ISSN 1809-127X (online edition) © 2010 Check List and Authors Chec List Open Access | Freely available at www.checklist.org.br Journal of species lists and distribution pecies s of Helminth parasites of freshwater fishes, Nazas River ists L basin, northern Mexico 1* 1 2 Gerardo 1 Pérez-Ponce de León , Rogelio 3 Rosas-Valdez , 1 Rogelio Aguilar-Aguilar 1 , Berenit Mendoza- Garfias 1, Carlos Mendoza-Palmero 1, Luis García-Prieto , Aline Rojas-Sánchez 4 , Rosario Briosio- Aguilar , Rodolfo Pérez-Rodríguez and Omar Domínguez-Domínguez

1 Universidad Nacional Autónoma de México, Instituto de Biología, Laboratorio de Helmintología. Ap. Postal 70-153. C.P. 04510. México D.F., Mexico. 2 Universidad Autónoma “Benito Juárez” de Oaxaca, Escuela de Ciencias. Oaxaca, Mexico. 3 Institute of Parasitology, [email protected] Centre, Academy of Sciences of the Czech Republic. Branišovská 31, 370 05 České Budějovice, Czech Republic 4 Universidad Michoacana de San Nicolás de Hidalgo, Facultad de Biología, Laboratorio de Biología Acuática. Morelia, Michoacán, Mexico. Abstract:* Corresponding author. E-mail:

This paper represents the first study of the helminth parasites of freshwater fishes from the Nazas River basin in northern Mexico. Between July 2005 and December 2008, 906 individual fish were collected and examined for helminth parasites in 23 localities along the river basin. Twenty-three species of fish were examined as a part of this inventory work. In total, 41 helminth species were identified: 19 monogeneans, 10 digeneans, seven cestodes, one acanthocephalan, and four nematodes. The biogeographical implications of our findings are briefly discussed.

Introduction et al. et al. del Mayran, in state of Coahuila (Castañeda-Gaytán Freshwater fish helminth parasites are undoubtedly 2005; Návar 2006). the most well-known group among vertebrate parasites Between July 2005 and December 2008, 906 individual in Mexico.et al. This group of parasites has been studied in fish belonging to 23 species were collected in 23 localities Mexico since the decade of the 1930´s (Pérez-Ponce along the Nazas River drainage, with sample sizes per de León 1996). Recently, Luque and Poulin (2007) species varying from 2 to 145 specimens (Figure 1; suggested that Mexico stands out as a hotspot of parasite Table 1). Fish were collected under the Cartilla Nacional diversity for freshwater fishes. Still,et al. the helminth fauna de Colector Científico de Flora y Fauna Silvestre (FAUT- of freshwateret al.fishes from northern river basins in Mexico 0057 issued to G.P.P.L.). Fish were collected with seine is poorly known (Garrido-Olvera 2006; Pérez-Ponce nets and electrofishing, and were kept alive and studied de León 2009). Recently, we started collecting for helminths no more that 4 hours after capture. All samples in that part of the country with the main objective internal organs were analyzed separately in Petri dishes of completing the inventory, mostlyet al. by considering with 0.65 % saline under the stereoscope. Gills from Nearctic freshwater fishes such as cyprinids, catostomids, each host were also obtained and placed in tap water ictalurids and centrarchids (Lee 1980), which to search for monogeneans. Monogeneans were fixed constituteet al. the most abundant and most species-rich host in glycerin ammonium-picrate (GAP) in order to study species in River basins in northern Mexicoet (Espinosa-al. their sclerotized structures. After the morphological Pérez 1993). The first results of that survey work evaluation, specimens fixed with GAP were remounted in were published by Pérez-Ponce de León (2009) Canada balsam following Ergens (1969); some specimens who described the endohelminth fauna of freshwater were fixed in hot formaline 4 %, stained with Gomori’s fishes from the upper Mezquital River basin. In this trichrome and mounted in Canada balsam to study their paper, we present the results of the survey work we internal organs. Endoparasites were removed to a Petri conducted in freshwater fishes of the Nazas River basin, dish with saline 0.65 %, prior to fixation. Digeneans and an interesting area from the biogeographical point of view cestodes were fixed with hot (steaming) 4 % formalin. that represents an interior (closed) basin that runs from Acanthocephalans were maintained at 4 °C for 12 hours in the Sierra Madre Occidental down to the lowlands of the distilled water, and then fixed in 70 % ethanol. Nematodes MaterialsMeseta del Norte. and Methods were fixed with hot (steaming) 4 % formalin or 70 % ethanol. All helminths were processed following standard procedures. Identification was made using specialized The Nazas River is an endorreic River basin located literature, and representative specimens of all helminth in the north of Mexico and it extends along the states of species were deposited at the Colección Nacional de Coahuila and Durango. It is only 560 Km in length, but Helmintos, Instituto de Biología, Universidad Nacional irrigates an area of 71,906 km² in the middle of the deserts ResultsAutónoma and de MéxicoDiscussion (UNAM), Mexico City (CNHE). of Coahuila and Durango states (Figure 1). The Nazas is also nurtured by the San Juan, Ramos, Potreritos, del Oro, Nazas, Santiago, Tepehuanes and Peñón Blanco Rivers. The In total, 41 helminth species were found, representing River starts at the Mexican Sierra Madre Occidental and 26 genera and 17 families. Of the 41 species we record drainsCheck through List | Volume state 6 | Issue of 1Durango | 2010 into the now dry Laguna herein, 19 were monogeneas, 10 digeneans, seven026 Pérez-Ponce de León et al. | Helminth parasites of freshwater fishes, Nazas River basin, northern Mexico

cestodes, one acanthocephalan, and four nematodes. The were collected for DNA work or scanning electron systematic position of each helminth species is presented microscopy are referred as “MW”. Some specimens were next, with information related with host (s), locality(s) and not collected and are referred as “NC”.

Figure 1. Map of the Mexican Republic showing the localities where fish were sampled along the Nazas River basin in state of Durango.

