Helminth communities of Xiphophorus malinche (Pisces: Poeciliidae), endemic freshwater fish from the Pánuco River, Hidalgo, Mexico

Comunidades de helmintos de Xiphophorus malinche (Pisces: Poeciliidae), especie dulceacuícola endémica del río Pánuco, Hidalgo, México

Christian Elizbeth Bautista-Hernández¹, Juan Violante-González², Scott Monks^1* y Griselda Pulido-Flores¹

¹ Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo. Apartado postal 1-10, 42001 Pachuca, Hidalgo, México. * scottmonks@hotmail.com

Recibido: 24 julio 2013
Aceptado: 30 abril 2014

Abstract

A total of 141 highland swordtails, Xiphophorus malinche, were collected from 2 localities in the Pánuco river drainage (Chicayotla and Malila) from Hidalgo, México. The parasite community structure of the 2 localities was examined and compared. Five taxa of helminths were recovered: 2 digeneans, adults of Paracreptotrema sp. and metacercariae of Uvulifer sp.; an adult monogenean, Urocleidoides vaginoclastrum; an adult cestode, Bothriocephalus acheilognathi, and an adult nematode, Rhabdochona xiphophori. Among them, Ur. vaginoclastrum was the most frequent and abundant species. The remaining species were rare and found at low mean abundance. Only 2 species of helminth were found at both localities. The observed species richness, individual abundance, and diversity were low at component community and infracommunity levels. Abundance of helminths and fish standard length were correlated. Uvulifer sp. was more abundant in small fish, but Ur. vaginoclastrum showed the opposite pattern, high abundance in larger fish. Differences observed in this study can be attributed to abiotic and biotic environmental factors resulting from the geographic separation of these localities during to the orogeny of the Sierra Madre Oriental that restricted fish to isolated headwaters.

Key words: component community, infracommunity, Sierra Madre Oriental, prevalence, abundance, diversity.

Resumen

Palabras clave: componente de comunidad, infracomunidad, sierra Madre Oriental, prevalencia, abundancia, diversidad.

Introduction

The genus Xiphophorus (Pisces: Poeciliidae) nominally has 26 species, commonly called swordtails or platyfish, which are distributed in freshwater streams from northeastern México to eastern Honduras. In the Mexican drainages, the species are found in parts of the coastal plain and on the eastern to southeastern slopes of the Sierra Madre Oriental, but never beyond the barrier range of the Mexican plateau (Kallman and Kazianis, 2006). Several studies of the phylogeny of the genus have been conducted (e.g., Meyer et al., 1994; Marcus and McCune, 1999) and the results support the recognition of 3 principal clades. Xiphophorus malinche Rauchengerber, Kallman and Morizot, 1990 (Highland swordtail) is 1 of 9 members of the clade that inhabits the tributaries of the Río Pánuco basin. Its distribution is restricted to headwaters and highland streams of the Río Pánuco (Kallman and Kazianis, 2006; Culumber et al., 2011). Xiphophorus malinche has been the focus of the variety of behavioral ecology studies (Culumber et al., 2012; Verzijden et al., 2012), but, to date, only 4 species of Xiphophorus have been examined for helminth parasites (Salgado-Maldonado et al., 2004, 2005; Salgado-Maldonado, 2006), and X. malinche was not included in any of those studies. Furthermore, none of those studies described the parasite communities in a quantitative form. Therefore, the main goal of the present work is to record the helminth fauna of X. malinche and to describe the structure of its helminth community.

