Helminth parasites of Xiphophorus birchmanni (Teleostei:Poeciliidae) from two localities of the Pánuco River drainage, Mexico

Helmintos parásitos de Xiphophorus birchmanni (Teleostei: Poeciliidae) de dos localidades de la cuenca del río Pánuco, México

A total of 55 adult specimens of X. birchmanni were collected using minnow traps. Fish were collected from 2 localities on separate rivers; the first locality, Benito Juárez, Veracruz (n = 29; 20°52’56.73” N, 98°12’14.55” W), is part of Río Zontecomatlán, and the second, Atlatipa, Hidalgo (n = 26; 21°2’17.78” N, 98°22’33.79” W), is part of Río Atlapexco. Fish were captured using minnow traps and taken alive to the laboratory of the Centro de Investigaciones Científicas de las Huastecas “Aguazarca” (CICHAZ), where they were sacrificed and internal and external organs were examined for helminths. Parasites were collected, counted, and processed according to Monks et al. (2005). Parasites were identified with the reference to original descriptions of species mentioned in previous studies of helminths of freshwater fish of the region (Arizmendi-Espinosa, 1992; Bautista-Hernández, Monks et al., 2014; Bautista-Hernández, Monks, & Pulido-Flores, 2015; Scholz & Salgado-Maldonado, 2001) and pertinent keys (Hoffman, 1999). Infection parameters were calculated and applied according to definitions proposed by Bush et al. (1997) and Bautista-Hernández, Monks, Pulido-Flores, & Rodríguez-Ibarra (2015); prevalence (percent of fish that were infected), abundance (number of helminths per examined fish ± standard deviation) and mean intensity (mean number of helminths per infected fish). 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 (Bautista-Hernández, Monks, Pulido-Flores, & Rodríguez-Ibarra, 2015; Zander, 2001)]. In order to determine 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 (Bautista-Hernández et al., 2013; 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). We used the Jaccard index and Morisita-Horn index to compare the component communities between localities qualitatively and quantitatively (Magurran, 2004). Infracommunity level parameters were described by using the mean number of species of helminth per fish, the mean number of individual helminths, and the mean Brillouin Diversity Index value per host. Differences in abundance for species recorded in the 2 localities were evaluated using χ²-test. Voucher specimens of helminths were deposited in the Colección Nacional de Helmintos (CNHE-11056-11063), Universidad Nacional Autónoma de México, México D.F.

Results

Ten species of helminth were recovered from fish inhabiting the 2 sampled sites. The helminthological record enlisted 6 species of larval digenean (metacercariae) (Posthodiplostomum sp., Uvulifer sp., Centrocestus formosanus, Ascocotyle sp., Haplorchis pumilio, and Echinostomatidae gen. sp.), 2 species of monogenean (Urocleidoides vaginoclastrum and Gyrodactylus sp.), a larval cestode (metacestode stage; Glossocercus auritus), and a larval nematode (Eustrongylides sp.).

The cumulative species curve and the nonparametric species richness estimator value indicate that the inventory for both localities can be considered nearly complete (bootstrap: Benito Juárez = 10.95; Atlatipa = 3.12). In the locality of Benito Juárez, the non-parametric estimator predicted that 1 more species of helminth should be present in that population of fish. Statistical analysis showed no significant difference in either abundance of parasite species between localities or in the correlations with host size.

Table 1

Ecological quantitative parameters for the helminths of Xiphophorus birchmanni from 2 localities in the Pánuco river drainage. Note: N = number of fish collected; n = total number of helminths collected; % = prevalence; Ab. = abundance; I.P. = mean intensity.

