Endohelminth parasites of seven goodein species (Cyprinodontiformes: Goodeidae) from Lake Zacapu , Michoacán, Central Mexico Plateau
Endohelmintos parásitos de siete especies de godeinos (Cyprinodontiformes: Goodeidae) del lago de Zacapu, Michoacán, en la Mesa Central de México
Andrés Martínez–Aquino,1,2 Rodolfo Pérez–Rodríguez,1,2 David I. Hernández–Mena,1,2 Lorena Garrido–Olvera,2,3 Rogelio Aguilar–Aguilar4 and Gerardo Pérez–Ponce de León1
1 Instituto de Biología, Universidad Nacional Autónoma de México (UNAM), Apartado Postal 70–153, México, D.F. 04510. México. E– mail: ppdleon@ibiologia.unam.mx
2 Posgrado en Ciencias Biológicas, UNAM. México, D.F. México.
]]> 3 Instituto de Ecología, UNAM, México, D.F. México.4 Departamento de Biología Comparada, Facultad de Ciencias, UNAM, México D.F. México.
Recibido: 15 de abril de 2011.
Aceptado: 19 de septiembre de 2011.
ABSTRACT
A total of 11 parasitic endohelminth taxa were found in 7 freshwater fish species of the subfamily Goodeinae in Zacapu Lake, Michoacan, Mexico. Six were adults (Margotrema cf. bravoae, Phyllodistomum sp., Saccocoelioides sogandaresi, Rhabdochona lichtenfelsi, Bothriocephalus acheilognathi and Caryophillidae gen. sp.), while the remaining 5 taxa (Clinostomum complanatum, Posthodiplostomum minimum, Tylodelphis sp., Eustrongylides sp. and Polymorphus brevis) were larvae. The taxa S. sogandaresi, Tylodelphis sp., and R. lichtenfelsi reached the highest levels of prevalence and mean abundance among all hosts, while the cestodes B. acheilognathi and Caryophillidae gen. sp. showed the lowest values. This study contributes with the inventory of the freshwater fish helminth fauna in Central Mexico Plateau, and particularly with the previous work that has been done with Goodeinae, a subfamily of freshwater fishes endemic to that part of the country.
Key words: Central Mexico Plateau, Goodeinae, helminth parasites.
]]> RESUMEN
En este trabajo se registran 11 taxa de helmintos endoparásitos de 7 especies de peces de la subfamilia Goodeinae del lago de Zacapu, Michoacán, en la mesa central de México. Seis taxa se registraron en estado adulto (Margotrema cf. bravoae, Phyllodistomum sp., Saccocoelioides sogandaresi, Rhabdochona lichtenfelsi, Bothriocephalus acheilognathi y Caryophillidae gen. sp.), en tanto que los 5 restantes correspondieron a larvas (Clinostomum complanatum, Posthodiplostomum minimum, Tylodelphys sp. y Eustrongylides sp. y Polymorphus brevis). Los taxa S. sogandaresi, Tylodelphis sp. y R. lichtenfelsi presentaron los valores más altos de prevalencia y abundancia en los peces estudiados, mientras que los céstodos B. acheilognathi y Caryophillidae gen. sp. presentaron los valores más bajos. Este estudio contribuye al inventario de la fauna helmintológica de peces de agua dulce de la mesa central de México y en particular al que ha sido realizado con Goodeinae, una subfamilia de peces dulceacuícolas endémica de esa parte del territorio nacional.
Palabras clave: Mesa central de México, Goodeinae, helmintos parásitos.
Goodeinae (Cyprinodontiformes: Goodeidae) represents a subfamily of viviparous freshwater fishes, which comprises 20 genera and 43 species, entirely endemic to river drainages and basins of central Mexico (Domínguez–Domínguez et al., 2012). The helminth fauna parasitizing these freshwater fishes has been intensively documented during the last two decades. Some papers have addressed the helminth assemblage in one single species of host (i.e., Martínez–Aquino et al., 2004, 2007b, 2009; Sánchez–Nava et al., 2004), while some others described the helminth fauna of three or more goodein species within the same locality (e.g., Peresbarbosa–Rojas et al., 1994; Pérez–Ponce de León et al., 2000; Mejía–Madrid et al., 2005; Romero–Tejeda et al., 2008).
