SciELO - Scientific Electronic Library Online

 
vol.46 número4Quantifying the morphology of key species caught in the southern Brazilian penaeid-trawl fishery as a precursor to improving selectionThe larval development from prezoea to megalopa and juvenile stages of Allopetrolisthes punctatus (Guérin, 1835) (Decapoda, Anomura, Porcellanidae) índice de autoresíndice de materiabúsqueda de artículos
Home Pagelista alfabética de revistas  

Servicios Personalizados

Revista

Articulo

Indicadores

Links relacionados

  • En proceso de indezaciónCitado por Google
  • No hay articulos similaresSimilares en SciELO
  • En proceso de indezaciónSimilares en Google

Compartir


Latin american journal of aquatic research

versión On-line ISSN 0718-560X

Lat. Am. J. Aquat. Res. vol.46 no.4 Valparaíso set. 2018

http://dx.doi.org/10.3856/vol46-issue4-fulltext-18 

Research Article

Feeding habits of the mojarras (Gerreidae) population in the hyperhaline lagoon system of Ría Lagartos, Yucatan, Mexico

Ariel Adriano Chi-Espínola1 

María Eugenia Vega-Cendejas1 

Walter Gabriel Canto-Maza1 

1Laboratorio de Taxonomía y Ecología de Peces, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad Mérida, Yucatán, México

ABSTRACT

The trophic preferences and ontogenic variations were evaluated and compared between five species of mojarras collected bimonthly for two years (2004-2005) in the hyperhaline lagoon system of Ría Lagartos, Yucatan Peninsula. A total of 361 specimens corresponding to Eucinostomus argenteus, Eucinostomus gula, Eucinostomus harengulus, Eugerres plumieri and Diapterus auratus were collected and used for trophic analysis. The trophic components were analyzed using the Relative Importance Index (RII) and multivariate analysis. The mojarras were defined as second-order consumers, feeding on microcrustaceans (amphipods, copepods, tanaidaceous, ostracods) and significant amounts of detritus with variations in the proportion and frequency of different types of food according to their ontogeny and food availability. Three species shared the same resources. However, differences were observed at the general and ontogenetic level, avoiding inter and intraspecific competition. Results provide evidence of the importance of these coastal habitats for the trophic requirements of marine-euryhaline juvenile fish species.

Keywords: mojarras; stomach content; food preferences; Ria Lagartos; Yucatán

INTRODUCTION

Coastal lagoons are highly productive systems regarding matter, energy and are an important source of food and resources for their biotic components (Prado et al., 2013). One of these components is the fish that participate actively in the processes of transformation, conduction, exchange, storage and regulation of the energy that flows in the system (Abascal-Monroy et al., 2016), which to some extent determine the size of the populations, speed of growth and living conditions of the fish (Mouillot et al., 2007). Due to these characteristics, several studies have been carried out contributing to the bio-ecological knowledge of representative families in these ecosystems. One of these is the analysis of stomach contents, which help us to understand and predict trophic relationships and energy flow between populations, so that these interrelations tend to define the ecological role of the organisms belonging to the ecosystem (Bondavalli & Bodini, 2014; Salcido-Guevara & Arreguín-Sánchez, 2014). However, these feeding habits may be different even in the same species depending on factors such as food availability, seasonality, age and/or sex (Chi-Espínola & Vega-Cendejas, 2016).

The distribution of food resources among fish that coexist in the same place has been studied extensively (Braga et al., 2012; Chi-Espínola & Vega-Cendejas, 2013) but few studies described the ontogenetic changes in the diet, even if it is a very common fish in the area (Ellioth & Hemingway, 2002). This variation in diet can be attributed to external or internal influences of the environment (Clark & Pessanha, 2014) availability of prey (Whitehouse et al., 2017), or just because of the increase in energy required for growth and metabolic activities (Specziár & Eros, 2014).

