Richness and endemism of helminth parasites offreshwater fishes in Mexico

ROGELIO AGUILAR-AGUILAR1*, GUILLERMO SALGADO-MALDONADO2,RAÚL CONTRERAS-MEDINA1,3 and ANDRÉS MARTÍNEZ-AQUINO2

1Facultad de Ciencias, Departamento de Biología Evolutiva, Apartado Postal 70-399, UniversidadNacional Autónoma de México, CP 04510, México2Instituto de Biología, Universidad Nacional Autónoma de México, Apartado Postal 70-153, CP04510, México3Ciencias 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 todetermine areas of high richness and endemism. Distribution maps were prepared for each taxon and overlaid ontoa map of Mexico divided into 1 ¥ 1 degree grid-cells. Richness was determined by counting recorded helminthspecies in each grid-cell. A corrected weighted endemism index was calculated for each grid-cell, and therelationship 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 theGulf 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 withdistributional patterns described for other freshwater taxa in Mexico. Patterns of richness and/or endemism in thestudied areas can be explained by the ichthyological composition of their bodies of water. The present studyestablishes an objective way of analysing the relationship between richness and endemicity, and suggests thathelminths can make valuable contributions to regionalization of geographical areas and for identification of richand biologically complex areas with potential for conservation of aquatic systems. © 2008 The Linnean Societyof London, Biological Journal of the Linnean Society, 2008, 94, 435–444.

ADDITIONAL KEYWORDS: Acanthocephala – biodiversity – Cestoda – hotspots – Monogenea – Nematoda– Trematoda.

INTRODUCTION

Mexico is located at the intersection of the Neotropi-cal and Nearctic biogeographical regions, and itsbiological diversity and geological history make itan interesting area for biogeographical research(Morrone, 2005). Many regions in Mexico are knownas areas of endemism for different taxa (Arriaga et al.,1997; Morrone, 2005, 2006); however, these studieshave been focused in terrestrial taxa, whereas thedistribution of epicontinental aquatic biodiversity hasreceived limited attention (Huidobro et al., 2006).In an effort to determine the patterns of biodiversity

and their similarity to the distributional patternsdescribed for other taxa in the country, we analysedthe distributional data of the helminth parasites offreshwater fish in Mexico in terms of species richnessand endemism. Both richness and endemism areimportant for biodiversity and constitute an essentialcomponent of the ‘hotspot’ concept (Myers, 1988, 1990;Mittermeier, Myers & Goettsch-Mittermeier, 1999;Contreras-Medina & Luna, 2007).

The known helminth parasite fauna of freshwaterfish in Mexico includes 262 nominal helminth species:164 adult and 98 larvae (Salgado-Maldonado, 2006).This richness is not homogeneously distributedthroughout the country. The south-east is rich inhelminth species (Aguilar-Aguilar, Contreras-Medina& Salgado-Maldonado, 2003), whereas central Mexico*Corresponding author. E-mail: raguilar@ibiologia.unam.mx

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is less so (Salgado-Maldonado et al., 2001b). Somehydrological systems, such as the Papaloapan,Grijalva-Usumacinta, and the Yucatan Peninsula, arericher than others such as the Balsas, Lerma, andPánuco systems (Salgado-Maldonado et al., 2001a, b,2004, 2005a, b). One explanation for this richnessdistribution concerns the basin’s geological ages, mag-nitudes, and ichthyofaunal compositions (Salgado-Maldonado et al., 2005a).

Recent published research has addressed the dis-tribution of the helminth parasites of freshwaterfishes in Mexico based on intuitive considerations(Pérez-Ponce de León, 2003; Salgado-Maldonado,2006) or by applying different formal biogeographicalmethods such as parsimony analysis of endemicity(Aguilar-Aguilar et al., 2003, 2005), panbiogeography(Rosas-Valdez & Pérez-Ponce de León) and numericalapproaches (Vidal-Martínez & Kennedy, 2000; Pérez-Ponce de León & Choudhury, 2005). This researchsuggests certain degree of endemism among helminthparasites in freshwater fish in different hydrologicalbasins in Mexico.

