Taxonomía y Sistemática

 

Helminth parasites of atherinopsid freshwater fishes (Osteichthyes: Atheriniformes) from central Mexico

 

Helmintos parásitos de aterinópsidos de agua dulce (Osteichthyes: Atheriniformes) del centro de México

 

Georgina Lira–Guerrero, Luis García–Prieto* and Gerardo Pérez–Ponce de León

 

Laboratorio de Helmintología, Instituto de Biología, Universidad Nacional Autónoma de México. Apartado postal 70–153, 04510, México, D. F., México.

 

*Correspondent:
gprieto@ibiologia.unam.mx

 

Recibido: 25 abril 2007
Aceptado: 21 noviembre 2007

 

Abstract

Between May 1997 and September 1998, 270 atherinopsids belonging to 7 fish species were analyzed for helminths in 6 lakes located in central Mexico. In addition, a database with all the available previous records of helminth parasites of atherinopsids was built. Based on both information sources, we analyze the composition of the helminth fauna parasitizing atherinopsid freshwater fishes from central Mexico, in order to determine some general species compositional patterns. The helminth fauna parasitizing this fish family in central Mexico is composed by 10 digeneans, 13 cestodes, 1 acanthocephalan, and 8 nematodes (24 of them as larval stage). Individual species richness ranged from 1 to 22 helminth species. Feeding habits of the hosts are identified as the main factor in determining helminth species composition (22 of them are acquired through ingestion). Helminth species composition of almost all host species was dominated by generalist helminth species. Only 2 specialist species were found: Allocreadium mexicanum and Spinitectus osorioi, representing the core helminth fauna of this group of fishes. These results corroborate the hypothesis that the parasite fauna in freshwater fishes is largely circumscribed by higher levels of monophyletic host taxa.

Key words: helminths, atherinopsids, central Mexico, freshwater fishes.

 

Resumen

Entre mayo de 1997 y septiembre de 1998, se recolectaron 270 aterinópsidos pertenecientes a 7 especies de peces en busca de helmintos, en 6 lagos del centro de México. Basados en esta información y en los registros previos sobre helmintos en este grupo de hospederos, se construyó una base de datos. El objetivo de este estudio es analizar dicha información, para establecer algunos patrones generales acerca de la composición de los helmintos que los parasitan. Treinta y dos especies de helmintos infectan a los peces de esta familia (10 digéneos, 13 cestodos, 1 acantocefalo y 8 nematodos), 24 de ellas en estado larvario. Los hábitos alimenticios de los aterinópsidos determinan la composición de la fauna helmintológica, ya que 22 especies son adquiridas por los peces vía ingestión. La riqueza por especie de pez varió de 1 a 22 especies de helmintos, predominando las generalistas; sólo 2 especies (Allocreadium mexicanum y Spinitectus osorioi) son específicas para esta familia de hospederos, lo que confirma la hipótesis de que la parasitofauna en peces de agua dulce está circunscrita a niveles superiores de taxa monofiléticos.

Palabras clave: helmintos, aterinópsidos, México, peces de agua dulce.

 

Introduction

Atherinopsids represent a group of fishes distributed worldwide, including both marine shoreline and freshwater elements. They were formerly included within the Atherinidae; however, this group of fishes has a complex taxonomic history (Miller et al., 2005). According to Miller et al. (2005), the group includes about 36 species in Mexico, with 10 marine shoreline elements (in the genus Atherinella), and 26 freshwater ones (in the genus Menidia). In this paper, we followed the traditional classification and nomenclature of the group; the genus names Chirostoma and Poblana are used here, even though their validity has not been settled (Miller and Chernoff, 1979; Echelle and Echelle, 1984; Chernoff, 1986).

To date, the helminth fauna of only 3 atherinopsid fish species has been systematically studied: Chirostoma attenuatum from Lago de Pátzcuaro and Lago de Zirahuén, Michoacán State, and Chirostoma estor and Chirostoma grandocule both from Lago de Pátzcuaro (Osorio–Sarabia et al., 1986; Pérez–Ponce de León et al., 1994; Espinosa–Huerta et al., 1996; Pérez–Ponce de León et al., 2000). In addition, numerous isolated records of helminths infecting some members of this family of fishes have been published so far (Perez–Ponce de León et al., 1996 and references therein; Salgado–Maldonado, 2006 and references therein). The aim of this study is to analyze the composition of the helminth fauna parasitizing atherinopsid freshwater fishes from central Mexico, incorporating new data to previous distributional records in order to determine some general species compositional patterns.