	Benito Juárez			Atlatipa
	(N = 29)			(N = 26)
Helminths (site infection)	n	%	Ab.	I.P		n	%	Ab.	I.P.
Larval Digenea
Centrocestus formosanus (gills)	1,263	96.6	42.1	43.5		291	84.6	11.1	13.2
Uvulifer sp. (skin and fins)	3	10	0.1	1		3	7.6	0.11	1.5
Ascocotyle sp. (intestinal wall)	9	6.6	0.3	4.5
Haplorchis pumilio (base of fins)	67	16.6	2.2	13.4
Echinostomatidae gen. sp. (mesentery)	6	20	0.2	1
Posthodiplostomum sp. (mesentery)	3	10	0.1	1
Larval Cestoda
Glossocercus auritus (mesentery)	1	3.3	0.03	—
Monogenea
Gyrodactylus sp. (fins)	2	3.3	0.06	—
Urocleidoides vaginoclaustrum (gills)	377	96.6	12.5	13		546	100	21	21
Larval Nematoda
Eustrongylides sp. (mesentery)	5.0	16.6	0.1	1

The fish of Benito Juárez harbored 10 species of helminths: Posthodiplostomum sp., Uvulifer sp., C. formosanus, Ascocotyle sp., H. pumilio, Echinostomatidae gen. sp., U. vaginoclastrum, Dactylogyrus sp., G. auritus, and Eustrongylides sp. At the component community level, C. formosanus was the most abundant species, infecting 100% of the fish with a mean of 42 worms per host. The second most abundant species was U. vaginoclaustrum, with a prevalence of 100%, with 12.6 worms per fish. The remaining species were rare, infrequent, and with very low abundance values (Table 1). At the level of the helminth infracommunities, of the 29 fish that were necropsied, 8 individuals harbored at least 2 species of helminths, 16 fish were infected with 3 species of helminths, and 5 of the 29 fish harbored more than 4 species. The total number of individuals of all parasite species per host varied from 1 to 200, with a mean number of helminths per host of 60 ± 51. The mean number of species per host was 2.9 ± 0.75. The Brillouin index ranged from 0.25-1.08 with a mean diversity value of 0.58 ± 0.21. The Berger-Parker dominance index values ranged from 0.40-0.93 (0.68 ± 0.16).

In Atlatipa, fish were infected with only 3 species; U. vaginoclastrum, C. formosanus, and Uvulifer sp. (Tabla 1). The monogenean and the metacercarie of C. formosanus represent the species with the highest prevalence (100% and 84%, respectively). Uvulifer sp., was found rarely and infrequently. The total number of individual helminths per host ranged from 1 to 67, with a mean number of 32.3 ± 15.2 individuals per fish. At the infracommunity level, 3 of the 26 fish necropsied harbored 1 species of helminth, 22 were infected with 2 species of helminth and just 1 fish was parasitized with 3 species. The mean number of species per host was 1.9 ± 0.39. The Brillouin index values ranged from 0.00-0.64 with a mean diversity value of 0.43 ± 0.19 and the Berger-Parker dominance index values ranged from 0.5-1 (0.75 ± 0.15).

The fish studied herein belong to the same species, but we observed a difference in parasite richness between localities. Only 3 of the 10 species were shared between component communities: U. vaginoclaustrum, C. formosanus, and Uvulifer sp., resulting in a Jaccard value of 0.3 and a Morisita-Horn value of 0.70. The Simpson index values were similar in both component communities (Benito Juárez = 0.42; Atlatipa = 0.45), despite the fact that the component community of Benito Juárez had the highest species richness and that fish from Atlatipa harbored only 3 species. The Berger-Parker dominance index (d) values were 0.72 in Benito Juárez, dominanted by C. formosanus, and 0.65 in Atlatipa, dominanted by U. vaginoclaustrum.

Discussion

All species of helminths listed herein have been recorded previously in freshwater fishes of Mexican river drainages, including in fishes of the Pánuco River drainage (Bautista-Hernández, Monks et al., 2014; Salgado-Maldonado, 2006; Salgado-Maldonado et al., 2004) except the metacercariae of H. pumilio. This is the first time this species has been reported in the Pánuco River drainage and the first report of it infecting a species of Xiphophorus.

