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The Introduction and Dispersal of Centrocestus formosanus (Nishigori, 1924) (Digenea: Heterophyidae) in Mexico: A Review.

TOMAS SCHOLZ [1]

ABSTRACT.--The taxonomy, distributional history, present occurrence, life cycle, morphology of developmental stages and epizootiology of the heterophyid trematode Centrocestus formosanus (Nishigori, 1924) in Mexico are reviewed. This parasite was most likely introduced to Mexico with the importation of the first intermediate host, the thiarid snail Melanoides tuberculata, from Asia in 1979. Centrocestus formosanus was first recorded in 1985 as metacercariae in fry of the first generation of black carp Mylopharyngodon piceus imported from China and subsequently in other fish from a farm in central Mexico. Since that time the trematode has spread rapidly over a wide area which includes central Mexico and both the Atlantic and Pacific coasts. This rapid spread has apparently been enabled by previous propagation of M. tuberculata in Mexico. Metacercariae of C. formosanus occur encysted on the gills of fish. They have been found in 39 species of fish of the families Atherinidae, Characidae, Cichlidae, Cyprinidae, Eleotridae, Gobiidae, Goodeidae, Ictaluridae, Mugilidae and Poeciliidae from 11 Mexican states (Colima, Guanajuato, Hidalgo, Jalisco, Michoacan, Morelos, San Luis Potosi, Sonora, Tabasco, Tamaulipas and Veracruz). The heron Butorides striatus is the only known natural definitive host in Mexico. Further research towards better understanding of all aspects of the life cycle, transmission, host-parasite relationships and the effective control of C. formosanus in Mexico is necessary. It should also include monitoring of the present distribution of M. tuberculata and its infection with larval stages of C. formosanus. Much more emphasis should be given to histopathological studies to assess actual impact of the parasite on fish of different species and age classes. The spectrum of natural definitive hosts and their epizootiological importance in the transmission and maintenance of the parasite in Mexico should also be better documented. Adequate preventive and control measures should be applied in aquaculture, wit h emphasis given to prevention of movement of infected fish stocks.

INTRODUCTION

The introduction of exotic species of fish to new areas has negative consequences which include introduction of fish parasites to new continents (Kennedy, 1994). There are numerous examples of dissemination of helminths of freshwater fish to new zoogeographical regions such as the cestode Bothriocephalus acheilognathi, monogeneans of the genera Pseudodactylogyrus and Cichlidogyrus and the nematode Anguillicola crassus (Hoffman, 1980; Buchmann et at., 1987; Kennedy, 1994; Williams and Jones, 1994; Scholz, 1999). Some of these helminth species may even endanger autochtonous fish populations (Font and Tate, 1994; Font, 1997).

Recently, several new fish parasites have been introduced to Mexico from other continents, including the heterophyid trematode Centrocestus formosanus (Nishigori, 1924). This species was originally described from Taiwan (then Formosa) and is widely distributed in Asia (Chen, 1942; Yamaguti, 1971; Premvati and Pande, 1974; Yanohara, 1985; Madhavi, 1986; Scholz et at., 1990; Scholz, 1991). Martin (1958) reported C. formosanus from Hawaii, where it has been introduced probably from the Orient.

In Mexico metacercariae identified as Centrocestus formosanus were first reported by Lopez-Jimenez (1987) from a fish farm at Tezontepec de Aldama (Hidalgo) from central Mexico. The identification of the metacercariae was confirmed by Arizmendi (1992) who described the life cycle of the parasite from cercariae to adults obtained from experimentally infected hosts.

Several studies (Arizmendi, 1992; Amaya-Huerta and Almeyda-Artigas, 1994; Salgado-Maldonado et at., 1995) contain data on the occurrence and morphology of developmental stages of Centrocestus formosanus in Mexico. However, the existing information is scarce and fragmentary and does not reflect the veterinary importance of this parasite which may represent a potential danger for autochthonous fish in Mexico because of its suitability to heavily infect a wide spectrum of fishes of different families, including cichlids or cyprinids.

In the present paper available information about Centrocestus formosanus in Mexico, including data on the occurrence of the parasite in fish intermediate hosts, is summarized in order to identify existing gaps in the knowledge of the biology and epizootiology of this potentially important parasite and to stimulate further research in this area of fish parasitology.

MATERIALS AND METHODS

Cercariae found in Melanoides tuberculata from the Cuitzmala River near the village of Emiliano Zapata, Jalisco in Dec. 1998 were observed live. Illustrations and measurements were made from material fixed with hot 4% formaldehyde solution (see Scholz et al., 2000). Data on the occurrence of Centrocestus farmosanus metacercariae are based on investigations into the fish parasites carried out by the present authors in the states of Guanajuato, Jalisco, Morelos and Veracruz between 1991 and 1998 (G.S.M.) and the State of Tabasco in Nov. 1998 (T.S.). Metacercariae found on the gills of cichlid fish from Tabasco (see Table 2) were fixed with ammonium-picrate as described by Scholz and Aguirre-Macedo (2000). The gills of Cichlasoma salvini from the Puyacatengo River, Tabasco, heavily infected with C. formosanus were fed to two laboratory mice which were examined after 6 d. Adult trematodes recovered from mice were fixed with hot 4% formalin and stained with Schuberg's carmine (Scholz and Hanzelova, 1998).