The concept of endemism is essential in historicalbiogeography (Henderson, 1991; Crisp et al., 2001;Linder, 2001a). A taxon is defined as endemic if itsdistribution is restricted to a given territory, regard-less of territory size (Anderson, 1994; Zunino &Zullini, 2003). Although endemism is a relativeconcept, there is a common trend to associate it tosmall areas; an area of endemism is defined as onedelimited by the congruent distribution of at least twospecies with a restricted range (Nelson & Platnick,1981; Morrone & Crisci, 1995; Espinosa, Aguilar &Escalante, 2001; Linder, 2001a). The higher thenumber of species restricted to an area of endemism,the greater its relevance, especially if these taxa areunrelated (Crisp et al., 2001). Areas of endemism arethe standard units of historical biogeography research(Nelson & Platnick, 1981; Humphries & Parenti,1999; Crisp et al., 2001) and allow hypotheses to beproposed with respect to the history of biogeographi-cal units and their biotas (Morrone & Crisci, 1995; DaSilva, De Sousa & Castelleti, 2004). Recognition ofareas of endemism is also important because it allowsdivision of terrestrial space into realms, regions,dominions, provinces, and districts (Contreras-Medina, Morrone & Luna, 2001).

Given that the concept of endemism is linked tospecific areas, identification of areas of endemism isdirectly dependent on the scale and density of thesample (Crisp et al., 2001). Areas of endemism arecommonly proposed intuitively by examining distribu-tion maps for overlapping areas of high concentrationsof species with limited distribution ranges (McAllisteret 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 determiningareas of endemism have been proposed (Morrone,1994; Espinosa et al., 2001; Linder, 2001a; Szumiket al., 2002; for criticism of these methods, see alsoHausdorf, 2002). Some of these methods are based onthe division of an extensive area into quadrats thatallow artificially delimited areas to be analysed with arelatively similar size on a minor scale in comparisonwith other geographical units (Morrone, 1994; Crispet 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 ende-mism by applying parsimony analysis of endemicity(Morrone, 1994). Although calculation of indices ofendemism is an interesting alternative for recognizingthese areas and has been used successfully with plants(Crisp et al., 2001; Linder, 2001b; Luna et al., 2004;Contreras-Medina & Luna, 2007), its application inother groups of organisms is desirable in order to verifytheir accuracy and repeatability. In the present study,the corrected weighted endemism index (CWEI) (Crispet al., 2001; Linder, 2001b) was calculated to identifyareas of endemism in Mexico, mapping, in a grid-cellsystem, the geographical distribution data of adulthelminth parasites of freshwater fishes. The relation ofhigh endemism and high richness of species let us tosuggest hotspots. Additionally, the study represents atest of the utility of CWEI for detection of endemismpatterns based on nonsessile organisms.

MATERIAL AND METHODS

We chose distribution records for 152 adult helminthparasite taxa from freshwater fish in Mexico (trema-todes, monogeneans, cestodes, acanthocephalans, andnematodes) from the database of Salgado-Maldonado(2006), as well as from our own research data (thecomplete list is available upon request). All recordswere taxonomically validated to correct erroneousidentifications, synonymies and other taxonomic prob-lems (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 acollected specimen, that is, all identifications arelinked to voucher specimens. Helminth parasiterecords from fish in aquaculture ponds or farms wereexcluded from the analysis because they do notrepresent natural distribution (López-Jiménez, 2001;Flores-Crespo & Flores-Crespo, 2003) but, given thatour interest is describing richness, we included intro-duced helminth species in all analyses (Jiménez-

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García, Vidal-Martínez & López-Jiménez, 2001;Salgado-Maldonado & Pineda-López, 2003; Salgado-Maldonado, 2006).

Distribution maps for each taxon were preparedusing GIS ArcView 3.2 (ESRI, 1999). Each collectionpoint was superimposed on a map of Mexico overlaidwith a 1 ¥ 1 degree grid. The grid method allows thedelimitation of smaller areas within hydrologicalbasins, which more clearly defines study regionlimits. Using this method, each basin can be subdi-vided into smaller analytical units of relatively equalsize, which, to a certain degree, reflect the distribu-tion of real fish and parasite species. It also enablesobjective joining of the parasitological faunas ofnearby bodies of water, thus preventing the excessivefragmentation that would lead to using each samplesite as an analytical unit. To simplify the distributiondata, we transformed them into presence/absence ofeach helminth species in each grid cell. A species wastreated as present in a cell when it had been recordedjust once or many times parasitizing a fish caught inany body of water within that cell; its absence indi-cated the lack of a record for a helminth species in acell. We determined richness by counting the helm-inth species recorded in each grid square.