Table 1. LocalitySpecies of freshwater fishes analyzed in this survey, with host name and sampleHost size perspecies locality. Sample size Astyanax mexicanus Cyprinodon nazas 1 Balneario “la Concha”, Peñón Blanco De Filippi, 1853 6 Poeciliopsis gracilis Miller, 1976 32 Astyanax mexicanus Heckel, 1848 6 Campostoma ornatum 2 Camino a San Rafael Jicorica 3 Catostomus nebuliferus Girard, 1856 1 Cyprinella garmani Garman, 1881 3 Gila conspersa Jordan, 1885 4 Lepomis megalotis Garman, 1881 12 Notropis chihuahua (Rafinesque, 1820) 9 Notropis nazas Woolman, 1892 12 Pimephales promelas Meek, 1904 15 Rhinichtys cataractae Rafinesque, 1820 5 Ictalurus pricei Valenciennes, 1842 15 Lepomis macrochirus 3 Charco las pitahayas, poblado Las Higueras Rutter, 1896 4 Gila conspersa Rafinesque, 1819 7 Oreochromis nilotica 1 Pimephales promelas Linnaeus, 1758 1 Poeciliopsis gracilis 2 Carassius auratus 9 Notropis chihuahua 4 Canal de Riego, poblado Dolores Hidalgo Linnaeus, 1979 1 Poeciliopsis gracilis 2 Campostoma ornatum 4 5 El Palmito 4

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Locality Host species Sample size Codoma ornata Notropis nazas Girard 1856 1 Astyanax mexicanus 10 Codoma ornata 6 Poza en el Arroyo Torreones 10 Gila conspersa 15 Ictalurus pricei 30 Notropis chihuahua 1 Campostoma ornatum 5 Catostomus nebuliferus 7 Puente en carretera Peñón Blanco-Yerbaniz 37 Codoma ornata 11 Cyprinella garmani 23 Cyprinus carpio 3 Gila conspersa 1 Notropis nazas 50 Pimephales promelas 6 Astyanax mexicanus 2 Catostomus nebuliferus 8 Puente Lajas I, poblado de San Juan Francisco Lajas 3 Gila conspersa 1 Astyanax mexicanus 39 Astyanax mexicanus 9 Puente Lajas II, poblado de San Juan Francisco Lajas 12 Campostoma ornatum 10 Río Covadonga, poblado de Peñón Blanco 4 Catostomus nebuliferus 20 Codoma ornata 19 Etheostoma pottsi 22 Gila conspersa Girard, 1859 20 Notropis nazas 51 Ictalurus pricei 17 Gila conspersa 11 Río Nazas, poblado de San Rafael Jicorica cf. 3 Ictalurus pricei 12 Río Nazas, puente Nazas, Poblado de Nazas 2 Notropis nazas cf. 1 Pimephales promelas 26 Poeciliopsis gracilis 11 Oreochromis niloticus 2 Lepomis macrochirus 1 Notropis nazas 13 Río Nazas, puente en carretera Rodeo-Hidalgo de Parral, desviación a Abasolo 7 Pimephales promelas 3 Asyanax mexicanus 21 Campostoma ornatum 14 Río San Juan en “El Cuarto” 10 Catostomus nebuliferus 16 Codoma ornata 5 Cyprinodon nazas 40 Gila conspersa 1 Poeciliopsis gracilis 32 Lepomis macrochirus 1 Lepomis macrochirus 15 Canal de riego, Tlahualillo 1 2 Cyprinus carpio 16 Canal de riego, Tlahualillo 2 4 Ictalurus pricei 17 Presa Francisco Zarco Linnaeus,1758 5 Ictalurus punctatus cf. 5 Campostoma ornatum Rafinesque,1818 5 Catostomus nebuliferus 18 Puente Carretera Paso Nacional 2 Ictalurus pricei 1 Lepomis macrochirus 2 Notropis nazas 4 Pimephales promelas 2 Pomoxis annularis 11 Astyanax mexicanus Rafinesque, 1918 4 19 Río Nazas, poblado de Santa Rita 22

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Locality Host species Sample size Carassius auratus Micropterus salmoides 1 Pimephales promelas Lacepède, 1802 2 Poeciliopsis gracilis 3 Pomoxis annularis 1 Oreochromis nilotica 1 Pomoxis annularis 1 Astyanax mexicanus 20 Río Nazas, salida de Presa Francisco Zarco, camino Graceros-Las Pirañas 16 Cyprinus carpio 21 Río Nazas, bomba de agua en Ciudad Lerdo 20 Micropterus salmoides 20 Astyanax mexicanus 20 Catostomus nebuliferus 22 Río en el Pueblo Emilio Carranza 26 Cyprinella garmani 1 Lepomis macrochirus 10 Micropterus salmoides 11 Notropis nazas 11 Catostomus nebuliferus 8 Ictalurus pricei 23 Río Ramos, poblado el Olote 16 cf. 19 Phylum Lepomis macrochirus Class Platyhelminthes Gegenbaur, 1859 Concha”, Peñon Blanco (MW), Río Covadonga, Peñón Blanco (CNHE 6485); Astyanax mexicanusCanal de riego en Order Trematoda Rudolphi, 1808 Tlahualillo 1 (MW); Heterophidae gen. sp. (metacercariae) Host and locality: Río Nazas, Ciudad Family Plagiorchiida La Rue, 1957 FamilyLerdo (MW).

