Journal of Fish Biology (2000) 57, 303–325doi:10.1006/jfbi.2000.1325, available online at http://www.idealibrary.com on

Helminth communities of native and introduced fishes inLake Patzcuaro, Michoacan, Mexico

G. P-P L*, L. G-P, V. L-R A. C†

Laboratorio de Helmintologıa, Instituto de Biologıa, Universidad Nacional Autonoma deMexico, Ap. Postal 70-154, C.P. 04510, Mexico D.F., Mexico

(Received 21 May 1999, Accepted 17 March 2000)

In Lake Patzcuaro in the Mesa Central of Mexico, a total of 19 species of helminths was foundin 598 fishes and comprised five digeneans, two monogeneans, four cestodes, oneacanthocephalan and seven nematodes, of which ten species were represented by larval orimmature states. The richest and most diverse helminth communities were found in the nativecarnivorous goodeid Alloophorus robustus. In general, the helminth communities in thedifferent fish species were not particularly species rich and the parasite assemblages werenumerically dominated by larvae of the bird trematode, Posthodiplostomum minimum. Patternsof helminth community richness and diversity were similar to those previously observed innorth-temperate freshwater fishes. Most enteric helminths occurred with low abundance andonly a small proportion of the gut helminth communities was numerically dominated by anyone species. Helminths dominating their enteric communities showed some level of hostspecificity. Helminth communities in carnivorous fish species were generally richer than thosein herbivores and detritivores, with the exception of the predominantly herbivorous Goodeaatripinnis. The helminth fauna of introduced fishes, Cyprinus carpio, Micropterus salmoides andOreochromis niloticus, consisted of either few or no host-specific adult helminth(s) translocatedfrom their original geographical areas and by larval stages of helminths of piscivorous birds.Based on the geological history of the area and the biogeography of the endemic fish fauna, itis hypothesized that host-switching and relationships with the nearctic fauna have beenfundamental in determining the helminth fauna of the endemic fish hosts.

� 2000 The Fisheries Society of the British Isles

Key words: helminths; communities; diversity; freshwater fishes; Patzcuaro; Mexico.

INTRODUCTION

Extensive studies on the parasites of freshwater fishes of the north temperateregions (mainly from the former Soviet Union) allowed Dogiel and co-workers(Dogiel et al., 1961; Dogiel, 1964) to conclude that the nature of the waterbody,diet, biogeography and history act synergistically to produce parasite faunaswith different characteristics in different hosts (see Fig. 203 of Dogiel, 1964).Studies on introduced fishes also led to the generalization (Dogiel et al., 1961)that translocated hosts generally suffer an impoverishment of their parasitefauna in their new environments. More recent years have seen an elaboration ofthese general principles. Kennedy et al. (1986) generalized that helminthassemblages in fish are generally depauperate and isolationist compared with

*Author to whom correspondence should be addressed. email: ppdleon@servidor.unam.mx†Present address: USGS-National Wildlife Health Center, 6006 Schroeder Road, Madison, WI 53711,

U.S.A.

303

0022–1112/00/080303+23 $35.00/0 � 2000 The Fisheries Society of the British Isles

304 . - .

those in other, mainly endothermic, vertebrates. Ectothermy, low vagility andthe structural simplicity of the gut were cited as possible reasons among othersfor these characteristics. Kennedy (1990) and Hartvigsen & Kennedy (1993)also characterized helminth assemblages in freshwater fishes as beingdepauperate and essentially stochastic in nature. It has been suggested also thatmore primitive (presumably meaning basal) fishes and those belonging totropical latitudes would have richer helminth assemblages (Kennedy, 1995;Salgado-Maldonado & Kennedy, 1997). Some of these generalizations havebeen premature (Sousa, 1994; Kennedy, 1995; Choudhury & Dick, 1998).

Until recently, most investigations into the community diversity of parasitesof freshwater fishes have been confined to the north temperate regions.Studies from other more tropical regions have focused generally on componentcommunities and have been used rarely to test some of the generalizationsregarding freshwater fish parasite communities, but that is changing(Kennedy, 1995; Vidal, 1995; Espinosa-Huerta et al., 1996; Rojas et al., 1997;Salgado-Maldonado & Kennedy, 1997).

Lake Patzcuaro in the Mesa Central of Mexico and its fish assemblage providean ideal opportunity to address aspects of parasite community structure from amore tropical freshwater system, as well as to address some aspects of thebiogeography of helminth assemblages. Lake Patzcuaro is biogeographicallyimportant because of its position along the neovolcanic axis; this represents thetransitional zone between the Nearctic and Neotropical zones, and determinesthe existence of a characteristic fauna with high levels of endemism. Further-more, the fish fauna of this lake includes also four established exotic (introduced)species [Micropterus salmoides Lacepede, Cyprinus carpio L., Oreochromisniloticus L. and Tilapia rendalli (Boulenger)] from three continents. LakePatzcuaro has been the site of a long-term study on fish parasites and over 3000fish have been examined from this lake between 1984 and 1998. Several studieshave investigated the helminth fauna of particular fish species in this lake(Osorio-Sarabia et al., 1986; Peresbarbosa et al., 1994; Perez-Ponce de Leonet al., 1994, 1996; Mendoza-Garfias et al., 1996) but few have studied thehelminth community structure in a host species in any detail (Espinosa-Huertaet al., 1996; Rojas et al., 1997). In this study, the helminth communities of theten common species of fishes in Lake Patzcuaro are described (of a total of 14present, some of which may be extinct or not valid), sampled concurrently, andthe results are discussed in relation to generalizations regarding diet, faunalexchange, translocation and biogeography in a tropical lake system.

