Taxonomía y sistemática

 

Metazoan parasites of Mycteroperca bonaci (Epinephelidae) off the coast of Yucatán, Mexico, with a checklist of its parasites in the Gulf of Mexico and Caribbean region

 

Parásitos metazoarios de Mycteroperca bonaci (Epinephelidae) de las costas de Yucatán, México, con una lista de sus parásitos registrados en el golfo de México y la región del Caribe

 

Juan F. Espínola-Novelo¹, Carlos González-Salas¹, Sergio Guillén-Hernández¹* and Ken MacKenzie²

 

¹ Departamento de Biología Marina, Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Yucatán, Carretera Mérida-Xmatkuil, Km 15.5. Itzimná, 97100 Mérida, Yucatán, México. *ghernand@uady.mx

² School of Biological Sciences (Zoology). The University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, UK.

 

Recibido: 11 octubre 2011
Aceptado: 30 junio 2013

 

Abstract

Samples of black grouper, Mycteroperca bonaci, totalling 161 specimens, were collected at 3 protected natural areas in Yucatán, Mexico: Reserva de la Biosfera Ría Celestún (RBRC), Reserva Estatal de Dzilam (RED), and the Parque Nacional Arrecife Alacranes (PNAA). In this study, we present the results of a survey of the metazoan parasite fauna of these fishes, together with a checklist of the metazoan parasites recorded previously from black grouper in the Gulf of Mexico and the Caribbean Sea. Twenty five taxa were found in the survey (21 adults and 4 larval stages). Nineteen taxa represent new host records for M. bonaci, increasing the total number of parasite taxa recorded for this host species to 59 in the geographic area referred above. Differences in species composition and infection parameters of each group of parasites are presented and discussed.

Key words: ectoparasites, endoparasites, marine fish, arrecife Alacranes, black grouper, Caribbean Sea, Dollfustrema sp.

 

Resumen

En este trabajo se presentan los resultados del estudio parasitológico de 161 "negrillos" Mycteroperca bonaci recolectados en 3 áreas naturales protegidas del estado de Yucatán, México: Reserva de la Biosfera Ría Celestún (RBRC), Reserva Estatal de Dzilam (RED) y el Parque Nacional Arrecife Alacranes (PNAA). Asimismo, se presenta la lista de metazoarios parásitos registrados en este hospedero hasta el momento en la región del golfo de México. Como resultado de este estudio, se reportan 25 taxa parasitando esta especie de pez, de los cuales 21 se encontraron en fase adulta y 4 en etapa larvaria. Diecinueve de los taxa encontrados son reportados por primera vez para este hospedero, incrementándose a 59 el número total para este hospedero en la región.

Palabras clave: ectoparasitos, endoparasitos, peces marinos, arrecife Alacranes, negrillos, mar Caribe, Dollfustrema sp.

 

Introduction

The black grouper, Mycteroperca bonaci (Poey, 1960), is one of the most important species for commercial fisheries in Bermuda, Gulf of Mexico, Cuba and Venezuela (Heemstra and Randall, 1993). In the Yucatán Peninsula, all the serranid species are included in the "mero" fishery (Sánchez-Salazar et al., 1999). By both number of individuals and weight of landings, M. bonaci is one of the 3 most important species in this fishery (Brulé et al., 2008). Unfortunately, information on the parasite fauna of this species in the Southeast of Mexico is limited to a few taxonomic records. In spite of the economic and ecological importance of M. bonaci in the region, only 3 parasite species have previously been recorded: 1 monogenean (Vidal-Martínez and Mendoza-Franco, 1998) and 2 nematodes (González-Solís et al., 2002; Mejía-Madrid and Guillén-Hernández, 2011).

Fish parasites can be important from the economic and medical point of view; they are also potentially useful as indicators of human impact on the environment, of possible phylogenetic relationships between host and parasite, of host diet and migrations, and can be used as biological tags in fish stock identification (Williams et al., 1992; Williams and Jones, 1994; Lafferty, 1997; MacKenzie and Abaunza, 2005; Marcogliese, 2005; Sasal et al., 2007). In the Gulf of Mexico and the Caribbean Sea, 40 taxa have previously been reported as parasites of M. bonaci: 3 monogeneans, 4 cestodes, 15 digeneans, 5 nematodes, 7 copepods, and 6 isopods.

The main goals of this paper are to present the results of a survey of metazoan parasites recorded from M. bonaci in 3 localities in the state of Yucatán, and to update the checklist of metazoan parasites reported for this fish species in the Gulf of Mexico and the Caribbean Sea.