Specimens studied are deposited at the National Helminthological Collection, Institute of Biology, UNAM, Mexico (CNHE Nos. 3708 and 3709); U.S. National Parasite Collection, Beltsville, Maryland, USA (USNPC No. 88539); Natural History Museum, London, UK (NHBM 1999.2.2.5); Institute of Parasitology, Ceske Budejovice, Czech Republic (IPCAS No. D-419); and Laboratory of Parasitology, CINVESTAV-IPN Merida, Mexico (CHCM Nos. 315).

RESULTS AND DISCUSSION

TAXONOMY AND SPECIES IDENTIFICATION

Identification of Mexican material of Centrocestus formosanus was based on comparison with existing descriptions of life cycle stages of this parasite from South East Asia and Hawaii (see Arizmendi, 1992).

In this study metacercariae found in fish from Mexico were conspecific with those from Laos (Scholz et at., 1990; Scholz, 1991) deposited in the helminthological collection of the Institute of Parasitology, [check{C}]esk[acute{e}] Bud[acute{e}]jovice (IPCAS No. D-271). Adult worms from Mexico also fully corresponded to those described from Asia (Chen, 1942; Premvati and Pande, 1974). It seems that this parasite has a low intraspecific variability because no marked morphological and biometrical differences among worms from the different zoogeographical regions were observed (Arizmendi, 1992; present study).

HISTORY OF INTRODUCTION

Centrocestus formosanus was first reported from Mexico by L[acute{o}]pez-Jim[acute{e}]nez (1987) as metacercariae encysted on the gills of the introduced cyprinid, the black carp Mylopharyngodon piceus, and other fish from a fish farm in central Mexico. L[acute{o}]pez-Jim[acute{e}]nez (1987) suggested that C. formosanus had been introduced to Mexico with the introduction of the black carp in 1979 and later infected other native fish in the Tezontepec de Aldama farm (L[acute{o}]pez-Jim[acute{e}]nez, 1987; V[acute{e}]lez-Fern[acute{a}]ndez et al., 1998).

Amaya-Huerta and Almeyda-Artigas (1994) and Salgado-Maldonado et at. (1995) questioned the introduction of the parasite directly with fish and doubted the possibility of reproducing black carp (around 1.5 m long) being eaten by birds or mammals, potential definitive hosts of the trematode. Amaya-Huerta and Almeyda-Artigas (1994) proposed that the parasite was imported as sporocyst or redial stages within the thiarid snall Melanoides tuberculata that was possibly introduced simultaneously with the black carp from China as a food for this malacophagous fish.

The following epizootiological data on Centrocestus formosanus support the contention about the parasite's introduction to Mexico in 1979 with snails (Melanoides tuberculata) from Asia: (1) Metacercariae of the trematode were not found on the gills of black carp brood stocks but on the gills of the first generation fry. This implies that these fish must have been infected at the farm with cercariae of C. formosanus, released from the first intermediate snail host. Furthermore, such small-sized fish would have easily been consumed by fish-eating birds or mammals and the life cycle would have been completed. Piscivorous birds are quite common around the Tezontepec de Aldama farm and they would have rapidly disseminated eggs of the parasite to new localities. (2) Metacercariae were found in a wide variety of fish cultured at Tezontepec de Aldama such as Ctenopharyngodon idellus, Cyprinus carpio, Ictalurus punctatus, Hypophthalmichthys molitrix, Megalobrana amblycephala, Mylopharyngodon piceus, Oreochromis aureu s, hybrids of O. mossambicus and O. urolepis hornorum and Poecilia reticulata (L[acute{o}]pez-Jim[acute{e}]nez, 1987 and pers. comm.). As these fish were then moved to other fish farms in the states of Morelos and Puebla they could have disseminated the parasite to these regions. (3) The parasite has recently been recorded in fish from other regions of Mexico (Tabasco) where it was most likely absent before the 1990s, as indicated by previous intensive parasitological research carried out 10-15 y ago (Pineda-L[acute{o}]pez, 1985; Pineda-L[acute{o}]pez et al., 1985a,b; Fucugauchi et al., 1988; Aguirre-Macedo and Garc[acute{i}]a-Magana, 1994). (4) Centrocestus formosanus has never been reported from countries where Melanoides tuberculatus lived for several decades, including regions with intensive parasitological research as the southern part of the United States, the Caribbean region or Brazil. As far the authors are aware, there had been no records of C. formosanus from the North American continent before it was reported by L[acute{o}]pez-Jim[acute{e}]nez (1987) from central Mexico.