The Gerreidae family has very abundant species in the coastal lagoons, where they form large shoals and feed mainly on benthic organisms. Its commercial importance lies in the use of bait for the sustenance of fishery resources in both local and artisanal fisheries (Araújo & Santos, 1999), without forgetting its biological importance as part of the structure and function of coastal ecosystems in tropical regions and subtropics of the world (González-Acosta et al., 2007). However, despite its biological, ecological, and economic importance, information on its feeding habits is insufficient in a hyperhaline lagoon system with the status of a Biosphere Reserve.

Based on the above, the present research was carried out under the hypothesis that the trophic structure of five species of the Gerreidae family; Eucinostomus argenteus (Bair & Girard, 1855), Eucinostomus gula (Quoy & Gaimard, 1824), Eucinostomus harengulus, (Goode & Bean, 1879), Eugerres plumieri (Cuvier, 1830) and Diapterus auratus (Ranzani, 1842), have variations in its diet both intraspecific and interspecific. With this information, it will be possible to contribute to the functional knowledge of this hyperhaline ecosystem in conservation status and to establish management strategies for future protected areas.

MATERIALS AND METHODS

Study area

The coastal lagoon of the Ría Lagartos Reserve is located in the far east coast of the state of Yucatan between 21°26’-21°38’N and 87°30’-88°15’W, it covers an area about 9,371 ha, a width of 0.25 to 3.5 km; a depth that varies between 0.5 to 3 m and a length of 80 km. Three seasonal climates represent the climate regime: dry (March to June), rainy (July to October) and northern (November to February) (Herrera-Silveira & Ramírez-Ramírez, 1997), the average annual temperature is 22°C. Considering its geomorphology, it has three basins, Ría Lagartos, Las Coloradas, and El Cuyo (INE, 1999). The system presents diverse types of substrates (sand, silt, and clay) and a marked salinity (Valdés-Lozano & Real-De León, 2004), with an internal zone of 4 to 5 times higher than seawater (>100) (Vega-Cendejas & Hernández de Santillana, 2004, Peralta-Meixueiro & Vega-Cendejas, 2011).

Sampling

Six samplings were carried out (October and December 2004, February, April, June and August 2005) that covered the three climatic seasons of the region (dry, rainy and northerly) through 30 sites distributed throughout the system (Fig. 1), the fishing gear used was a 15 m long beach seine with 1.5 m fall and one inch of mesh size. The individuals collected were injected with 10% formaldehyde in the abdominal cavity for the preservation of the stomach contents, and later they were placed in plastic bags labeled for their transfer.

Figure 1 Location of sampling sites in Ría Lagartos coastal lagoon, Yucatan. 

Data analysis

The components of the diet were analyzed by numerical percentage (Nr), gravimetric (Gr), frequency of occurrence (FO) proposed by Chavance et al. (1983) and the Relative Importance Index (RII) developed by Pinkas et al. (1971) and modified by Yañez-Arancibia et al. (1985). The gravimetric corresponds to the weight of each component using an analytical balance, and the frequency of occurrence (FO) to count the times a given prey appears in the stomach content of the group of fish (NE) expressed as a percentage FO = (n×NE-1)×(100)] (Tresierra-Aguilar & Culquichicón-Malpica, 1995). Finally, the RII unifies the percentage values of the area and weight with the frequency of occurrence [RII = (Nr +Gr)×FO]. Food was classified as preferential (FO >50%), secondary (50% > FO > 10%) and accidental (FO <10%) based on FO values (Yañez-Arancibia et al., 1976).

A cluster analysis was developed using the RII matrix of the food components against the species of study, applying the similarity index of Bray & Curtis (1957) using the PAST statistical package (Hammer et al., 2001). A cut line was arbitrarily applied to 0.6 to define the size of the groups (Herrera-Moreno, 2000).

