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Helminths of Freshwater Fishes from the Metztitlán CanyonReserve of the Biosphere, Hidalgo, MexicoAuthor(s): Scott Monks , Víctor Rafael Zárate-Ramírez , Griselda Pulido-FloresSource: Comparative Parasitology, 72(2):212-219. 2005.Published By: The Helminthological Society of WashingtonDOI: http://dx.doi.org/10.1654/4139URL: http://www.bioone.org/doi/full/10.1654/4139

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Helminths of Freshwater Fishes from the Metztitlan Canyon Reserveof the Biosphere, Hidalgo, Mexico

SCOTT MONKS,1,3 VICTOR RAFAEL ZARATE-RAMIREZ,2 AND GRISELDA PULIDO-FLORES1

1 Universidad Autonoma del Estado de Hidalgo, Centro de Investigaciones Biologicas, Ciudad Universitaria,

Apdo. Postal 1-69, Pachuca, CP 42001, Hidalgo, Mexico (e-mail: smonks@uaeh.edu.mx; gpulido@uaeh.edu.mx) and2 El Colegio de la Frontera Sur-Unidad Chetumal, Avenida Centario Km. 5.5,

CP 77001, Chetumal, Quintana Roo, Mexico

ABSTRACT: The occurrence of 6 species of helminth parasites (Clinostomum complanatum, Diplostomidae gen. sp.,

Posthodiplostomum minimum, Bothriocephalus acheilognathi, Glossocercus sp., Contracaecum sp.) is reported from

7 species of freshwater fishes (Chirostoma jordani, Astyanax mexicanus, Herichthys labridens, Oreochromis niloticusniloticus, Abramis brama, Cyprinus carpio carpio, and Poeciliopsis gracilis) in Metztitlan Lake (Laguna de Metztitlan),

Reserva de la Biosfera Barranca de Metztitlan, Hidalgo, Mexico. Fish were collected between July 2002 and June 2003. The

helminth fauna of H. labridens, an endangered species of Cichlidae, is described for the first time. Migratory birds of the

families Ardeidae and Phalacrocoracidae appear to play an important role in the helminth species composition of fishes from

Metztitlan Lake. All helminth species represent new records for this federally protected area of Hidalgo.

KEY WORDS: Digenea, Cestoda, Nematoda, Poeciliidae, Cyprinidae, Cichlidae, Characidae, Atherinidae, Clinostomum

complanatum, Posthodiplostomum minimum, Bothriocephalus acheilognathi, Glossocercus, Contracaecum, Chirostoma

jordani, Astyanax mexicanus, Herichthys labridens, Oreochromis niloticus niloticus, Abramis brama, Cyprinus carpiocarpio, Poeciliopsis gracilis, zoonosis, Hidalgo, Mexico.

The Biosphere Reserve projects combine conser-

vation with human development in a context of

sustainable development and scientific investigation.

The ‘‘Metztitlan Canyon’’ (Barranca de Metztitlan)

Reserve of the Biosphere, in the northern part of the

centrally located state of Hidalgo, Mexico, has a high

level of endemism in plants and animals (SEMAR-

NAP, 1999) because of its geomorphologic origin.

No extensive survey of fish parasites has been con-

ducted in Hidalgo.