MATERIALS AND METHODS

STUDY SITELake Patzcuaro (Fig. 1) is a tropical high-altitude waterbody located at 2035 m a.s.l. in

the southern portion of the Mexican Altiplano, in the State of Michoacan, and liesbetween 19�32�–19�42� N and 101�32�–101�43� W. The drainage basin is 929 km2 with atotal lake surface area of 130 km2 and a mean depth of 4·97 m (Chacon, 1993;Bernal-Brooks, 1998). Spatial and temporal variation in both physical and biologicalconditions make it difficult to assign a specific trophic state to Lake Patzcuaro, as a resultit has been considered eutrophic (Berlanga et al., 1997; Bernal-Brooks, 1998),mesotrophic (Rosas et al., 1993), or even within a range from hypereutrophic to

305

oligomesotrophic in different areas (Chacon, 1993). The fish composition of the lakecomprises 14 species of the following families, Goodeidae (4 spp.), Atherinidae (5 spp.),Cyprinidae (2 spp.), Centrarchidae (1 sp.) and Cichlidae (2 spp.).

SAMPLINGIn May and October 1993, 598 fish representing ten species, with sample sizes varying

between 40 and 70 fish species�1 were collected using gill nets, seines, and spoon nets(Table I). Fish were kept on ice and examined within 4 h of capture. Organs examinedincluded gills, eyes, brain, muscle, mesentery, liver, spleen, heart, gonads and thegastrointestinal tract. Examinations were made using a dissecting microscope. Allhelminths were counted in situ, recovered from the organs, and processed according toprocedures described in Mendoza-Garfias et al. (1996). The fork length was measured tothe nearest mm using a measuring board.

ANALYSISPrevalence, intensity of infection and abundance were calculated and used as defined in

Margolis et al. (1982). Shannon–Wiener’s index (H�) and Brillouin’s index (H) werecalculated as measures of community diversity (Peet, 1974; Pielou, 1975; Magurran,1988) and the terms diversity and diverse are used to reflect the values of these diversityindices. Numeric dominance, as used here, was determined using the Berger–Parkerdominance index (Magurran, 1988). Species richness (s) refers to the number of species.Infracommunity refers to the community of parasite species in a host individual,component community refers to the assemblage of parasites recovered from a sample ofa host species while compound community refers to the assemblage of parasites in allhost species in a locality (Sousa, 1994). The community characteristics and diversity ofgut helminth communities have been calculated separately because these provide a basisfor comparison of parasite community patterns as they relate to trophic interactions ofthe hosts and because parasite assemblages in the gut are due to a common process(ingestion). Correlations between size (length) of fish and the parasite burden (totalnumber of parasites in an individual fish) and infracommunity parasite species richnesswere calculated using Spearman’s rank correlation and Pearson’s correlation coefficient.Jaccard’s similarity index (Ji) was used to assess qualitative similarity among com-ponent communities of the different hosts (Southwood, 1978) and calculated as

Michoacan StatePatzcuaro

N

Tropic of Cancer Mexico

Pacific Ocean

Gulfof

Mexico

Guatemala

United States

Lake Patzcuaro

F. 1. Map of Mexico showing the localization of Lake Patzcuaro in the state of Michoacan.

306 . - .

100c (a+b)�1�c, where a=the number of parasite species in one sample, b=number ofparasite species in the other sample and c=number of species common to both samples.Host specificity, as used here, refers to the phenomenon of a parasite being specific, notnecessarily to the host species, but, as is more commonly observed in nature, to highertaxa of presumed monophyletic host groups (genera, family etc.).

RESULTS

A total of 19 species of helminths (five digeneans, two monogeneans, fourcestodes, one acanthocephalan and seven nematodes) was found in the 598 fishescollected in 1993 (Table II). Nine of the 19 species were found as adult stages,infecting the digestive tract (Allocreadium mexicanum, Crepidostomum cornutum,Bothriocephalus acheilognathi, Capillaria patzcuarensis, Rhabdochona lichtenfelsi,Spinitectus sp.), the gills (Ancyrocephalidae sp. gen., Octomacrum mexicanum),or the body cavity (Philometridae sp. gen.,) of their hosts (Table II). Of these,A. mexicanum and Spinitectus sp. were found only in the atherinids (Chirostomaspp.), Crepidostomum cornutum in M. salmoides only, O. mexicanum on thecyprinid A. lacustris and R. lichtenfelsi in the goodeids only (Tables III and IV).Fishes in Lake Patzcuaro are potential intermediate hosts for at least sevenspecies of helminths whose life cycles are completed when fishes are eaten, mostlyby fish-eating birds (hosts for Clinostomum complanatum, Posthodiplostomumminimum, Ligula intestinalis, Cyclophyllidea sp. gen., Polymorphous brevis,Contracaecum sp., and Eustrongylides sp.), or by other vertebrates such asreptiles (garter snakes for Ochetosoma sp., and turtles for Spiroxys sp.),amphibians, or even other fishes (hosts for Proteocephalidea sp. gen.). Five ofthese species, all of them as larval stages (Posthodiplostomum minimummetacercariae, Proteocephalidea sp. gen. plerocercoids, Polymorphus brevis

