Parasite community analysis of the gray snapper Lutjanus griseus (Perciformes,Lutjanidae) in a tropical region of the Southern Gulf of Mexico

Parasites can play a fundamental role in the life of fish, as they can

alter their biological effectiveness, affect their behavior, growth, fecundity, migratory patterns, and mortality (Barber & Poulin, 2002; Marcogliese 2004; Luque & Poulin 2007; Raissy & Ansari, 2012). In the case of the snappers (Family Lutjanidae), this fish group is commonly associated with the seabed where feed mainly on benthic organisms such as nocturnal fish, crustaceans (crabs, shrimp, stomatopods), molluscs (gastropods and cephalopods) and plankton from shallow waters to bottoms located between 400 and 500 m deep (Anderson, 2002; Brulé, 2004; Guevara et al., 2007). These organisms on which they feed can include intermediate hosts of helminths, which in addition to infecting the snapper, can cause negative impacts on their commercialization, on the farming of the species and generate public health problems (e.g., in the case of have nematode species that cause anisakiasis or gnathostomiasis) (Emmel et al., 2006; Shamsi et al., 2013; Alda et al., 2015; Mattiucci et al., 2017; Drietrich et al., 2018; Ikuno et al., 2018; Yuan et al., 2018; Juárez-Camargo et al., 2020).

In the case of the commercially important snapper species on the coasts of the Mexican Atlantic (Gulf of Mexico and Caribbean), there is relatively little knowledge about their parasitic fauna (González-Solís et al., 2002; González-Solís et al., 2007a, b; Argáez-García et al., 2010; Montoya-Mendoza et al., 2014; Mendoza-Franco et al., 2018). This may be because marine fish from this region (southeast of Mexico) have been relatively less studied (from a parasitological point of view) than freshwater fish (Salgado-Maldonado, 2006).

The gray snapper, Lutjanus griseus (Linnaeus, 1758), is a commercial important fish that distributes from Massachusetts USA to Brazil, including the Gulf of Mexico and Caribbean, and characterize by feeds on fish and large invertebrates (Guevara et al., 2007; Juárez-Camargo et al. 2020), which, as mentioned above, are possible intermediate hosts and / or vectors of parasitic helminths and crustaceans. However, despite the high commercial value of this fish in the Mexican coasts and that has been considerate a good candidate for aquaculture in this region (Riley et al., 2008), there are still few parasitological studies on this species (e.g., Salgado-Maldonado, 1979; Lamothe-Argumedo et al., 1997; Argáez-García et al., 2010). Therefore, knowing the diversity of species of parasites that infect this fish species as well as their prevalence and intensities is relevant, since these organisms can negatively affect the host populations. For example, recent helminthological examinations of specimens of the grey snapper in the northern Gulf of Mexico (Florida, USA) described a myxozoan infection causing high mortalities in juvenile of this fish species, which was associated with increases in seawater temperature (Holzer et al., 2013).

In the Mecoacán lagoon system in the southern Gulf of Mexico (Tabasco, Mexico) the gray snapper L. griseus is a highly consumed fish notable for its size and abundant catch by artisanal fishing throughout the year (Hernández-Ojendi et al., 2020). However, for this region there are no parasitological records on this fish species. Therefore, the aims of this research were: (1) to generate a taxonomic list of the parasitic fauna present in L. griseus in the Mecoacán lagoon system, (2) to evaluate infection levels (prevalence, intensity and abundance) for each parasite species found, (3) to determine the relationship between the fish size and condition factor with the abundance of parasites in two periods of the year and (4) to determine whether any of the parasite species found can be pathogenic for human or cause negative effects to aquaculture rearing systems.