 

Materials and methods

Samples were taken from 3 protected natural areas (Table 1): Reserva de la Biosfera Ría Celestún (RBRC) (20^o51'34" N and 90^o24'69" W), Reserva Estatal de Dzilam (RED) (21^o24'00" N and 88^o50'52" W), and Parque Nacional Arrecife Alacranes (PNAA) (22^o22'41" N and 89^o30'57" W). The RBRC is located in the east region and RED in the west region of the state; both areas are coastal and include 2 of the main ports of the state. On the other hand, PNAA is a reef located at 130 km from the coast and is an important fishing area.

Fish were provided by the artisanal fishermen or caught with hook and line. When fish were obtained by artisanal fishermen, only the viscera were examined. During 2008 and 2009 only viscera were examined (see Table 1); during 2010 and 2011 further samples were collected and each entire fish was examined for both ecto- and endoparasites. A total of 161 hosts were examined from the 3 natural protected areas. Fish obtained by artisanal fishermen were not measured or weighed, but those caught with hook and line were measured (total length and standard length) and weighed (P). At PNNA 63 fish were collected and 23 were measured (TL= 40.14 ± 8.25; SL= 34.15 ± 7. 54; P= 873.44 ± 656. 08), at RBRC 54 fishes were examined and 38 were measured (Lt= 35.75 ± 7.52; Le= 31.17 ± 6.63; P= 605.59 ± 734.74) and finally at RED 44 fish were examined but none was measured or weighed.

Samples were transported to the laboratory in containers with ice and examined under microscopes. All parasites were studied fresh, counted in situ and then preserved in 70% alcohol and processed for subsequent identification by means of conventional helminthological methods (Lamothe-Argumedo, 1997). Parasitic copepods and isopods were fixed and stored in 70% alcohol. Voucher specimens of helminth species were deposited at Coleccion Nacional de Helmintos, Instituto de Biología, Universidad Nacional Autónoma de México, México City. Ecological parameters such as prevalence, mean intensity, and mean abundance were calculated following Bush et al. (1997).

 

Results

A total of 28 654 individual parasites belonging to 25 taxa, 9 of which were identified to species level, were found in the 161 fish examined (Table 2). Twenty-one taxa were found as adults and only 4 as larvae. Digeneans and nematodes were the groups with the highest number of taxa (8 each); monogeneans, acanthocephalans, isopods, and copepods had 2 each and only one taxon of cestodes was found. Twenty out of the 25 taxa are new host records for M. bonaci.

The greatest number of taxa were found at Celestún (20) followed by Arrecife Alacranes (18) and Dzilam de Bravo (9). Arrecife Alacranes and Celestún share 58.3% (14 out of 24 species) of the parasite species, while Arrecife Alacranes and Dzilam share 6 (46.1%) and Celestun and Dzilam 7 (53.8%) of the 13 species found in the intestine of this host species.

The intestine was the site of infection where the largest number of different parasite taxa (13) was found. This was followed by the gills with 7 taxa. Gills were examined only in fish samples from Arrecife Alacranes and Celestun; 4 parasite taxa were shared between those samples.

Overall, digeneans showed the highest prevalence values, particularly Prosorhynchus sp., and P. atlanticus as adults. As larval stages (metacercariae), Dollfustrema sp. showed high prevalences at both Alacranes and Celestún, but mean abundance and mean intensity values were higher in samples collected from Celestún. Parasites with direct life cycles such as monogeneans, copepods, and isopods also showed high prevalences, but with lower mean abundances values than digeneans.

 

Discussion

Prior to this study, 40 metazoan parasite taxa were known to parasitize M. bonaci in the Gulf of Mexico and throughout the Caribbean Sea, but no data on infection levels were given in any of those studies. Previous records in Mexico showed the presence of 1 monogenean (Vidal-Martínez and Mendoza-Franco, 1998) and 2 nematodes in this host (González-Solís et al., 2002; Mejía-Madrid and Guillén-Hernández, 2011). Our data show that 19 out of the 25 species found at the 3 study sites in Yucatán are new records for M. bonaci, increasing the total number of parasite taxa recorded for this host species to 59 (Table 3).

Three species of monogeneans have been previously reported from M. bonaci: Pseudorhabdosynochus capurroi in Mexico and Puerto Rico (Vidal-Martínez and Mendoza-Franco, 1998; Medina-Ríos, 2008), P. kritskyi in Puerto Rico (Medina-Ríos, 2008) and Diplectanum sp. in Venezuela (Fuentes et al., 2009). It is possible that the monogeneans identified as Pseudorhabdosynochus sp. in this study belong to the species P. kritskyi, but the small number of collected individuals and the poor condition of the material precludes it specific determination.

Eight out of the 15 digenean taxa previously reported in M. bonaci were found in the present study. Bucephalids were the best represented with 4 taxa which constitute 50% of the taxa found. The high number of species belonging to this family recorded in the present survey, and the previous record of at least 37 species of the genus Prosorhynchus as parasites of Mycteroperca spp., may be an indication of a close phylogenetic relationship between this group of hosts and their parasites (Cribb et al., 2002).