Allocreadiidae Looss, 1902 Magnivitellinum Macroderoididaesimplex McMullen, 1937 Codoma ornata Astyanax mexicanus Río Allocreadiidae gen. sp. (adult) Kloss, 1966 (adult) Host and localities: Río Covadonga, Host and locality: Covadonga, Familypoblado de Peñon Blanco (CNHE 6706) AlloglossidiumPeñón Blanco (CNHE corti 6311-6313). Ictalurus . pricei Clinostomum Clinostomatidaecomplanatum Lühe, 1901 Lamont,Ictalurus 1921 pricei (adult) Hosts and localities: cf Camino a San Rafael Astyanax (Rudolphi, mexicanus 1814) Braun, 1899 Jicorica (CNHE 6239); Charco las pitahayas, (metacercariae) Catostomus nebuliferus FamilyLas Higueras (CNHE 6647-6748). Hosts and localities: RíoEtheostoma San Juan pottsien “El Cuarto” (CNHE 6315); Río Diplostomum Diplostomidae Poirier, 1886 Covadonga,Lepomis poblado macrochirus Peñón Blanco (MW); Pimephales promelas Río Covadonga,Micropterus poblado salmoides de Peñón Blanco (CNHE sp. (metacercariae) 6316); CanalNotropis de chihuahua riego, Tlahualillo Hosts and locality: Río Nazas, 2 (CNHE 6314); Poeciliopsis gracilisRío en el Pueblo PosthodiplostomumPoblado de Nazas (MW). minimum Emilio Carranza (CNHE 6225); Camino a San Rafael Jicorica (MW); Charco las Astyanax (Lutz, mexicanus 1928) Dubois, 1970 Familypitahayas, Las Higueras (MW). (metacercariae) Campostoma ornatum Hosts and localities: Camino a San Phyllodistomum Gorgoderidaelacustri Loos, 1901 Rafael Jicorica (MW); Camino a San Rafael Jicorica (MW), Puente carretera Peñon Blanco- Ictalus (Loewen,pricei 1929) Lewis, 1935 Yerbaniz (CNHE 6333), Río Covadonga, Peñón Codoma Blanco (adult) ornata(6318), Puente carretera Paso Nacional-Lázaro Cárdenas Hosts and localities: Ictalurus cf. priceiRío Ramos, poblado (CNHE 6327), Río San Juan en “El Cuarto” (6324); el Olote (CNHE 5932), Río Nazas, poblado de San Rafael Puente carretera Peñon Blanco-YerbanizCyprinella (CNHE Jicorica (CNHE MW); Poza en el Arroyo garmani6320-6321), Río Covadonga, Peñón Blanco (6325-6326, FamilyTorreones (MW). 6328), Río San Juan Gila en “El conspersa Cuarto” (6329); Puente carretera Paso Nacional-Lázaro Cárdenas Centrocestus Heterophidae formosanus Odhner, 1914 (CNHE 6330-6331); Poza en el Arroyo Torreones (MW), Camino a San Rafael Jicorica (CNHE 6613), Astyanax (Nishigori, mexicanus 1924) Price, 1932 Puente carreteraIctalurus Peñon punctatus Blanco-Yerbaniz (CNHE 6332), (metacercariae) Río Covadonga, Peñón Blanco (6317), Río San Juan en “El Hosts and localities: Balneario “La Cuarto” (6223); Presa Francisco Zarco Check List | Volume 6 | Issue 1 | 2010 029 Pérez-Ponce de León et al. | Helminth parasites of freshwater fishes, Nazas River basin, northern Mexico

Lepomis macrochirus Family

(CNHE 6319); ), Río en el Pueblo EmilioCharco Carranza las pitahayas, (CNHE Dactylogyrus Dactylogyridae anchoratus Yamaguti, 1963 Las Higueras (CNHELepomis 6646), megalotis Canal de Río riego, Tlahualillo 2 (CNHE 6337 Notropis chihuahua Carassius (Dujardin,1845) auratus Wagener, 1857 6222, 6224, 6524); Nazas, poblado (adult) de San Rafael Jicorica (CNHE 6641);Notropis nazas Host and locality: Canal de Riego, en Canal de Riego, poblado Dolores Hidalgo (MW), Camino a Dactylogyruspoblado Dolores dulkeiti Hidalgo (CNHE 6359). San Rafael Jicorica (not collected); Camino Carassius auratus a San RafaelPimephales Jicorica promelas (MW), Río Covadonga, poblado de Bychowsky, 1936 (adult) Peñon Blanco (not collected), Río Nazas, Poblado de Nazas Host and locality: Canal de Riego, en (6295); Río Nazas, Poblado de Nazas Dactylogyruspoblado Dolores extensus Hidalgo (CNHE 6360). (6236), Río en el Pueblo Emilio Carranza (6334), Camino a San Rafael Jicorica (MW), Puente carretera Paso Nacional- CyprinusMueller carpio and Vam Cleave, 1932 Lázaro Cárdenas(CNHE 6325), Charco las pitahayas, Las (adult) Higueras (MW),Pomoxis Río Nazas, annularis puente en la carretera Rodeo- Host and locality: Pozo San Fernando Hidalgo de Parral, desviación al poblado de Abasolo Rhinichthys (CNHE Dactylogyrus(CNHE 6951), cataractae6237-6238); Río Nazas, salida de la Gila conspersa Presa Francisco Zarco (CNHE 6322-6323); sp 1 (adult) Uvulifer Camino a San Rafael Jicorica (MW). Hosts and localities: Poza en el Arroyo Campostoma ornatum Río DactylogyrusTorreones (CNHE 6952), Puente Lajas I (CNHE 6953). sp. (metacercariae) Gila conspersa Gila conspersa Host and locality: NotropisCovadonga, nazas sp. 2 (adult) poblado de Peñon Blanco (CNHE 6483); NotropisHosts and nazas localities: Poza en el Arroyo Río Covadonga, Peñón Blanco (6484); Río Torreones (CNHE 6954), Puente Lajas I (CNHE 6955); Nazas, Poblado de Nazas (CNHE 6505), Río Covadonga, Cichlidogyrus sclerosus Río Nazas, Poblado de Nazas (NC). Classpoblado de Peñon Blanco (MW). Oreochromis Paperna y Thurston, 1969 (adult) Order Monogenea Carus, 1863 Host and locality: nilotica Río Nazas, Poblado Familyde Nazas (CNHE 6956) Family Dactylogyridea Bychowsky, 1937 Gyrodactylus Gyrodactylidae spathulatus Van Beneden and Hesse, 1863 Cleidodiscus Dactylogyridae bedardi Bychowsky, 1933 Catostomus nebuliferus Lepomis macrochirus Mueller,Gila conspersa 1936 (adult) Mizelle,1936 (adult) Hosts and localities: Torreones Ictalurus Río Ramos,pricei Host and locality: Río Nazas, puente poblado el Olote (MW); Puente Lajas I en la carretera Rodeo-Hidalgo de Parral, desviación a (MW), Poza en el Arroyo (NC); cf. OnchocleidusAbasolo (CNHE spiralis6363). GyrodactylusRío Nazas, Poblado de Nazas (NC). Gila conspersa Lepomis (Mueller, macrochirus 1937) Mizelle and sp. 1 (adult) Hudges,1938 Host and locality: Puente Las Lajas I (CNHE Host and locality: Río Nazas, puente Gyrodactylus6957). en la carretera Rodeo-Hidalgo de Parral, desviación a Catostomus nebuliferus LigictaluridusAbasolo (CNHEmirabilis 6512). sp. 2 (adult) Ictalurus . pricei Host and locality: Río Ramos, Muller, 1937 (adult) Gyrodactyluspoblado el Olote (CNHE 6958) Host and locality: cf Río Nazas, poblado de Notropis nazas LigictaluridusSan Rafael Jicoricapricei (CNHE 6478, 6506); sp. 3 (adult) Ictalurus . pricei Host and locality: Río Nazas, Poblado de Muller, 1936 (adult) GyrodactylusNazas (CNHE 6959). Hosts and localities: cf Río Nazas, poblado Campostoma ornatum de San Rafael Jicorica (CNHE 6482, 6507), Río Nazas, sp. 4 (adult) CharacitheciumPoblado de Nazas costaricensis (CNHE 6481, 6508). Hosts and localities:Pimephales promelas Río Nazas, puente en la carretera Rodeo-Hidalgo de Parral, desviación Astyanax mexicanus(Price and Bussing, 1967) a Abasolo (MW); Río Nazas, puente Mendoza-Franco, Reyna, and Torchin, 2009 (adult) en la carretera Rodeo-Hidalgo de Parral, desviación a Host and locality: Puente Lajas II. GyrodactylusAbasolo (NC). (MW).Urocleidoides strombicirrus Astyanax mexicanus sp. 5 (adult) “ ” Astyanax mexicanus(Price and Bussing, 1967) Host and locality: Poza en el Arroyo Kritsky and Thatcher, 1974 (adult) GyrodactylusTorreones (NC), Puente Lajas II (CNHE 6960). Host and locality: Puente Lajas II Lepomis macrochirus (CNHE 6510-6511). sp. 6 (adult) Check List | Volume 6 | Issue 1 | 2010 Host and locality: Río Nazas, puente030 Pérez-Ponce de León et al. | Helminth parasites of freshwater fishes, Nazas River basin, northern Mexico