Materials and methods

Between May 2008 and July 2009, 141 adult specimens of X. malinche were collected using minnow traps. Fish were collected from 2 localities; Chicayotla (n= 81; 20°55'30" N, 98°34''36" W) and Malila (n= 60; 20°44'2" N, 98°42'54" W), belonging to the Arroyo Xontla and Río Conzintla, respectively, in the Pánuco drainage in Hidalgo, Mexico. Fish were taken alive to the laboratory of Centro de Investigaciones Científicas de las Huastecas Aguazarca (CICHAZ), pithed, and internal and external organs were examined for helminths. Helminths were collected, counted, and processed according to Monks et al. (2005). Infection parameters were calculated and applied according to definitions proposed by Bush et al. (1997). Analyses were made at the levels of component community (i.e., all the helminths in all fish collected per site) and infracommunity (i.e., all the helminths in each individual host, Holmes, 1986; Zander, 2001). In order to determinate if the sample size was sufficient, accumulative species curve was plotted and the observed values fitted to the Clench Model to assess an asymptotic trend (Clench, 1979; Magurran, 2004). The non-parametric species richness estimator Bootstrap was calculated to estimate the number of missing species for each component community (Poulin, 1998). To describe the component community, the total number of species of helminth, the total number of individual helminths, the Simpson index (H), as a measure of diversity, and the Berger-Parker Index, as a measure of numerical dominance, were used (Magurran, 2004). Infracommunity level parameters were described by using the mean of number of species of helminth per fish, the mean number of individual helminths, and the mean Brillouin Diversity Index value per host. Finally, the infracommunities were compared qualitatively within the locality using the Jaccard similarity index and quantitatively using the Morisita-Horn index (Magurran, 2004). Possible differences in abundance for species recorded in the 2 localities were evaluated using Chi²-test. Correlations were carried out using Spearman's Rank test. Voucher specimens of helminths were deposited in the Colección Nacional de Helmintos (CNHE), Universidad Nacional Autónoma de México, México D. F.; the Harold W. Manter Laboratory of Parasitology, University of Nebraska Lincoln, Lincoln, Nebraska, USA; and the Colección de Helmintos, (CHE), Universidad Autónoma del Estado de Hidalgo, Mexico. Specimens deposited include Bothriocephalus acheilognathi Yamaguti 1934 (CNHE-9267), Paracreptotrema sp. (CHE-9263 to 9266; HWML-75051 to 75054), Urocleidoides vaginoclastrum Jogunoori, Kritsky and Venkatanarasaiah, 2004 (CNHE4376, 9270 to 9275; HWML-75046 to 75050, 64628 to 64633), and Rhabdochona xiphophori Caspeta-Mandujano, Moravec and Salgado-Maldonado, 2001 (CHE-9268, 9269; HWML-64624 to 64627).

Results

In Chicayotla, 2 067 individual helminths were collected, represented by 4 species; Uvulifer sp., R. xiphophori, U. vaginoclastrum and B. acheilognathi. Infection parameter values for each taxon are shown in Table 1. The data indicate that U. vaginoclastrum, as well as R. xiphophori and Uvulifer sp. were frequent (prevalence > 60%) and abundant (mean intensity > 3.8), and B. acheilognathi was the only rare species (infrequent and of low mean intensity). Of the 81 individual fish, 20 were infected with at least 1 species of helminth, 36 harbored 2 species, and 22 fish had a maximum of 3 species. The total number of individuals of all species per fish ranged from 1 to 161, with a mean number of helminths per host 25.51±33.35. The mean number of species per fish was 1.95±0.82. The Brillouin index ranged from 0 to 0.85, with a mean diversity value of 0.39±0.20. The Berger-Parker dominance index values ranged from 0.5 to 0.99, with a mean value of 0.83±0.12.

In the locality of Malila 417 individual helminths of 3 species were collected: Ur. vaginoclastrum, R. xiphophori, and Paracreptotrema sp. Infection parameters for each taxa of helminth are given in Table 1. Urocleidoides vaginoclastrum had the highest prevalence and abundance (57% and 6.7 helminths per fish, respectively), and the remaining species were rare and infrequent. The total number of individual helminths of all species per fish ranged from 1 to 67, with a mean number of 6.95±12.44 individuals per host. The infracommunity in fish of Malila was species-poor; of 60 fish, 35 were infected with 1 species of helminth, 3 fish had 2 species, and 1 fish had a maximum of 3 species. The mean number of species per host was 0.70±6.95. It was not possible to calculate the Brilloin index because the number of infracommunities with more than 2 species of helminth was low. The Berger-Parker dominance index values ranged from 0.50 to 0.98, with a mean of 0.75±0.17.