Eight of the 10 species reported in this study were represented by larval stages; as adults, all are parasites of fish-eating birds that serve as their definitive host. Centrocestus formosanus and H. pumilio are exotic species in México. These 2 species were introduced to Mexico along with the snail Melanoides tuberculata as a food resource for Mylopharyngodon piceus, a carp that also was introduced into the country for economic, fish-farming purposes (López-Jiménez, 1987). Many studies have focused on C. formosanus due to its importance as a widespread exotic species inhabiting many freshwater bodies in México, and for its relationship to fish aquaculture (Arizmendi-Espinosa, 1992; López-Jiménez, 1987; Scholz & Salgado-Maldonado, 2000). More recently, the metacercariae of Haplorchis pumilio have been found parasitizing native freshwater fishes in Mexico (Salgado-Maldonado et al., 2005; Scholz & Salgado-Maldonado, 2001; Vidal-Martínez et al., 2001). Until now, only 8 species of fish had been reported infected with this metacercariae; X. birchmanni now is added to this list. Ascocotyle sp., Uvulifer sp., and Posthodiplostomum sp. are generalists that are widely distributed in México due to the mobility of their final host, piscivorous birds. Salgado-Maldonado et al. (2004) found that Posthodiplostomum minimum was a common parasite of fishes in the Pánuco river drainage, infecting 10 species. Uvulifer ambloplitis has been found in just 4 species of fish of the region, and metacercariae of the Ascocotyle complex, Ascocotyle (Ascocotyle) tenuicollis, in just 1 species. Although the larvae Echinostomatidae gen. sp, could not be identified to the species level, digeneans of this family is known to use freshwater fishes as a second intermediate host, primarily through infection of fish-eating birds, as well as through mammals and reptiles (Hernández-Hernández, 2008).

Glossocercus auritus and Eustrongylides sp. also are parasites of fish-eating birds, but they are less widely distributed than the metacercariae mentioned above. Metacestodes of Glossocercus have been recorded before in the state of Hidalgo (Monks et al. [2005] reported Glossocercus sp.; Scholz & Salgado-Maldonado [2001] reported G. auritatus) with a low prevalence and abundance (a mean of 1 worm per fish). Scholz & Salgado-Maldonado (2001) suggested that G. auriatus could have a narrow definitive host specificity, limited to herons (Egretta and Casmerodius); however, since our specimens could not be identified to species, no hypotheses about specificity can be made. This is the first record of a species of Glossocercus infecting a species of Xiphophorus from the Pánuco drainage. Eustrongylides sp. has a wider distribution in Mexican drainages, but in the Pánuco River drainage larvae of the species have been reported previously from only 2 species, Herichthys labridens and Poecilia mexicana (Salgado-Maldonado et al., 2004).

Urocleidoides vaginoclaustrum was originally described from introduced aquarium fish X. hellerii in India; however, recently studies had been expanded its distribution to others hosts in Mexican drainages. So far, it has been found infecting mainly poeciliids, such as, X. hellerii (Mendoza-Franco et al., 2015; Mendoza-Palmero & Aguilar-Aguilar, 2008), Pseudoxiphophorus bimaculata (Salgado-Maldonado et al., 2014), X. malinche (Bautista-Hernández, Monks et al., 2014) and X. birchmanni (present work), but recently it had been recorded from the profundulid Profundulus labialis (Mendoza-Franco et al., 2015).

Gyrodactylus is a widely distributed genus of monogeneans that infect freshwater fishes. Due to its strict host and niche specificity, this genus typically is highly diverse. García-Vásquez et al. (2015) and Rubio-Godoy et al. (2010) have worked extensively working in the description of new species of Gyrodactylus infecting poeciliids in Mexican drainages; to date, there are 11 known species, parasitizing 4 species of poeciliid (Xiphophorus hellerii, Pseudoxiphophorus bimaculata, Poecilia mexicana, and Poecilopsis gracilis). Furthermore, García-Vasquez et al. (2015) reported the presence of up to 6 species of Gyrodactylus in a single species of host, suggesting that there exists a vast hidden diversity of parasites infecting this family of freshwater fish. In the Pánuco River drainage, the only record is of Gyrodactylus sp., infecting Astyanax mexicanus (Salgado-Maldonado et al., 2004), but those authors suggested that this unidentified species could be specific to characids.