A canonical correspondence analysis (CCA) was carried out (TerBraak & Smilauer, 2002) using the matrix of preferential and secondary diets against the presence of the species of fish, however incidental prey and size were included as covariates. The Monte Carlo test was performed to determine if the measured variables have significance in the study (Kupschus & Tremain, 2001). For this analysis, the statistical package CANOCO 4.5 was used.

The ontogenetic analysis of the diet was analyzed by means of the Sturges rule (Sturges, 1926) which divides the categories of the sizes based on the standard length of the specimens collected (Table 1) (Class interval = maximum size - minimum size/number of classes), where number of classes = 1+ (3.3 log n).

Table 1 Class intervals generated by the Stages’ rule for standard length (Ls) (cm) of the fish species, where occurrence frequency is indicated in brackets. 

Species/class A B C D E F G H
E. argenteus 2,2-3,2 (16) 3,3-4,2 (38) 4,3-5,2 (29) 5,3-6,2 (26) 6,3-7,2 (14) 7,3-8,2 (8)
E. gula 2,5-3,2 (5) 3,3-3,9 (16) 4,0-4,6 (15) 4,7-5,3 (22) 5,4-6,0 (19) 6,1-6,7 (4) 6,8-7,4 (5) 7,5-8,1 (2)
E. harengulus 2,7-3,3 (3) 3,4-3,9 (6) 4,0-4,5 (2) 4,6-5,1 (4) 5,2-5,7 (4) 5,8-6,3 (6) 6,4-6,9 (5) 7,0-7,5 (3)
E. plumieri 4,1-5,1 (8) 5,2-6,1 (10) 6,2-7,1 (17) 7,2-8,1 (6) 8,2-9,1 (2) 9,2-10,1 (2) 10,2-11,1 (2)
D. auratus 2,5-3,3 (11) 3,4-4,1 (11) 4,2-4,9 (17) 5,0-5,7 (18) 5,8-6,5 (1) 6,6-7,3 (2) 7,4-8,1 (1)

RESULTS

Trophic structure

A total of 382 stomach contents of the Eucinostomus argenteus species (142 specimens), Eucinostomus gula (93), Eucinostomus harengulus (36), Eugerres plumieri (49) and Diapterus auratus (62) were analyzed. The 15% of the total stomachs were full, 52% contained some kind of food, and 33% contained very little food. The species with empty stomachs were Eucinostomus argenteus (11), Eucinostomus gula (5), Eucinostomus harengulus (2), Eugerres plumieri (2) and Diapterus auratus (1).

We identified 67 food items belonging to 26 trophic categories. The amphipod, copepod, tanaidaceous and polychaete trophic groups being the preferential food (FO >50%) in at least three of the species studied; and the foraminifera, ostracods and UOM (unidentified organic matter) were present preferentially in some of the species analyzed (E. harengulus, E. plumieri and D. auratus). The highest RII values in most of the species corresponded to amphipods, copepods, tanaidaceous, ostracods, foraminifera, polychaetes and bivalves (Table 2).

Table 2 Food items Frequency of Occurrence (FO) and percent of Relative Importance Index (RII) of family Gerreidae species in coastal lagoon in Ría Lagartos coastal lagoon, Yucatan, Mexico. 

