Richness and endemism of helminth parasites of freshwater fishes in Mexico

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1 Biological Journal of the Linnean Society, 2008, 94, With 3 figures Richness and endemism of helminth parasites of freshwater fishes in Mexico ROGELIO AGUILAR-AGUILAR 1 *, GUILLERMO SALGADO-MALDONADO 2, RAÚL CONTRERAS-MEDINA 1,3 and ANDRÉS MARTÍNEZ-AQUINO 2 1 Facultad de Ciencias, Departamento de Biología Evolutiva, Apartado Postal , Universidad Nacional Autónoma de México, CP 04510, México 2 Instituto de Biología, Universidad Nacional Autónoma de México, Apartado Postal , CP 04510, México 3 Ciencias Biológicas, Universidad Westhill, CP 05610, México Received 6 February 2007; accepted for publication 24 August 2007 Distribution records of 152 adult helminth taxa parasites of freshwater fishes in Mexico were analysed to determine areas of high richness and endemism. Distribution maps were prepared for each taxon and overlaid onto a map of Mexico divided into 1 1 degree grid-cells. Richness was determined by counting recorded helminth species in each grid-cell. A corrected weighted endemism index was calculated for each grid-cell, and the relationship between richness and endemicity was analysed with an Olmstead Tukey corner test of association. Five areas of high richness and endemism were identified: (1) Los Tuxtlas and the Papaloapan river basin, on the Gulf of Mexico; (2) the Grijalva-Usumacinta basin near the Gulf of Mexico coastal plain; (3) the Yucatan Peninsula; (4) the Sierra de Manantlán Biosphere Reserve in western Mexico; and (5) the Pátzcuaro lake, in central Mexico. The distribution of richness and endemism of helminth parasites of freshwater fishes in Mexico is congruent with distributional patterns described for other freshwater taxa in Mexico. Patterns of richness and/or endemism in the studied areas can be explained by the ichthyological composition of their bodies of water. The present study establishes an objective way of analysing the relationship between richness and endemicity, and suggests that helminths can make valuable contributions to regionalization of geographical areas and for identification of rich and biologically complex areas with potential for conservation of aquatic systems The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 94, ADDITIONAL KEYWORDS: Acanthocephala biodiversity Cestoda hotspots Monogenea Nematoda Trematoda. INTRODUCTION Mexico is located at the intersection of the Neotropical and Nearctic biogeographical regions, and its biological diversity and geological history make it an interesting area for biogeographical research (Morrone, 2005). Many regions in Mexico are known as areas of endemism for different taxa (Arriaga et al., 1997; Morrone, 2005, 2006); however, these studies have been focused in terrestrial taxa, whereas the distribution of epicontinental aquatic biodiversity has received limited attention (Huidobro et al., 2006). In an effort to determine the patterns of biodiversity *Corresponding author. raguilar@ibiologia.unam.mx and their similarity to the distributional patterns described for other taxa in the country, we analysed the distributional data of the helminth parasites of freshwater fish in Mexico in terms of species richness and endemism. Both richness and endemism are important for biodiversity and constitute an essential component of the hotspot concept (Myers, 1988, 1990; Mittermeier, Myers & Goettsch-Mittermeier, 1999; Contreras-Medina & Luna, 2007). The known helminth parasite fauna of freshwater fish in Mexico includes 262 nominal helminth species: 164 adult and 98 larvae (Salgado-Maldonado, 2006). This richness is not homogeneously distributed throughout the country. The south-east is rich in helminth species (Aguilar-Aguilar, Contreras-Medina & Salgado-Maldonado, 2003), whereas central Mexico 435