The specimens assigned to Echinostomatidae gen. sp. cannot be dealt with further because they could only identified to the family; we assume that they are members of the same species but the validity of this assumption was not tested. For the same reason, we also cannot provide comparative data because of the differences in life-cycles of the members of the genus in México. Further collections and identification using molecular markers would be necessary to identify the species reported herein.

Component communities of the same species of host often share species of parasites but rarely have an identical species composition (Valtonen et al., 2001). In the present study we found that X. birchmanni had a distinct component community in each locality. Fish from Benito Juárez harbored 10 species of helminth and fish from Atlatipa were infected with just 3 species. Although the Simpson index indicated similar diversity of the two populations (Benito Juárez = 0.42; Atlatipa = 0.45), the localities share only 3 parasite species (J = 0.3), emphasizing that the Simpson index was biased by the dominant species (Magurran, 2004). Thus, as suggested by Valtonen et al. (2001) these assemblages of component communities were influenced and maintained by the pool of both current and locally-available species of helminth, driven by the biotic and abiotic factors on the availability of intermediate and definitive hosts.

At the infracommunity level, X. birchmanni harbored species-poor infracommunities; each individual host had, on average, 2 species of parasites, and each was dominated by 1 species, an autogenic species (U. vaginoclaustrum) in Atlatipa and an allogenic species in Benito Juárez (C. formosanus). Previous studies (Martínez-Aquino et al. 2004, 2007; Pineda-López et al., 2005) suggested that species-poor infracommunities that are dominated strongly by an allogenic species is a common pattern in freshwater fish in Mexico due to the trophic position of the small fish in the food web as prey of many species of piscivorous birds that disperse the generalist parasite species. This is true for the host population of Benito Juárez, which is dominated by C. formosanus. However, this prediction does not fit the results found in Atlatipa, where the dominant species was an autogenic, specialist species, U. vaginoclaustrum; this demonstrates how parasite communities can be influenced by locally-available species.

The helminth fauna of fish of the Pánuco River drainage is interesting to parasitologists because of the complexity of the populations of fish; however, the majority of the studies have not gone beyond simple lists of helminths parasites of different species of fish from this region (Salgado-Maldonado et al., 2004), or the description of new species (Bautista-Hernández, Monks, Pulido-Flores, & Miranda, 2015; Caspeta-Mandujano et al., 2001; Falcón-Ordaz et al., 2015), and few studies have focused on the analysis of parasite communities.

Bautista-Hernández, Monks et al. (2014), and  Bautista-Hernández, Monks, & Pulido-Flores (2015) described the communities of 3 species, including X. birchmanni, contrasting the helminth communities of a native species of fish with an introduced species in sympatry. Those authors reported 3 species of helminth infecting X. birchmanni, a monogenean, U. vaginoclaustrum, and two metacercariae, Uvulifer sp. and C. formosanus, in communities that were highly dominated by the monogenean. However, the 2 localities that they sampled belong to streams of the Pánuco River drainage (San Pedro and Huiznopala), where it was discovered later that the identification of specimens of X. birchmanni was problematic due to the potential presence of hybrid specimens of X. malinche and X. birchmanni in those populations (Culumber et al., 2011; Rosenthal et al., 2003). The specimens of X. birchmanni (collected in 2008) for the study of Bautista-Hernández, Monks et al. (2014), and Bautista-Hernández, Monks, & Pulido-Flores (2015) were identified using only morphological characters, which did not suggest evidence of hybridization at San Pedro nor at Huitznopala. However, in a study of reproductive and mating behavior of females using molecular markers, Paczolt et al. (2015) detected the presence of hybrid individuals at San Pedro.