Subsequent spread of the parasite might have been by dissemination of the different developmental stages: eggs released by the definitive hosts (fish-eating birds), intramolluscan stages in infected Melanoides tuberculata snails, cercariae swimming freely in the water or metacercariae encysted in fish. It is obvious, however, that further spread of Centrocestus farmosanus and its successful colonization of new localities was only possible due to the presence of a suitable first intermediate host, M. tuberculata snails, throughout a wide area of Mexico (Contreras-Arquieta et at., 1995a; Salgado-Maldonado et al., 1995).

Although it cannot be ruled out that Centrocestus formosanus was introduced to Mexico more than once, all existing data listed above indicate only one introduction. In any case, it is evident that the trematode has established successfully in Mexico and it has become an integral part of the helminth fauna of fishes in this country.

PRESENT DISTRIBUTION IN MEXICO

Centrocestus formosanus was first reported in the State of Hidalgo in 1985 (L[acute{o}]pez-Jim[acute]{e}nez, 1987) but it was then found in other Mexican states in central Mexico (Michoac[acute{a}]n, Morelos) and the Atlantic coast of Mexico (Veracruz, Tabasco) (Arizmendi, 1992; Amaya-Huerta and Almeyda-Artigas, 1994; Salgado-Maldonado et at., 1995; P[acute{e}]rez-Ponce de Le[acute{o}]n et at., 1996; Table 1).

The present geographical distribution of Centrocestus formosanus metacercariae in Mexico now includes the states of Colima, Guanajuato, Hidalgo, Jalisco, Michoac[acute{a}]n, Morelos, San Luis Potos[acute{i}], Sonora, Tabasco, Tamaulipas and Veracruz (Tables 1, 2). However, the occurrence of the parasite in other states is highly probable and its absence is likely due to lack of investigations into the fish parasites in these states rather than actual absence of the parasite. Recently, C. formosanus (cercariae in Melanoides tuberculata and metacercariae in fish) was found in the State of Jalisco at the Pacific Coast of Mexico. This finding indicates a high potential of the parasite to colonize geographically very distant regions. Metacercariae of C. formosanus are now very frequent in numerous fish species in several localities throughout western, central and southeastern parts of Mexico and prevalence and infection intensity may reach extraordinarily high values.

LIFE CYCLE

The life cycle of Centrocestus formosanus was elucidated many years ago (see Yamaguti, 1975 for review). In Mexico, most developmental stages of the parasite were described in detail by Arizmendi (1992) from naturally infected first and second intermediate hosts and experimental definitive host.

First intermediate host.--The thiarid snail Melanoides tuberculata serves as the first intermediate host of Centrocestus formosanus in Mexico (Arizmendi, 1992; Amaya-Huerta and Almeyda-Artigas, 1994; Amaya-Huerta, 1995; Salgado-Maldonado et at., 1995; present data).

This snail is native to India and was introduced to the southern United States during the 1940s and was later found in Venezuela and on several islands of the Lesser Antilles (Murray, 1971; Abbott, 1973; Perera et at., 1987). In Martinique the snail was first found in 1979. It was also purposely introduced in 1985 to D[acute{e}]sirade Island (Lesser Island) to eliminate populations of Biomphataria glabrata, the intermediate host of human schistosomiasis (Pointier et al., 1991, 1993). The snail appeared in Cuba as late as 1983 (Perera et at., 1987), supposedly having been transported by migratory birds.

The snail was introduced to Mexico probably around the 1960s (Contreras-Arquieta et at., 1995a). It was first reported by Abbott (1973) from Veracruz but then spread rapidly and, in 1995, was reported from more than 70 localities in 12 Mexican states (Chiapas, Chihuahua, Coahuila, Durango, Morelos, Nayarit, Nuevo Le[acute{o}]n, Puebla, Quintana Roo, Tabasco, Tamaulipas, Veracruz) (Contreras-Arquieta et at., 1995a; Contreras-Arquieta, 1998). The presence of Metanoides tubercutata in Mexico seems to have a negative impact on populations of native molluscs (Contreras-Arquieta et at., 1995b).

Despite the wide distribution of Melanoides tuberculata in Mexico and its role as an intermediate host of numerous trematodes (Yamaguti, 1975), there are scanty data on the occurrence of larval stages of Centrocestus formosanus in naturally infected snails in Mexico (Arizmendi, 1992; Salgado-Maldonado et al., 1995). Amaya-Huerta and Almeyda-Artigas (1994) provided data on the chaetotaxy of C. formosanus cercana.

In addition to larval stages of Centrocestus formosanus, rediae and cercariae of two other trematodes were found in Melanoides tuberculata in Mexico, namely those of Hap lorchis pumilio (Looss, 1896) (Heterophyidae) and Philophthalmus gralli Mathis et Leger, 1910 (Philophthalmidae) (Scholz et at., 2000). It is probable that at least the former species, previously not reported from Mexico, was introduced with infected M tuberculata snails.