The comparison between the helminth fauna of both study sites indicated that there are differences in the composition of species present in each site. Uvulifer sp. and B. acheilognathi were found only in fish of Chicayotla, and Paracreptotrema sp. was collected only from fish of Malila. Rhabdochona xiphophori and U. vaginoclaustrum were the species common to both component communities (Table 1), resulting in a Jaccard value of 0.40 and Morisita-Horn value of 0.97. The latter value showed that the component communities were highly influenced by the abundance of the dominant species. The Simpson diversity index was 0.31 in Chicayotla and 0.04 in Malila; the community at Chicayotla was more diverse than that at Malila. Evenness values were 0.46 in Chicayotla and 0.37 in Malila, relatively similar values. The Berger-Parker dominance index values were 0.81 in Chicayotla and 0.97 in Malila, and both localities were numerically dominated by Ur. vaginoclastrum.

No differences were observed between the sex of fish and the infection parameters or richness for any of the recorded helminth species. However, a significant correlation between mean abundance and fish size was observed. In Chicayotla, host size had a negative correlation with mean abundance of the metacercariae, Uvulifer sp. (r_s= -1; p< 0.01); and in Malila, mean abundance of U. vaginoclastrum was positively correlated with host size (r_s= 0.34; p< 0.04); none of the remaining species had a significant correlation in either population.

Discussion

Most of the species of helminths registered in this study have been recorded previously as parasites of species of Xiphophorus in other bodies of water in México (Salgado-Maldonado, 2006; Mendoza-Palmero and Aguilar-Aguilar, 2008). However, this is the first report of the digenean Paracreptotrema in Xiphophorus, although P. heterandriae has been reported recently from a species of Poeciliidae (Heterandria bimaculata [Heckel, 1848], sensu Salgado-Maldonado et al. 2012; =Pseudoxiphophorus "bimaculata" sensu Agorreta et al. 2013), P. profundulusi from 2 species of Profundulidae (Profundulus punctatus [Günther, 1866] and P. balsanus Ahl, 1935), and P. blancoi Choudhury, Pérez-Ponce de León, Brooks, and Daverdin, 2006 from P. punctatus, P. balsanus, and P. oaxacae (Meek, 1902) (Salgado-Maldonado et al., 2011). It should be noted that Salgado-Maldonado et al. (2011) did not find specimens of Paracreptotrema in individuals of X. hellerii Heckel, 1848 sympatric with P. balsanus and P. punctatus.

With respect to the other species of helminth, Urocleidoides vaginoclaustrum is a species originally described from Xiphophorus hellerii Heckel, 1848, a commonly kept aquarium species native to southern México and Central America that had been introduced to India (Jogunoori et al., 2004). It is possible that this monogenean originated in the neotropics, where its host also originated. Recently, Mendoza-Palmero and Aguilar-Aguilar (2008) made the first report of U. vaginoclaustrum in a natural habitat, parasite of the gills of X. hellerii introduced to the Los Berros spring, Durango, México. However, the authors observed that there were slight morphological differences in the sclerotized structures of the haptor in their specimens with respect to the specimens described from India, which they speculated might be due to differences in the fixation method used in their study. Although the specimens collected in the present study conform generally to previous descriptions, the fine morphology of the worms collected in Malila and Chicayotla should be reviewed and compared to the specimens of U. vaginoclaustrum from Durango and those from India to determine whether morphological differences are real or just artifacts of fixation methods. Xiphophorus hellerii also has been introduced to Hidalgo (Culumber et al., 2013), although its helminthofauna has not been reported.