2 436 R. AGUILAR-AGUILAR ET AL. is less so (Salgado-Maldonado et al., 2001b). Some hydrological systems, such as the Papaloapan, Grijalva-Usumacinta, and the Yucatan Peninsula, are richer than others such as the Balsas, Lerma, and Pánuco systems (Salgado-Maldonado et al., 2001a, b, 2004, 2005a, b). One explanation for this richness distribution concerns the basin s geological ages, magnitudes, and ichthyofaunal compositions (Salgado- Maldonado et al., 2005a). Recent published research has addressed the distribution of the helminth parasites of freshwater fishes in Mexico based on intuitive considerations (Pérez-Ponce de León, 2003; Salgado-Maldonado, 2006) or by applying different formal biogeographical methods such as parsimony analysis of endemicity (Aguilar-Aguilar et al., 2003, 2005), panbiogeography (Rosas-Valdez & Pérez-Ponce de León) and numerical approaches (Vidal-Martínez & Kennedy, 2000; Pérez- Ponce de León & Choudhury, 2005). This research suggests certain degree of endemism among helminth parasites in freshwater fish in different hydrological basins in Mexico. The concept of endemism is essential in historical biogeography (Henderson, 1991; Crisp et al., 2001; Linder, 2001a). A taxon is defined as endemic if its distribution is restricted to a given territory, regardless of territory size (Anderson, 1994; Zunino & Zullini, 2003). Although endemism is a relative concept, there is a common trend to associate it to small areas; an area of endemism is defined as one delimited by the congruent distribution of at least two species with a restricted range (Nelson & Platnick, 1981; Morrone & Crisci, 1995; Espinosa, Aguilar & Escalante, 2001; Linder, 2001a). The higher the number of species restricted to an area of endemism, the greater its relevance, especially if these taxa are unrelated (Crisp et al., 2001). Areas of endemism are the standard units of historical biogeography research (Nelson & Platnick, 1981; Humphries & Parenti, 1999; Crisp et al., 2001) and allow hypotheses to be proposed with respect to the history of biogeographical units and their biotas (Morrone & Crisci, 1995; Da Silva, De Sousa & Castelleti, 2004). Recognition of areas of endemism is also important because it allows division of terrestrial space into realms, regions, dominions, provinces, and districts (Contreras- Medina, Morrone & Luna, 2001). Given that the concept of endemism is linked to specific areas, identification of areas of endemism is directly dependent on the scale and density of the sample (Crisp et al., 2001). Areas of endemism are commonly proposed intuitively by examining distribution maps for overlapping areas of high concentrations of species with limited distribution ranges (McAllister et al., 1994; Long et al., 1996; Crisp et al., 2001; Linder, 2001a; Morrone, 2001; Da Silva et al., 2004). Because this procedure cannot be replicated (Linder, 2001a; Hausdorf, 2002), some formal methods for determining areas of endemism have been proposed (Morrone, 1994; Espinosa et al., 2001; Linder, 2001a; Szumik et al., 2002; for criticism of these methods, see also Hausdorf, 2002). Some of these methods are based on the division of an extensive area into quadrats that allow artificially delimited areas to be analysed with a relatively similar size on a minor scale in comparison with other geographical units (Morrone, 1994; Crisp et al., 2001; Linder, 2001b; Morrone & Escalante, 2002; Da Silva et al., 2004; Luna, Alcántara & Contreras- Medina, 2004; Rovito, Arroyo & Pliscoff, 2004; Biondi & D Alessandro, 2006; Contreras-Medina & Luna, 2007). Most of these studies identify areas of endemism by applying parsimony analysis of endemicity (Morrone, 1994). Although calculation of indices of endemism is an interesting alternative for recognizing these areas and has been used successfully with plants (Crisp et al., 2001; Linder, 2001b; Luna et al., 2004; Contreras-Medina & Luna, 2007), its application in other groups of organisms is desirable in order to verify their accuracy and repeatability. In the present study, the corrected weighted endemism index (CWEI) (Crisp et al., 2001; Linder, 2001b) was calculated to identify areas of endemism in Mexico, mapping, in a grid-cell system, the geographical distribution data of adult helminth parasites of freshwater fishes. The relation of high endemism and high richness of species let us to suggest hotspots. Additionally, the study represents a test of the utility of CWEI for detection of endemism patterns based on nonsessile organisms. MATERIAL AND METHODS We chose distribution records for 152 adult helminth parasite taxa from freshwater fish in Mexico (trematodes, monogeneans, cestodes, acanthocephalans, and nematodes) from the database of Salgado-Maldonado (2006), as well as from our