T I. Fishes examined from lake Patzcuaro: sample sizes, lengths and habits

Host Length (mm)X�.. (range) n Sex DietM F J*

AtherinidaeChirostoma attenuatum 78·8�9·2 (60–100) 60 26 34 InvertebratesChirostoma estor 192·2�28·3 (148–255) 64 26 38 Invertebrates+fishChirostoma grandocule 83 �10·8 (61–110) 70 26 44 Invertebrates

GoodeidaeAlloophorus robustus 100·7�13·5 (62–132) 67 41 26 Insects+fishGoodea atripinnis 90·3�13·2 (69–116) 59 35 24 Plant matter, algaeAllotoca diazi 71·1�7·6 (60–90) 40 15 25 Invertebrates

CyprinidaeAlgansea lacustris 124·1�45·4 (62–247) 63 28 16 9 Invertebrates, plant matterCyprinus carpio 176 �46·4 (100–300) 48 26 8 14 Plant matter, invertebrates

CentrarchidaeMicropterus salmoides 164·24�25·5 (125–250) 66 39 27 Fish, invertebrates

CichlidaeOreochromis niloticus 122·93�31·7 (67–190) 61 11 18 32 Detritus, invertebrates

*M, Male; F, female; J, juvenile.

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310 . - .

cystacanths, and the nematodes Eustrongylides sp. and Spiroxys sp.) were themost widely distributed parasites in the fish species examined (Tables III and IV).

Alloophorus robustus (Bean) possessed, on average, the richest helminthcommunities (Table V) while only one helminth species was found in O. niloticus,making its helminth community the poorest of all fish species examined(Table VI). At the overall infracommunity level (Tables V and VI), meanBrillouin’s values ranged from 0·53 in A. robustus to 0·005 in C. grandocule(Steindachner) (the value for O. niloticus was not calculated).Posthodiplostomum minimum dominated the infracommunities of six of the tenfish species in this study and the percentage of communities dominated by thisone species ranged from 48·5 to 88·3% (Table V). The richest gut helminthcommunities, on average, were found also in A. robustus. In most cases, the guthelminth communities were dominated by species showing some level of hostspecificity but only a very small proportion of the gut infracommunities wasdominated by a single species (Tables VII and VIII). There was no significantcorrelation between helminth burden or helminth infracommunity richness andsize of hosts individuals for any of the fish species examined.

T IV. Mean abundance, range and prevalence of helminth parasites of introducedfishes of Lake Patzcuaro

Host speciesCyprinus

carpioMicropterus

salmoidesOreochromis

niloticus

Helminth species*Digenea

Crepidostomum cornutum — 7·2�25·5 —(1–191) 25·7

Posthodiplostomum minimum — 0·02�0·12 —(1) 1·5

MonogeneaAncyrocephalidae sp. gen. — 97·1�159 —

(2–662) 62·1Cestoidea

Bothriocephalus acheilognathi 0·04�0·2 — —(1) 4·2

Proteocephalidea sp. gen. 0·02�0·14 0·06�0·3 —(1) 2·1 (1–2) 4·5

AcanthocephalaPolymorphus brevis — 0·11�0·47 —

(1–3) 6·1Nematoda

Capillaria patzcuarensis 0·02�0·14 — —(1) 2·1

Eustrongylides sp. (1) 0·06�0·43 0·05�0·21 —(3) 2·1 (1) 4·5

Spiroxys sp. (1) 0·02�0·12 0·06�0·39(1) 1·5 (1–3) 3·28

*Values are mean�.. followed by range within parentheses and prevalence (in %).

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Calculation of Jaccard’s similarity index values indicate that the atherinidsC. attenuatum Meek and C. estor Jordan showed high levels of similarity (63%)and the goodeids, A. robustus, Goodea atripinnis Jordan and Allotoca diazi Meekalso possessed assemblages with relatively high levels of similarity between oneanother (50%–60%). Similarity values between helminth communities ingoodeids and those of other fish species were lower (11·1–40%) with theexception of M. salmoides (Ji=40–50%). Low levels of similarity characterize thecomparison between helminth communities of O. niloticus and C. grandocule andthose of other fish species in the lake (Table IX).

DISCUSSION

SPECIES COMPOSITIONThe number of helminth species (19) recovered represents 86% of the total

number of species of helminths (22) reported in fishes of Lake Patzcuaro to date(Perez-Ponce de Leon et al., 1996). Metazoan parasite species missing from thesamples, but previously recorded from the area, include the ectoparasitic leechMyzobdella patzcuarensis (it often detaches and is usually lost during the captureand storage of hosts on ice), and three digeneans, the metacercariae ofDiplostomum (Tylodelphys) sp., and two adult forms, a microphallid and awallinine (possibly a species of Microphallus and Margotrema respectively).Diplostomum sp. requires a fish-eating bird to complete its life cycle, andapparently its presence in the lake is uncommon (Osorio-Sarabia et al., 1986;Espinosa-Huerta et al., 1996). The two adult trematodes represent occasionalfindings, with only a few specimens collected from the intestine of A. robustus in1994 (unpubl. obs.). To date, these two heminths have not been identified tospecies because of very few, poorly preserved, specimens. In general, thehelminth fauna of each host species corresponds, in taxonomic composition andin general prevalences and abundances of infection, to that described in previoussurveys [Osorio-Sarabia et al., 1986 for C. estor; Perez-Ponce de Leon et al.,