Zacapu Lake, located in Central Mexico Plateau, in the state of Michoacán, is a medium–size water body fed by several springs, which shows a relatively low level of environmental degradation, and serves as habitat for diverse freshwater taxa. Because of this, it has been argued that this area is important from a conservational point of view (Medina–Nava et al., 2005; Domínguez–Domínguez et al., 2006; Martínez–Aquino et al., 2007a). The freshwater fish fauna of the lake includes 7 goodein species of which 6 have been partially studied for helminth parasites (Galicia–Guerrero, 2001; Pérez–Ponce de León, 2001; Mejía–Madrid et al., 2005). The aim of this work is to record the endohelminth parasite fauna of all the species of goodeins inhabiting Zacapu Lake, and provide the ecological infection parameters, such as prevalence and abundance.
On July 2009, a total of 161 adult specimens of goodeins belonging to the species Alloophorus robustus (Bean, 1892) (n = 17), Allotoca zacapuensis Meyer, Radda & Domínguez–Domínguez, 2001 (n = 32), Goodea atripinnis Jordan, 1880 (n = 20), Hubbsina turneride Buen, 1940 (n = 20), Skiffia lermae Meek, 1902 (n = 19), Xenotoca variata (Bean, 1887) (n = 21), and Zoogoneticus quitzeoensis (Bean, 1898) (n = 32), were collected in Zacapu Lake (19°49'35" N; 101°47'10'' W), using seine nets and electrofishing. Fishes were taken alive to the laboratory, sacrificed by pithing, and individually examined for endohelminth parasites. After dissection, gastrointestinal tract was removed and placed in a Petri dish with 0.65% saline. Other organs (eyes, liver, spleen, gall, swim and urinary bladders), and body cavity, were examined under a stereomicroscope in separate Petri dishes with saline 0.65%. Digeneans, nematodes and cestodes were fixed with 4% (steaming) formalin. Acanthocephalans were placed during 24 hrs in distilled water at 4 °C, and preserved in absolute ethanol. Plathyhelminths and acanthocephalans were stained with Mayers paracarmine. Nematodes were cleared with glycerin for light microscopy study. Voucher specimens of all taxa were deposited in the Colección Nacional de Helmintos (CNHE), Instituto de Biología, Universidad Nacional Autónoma de México, Mexico City. The use of prevalence (% infected), and abundance (mean number of parasites of a single species in the sample) follows Bush et al. (1997).
In total, 11 endohelminth parasite taxa were collected from the 7 analyzed host species. The endohelminth fauna includes 6 taxa of digeneans (3 adults and 3 larval stages), 2 adult cestodes, 2 nematodes (1 adult and 1 larvae), and 1 acanthocephalan (cystacanth). Rhabdochona lichtenfelsi Sánchez–Álvarez, García–Prieto & Pérez–Ponce de León, 1998, Tylodelphys sp., and Polymorphus brevis (Van Cleave, 1916), were the most widely distributed taxa among the host species. The adult nematode R. lichtenfelsi reached the highest levels of prevalence and mean abundance. Allotoca zacapuensis harbored 7 endohelminth taxa, whereas the remaining fish hosts were parasitized by 4–5 endohelminth taxa. Endohelminth parasite taxa, prevalence and abundance, as well as the new host and locality records herein established are shown in Table 1.
Four endohelminth taxa are reported in Zacapu Lake for the first time, and in addition to that, 21 new host records are established in this paper. The endohelminth fauna of Skiffia lermae is reported for the first time, meanwhile for the goodeins Allotoca zacapuensis, Hubssina turneri, and Zoogoneticus quitezeoensis, the known endohelminth parasite fauna was duplicated with respect to previous records. Our study brings the total number of helminth parasites of goodeins in Zacapu Lake to 18 (Galicia–Guerrero, 2001; Pérez–Ponce de León, 2001; Mejía–Madrid et al., 2005). Additionally, with 64.3% of the fish fauna studied thus far for helminth parasites, our data increase the knowledge about the freshwater fish parasite fauna of this locality in 30%.