own research data (the complete list is available upon request). All records were taxonomically validated to correct erroneous identifications, synonymies and other taxonomic problems (Scholz et al., 1997; Moravec, 1998; Scholz, Aguirre-Macedo & Salgado-Maldonado, 2001; Vidal- Martínez et al., 2001; Aguirre-Macedo & Scholz, 2005; Caspeta-Mandujano, 2005). Each datum represents a collected specimen, that is, all identifications are linked to voucher specimens. Helminth parasite records from fish in aquaculture ponds or farms were excluded from the analysis because they do not represent natural distribution (López-Jiménez, 2001; Flores-Crespo & Flores-Crespo, 2003) but, given that our interest is describing richness, we included introduced helminth species in all analyses (Jiménez-

3 RICHNESS AND ENDEMISM OF HELMINTHS 437 García, Vidal-Martínez & López-Jiménez, 2001; Salgado-Maldonado & Pineda-López, 2003; Salgado- Maldonado, 2006). Distribution maps for each taxon were prepared using GIS ArcView 3.2 (ESRI, 1999). Each collection point was superimposed on a map of Mexico overlaid witha1 1 degree grid. The grid method allows the delimitation of smaller areas within hydrological basins, which more clearly defines study region limits. Using this method, each basin can be subdivided into smaller analytical units of relatively equal size, which, to a certain degree, reflect the distribution of real fish and parasite species. It also enables objective joining of the parasitological faunas of nearby bodies of water, thus preventing the excessive fragmentation that would lead to using each sample site as an analytical unit. To simplify the distribution data, we transformed them into presence/absence of each helminth species in each grid cell. A species was treated as present in a cell when it had been recorded just once or many times parasitizing a fish caught in any body of water within that cell; its absence indicated the lack of a record for a helminth species in a cell. We determined richness by counting the helminth species recorded in each grid square. The endemism analysis is based on CWEI (Crisp et al., 2001; Linder, 2001b), which in turn is a modification of the weighted endemism index (WEI) used by cited authors. To calculate the WEI, each species is weighted for the inverse of its range such that each endemic species in a grid-cell has a maximum weight of 1; if a species is present in five grid-cells, it has a weight of 0.20 and one in 20 grid-cells has a weight of To calculate the value of each grid-cell, the weight values for all the species in that grid-cell are added so that squares with a high number of restricted range species have a higher score than grid-cells with fewer restricted range species (Linder, 2001b). To correct for the correlation with species richness, and to generate the CWEI, the weighted endemism is divided by the total number of species in a grid-cell (Crisp et al., 2001). We evaluated the relationship between richness and endemism with an Olmstead Tukey corner test of association (Steel & Torrie, 1980). This produces a graph in which each grid-cell is placed in one of four quadrants when mean richness and CWEI values are plotted. Grid-cells in the quadrat of high richness and endemism values are identified as hotspots, although this does not take into consideration threats to species at these locations (Myers, 1988, 1990). RESULTS AND DISCUSSION The 152 adult helminth species from freshwater fishes analysed in the present study were distributed in 66 grid-cells, which included at least one record of an adult helminth species (Fig. 1). The two helminth species with the highest number of records were the cestode Bothriocephalus acheilognathi Yamaguti, 1934 (25 grid-cells) and the trematode Crassicutis cichlasomae Manter, 1936 (24 grid-cells), whereas 56 taxa had records in just one grid-cell. The Mexican Nearctic, north of the Transmexican Volcanic Belt (19 20 N), had many empty squares; all the cells in this northern area with helminth records had a richness of less than ten species. Richness in the 66 grid squares with records was in the range 1 47 species per grid-cell (mean = 9.1 species). Just one helminth species was recorded in ten grid-cells. The two areas with the highest helminth species richness are in the south-east, near