Metztitlan Lake (Laguna de Metztitlan; ‘‘Lugar de

la Luna’’) is located in the northwest end of an

enclosed basin or endorreic and has a surface area of

3,230 km2. The lake was formed naturally when

a prehistoric rockslide closed off the exit for the

outflow of Metztitlan River, which today still feeds

the lake. The local fishery has an ancient history, and

the catch of native species of fishes has had a large

economic and nutritional impact on indigenous

people. Water level in the lake fluctuates greatly

depending on the season and rainfall within the

watershed, and the lake has been known to

completely dry up at least twice in recent times. In

the past, native species from rivers and streams that

feed the lake have repopulated the lake after its

return. In the past decade, the Mexican government

began extensive introductions of exotic Cichlidae,

‘‘tilapia,’’ and Cyprinidae ‘‘carpas’’ (Ibanes-Aguirre

et al., 2002) before efforts were successful in getting

the area recognized as a reserve. The full consequen-

ces of these introductions of exotic species on the

survival of native fauna are not known, although it is

expected that the cointroduced helminths will have

negative effects (Osorio-Sarabia et al., 1986; Sal-

gado-Maldonado et al., 1986). Also, Metztitlan Lake

is visited by migratory birds (mainly Ardeidae and

Phalacrocoracidae), and the potential is high for the

spread of introduced helminths, mainly digeneans

and nematodes, to other Mexican localities (Lamothe-

Argumedo and Perez-Ponce de Leon, 1986; Ramos-

Ramos, 1995). This article represents the first report

of helminth parasites of freshwater fish from this

protected area of Hidalgo, Mexico, many of which

are new reports for fishes from the Panuco River

Basin.

MATERIALS AND METHODS

This study focused on fish from Metztitlan Lake (locatedbetween 988239000 and 988579080W and between 208149150and 208459260 N), municipio of Metztitlan, Hidalgo,Mexico. Monthly collections were made from July 2002 toJune 2003, and 366 fishes were obtained, mostly with thehelp of a local fisherman. All species of fish that are knownto inhabit the lake were collected. The majority of fish weretransported live to the laboratory in containers of lake water,but when the number of fish was large, some fish were keptin plastic bags and chilled on ice; fish were examined within4–8 hr of capture. Fish were identified using the study of3 Corresponding author.

Comp. Parasitol.72(2), 2005, pp. 212–219

212

Alvarez (1950) and by comparison with previouslyidentified voucher specimens. Voucher specimens of eachspecies are deposited in the Coleccion de Helmintos, Centrode Investigacion Biologicas, Universidad Autonoma delEstado de Hidalgo, Hidalgo, Mexico. External surface,internal visceral organs, eyes, and gills of each fish wereexamined using a dissecting microscope and standardparasitological techniques (Pritchard and Kruse, 1982).Live parasites were held briefly in saline, cleaned, andkilled by rapid immersion in hot water, warm Alchohol-Formalin-Acetic acid (AFA), or Berland solution (forNematoda). Platyhelminths were flattened under slightcoverslip pressure and fixed with AFA, subsequentlytransferred to 70% ethanol, stained with Gomori trichrome,Mayer carmalum, or Ehrlich hematoxylin, dehydrated in analcohol series, cleared in methyl salicilate, and mounted inCanada balsam. Nematodes were stored in 70% ethanol,cleared in a mixture of glycerin and ethanol by evaporation,and examined in temporary glycerin mounts. Voucherspecimens of helminths were deposited in the ColeccionNacional de Helmintos (CNHE), Universidad Autonoma deMexico, D. F., Mexico; the Harold W. Manter Laboratory ofParasitology, University of Nebraska Lincoln, Lincoln,Nebraska, U.S.A.; and the Coleccion de Helmintos,(CHE), Hidalgo, Mexico. Infection parameters follow thestudy of Margolis et al. (1982).

RESULTS

During the 12-mo study period, 366 fish were

necropsied as follows: Atherinidae, Chirostomajordani Woolman, 1894 (n ¼ 87); Characidae,

Astyanax mexicanus (De Filippi, 1853) (n ¼ 64);

Cichlidae, Herichthys labridens (Pellegrin, 1903) (n¼ 47) and Oreochromis niloticus niloticus Linnaeus,

1758 (n¼ 48); Cyprinidae, Abramis brama Linnaeus,

1758 (n¼ 10) and Cyprinus carpio carpio Linnaeus,

1758 (n ¼ 46); and Poecilidae, Poeciliopsis gracilisHeckel, 1848 (n ¼ 64). Members of Cyprinidae and

Cichlidae were the most abundant, with 2 species

from each family. Three native species were collected

(Ast. mexicanus, H. labridens, and P. gracilis), 3

exotic species (O. n. niloticus, Abr. brama, and C. c.carpio), and 1 species probably translocated from

another Mexican state (Ch. jordani). Six parasitic

helminth taxa (Clinostomum complanatum [Rudol-

phi, 1814], Diplostomidae gen. sp., Posthodiplosto-mum minimum [MacCallum, 1921], Bothriocephalusacheilognathi [Yamaguti, 1934], Glossocercus sp.,

and Contracaecum sp., Figs. 1–8) were collected

from the 7 species of fish.