en la carretera Rodeo-Hidalgo de Parral, desviación a Poza en el Arroyo Torreones (CNHE 6430-6432, 6457- ClassAbasolo (CNHE 6513). 6458), Puente carretera Peñon Blanco-Yerbaniz (CNHE 6220, 6351), Río Covadonga, Peñón Blanco (6216, 6353- Order Cestoda Rudolphi, 1808 6355), Río San Juan en Notropis “El Cuarto” chihuahua (6215, 6345-6347); Lepomis macrochirus Puente carretera Paso Nacional- Family Caryophyllidea van Beneden in Carus, 1863 Lázaro Cárdenas (MW); Camino a San Rafael Jicorica (not collected),Notropis nazas Poza en Arroyo Torreones Khawia Lytocestidaesinensis Hunter, 1927 (CNHE 6434), Canal de Riego, poblado Dolores Hidalgo Cyprinus carpio (CNHE 6427-6428); El Palmito (MW), Río Hsu, 1935 (adult) Covadonga, poblado de Peñon BlancoPimephales (6218, 6397, promelas 6456), Host and locality: Presa Francisco Zarco Río en el Poblado de Emilio Carranza (6217), Río Nazas, Family(6515-6516). Poblado de NazasRío Nazas (CNHE 6429); Puente carretera Paso Nacional-Lázaro Cárdenas(CNHE Caryophyllaeidae Leuckart, 1878 6339, 6451), en Sta. Rita (not collected), Camino Notropis nazas a San Rafael Jicorica (not collected), Río Nazas, Poblado Caryophyllidea gen. sp. de NazasPoeciliopsis (CNHE 6425), gracilis Río Nazas, puente en carretera Host and locality: Río en el Poblado Emilio Rodeo-Hidalgo de Parral, desviación a Abasolo (CNHE IsoglaridacrisCarranza (CNHE 6797). 6435); Río San Juan en “El Cuarto” Catostomus nebuliferus Order(CNHE 6348, 6455). sp. (adult) Host and locality: Río Covadonga, Family Cyclophyllidae van Beneden in Brun,1900 Orderpoblado Peñón Blanco (CNHE 6802) Neovalipora Dilepididae Railliet and Henry, 1909 Family Proteocephalidea Mola, 1928 Ictalurus pricei sp. (cysticercoid) Corallobothrium Proteocephalidae fimbriatum La Rue, 1911 Host and locality: cf. Presa Francisco Zarco Ictalurus pricei Phylum(CNHE 6530). Ictalurus Essex, pricei 1927 (adult) Hosts and localities: cf. Presa Francisco Class Acanthocephala Rudolphi, 1808 Zarco (CNHE 6517); Puente carretera Paso MegathylacoidesNacional-Lázaro giganteumCárdenas (MW). Order Palaeacantocephala Meyer, 1931 Ictalurus pricei Essex,1928 (adult) Family Polymorphida Petrochenko, 1956 Hosts and localities: cf. Río Ramos, poblado el Olote (MW), Río Nazas, poblado de San Rafael Jicorica Polymorphidae Meyer, 1931 (not collected),Ictalurus Presa punctatus Francisco Zarco (6519); Ictalurus Polymorphus pricei Puente carretera Paso Nacional-Lázaro Cárdenas Astyanax mexicanus (MW); Presa Francisco Zarco (CNHE sp. (cystacanth)Micropterus salmoides Order6520). Hosts and localities: Río Nazas, Ciudad Lerdo (CNHE 6929-6930); Río en Family Pseudophyllidae Carus, 1863 el Pueblo Emilio Carranza (NC), Río Nazas, Ciudad Lerdo Phylum(CNHE 6928). Bothriocephalus Bothriocephalidaeacheilognathi Blanchard, 1849 Astyanax mexicanus Class Nematoda Rudolphi,1808 Yamaguti, 1934 (adult) Hosts and localities: Puente Lajas I Order Secernentea Von Linstow, 1905 (CNHE 6439), RíoCampostoma Covadonga, ornatum Peñón Blanco (MW), Río Nazas, Ciudad Lerdo (CNHE 6452), Río San Juan en “El Family Ascaridida Skrjabin and Schulz, 1938 CodomaCuarto” ornata (MW); Río Covadonga, Peñón Blanco (6352), Río San Juan en “El Cuarto” (6343); Anisakidae (Railliet and Henry, 1912) Skrjabin and Poza en el Arroyo Torreones (CNHE 6433, ContracaecumKarokhin, 1945 6449), Puente carretera Peñon Blanco-YerbanizCyprinella garmani (CNHE Astyanax mexicanus Río Nazas Camino6395-6396), Río Covadonga, Peñón Blanco (6394), Río sp. (larvae) Cyprinella garmani San Juan en “El Cuarto” (6349-6350); Hosts and localities: Gila conspersa, a San Rafael Jicorica (not collected), Puente Emilio Carranzas (CNHE 6388-6389); Ictalurus pricei carretera Peñon Blanco-Yerbaniz (not collected), Puente Camino a San Rafael Jicorica (CNHE 6728);Ictalurus pricei carretera Peñon Blanco-Yerbaniz (CNHE 6341, 6514), Camino a San Rafael Jicorica (MW); cf. Río en el Pueblo Emilio CarranzaGila (6219); conspersa Cyprinus carpio Presa Francisco Zarco (CNHE 6392-6393); Ictalurus Presa Francisco Zarco (6340, 6342), Río Nazas, Bombas de punctatusCharco las pitahayas, Las Higueras (CNHE 6726),Pomoxis Puente agua en Ciudad Lerdo (6338); Camino a San annulariscarretera Paso Nacional-Lázaro Cárdenas (MW); Rafael Jicorica (not collected), Puente Lajas I (CNHE 6436- Presa Francisco Zarco (CNHE 6387); 6438,Check 6447), List | Volume Río 6Nazas, | Issue 1 | Poblado2010 de Nazas (6426, 6454), Río Nazas, salida de la Presa Francisco Zarco031 Pérez-Ponce de León et al. | Helminth parasites of freshwater fishes, Nazas River basin, northern Mexico