T VI. Characteristics of the helminth infracommunities in introduced fishes of LakePatzcuaro

Cyrpinuscarpio

Micropterussalmoides

Oreochromisniloticus

Mean S 0·1�0·31 (0–1) 1·06�0·9 (0–3) 0·032�0·18 (0–1)Mean helminth burden 0·15�0·5 (0–3) 111·3�186·7 (0–663) 0·06�0·4 (0–3)Mean H� — 0·14�0·29 (0–1·5) —Mean H� (E) — 0·13�0·26 (0–0·99) —Mean H — 0·12�0·24 (0–0·94) —Mean H (E) — 0·13�0·26 (0–1) —Dominant species B. acheilognathi Ancyrocephalidae Spiroxys sp.% communities dominated 4·1 13·6 3·3

Mean S, Mean species richness; H�, Shannon–Wiener index; H, Brillouins index; H�E, evenness ofShannon–Wiener’s index; HE, evenness of Brillouin’s index.

Values are mean�.. followed by range in parentheses.

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314 . - .

1994 for C. attenuatum; Peresbarbosa et al., 1994 and Rojas et al., 1997 forthree species of goodeids—A. diazi, A. robustus and G. atripinnis; andMendoza-Garfias et al., 1996 for Algansea lacustris (Steindachner)]. This alsoindicates some temporal consistency in the parasite assemblages. Further workon the helminths of Lake Patzcuaro has revealed that some species weremisidentified and some, in fact, represent new species. These include the typicalbass trematode, C. cornutum, previously reported as C. cooperi, theacanthocephalan Polymorphus brevis, previously identified as Arhythmorhynchus

T VIII. Characteristics of the enteric helminth infracommunities in introduced fishesof Lake Patzcuaro

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niloticus

Mean S 0·08�0·28 0·32�0·5 0·03�0·18Range 0–1 0–2 0–1Mean helminth burden 0·08�0·28 7·24�25·5 0·06�0·4Range 0–1 0–191 0–3Mean H� — 0·01�0·11 —Range 0–0·97Mean H� (E) — 0·01�0·11 —Range 0–0·97Mean H —0·008�0·06 —Range 0–0·53Mean H (E) — 0·01�0·12 —Range 0–1Dominant species B. acheilognathi C. cornutum Spiroxys sp.% communities dominated 4·2 1·5 3·3

Mean S, Mean species richness; H�, Shannon–Wiener index; H, Brillouins index; H�E, evenness ofShannon–Wiener’s index; HE, evenness of Brillouin’s index.

T IX. Jaccard’s Similarity Index values for total helminth assemblages in LakePatzcuaro fishes

Fish species C.e. C.g. A.l. A.r. G.a. A.d. C.c. M.s. O.n.

Chirostoma attenuatum (C.a) 63·6 20 30·8 38·5 38·5 41·7 27·3 41·7 10C. estor (C.e.) 25 36·7 45·4 33·3 25 50 36·4 12·5C. grandocule (C.g.) 12·5 11·1 11·1 12·5 0 12·5 0Algansea lacustris (A.l.) 50 36·4 40 22·2 40 14·3Alloophorus robustus (A.r.) 60 54·5 33·3 50 25Goodea atripinnis (G.a.) 50 20 50 12·5Allotoca diazi (A.d.) 10 27·3 14·3Cyprinus carpio (C.c.) 22·2 0Micropterus salmoides (M.s.) 14·3O.n.=Oreochromis niloticus

315

brevis, R. lichtenfelsi (Sanchez-Alvarez et al., 1998), previously reported asR. milleri, and the species of Spinitectus currently being described as a separatespecies by two of us (AC and GPPL) but previously reported as S. carolini(Osorio-Sarabia et al., 1986).

The composition of helminth parasite communities has been used also toaddress the issue of trophic status of the waterbody being studied. Wisniewski(1958) and Chubb (1963, 1964) proposed that the trophic conditions of lakesdetermine ultimately the assemblage of fishes, which in turn determines thepresence of parasite species. Later, Esch (1971) made a distinction between typesof parasites found in oligotrophic and eutrophic systems, suggesting that the lackof interaction with organisms outside the system, like birds and mammals, inoligotrophic lakes causes the presence of more adult parasites and fewer larvalstages than in eutrophic lakes. A first attempt to test this hypothesis with fishesfrom more tropical latitudes was made by Espinosa-Huerta et al. (1996) whostudied helminth communities of the atherinid C. attenuatum from LakePatzcuaro and the deeper oligotrophic Lake Zirahuen. They concluded that asignificant difference between helminth communities of the two lakes is related toabiotic and biotic conditions that favour the presence of several populations offish-eating birds in Lake Patzcuaro. Consequently, a greater species richness andabundance of larval stages was found in fishes from this lake, indicating itsprobable eutrophic status. However, only one species of host was considered.In this study, about half the helminth species were found as larval stagesin the ten species of fish analysed, and seven of the ten larval parasiteswere species maturing in fish-eating birds. This observation is consistent withthe contention that Lake Patzcuaro is either a eutrophic lake, or in the processof eutrophication, as suggested by Berlanga et al. (1997) and Bernal-Brooks(1998).