The endohelminth fauna of goodeins in Zacapu Lake include at least 2 species which have been considered as specialists to Goodeinae, i.e., Margotrema cf. bravoae Lamothe–Argumedo, 1970, and Rhabdochona lichtenfelsi (Pérez–Ponce de León et al., 2000; Mejía–Madrid et al., 2005, 2007; Pérez–Ponce de León & Choudhury, 2005). The adult digenean Phyllodistomum sp., could represent a third specialist species; however, this need to be determined once the taxonomic identity of the species is established. Morphologically similar specimens were recently recorded in the goodein fish Zoogoneticus purhepechus Domínguez–Domínguez, Pérez–Rodríguez et Doadrio, 2008 from a relatively close locality in the lower Lerma River (Martínez–Aquino et al., 2011). These specimens, along with those reported as Dendrorchis sp. by Martínez–Aquino et al. (2009) have been only recorded in goodeins in central Mexico and may be conspecific. Moreover, they could represent a new species; although until additional taxonomic work based on morphology and molecular markers is carried out, their identities remain uncertain. In contrast, 8 generalist helminth taxa were recorded in the analyzed hosts both as adult or larval stages: Saccocoelioides sogandaresi Lumsden, 1963, Clinostomum complanatum (Rudolphi, 1819), Posthodiplostomum minimum (MacCallum, 1921), Tylodelphys sp., Bothriocephalus acheilognathi Yamaguti, 1934, Caryophyllidae gen. sp., Eustrongylides sp., and P. brevis.
]]> For this survey, specimens were collected only in one period during the year, preventing us from establishing a robust comparison of the parasite fauna among analyzed species of hosts, or even between the records we establish in this work, and those previously made for other authors. However, our data correspond with the general pattern described for most species of freshwater fishes occurring in different river basins in central Mexico, i.e., a species–poor helminth fauna, highly dominated by one species of helminth (Pérez–Ponce de León et al., 2000). In particular, ecological parameters of the parasitic infections herein reported coincide with those previously reported for other species of goodeins, i.e., the nematode Rhabdochona lichtenfelsis, as well as larval digeneans reach the highest prevalence and abundance values (Martínez–Aquino et al., 2004, 2007b; Romero–Tejeda et al., 2008),The results we provide in this paper contribute to our understanding of the helminth parasite fauna of goodeins in Central Mexico Plateau, but also further contribute with the inventory of the Mexican freshwater fish parasite fauna.
ACKNOWLEDGEMENTS
We thank the local people of Zacapu for providing access to Zacapu Lake, particularly we are gratefull with those in charge of "Balneario La Angostura" for access to the type locality of Allotoca zacapuensis. We appreciate the valuable comments of reviewers. A.M.A., R.P.R., L.G.O., and D.I.H.M. thank to CONACyT for the scholarship received to complete their graduate programs within the Posgrado en Ciencias Biológicas, UNAM. This work was partially supported by grants from the Consejo Nacional de Ciencia y Tecnología (CONACyT 83043), and Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT–UNAM IN 209608 and IN202111) to G.P.P.L.
REFERENCES
Bush, A. O., K. D. Lafferty, L. L. Lotz & A. W. Shostak. 1997. Parasitology meets ecology on its own terms: Margolis et al., revisited. Journal of Parasitology 83 (4): 575–583. [ Links ]
Domínguez–Domínguez, O., E. Martínez–Meyer, L. Zambrano & G. Pérez–Ponce de León. 2006. Using ecological–niche modeling as a conservation tool for freshwater species: live–bearing fishes in Central Mexico. Conservation Biology 20 (6): 1730–1739. [ Links ]
Domínguez–Domínguez, O., C. Pedraza–Lara, N. Gurrola–Sánchez, R. Pérez–Rodríguez, I. Israde–Alcántara, V. H. Garduño–Monroy, I. Doadrio, G. Pérez–Ponce de León & D. R. Brooks. 2012. Historical biogeography of the Goodeinae (Cyprinodontiforms). In Uribe–Aranzabal, M. C. & H. Grier (Eds.). Viviparous Fishes Vol II. New Life Publications, Homestead, pp. 13–30. [ Links ]