Species of Rhabdochona are well known for host specialization at the family, genus and species level (Sánchez-Álvarez et al., 1998; Mejía-Madrid and Pérez-Ponce de León, 2003). Rhabdochona xiphophori originally was described in Xiphophorus sp. from the Pánuco drainage (Caspeta-Mandujano et al., 2001) and is now considered a specialist parasite of the Poeciliidae because it has been reported only from water bodies inhabited by X. hellerii, infecting only that species of fish (Mejía-Madrid et al., 2005). However, Mejía-Madrid et al. (2005) reported R. xiphophori as a parasite of 2 species of goodeids (Allotoca catarinae [de Buen, 1942] and Xenotoca eiseni [Rutter, 1896]), those authors suggested that this infection likely occurred due to ecological host-extension.

Habitat characteristics, both biotic and abiotic, may facilitate the establishment and spread of helminths in certain populations of host. Some variables, such as the size of the water body, physical-chemical characteristics of the water, and the distance between each body of water in the region, are factors that have been associated with the number of species of helminth in fish populations and the mean abundance of a given species of helminth (Bagge et al., 2004).

Another aspect that affects the community structure of parasites are the characteristics of the host (body size, age, geographic distribution, food habits, etc.), which can make certain potential hosts more susceptible to colonization by new parasites, in addition to the fact that evolutionarily older species have typically accumulated more parasites than comparatively younger species (Poulin, 1997). In the case of X. malinche, the species is restricted to headwaters of the Pánuco drainage, a habitat/locality that was formed during the uplifting and folding of the Sierra Madre Oriental. During this process populations became isolated in the headwaters of multiple, disconnected streams (Kallman and Kazianis, 2006). Differences in the habitat or environment, such as the aforementioned water chemistry, distance to other populations, etc., of these disconnected stream populations may account for differences in the parasite communities. However, more populations of fish must be sampled consistently in order to elucidate a strong hypothesis about structuring factors.

Pineda-López et al. (2005) pointed out that an important component in the determination of helminth parasite community composition of Mexican poeciliids is the dominance of generalist, allogenic species that use freshwater fish as a secondary intermediate host or as a paratenic host. Salgado-Maldonado (2006) documented the helminths parasites of 24 species of poeciliids and 100% of the communities of helminths of those hosts were dominated proportionally by larval stages (larval Digenea, Cestoda, Nematoda, and Acanthocephala). The only 4 species of Xiphophorus for which parasites were reported (Salgado-Maldonado, 2006) had the same pattern; the only other mention of the helminths of a species of Xiphophorus does not provide complete data (Salgado-Maldonado et al., 2011).

However, our data does not fit their prediction. The component community of X. malinche is dominated by adult helminths (mostly monogeans), although an allogenic species is present (1 of 5 species; 189 of 2067 individuals= 9%). One possible explanation for the low number of allogenic species and of larval parasites in general in our data is that fish-eating birds are rarely observed at the localities included in this study (CEBH personal observation). Migratory waterfowl play an important role on the transmission and spread of allogenic species (Pineda-López et al., 2005; Salgado-Maldonado, 2006). Martínez-Morales et al. (2007) reported few piscivorus birds within the distribution of X. malinche. The absence of large, ictiophagus birds in the region could be because of the relative lack of open areas around the upstreams of the Pánuco drainage and abiotic factors (i.e. water speed, type of perching area, etc.). However, 4 species of kingfisher have been reported in the Huasteca region (Martínez-Morales et al., 2007), although their helminths have not been studied. These species could be the definitive hosts of the larval digenean, Uvulifer sp., reported herein.

The infracommunities studied herein were generally species-poor (on average, only 1-2 species of helminth per fish) and were dominated by the monogenean Urocleidoides vaginoclaustrum. This is consistent with infracommunities reported for other freshwater fishes in México (Martínez-Aquino et al., 2004, 2007; Martínez-Aquino and Aguilar-Aguilar, 2008). Kennedy (1989) suggested that infracommunities with low rates of colonization, low numbers of species and of individuals, and with low or no presence of interspecific interactions is a general pattern in freshwater fishes. As well, the diet of a species of fish may also influence parasite species richness; this may be an influencing factor in the present study because 3 of the 5 species reported here for X. malinche infect the fish via dietary habits.