COMMUNITY STRUCTURE AT COMPONENT COMMUNITY ANDINFRACOMMUNITY LEVELS

The helminth communities of fishes of Lake Patzcuaro indicate that they are adepauperate assemblage, with low levels of species richness and diversity andrelatively low abundance of most constituent species. The values obtained forvarious descriptors of the parasite community are quite similar to those obtainedin many other freshwater fishes (Kennedy, 1990). However, this comparisonshould be viewed with caution because data sets are different in terms of samplesize, periodicity and other ecological factors that may affect community richnessand diversity. The helminth species recovered in this study show differentdegrees of host specificity. Host specificity is more obvious in adult helminthssince larval helminths tend to be more generalist in their host associations. Mostadult endothelminths were associated either with one host species or with agroup of related hosts. Allocreadium mexicanum and Spinitectus sp. are foundonly in the atherinids (represented by three species of Chirostoma),Crepidostomum cornutum ony in the large-mouth bass, and Rhabdochonalichtenfelsi in the goodeids only. This is true also for the ectoparasitic helminths;Octomacrum mexicanum and the ancryocephalid that parasitise Algansealacustris and Micropterus salmoides, respectively. This pattern of host specificityfollows the pattern observed in helminths of freshwater fishes in general, where

316 . - .

a group of helminths is typical and often specific for higher taxa of host (e.g.families of fishes) (VanCleave & Mueller, 1934; Dogiel et al., 1961; Chubb, 1963,1970; Dick & Choudhury, 1996; Choudhury & Dick, 1998). A perusal of theinformation on adult helminths and their host associations in compilations suchas Hoffman (1999); Margolis & Arthur (1979) and McDonald & Margolis (1995)also provides some evidence of this pattern.

Almost 50% of the helminth fauna of fishes of Lake Patzcuaro is comprised oflarval stages (Table II), and many of them are shared by the majority of hostspecies. This suggests that fishes play an important role in helminth life cycles inthis lacustrine ecosystem, mainly those of fish-eating birds, and to a lesser extentthose of garter snakes, turtles and frogs, hosts that either feed on fishes or sharethe food web with them. The helminths of several vertebrate species in thelocality have been examined (Garcıa et al., 1993; Ramos, 1994; Perez-Ponce deLeon et al., 2000, unpubl. obs.) and the potential adult parasites of the larvalstages, such as Diplostomum (Tylodelphys) americana in the podicipedidPodylimbus podiceps, Ochetosoma brevicaecum in the garter snake Thamnophismelanogaster, the tapeworms Proteocephalus variabilis and P. filaroides fromgarter snakes and frogs (Rana dunni Zweifel) respectively, Contracaecum rudolphifrom Casmerodius albus L., Egretta thula Molina and Nycticorax nycticorax L,and Spiroxys contortus from the turtle Kinosternon hirtipes Wagler have beenreported. However, some of the larval helminths in the fishes are considered asundetermined species until more detailed studies about life cycles (experimentalinfections) allow corroboration of the relationships of the larval stages withadults of the aforementioned species.

It has been proposed that host geographical range is not a major determinantof helminth communities, but that species richness is influenced by localavailability of parasite species and their possibility of colonization, withinfracommunities (the lowest level) as subsets of the component community(Poulin, 1995, 1997). The present data set supports that idea in that the richnessof the helminth communities depends mainly on the local characteristics of thelake and not the richness of the regional pool of parasites for a host species alongits distributional range. However, the actual taxonomic composition of adulthelminths probably depends on processes acting at the level of highermonophyletic host taxa (as a result of phylogeny and coevolution) and maybe largely independent of the pool of parasites available in the compoundcommunity, assuming there is dietary overlap and consequently the ecologicalopportunity for colonization, i.e. assuming specificity is also physiologicaland not only ecological. Consequently, the helminth infracommunities, whilenecessarily being subsets of the component community, are not random subsetsof the compound community.

The patterns of similarity in helminth communities of fishes in Lake Patzcuaroreflect some level of host taxonomic affinity. Two species of Christoma possessedhelminth communities with a greater level of similarity than with those of otherfishes, while the three species of goodeids also possessed relatively more similarhelminth communities (Table IX). This pattern of similarity also appears to becaused by the patterns of host specificity shown by the native helminths (seeabove). However, similarity values for helminth communities in two goodiedsand in the introduced M. salmoides are also relatively high (50%) and a perusal

317

of the data (Tables III and IV) indicates that sharing of the more generalist larvalhelminths results in this similarity.

Digeneans have been suggested as the dominant group parasitizing freshwaterfishes in tropical latitudes (Salgado-Maldonado & Kennedy, 1997). While thisgeneralization is not supported in terms of the number of species of any one type(cestodes, nematodes etc.) recovered in this study (most of the species werenematodes). The bird digenean Posthodiplostomum (as a larval stage) wasnumerically dominant in six of the ten assemblages analysed; this species, ageneralist as a larval stage, is also found in about 100 species of fish in other partsof North America (Margolis & Arthur, 1979; McDonald & Margolis, 1995;Perez-Ponce de Leon et al., 1996; Hoffman, 1999). The prevalence and abun-dance of Posthodiplostomum minimum in fishes of Lake Patzcuaro indicates itslack of specificity for its second intermediate hosts and possibly the abundance ofsuitable bird hosts and favourable conditions for the first intermediate molluschosts of this parasite. Its primary definitive host in the lake is a fish-eating bird(Ardeidae) although adults may also be found in turtles and salamanders(Perez-Ponce de Leon, 1995). When intestinal helminth communities wereconsidered separately (Tables VII and VIII), host-specific helminths were thedominant species in most cases, with Allocreadium mexicanum, Capillariapatzcuarensis, Crepidostomum cornutum and Rhabdochona lichtenfelsi dominat-ing their infracommunities, and Spinitectus sp., Crepidostomum cornutum andRhabdochona lichtenfelsi dominating at the level of component community. Insome particular cases, the introduced and generalist cestode, Bothriocephalusacheilognathi, was the dominant species. In all cases, irrespective of the level ofcommunity (infra or component), or scale (over all or intestinal helminth fauna),dominance values were high and the communities were composed of numerousrare species with low abundances. As a result, evenness values were usually low,resulting in lower diversity values.