The Mecoacán lagoon system is in the Tabasco state in southeastern Mexico (between 18° 16’ N and 18° 26’ N- 93° 04’ W and 93° 14’ W) (Fig. 1). Through commercial catches the specimens were collected in two seasons of the year (dry and rain seasons). Thirty fish were collected for each season. The fish were kept in coolers with ice and transported to the Laboratory which conducted a parasitological examination. For each fish general measurements were taken; total length (cm) and weight (g). Examination of eyes, fins, skin, gill cavity and internal organs; intestinal caeca and coelomic cavity, stomach wall, stomach, intestine, spleen, gall bladder, liver, kidneys and heart were carefully examined for ectoparasites and endoparasites under a stereoscopic microscope (LEICA-DMBL 10), and all parasites were removed. Monogeneans and digeneans were fixed in AFA (acetic acid-formaldehyde-alcohol) solution for 24 h, then preserved in ethylic alcohol (70 %), and stained with Gomori’s trichromic stain (Lamothe-Argumedo, 1997; Eiras et al., 2003; Guzman-Cornejo et al., 2012). Nematodes were fixed in Berland’s liquid, preserved in ethylic alcohol (70 %), cleared with a solution of phenol-ethanol (Lent’s solution), and mounted on slides covered with glycerin-gelatin (Moravec, 1992). For the generic and specific description of the parasites, the keys proposed by the following authors were used (Amin, 1985; Anderson et al., 1974 – 1983; Blend & Dronen, 1997; Gibson, 2002; Fuentes et al., 2003; Gibbons, 2010; Kritsky, 2012; Al-Zubaidy & Mhaisen, 2012). The parasitological material was deposited in the Helminthological Collection in the Academic Division of Biological Sciences of the Universidad Juárez Autónoma de Tabasco (Mexico). Species richness, prevalence (%), abundance (parasite number / host), and intensity (parasite number / infected hosts) of parasites were determined according to Bush et al. (1997). The status of parasite species as core, secondary, satellite or rare species, was described by abundance: > 2 individuals / host = core species; 0.6 – 2 = secondary species; 0.2 – 0.6 = satellite species; < 0.2 = rare species (Zander et al., 2000; Zander, 2003).

Fig. 1

For the seasons sampled (dry and rainy seasons) a Spearman correlation analysis was made between the total length of the fish and the abundance of parasites, and for the condition of the fish and the abundance of parasites. The condition of the fish was determined by means of the Fulton Condition Factor Index (Fulton, 2002).

For this study formal consent is not required

This is the first study of parasite communities in the gray snapper (L. griseus) in the lagoon of Mecoacán Tabasco, Mexico. Therefore, the 17 recorded parasite species comprise new records of geographic distribution. The most diverse groups of parasites were that of the acanthocephalans (six species) and nematodes (four species). A factor that can influence the presence of these species are the host’s eating habits (Shamsi, 2013). Guevara et al. (2007) conducted a study on feeding habits and trophic ecology of L. griseus where they mention that they have preference for areas of submerged vegetation, as well as an increase in their abundance during the night. They also found that macrocrustaceans are the main component in the diet of this fish species (Guevara et al., 2007). This could explain that a greater number of acanthocephalan and nematode species are present and, since these groups present an indirect life cycle where their first intermediate host is generally a crustacean or other invertebrate.

It’s important to recognized valuable research concerning helminthological examinations of specimens of the grey snapper in the Gulf of Mexico (González-Solís et al., 2002; González-Solís & Tuz-Paredes, 2007), earlier Argáez-García et al. (2010) elaborated a detailed contribution list of just internal (intestinal) parasites of Lutjanus griseus at the Yucatán region. In our study 17 parasite species were found and Argáez-García et al. (2010) reported 20 helminth species at the Yucatán Peninsula, therefore both of the community parasite composition are similar, nevertheless, our present study in Mecocacan, Tabasco reports new taxonomical groups, such as: Myxozan in the wet season (33.3 %), and ectoparasites Euryhaliotrema griseus and E. fastigatum in both seasons both with the highest prevalence in the wet seasons (100 %). Our study has increased the knowledge of parasites presence with new records for Lutjanus griseus in the the Gulf of Mexico.

