p>Prevalence, total number of worms recovered, andrelative density (intensity) by host taxon: Astyanaxmexicanus, 2 of 64, 2, 0.03 (1); Ch. jordani, 7 of 87,15, 0.17 (17); O. n. niloticus, 1 of 48, 1, 0.02 (1);P. gracilis, 27 of 64, 212, 3.31 (135).</p><p>Sites of infection: Muscle, mesentery, and bodycavity.</p><p>Specimens deposited: CHE-P00010P00019; CNHE-5265.</p><p>Posthodiplostomum minimum(MacCallum, 1921)</p><p>Metacercariae of Po. minimum (Fig. 2) werecollected only from the endemic fish, H. labridens.This digenean has been reported widely throughout</p><p>the Americas, with previous records in Mexico</p><p>(Perez-Ponce de Leon et al., 1996). The metacercarial</p><p>stage has epizootic potential in natural and cultivated</p><p>fish populations (Osorio-Sarabia et al., 1986). In</p><p>Mexico, adults of this species have been recovered</p><p>from Egretta thula (Molina, 1782) (Ardeidae) fromLake Patzcuaro, Michoacan (Lamothe-Argumedo and</p><p>Perez-Ponce de Leon, 1986), a species that also</p><p>frequents Metztitlan Lake (SEMARNAP, 1999).</p><p>MONKS ET AL.HELMINTHS OF METZTITLAN LAKE FISHES 213</p></li><li><p>Hosts in Laguna de Metztitlan: Herichthys labridens.</p><p>Prevalence, total number of worms recovered, andrelative density (intensity): 5 of 47, 35, 0.74 (123).</p><p>Site of infection: Muscle.</p><p>Specimens deposited: CHE-P00022; CNHE-5264.</p><p>Clinostomum complanatum(Rudolphi, 1814)</p><p>Single metacercariae of Cl. complanatum (Fig. 3)were collected from the mouths of only 3 specimens</p><p>of P. gracilis. A cosmopolitan species (Yamaguti,1971), these metacercariae are known from several</p><p>states of Mexico (Perez-Ponce de Leon et al., 1996).</p><p>Hosts in Laguna de Metztitlan: Poeciliopsis gracilis.</p><p>Prevalence, total number of worms recovered, andrelative density (intensity): 3 of 64, 3, 0.05 (1).</p><p>Site of infection: Mouth.</p><p>Specimens deposited: CHE-P00020; CNHE-5263.</p><p>Glossocercus sp.</p><p>Six fish representing 2 species were infected with</p><p>single metacestodes of Glossocercus sp. (Figs. 4, 5).</p><p>We can only assign these larvae to the genus</p><p>Glossocercus until adults are recovered. The lifecycle is not known, but it may use a copepod as</p><p>intermediate host and birds as definitive hosts (Khalil</p><p>et al., 1994). These specimens were collected after</p><p>migratory birds were seen visiting the lake, although</p><p>we have no direct evidence that the birds were</p><p>infected with this species.</p><p>Hosts in Laguna de Metztitlan: Chirostoma jordani,P. gracilis.</p><p>Prevalence, total number of worms recovered, andrelative density (intensity) by host taxon: Chirostomajordani, 2 of 87, 2, 0.02 (1); P. gracilis, 4 of 64, 4,0.06 (1).</p><p>Site of infection: Mesentery.</p><p>Specimens deposited: CHE-P00005, P00006.</p><p>Contracaecum sp.</p><p>Larvae of Contracaecum sp. (Fig. 8) were re-covered from 5 of the 7 species of fish collected. Fish</p><p>serve either as second intermediate hosts or as</p><p>paratenic hosts (Moravec et al., 1995) for members</p><p>of this genus, and the parasites are rare human</p><p>Figures 13. Larval digeneans parasitizing fishes of Metztitlan Lake, Mexico. 1. Diplostomidae gen. sp. 2.Posthodiplostomum minimum. 3. Clinostomum complanatum.</p><p>214 COMPARATIVE PARASITOLOGY, 72(2), JULY 2005</p></li><li><p>pathogens (Moravec, 1998). This is the only parasite</p><p>that is commonly reported by local fishermen. They</p><p>reported the nematode in fish muscle, which rendered</p><p>the flesh unattractive for sale, but found no nematode</p><p>in fish muscle, and so this may not be the species that</p><p>local fishermen report.</p><p>Hosts in Laguna de Metztitlan: Abramis brama, Ast.mexicanus, C. c. carpio, H. labridens, P. gracilis.</p><p>Prevalence, total number of worms recovered, andrelative density (intensity) by host taxon: Abramisbrama, 2 of 10, 3, 0.03 (12); Ast. mexicanus, 8 of64, 15, 0.23 (14); C. c. carpio, 1 of 46, 1, 0.02 (1);H. labridens, 4 of 47, 5, 0.11 (12); P. gracilis, 4 of64, 4, 0.06 (1).</p><p>Sites of infection: Mesentery and body cavity.</p><p>Specimens deposited: CHE-F00013.</p><p>Adult forms</p><p>Bothriocephalus acheilognathi(Yamaguti, 1934)</p><p>This tapeworm (Figs. 6, 7) was initially imported</p><p>along with its host, Ctenopharyngodon idella (Va-lenciennes, 1844), by the aquaculture facilities of</p><p>Tezontepec de Aldama, Hidalgo (Lopez-Jimenez,</p><p>1981) and has been reported widely from Mexico</p><p>since the 1980s. Although all the fish species</p><p>examined except for O. n. niloticus were infectedwith B. acheilognathi, Ch. jordani appears to be themost important definitive host (prevalence 80%;abundance 31.1; and range 1106). It is not knownwhether the helminth was introduced to Laguna de</p><p>Metztitlan with C. c. carpio or Ch. jordani becauseboth are introduced species of undetermined origin</p><p>(Ibanes-Aguirre et al., 2002). Studies are necessary to</p><p>quantify the damage that this parasite may cause the</p><p>indigenous fish species H. labridens and P. gracilis.</p><p>Hosts in Laguna de Metztitlan: Abramis brama, Ast.mexicanus, Ch. jordani, C. c. carpio, H. labridens,P. gracilis.</p><p>Prevalence, total number of worms recovered, andrelative density (intensity) by host taxon: Abramis</p><p>Figures 48. Cest...</p></li></ul>