N° Species Eucinostomus argenteus Eucinostomus gula Eucinostomus harengulus Eugerres plumieri Diapterus auratus
131 88 33 47 61
Phytoplankton (Gr FO %Gr RII %RII) (Gr FO %Gr RII %RII) (Gr FO %Gr RII %RII) (Gr FO %Gr RII %RII) (Gr FO %Gr RII %RII)
1. Bacillariophyceae 0.0 14.5 0.6 12.9 0.1 0.0 31.8 0.6 33.6 0.3 0.0 29.2 0.6 32.0 0.2 0.0 32.8 0.7 49.5 0.4
2. Cyanophyceae 0.0 3.1 0.2 0.7 0.0 0.0 3.4 0.4 2.8 0.0 0.0 2.1 0.0 0.0 0.0
Macrophytes
3. Unident, algae 0.0 4.6 0.3 2.1 0.0 0.0 3.4 0.6 3.8 0.0
4. Unident, seagrass 0.1 16.8 1.1 29.0 0.3 0.0 20.5 1.1 48.8 0.5 0.1 27.3 0.8 72.7 0.9 0.1 31.3 1.4 94.8 0.7 0.0 6.6 0.2 1.8 0.0
Protozoa
5. Dinoflagellida 0.0 1.5 0.1 0.3 0.0 0.0 2.3 0.0 0.1 0.0 0.0 4.2 0.0 0.1 0.0
6. Foraminifera 0.1 33.6 1.3 89.8 0.9 0.0 21.6 0.3 17.5 0.2 0.0 *72.7 0.2 133.8 1.6 0.2 *72.9 2.6 405.1 3.1 0.1 44.3 1.7 169.7 1.5
Porifera
7. Sponge spicules 0.0 3.4 0.1 0.9 0.0 0.0 3.0 0.0 0.1 0.0 0.0 1.6 0.0 0.1 0.0
Nematoda
8. Nematoda 0.0 20.6 0.4 23.1 0.2 0.0 14.8 0.5 24.6 0.2 0.0 18.2 0.0 9.1 0.1 0.0 20.8 0.3 11.2 0.1 0.1 23.0 1.8 110.0 0.9
Annelidae
9. Polychaeta 1.8 *59.5 27.6 2208.2 22.4 0.8 *69.3 20.1 2784.0 27.2 6.9 36.4 51.8 2686.7 32.0 0.1 18.8 2.2 95.4 0.7 0.1 6.6 2.0 25.3 0.2
10. Oligochaeta 0.0 3.8 0.5 3.0 0.0 0.0 2.3 0.1 0.5 0.0 0.0 2.1 0.4 1.1 0.0 0.0 1.6 0.3 1.1 0.0
Echiuridae
11. Echiuridae 0.1 11.4 2.3 63.3 0.6
Mollusca
12. Bivalvia 0.0 7.6 0.7 8.1 0.1 0.0 3.4 0.2 1.3 0.0 0.3 9.1 2.2 24.1 0.3 0.2 16.7 2.5 83.7 0.6 0.0 3.3 0.1 0.6 0.0
13. Gastropoda 0.0 6.9 0.5 5.4 0.1 0.1 15.9 1.8 64.9 0.6 0.0 3.0 0.0 0.3 0.0 0.2 18.8 2.4 93.4 0.7 0.0 6.6 0.6 10.9 0.1
Crustacea
14. Amphipoda 1.3 *66.4 18.9 2047.5 20.8 0.8 *61.3 21.5 2597.8 25.4 0.2 *63.6 1.8 1227.6 14.6 2.6 *97.9 39.3 7848.9 60.7 1.4 *75.4 41.3 6311.7 54.0
15. Copepoda 0.3 48.1 4.2 350.9 3.6 0.4 *63.6 9.3 1014.2 9.9 0.0 33.3 0.3 151.6 1.8 0.4 *89.5 6.3 1219.2 9.4 0.4 *88.5 12.7 2396.5 20.5
16. Ostracoda 0.1 32.8 1.6 96.8 1.0 0.0 20.5 1.2 59.1 0.6 0.0 42.4 0.0 67.8 0.8 0.5 41.7 7.5 590.8 4.6 0.4 *63.9 11.9 1900.4 16.3
17. Cummacea 0.0 3.1 0.3 1.3 0.0 0.0 4.5 0.3 2.5 0.0 0.1 6.3 0.8 8.1 0.1 0.0 1.6 0.1 0.3 0.0
18. Mysidacea 0.0 4.6 0.7 5.5 0.1 0.0 3.4 0.3 4.4 0.0 0.0 3.0 0.0 0.1 0.0 0.1 10.4 2.0 37.6 0.3 0.1 14.8 1.7 50.2 0.4
19. Isopoda 0.0 2.3 0.1 0.5 0.0 0.1 9.1 1.5 26.9 0.3 0.0 9.1 0.1 6.6 0.1
20. Tanaidacea 0.9 *55.7 14.1 1368.7 13.9 0.6 *59.0 15.0 1770.2 17.3 3.6 *57.5 27.3 2575.6 30.7 0.5 *52.0 7.5 837.2 6.5 0.1 23.0 2.5 133.7 1.1
21. Decapoda 0.1 7.6 0.8 32.6 0.3 0.1 21.6 3.9 151.2 1.5 0.1 12.1 0.8 103.1 1.2 0.0 4.2 0.6 5.1 0.0 0.0 8.2 0.6 12.5 0.1
Insecta
22. Insect 0.1 13.7 2.1 68.3 0.7 0.0 1.1 0.2 0.4 0.0 0.0 9.1 0.2 22.6 0.3 0.0 4.2 0.8 6.0 0.0 0.2 19.7 4.5 174.2 1.5
Fish
23. Fish 0.0 6.1 0.5 5.0 0.1 0.0 1.1 0.0 0.1 0.0 0.0 6.1 0.0 0.9 0.0 0.0 2.1 0.0 0.1 0.0 0.4 13.1 12.1 165.5 1.4
Detritus
24. Detritus 1.1 45.8 17.2 2837.5 28.8 0.4 45.5 11.2 1008.3 9.9 1.7 18.2 12.6 353.4 4.2 1.2 39.6 18.9 1372.3 10.6 0.1 19.7 2.2 78.9 0.7
UOM
25. UOM 0.4 48.1 6.5 650.0 6.6 0.2 39.8 6.3 515.5 5.0 0.2 *60.6 1.6 952.5 11.3 0.3 22.9 3.9 178.3 1.4 0.1 18.0 1.9 72.5 0.6
Others
26. Others 0.1 8.0 1.4 23.0 0.2 0.0 6.1 0.2 6.7 0.1 0.0 8.2 0.9 18.5 0.2