the Gulf of Mexico, and in western Mexico. The first includes the Papaloapan river basin, Los Tuxtlas in Veracruz (the highest species/grid-cell with 47 species), and different sites in the states of Tabasco and north-east Chiapas. The second is located in the Ayuquila river, within the Sierra de Manantlán Biosphere Reserve in the state of Jalisco (Fig. 1). The endemism analysis was performed with the 56 grid-cells containing at least two helminth species. The resulting CWEI values were in the range (mean value of 0.25) and 25 grid-cells had high endemism values (i.e. CWEI 0.25) (Fig. 2). Of these 25, 15 grid-cells had high CWEI values but low richness. Two of these grid-cells were considered areas of endemism due to the species found in them, although they had low richness: El Toboso and Abraham González springs, state of Durango (grid-cell 6); and Chicnahuapan lake along with different bodies of water in the upper Lerma river basin, state of México (grid-cell 34) (Fig. 3). Eight grid-cells with high richness and endemism values were identified (Fig. 2). They can be grouped into five hotspots: (1) Los Tuxtlas, in Veracruz, and the Papaloapan river basin; (2) lower reaches of Grijalva-Usumacinta hydrological basin, at the Gulf of Mexico coastal plain in Tabasco and the north-east of Chiapas; (3) central Yucatan Peninsula; (4) the Sierra de Manantlán Biosphere Reserve; and (5) Pátzcuaro Lake, in the state of Michoacán and the La Laja river, in the state of Guanajuato, both in the Lerma river basin (Fig. 3). RICHNESS AND ENDEMISM South-eastern Mexico has a high richness of helminth parasite species in freshwater fishes. This area probably runs continuously from the Papaloapan river basin (including Los Tuxtlas, the Tabasco coastal plain and north-east Chiapas) to the Yucatan Peninsula (Fig. 1). Within this area, the Coatzacoalcos

4 438 R. AGUILAR-AGUILAR ET AL. Figure 1. Richness of helminth parasites of freshwater fishes in Mexico. Figure 2. Olmstead Tukey corner test of association between richness and corrected weighted endemism index (CWEI). Empty squares ( ) identify two grid-cells where richness = 1; these were not considered as areas of endemism. river, in the state of Veracruz, appears empty because it has not been sampled. Given that this river s ichthyological composition is similar to that of the neighbouring Papaloapan and Grijalva-Usumacinta basins, it is likely that it is equally rich in helminth parasite species. A second empty space on the regional map results from the lack of surface water on the Yucatan Peninsula, except for sinkholes. The rich Sierra de Manantlán area in western Mexico is apparently isolated from other localities in central Mexico. Although grouping this site with the others in central Mexico (all within the Lerma river basin) creates a large area of relatively high richness, no other sites in the area have nearly as many recorded helminth species (Fig. 1). The CWEI can be compromised by insufficient or unbalanced samples (Crisp et al., 2001). Thirteen of the grid-cells with insufficient samples had low richness and high endemism values, and the high CWEI values in some of these squares can be explained by the accidental presence of a single, broadly distrib-

5 RICHNESS AND ENDEMISM OF HELMINTHS 439 Figure 3. Hostspots and areas of endemism for helminth parasites of freshwater fishes in Mexico. uted but infrequent helminth species. For example, high CWEI values for two of these grid-cells were due to records for Crepidostomum cornutum (Osborn, 1903) and Rhabdochona cascadilla Wingdor, 1918 (grid-cell 1), and Neocucullanus neocucullanus Travassos, Artigas & Pereira, 1928 and Rhabdochona acuminata (Molin, 1860) (grid-cell 66) in a single host species. These four helminth species are widely distributed in North and South America, respectively but, in Mexico they have only been collected at a single site (Valles-Ríos & Ruiz-Campos, 1997; Caspeta-Mandujano et al., 2005). The higher values of endemism for other cells are the result of records based on studies that do not include all the helminths parasitizing a given host, or that do not provide a complete inventory of the helminth species from a certain site (e.g. taxonomic studies such as new species descriptions). For example, the high CWEI value in grid-cell 53 is due to