Some studies have reported significant differences in parasite communities between parental species and their hybrids (El Gharbi et al., 1992; Moulia, 1999; Šimková et al., 2013). Since only morphological characters had been used for identification of the fish, we could not assume that the samples from 2008 were pure X. birchmanni. Thus, for this study we sought to add additional populations where hybridization was not probable, such as the localities studied herein. As such, the results of the present study of X. birchmanni and the comparisons with X. malinche, reported previously by Bautista-Hernández, Monks et al. (2014), represent records of parasite communities from pure populations of the parental species.

Bautista-Hernández, Monks et al. (2014) recently described the component communities of genetically-pure populations of X. malinche, a closely related species (Cui et al., 2013), in 2 localities in Hidalgo (Chicayotla and Malila). In Chicayotla, 4 species were reported (Uvulifer sp., U. vaginoclaustrum, Schyzocotyle acheilognathi, and Rhabdochona xiphophori) and in Malila, 3 species (Paracreptotrema rosenthali. R. xiphophori, and U. vaginoclaustrum). Although populations of X. malinche and X. birchmanni inhabit the same streams of the Pánuco drainage, pure populations are confined to different altitudes; X. malinche is restricted to highland streams, while X. birchmanni is found at lower elevations (Culumber et al., 2011) (populations containing hybrids are found in the junction of the 2 species). As had been observed, these 2 species have distinct helminth communities as a result of more than just having different specific identities. The former species had communities harboring 4 adult species of the 5 species that were reported and the latter had communities comprised mostly of larval stages (8 of 10 species).

Garrido-Olvera et al. (2012) observed a positive correlation between the geographic distribution (range) of hosts and their helminth species richness and argued that one of the most important factors that determine the composition of helminth communities in freshwater fish in México is the geographic range of the host. Thus, species with broad distributions had richer assemblages than those with a limited distribution because the members inhabit more localities and feed on a wider variety of prey. As well, the latter populations are exposed locally to colonization by more species of parasite than fishes with a narrow distribution. Culumber et al. (2011) reported that X. malinche is confined to fewer localities in the Pánuco drainage than X. birchmanni. Thus, according to the hypotheses of Garrido-Olvera et al. (2012), the difference in the distribution of these 2 species of fish is an important factor contributing to the differences in the structure of their helminth communities.

Finally, it has been shown that there is a correlation between altitude and species richness in most taxa (Laakkonen et al., 2003); a factor that could contribute to the differences in the helminth communities of the 2 species is a greater availability of intermediate hosts in downstream localities compared to upstream ones. Blasco-Costa et al. (2013) observed a correlation between the abundance of digeneans infecting fish and river flow, and found that parasites were more abundant downstream, which they attributed to the downstream flow of water favoring the displacement and dispersion of invertebrates (including both intermediate hosts and infective stages of the helminths). The helminth communities in the Pánuco River drainage reflect this pattern; X. birchmanni (in Benito Juárez, a downstream locality) harbored a richer community of helminths than fish in the upstream locality (X. malinche in Malila), as would be expected if there was a greater diversity of invertebrate intermediate hosts.

Acknowledgments

We thank Zachary W. Culumber for help with fish collection and identification. This work was supported by the project “El efecto de hibridización en la diversidad de helmintos parásitos de peces del género Xiphophorus” (Clave 0127310) to SM and a scholarship from Conacyt to CEB-H (336764) during her Ph.D. studies.

References

Arizmendi-Espinosa, M. A. (1992). Descripción de algunas etapas larvarias & de la fase adulta de Centrocestus formosanus de Tezontepec de Aldama, Hidalgo. Anales del Instituto de Biología, Universidad Nacional Autónoma de México, Serie Zoología, 63, 1–11.

Bautista-Hernández, C. E., Monks, S., & Pulido-Flores, G. (2013).  Los parásitos y el estudio de su biodiversidad: un enfoque sobre los estimadores de la riqueza de especies.  In G. Pulido-Flores, & S. Monks (Eds.), Estudios científicos en el estado de Hidalgo y zonas aledañas (pp.13–17). Lincoln, Nebraska: Zea Books.