DIET OF THE HOSTTrophic interactions appear to be important determinants of the patterns

of helminth community structure in Lake Patzcuaro. With the exception ofthree helminth species (O. mexicanum, the ancyrocephalid, and the nematodeC. patzcuarensis) with direct life cycles, and two digeneans (P. minimum, andC. complanatum), whose cercariae penetrate the fish host through the skin, the 14other helminth species are transmitted via invertebrates in the diet. Host dietplays a major role in determining helminth community structure, with ageneralization that richer enteric helminth communities are found in carnivorous(insectivorous-piscivorous) fishes, compared with those in algal feeders andherbivores (Dogiel et al., 1961; Dogiel, 1964). The present data set provideslimited support for this generalization. Carnivorous fishes (C. attenuatum, A.robustus, C. estor, A. diazi, M. salmoides) possessed richer helminth infracom-munities than some herbivores and detritivores such as O. niloticus and C. carpioand the omnivorous A. lacustris. The goodeid G. atripinnis possessed a helminthassemblage that was richer than some carnivores such as C. estor, C. grandocule,M. salmoides and the omnivorous A. lacustris. Although G. atripinnis wascharacterized as a herbivore (Rosas, 1976), its helminth fauna supportsthe conclusions of Barragan & Magallon (1994) that it is omnivorous with

318 . - .

preferences for plant matter. Of the eight species of helminths found in this fish,L. intestinalis and possibly also the unidentified proteocephalidean are transmit-ted by copepods, the acanthocephalan Polymorphus brevis by amphipods, whilespecies of Rhabdochona also require an aquatic arthropod intermediate host,commonly ephemeropteran nymphs. Species of Eustrongylides are commonlytransmitted by oligochaetes and Spiroxys sp. by microcrustaceans in the diet.The relatively low richness and diversity of helminths in the top carnivore in thisecosystem, M. salmoides, is arguably not related to the feeding habits of the host,but to historical and biogeographical reasons as discussed below for this and theother introduced species. Although O. niloticus is considered an omnivore, itsdepauperate helminth fauna may indicate also its detritivorous habits and, as inM. salmoides, must be interpreted with reference to the effects of biogeographyand translocation (see below).

The low species richness and diversity of helminth communities in C.grandocule are more difficult to explain since the species lives in apparentsympatry with C. attenuatum and has similar carnivorous feeding habits (Rosas,1976; Berlanga et al., 1997). The differences in the parasite assemblages mayindicate that there are some differences in habitat and feeding behaviour(Marcogliese & Cone, 1997) too fine-tuned to be uncovered by the informationcurrently available on the biology of these species. The absence of Polymorphusbrevis, a bird acanthocephalan transmitted to the fish intermediate host byamphipods, in C. grandocule, may be indicative of such ecological differences.The absence of Spinitectus sp. in C. grandocule and its presence in C. attenuatumand C. estor is also consistent with the possibility of subtle ecological shifts sincespecies of Spinitectus commonly utilize benthic ephemeropteran nymphs for theirtransmission (Hoffman, 1999). Alternatively, the differences could be physio-logical and (or) immunological. Although the data do not allow any firmconclusions at this stage, they are strongly suggestive of real biological differ-ences between C. grandocule and the other Chirostoma spp. sampled in this study(see Marcogliese & Cone (1997) for a detailed discussion of the significance ofparasites in food web studies).

TRANSLOCATION AND INTRODUCTION OF HOSTSDogiel (1964) and Petrushevski (in Dogiel et al., 1961) generalized that host

species that are translocated and introduced into areas outside their naturaldistributional range suffer a reduction in the number of their parasite species ora loss of their original parasite fauna. They identified several factors, includingthe degree of difference of the new area, manifested in the existing communitycomposition of hosts (intermediate and definitive) in this new area, age and stage(eggs, larvae, fry, etc.) of the hosts being translocated, and the nature of theparasites. The empirical evidence suggested that parasites with complex lifecycles involving intermediate hosts were more susceptible to extirpation in thenew area than parasites such as monogeneans with direct life cycles. Kennedy &Bush (1994) have elaborated on these general principles, using the translocationof rainbow trout Oncorhynchus mykiss (Walbaum) as a case study, but dealt withabsolute distance from source populations. Their study reinforces the conceptsdiscussed by Dogiel (1964) and Petrushevski (in Dogiel et al., 1961) but the useof absolute distance (Kennedy & Bush, 1994) is problematical since the relevant