In the present study, U. vaginoclaustrum was the dominant species, but the abundance of the species varied significantly between the 2 localities (χ²= 7.11; p< 0.05). One factor that may determine the abundance of monogeneans on a host is the parasite's body size. Several studies have observed that as helminth body length increases, its abundance decreases, with the largest species of parasites naturally requiring more space and resources (Blackburn and Gaston, 1997; Poulin and Justine, 2008; Randhawa and Poulin, 2009). However, Poulin et al. (2008) has argued that this pattern does not always determine helminth parasite communities and those differences may be attributed to other interspecific factors.

Across all fish from Chicayotla, the metacercariae of Uvulifer sp. was found to have a negative correlation between parasite abundance and host body length. Lemly and Esch (1984) suggested that metacercariae of Uvulifer ambloplitis base their survival success and the completeness of their life cycle on the size of fish that it infects, such that the smaller the size of the host, the greater the abundance of metacercariae. Violante-González et al. (2009) found a similar pattern in cultivated fish, Oreochromis niloticus (Linnaeus, 1758), infected by Diplostomum (Austrodiplostomum) compactum (Lutz, 1928) Dubois, 1970. The authors suggested that this negative correlation might be due to behavioral differences between fingerlings and adults. Their reasoning was that small fish could get refuge among the aquatic vegetation, where they would be in constant proximity to snails (intermediate hosts), greatly increasing the probability of becoming infected (Violante-González et al., 2009).

The infections of U. vaginoclaustrum in fish from Malila revealed a positive correlation between parasite abundance and host body length. Öztürk and Altunel (2006) and Cable and van Oosterhout (2007) suggested independently that the abundance of this species of helminth increased with the age/size of the fish, since larger (and older) fish have a greater gill surface area, which permits abundance to increase over time, correlated with the increasing size of the host.

Because this is the first ecological study of the parasites of X. malinche, we cannot offer conclusive hypotheses, but, overall, our data indicate that the parasite communities of this species of fish are different in structure at the component level in each locality. We suggest that this is likely attributed to differences in local abiotic and biotic factors that determine the pool of species present in each locality. However, more solid hypotheses must await studies from additional localities and from sympatric species.

Acknowledgments

The authors thank all those who made possible the examination of specimens, especially Scott L. Gardner of HWML and Gabor Racz, Curator and Collection Manager, respectively, at the HWML, and Mary Hanson Pritchard, Affiliate of the HWML, who provided access to literature in the laboratory archives, and Luis García-Prieto (CNHE) who provided access to literature and specimens. Part of this manuscript was prepared during a Postdoctoral research visit to the HWML by the authors (SM and GPF); the HWML provided office and laboratory space, access to computers, the reprint collection, and microscopes. This study was supported by funds from the Patronato Universitario (Gerardo Soza Castelán, President), Universidad Autónoma del Estado de Hidalgo (UAEH), and the Consorcio de Universidades Mexicanas. We thank Gil G. Rosenthal, co-director of Centro de Investigaciones Científicas de las Huastecas Aguazarca, for allowing us to use the facilities and for the hospitality of the Laboratorio de Ecología, Unidad Académica de Ecología Marina, Universidad Autónoma de Guerrero, during a visit by CEBH (with a scholarship from the "Espacio Común de Educación Superior"). Zachary W. Culumber helped with collection and identification of fish. This work was supported by the project "Helmintos de algunas especies de Xiphophorus de la Huasteca Hidalguense" (Clave 091431) to SM from the Consejo Nacional de Ciencia y Tecnología and a scholarship from Conacyt to CEBH during her Ph.D. research project (217861).