Bautista-Hernández, C. E., Monks, S., & Pulido-Flores, G. (2014). Comunidades de helmintos parásitos de algunas especies de peces de dos localidades de la Huasteca Hidalguense. Revista Biológico Agropecuaria Tuxpan, 2, 476–480.

Bautista-Hernández, C. E., Monks, S., & Pulido-Flores, G. (2015). Evaluación de las infracomunidades de tres especies de peces en dos localidades de la Huasteca hidalguense.  In G. Pulido-Flores, S. Monks, & López-Herrera, M. (Eds.), Estudios en biodiversidad Vol. I (pp. 44–51). Lincoln, Nebraska: Zea Books.

Bautista-Hernández, C. E., Monks, S., Pulido-Flores, G., & Miranda, R. (2015). A new species of Paracreptotrema (Digenea, Plagiorchiformes, Allocreadiidae) infecting two species of poeciliids in Río Malila of the Río Pánuco basin, Hidalgo, México, with a key to the species of the genus. ZooKeys, 482, 55–66.

Bautista-Hernández, C. E., Monks, S., Pulido-Flores G., & Rodríguez-Ibarra, A. E. (2015). Revisión bibliográfica de algunos términos ecológicos usados en parasitología, y su aplicación en estudios de caso.  In G. Pulido-Flores, S. Monks, & M. López-Herrera (Eds.), Estudios en biodiversidad Vol. I (pp. 11–19). Lincoln, Nebraska: Zea Books.

Bautista-Hernández, C. E., Violante-González, J., Monks, S., & Pulido-Flores, G. (2014). Helminth communities of Xiphophorus malinche (Pisces: Poeciliidae), endemic freshwater fish from the Pánuco River drainage, México. Revista Mexicana de Biodiversidad, 85, 838–844.

Blasco-Costa, I., Koehler, A. V., Martin, A., & Poulin, R. (2013). Upstream-downstream gradient in infection levels by fish parasites: a common river pattern?  Parasitology, 140, 266–274.

Bush, A. O., Lafferty, K. D., Lotz, J. M., & Shostak, A.W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited.  Journal of Parasitology, 83, 575–583.

Caspeta-Mandujano, J. M., Moravec, F., & Salgado-Maldonado, G. (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.

Cui, R., Schumer, M., Kruesi, K., Walter, R., Andolfatto, P., & Rosenthal, G. G. (2013). Phylogenomics reveals extensive reticulate evolution in Xiphophorus fishes. Evolution, 67, 2166–2179.

Culumber, Z. W., Fisher, H. S., Tobler, M., Mateos, M., Barber, P. H., Sorenson, M. D. et al. (2011). Replicated hybrid zones of Xiphophorus swordtails along an elevational gradient. Molecular Ecology, 20, 342–356.

Culumber, Z. W., & Rosenthal, G. G. (2013). Population-level mating patterns and fluctuating asymmetry in swordtail hybrids. Naturwissenschaften, 100, 801–804.

Culumber, Z. W., Shepard, D. B., Coleman, S. W., Rosenthal G. G., & Tobler, M. (2012). Physiological adaptation along environmental gradients and replicated hybrid zone structure in swordtails (Teleostei: Xiphophorus). Evolutionary Biology, 25, 1800–1814.

de la Vega-Salazar, M. Y. (2003). Situación de los peces dulceacuícolas en México. Ciencias, 72, 20–30.

El Gharbi, S., Renaud, F., & Lambert, A. (1992). Dactylogyrids (Plathyhelminthes: Monogenea) of Barbus spp. (Teleostei, Cyprinidae) from the Iberian Peninsula. Research and Review in Parasitology, 52, 103–116.

Falcón-Ordaz, J., Monks, S., Pulido-Flores, G., Bautista-Hernández, C. E., & Hernández-Hernández S. (2015). Nuevos registros y redescripción de Rhabdochona xiphophori Caspeta-Mandujano, Moravec y Salgado- Maldonado, 2001 (Nematoda: Rhabdochonidae) en el Estado de Hidalgo, México. In G. Pulido-Flores, S. Monks, & M. López-Herrera (Eds.), Estudios en biodiversidad. Vol. I (pp. 38–43). Lincoln, Nebraska: Zea Books.