319

distance here is ecological distance and can be measured only in terms of thedegree of difference between the original and the new environment. Thesignificant effect of absolute geographical distance may be a statistical artifact ofthe probability that as distance from source increases, so does the ecologicaldistance, and consequently does not make for a robust hypothesis. Theinformation from this study indicates that native fish species generally harbourricher and more diverse helminth communities than introduced ones, with onenotable exception (M. salmoides, see below). The native goodeid Alloophorusrobustus possessed the richest and most diverse helminth communities at bothcomponent- and infracommunity levels (Tables V and VII). However,Micropterus salmoides shows higher values than those obtained from some of thenative species such as Chirostoma grandocule and Algansea lacustris (Tables Vand VI). The data also demonstrate that the relative richness of parasitecommunities in a fish species is influenced by biological and biogeographicalfactors beyond a characterization as a native or introduced species. The datafrom this study also allow comparison of the effects of translocation in threespecies of fishes (C. carpio, M. salmoides and O. niloticus) that have beenintroduced into Lake Patzcuaro over the last few decades for several reportedreasons (fisheries enhancement, ecological control of vegetation, etc.).

The tilapia, O. niloticus, was introduced from Africa into several waterbodies,mainly in southern Mexico, where the fish fauna, and consequently the helminthfauna, is dominated by neotropical elements such as other, neotropical cichlids.In those areas, O. niloticus can be infected by at least nine species of parasites(Perez-Ponce de Leon et al., 1996), although very few of these are adulthelminths. The adult helminth fauna of O. niloticus within its original Africandistributional range is not particularly species rich (Khalil, 1969; Ukoli, 1969;Okaeme, 1991) and comprises species that are typical of African cichlids. Thedepauperate nature of its original adult parasite fauna is due partially to itsdetritivorous habits. This study indicates that it has not retained any of itsoriginal parasite fauna nor been able to act as a normal definitive host forhelminths found in Lake Patzcuaro. Only one species from its original Africanadult helminth fauna, the monogenean Cichlidogyrus sclerosus, has been foundfrom tilapia in southern Mexico (Kritsky et al., 1994), which apparently itretained during the translocation process. This corroborates the generalizationthat parasites with direct life cycles such as monogeneans are resistant toextirpation and often the only adult helminths that survive the translocationprocess.

The carp (C. carpio), a cyprinid of Eurasian origin, has attained a widedistribution following its successful introduction into North America (Lee et al.,1980). Carp were introduced into several waterbodies in Mexico, originally fromEurasia, and possibly later from other locations in North America. In Mexico,at least 14 species of helminths have been recorded as parasites of differentsubspecies of this carp (Perez-Ponce de Leon et al., 1996), which includes sometypically nearctic elements, some generalist larval stages, as well as species (e.g.Bothriocephalus acheilognathi) that were introduced, probably with carp, fromoutside Mexico. Bothriocephalus acheilognathi was introduced into Europe andNorth America through introductions of one the parasite’s native hosts, thegrass carp Ctenopharyngodon idella (Valenciennes) (Bauer, 1991; Kennedy, 1991;

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Hoffman, 1999; Scholz, 1999). This has been followed by further spread of theparasite in North America by inadvertent stocking of infected grass carp andinfected cyprinid species including C. carpio (Hoffman, 1999). This tapewormhas become widely disseminated in Mexico also and has been found in sixMexican states in at least 15 fish species (Garcıa-Prieto & Osorio-Sarabia, 1991;Scholz, 1997). Although the tapeworm is capable of infecting a range of fishhosts (Garcıa-Prieto & Osorio-Sarabia, 1991; Scholz, 1997), the data suggest thatit shows a preference for cyprinid hosts in areas where it has been introduced(Brouder & Hoffnagle, 1997; Clarkson et al., 1997; Hoffman, 1999). In LakePatzcuaro, this tapeworm, dominates only the enteric communities of C. carpioalthough it occurs in other fish species as well (Table III). In those species B.acheilognathii reaches higher values of abundance than in carp, probably as aresult of a more intense feeding on copepods by fish species that were foundinfected in this study, which may be a reflection of the size ranges sampled.Bothriocephalus acheilognathi appears to parasitise younger grass carp whilethey are still predominantly planktivorous and before the switch to a moreherbivorous diet is made (Bauer, 1991), and this may be true of C. carpio as well.Similarly, the mixed herbivorous-invertebrate feeding habits of the nativecyprinid, A. lacustris, (Table I) may preclude exposure to planktonicintermediate hosts (copepods) of this tapeworm.

The largemouth bass was introduced into the lake 70 years ago, from theU.S.A. where it possesses a rich and diverse helminth fauna along its distri-butional range (Aho & Bush, 1993; Hoffman, 1999). Of these, bass seemed tohave retained at least two species which are host-specific, an ancyrocephalidmonogenean, and the trematode Crepidostomum cornutum. The latter helminthis a common and characteristic parasite of centrarchids, particularly ofMicropterus spp. (Aho & Bush, 1993; McDonald & Margolis, 1995; Hoffman,1999) and is transmitted by crayfishes (Cambaridae) (Hoffman, 1999) which arecommon constituents of bass diets. In Lake Patzcuaro, stomach contents of bassincluded crayfish (Cambarellus montezumae or C. patzcuarensis) (unpubl. obs.)and it is speculated that these crayfish function as suitable intermediate hosts.Clearly, this trematode also has a suitable first intermediate pelecypod molluschost in this lake system, which remains unknown. These host-specific speciesdominate the community at both hierarchical levels, the monogenean for theoverall community, and the digenean, for the intestinal component. Neither ofthese species has been transferred to the native or the other exotic species, andthe helminth community of the bass has been enriched by the generalistcomponent in Lake Patzcuaro.