The endemism analysis is based on CWEI (Crispet al., 2001; Linder, 2001b), which in turn is a modi-fication of the weighted endemism index (WEI) usedby cited authors. To calculate the WEI, each species isweighted for the inverse of its range such that eachendemic species in a grid-cell has a maximum ‘weight’of 1; if a species is present in five grid-cells, it has aweight of 0.20 and one in 20 grid-cells has a weight of0.05. To calculate the value of each grid-cell, theweight values for all the species in that grid-cell areadded so that squares with a high number ofrestricted range species have a higher score thangrid-cells with fewer restricted range species (Linder,2001b). To correct for the correlation with speciesrichness, and to generate the CWEI, the ‘weighted’endemism is divided by the total number of species ina grid-cell (Crisp et al., 2001).

We evaluated the relationship between richnessand endemism with an Olmstead–Tukey corner test ofassociation (Steel & Torrie, 1980). This produces agraph in which each grid-cell is placed in one of fourquadrants when mean richness and CWEI values areplotted. Grid-cells in the quadrat of high richness andendemism values are identified as hotspots, althoughthis does not take into consideration threats tospecies at these locations (Myers, 1988, 1990).

RESULTS AND DISCUSSION

The 152 adult helminth species from freshwaterfishes analysed in the present study were distributed

in 66 grid-cells, which included at least one record ofan adult helminth species (Fig. 1). The two helminthspecies with the highest number of records were thecestode Bothriocephalus acheilognathi Yamaguti,1934 (25 grid-cells) and the trematode Crassicutiscichlasomae Manter, 1936 (24 grid-cells), whereas 56taxa had records in just one grid-cell. The MexicanNearctic, north of the Transmexican Volcanic Belt(19–20°N), had many empty squares; all the cells inthis northern area with helminth records had a rich-ness of less than ten species.

Richness in the 66 grid squares with records was inthe range 1–47 species per grid-cell (mean = 9.1species). Just one helminth species was recorded inten grid-cells. The two areas with the highest helm-inth species richness are in the south-east, near theGulf of Mexico, and in western Mexico. The firstincludes the Papaloapan river basin, Los Tuxtlas inVeracruz (the highest species/grid-cell with 47species), and different sites in the states of Tabascoand north-east Chiapas. The second is located in theAyuquila river, within the Sierra de Manantlán Bio-sphere Reserve in the state of Jalisco (Fig. 1).

The endemism analysis was performed with the 56grid-cells containing at least two helminth species.The resulting CWEI values were in the range 0.05–1.0 (mean value of 0.25) and 25 grid-cells had highendemism values (i.e. CWEI � 0.25) (Fig. 2). Of these25, 15 grid-cells had high CWEI values but low rich-ness. Two of these grid-cells were considered areas ofendemism due to the species found in them, althoughthey had low richness: El Toboso and AbrahamGonzález springs, state of Durango (grid-cell 6); andChicnahuapan lake along with different bodies ofwater in the upper Lerma river basin, state of México(grid-cell 34) (Fig. 3).

Eight grid-cells with high richness and endemismvalues were identified (Fig. 2). They can be groupedinto five hotspots: (1) Los Tuxtlas, in Veracruz, andthe Papaloapan river basin; (2) lower reaches ofGrijalva-Usumacinta hydrological basin, at the Gulfof Mexico coastal plain in Tabasco and the north-eastof Chiapas; (3) central Yucatan Peninsula; (4) theSierra de Manantlán Biosphere Reserve; and (5)Pátzcuaro Lake, in the state of Michoacán and the LaLaja river, in the state of Guanajuato, both in theLerma river basin (Fig. 3).

RICHNESS AND ENDEMISM

South-eastern Mexico has a high richness of helminthparasite species in freshwater fishes. This area prob-ably runs continuously from the Papaloapan riverbasin (including Los Tuxtlas, the Tabasco coastalplain and north-east Chiapas) to the Yucatan Penin-sula (Fig. 1). Within this area, the Coatzacoalcos

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river, in the state of Veracruz, appears empty becauseit has not been sampled. Given that this river’s ich-thyological composition is similar to that of the neigh-bouring Papaloapan and Grijalva-Usumacinta basins,it is likely that it is equally rich in helminth parasitespecies. A second empty space on the regional mapresults from the lack of surface water on the YucatanPeninsula, except for sinkholes.

The rich Sierra de Manantlán area in westernMexico is apparently isolated from other localities incentral Mexico. Although grouping this site with theothers in central Mexico (all within the Lerma riverbasin) creates a large area of relatively high richness,no other sites in the area have nearly as manyrecorded helminth species (Fig. 1).