García-Vásquez, A., Razo-Mendivil, U., & Rubio-Godoy, M.  (2015). Morphological and molecular description of eight new species of Gyrodactylus von Nordmann, 1832 (Platyhelminthes: Monogenea) from poeciliid fishes, collected in their natural distribution range in the Gulf of Mexico slope, Mexico. Parasitology Research, 114, 3337–3355.

Garrido-Olvera, L., Arita, H. T., & Pérez-Ponce de León, G. (2012). The influence of host ecology and biogeography on the helminth species richness of freshwater fishes in Mexico. Parasitology, 139, 1652–1665.

Gutiérrez-Rodríguez, C., Shearer, A. E., Morris, M. R., & De Queiroz, K. (2008). Phylogeography and monophyly of the swordtail fish species Xiphophorus birchmanni (Cyprinodontiformes, Poeciliidae). Zoologica Scripta, 37, 129–139.

Hernández-Hernández, D. L. (2008). Helmintofauna de Chirostoma jordani Woolman, 1894 del lago de Tecocomulco, Hidalgo, Mexico (Bachelor thesis). Centro de Investigaciones Biologicas, Universidad Autónoma del Estado de Hidalgo. Hidalgo, México.

Hoffman, G. L. (1999). Parasites of North American freshwater fishes. Ithaca, New York: Cornell University Press.

Kindsvater, H., Rosenthal, G. G., & Alonzo, S. (2012). Maternal size and age shape offspring size in a live-bearing fish, Xiphophorus birchmanni. Plos One, 7, e48473.

Laakkonen, J., Fisher, R. N., & Case, T. J. (2003). Microparasite assemblages of conspecific shrew populations in Southern California. Journal of Parasitology, 89, 1153–1158.

López-Jiménez, S. (1987). Enfermedades más frecuentes de las carpas cultivadas en México. Acuavisión. Revista Mexicana de Acuacultura, 2, 11–13.

Magurran, A. E. (2004). Measuring biological diversity. Malden, Massachusetts: Blackwell Publishing Company.

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

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

Mendoza-Franco, E. F., Caspeta-Mandujano, J. M., Salgado-Maldonado, G., & Matamoros, W. A. (2015). Two new species of Urocleidoides Mizelle et Price, 1964 (Monogenoidea) from the gill lamellae of profundulids and poeciliids from Central America and southern Mexico. Folia Parasitologica, 62, 59.

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

Monks, S., Zárate-Ramírez, V. R., & Pulido-Flores, G. (2005).  Helminths of freshwater fishes from the Metztitlán Canyon Reserve of the Biosphere, Hidalgo, Mexico. Comparative Parasitology, 72, 212–219.

Moulia, C. (1999). Parasitism of plant and animal hybrids: are facts and fates the same?  Ecology, 80, 392–396.

Paczolt, K., Passow, C. N., Delclos, P. J., Kindsvater, H. K., Jones, A. G., & Rosenthal, G. G. (2015). Multiple mating and reproductive skew in parental and introgressed females of the live-bearing fish Xiphophorus birchmanni.  Journal of Heredity, 106, 57–66.

Pineda-López, R., Salgado-Maldonado, G., Soto-Galera, E., Hernández-Camacho, N., Orozco-Zamorano, A., Contreras-Robledo, S. et al. (2005). Helminth parasites of viviparous fishes in Mexico. In H. Grier, & M. C. Uribe (Eds.), Viviparous fishes (pp. 437–456). Homestead, Florida: New Life Publications.

Poulin, R. (1998). Comparison of three estimators of species richness in parasite component communities. Journal Parasitology, 84, 485–490.

Rauchenberger, M, Kallman, K. D., & Morizot, D. C. (1990). Monophyly and geography of the Río Pánuco Basin swordtails (genus Xiphophorus) with descriptions of 4 new species. American Museum Novitates, 2975, 1–41.