Centrarchidae Lepomis macrochirus Family(CNHE 6386). Centrocestus formosanus (n = 37) Spiroxys Gnathostomidae Railliet, 1895 ClinostomumDigenea complanatum Astyanax mexicanus Posthodiplostomum minimum sp. (larvae) Campostoma ornatum Hosts and localities: PuenteCyprinodon Lajas I Bothriocephalus acheilignathi (CNHEnazas 6382), Puente Lajas II (NC); Gila conspersa Cestoda Puente carretera Peñon Blanco-Yerbaniz (MW); Cleidodiscus bedardi Río San Juan en “El Cuarto” (MW); GyrodactylusMonogenea Puente carretera Peñon Blanco-YerbanizNotropis (not chihuahua collected), Onchocleidus spiralis Puente Las Lajas I (CNHE 6380-6381, 6450),Notropis Poza nazas en el Lepomis megalotissp. 6. Arroyo Torreones (CNHE 6384-6385); . Poza en el Arroyo Torreones (CNHE 6383); Posthodiplostomum minimum (n = 9) OrderPuente carretera Peñon Blanco-Yerbaniz (MW); DigeneaMicropterus salmoides

Family Spirurida Chitwood, 1933 Clinostomum complanatum (n = 33) Digenea Rhabdochonidae (Travassos, Artigas and Pereira, Polymorphus . Rhabdochona1928) Skrjabin, canadensis 1946 AcanthocephalaPomoxis annularis Campostoma ornatum sp. MoravecCodoma and Arai, ornata 1971 (adult) Posthodiplostomum minimum (n = 21) Hosts and localities: Puente carretera Digenea Peñon Blanco-Yerbaniz (MW); Puente Contracaecum carretera PeñonCyprinella Blanco-Yerbaniz garmani (MW), Río Covadonga, Nematoda Peñón Blanco (MW),Gila Poza conspersa en el Arroyo Torreones (CNHE Characidae sp. 6698-6699); Camino a San Rafael Astyanax mexicanus Jicorica (MW); PuenteNotropis carretera chihuahua Peñon Blanco-Yerbaniz (MW), Río Covadonga,Notropis Peñón nazas Blanco Centrocestus formosanus (n = 135) (NC), Puente Las Lajas I (CNHE 6701); ClinostomumDigenea complanatum Camino a San Rafael Jicorica (NC); Puente carretera Peñon Blanco-Yerbaniz (MW), Río Covadonga, Magnivitellinum simplex poblado de Peñon Blanco (CNHE 6705); Pimephales PosthodiplostomumHeterophydae gen. sp. minimum promelas Río Nazas, puente en la carretera Rodeo-Hidalgo Rhabdochonade Parral, desviación catostomi al poblado de Abasolo (CNHE 6700). Bothriocephalus acheilognathi Cestoda Kayton,Catostomus Kritsky, nebuliferus and Tobias, 1979 Characithecium costaricensis (adult) GyrodactylusMonogenea Hosts and localities: Puente carretera Peñon Blanco-Yerbaniz (CNHE 6702), Río Polymorphus sp. 5 Covadonga, poblado Peñón Blanco (CNHE 6704), Río Acanthocephala Host-ParasiteRamos, poblado List. el Olote (CNHE 6703). Contracaecumsp. SpiroxysNematoda sp. The host-parasite list is presented below in alphabetical Cichlidae sp. order by fish family. In each host species sample size as Oreochromis niloticus the sum of all the sampled localities is presented. The list of helminth species per host species is ordered by Cichlidogyrus sclerosus (n =3) helminth parasite group, and within each helminth group, Monogenea Catostomidaein alphabetical order. Cyprinidae Catostomus nebuliferus Campostoma ornatum

Clinostomum complanatum (n = 58) Posthodiplostomum minimum (n = 80) Digenea UvuliferDigenea Gyrodactylus spathulatus GyrodactylusMonogenea Gyrodactylussp. UrocleidoidesMonogenea strombicircus Isoglaridacrissp. 2 sp. 4 Cestoda Bothriocephalus acheilognathi Rhabdochona catostomisp. Cestoda Nematoda Rhabdochona canadensis Nematoda Check List | Volume 6 | Issue 1 | 2010 032 Pérez-Ponce de León et al. | Helminth parasites of freshwater fishes, Nazas River basin, northern Mexico