HOST AND PARASITE BIOGEOGRAPHYThe native fish fauna of the Mesa Central lakes of Mexico represents a mixture

of Nearctic freshwater elements and some unique secondary division freshwaterfishes endemic to the region. In Lake Patzcuaro, the Nearctic freshwaterelements include the cyprinid Algansea lacustris, and possibly the goodeids(Parenti, 1981) while the atherinids (Atheriniformes) represent fishes that havespeciated arguably from marine or brackish water ancestors following isolationin these high altitude lakes along the neo-volcanic axis. Consequently, theparasite fauna of these fish provide an ideal opportunity to investigate the extent

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of host-switching and coevolution (Brooks & McLennan, 1993). The cyprinidAlgansea lacustris is parasitized by a host-specific gill monogenean, Octomacrummexicanum which, like its host, has its sister taxa among the nearctic fauna.Other Octomacrum spp. parasitize cyprinids in other parts of North America(Canada and the U.S.A.) and one species, Octomacrum lanceatum, is a parasitespecific to the catostomids (suckers) a potential sister group of the cyprinids(Smith, 1992; Margolis & Arthur, 1979; McDonald & Margolis, 1995; Hoffman,1999). The goodeids are parasitized by an apparently host-specific nematode,Rhabdochona lichtenfelsi, which is morphologically similar to the nearcticspecies, R. milleri, also a parasite of catostomids, but recognized recently anddescribed as a separate species. It follows from the hypothesis of the sisterrelationships of goodeids to cyprinodontoids of the south-western U.S.A.(Parenti, 1981) and from the faunal history of the Mesa Central region, that thisnematode should be related more closely to the nearctic species of Rhabdochonathan to the neotropical species in the genus. This relationship would imply alsothat at some time in the past, the hosts of the sister Rhabdochona spp. must havebeen sympatric in their distribution with the goodeids or their ancestors. Thecase of Allocreadium mexicanum in the native endemic atherinids is similar.Allocreadium is a north temperate (holarctic) genus, typical of cyprinids(Bykhovskaya-Pavlovskaya & Kulakova, 1987; Gibson, 1996; Hoffman, 1999).Interestingly, the only native cyprinid in the lake, A. lacustris is not parasitizedby it or by any species of Allocreadium. As in the case of R. lichtenfelsi ingoodeids, the presence of A. mexicanum in atherinids can be hypothesized to bea result of a host-switching event. In both cases, the hypotheses are testable byphylogenetic analyses of the two groups of parasites (Brooks & McLennan,1991, 1993) and in both cases it would appear that the hosts of the sister taxa areno longer present in the area. Surveys of other lakes in the Mesa Centralcombined with phylogenetic studies on the helminths of fishes and othervertebrates such as frogs are underway to test these hypotheses. The digeneanfauna of amphibians in central Mexico also demonstrates such nearctic influ-ences and reflects the historical biogeography of their hosts (Perez-Ponce deLeon et al., 2000).

Recent years have seen investigations into latitudinal richness gradients ofparasites (Rohde, 1993; Rohde & Heap, 1998) and suggestions of richerparasite communities in tropical fishes (Kennedy, 1995; Salgado-Maldonado &Kennedy, 1997). However, analyses of data from tropical freshwater fishes (A.Choudhury and T. A. Dick, unpub. data) indicate that the helminth communi-ties of tropical freshwater fishes are not necessarily species rich. Biogeographi-cal influences are probably important and although the Mesa Central lakes lieat lower latitudes, their fish fauna reflects an endemic or nearctic character.Studies from other areas of Mexico including areas showing clear neotropicalinfluences (e.g. the Yucatan peninsula) indicate that richer parasite communi-ties are characteristic of some cichlids (Vidal, 1995; Salgado-Maldonado &Kennedy, 1997) but not of other species of fishes examined from those andother areas (Perez-Ponce de Leon et al., 1992; Leon-Regagnon, 1993; Vidal,1995).

The above discussion indicates that the intestinal communities of native fishesin Lake Patzcuaro are characterized and dominated by host-specific helminths

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whose geographical distributions are restricted to the Mesa Central of Mexico,and that those of the introduced species are also often dominated by host-specifichelminths, which were introduced into the lake with those hosts. The larvalhelminths provide the local ecological noise that enhances the stochastic natureof the communities. The patterns observed in this study indicate clearly thatlatitude alone does not contribute necessarily to a rich and diverse parasitecommunity and that a combination of historical and contemporary ecologicalfactors (Janovy et al., 1992; Poulin, 1995, 1997) plays an important role indetermining helminth community diversity and structure in these freshwaterfishes.

The authors thank B. Mendoza-Garfias, G. Pulido-Flores, E. Peresbarbosa, I. Garcıaand E. Espinosa for help during this study. This study was partially funded by a NationalCouncil for Science and Technology (CONACYT) grant No. 27996 N to GPPL andgrant No. IN 219198 under the PAPIIT-UNAM program to GPPL and VLR. Weacknowledge unpublished analyses from a submitted, but as yet unpublished, manuscripton the richness and diversity of tropical freshwater fish parasite communities, by A.Choudhury and T. A. Dick. AC acknowledges the financial support of an NSERCpost-doctoral fellowship at the University of Toronto, Canada, and an NSERC grantA7696 to Dan Brooks in whose laboratory AC held the NSERC fellowship.

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