Rosenthal, G., de la Rosa-Reina, X., Kazianis, S., Stephens, M., Morizot, D. C., Ryan, M. et al. (2003). Dissolution of sexual signal complexes in a hybrid zone between the swordtails Xiphophorus birchmanni and Xiphophorus malinche (Poeciliidae). Copeia, 2003, 299–307.

Rubio-Godoy, M., Paladini, G., García-Vásquez, A., & Shinn, A. P. (2010). Gyrodactylus jarocho sp. nov. and Gyrodactylus xalapensis sp. nov. (Platyhelminthes: Monogenea) from Mexican poeciliids (Teleostei: Cyprinodontiformes), with comments on the known gyrodactylid fauna infecting poeciliid fish. Zootaxa, 2509, 1–29.

Salgado-Maldonado, G. (2006). Checklist of helminth parasites of freshwater fishes from Mexico. Zootaxa, 1324, 1–357.

Salgado-Maldonado, G., Aguilar-Aguilar, R., Cabañas-Carranza, G., Soto-Galera, E., & Mendoza-Palmero, C. A. (2005). Helminth parasites in freshwater fish from the Papaloapan River basin, Mexico. Parasitology Research, 96, 69–89.

Salgado-Maldonado, G., Cabañas-Carranza, G., Soto-Galera, E., Pineda-López, R., Caspeta-Mandujano, J. M., Aguilar-Castellanos, E. et al. (2004). Helminth parasites of freshwater fishes of the Pánuco River Basin, East Central Mexico. Comparative Parasitology, 71, 190–202.

Salgado-Maldonado, G., Novelo-Turcotte, M. T., Vázquez, G., Caspeta-Mandujano, J., Quiroz-Martínez, B., & Favila, M. (2014). The communities of helminth parasites of Heterandria bimaculata (Teleostei: Poeciliidae) from the upper Río La Antigua basin, east-central Mexico show a predictable structure. Parasitology, 141, 970–980.

Scholz, T., & Salgado-Maldonado, G. (2000). The introduction and dispersal of Centrocestus formosanus (Nishigori, 1924) (Digenea: Heterophyidae) in Mexico: a review. American Midland Naturalist, 143, 185–200.

Scholz, T., & Salgado-Maldonado, G. (2001). Metacestodes of the family Dilepididae (Cestoda: Cyclophyllidea) parasitising fishes in Mexico. Systematic Parasitology, 49, 23–40.

Šimková, A., Dávidová, M., Papoušek, I., & Vetešník, L. (2013). Does interspecies hybridization affect the host specificity of parasites in cyprinid fish? Parasites & Vectors, 6, 95.

Valtonen, E.T., Pulkkien, K., Poulin, R., & Julkunen, M. (2001). The structure of parasite component communities in brackish water fishes of the northeastern Baltic Sea. Parasitology, 122, 471–481.

Vidal-Martínez, V. M., Aguirre-Macedo, M. L., Scholz, T., González-Solís, D., & Mendoza-Franco, E. F. (2001). Atlas of the helminth parasites of cichlid fish of Mexico. México D.F.: Instituto Politécnico Nacional.

Willis, P. M., Rosenthal, G. G., & Ryan, M. J.  (2012). An indirect cue of predation risk counteracts female preference for conspecifics in a naturally hybridizing fish Xiphophorus birchmanni.  Plos One, 7, e34802.

Wilson, A. J., Grimmer A., & Rosenthal, G. G. (2013). Causes and consequences of contest outcome: aggressiveness, dominance and growth in the sheepshead swordtail, Xiphophorus birchmanni. Behavioral Ecology and Sociobiology, 67, 1151–1161.

Wong, B. B. M., & Rosenthal, G. G. (2005). Shoal choice in swordtails when preferences conflicts. Ethology, 111, 179–186.

Zander, C. D. (2001). The guild as a concept and a means in ecological parasitology. Parasitology Research, 87, 484–488.