Larval forms

DigeneaDiplostomidae gen. sp.

Metacercariae that could only be identified as

being a member of the Diplostomidae were collected

from Ast. mexicanus, Ch. jordani, O. n. niloticus, and

P. gracilis. These specimens resemble those collected

by Vidal-Martınez et al. (2001) from native cichlids

of Southeastern Mexico in general characteristics, but

these specimens have the cecum surrounding the

tribocytic organ (Fig. 1). The specimens collected

most resemble a species of Austradiplostomum Szidat

and Nani, 1951, but have a well-developed muscular

acetabulum, almost equal in size to that of the oral

sucker, in contrast to members of Austradiplosto-mum, which lack the acetabulum. They also some-

what resemble Diplostomum compactum (Lutz,

1928), a parasite of cichlids from various localities

of Mexico (Vidal-Martınez et al., 2001), but our

specimens have a more conspicuous muscular

acetabulum. In the same manner, our specimens are

somewhat similar to members of the genus Bursa-tintinnabulus Tehrany, Dronen and Wardle, 1999,

and Bursacetabulus Dronen, Tehrany and Wardle,

1999 (Diplostomidae), but members of both genera

lack an acetabulum (Gibson et al., 2002). The biology

of this species remains unknown, but similar to other

members of the family Diplostomidae, a bird serves

as the definitive host (Yamaguti, 1971).

Hosts in Laguna de Metztitlan: Astyanax mexicanus,

Ch. jordani, O. n. niloticus, P. gracilis.

Prevalence, total number of worms recovered, andrelative density (intensity) by host taxon: Astyanaxmexicanus, 2 of 64, 2, 0.03 (1); Ch. jordani, 7 of 87,

15, 0.17 (1–7); O. n. niloticus, 1 of 48, 1, 0.02 (1);

P. gracilis, 27 of 64, 212, 3.31 (1–35).

Sites of infection: Muscle, mesentery, and body

cavity.

Specimens deposited: CHE-P00010–P00019; CNHE-

5265.

Posthodiplostomum minimum(MacCallum, 1921)

Metacercariae of Po. minimum (Fig. 2) were

collected only from the endemic fish, H. labridens.

This digenean has been reported widely throughout

the Americas, with previous records in Mexico

(Perez-Ponce de Leon et al., 1996). The metacercarial

stage has epizootic potential in natural and cultivated

fish populations (Osorio-Sarabia et al., 1986). In

Mexico, adults of this species have been recovered

from Egretta thula (Molina, 1782) (Ardeidae) from

Lake Patzcuaro, Michoacan (Lamothe-Argumedo and

Perez-Ponce de Leon, 1986), a species that also

frequents Metztitlan Lake (SEMARNAP, 1999).

MONKS ET AL.—HELMINTHS OF METZTITLAN LAKE FISHES 213

Hosts in Laguna de Metztitlan: Herichthys labridens.

Prevalence, total number of worms recovered, andrelative density (intensity): 5 of 47, 35, 0.74 (1–23).

Site of infection: Muscle.

Specimens deposited: CHE-P00022; CNHE-5264.

Clinostomum complanatum(Rudolphi, 1814)

Single metacercariae of Cl. complanatum (Fig. 3)

were collected from the mouths of only 3 specimens

of P. gracilis. A cosmopolitan species (Yamaguti,

1971), these metacercariae are known from several

states of Mexico (Perez-Ponce de Leon et al., 1996).

Hosts in Laguna de Metztitlan: Poeciliopsis gracilis.

Prevalence, total number of worms recovered, andrelative density (intensity): 3 of 64, 3, 0.05 (1).

Site of infection: Mouth.

Specimens deposited: CHE-P00020; CNHE-5263.

Glossocercus sp.

Six fish representing 2 species were infected with

single metacestodes of Glossocercus sp. (Figs. 4, 5).

We can only assign these larvae to the genus

Glossocercus until adults are recovered. The life

cycle is not known, but it may use a copepod as

intermediate host and birds as definitive hosts (Khalil

et al., 1994). These specimens were collected after

migratory birds were seen visiting the lake, although

we have no direct evidence that the birds were

infected with this species.