Second intermediate host.--Cercariae liberated from snails encyst on the gills of fish. In Mexico, a number of fresh- or brackishwater fish of the families Atherinidae, Cichlidae, Cyprinidae, Eleotridae, Goodeidae, Ictaluridae and Poeciliidae have been reported to harbour Centrocestus formosanus metacercariae (Table 1). It seems that there is a low host specificity of the trematode at the level of the second intermediate host but there are undoubtedly differences in susceptibility of respective fish species (Table 2). In addition to fish, Amaya-Huerta (1995) reported the frog Spea multiplicata (Pelobatidae) as an experimental second intermediate host of C. formosanus.

Definitive host.--The heron Butorides striatus is the only natural definitive host of Centrocestus formosanus reported from Mexico (Amaya-Huerta, 1995). However, it is probable that other fish-eating birds such as herons, cormorants or pelicans and mammals, like some rodents and carnivores, serve as definitive hosts of the parasite since chicks, ducklings and mice were also suitable experimental hosts (Arizmendi, 1992; Salgado-Maldonado et at,, 1995; present data).

MORPHOLOGY OF DEVELOPMENTAL STAGES

Most of the developmental stages of Centrocestus formosanus from Mexico were described and illustrated by Arizmendi (1992). In addition, Salgado-Maldonado et at. (1995) provided measurements of C. formosanus cercaria, metacercaria and adult. However, there are slight differences in the morphology of developmental stages as described by the above mentioned authors and those obtained in this study. In addition, published data contain some inaccuracies in measurements of their respective developmental stages as indicated by much larger dimensions of organs in metacercariae than in adults (e.g. the oral sucker of the metacercaria was reported to be twice as long as that in the adult and the pharynx was also reported as being much larger in the metacercaria than in the adult) or incorrect length of the cercarial tail (Salgado-Maldonado et at., 1995; Table 1).

The flame cell pattern of Centrocestus formosanus from Mexico is 2 [(2 + 2) + (2 + 2)] (Arizmendi, 1992; present data; Fig. 1) and corresponds to that reported by Martin (1958) from Hawaii. Flame cells are arranged in pairs, most cells of each pair being close one to another.

Redia.--The redia of Centrocestus formosanus from Melanoides tuberculata from Mexico was described and illustrated by Arizmendi (1992; Fig. 1). It is elongate with a short gut and contains several cercariae in different developmental stages.

Cercaria.--The cercaria of Centrocestus formosanus is small, oculate, gymnocephalous (distome, leptocercous according to Amaya-Huerta and Almeyda-Artigas, 1994). It has a pyriform body and a narrow tail tapering posteriorly and provided with transverse tegumental annulations (Fig. 1). The cercaria was first reported from Mexico by Arizmendi (1992). The present study enabled us to describe some morphological details (Fig. 1), including the morphology of the gland cells. Each gland has a duct and these ducts from both sides do not connect together as described by Arizmendi (1992). Arizmendi described the cercaria of Centrocestus formosanus as possessing a well-developed acetabulum. However, only a cluster of cells representing a primordium of the acetabulum was observed in this study (Fig. 1) which agrees with the observations of Martin (1958).

The cercaria of Centrocestus formosanus resembles that of Ascocotyle (Phagicola) diminuta and A. (P.) nana in the shape of the body and tail, the presence of acicular spines on the dorsal side of the mouth opening and a spine on the tip of the tail (Fig. 1; Ostrowski de Nunez, 1993; Ditrich et al., 1997). Amaya-Huerta and Almeyda-Artigas (1994) studied the chaetotaxy of cercariae from Melanoides tuberculata from Mexico (Morelos) and confirmed their identity with C. formosanus.

Metacercaria.--The metacercaria of Centrocestus formosanus from Mexico was described in detail by Arizmendi (1992). The metacercariae encyst on the gills and are surrounded by a semispherical, mechanically fairly resistant cyst. The metacercarial cysts invade the cartilage of the gill filaments and are usually located near the base of the gill cartilage (Velez-Hernandez et al., 1998; present study). Due to their location, the cysts are difficult to isolate. Beside the typical site of location, the shape and size of cysts, the most characteristic feature of C. formosanus metacercariae is the presence of X-shaped excretory bladder containing dark excretory granules (Fig. 2). The metacercariae are pyriform or conical in shape when liberated from a cyst and entirely covered with tegumental spines (Fig. 2). The mouth is surrounded by two complete rows of 16 spines each; the number of circumoral spines appears to be quite constant (Figs. 4, 5). The genitalia are well developed, including the primordium of the uter us. Within the definitive host, trematodes mature rapidly becoming gravid within a few days (6 d postinfection; present data).

Adult.--Adult trematodes are small, pyriform, with a spinous tegument (Fig. 3). The oral sucker is armed with 32 spines forming two circlets of circumoral spines but it lacks the posterior appendage (solid prolongation) typical of other heterophyids of the subfamily Phagicolinae which occur simultaneously in fish in Mexico (Scholz et al., 1997). The acetabulum of Centrocestus formosanus is well developed and is not transformed into a ventrogenital sac as in members of other heterophyid genera such as Assocotyle or Haplorchis (Pearson, 1964; Scholz et al., 1997).