records for the two new species Rhabdochona salgadoi Caspeta-Mandujano & Moravec (2000) and Spinitectus humbertoi Caspeta- Mandujano & Moravec (2000), but the original study did not document other helminth species in the studied hosts from that site (Caspeta-Mandujano & Moravec, 2000). An additional factor that contributing to increase the CWEI value is the record of some helminth taxa found in fresh waters but parasitizing brackish fishes. These hosts and parasite taxa have been recorded in the same localities where typical freshwater species has been collected together with brackish species and, for this reason, were considered as freshwater taxa by Salgado-Maldonado (2006). For example, the grid-cell 52 contains records for a coastal lagoon, where strictly freshwater fish were not intensively examined and therefore data on them are scarce. In this grid-cell in particular, the high CWEI value is associated with the record of the acanthocephalan Pseudoleptorhynchoides lamothei Salgado-Maldonado, 1977 (Salgado-Maldonado, 2006). Another case that represents difficulty to strictly delimit fresh and brackish environment is the trematode Pseudoacanthostomum panamense, which

6 440 R. AGUILAR-AGUILAR ET AL. contributes with a relatively high value of CWEI for those three grid-cells in which occurs. More complete samples diminish the effect of these factors on the CWEI (Crisp et al., 2001). Grid-cell 6 (containing El Toboso and Abraham González springs, Durango) and grid-cell 34 (containing Chicnahuapan lake, state of México, and other bodies of water in the upper Lerma river basin) both had low richness but high CWEI values, which indicates areas of endemism. By contrast to the above discussed grid-cells 52 and 53, all the fish species in these waters have been examined, meaning that helminth richness in them will probably not increase substantially with new samples. The high endemism value in these squares is associated with four helminth species of restricted distribution: Allocreadium mexicanum Osorio-Sarabia, Pérez-Ponce de León & Salgado-Maldonado, 1986 and Margotrema bravoae Lamothe-Argumedo, 1970 in grid-cell 34; and these two species plus Margotrema guillerminae Pérez-Ponce de León, 2001 and Atactorhynchus duranguensis Salgado-Maldonado, Aguilar-Aguilar & Cabañas-Carranza, 2005 in grid-cell 6. These data suggest that some bodies of water can be centres of endemicity without having a high richness. The analyses identified five hotspots for helminth parasites of freshwater fish in Mexico: (1) Papaloapan river basin; (2) Grijalva-Usumacinta basin; (3) the Yucatan Peninsula; (4) Lerma river basin; and (5) the Sierra de Manantlán Biosphere Reserve. All five have previously been indicated as areas of endemism for different taxa; in fact, the Papaloapan, Grijalva- Usumacinta and Yucatan Peninsula hotspots fall within the Mesoamerican hotspot (Mittermeier et al., 1999). The most significant of the five in terms of richness and endemism is the Papaloapan river basin from its upper third to its drainage into Alvarado Lagoon in Veracruz, including the Catemaco lake and other bodies of water in the Los Tuxtlas region. The entire region is already considered a centre of endemism for other taxa such as freshwater fish and crustaceans (Miller, 1986; Álvarez & Villalobos, 1997; Rojas, Álvarez & Villalobos, 1997; Espinosa et al., 1998). The Grijalva-Usumacinta Basin near the Tabasco coastal plain and in north-east Chiapas has been reported as an area of endemism for freshwater fish (Miller, 1966). The Sierra de Manantlán has also been considered a centre of endemism for many freshwater and terrestrial taxa (Arriaga et al., 2000). The Lerma river basin and Yucatan Peninsula have a comparatively lower richness than the first three hotspots but remain important for the endemicity of their helminth species. Indeed, the Pátzcuaro lake and other bodies of water in the Lerma river basin, as well as the Usumacinta river and the sinkholes of the Yucatan Peninsula, are considered centres of endemism for helminths (Moravec et al., 1995; Scholz et al., 1996; Salgado-Maldonado et al., 2001b) and freshwater fishes (Espinosa et al., 1998). In other words, the data for helminth parasites of freshwater fish tends to further support the patterns described for other taxa in Mexico. A number