Galicia–Guerrero, S. 2001. Helmintos parásitos de algunas especies de peces en el Lago de Zacapu, Michoacán. Tesis de Maestría, Facultad de Ciencias, UNAM, México. 127 p. [ Links ]
Martínez–Aquino, A., G. Salgado–Maldonado, R. Aguilar–Aguilar, G. Cabañas–Carranza & M. P. Ortega–Olivares. 2004. Helminth parasites of Chapalichthys encaustus (Pisces: Goodeidae), an endemic freshwater fish from Lake Chapala, Jalisco, Mexico. Journal of Parasitology 90 (4): 889–890. [ Links ]
Martínez–Aquino, A., R. Aguilar–Aguilar, H. O. Santa Anna del Conde–Juárez & R. Contreras–Medina. 2007a. Empleo de herramientas panbiogeográficas para detectar áreas para conservar: un ejemplo con taxones dulceacuícolas. In: Luna, I., J. J. Morrone & D. Espinosa (Eds.). Biodiversidad de la Faja Volcánica Transmexicana. Facultad de Ciencias, Universidad Nacional Autónoma de México. México, D. F., pp. 449–460. [ Links ]
Martínez–Aquino, A., G. Salgado–Maldonado, R. Aguilar–Aguilar, G. Cabañas–Carranza & C. A. Mendoza–Palmero. 2007b. Helminth parasite communities of Characodon audax and C. lateralis (Pisces: Goodeidae), endemic freshwater fishes from Durango, Mexico. The Southwestern Naturalist 52 (1): 125–130. [ Links ]
Martínez–Aquino, A., R. Aguilar–Aguilar, R. Pérez–Rodríguez & G. Pérez–Ponce de León. 2009. Helminth parasites of Xenotaenia resolanae (Osteichthyes: Cyprinodontiformes: Goodeidae) from the Cuzalapa Hydrological System, Jalisco, Mexico. Journal of Parasitology 95 (5): 1221–1223. [ Links ]
Martínez–Aquino, A., D. I. Hernández–Mena, R. Pérez–Rodríguez, R. Aguilar–Aguilar & G. Pérez–Ponce de León. 2011. Endohelminth parasites of the freshwater fish Zoogoneticus purhepechus (Cyprinodontiformes: Goodeidae) from two springs in the lower Lerma River, Mexico. Revista Mexicana de Biodiversidad82 (4): 1132–1137. [ Links ]
Medina–Nava, M., J. Lyons, T. Zubieta–Rojas, E. Solorio–Ornelas, J. P. Ramírez–Herrejón & R. Galván–Morales. 2005. Conservation of two sites in Central Mexico with a high diversity of livebearing fishes. In: Uribe, M. C. & H. Grier (Eds.). Viviparous Fishes. New Life Publications. Homestead, pp. 499–504. [ Links ]
Mejía–Madrid, H., O. Domínguez–Domínguez & G. Pérez–Ponce de León. 2005. Adult endohelminth parasites of Goodeinae (Cyprinodontiformes: Goodeidae) from Mexico with biogeographical considerations. Comparative Parasitology 72 (2): 200–211. [ Links ]
Mejía–Madrid, H., E. Váquez–Domínguez & G. Pérez Ponce de Léon. 2007. Phylogeography and freshwater basins in central Mexico: recent history as revealed by the fish parasite Rhabdochona lichtenfelsi (Nematoda). Journal of Biogeography 34: 787–801. [ Links ]
Peresbarbosa–Rojas, E., G. Pérez–Ponce de León & L. García–Prieto. 1994. Helmintos parásitos de tres especies de peces (Goodeidae) del lago de Pátzcuaro, Michoacán. Anales del Instituto de Biología, Universidad Nacional Autónoma de México, Serie Zoología 65 (1): 201–204. [ Links ]
Pérez–Ponce de León, G. 2001. Margotrema guillerminae n. sp. (Trematoda: Macroderoididea) from two species of freshwater fishes in Lake Zacapu. Michoacan state, Mexico, and new records of Margotrema bravoae Lamothe, 1970. Journal of Parasitology 87 (5): 1112–1114. [ Links ]
Pérez–Ponce de León, G., L. García–Prieto, V. León–Regagnon & A. Choudhury. 2000. Helminth communities of native and introduced fishes in Lake Pátzcuaro, Michoacán, Mexico. Journal of Fish Biology 57 (2): 303–352. [ Links ]
Pérez–Ponce de León, G. & A. Choudhury. 2005. Biogeography of helminth parasites of freshwater fishes in Mexico: the search for patterns and processes. Journal of Biogeography 32: 645–659. [ Links ]
Romero–Tejeda, M. L., L. García–Prieto, L. Garrido–Olvera & G. Pérez–Ponce de León. 2008. Estimation of the endohelminth parasite species richness in freshwater fishes from La Mintzita reservoir, Michoacán, Mexico. Journal of Parasitology 94 (1): 288–292. [ Links ]
Sánchez–Nava, P., G. Salgado–Maldonado, E. Soto–Galera & B. Jaimes–Cruz. 2004. Helminth parasites of Girardinichthys multiradiatus (Pisces: Goodeidae) in the upper Lerma River sub–basin, Mexico. Parasitology Research 93 (5): 396–402. [ Links ]
]]>