Literature cited

Agorreta, A., O. Domínguez-Domínguez, R. G. Reina, R. Miranda, E. Bermingham and I. Doadrio. 2013. Phylogenetic relationships and biogeography of Pseudoxiphophorus (Teleostei: Poeciliidae) based on mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution 66: 80-90.         [ Links ]

Bagge, A. M., R. Poulin and E. T. Valtonen 2004. Fish population size, and not density, as the determining factor of parasite infection: a case study. Parasitology 128:305-313.         [ Links ]

Blackburn, T. M. and K. J. Gaston. 1997. A critical assessment of the form of the interspecific relationship between abundance and body size in animals. Journal of Animal Ecology 66:233-249.         [ Links ]

Bush, A. O., K. D. Lafferty, J. M. Lotz and A. W. Shostak. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83:575-583.         [ Links ]

Cable, J. and C. van Oosterhout. 2007. The impact of parasites on the life history evolution of guppies (Poecilia reticulata): the effects of host size on parasite virulence. International Journal for Parasitology 37:1449-1458.         [ Links ]

Caspeta-Mandujano, J. M., F. Moravec and G. Salgado-Maldonado. 2001. Two new species of rhabdochonids (Nematoda: Rhabdochonidae) from freshwater fishes in Mexico, with a description of a new genus. Journal of Parasitology 87:139-143.         [ Links ]

Clench, H. 1979. How to make regional lists of butterflies: some thoughts. Journal of the Lepidopterists' Society 33:216-231.         [ Links ]

Culumber, Z. W., H. S. Fisher, M. Tobler, M. Mateos, P. H. Barber, M. D. Sorenson and G. G. Rosenthal. 2011. Replicated hybrid zones of Xiphophorus swordtails along an elevational gradient. Molecular Ecology 20:342-356.         [ Links ]

Culumber, Z. W., S. Monks and R. Miranda. 2013. Report of Xiphophorus hellerii in the arid Metztitlán Canyon Biosphere Reserve in Mexico. Environmental Biology of Fishes online first print:1-5.         [ Links ]

Culumber, Z. W., D. B. Shepard, S. W. Coleman, G. G. Rosenthal and M. Tobler. 2012. Physiological adaptation along environmental gradients and replicated hybrid zone structure in swordtails (Teleostei: Xiphophorus). Evolutionary Biology 25:1800-814.         [ Links ]

Gutiérrez-Cabrera, A. E., G. Pulido-Flores, S. Monks and J. C. Gaytán-Oyarzún. 2005. Presencia de Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoidea: Bothriocephalidae) en peces de Metztitlán, Hidalgo, México. Hidrobiológica 15:283-288.         [ Links ]

Holmes, J. C. 1986. The structure of helminth communities. International Journal for Parasitology 17:203-208.         [ Links ]

Kallman, K. D. and S. Kazianis. 2006. The Genus Xiphophorus in Mexico and Central America. Zebrafish 3:271-285.         [ Links ]

Jogunoori, W., D. C. Kritsky and J. Venkatanarasaiah. 2004. Neotropical Monogenoidea 46. Three new species from the gills of introduced aquarim fishes in India, the proposal of Heterodylus n. g. and species of Urocleidoides Mizelle and Price, 1964 (Polyonchoinea: Dactylogyridae). Systematic Parasitology 58:115-124.         [ Links ]

Kennedy, C. R. 1989. Helminth communities in freshwater fish: structured communities or stochastic assemblages? In Pattern and processes in helminth parasite communities, G. W. Esch, A. O. Bush and J. M. Aho (eds.). Springer Netherlands, Houten. p. 131-156.         [ Links ]

Lemly, A. D. and G. W. Esch. 1984. Effects of the trematode Uvulifer ambloplitis on juvenile bluegill sunfish, Lepomis macrochirus: ecological implications. Journal of Parasitology 70:475-492.         [ Links ]

Magurran, A. E. 2004. Measuring biological diversity. Blackwell Publishing Company, Malden, Mass. 256 p.         [ Links ]