The CWEI can be compromised by insufficient orunbalanced samples (Crisp et al., 2001). Thirteen ofthe grid-cells with insufficient samples had low rich-ness and high endemism values, and the high CWEIvalues in some of these squares can be explained bythe accidental presence of a single, broadly distrib-

Figure 1. Richness of helminth parasites of freshwater fishes in Mexico.

Figure 2. Olmstead–Tukey corner test of associationbetween richness and corrected weighted endemism index(CWEI). Empty squares (�) identify two grid-cellswhere richness = 1; these were not considered as areas ofendemism.

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uted but infrequent helminth species. For example,high CWEI values for two of these grid-cells were dueto records for Crepidostomum cornutum (Osborn,1903) and Rhabdochona cascadilla Wingdor, 1918(grid-cell 1), and Neocucullanus neocucullanusTravassos, Artigas & Pereira, 1928 and Rhabdochonaacuminata (Molin, 1860) (grid-cell 66) in a single hostspecies. These four helminth species are widely dis-tributed in North and South America, respectivelybut, in Mexico they have only been collected ata single site (Valles-Ríos & Ruiz-Campos, 1997;Caspeta-Mandujano et al., 2005). The higher values ofendemism for other cells are the result of recordsbased on studies that do not include all the helminthsparasitizing a given host, or that do not provide acomplete inventory of the helminth species from acertain site (e.g. taxonomic studies such as newspecies descriptions). For example, the high CWEIvalue in grid-cell 53 is due to records for the two newspecies Rhabdochona salgadoi Caspeta-Mandujano &Moravec (2000) and Spinitectus humbertoi Caspeta-

Mandujano & Moravec (2000), but the original studydid not document other helminth species in thestudied hosts from that site (Caspeta-Mandujano &Moravec, 2000). An additional factor that contributingto increase the CWEI value is the record of somehelminth taxa found in fresh waters but parasitizingbrackish fishes. These hosts and parasite taxa havebeen recorded in the same localities where typicalfreshwater species has been collected together withbrackish species and, for this reason, were consideredas freshwater taxa by Salgado-Maldonado (2006).For example, the grid-cell 52 contains records for acoastal lagoon, where strictly freshwater fish were notintensively examined and therefore data on them arescarce. In this grid-cell in particular, the highCWEI value is associated with the record of theacanthocephalan Pseudoleptorhynchoides lamotheiSalgado-Maldonado, 1977 (Salgado-Maldonado,2006). Another case that represents difficulty tostrictly delimit fresh and brackish environment is thetrematode Pseudoacanthostomum panamense, which

Figure 3. Hostspots and areas of endemism for helminth parasites of freshwater fishes in Mexico.

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contributes with a relatively high value of CWEI forthose three grid-cells in which occurs. More completesamples diminish the effect of these factors on theCWEI (Crisp et al., 2001).

Grid-cell 6 (containing El Toboso and AbrahamGonzález springs, Durango) and grid-cell 34 (contain-ing Chicnahuapan lake, state of México, and otherbodies of water in the upper Lerma river basin) bothhad low richness but high CWEI values, which indi-cates areas of endemism. By contrast to the abovediscussed grid-cells 52 and 53, all the fish species inthese waters have been examined, meaning that hel-minth richness in them will probably not increasesubstantially with new samples. The high endemismvalue in these squares is associated with fourhelminth species of restricted distribution: Allocre-adium mexicanum Osorio-Sarabia, Pérez-Ponce deLeón & Salgado-Maldonado, 1986 and Margotremabravoae Lamothe-Argumedo, 1970 in grid-cell 34;and these two species plus Margotrema guillerminaePérez-Ponce de León, 2001 and Atactorhynchusduranguensis Salgado-Maldonado, Aguilar-Aguilar &Cabañas-Carranza, 2005 in grid-cell 6. These datasuggest that some bodies of water can be centres ofendemicity without having a high richness.