 

Materials and methods

Between May 1997 and September 1998, 270 atherinopsids were collected from 6 lakes located in central Mexico. We sampled 30 individuals of each of 7 species of atherinopsids in the following localities: 4 in the State of Michoacán: Lago de Cuitzeo: Chirostoma jordani; Lago de Pátzcuaro: C. attenuatum, C. estor, and C. grandocule; Lago de Zacapu: Chirostoma humboldtianum; Lago de Zirahuén: C. attenuatum and C. estor, and 2 in the State of Puebla: Lago Las Minas: Poblana letholepis and Lago Quechulac: Poblana alchichica squamata. Hosts were collected with a seine net, kept on ice, and examined using a dissecting microscope, within 4 hr after capture. Organs examined included gills, eyes, brain, muscle, mesentery, liver, spleen, heart, gonads, and the gastrointestinal tract. All helminths were counted in situ, recovered from the tissues, and processed according to procedures described in Mendoza–Garfias et al. (1996). Voucher specimens were deposited in the Colección Nacional de Helmintos (CNHE), Instituto de Biología, Universidad Nacional Autónoma de México, México City.

In order to analyze the information we obtained in this study in a wider (regional) scope, a database with all the available records of helminth parasites of atherinopsids was assembled, based on all published accounts where at least 1 helminth species was recorded.

 

Results

In total, 11 653 specimens of helminths were collected from the 7 species of atherinopsids, representing 14 taxa (6 digeneans, 3 cestodes, 1 acanthocephalan, and 4 nematodes). Ten of the 14 species were represented by larval stages. Body cavity, liver and mesentery were the habitats with the highest species richness with 5 helminth species each one, all as larval stages. Eleven host records are new and the geographic ranges of 9 species are expanded by these records: Tylodelphis sp., Ochetosoma sp., Posthodiplostomum minimum, Pygidiospis sp., Uvulifer sp., (digeneans), Bothriocephalus acheilognathi, Ligula intestinalis, Paradilepis sp., (cestodes), and Eustrongylides sp. (nematode). The metacercariae of Pygidiopsis sp. are recorded for the first time in fishes from water bodies of central Mexico (Tables 1 and 2).

In addition, Tables 1 and 2 include all available information on the composition of the helminth parasite fauna of atherinopsids in central Mexico. To date, 18 species of hosts in 23 localities corresponding to 9 States of the Mexican Republic have been studied.

 

Discussion

Previous records as well as the new information provided by the present study indicate that the helminth fauna parasitizing atherinopsid fishes in water bodies in central Mexico is composed by 32 taxa (10 digeneans, 13 cestodes, 1 acanthocephalan, and 8 nematodes). Eight of the 32 species were adult forms: Allocreadium mexicanum, Proteocephalus amploplites, B. acheilognathi, Atractis bravoae, Ornithocapillaria appendiculata, P. tomentosa, Rhabdochona sp., and Spinitectus osorioi, all of them recovered from the intestine of their hosts; the record of 3 of these species, i. e., P. ambloplites, O. appendiculata, and Rhabdochona sp. is uncommon. On the one hand, P. ambloplites, the bass tapeworm, is a common parasite of centrarchid fishes in North America (Hoffman, 1999), so its presence in C. jordani from the Río La Laja, Guanajuato State (Salgado–Maldonado, 2006) needs further verification given that no specimens are deposited in a parasite collection. On the other hand, the nematode O. appendiculata is an intestinal parasite of cormorants (Phalacrocorax sp.) in Brazil (Moravec et al., 2000), and therefore its record in C. estor from Lago de Pátzcuaro clearly represents an accidental infection. Finally, Rhabdochona sp. was recorded as a larval form by Salgado–Maldonado (2006); this larva was found in the gut, which means that it could be an immature form (L3, L4) that either was unable to develop further or was simply transmitted in the diet. That record may represent the first one of a species of Rhabdochona in atherinopsids, since congeneric species commonly occur in goodeids in the same geographic region (Mejia–Madrid et al., 2005); however, there are no specimens available to confirm their identity.