Spiroxys Carassius auratus Diplostomum sp. (N). PosthodiplostomumDigenea minimum Dactylogyrus anchoratus (n = 2) sp. DactylogyrusMonogenea dulketi Gyrodactylus (D). Codoma ornata Monogenea Bothriocephalussp. acheilognathi4 Posthodiplostomum (n minimum = 101) Cestoda Digenea Rhabdochona canadensis Bothriocephalus acheilognathi NematodaRhinichthys cataractae Cestoda (N). Rhabdochona canadensis Posthodiplostomum minimum (n = 15) NematodaCyprinella garmani Digenea Cyprinodontidae (D). Posthodiplostomum minimum (n = 19) Cyprinodon nazas Digenea Bothriocephalus acheilognathi Spiroxys (n = 33) Cestoda Nematoda Contracaecum Ictaluridaesp. (N). RhabdochonaNematoda canadensis Ictalurus pricei Cyprinus carpio sp. Alloglossidium corti cf. (n = 9) Bothriocephalus acheilognathi (n = 26) PhyllodistomumDigenea lacustri KhawiaCestoda sinensis Gila conspersa Gyrodactylus spathulatus. LigictaluridusMonogenea mirabilis Posthodiplostomum (n minimum = 217) Ligictaluridus pricei . UvuliferDigenea Corallobothrium fimbriatum Dactylogyrussp. MegathylacoidesCestoda giganteum MonogeneaDactylogyrus Neovalipora Gyrodactylus spathulatussp. 1. Gyrodactylus sp. 2. Contracaecumsp. Nematoda Bothriocephalussp. acheilognathi1. Ictalurussp. pricei Cestoda Contracaecum Alloglossidium corti (n = 7) RhabdochonaNematoda canadensis PhyllodistomumDigenea lacustri Spiroxys sp. Notropis chihuahua Corallobothrium fimbriatum sp. MegathylacoidesCestoda giganteum Clinostomum complanatum (n = 19) PosthodiplostomumDigenea minimum Contracaecum NematodaIctalurus punctatus Bothriocephalus acheilognathi sp. Cestoda Posthodiplostomum minimum (n = 6) Rhabdochona canadensis Digenea SpiroxysNematoda Megathylacoides giganteum Notropis nazas Cestoda sp. Contracaecum Posthodiplostomum (n minimum = 87) Nematoda UvuliferDigenea Percidae sp. Etheostoma pottsi Dactylogyrus sp. MonogeneaGyrodactylus Clinostomum complanatum (n = 20) sp. 2. Digenea Bothriocephalussp. acheilognathi3. Poeciliidae Cestoda Poeciliopsis gracilis

RhabdochonaCaryophyllidea canadensis gen. sp. Clinostomum complanatum (n = 20) SpiroxysNematoda Digenea Pimephales promelas Bothriocephalus acheilognathi sp. Cestoda Check List | Volume 6 | Issue 1 (n| 2010 = 55) 033 Pérez-Ponce de León et al. | Helminth parasites of freshwater fishes, Nazas River basin, northern Mexico

Rhabdochona catostomi

This list of helminth species we present herein the nematode and one species represents the continuation of our efforts to describe the Khawiaof caryophillidean sinensis tapeworm were recorded,Dactylogyrus while in biodiversity of this group of parasites in their freshwater cyprinids,Gyrodactylus an allocreadiid digenean, the caryophillideanRhabdochona fish hosts in Mexico. The inventory is not complete yet, but canadensis , monogeneans of the genera we are targeting River basins in the northern parts of the and , and the nematode country, which still remain the less explored regions for were collected. Further evidence was found by helminth parasites (Pérez-Ponce de León and Choudhury analyzing other freshwater fishes,Phyllodistomum such as ictalurids lacustri which 2005). In this case, we adopted a geographical region harboredAloglossidium at least six corti members of the biogeographical core approach to conduct the survey work by considering 23 fauna, Ligictaluridus including the digeneans Magathylacoides localities along the Nazas River et basin. al. We surveyed 23 giganteumand Corallobothrium, two species of fimbriatummonogeneans of the host species which account for most of the species found genus , and the tapeworms along the River basin (see Miller 2005). These host , and . The species represent 18 genera and nine families. Most of the centrarchids also harbored at least two species of freshwater fish fauna in the basin are typically Nearctic Cleododiscusmonogeneans bedardi commonlyOnchochelidus found in members spiralis. of the fish elements, i.e., minnows (cyprinids), catfishes (ictalurids), group in other parts of North America, north of Mexico, darters (etheostomids), suckers (catostomids), sunfishes and and basses (centrarchids). These fishes account for 19 of In contrast, larval forms were found in most host the 23 studied species. species and in particular, three of them were found asP. In total, in this survey work we recorded 41 species of generalistminimum parasites,C. complanatum occurring in a large proportion helminths, and since the region was previousGyrodactylus unexplored, ofContracaecum the analyzed hosts. That is, the metacercariae of spathulatus,this accounts for Dactylogyrus 74 and 71 new dulkeiti, locality D. and anchoratus, new host B. acheilognathi and , and the larval nematode Cleidodiscusrecords, respectively. bedardi, Ligictaluridus The monogeneans pricei sp. A fourth species, the Asian tapeworm, Khawia sinensis Isoglaridachris , which represents an introduced species, , as well as the was also commonly found in most host species. Overall, the cestodes and sp., are aforementioned species were found in 13, six, six, and 11 recorded for the first time in Mexico. All these species, of the 23 species studied in this survey, respectively. More however, have been previously recorded in other North importantly, these helminths were recovered from four to American freshwater fishes (see Margolis and Arthur six of theet nineal. families to which fish are allocated which 1979; McDonald and Margolis 1995; Hoffman 1999). The further demonstrates its generalist character (Pérez-Ponce unidentified species of monogeneans and caryophyllideans de León 1996; 2007; Rojas-Sánchez and García-Prieto await further taxonomic work, and they represent new personal communication; Hernández-Mena and Osorio- records for the country (and most likely they represent Sarabia personal communication). new species) that will be describedet al. in a separate paper. A lower proportion of larval helminths in comparison Some studies (e.g. Pérez-Ponce de León and Choudhury to adults was found in our study. This seems to be a 2002; 2005; Aguilar-Aguilar 2008) have corroborated striking result when compared with other freshwater the fact that the historical biogeography of the parasites is fish parasite surveys in other regions of Mexico, at both closely link to that of their hosts, leading to the prediction regional (basin) and local scales. In this study, 10 out of the made by Pérez-Ponce de León and Choudhury (2005) 41 recorded species were larval forms Spiroxys(25 %). All these that the parasite fauna is largely circumscribed by higher larval forms (metacercariae, 3rd stage larvae, cystacanths, levels of monophyletic host taxa, especially to the level of or cysticercoids), with the exception of sp. which fish family. Our inventory work in the Nazas River basin is a parasite of turtles, develop to the adult stage in fish- provides further empirical evidence to corroborate that eating birds. In other studies, the percentage of larval prediction. In a recent study of the helminth parasite forms tends to be higher, with 33 %, 42 %, 43et % al. or 44 % fauna in freshwater fishes from a nearby basin, the for the Papaloapan, Pánuco, Ayuqila, andet Mezquital al. River Mezquital River, Pérez-Ponce de León et al (2009) found basins, respectively (Salgado-Maldonado 2004a, no support for that prediction by analyzing the faunal 2004b, 2005; Pérez-Ponce de León 2009). This composition of the parasite fauna in typically Nearctic clearly may be the result of a sampling artifact, due to the fish groups such as cyprinids and catostomids. The Nazas fact that monogeneans were not studied in detail in the River basin shows no connection with River basins from aforementioned surveys, which is not unexpected since central areas of Mexico, as the Mezquital River does. In their collection may result a time consuming activity due to this context, findings made through this survey work their small size and need for proper fixation. On the other allowed us to increase not only the sample size, but also hand, it has been suggested that digeneans and nematodeset the species diversity for nearctic fish families, particularly al.represent the most species-rich groups in the parasite the cyprinidae. In the former study, only three species of fauna of freshwater fishes of Mexico (Salgado-Malonado cyprinids (with 123 individuals), and only one species of , 2005). In our study, however, monogeneans accounted catostomid (with five individuals) were collected. Here, for the greatest species richness, with 19 recorded species, we increased our sampling effort and the same catostomid while digeneans and nematodes had 10 and four species, species was sampled, albeit with 58 specimens, while 10 respectively. A larger proportion of monogeneans in our species of cyprinids were collected, accounting for 597 samplings increase the proportion of adult helminth specimens. In this case, typical Nearctic helminth species parasites. Whether this trend is the result of a sampling that are part of the biogeographical core fauna of both, artifact due to the paucity of studies on monogeneans catostomidsCheck List | Volume and 6 cyprinids, | Issue 1 | 2010 were found. In catostomids, in freshwater fishes of Mexico, or it is related to the fact034 Pérez-Ponce de León et al. | Helminth parasites of freshwater fishes, Nazas River basin, northern Mexico