The analyses identified five hotspots for helminthparasites of freshwater fish in Mexico: (1) Papaloapanriver basin; (2) Grijalva-Usumacinta basin; (3) theYucatan Peninsula; (4) Lerma river basin; and (5) theSierra de Manantlán Biosphere Reserve. All five havepreviously been indicated as areas of endemism fordifferent taxa; in fact, the Papaloapan, Grijalva-Usumacinta and Yucatan Peninsula hotspots fallwithin the Mesoamerican hotspot (Mittermeier et al.,1999). The most significant of the five in terms ofrichness and endemism is the Papaloapan river basinfrom its upper third to its drainage into AlvaradoLagoon in Veracruz, including the Catemaco lake andother bodies of water in the Los Tuxtlas region. Theentire region is already considered a centre of ende-mism for other taxa such as freshwater fish andcrustaceans (Miller, 1986; Álvarez & Villalobos, 1997;Rojas, Álvarez & Villalobos, 1997; Espinosa et al.,1998). The Grijalva-Usumacinta Basin near theTabasco coastal plain and in north-east Chiapas hasbeen reported as an area of endemism for freshwaterfish (Miller, 1966). The Sierra de Manantlán has alsobeen considered a centre of endemism for many fresh-water and terrestrial taxa (Arriaga et al., 2000).The Lerma river basin and Yucatan Peninsula havea comparatively lower richness than the first threehotspots but remain important for the endemicity oftheir helminth species. Indeed, the Pátzcuaro lakeand other bodies of water in the Lerma river basin, aswell as the Usumacinta river and the sinkholes of theYucatan Peninsula, are considered centres of ende-

mism for helminths (Moravec et al., 1995; Scholzet al., 1996; Salgado-Maldonado et al., 2001b) andfreshwater fishes (Espinosa et al., 1998). In otherwords, the data for helminth parasites of freshwaterfish tends to further support the patterns describedfor other taxa in Mexico.

A number of factors acting in conjunction can leadto restriction of taxa distribution and therefore gen-erate an area of endemism. The extent of a taxon’srange can also be restricted by a history of vicariancefollowed by speciation in isolation (Nelson & Platnick,1981; Brown & Lomolino, 1998; Humphries &Parenti, 1999; Crisp et al., 2001). Hosts comprise theparasites’ immediate environment and therefore cor-respond to an ecological factor that may limit theestablishment of a given helminth taxon in a body ofwater. The endemism of fishes in Mexico is seen as aresult of vicariance processes caused mainly by frag-mentation of bodies of water and a consequently highspeciation rate (Espinosa et al., 1998; Miller, 1986).

HELMINTH TAXA

The high richness and endemism of the hotspots thathave been identified in the present study can beexplained by helminth species specificity to host fami-lies. This result show a strong correspondence withthe first prediction proposed by Pérez-Ponce de León& Choudhury (2005), in relation to distributionalpatterns of host–parasite associations in freshwaterfishes of Mexico, which suggests that parasite faunais largely circumscribed by higher levels of monophyl-etic host taxa, especially to the level of fish family. Ashelminth 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 endemismof the hotspots by the ichthyological composition intheir waters and the helminths associated with thefish families in them. For example, cichlids providerichness to grid-cells because they have very richhelminth communities, but they do not contributesignificantly to endemism due to their broad distri-bution. Other fish families, in contrast, contributesubstantially to endemism and little to richness.Atherinopsidae and Goodeidae, for example, are para-sitized by helminth species that are highly specific tothem and of limited distribution, but their helminthcommunities are comparatively poor (Choudhury &Dick, 2000; Salgado-Maldonado, 2006).

The south-eastern Mexico hotspots (Papaloapan,Grijalva-Usumacinta, and Yucatan Peninsula) existin response to the high degree of endemicity of thehelminth parasites in the families Synbranchidae,Heptapteridae, Characidae, Lepisosteidae, Poecili-idae, and Eleotridae. More specifically, the high value

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of CWEI in these hotspots is mainly due to thefollowing limited-distribution species: Monticelliaophisterni Scholz, de Chambrier & Salgado-Maldonado, 2001, Philometra ophisterni Moravec,Salgado-Maldonado & Aguilar-Aguilar, 2002,Pseudocapillaria ophisterni Moravec, Salgado-Maldonado & Jiménez-García, 2000 and Gibsonemaophisterni (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 Para-capillaria rhamdiae Moravec, González-Solís, Vargas-Vázquez, 1995 in the Heptapteridae; Genarchellaastyanacthys (Watson, 1976) and Proteocephalusbrooksi García-Prieto, Rodríguez & Pérez-Ponce deLeón, 1996 in the Characidae; Cystoopsis atractosteiMoravec & Salgado-Maldonado, 2003 and Perezitremabychowskyi (Caballero y Caballero, 1975) in theLepisosteidae; Spinitectus mexicanus Caspeta-Mandujano, Moravec & Salgado-Maldonado, 2000 inthe Poeciliidae; Guavinella tropica Mendoza-Franco,Scholz & Cabañas-Carranza, 2003 in the Eleotridae;and Spinitectus agonostomi Moravec & Barus, 1971 inthe Mugilidae. With their high helminth speciesdiversity, the Cichlidae contribute both richness andendemism to these hotspots through these familyspecific species: Sciadicleithrum bravohollisaeKritsky, Vidal-Martínez & Rodríguez-Canul, 1994,Crassicutis cichlasomae, Oligogonotylus manteriWatson, 1976, Genarchella isabellae (Lamothe-Argumedo, 1977), Neoechinorhynchus golvaniSalgado-Maldonado, 1978, Rhabdochona kidderiPearse, 1936, and Mexiconema cichlasomae Moravec,Vidal-Martínez & Salgado-Maldonado, 1992 (Salgado-Maldonado, 2006).