Adults of Centrocestus formosanus have been reported in Mexico only from experimental hosts such as chicks, ducks and mice (Arizmendi, 1992; Salgado-Maldonado et at., 1995), except for the finding of adults in the heron Butorides striatus from Morelos (Amaya-Huerta, 1995).

The paucity of records of adult trematodes from Mexico is undoubtedly related to scarcity of studies on the helminth fauna of fish-eating birds and mammals in this country. Moreover, adult trematodes are very small and they may easily be overlooked in the intestine of the host or may be misidentified if definitive hosts are examined a long time after their capture and only dead trematodes lacking circumoral spines are found. Although there are almost no field observations, it can be assumed that the present wide distribution of Cen trocestus formosanus in Mexico has been facilitated by high vagility of its definitive hosts which might have disseminated parasite eggs into other areas.

PATHOLOGY IN FISH

Despite the fact that infections with Centrocestus formosanus metacercariae are often heavy and that this trematode has been reported as a causative agent of diseases of cultured fish in Asia, there are very few data on pathogenicity of metacercariae in fish hosts in Mexico. Lopez-Jimenez (1987) claimed that metacercariae may cause severe problems, e.g., decreasing respiratory capacity of fish and, in heavy infections, may lead to the death of fry, but it is not clear whether these data were based on the author's own observations.

Velez-Hernandez et at. (1998) did not observe pathological changes due to metacercarical cysts on gross examination of the gills of common carp (Centrocestus carpio) but microscopical examination by these authors revealed moderate to severe hyperplasia of cartilage of the primary lamellae. Other histological findings included mild hyperplasia of the lymphoid tissue in the gills, epithelial hyperplasia of lamellae, gill hyperaemia and congestion (Velez-Hernandez et at., 1998). It should, however, be pointed out that Velez-Hernandez et al. (1998) studied fish infected with quite low parasite burden (a total of 377 metacercariae in 28 carp) whereas infection of some fish may reach almost 6000 metacercarial cysts per fish (Table 2). It was observed that cichlid fish from the Puyacatengo River in Tabasco infected with several hundreds of C. formosanus metacercariae maintained in the laboratory died much more quickly after capture that uninfected congeners.

In view of the fact that that this trematode has a fairly low specificity to its second intermediate host, which enables it to infect a wide spectrum of fish species, evaluation of the pathogenicity of metacercariae is important for feral fish populations as well as aquaculture operations.

EPIZOOTIOLOGY

The history of the spread of Centrocestus formosanus after its introduction to this country clearly demonstrates that very little, if any, attention has been paid to the potential problem for aquaculture. The occurrence of C. formosanus in numerous species of native fish from a large part of Mexico also shows that efforts to eliminate this parasite or at least to prevent its rapid spreading throughout the Mexican territory have been negligible.

All available data suggest that Centrocestus formosanus has had favourable conditions for its rapid and wide range-expansion in Mexico: (1) a wide distribution of its first intermediate host that now encompasses 13 Mexican states (Contreras-Arquieta et al., 1995a, b; Contreras-Arquieta, 1998; present data); (2) a low specificity at the level of the second intermediate host (Tables 1, 2) and, therefore, availability of potential fish hosts almost everywhere; (3) a wide spectrum of potential definitive hosts that may serve as reservoirs of the parasite; (4) the high mobility of definitive hosts enabling them to cross natural barriers that prevent spreading of parasite stages in aquatic animals (snails, fish) and to disseminate eggs to new regions; (5) lack of effective methods of prevention and control in fish farms which makes it possible to move infected fish stocks throughout the country.

Extraordinarily rapid distribution of the trematode to an extremely large area of Mexico since its first appearance in 1979 seems to have been realized mainly in two principal ways: (1) disseminaton of eggs with definitive hosts, in particular fish-eating birds; (2) movement of infected fish stocks from one fish farm to others throughout Mexico. Dissemination of the parasite into natural waters by infected feral fish may also have taken place in addition to accidental transfer of infected Melanoides tuberculata snails either by humans or birds.

PROSPECTS

Centrocestus formosanus is now a widely distributed parasite that infects a wide range of fish of different families. Recent records of C. formosanus in new hosts and regions, including the Pacific coast (Table 2), suggests that it continues its range-expansion. The parasite is already established in natural water bodies and its elimination is now practically impossible. It also seems unlikely that further spread of C. formosanus to new areas can be prevented because of favorable conditions that might allow the parasite to successfully colonize other parts of Mexico.