of factors acting in conjunction can lead to restriction of taxa distribution and therefore generate an area of endemism. The extent of a taxon s range can also be restricted by a history of vicariance followed by speciation in isolation (Nelson & Platnick, 1981; Brown & Lomolino, 1998; Humphries & Parenti, 1999; Crisp et al., 2001). Hosts comprise the parasites immediate environment and therefore correspond to an ecological factor that may limit the establishment of a given helminth taxon in a body of water. The endemism of fishes in Mexico is seen as a result of vicariance processes caused mainly by fragmentation of bodies of water and a consequently high speciation rate (Espinosa et al., 1998; Miller, 1986). HELMINTH TAXA The high richness and endemism of the hotspots that have been identified in the present study can be explained by helminth species specificity to host families. This result show a strong correspondence with the first prediction proposed by Pérez-Ponce de León & Choudhury (2005), in relation to distributional patterns of host parasite associations in freshwater fishes of Mexico, which suggests that parasite fauna is largely circumscribed by higher levels of monophyletic host taxa, especially to the level of fish family. As helminth distribution is linked to their hosts (Dogiel, 1961; Wootten, 1973; Pérez-Ponce de León & Choudhury, 2005; Salgado-Maldonado et al., 2005a), this allows us to explain the richness and endemism of the hotspots by the ichthyological composition in their waters and the helminths associated with the fish families in them. For example, cichlids provide richness to grid-cells because they have very rich helminth communities, but they do not contribute significantly to endemism due to their broad distribution. Other fish families, in contrast, contribute substantially to endemism and little to richness. Atherinopsidae and Goodeidae, for example, are parasitized by helminth species that are highly specific to them and of limited distribution, but their helminth communities are comparatively poor (Choudhury & Dick, 2000; Salgado-Maldonado, 2006). The south-eastern Mexico hotspots (Papaloapan, Grijalva-Usumacinta, and Yucatan Peninsula) exist in response to the high degree of endemicity of the helminth parasites in the families Synbranchidae, Heptapteridae, Characidae, Lepisosteidae, Poeciliidae, and Eleotridae. More specifically, the high value

7 RICHNESS AND ENDEMISM OF HELMINTHS 441 of CWEI in these hotspots is mainly due to the following limited-distribution species: Monticellia ophisterni Scholz, de Chambrier & Salgado- Maldonado, 2001, Philometra ophisterni Moravec, Salgado-Maldonado & Aguilar-Aguilar, 2002, Pseudocapillaria ophisterni Moravec, Salgado- Maldonado & Jiménez-García, 2000 and Gibsonema ophisterni (Moravec, Salgado-Maldonado & Aguilar- Aguilar, 2002), associated with the Synbranchidae; Cucullanus mexicanus Caspeta-Mandujano, Moravec & Aguilar-Aguilar, 2000, Neophilometroides caudatus (Moravec, Scholz & Vivas-Rodríguez, 1995) and Paracapillaria rhamdiae Moravec, González-Solís, Vargas- Vázquez, 1995 in the Heptapteridae; Genarchella astyanacthys (Watson, 1976) and Proteocephalus brooksi García-Prieto, Rodríguez & Pérez-Ponce de León, 1996 in the Characidae; Cystoopsis atractostei Moravec & Salgado-Maldonado, 2003 and Perezitrema bychowskyi (Caballero y Caballero, 1975) in the Lepisosteidae; Spinitectus mexicanus Caspeta- Mandujano, Moravec & Salgado-Maldonado, 2000 in the Poeciliidae; Guavinella tropica Mendoza-Franco, Scholz & Cabañas-Carranza, 2003 in the Eleotridae; and Spinitectus agonostomi Moravec & Barus, 1971 in the Mugilidae. With their high helminth species diversity, the Cichlidae contribute both richness and endemism to these hotspots through these family specific species: Sciadicleithrum bravohollisae Kritsky, Vidal-Martínez & Rodríguez-Canul, 1994, Crassicutis cichlasomae, Oligogonotylus manteri Watson, 1976, Genarchella isabellae (Lamothe- Argumedo, 1977), Neoechinorhynchus golvani Salgado-Maldonado, 1978, Rhabdochona kidderi Pearse, 1936, and Mexiconema cichlasomae Moravec, Vidal-Martínez & Salgado-Maldonado, 1992 (Salgado- Maldonado, 2006). Endemism in the Sierra de Manantlán hotspot in western Mexico is due to the helminths Paracapillaroides agonostomi Moravec, Salgado-Maldonado & Caspeta-Mandujano, 1999 in the Mugilidae; Proteocephalus chamelensis Pérez-Ponce de León, Brooks & Berman, 1995, Procamallanus jalisciencis Moravec, Salgado-Maldonado & Caspeta-Mandujano, 2000, and Procamallanus gobiomori Moravec, Salgado- Maldonado & Caspeta-Mandujano, 2000 in the Eleotridae; and Rhabdochona guerreroensis Caspeta- Mandujano, Aguilar-Aguilar & Salgado-Maldonado, 2002 in the Gobiidae. These fish families have rich helminth communities, which contribute considerable richness to this hotspot. Its richness is further enhanced by other more broadly distributed helminth species, such as Magnivitellinum simplex Kloss, 1966, Rhabdochona kidderi and Capillaria cyprinodonticola Huffman & Bullock, 1973, as well as the introduced species Bothriocephalus acheilognathi and Cychlidogyrus sclerosus Paperna & Thurston, The analysis of this hotspot could be further modified with additional sampling, because the above-mentioned helminth taxa are associated with secondary widely distributed fish families. The hotspot in central Mexico qualifies as an area of endemism because of the helminth species: Margotrema bravoae, M. guillerminae, Salsuginus sp. and Gyrodactylus sp. in the Goodeidae; A. mexicanum and Spinitectus osorioi Choudhury & Pérez-Ponce de León, 2001 in the Atherinopsidae; and the monogenean Octomacrum mexicanum Lamothe-Argumedo, 1981 in the Cyprinidae. The grid-cells in this hotspot barely surpass the average richness threshold, and their richness is mainly due to the contribution of broadly distributed species. CONCLUSIONS The biological characteristics of the helminth parasites of freshwater fish make them excellent indicators of aquatic environment health (Aguilar-Aguilar & Salgado-Maldonado, 2006). Determining helminth hotspots is relevant to this function because it helps in detecting areas with good environmental conditions that have a diversity of intermediate and definitive hosts in population densities sufficient to sustain high parasite species richness. In the present study, we found herein that areas that are both species rich and contain endemic species qualify as hotspots because they contain fish species parasitized by a large number of helminth species, and which live sympatrically with other fish species parasitized by fewer helminth species but ones with limited distribution. The results of the present study suggest that the distribution of richness and endemism in the helminth parasites of freshwater fish in Mexico is congruent with patterns described for other taxa in Mexico and thus reinforces established generalizations. Being aquatic taxa, helminth species can provide valuable data for identification of areas with potential relevance in terms of conservation, and for regionalization of geographical areas. Helminth richness and endemism in the studied regions basically responds to the ichthyological composition of their bodies of water. This study makes analysis of regional biotic distribution possible by establishing an objective way of studying the relationship between richness and endemism. The validity and repeatability of the analysis will depend on its application to other taxa, both aquatic and terrestrial. ACKNOWLEDGEMENTS We thank Juan José Morrone for review of the manuscript and to Othón Alcántara and Hamlet Santa

8 442 R. AGUILAR-AGUILAR ET AL. Anna del Conde for technical assistance. Thanks also due to Miguel Ángel Aguilar Aguilar, Guillermina Cabañas Carranza, Juan Manuel Caspeta Mandujano, Violeta E. González Máynez, Guadalupe Lara Figueroa, Mirza P. Ortega Olivares, Ana Lucía Sereno Uribe, Carlos A. Mendoza Palmero, Norman Mercado Silva, Frantisek Moravec, Itziar Rebollar, Tomás Scholz, Eduardo Soto, Edmundo Díaz, and Raúl Pineda for help in field and laboratory. R.A.A. was supported by a Postdoctoral Fellowship from Dirección General de Asuntos del Personal Académico (DGAPA), UNAM, México. This work was partially supported by project IN to G.S.M. from PAPIIT-UNAM. REFERENCES Aguilar-Aguilar R, Contreras-Medina R, Martínez- Aquino A, Salgado-Maldonado G, González-Zamora A Aplicación del análisis de parsimonia de endemismos (PAE) en los sistemas hidrológicos de México: Un ejemplo con helmintos parásitos de peces dulceacuícolas. In: Llorente J, Morrone JJ, eds. 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