Four taxa of cestodes had been previously reported in M. bonaci (Table 3). Since the cestode found in the present survey is a larval form, it was not possible to identify it to species level. Tetraphyllidean cestodes exhibit a narrow specificity to their final hosts (Williams and Jones, 1994; Marcogliese, 1995) and it is known that the elasmobranchs Carcharhinus plumbeus and Sphyrna mokarran prey on serranids (Jory and Iversen, 1989), so it is possible that adults of this parasite are present in those hosts.

This is the first time that the acanthocephalans Gorgorhynchus sp. and Serrasentis sp. have been reported as parasites of M. bonaci. Prevalence and mean abundance values for Gorgorhynchus sp. were lowest at Arrecife Alacranes, probably as a consequence of the intermediate host distribution. Prior to this report, Gorgorhynchus gibber was found in Mycteroperca venenosa (see Amin, 1998) and G. clavatus in Epinephelus morio (see Moravec et al., 1997). Serrasentis sp. infection in M. bonaci may be accidental or the parasite may use this fish as a paratenic host, since the parasites were found encysted in the mesenteries.

After digeneans, nematodes are the second group with most species parasitizing M. bonaci. Previous records in Mexico and the Yucatán Peninsula include Dichelyne bonacii (González-Solís et al., 2002) and Cucullanus mycteropercae (Mejía-Madrid and Guillén-Hernández, 2011). Raphidascaris anchoviellae has been found in M. bonaci from Florida (Linton, 1908), Philometra lateolabracis in Bermuda (Rees, 1970), and Anisakis simplex in Puerto Rico (Medina-Ríos, 2008), but they have not been found previously in Mexico. This last species uses cetaceans as natural final hosts but also can infect humans (Anderson, 2000).

Both Lernanthropus sp. (Copepoda) and Gnathia sp. (Isopoda) are new records for M. bonaci. Species of the genus Gnathia are not parasitic as adults, but their praniza larvae are (Kabata, 1970). Rohde (2005) reported that the Caribbean region shows a high diversity of ectoparasites; the small number of those parasites reported in Mexico could be a consequence of the lack of parasitological studies on those groups.

Previous studies on marine fish parasites off Yucatán had shown a pattern where the intestinal helminthfauna was dominated by digenean species (Moravec et al., 1997; Sánchez-Ramírez and Vidal-Martínez, 2002; Argáez-García et al., 2010). The present study shows a similar pattern for M. bonaci, where 7 digenean taxa vs 4 nematode taxa were found in this organ.

The high number of parasites in adult stages in this host is probably a result of its role as a predator in the ecosystem (Parrish, 1987). The larval taxa found in this host comprised 1 cestode (Tetraphyllidea gen. sp.), 1 digenean (Dollfustrema sp.) and 1 nematode (Pseudoterranova sp.), which complete their life cycles in large predatory fishes or sea mammals.

Differences in the number of taxa and their infection levels found between localities may be related to sample size, season or the biotic and abiotic conditions at each locality. Dzilam de Bravo was the site with the lowest sample size and only fish intestines were examined, also samples were collected during only 2 months of the year. However, samples from Arrecife Alacranes and Celestun were larger, ecto and endoparasites were obtained, and samples were caught at different times of the year. These factors increased the probability of finding parasite taxa with strong seasonality or low prevalence values.

Differences in parasite abundances between localities, mainly those which infect the intestine, can be a result of the abundance and geographical distribution of the intermediate hosts, since most of these reach their final hosts via a predator-prey relationship. Ectoparasites such as monogeneans and copepods, on the other hand, are strongly influenced by external environmental conditions. Previously 2 species belonging to the genus Pseudorhabdosynochus had been reported off the coast of Yucatán (P. capurroi in M. bonaci by Vidal-Martínez and Mendoza-Franco [1998] and P. yucatanensis in E. morio by Vidal-Martínez et al. [1997]). In the present survey, however, just 1 species was found at Celestún and 2 at Arrecife Alacranes. This difference may be related to the geographical distribution of the parasites, rather than a seasonal pattern, since that samples from Celestún were collected at different times of the year, which would rule out seasonality as an explanation for the difference. Prevalence and mean abundance values for Gorgorhynchus sp. were lower at Arrecife Alacranes, probably as a consequence of the intermediate host distribution.

 

Acknowledgements

This study was funded by the Project Promep 103.25/2575. The authors thank Conam and Secretaría de Comunicaciones y Transportes for transportation to the Arrecife Alacranes. We also thank Dr. David González Solís for the identification of some nematode species, and Jorge Peniche, Mercedes Quintanilla, Arlett Rosado and Don Cuco for assistance in field and laboratory. Ken MacKenzie's participation was partly funded by The Royal Society of Edinburgh through their open international Exchange Programme.

 

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