Despite this pesimistic scenario, the negative impact of this recently imported parasite on cultured fish might be decreased by the application of adequate preventive and control measures based on better knowledge of its biology and epizootiology. Some of these measures are briefly mentioned below: (1) cultured fish, in particular those intended for introduction to other farms, should be examined regularly for the presence of parasites and movement of parasite-free stocks of fish only should be allowed; (2) populations of snails (Melanoides tuberculata) in fish farms should be eliminated in order to prevent contact of emerged cercariae with fish and their infection; (3) fish-eating birds and mammals should be prevented from feeding on fish or their carcasses in fish farms.

Numerous aspects of Centrocestus formosanus biology and epizootiology remain to be clarified. Despite extensive data on secondary intermediate hosts of the parasite in Mexico, actual susceptibility of these fish to C. formosanus infection needs to be better known. Moreover, the role of individual fish species in the maintainance and transmission of the trematode also needs study. Little is also known about the occurrence of Melanoides tuberculata in some parts of Mexico (Contreras-Arquieta et al., 1995a). It is evident that the parasite cannot complete its life cycle in localities where a suitable intermediate host is absent. Therefore, monitoring of the present distribution of M. tuberculata and its infection with larval stages of C. formosanus is essential to predict the occurrence of the trematode in new areas and to prevent its introduction to fish farms in these regions. Much more emphasis should also be given to histopathological studies to assess the actual impact of the parasite on fish of different species and age classes. Spectrum of natural definitive hosts and their epizootiological importance in transmission and maintaining the parasite in Mexico should also be known better.

V[acute{e}]lez-Hern[acute{a}]ndez et al. (1998) questioned the possible impact of Centrocestus formosanus on human health in Mexico. Taking into account the site of infection of metacercariae (gills of fish), it seems unlikely that this parasite might have any zoonotic importance in this country. Nevertheless, lightly fried fish are eaten whole, including gills, in some localities in Mexico as P[acute{a}]atzcuaro Lake. In any case, thorough cooking of fish is necessary to prevent potential human diseases caused by C. formosanus.

Centrocestus formosanus is undoubtedly an important parasite which should attract more attention of fish parasitologists, veterinarians, aquaculturist and fishery managers in Mexico. It is hoped that this review will stimulate further research for a better understanding of all aspects of the life cycle, transmission, host-parasite relationships and effective control of C. formosanus.

Acknowledgments.--The authors are deeply indebted to the following Mexican coworkers who helped them in collection of snails and fish and their examination for parasites: Guillermina Caba[tilde{n}]as-Caranza and Rafael B[acute{a]}ez-Val[acute{e}], Institute of Biology, UNAM, Mexico, Juan Manuel Caspeta-Mandujano, University of Morelos, Cuernavaca, Dr. Victor Vidal-Martinez, David Gonz[acute{a}]lez-Solis, Clara Vivas-Rodriguez, Edgar Mendoza-Franco and Gregory Arjona-Torres, all CINVESTAV-IPN M[acute{e}]rida. Thanks are due to Serapio L[acute{o}]pez-Jim[acute{e}]nez, University of Tabasco (UJAT), Villahermosa, for providing unpublished data on the occurrence of Centrocestus formosanus metacercariae and valuable advice, Dr. Jos[acute{e}] Luis Dominguez-Alpizar, Faculty of Veterinary Sciences, University of Yucatan (UADY), Merida, for providing laboratory mice for experiments, Dr. Leopoldina Aguirre-Macedo for help with experimental infections, Dr. Rossanna Rodriguez-Canul for helpful suggestions to an early dr aft of the paper and Drs. Victor Vidal-Martinez and L. Aguirre-Macedo (all CINVESTAV-IPN M[acute{e}]rida) for permission to present unpublished data on the occurrence of C. formosanus metacercariae in cichlid fish from Tabasco. This study was supported by projects Nos M-135, B021 and H007 of the National Comission for Study and Use of Biodiversity (CONABIO), Mexico. The stay of one of the authors (T.S.) in Mexico was supported by the National Council for Science and Technology of Mexico (CONACyT--catedra patrimonial) and his short stay at the Biological Station at Chamel[acute{a}], Jalisco, by the Institute of Biology, UNAM, M[acute{e}]xico.

(1.) Permanent address: Institute of Parasitology, Academy of Sciences of the Czech Republic, Branisovska 31, 370 05 Ceske Budejovice, Czech Republic. e-mail: tscholz@paru.cas.cz