(*)Corresponds to preferential food (FO > 50 %). The number 0,0 corresponds to very low values.

UOM: Unidentified organic matter.

Similarity analysis

Regarding the cluster analysis and using the Bray-Curtis similarity index, three groups were obtained by applying a cut line of 60%. The first group corresponded to the species E. argenteus and E. gula, the second to E. harengulus and E. plumieri, and finally, the third group conformed solely with D. auratus (Fig. 2).

Figure 2 Trophic similarity dendrogram of the Bray-Curtis index (1957) among species of the Gerreidae family registered in Ría Lagartos. 

Variation in the trophic structure

The canonical correspondence analysis (CCA), reflects the general food trend of the species in the ecosystem, therefore the three representatives of the genus Eucinostomus, had a higher preference for the consumption of tanaidaceous, UOM and detritus, while D. auratus was related with the consumption of nematodes and ostracods, and finally E. plumieri consumed amphipods preferentially (F = 21.22, P = 0.002) (Fig. 3).

Figure 3 Biplot of CCA sorting of the preferential and secondary food resources registered with the fish species of the Gerreidae family, using sizes and accidental food as covariables. 

Trophic ontogeny

The diet of sizes A and B of E. argenteus consist mainly of amphipods. However, with the increase in size (>C) the consumption of amphipods is reduced and replaced by tanaidaceous, annelids and detritus. On the other hand, E. gula consumes copepods and annelids, which grow (>D) to include tanaidaceous and detritus. In the diet of E. harengulus, amphipods were present in sizes A to E. Annelids, tanaidaceous, and UOM being the main diet of sizes F to H. The main component of the trophic spectrum of E. plumieri in the sizes A to D are the amphipods, copepods and tanaidaceous, however in the later sizes (>E), detritus and ostracods were part of their main diet. In sizes A to C of D. auratus, ostracods and copepods were the major components of their diet, although subsequently, amphipods form their dominant diet (Fig. 4).