Comparative Parasitology Dactylogyrus (Siluriformes: Heptapteridae), from a cenote on the Yucatán that Gyrodactylus Nearctic components of the parasite fauna include Peninsula, Mexico.Atlas of North American freshwater 70(2): 136-139. fishes more species of monogeneans such as spp. Lee D., C.R. Carter, C.H. Hoccut, R.E. Jenkins, D.E. McAllister and J.R. and spp (see Hoffman 1999), needs to be Stauffer. 1980. . Raleigh: North Carolina Biological Survey. 854 p. determined with more survey work in northern regions Luque,Parasitology J.L. and R. Poulin. 2007. Metazoan parasite species richness in of Mexico. Although, recent studies by monogenean Neotropical fishes: hotspots and the geography of biodiversity. taxonomists have demonstrated that the species richness Bulletin 134: of 865-878. the Fisheries Research Board of Canada Margolis, L. and J.R. Arthur. 1979. Synopsis of the parasites of fishes of of this parasitic group in freshwater fishes of Mexico Canada. Canadian Special Publication of Fisheries and 199: Aquatic 1-269. is increasing very rapidlyet al. (see Kritsky and Mendoza-et McDonaldSciences T. and L. Margolis. 1995. Synopsis of the parasites of fishes Francoal. 2003; Mendoza-Palmero and Aguilar-Aguilar of Canada. 122: 1-265. Astyanax 2008; Mendoza-Franco 2009; Mendoza-Palmero Mendoza-Franco, E., R.G. Reina and M. Torchin.Diaphorocleidus 2009. Dactylogyrids 2009). From a biogeographical perspective, it is also (Monogenoidea)Characithecium parasitizing the gillsJournal of of Parasitology spp (Characidae) possible that the Nearctic freshwater fish host a larger from Panama and Mexico, a new species of and a proposal for n. gen. Urocleidoides 95(1): proportion of adult helminth parasites than larval forms. vaginoclaustrum46-55. Our data seems to support that contention, however, a Mendoza-Palmero, C. and R. Aguilar-Aguilar. 2008. Record of comparative analysis needs to be conducted to corroborate Parasitology Research Jogunoori, Kritsky and Venkatanarasaiah, 2004 (Monogenea: Dactylogyridae) from a freshwater fish in Mexico. that observation, and to determine if this may rule out as Gyrodactylus 103: 1235-1236. a general pattern or if it is only found for some particular Mendoza-Palmero, C., A.L. Sereno-Uribe andGirardinichthys G. Salgado-Maldonado. multiradiatus 2009. host groups such as ictalurids. For instance, Rosas-Valdez Two new species of Von Nordmann, 1832 (Monogenea: Gyrodactylidae)Journal parasitizing of Parasitology and Pérez-Ponce de León (2008) compared the helminth (Monogenea: Gyrodactylidae), an endemic freshwaterFreshwater fish fishes from of parasite fauna of ictalurids (a Nearctic element) and MexicoCentral Mexico. 95(2): 315-318. heptapterids (a Neotropical element) in Mexico. These Miller, R.R., W.L. Minckley and S.M. Norris. 2005. . Chicago: The University of Chicago Press. 490 p. In authors found that the former harbors 33 adults and 18 Návar, J., H. Hernández and J. Ríos. 2006. Temporal Tendencies of River larvae along its distributional range, while heptapterids MonitoringDischarge ofScience Five Watershedsand Technology of Northern Symposium: Mexico; Unifying p. 710-714Knowledge are parasitized by 20 adults and 32 larvae. forAguirre-Bravo, Sustainability C., J.P. in Pellicane, the Western D.P. Burns Hemisphere and S. Draggan (ed). Much has been accomplished in the last few years in . Forth Collins: terms of survey work on the helminth parasite fauna Proceedings RMRS-P-42CD, U.S. Department of Agriculture, Forest of freshwater fishes in Mexico. Still, inventory work Service, Rocky Mountain Research Station. Pérez-Ponce de León, G. and A. Choudhury. 2002. Adult endohelminthComparative is required in other northern portions of the country, Parasitologyparasites of ictalurid fishes (Osteichthyes: Ictaluridae) in Mexico: but the information gathered thus far allow us to seek empirical evidence for biogeographical patterns. for general patterns about the way this host-parasite 69(1): 10-19. Pérez-Ponce de León, G. andJournal A. Choudhury.of Biogeography 2005. Biogeography of association is established, addressing the evolutionary and helminth parasites of freshwater fishes in México: the search for Acknowledgements:biogeographical factors that determine such association. patterns and processes. 