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                     Second intermediate hosts (fish)
                   of Centrocestus formosanus in Mexico
       Fish species               State
ATHERINIDAE
Chirostoma humboldtianum      Michoac[acute{a}]n
CICHLIDAE
 Oreochromis aureus           Hidalgo
 O. mossambicus X O. urolepis Hidalgo
  hornorum
CYPRINIDAE
 Carassius auratus            Morelos
 Ctenopharyngodon idella      Hidalgo
 Cyprinus carpio              Colima
                              Hidalgo
                              San Luis Potos[acute{i}]
 Hypophthalmichthys molitrix  Hidalgo
 Megalobrema amblycephala     Hidalgo
 Mylopharyngodon piceus       Hidalgo
ELEOTRIDAE
 Gobiomorus maculatus         Veracruz
                              Veracruz
GOODEIDAE
 Ilyodon whitei               Morelos
ICTALURIDAE
 Ictalurus punctatus          Hidalgo
       Fish species                 Locality
ATHERINIDAE
Chirostoma humboldtianum      Laguna de Zacapu
CICHLIDAE
 Oreochromis aureus           Tezontepec de Aldama
 O. mossambicus X O. urolepis Tezontepec de Aldama
  hornorum
CYPRINIDAE
 Carassius auratus            Las Estacas
 Ctenopharyngodon idella      Tezontepec de Aldama
 Cyprinus carpio              Laguna de Amela
                              Tezontepec de Aldama
                              El Peaje
 Hypophthalmichthys molitrix  Tezontepec de Aldama
 Megalobrema amblycephala     Tezontepec de Aldama
 Mylopharyngodon piceus       Tezontepec de Aldama
ELEOTRIDAE
 Gobiomorus maculatus         R[acute{i}]o Tecolutla
                              Guti[acute{e}]rrez Zamora, El
                              Salmoral, Tlacotalpan
GOODEIDAE
 Ilyodon whitei               R[acute{i}]o Amacuzac
ICTALURIDAE
 Ictalurus punctatus          Tezontepec de Aldama
       Fish species                      Reference
ATHERINIDAE
Chirostoma humboldtianum      Ar[acute{e}]valo et al. (1994)
CICHLIDAE
 Oreochromis aureus           L[acute{o}]pez-Jim[acute{e}]nez
                              (pers.comm.)
 O. mossambicus X O. urolepis L[acute{o}]pez-Jim[acute{e}]nez (pers.
  hornorum                    comm.)
CYPRINIDAE
 Carassius auratus            Amnaya-Huerta and Almeyda-
                              Artigas (1994)
                              Salgado-Maldonado et al. (1995)
 Ctenopharyngodon idella      L[acute{o}]pez-Jim[acute{e}]nez (1987),
                              Arizmendi (1992)
 Cyprinus carpio              V[acute{e}]lez-Hern[acute{a}]ndez
                              et al. (1998)
                              L[acute{o}]pez-Jim[acute{e}]nez (1987),
                              Arizmendi (1992)
                              L[acute{o}]pez-Jim[acute{e}]nez (pers.
                              comm.)
 Hypophthalmichthys molitrix  L[acute{o}]pez-Jim[acute{e}]nez (1987),
                              Arizmendi (1992)
 Megalobrema amblycephala     L[acute{o}]pez-Jim[acute{e}]nez (1987),
                              Arizmendi (1992)
 Mylopharyngodon piceus       L[acute{o}]pez-Jim[acute{e}]nez (1987),
                              Arizmendi (1992)
ELEOTRIDAE
 Gobiomorus maculatus         Campos (1992)
                              Vel[acute{a}]zquez-et al. (1994)
GOODEIDAE
 Ilyodon whitei               Caspeta-Mandujano (1994)
ICTALURIDAE
 Ictalurus punctatus          L[acute{o}]pez-Jim[acute{e}]nez (1987--
                               as "barge"; pers. comm.)
POECIILIDAE
 Heterandria bimaculata Morelos Las Estacus
 Poecilia latipinna     Morelos Las Estacus
 Poecilia reticulata    Hidalgo Tezontepec de Aldama
 Poecilia sphenops      Morelos Las Estacas
 Xiphophours helleri    Morelos Las Estacas
 Xiphophorus maculatus  Morelos Las Estacas
POECIILIDAE
 Heterandria bimaculata Amaya-Huerta and Almeyda-Artigas (1994)
                        Salgado-Maldonado et al. (1995)
 Poecilia latipinna     Amaya-Huerta and Almeyda-Artigas (1994)
                        Salgado-Maldonado et al. (1995)
 Poecilia reticulata    L[acute{o}]pez-Jim[acute{e}]nez
                        (unpubl. data)
 Poecilia sphenops      Amaya-Huerta and Almeyda-Artigas (1994)
                        Salgado-Maldonado et al. (1995)
 Xiphophorus helleri    Amaya and Almeyda (1994)
                        Salgado-Maldonado et al. (1995)
 Xiphophorus maculatus  Amaya and Almeyda (1994)
                        Salgado-Maldonado et al. (1995)
                  New records of Centrocestus formosanus
              matacercariae in Mexico. Date = month and year;
                        N = number of fish examined
           Family
        Fish Species        State            Locality
CHARACIDAE
  Bramocharax caballeroi    Veracruz   R[acute{i}]o La Palma
CICHLIDAE
  Cichlasoma gadovii        Veracruz   R[acute{i}]o La Palma
  Cichlasoma geddesi        Tabasco    Yumka
  Cichlasoma helleri        Tabasco    Yumka
  Cichlasoma managuense     Tabasco    El Horizonte