Marcus, J. M. and A. R. McCune. 1999. Ontogeny and phylogeny in the northern swordtail clade of Xiphophorus. Systematic Biology 48:491-522.         [ Links ]

Martínez-Aquino, A. and R. Aguilar-Aguilar. 2008. Helminth parasites of the pupfish Cyprinodon meeki (Pisces: Cyprinodontiformes), an endemic freshwater fish from North-Central Mexico. Helminthologia 45:48-51.         [ Links ]

Martínez-Aquino, A., G. Salgado-Maldonado, R. Aguilar-Aguilar, G. Cabañas-Carranza and C. Mendoza-Palmero. 2007. Helminth parasite communities of Characodon audax and C. lateralis (Pisces: Goodeidae), endemic freshwater fishes from Durango, Mexico. Southwestern Naturalist 52:125-130.         [ Links ]

Martínez-Aquino, A., G. Salgado-Maldonado, R. Aguilar-Aguilar, G. Cabañas-Carranza and M. P. Ortega-Olivares. 2004. Helminth parasites of Chapalichthys encaustus (Pisces: Goodeidae), an endemic freshwater fish from lake Chapala, Jalisco, Mexico. Journal of Parasitology 90:889-890.         [ Links ]

Martínez-Morales, M. A., R. Ortiz-Pulido, B. de la Barreda, I. L. Zuria, J. Bravo-Cadena and J. Valencia-Herverth. 2007. Hidalgo. In Avifaunas estatales de México: sociedad para el estudio y conservación de la aves en México, R. Ortiz-Pulido, A. Navarro-Sigüenza, H. Gómez-de Silva, O. Rojas-Soto and T. A. Peterson (eds.). CIPAMEX Pachuca, Hidalgo, México. p. 49-95.         [ Links ]

Mejía-Madrid, H. H., O. Domínguez-Domínguez and G. Pérez-Ponce de León. 2005. Adult endohelminth parasites of Goodeinae (Cyprinodontiformes: Goodeidae) from Mexico with biogeographical considerations. Comparative Parasitology 72:200-211.         [ Links ]

Mejía-Madrid, H. H. and G. Pérez-Ponce de León. 2003. Rhabdochona ahuehuellensis n. sp. (Nematoda: Rhabdochonidae) from the Balsas goodeid, Ilyodon whitei (Osteichthyes: Gooedeidae), in Mexico. Journal of Parasitology 89:356-361.         [ Links ]

Mendoza-Palmero, C. A. and R. Aguilar-Aguilar. 2008. Record of Urocleidoides vaginoclaustrum Jogunoori, Kritsky and Venkatanarasaiah, 2004 (Monogenea: Dactylogyridae) from a freshwater fish in Mexico. Parasitology Research 103:1235-1236.         [ Links ]

Meyer, A., J. M. Morrissey and M. Schartl. 1994. Recurrent origin of a sexually selected trait in Xiphophorus fishes inferred from a molecular phylogeny. Nature 368:539-542.         [ Links ]

Monks, S., V. R. Zárate-Ramírez and G. Pulido-Flores. 2005. Helminths of freshwater fishes from the Metztitlán Canyon Reserve of the Biosphere, Hidalgo, Mexico. Comparative Parasitology 72:212-219.         [ Links ]

Öztürk, M. O. and F. N. Altunel. 2006. Occurrence of Dactylogyrus infection linked to seasonal changes and host fish size on four cyprinid fishes in lake Manyas, Turkey. Acta Zoologica Academiae Scientiarum Hugaricae 52:407-415.         [ Links ]

Pineda-López, R., G. Salgado-Maldonado, E. Soto-Galera, N. Hernández-Camacho, A. Orozco-Zamorano, S. Contreras-Robledo, G. Cabañas-Carranza and R. Aguilar-Aguilar. 2005. Helminth parasites of viviparous fishes in Mexico. In Viviparous fishes, H. Grier and M. C. Uribe (eds.). New life publications, Homestead, Florida. p. 437-456.         [ Links ]