The nematode P. tomentosa and the tapeworm B. acheilognathi are introduced species; both are intestinal parasites of freshwater fishes with a very low degree of host specificity (Moravec et al., 2001; Salgado–Maldonado and Pineda–López, 2003). Their presence in atherinopsids from central Mexico is due to the introduction of cyprinid fishes for aquaculture.

Twenty four of the 32 helminth taxa (75%) were represented by larval stages inhabiting 9 different sites of the host body. Twenty of them complete their life cycle when fishes are eaten by fish–eating birds; the remaining 4 species complete their development in fishes, amphibians or reptiles (Ochetosoma sp., Proterodiplostomum sp., Proteocephalidea gen. sp., and Spiroxys sp.).

Chirostoma jordani possesses the highest helminth species richness (22 taxa), followed by C. attenuatum with 13, and C. estor and C. humboldtianum with 12, each. The composition of the helminth fauna of the other fish species ranged from 1 to 5 species. The most widely distributed helminth species among the hosts was the cestode B. acheilognathi, recovered from 10 atherinopsid species, as well as the digeneans P. minimum and A. mexicanum from 9 and 7 host species, respectively. On the other hand, 17 of the 32 helminth species have been recorded parasitizing only 1 host species; this group is composed basically by larval stages of cestodes and digeneans (Table 1).

Helminth faunal composition of almost all species of hosts was dominated by generalist species, which are commonly found in phylogenetically unrelated freshwater fishes and even in amphibians and reptiles. The most frequent association of generalist helminth species is constituted by the digenean P. minimum, the tapeworm B. acheilognathi and the acanthocephalan P. brevis, which co–exist in 5 atherinopsid species; however, most of the generalist species were recovered from only 1 species of host. Helminth species specialized on atherinopsids uncommonly co–occur in the same host species: A. mexicanum and S. osorioi were found together only in 3 fish species: C. attenuatum, C. estor and C. grandocule, all of them in Lago de Pátzcuaro, while A. bravoae has been exclusively registered as a parasite of Atherinella balsana in Presa El Infiernillo.

The most widely distributed helminth species among localities was B. acheilognathi which was found in 12 of the 23 localities studied, followed by the metacercariae of P. minimum in 10 sites; 12 helminth taxa were found in only 1 locality. The highest number of helminth species was in fishes from Lago de Pátzcuaro (15 species), Río La Laja (15 species), and Lago de Zacapu (10 species), while in 8 localities, the number of helminth species was only 1 (Table 2).

In terms of the factors that determine the helminth species composition of atherinopsids in central Mexico, the feeding habits of the hosts are the most important, given that 22 of the helminth species parasitizing these fishes are acquired through prey. The species transmitted by direct penetration are exclusively larval digeneans (9 species). The life cycle of the nematode A. bravoae has not been studied. However, eggs of atractids hatch and larvae develop to third stage in the uteri. Thus, autoinfection seems to be the rule regarding this parasite. Their transmission from host to host is not completely understood (Anderson, 2000).

This is the second study examining species composition of the helminth fauna in specific freshwater fish families along their distributional range in central Mexico, the first one being conducted by Mejía–Madrid et al. (2005) with goodeids. The results we obtained in this study corroborate the hypothesis that the parasite fauna in freshwater fishes is largely circumscribed by higher levels of monophyletic host taxa (Pérez–Ponce de León and Choudhury, 2005). In the case of atherinopsids, the core helminth fauna is represented by the digenean A. mexicanum, and the nematode S. osorioi. There are sporadic records of A. mexicanum in hosts other than atherinopsids (Mejía–Madrid et al., 2005; Salgado–Maldonado, 2006) albeit with very low abundance values that indicate that its presence in these hosts does not represent an established infection. New host and locality records of this digenean have been made in the last few years, so its geographical range has been expanded and it is no longer regarded a species endemic to Lago de Pátzcuaro (Salgado–Maldonado, 2006). Instead, S. osorioi has only been found in atherinopsids from Lago de Pátzcuaro and Lago de Zirahuén (Garrido–Olvera et al., 2006).

 

Acknowledgements

To Berenit Mendoza, Agustín Jiménez, and Jorge Falcón for their help in field work. To Fernando Bernal–Brooks for his comments to an early version of the manuscript. This study was funded by projects CONACyT–472233 and PAPIIT–UNAM–IN220605 to GPPL.

 

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