Figure 4 Percent Relative Importance Index (%RII) of the stomach contents of the Gerreidae family species, where the x-axis corresponds to the size category generated by the Sturges’ rule. 

DISCUSSION

The family Gerreidae was very abundant species in Ría Lagartos coastal lagoon (Vega-Cendejas & Hernández de Santillana, 2004; Peralta-Meixueiro & Vega-Cendejas, 2011). According to the present study, this family consumes a wide variety of food items (67). Therefore, this high density, abundance, and distribution of prey could favor the coexistence of related species and therefore minimize interspecific competition for food resources (Vinagre et al., 2005) among the species captured.

In the analysis of the diet of E. argenteus, E. gula, E. harengulus, E. plumieri and D. auratus, consumption of the same prey was observed, but with evident variations in the proportion and frequency of the food items. This variation is possibly the result of a series of morphological, physiological and behavioral adaptations. It allowed them to reduce inter and intraspecific competition for food (Arenas-Granados & Acero, 1992), or as mention by Pereira et al. (2004) it is a reflection of the availability of resources or a wide range of dietary strategies that allow them to exploit the variety of resources available. Consequently, the species of the Gerreidae family possess a characteristic mandibular morphology, this is a mechanism of pressure suction (Nelson, 2006), which allows them to feed on a great variety of prey on the surface of the substrate (Cyrus & Blaber, 1982). However, in this study the volume of detritus consumed is large, this may be due to the voracity of the fish when capturing the prey. Although the detritus is accidentally consumed, an important amount of benthic invertebrates, bacteria, protozoa and organic matter are obtained from it (Laegdsgaard & Johnson, 2001; Gning et al., 2008). On the other hand, the high incidence of UOM in E. harengulus could reflect the high degree of digestion of the prey.

The analysis of similarity showed a distribution of food resources according to the genus (Eucionostomus, Diapterus, and Eugerres), behavior that can be closely related to the type of habitat, where they are developed (Pereira et al., 2004; Russo et al., 2008), the feeding habit (Bacha & Amara, 2009) or the increase in size possibly allowed them to consume larger prey to compensate their metabolic requirements (Wootton, 1990, Hammerschlag et al., 2010).

With the ACC it was possible to validate the grouping among the three species of the genus Eucinostomus (E. argenteus, E. gula, and E. harengulus), which obtained a high correlation with the consumption of tanaidaceous, detritus and UOM; apparently this genus has a broad diet range consisting of benthic invertebrates such as polychaetes, copepods, tanaidaceous, mollusks (Odum & Heald, 1972; Hofling et al., 1998; Denadai et al., 2012; Almeida et al., 2014; Pessanha & Araújo, 2014) and ostracods as the main diet (Santos & Araújo, 1997; Gning et al., 2010). It could be an indication that the genus Eucinostomus presents an opportunistic trophic behavior since it consumes prey items available and abundant in the environment (Denadai et al., 2012).

On the other hand, the ACC in Eugerres plumieri indicated a high correlation with the consumption of amphipods. This diet has also been reported by Aguirre-León & Díaz-Ruiz (2000) in Términos Lagoon. However, in other studies (Aguirre-León & Yáñez-Arancibia, 1986; López-López et al., 1991; Arenas-Granados & Acero, 1992) the use of different food categories such as ostracods, foraminifera, tanaidaceous, and copepods has been documented, which were part of the secondary food in the present study. Possibly the high incidence of amphipods in the diet of E. plumieri, as well as in the other species of gerrids in the present study the studies, is a reflection of the high abundance of this resource in the lagoon of Ría Lagartos and adjacent areas (Pech et al., 2007; Kuk-Dzul et al., 2012).