Hosts in Laguna de Metztitlan: Chirostoma jordani,P. gracilis.

Prevalence, total number of worms recovered, andrelative density (intensity) by host taxon: Chirostomajordani, 2 of 87, 2, 0.02 (1); P. gracilis, 4 of 64, 4,

0.06 (1).

Site of infection: Mesentery.

Specimens deposited: CHE-P00005, P00006.

Contracaecum sp.

Larvae of Contracaecum sp. (Fig. 8) were re-

covered from 5 of the 7 species of fish collected. Fish

serve either as second intermediate hosts or as

paratenic hosts (Moravec et al., 1995) for members

of this genus, and the parasites are rare human

Figures 1–3. Larval digeneans parasitizing fishes of Metztitlan Lake, Mexico. 1. Diplostomidae gen. sp. 2.Posthodiplostomum minimum. 3. Clinostomum complanatum.

214 COMPARATIVE PARASITOLOGY, 72(2), JULY 2005

pathogens (Moravec, 1998). This is the only parasite

that is commonly reported by local fishermen. They

reported the nematode in fish muscle, which rendered

the flesh unattractive for sale, but found no nematode

in fish muscle, and so this may not be the species that

local fishermen report.

Hosts in Laguna de Metztitlan: Abramis brama, Ast.mexicanus, C. c. carpio, H. labridens, P. gracilis.

Prevalence, total number of worms recovered, andrelative density (intensity) by host taxon: Abramisbrama, 2 of 10, 3, 0.03 (1–2); Ast. mexicanus, 8 of

64, 15, 0.23 (1–4); C. c. carpio, 1 of 46, 1, 0.02 (1);

H. labridens, 4 of 47, 5, 0.11 (1–2); P. gracilis, 4 of

64, 4, 0.06 (1).

Sites of infection: Mesentery and body cavity.

Specimens deposited: CHE-F00013.

Adult forms

Bothriocephalus acheilognathi(Yamaguti, 1934)

This tapeworm (Figs. 6, 7) was initially imported

along with its host, Ctenopharyngodon idella (Va-

lenciennes, 1844), by the aquaculture facilities of

Tezontepec de Aldama, Hidalgo (Lopez-Jimenez,

1981) and has been reported widely from Mexico

since the 1980s. Although all the fish species

examined except for O. n. niloticus were infected

with B. acheilognathi, Ch. jordani appears to be the

most important definitive host (prevalence ¼ 80%;

abundance¼ 31.1; and range 1–106). It is not known

whether the helminth was introduced to Laguna de

Metztitlan with C. c. carpio or Ch. jordani because

both are introduced species of undetermined origin

(Ibanes-Aguirre et al., 2002). Studies are necessary to

quantify the damage that this parasite may cause the

indigenous fish species H. labridens and P. gracilis.

Hosts in Laguna de Metztitlan: Abramis brama, Ast.mexicanus, Ch. jordani, C. c. carpio, H. labridens,

P. gracilis.

Prevalence, total number of worms recovered, andrelative density (intensity) by host taxon: Abramis

Figures 4–8. Cestodes and nematodes parasitizingfishes of Metztitlan Lake, Mexico. 4. Glossocercus sp.,anterior end showing scolex with rostrum. 5. Large rostralhook of Glossocercus sp. 6. Bothriocephalus acheilognathi,anterior end showing scolex. 7. Mature proglottid of B.acheilognathi. 8. Posterior (left) and anterior (right) ends ofContracaecum sp.

MONKS ET AL.—HELMINTHS OF METZTITLAN LAKE FISHES 215

brama, 2 of 10, 60, 6 (2–58); Ast. mexicanus, 1 of 64,

3, 0.05 (3); Ch. jordani, 70 of 87, 2,704, 31.1 (1–

106); C. c. carpio, 1 of 46, 4, 0.09 (4); H. labridens,

11 of 47, 443, 9.43 (1–128); P. gracilis, 10 of 64, 23,

0.36 (1–5).

Sites of infection: Stomach, large intestine, and small

intestine.

Specimens deposited: CHE-P00001–P00004; CNHE-

5097, 5098.