Poulin, R. 1997. Species richness of parasite assemblages: evolution and patterns. Annual Review of Ecology and Systematics 28:341-358.         [ Links ]

Poulin, R. 1998. Comparison of three estimators of species richness in parasite component communities. Journal Parasitology 84:485-490.         [ Links ]

Poulin, R. and J.-L. Justine. 2008. Linking species abundance distributions and body size in monogenean communities. Parasitology Research 103:187-193.         [ Links ]

Poulin, R., J. L. Luque, F. Guilhaumon and D. Mouillot. 2008. Species abundance distributions and numerical dominance in gastrointestinal helminth communities of fish hosts. Journal of Helminthology 82:193-202.         [ Links ]

Randhawa, H. S. and R. Poulin. 2009. Determinants and consequences of interspecific body size variation in tetraphyllidean tapeworms. Oecologia 169:759-769.         [ Links ]

Rauchenberger, M., K. D. Kallman and D. C. Morizot. 1990. Monophyly and geography of the Río Pánuco Basin swordtails (genus Xiphophorus) with descriptions of four new species. American Museum Novitates 2975:1-41.         [ Links ]

Salgado-Maldonado, G. 2006. Checklist of helminth parasites of freshwater fishes from Mexico. Zootaxa 1324:1-357.         [ Links ]

Salgado-Maldonado, G., R. Aguilar-Aguilar, G. Cabañas-Carranza, E. Soto-Galera and C. Mendoza-Palmero. 2005. Helminth parasites in freshwater fish from the Papaloapan River basin, Mexico. Parasitology Research 96:69-89.         [ Links ]

Salgado-Maldonado, G., G. Cabañas-Carranza, E. Soto-Galera, R. F. Pineda-López, J. M. Caspeta-Mandujano, E. Aguilar-Castellanos and N. Mercado-Silva. 2004. Helminth parasites of freshwater fishes of the Pánuco River Basin, East Central Mexico. Comparative Parasitology 71:190-202.         [ Links ]

Salgado-Maldonado, G., J. M. Caspeta-Mandujano and E. Martínez-Ramírez. 2011. Paracreptotrema profundulusi n. sp. and P. blancoi Choudhury, Pérez-Ponce de León, Brooks, and Daverdin, 2006 (Trematoda: Allocreadiidae) from freshwater fishes of the Genus Profundulus (Teleostei: Profundulidae) in Southern México. Journal of Parasitology 97:707-712.         [ Links ]

Salgado-Maldonado, G., J. M. Caspeta-Mabdujano and G. Vázquez. 2012. A new allocreadiid (Trematoda) species from freshwater fish Heterandria bimaculata (Teleostei: Poeciliidae) in Southeastern Mexico Journal of Parasitology 98:404-407.         [ Links ]

Salgado-Maldonado, G. and R. F. Pineda-López. 2003. The Asian fish tapeworm Bothriocephalus acheilognathi: a potential threat to native freshwater fish species in Mexico. Biological Invasions 5:261-268.         [ Links ]

Sánchez-Álvarez, A., L. García-Prieto and G. Pérez-Ponce de León. 1998. A new species of Rhabdochona Railliet, 1916 (Nematoda: Rhabdochonidae) from endemic goodeids (Cyprinodontiformes) from two mexican lakes. Journal of Parasitology 84:840-845.         [ Links ]

Verzijden, M. N., Z. W. Culumber and G. G. Rosenthal. 2012. Opposite effects of learning cause asymmetric mate preferences in hybridizing species. Behavioral Ecology 23:1133-1139.         [ Links ]

Violante-González, J., M. García-Varela, A. Rojas-Herrera and S. Guerrero. 2009. Diplostomiasis in cultured and wild tilapia Oreochromis niloticus in Guerrero State, Mexico. Parasitology Research 105:803-807.         [ Links ]

Zander, C. D. 2001. The guild as a concept and a means in ecological parasitology. Parasitology Research 87:484-488.         [ Links ]