Introduction

Fishes of the family Goodeidae inhabit the shallow freshwater of the Mexican highland plateau (Goodeinae) and the western Great Basin of the United States (Empetrichthyinae; Webb 1998). It is thought this family of cyprinodontid, viviparous fish originated in the southern area of the Mexican highland plateau, the Mesa Central. Most species have a known distribution confined to the Mesa Central, with its center of abundance being the isolated basin of the Lerma River (Uyeno et al. 1983). The Goodeinae contain approximately 36 livebearing species in 17 genera, six of which are monotypic, distributed primarily across the Mesa Central, at elevations between 1000 m and 2300 m, although several species occupy Atlantic and Pacific systems which drain the margins of the southern highland plateau (Webb 1998).

The species Girardinichthys multiradiatus (Meek 1904) is a typical representative of the endemic Goodeid fish species of the upper Lerma River sub-basin (Díaz-Pardo et al. 1993). Occupying the far southeastern part of the Mesa Central, G. multiradiatus occurs in the headwaters of the Balsas and Lerma drainage areas and in the lake Laguna de Zempoala basin (Webb 1998). It is a key component in the aquatic food web and constitutes a major food item for many migratory bird species and other predators, like garter snakes. G. multiradiatus constitutes a good study system of the composition and structure of helminth parasite communities in these species. This species is highly resistant to pollution, widely distributed and is a typical species of highlands habitats. Its parasite fauna, however, is little studied, with a total of only nine helminth taxa reported from small numbers of G. multiradiatus examined (Lamothe-Argumedo 1970; Lamothe-Argumedo and Cruz-Reyes 1972; García-Prieto et al. 1987; León-Regagnon 1992; Astudillo-Ramos and Soto-Galera 1997; Salgado-Maldonado et al. 2001b, 2004a; Scholz and Salgado-Maldonado 2001; Pineda-López et al. 2004).

The objective of the present report is to provide basic survey information on the helminth parasites of G. multiradiatus from freshwater localities in the upper Lerma River sub-basin, covering the entire geographical range of this species. Data generated in this study are useful in exploring hypotheses on the origin and evolution of helminth communities in the fish of the Mexican highland plateau and in freshwater fish in general.

Materials and methods

Between June 1999 and November 2001, a total of 754 Girardinichthys multiradiatus (12–58 mm), collected from 20 sites in the upper Lerma River sub-basin in the states of Mexico, Morelos and Michoacan (Table 1, Fig. 1), were examined for helminth parasites. Samples were taken at every site where an established G. multiradiatus population existed, such that the species was sampled throughout its entire current geographical range. Collection sites included three lakes, seven reservoirs, three small channels and seven man-made ponds (locally called bordos) used to store water during dry seasons, which represent the totality of the current geographical distribution of this fish species. Fish were collected using an electrofishing device and nets or traps on the bottoms of different bodies of water. The numbers of fish examined at each locality and collection data are given in Table 1.

Table 1 Codes and features of the localities at which hosts were collected. Aproximate location of localities without coordinates are shown in Fig. 1. B Bordo or man-made pond, C channel or small stream, D dammed lake, L natural lake
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Fig. 1
figure 1

Location of each locality at which hosts were collected

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Once collected, the fish specimens were stored live and immediately transported to the laboratory for examination within the next 12 h. A complete examination of each specimen for helminth parasites was conducted. External surfaces, including scales, skin and fins, were examined for ectoparasites, using a stereomicroscope. Gills were recovered and the arches examined individually. The buccal cavity, opercula and eyes were examined separately. The external surfaces of the internal organs (heart, liver, spleen, gall bladder, digestive tract, gonads, swim bladder, kidney, entire body cavity, mesentery) were inspected for free or encapsulated parasites and then separated and examined individually. The intestine was opened longitudinally. The liver, spleen, kidney and heart were compressed between glass plates and examined for parasites. The body musculature was removed from the vertebral column, the skin removed from the fillets and the fillets compressed between glass plates and inspected for helminths, using a stereomicroscope. All collected helminths were sorted by taxon, cleaned and counted by organ.

Trematodes (adults, metacercariae), monogeneans, cestodes (adults, metacestodes) and nematodes were fixed in hot 4% formalin. Acanthocephalan cystacanths were placed in distilled water, refrigerated overnight (6–12 h) to evert the proboscis and then fixed in hot 4% formalin. Trematodes, monogeneans, cestodes and acanthocephalans were stained with Mayer’s paracarmine or Ehrlich’s haematoxylin, dehydrated using a graded alcohol series, cleared in methyl salicylate and mounted whole. To study sclerotized parts, several specimens of each species of monogenean were fixed following Malmberg’s semi-permanent mount method (see Ergens 1969; Vidal-Martínez et al. 2001). Nematodes were cleared with glycerin for light microscopy and stored in 70% ethanol. Voucher specimens of all taxa have been deposited in the National Helminth Collection (Colección Nacional de Helmintos, Institute of Biology, National Autonomous University of Mexico, Mexico City).

The infection parameters utilized are those proposed by Bush et al. (1997), i.e. prevalence (% infected) and mean intensity of infection (number of parasites per infected fish).

Results

The parasites encountered, their collection locations, infection sites, prevalence and intensity of helminth species are summarized in Table 2.

Table 2 Parasite–host list of helminths collected from Girardinichthys multirdiatus in the upper Lerma River sub-basin of Central Mexico
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A total of 13 helminth species were collected, including: one adult trematode, three metacercariae, one monogenean, one adult cestode, three metacestode, three nematode larvae and one cystacanth (Table 2). The records of the metacercariae of Tylodelphys sp. and Ochetosoma brevicaecum, the larvae of the nematodes Contracaecum sp. and Falcaustra sp. and the cystacanth of Polymorphus brevis are all new records for this host.