DISCUSSION

Metztitlan Reserve of the Biosphere is a multiple-

use area that also contains many irrigated fields where

green beans, chili peppers, squash, and corn are

grown. The area appears to be an ideal locality for

rich natural communities of fishes and their parasites

based on the assumptions that as part of a reserve, the

local fauna has been protected and represents a natural

endemic community, and that the lake waters are

relatively uncontaminated. This is not the case. The

local fauna does not represent a natural, endemic

community. We collected and report all known fish

species in the lake. Local people consider the

aquaculture practices initiated before the reserve

was established to have caused the loss of diversity

of fish in the lake and associated river, although no

scientific survey records exist to document this trend.

In addition, the lake has been contaminated to an

unknown degree, although a complete contamination

profile is still under study (Ibanes-Aguirre et al.,

2002).

All helminths described in this study represent new

locality reports for the Metztitlan Reserve and for

Hidalgo, with the exception of B. acheilognathi,which was reported previously by Lopez-Jimenez

(1981). Represented by 3 species, digenea is the

richest component of the Metztitlan Reserve fish

parasite community, a pattern consistent with other

studies of helminth communities in freshwater fishes

from Mexico (Salgado-Maldonado and Kennedy,

1997), southwestern Mexico (Salgado-Maldonado

et al., 2001a), and Nicaragua (Aguirre-Macedo,

2001). Most of the parasite species reported in this

study are represented by juvenile stages, thus we

cannot determine whether the Metztitlan Reserve

helminth community contains endemic species or is

composed entirely of allogenic and introduced

species. In comparison with other surveys, (e.g.,

Perez-Ponce de Leon et al., 1994; Salgado-Maldo-

nado and Kennedy, 1997; Scholz and Vargas-

Vazquez, 1998; Aguirre-Macedo, 2001; Salgado-

Maldonado et al., 2001a, b) the helminth community

of fishes of Metztitlan Lake is depauperate. Reports

of the fish helminth community of Patzcuaro Lake are

similar to that of Metztitlan Lake, comprising 19

helminth species from 10 species of native and

introduced fishes (Osorio-Sarabia et al., 1986;

Salgado-Maldonado and Osorio-Sarabia, 1987;

Perez-Ponce de Leon et al., 1994; Perez-Ponce de

Leon et al., 2000), but the 6 helminth species from 7

species of fishes reported in this study is considerably

lower than that reported for Patzcuaro Lake.

We found no monogenean parasitizing a fish in

this study. Monogeneans are poorly represented in

the previously cited studies, although Salgado-

Maldonado et al. (2001b) reported 2 species of

Monogenea in a study of southeastern Mexican fish.

Kritsky et al. (1994), Mendoza-Franco et al. (1999),

Kritsky et al. (2000), and Mendoza-Franco et al.

(2000) demonstrate that monogeneans are not as

uncommon as the scarcity of previous records would

suggest. Considering this, we took particular care to

ensure that fish were not injured and that mono-

geneans were not lost during transport, and we

examined some fish in the field for monogeneans.

Despite these measures, we collected no mono-

genean. Environmental contamination may be such

that no monogenean is established in Metztitlan Lake.

Studies quantifying actual levels of contaminants are

underway, but the best explanation for the absence of

monogeneans is that high contamination levels in the

river that feeds the lake prevent the establishment

of monogeneans.

Metztitlan Lake is visited regularly by migrating

waterfowl (SEMARNAP, 1999), thus we expected to

find allogenic species of larval acanthocephalans that

parasitize birds as adults, a pattern consistent with

other Mexican lakes (Perez-Ponce de Leon et al.,

2000). The absence of adult acanthocephalans was

not unexpected. The majority of acanthocephalans

reported as adults from fishes of Mexico are from

waters that have a marine connection (see Amin,

2000 for a recent review of the distribution of

acanthocephalans in Mexico, the previously cited

surveys of Mexican fishes, and Lamothe-Argumedo

et al., 1997).