32: 645–659. Pérez-Ponce de León, G., L. García-Prieto and B. Mendoza-Garfias. 2007. This study was supported by grants from the Trematode Parasites (Platyhelminthes) of Wildlife Vertebrates in Comisión Nacional para el Conocimiento y Uso de la Biodiversidad Mexico. Zootaxa 1534: 1-250.Listados faunísticos de México VI. Helmintos (CONABIO FM001), Consejo Nacional de Ciencia y Tecnología (CONACyT Pérez-Ponceparásitos de peces León, de G.,aguas L. García-Prieto,continentales de D. México Osorio-Sarabia and V. 83043), and Programa de Apoyo a Proyectos de Investigación e León-Règagnon. 1996. Innovación Tecnológica (PAPIIT-UNAM IN 209608) to G.P.P.L. Thanks are . México D.F.: Serie also due to Jorge Falcón, David Hernández, Mirza Ortega, Miguel A. Piñón, Listados Faunísticos del Instituto de Biología, Universidad Nacional Oscar J. Pérez, and Omar Villegas for their help during some field trips. Autónoma de México.100 p. Mirza Ortega identified the cysticercoids and Lorena Garrido identified Pérez-Ponce de León, G., R. Rosas-Valdez, B. Mendoza-Garfias, R. Aguilar- the larval nematodes. This paper was written during the sabbatical leave Aguilar, J. Falcón-Ordaz, L. Garrido-Olvera and R. Pérez-Rodríguez.Zootaxa of G.P.P.L. at the University of California-Davis under the support of a 2009. Survey of the endohelminth parasites of freshwater fishes in fellowship granted by the program UC MEXUS-CONACyT (University of the upper Mezquital River Basin, Durango State, Mexico. California Institute for Mexico and the United States-Consejo Nacional de 2164: 1-20. Ciencia y Tecnología). Thanks are also due to Steve Nadler for facilities Rosas-Valdez, R. and G. Pérez-Ponce de León. 2008. Composición providedLiterature in his cited laboratory during sabbatical. taxonómica de los helmintos parásitosRevista de ictalúridos Mexicana de y heptaptéridos Biodiversidad (Osteychthyes: Siluriformes) de México, con una hipótesis de homología biogeográfica primaria. Aguilar-Aguilar, R., G. Salgado-Maldonado, R.Biological Contreras-Medina Journal of and the 79(2): 473-499. A.Linnean Martínez-Aquino. Society 2008. Richness and endemism of helminth Salgado-Maldonado, G., N. Mercado-Silva, G. Cabañas-Carranza, J. Caspeta- parasites of freshwater fishes in Mexico. Mandujano, R. Aguilar-Aguilar and I. Iñiguez-Dávalos.Comparative 2004a. 94: 435-444. ParasitologyHelminth Parasites of Freshwater Fishes of the Ayuquila River, Sierra Castañeda-Gaytán, G., C. García-de la Peña, D. Lazcano Bulletin and A. Salas-of the de Manantlán Biosphere Reserve, West Central Mexico. ChicagoWestphal. Herpetological 2005. Notes Societyon Herpetofauna 7: Herpetological Diversity 71(2): 67-72. of the Low Basin of the Nazas River, Durango, México. Salgado-Maldonado, G., G. Cabañas-Carranza, E. Soto-Galera, R. Pineda- Listados Faunísticos de México III. 40(3): Los Peces 34-37. Dulceacuícolas Mexicanos López, J. Caspeta-Mandujano, E. Aguilar-CastellanosComparative Parasitology and N. Mercado- Espinosa-Pérez, H., M.T. Gaspar-Dillanés and P. Fuentes-Mata. 1993. Silva. 2004b. Helminth Parasites of Freshwater Fishes of the Pánuco . River Basin, East Central Mexico. 71(1): México D.F.: Instituto de Biología Universidad Nacional Autónoma de 190-202. México. 98 p. Folia Parasitologica Salgado-Maldonado, G., R. Aguilar-Aguilar, G Cabañas-Carranza,Parasitology E. Ergens, R. 1969. The suitability of ammonium picrate-glycerin in ResearchSoto-Galera and C. Mendoza-Palmero. 2005. Helminth parasites in preparing slides of lower monogenoidea. 16: 320 freshwater fish from the Papaloapan River basin, Mexico. Garrido-Olvera, L., L. García-PrietoZootaxa and G. Pérez-Ponce de León. (2006) 96: 69-89. Checklist of the Parasites adult nematode of North parasitesAmerican offreshwater fishes in fishes freshwater localities from Mexico. , 1201: 1-45. Hoffman, G.L. 1999. , 2 ed. Received: June 2009 Ithaca:Pavanelliella Cornell University scaphiocotylus Press. 539 p. Revised: October 2009 Kritsky, D.C. and Mendoza-Franco, E. 2003. NeotropicalRhamdia Monogenoidea guatemalensis Accepted: November 2009 42. sp. nov. (Dactylogyridae) from the Published online: February 2010 nasal cavity of the Guatemalan Chulin, Editorial responsibility: Luis C. Muniz Check List | Volume 6 | Issue 1 | 2010 035