The most widely distributed and abundant helminth species recorded in this study was Tylodelphys sp. The metacercariae of this species were collected from 15 of the 20 sampling localities and its prevalence varied from 3.2% to 72.7% (Table 2). The metacestode of Valipora campylancristrota were the second most widely distributed, with specimens collected from 11 of the sampling localities. The adult cestode Bothriocephalus acheilognathi was third, with specimens collected from ten of the localities.

The number of helminth species collected at each locality varied between one and eight. The highest number of species was collected at Lago Chicnahuapan, although the localities of San Juanico, Rancho La Venta and Parque Sierra Morelos were also rich in parasites.

Discussion

This study constitutes a complete and extensive inventory of the helminth parasites in a freshwater fish species across its entire current geographic distribution.

The data indicate a poor helminth community with few specialist species, plus a number of wide-distribution generalist species. A third component are two anthropogenically introduced species.

The only helminth species that has developed a close relationship with Girarninichthys multiradiatus is Margotrema bravoae, a trematode only found parasitizing Goodeidae, endemic to but infrequent in the study area (Lamothe-Argumedo 1970; Pérez 2001; Salgado-Maldonado et al. 2001b, 2004a; Pineda-López et al. 2004).

The metacercariae of Tylodelphys sp. is the most frequent species in this host throughout its geographic distribution range. Widely distributed Nearctic generalist species, such as Posthodiplostomum minimum, Ligula intestinalis, Cyclustera ralli, Valipora campylancristrota, Contracaecum sp. and Polymorphus brevis enrich the community. The presence of all these species can be related to predation of the Goodeidae, small fish that live in shallow waters, by migratory birds from Nearctic climes (Salgado-Maldonado et al. 2001b).

The larvae of Ochetosoma brevicaecum and Spiroxys sp. are two helminth species that mature in reptiles. The larvae of Spiroxys sp. are found frequently in freshwater fish of Neotropical Mexico (Moravec 1998; Salgado-Maldonado et al. 2001a, 2001b, 2004, 2004a, 2004b), suggesting that reptiles prey extensively on fish. The presence of O. brevicaecum in G. multiradiatus is thus probably an accidental infection. This helminth is common in the Mexican Mesa Central. The most common intermediate hosts of the metacercariae are amphibians (García-Altamirano et al. 1993; unpublished data), although metacercariae have also been collected from fish (Peresbarbosa et al. 1994). Adult stages parasitize several species of snakes of the genus Thamnophis (Caballero y Caballero 1941; Bravo-Hollis 1943; Pérez et al. 2001).

Larvae of the nematode Falcaustra sp. are found infrequently. Very little is known about the transmission of this nematode, except that they are intestinal parasites of reptiles, frogs and freshwater fishes (Moravec 1998).

The recorded helminth parasites also include two anthropogenically introduced species, Bothriocephalus acheilognathi and Gyrodactylus elegans. The Asian fish tapeworm, B. acheilognathi is widely dispersed among the freshwater fish of Mexico, being recorded to date in 49 fish species from 26 genera, seven families and five orders (see Salgado-Maldonado and Pineda-López 2003). The monogenean G. elegans is a common species in Europe, although its occurrence in North America needs more study. Several unidentified species of Gyrodactylus have been reported from Mexican freshwater fishes (Salgado-Maldonado et al. 1997, 2001a, 2001b; Vidal-Martínez et al. 2001). The genus Gyrodactylus includes more than 150 species and its taxonomy is very complicated (Vidal-Martínez et al. 2001).

The taxonomic composition of the helminth communities of the Goodeidae suggests a depauperate helminth community open to invasion, which developed in association with evolutionarily young and isolated fish communities. These characteristics have also been observed in other fish helminth communities in the Mexican Mesa Central, especially in the Lerma River basin (Salgado-Maldonado et al. 2001b). The helminth communities of these fish are poor, with the richest documented community components reaching no more than ten species (Salgado-Maldonado and Osorio-Sarabia 1987; Choudhry and Dick 2000; Pérez et al. 2000). Each of these communities includes very few helminth specialists: the monogenean Octomacrum mexicanum Lamothe-Argumedo, 1981 in the cyprinid Algansea lacustris, the trematode Allocreadium mexicanum Osorio-Sarabia, Pérez and Salgado-Maldonado, 1986 in the atherinid Chiorostoma estor and the nematode Rhabdochona lichtenfelsi Sánchez-Álvarez, García and Pérez, 1998 in the goodeid Goodea atripinnis (see Salgado-Maldonado et al. 2001b). The presence of 14 bird-transported allogenic species (see Esch et al. 1988) and three anthropogenically introduced helminth species has been recorded among the 43 documented helminth species in the Lerma Santiago basin of the Mexican Mesa Central (Salgado-Maldonado et al. 2001b). Anthropogenic introduction of helminths in central Mexico and other geographic areas of Mexico has been documented by Scholz and Salgado-Maldonado (2000) and by Salgado-Maldonado and Pineda-López (2003).

Data collected during the present study show the helminth parasite community of Girardinichthys multiradiatus to be relatively poor when compared with helminth communities of freshwater fish from other parts of Mexico. This community includes a number of generalist helminth species, mostly transported by birds. A further component of this community consists of helminth species that have been introduced anthropogenically.