  Cichlasoma nigrofasciatum Morelos    Rio Amacuzac
  Cichlasoma pasionis       Tabasco    Yumka
  Cichlasoma salvini        Tabasco    R[acute{i}]o Puyacatengo
CYPRINIDAE
  Algansea tincella         Guanajuato Persa Ignacio Allende
  Yuriria alta              Guanajuato Presa Ignacio Allende
ELEOTRIDAE
  Dormitaror latifrons      Jalisco    R[acute{i}]o Purification
  Gobiomorus dormitor       Veracruz   R[acute{i}]o La Antigua
                            Veracruz   R[acute{i}]o Tecolutla
                            Veracruz   R[acute{i}]o Papaloapan
                            Veracruz   R[acute{i}]o La Palma
                            Veracruz   Aroyo Balzapote
                            Veracruz   R[acute{i}]o M[acute{a}]quinas
  Gobiomorus maculatus      Jalisco    R[acute{i}]o Purification
                            Jalisco    R[acute{i}]o Cuitzmata
  Gobiomorus polylepis      Jalisco    R[acute{i}]o Cutizmala
                                                   Intensity
           Family                       Prevalence
        Fish Species        Date      N    [%]       Mean     Range
CHARACIDAE
  Bramocharax caballeroi     2.97     7     43         3       1-5
CICHLIDAE
  Cichlasoma gadovii        11.96    14     14        14       7-20
  Cichlasoma geddesi        11.98     3     67        21       3-38
  Cichlasoma helleri        11.98    10     10         4        4
  Cichlasoma managuense     11.98     2    100      1974     565-3383
  Cichlasoma nigrofasciatum 12.95    22     5          1        1
  Cichlasoma pasionis       11.98     3     33         7        7
  Cichlasoma salvini        11.98    13     31        57       5-164
CYPRINIDAE
  Algansea tincella          4.95    22     14        58       2-168
  Yuriria alta               6.97    14     21         2       1-4
                             9.97     3     33         5        5
ELEOTRIDAE
  Dormitaror latifons        3.95     1    100         3        3
  Gobiomorus dormitor       4.-10.91 30    100       133      10-670
                             8.91    60     98       123       2-660
                            5.-7.91  30     70        19       1-163
                             6.96     4     25        89        89
                            11.96     7     57        67      29-181
                             2.97    23     17        71       1-161
                            11.96     4    100       949     110-2580
                            11.96     7     71        86       4-188
  Gobiomorus maculatus       3.95     5    100      1260      92-2400
                             1.95    21     90       850     330-1542
                             3.95    37     92       822      28-2187
                             9.95    30     43      2824       1-5935
  Gobiomorus polylepis       9.95     8     63       594     151-1167
GOBIIDAE
 Gobionellus microdon  Jalisco    R[acute{i}]o Cuitzmala
GOODEIDAE
 Goodea atripinnis     Guanajuato Presa Ignacio Allende
 Ilyodon whitei        Morelos    R[acute{i}]o Amacuzac
 Goodeidae gen. sp.    Jalisco    La Manzanilla
MUGILIDAE
 Agonostomus monticola Jalisco    R[acute{i}]o Cuitzmala
                       Jalisco    R[acute{i}]o Purificaci[acute{o}]n
                       Veracruz   R[acute{i}]o La Palma
                       Veracruz   R[acute{i}]o M[acute{a}]quinas
POECILIIDAE
 Heterandria sp.       Veracruz   R[acute{i}]o La Palma
 Poecilia sphenops     Jalisco    R[acute{i}]o Purificaci[acute{o}]n
                       Morelos    R[acute{i}]o Amacuzac
                       Veracruz   R[acute{i}]o La Palma
 Poecilia sp.          Guanajuato Presa Ignacio Allende
 Poeciliopsis gracilis Morelos    R[acute{i}]o Amacuzac
 Xiphophorus helleri   Veracruz   R[acute{i}]o M[acute{a}]quinas
GOBIIDAE
 Gobionellus microdon      1.95     10  30  349 177-543
GOODEIDAE
 Goodea atripinnis         6.97     11  27    5   2-11
 Ilyodon whitei        11.94-11.95 520  49   73   1-690
                          12.95     22  82  107   1-426
 Goodeidae gen. sp.       11.94      1 100    1    1
MUGILIDAE
 Agonostomus monticola     1.95      7  86  415 235-740
                           9.95     40  20  153  14-693
                           3.95      2 100  915 818-1012
                          11.96      6  50    6   1-17
                          11.96     13  15    3      3
POECILIIDAE
 Heterandria sp.           2.97      4  25    1      1
 Poecilia sphenops         3.95     22   5 1277   1277
                           3.95     11   9    1      1
                          12.95     43  14    5   1-13
                          11.96     19  11   20   2-38
 Poecilia sp.              6.97      1 100    1      1
 Poeciliopsis gracilis     3.95     18   6    8      8
                          12.95     15  20    1   1-2
 Xiphophorus helleri      11.96     11  36   30   8-95
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