The monogenean species E. fastigatum and E. griseus showed high levels of infection and are dominant, both for the dry season and the rainy season. This is because monogeneans are highly host-specific and have a direct life cycle where one free swimming larva called oncomiracidium must infect a host to complete its life-cycle. It is so that when the fish move in the middle, it can acquire a large quantity of these parasites, as they have specialized hooks that they use to adhere and survive in their host. It is worth mentioning that temperature is considered as the main abiotic factor that regulates the dynamics of monogeneans (Tinsley & Jackson, 2002; Soler-Jiménez & Fajer-Ávila, 2012; Ogawa, 2014). In the lagoon, warm waters are maintained (24 ° to 32 ° C) with an average of 26 ° C (García-Cubas et al., 1990). In the present study, the average condition factors were 1.34 in dry and 1.55 in rain season, which indicate that, on average, they presented healthy condition. Bashirullah (1975) determined that the average condition factor of

L. griseus is 1.51 in males and 1.48 in females. In this study the fish presented good condition, it is a factor that statistically had no relationship with the parasitic load. Muñoz and Delorme (2011) pointed out that there is a relationship between the size of the fish and the parasite load, and that larger fish provide a greater contact surface for the parasites, and this is how the probability of encounter between the parasites increases. However, in the present study there was no correlation between the total length of the fish and the abundance of parasites. One factor that could influence these results are the total length of the fish that were reviewed in this study (12 – 29.2 mm) and that they can reach sizes greater than 40 cm (Castro-Aguirre et al., 1999). On the other hand, Samano-Zapata et al. (1998) studied that snappers increase in size, and also increasing diversity and volume of food in the coastal lagoons. This condition may explain the similarity in prevalence and mean abundance values for parasite species in specimens from other previous report in coastal lagoons (González-Solís et al., 2007; Argáez-García et al., 2010) as well as the increase in parasite species richness for specimens.

In the Acanthocephala group, the adults of Neoechinorhynchus are usually found in the intestine of freshwater and brackish water fish (Pinacho-Pinacho et al., 2014). These authors also reported low prevalence indicating probably an accidental infection of the specimens from eleotrif fishes in coastal lagoons across the Gulf of Mexico. In the comparison with intestinal parasites the prevalence is similar with our results and in the particular case of the acanthocephala and cestoda group the prevalence was very low (3 %) in the dry season and non-existing in the wet season. Argáez-García et al. (2010) also reported the presence of only of Tetraphyllidae organisms, in our study we reported the presence also the Pseudophyllidea individuals (3 %). The low prevalence may be an indicator of an accidental infection; these results justify further research.

Although, the latest authors mentioned that the helminth fauna of the gray snapper is replaced by new species after fish leave coastal lagoons, in our results show an addition of species for specimens from this lagoon in the same way, nematodes species found in fish from the Mecoacán lagoon system in Tabasco, Mexico were also present in specimens from others coastal lagoon in Quintana Roo according with Argáez-García et al. (2010). Perhaps the most reasonable hypothesis according these authors is that the gray snapper specimens sampled offshore are subject to rather slow replacement process of parasite species.

The parasite transmitted to humans by animals is known as zoonosis (Beaver et al., 1984). In particular, those infected by the intake of raw fish meat are called ichthyozoonosis. In the present work, it was found that species representing the group of nematodes may generate public health problems, particularly the species: Contracaecum sp. type 1 and 2, and Pseudoterranova sp., which belong to the Anisakidae family, among these parasites are known to have zoonotic importance. Rojas-Sánchez et al. (2014) point out that of the almost 100 known ichthyozoonosis worldwide, 12 have been recorded in Mexico that could affect humans. Anisakiasis, caused by members of the Anisakidae family to which Contracaecum sp type 1 and 2 reported in this study and gnathostomiasis, caused by members of the genus Gnathostoma sp, are the two most frequent cases. Therefore, the habit of eating raw fish, such as ceviche and sushi, or insufficiently cooked fish should be avoided. Monogeneans are ectoparasites that cause problems in aquaculture (Whittington, 2005). This study recorded two species of genus Euryhaliotrema (E. griseus and E. fastigatum), with the highest values of intensity, prevalence, and mean abundance, which is consistent with that previously reported for this fish species from the Venezuela coasts (Zambrano et al., 2003). In that study, a species of Euryhaliotrema with relatively high values of prevalence, intensity, and mean intensity was also reported, and it was suggested that due to the fragility of the parasitized organ (gills) these ectoparasites could eventually represent a serious problem for L. griseus in captivity (Zambrano et al., 2003).