Poeciliopsis gracilis hosted the highest helminth

species richness, comprising 5 of the 6 helminth taxa

reported. Although a small fish, P. gracilis exhibits

an omnivorous diet including a range of potential

intermediate hosts (Wischnath, 1993). Interestingly,

the introduced fish species, O. n. niloticus, Abr.brama, and C. c. carpio, were the least parasitized

hosts in Metztitlan Lake. This phenomenon, in which

216 COMPARATIVE PARASITOLOGY, 72(2), JULY 2005

introduced fishes harbor fewer species of introduced

parasites, including those species that were intro-

duced with them, than do native fish species, has been

discussed (Perez-Ponce de Leon et al., 2000; Rego,

2000) in the context of B. acheilognathi. Bothrioce-phalus acheilognathi parasitized 86% (6 of 7) of

the freshwater fish species examined in this study,

demonstrating the ecological invasiveness of this

tapeworm in the Panuco Basin. Prevalence of B.acheilognathi in Ch. jordani (80%), a translocated

atherinid with high commercial value, is relatively

high, suggesting that this host should be monitored

in commercial facilities.

Some helminths reported in this survey have been

reported previously from other locations of Mexico

and the world. Some, such as Cl. complanatum(Yamaguti, 1971), have a cosmopolitan distribution

and others, such as B. acheilognathi (Salgado-

Maldonado et al., 1986), exhibit high ecological

invasiveness. Bothriocephalus acheilognathi is the

only autogenic species reported. The 3 digenean taxa

reported in this study, Cl. complanatum, Diplostomi-

dae gen. sp., and Po. minimum; 1 cestode, Glosso-cercus sp.; and 1 nematode, Contracaecum sp., were

found in metacercarial, metacestode, and juvenile

stages, respectively, indicating that these are allogen-

ic species that reach adult form in other vertebrates,

probably fish-eating birds of the families Ardeidae

and Phalacrocoracidae (Yamaguti, 1971). Subsequent

studies should focus on the helminth fauna of birds

from the reserve to clarify their role in the

composition of the helminth community of Metztitlan

Lake.

This study is the first report of helminths recovered

from H. labridens (Mojarra Huasteca; curve-bar

cichlid), a species endemic to the Panuco River

Basin. Designated in danger of extinction and

included in the NOM-059-1994 and IUCN lists, the

species remains a large component of the local diet.

Our finding of Po. minimum and B. acheilognathi in

this autochthonous cichlid and the information on

helminth abundance and intensity interval will aid the

administrators of the Metztitlan Canyon Reserve to

formulate an adequate management plan to ensure the

survival of this threatened species.

The presence of Contracaecum sp. in exploited

species of commercial fishes represents a potential

public health threat (Moravec, 1998). Human in-

fection can occur by eating ‘‘ceviche’’ (raw fish), as

occurs with zoonotic anisakids (Laffon-Leal et al.,

2000), as well as by introduction of the worm into

ocular openings or open wounds. The corroboration

of the fishermen’s claims of a worm that was

infecting the fish of this lake, and its subsequent

identification, will allow the managers of this

protected area to establish monitoring plans in

coordination with workers from the health services

to guard against potential outbreaks.

ACKNOWLEDGMENTS

The authors are grateful to the CONANP (Com-

ision Nacional de Areas Naturales Protegidas) and the

Administration of the Reserva de la Barranca de

Metztitlan Reserva de la Biosphera for the opportu-

nity to work within the reserve. Senor Andres Lopez-

Morales, brigadista for the Reserve, was our field

guide during the project, and he facilitated our

contact with local fishermen and helped with capture

of fish in some areas of the lake. Senor Telesforo,

a local fisherman from San Cristobal, Hidalgo,

provided us with many of the fish examined as part

of this study. Shayuri Moreno-Flores and Ana Erika

Gutierrez-Cabrera helped with collection of parasites,

and Luis Armando Zarate-Ramırez helped with the

drawings. Financial aid included a grant from the

Programa de Apoyo a Tesis de Maestrıa to V.R.Z.-R.

provided by El Colegio de la Frontera Sur, Unidad

Chetumal and a graduate student stipend from the

Consejo Nacional de Ciencia y Tecnologıa (grant

169593) to V.R.Z.-R. The Sistema de Investigacion

Ignacio Zaragoza (SIZA-CONACYT, grant 20020803006)

and the Programa de Mejoramiento del Profesorado

(PROMEP) provided funds to S.M. for fieldwork and

laboratory supplies.

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