Endemism in the Sierra de Manantlán hotspot inwestern Mexico is due to the helminths Paracapil-laroides agonostomi Moravec, Salgado-Maldonado &Caspeta-Mandujano, 1999 in the Mugilidae; Proteo-cephalus 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 theEleotridae; and Rhabdochona guerreroensis Caspeta-Mandujano, Aguilar-Aguilar & Salgado-Maldonado,2002 in the Gobiidae. These fish families have richhelminth communities, which contribute considerablerichness to this hotspot. Its richness is furtherenhanced by other more broadly distributed helminthspecies, such as Magnivitellinum simplex Kloss, 1966,Rhabdochona kidderi and Capillaria cyprinodonticolaHuffman & Bullock, 1973, as well as the introducedspecies Bothriocephalus acheilognathi and Cychlid-ogyrus sclerosus Paperna & Thurston, 1969. The

analysis of this hotspot could be further modified withadditional sampling, because the above-mentionedhelminth taxa are associated with secondary widelydistributed fish families.

The hotspot in central Mexico qualifies as an areaof endemism because of the helminth species: Mar-gotrema bravoae, M. guillerminae, Salsuginus sp. andGyrodactylus sp. in the Goodeidae; A. mexicanum andSpinitectus osorioi Choudhury & Pérez-Ponce deLeón, 2001 in the Atherinopsidae; and the monoge-nean Octomacrum mexicanum Lamothe-Argumedo,1981 in the Cyprinidae. The grid-cells in this hotspotbarely surpass the average richness threshold, andtheir richness is mainly due to the contribution ofbroadly distributed species.

CONCLUSIONS

The biological characteristics of the helminth para-sites of freshwater fish make them excellent indica-tors of aquatic environment health (Aguilar-Aguilar& Salgado-Maldonado, 2006). Determining helminthhotspots is relevant to this function because it helpsin detecting areas with good environmental condi-tions that have a diversity of intermediate and defini-tive hosts in population densities sufficient to sustainhigh parasite species richness. In the present study,we found herein that areas that are both species richand contain endemic species qualify as hotspotsbecause they contain fish species parasitized by alarge number of helminth species, and which livesympatrically with other fish species parasitized byfewer helminth species but ones with limited distri-bution.

The results of the present study suggest that thedistribution of richness and endemism in the helm-inth parasites of freshwater fish in Mexico is congru-ent with patterns described for other taxa in Mexicoand thus reinforces established generalizations.Being aquatic taxa, helminth species can providevaluable data for identification of areas with potentialrelevance in terms of conservation, and for regional-ization of geographical areas. Helminth richness andendemism in the studied regions basically responds tothe ichthyological composition of their bodies of water.This study makes analysis of regional biotic distribu-tion possible by establishing an objective way ofstudying the relationship between richness and ende-mism. The validity and repeatability of the analysiswill depend on its application to other taxa, bothaquatic and terrestrial.

ACKNOWLEDGEMENTS

We thank Juan José Morrone for review of the manu-script and to Othón Alcántara and Hamlet Santa

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Anna del Conde for technical assistance. Thanks alsodue to Miguel Ángel Aguilar Aguilar, GuillerminaCabañas Carranza, Juan Manuel Caspeta Mandu-jano, Violeta E. González Máynez, Guadalupe LaraFigueroa, Mirza P. Ortega Olivares, Ana Lucía SerenoUribe, Carlos A. Mendoza Palmero, Norman MercadoSilva, Frantisek Moravec, Itziar Rebollar, TomásScholz, Eduardo Soto, Edmundo Díaz, and RaúlPineda for help in field and laboratory. R.A.A. wassupported by a Postdoctoral Fellowship from Direc-ción General de Asuntos del Personal Académico(DGAPA), UNAM, México. This work was partiallysupported by project IN229807 to G.S.M. fromPAPIIT-UNAM.

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