The ACC on Diapterus auratus showed a very strong correlation with ostracods and nematodes, although, the trophic information on this species is null, the diet of the genus Diapterus has been widely studied in the estuaries of Brazil where a high incidence of polychaetes is reported, amphipods, ostracods, copepods, mollusks (Denadai et al., 2012; Ramos et al., 2014), nematodes and algae (Pessanha & Araújo, 2014; Almeida-Silva et al., 2015). Also, in the Pom-Atasta system in Mexico, Diapterus sp. feeds on foraminifera, ostracods, and tanaidaceous (Aguirre-León & Díaz-Ruiz, 2000). The occurrence of undigested nematodes in the stomach contents were considered as parasites (Denadai et al., 2012), so their registration and correlation with D. auratus are not considered as part of their trophic spectrum. However, this data can be a starting point for the study of the parasitic incidence in the species.

In the vast majority of studies, polychaetes have been the main prey in Gerridae species (Cyrus & Blaber, 1982; Arenas-Granados & Acero, 1992; Branco et al., 1997; Hofling et al., 1998; Denadai et al., 2012; Pessanha & Araújo, 2014). However, in the present work, it was only an accidental element. Although the absence of this group could be related given its low tolerance to salinity (Nicolaidou et al., 2006; Pech et al., 2007), granulometric characteristics of the sediment, or the presence of organic matter in it (Beukema & Flach, 1995; Pech et al., 2007), conditions that restrict its abundance in this hyperhaline coastal lagoon.

Although, E. argenteus and E. gula exhibited a similar diet, both general and by sizes, competition for food is limited due to its distribution in the lagoon according to the salt gradient, where E. argenteus is distributed to the inner zone of the lagoon (hyperhaline condition), contrary to E. gula that is limited to the inlet and intermediate (Vega-Cendejas & Hernández de Santillana, 2004; Peralta-Meixueiro & Vega-Cendejas, 2011). Their diets have been reported in the region of Celestun, Yucatan, where microcrustaceans such as copepods and amphipods were significant items (Arceo-Carranza et al., 2013), in Términos Lagoon they consume algae and detritus (Pineda-Peralta et al., 2016) or in other regions (Branco et al., 1997; Bouchereau & Chantrel, 2009), which report microcrustaceans as the main diet. Ontogenetically, a change was observed in the food consumed, where small fish feed on microcrustaceans present in the water column and as the size increases, the diet changes on benthic organisms (Pereira et al., 2004; Vega-Cendejas et al., 2012).

The ontogenetic analysis of E. plumieri recorded a wide trophic range with a marked consumption of amphipods through sizes A to C. Possibly reflecting the high abundance of these invertebrates, rather than a dietary preference (Kuk-Dzul et al., 2012). Later, in sizes E to G, higher consumption of detritus and ostracods was observed, elements that have been reported in other coastal systems (López-López et al., 1991; Aguirre-León & Díaz-Ruiz, 2000). It has been observed that the ontogenetic variation of E. plumieri depends on the environmental conditions during its development (Aguirre-León & Díaz-Ruiz, 2000) since it uses transparent waters, low salinity and availability of organic matter (Aguirre-León & Yáñez-Arancibia, 1986; Rueda, 2001), which was observed in the present study.

Like the other species, the diet of D. auratus was based mainly on microcrustaceans; however, it presented a higher consumption of copepods and ostracods in sizes A to C, and amphipods in sizes D to G. These elements have been reported previously forming an important part of the diet of these mojarras (López-López et al., 1991; Arenas-Granados & Acero, 1992; Franco-López et al., 2011; Almeida-Silva et al., 2015). It has been observed that the organisms of the genus Diapterus use different environments adjacent to the coastal lagoons to complete their life cycle (Aguirre-León & Díaz-Ruiz, 2006; Ramos et al., 2014). In this regard, Pessanha & Araújo (2012), establishes that this selection of habitats is related to the abundance of the prey and the obtaining of the food in a minimum time (optimal foraging theory) (Griffits, 1975), since there is a higher preference on sedentary organisms like ostracods, or of easy capture as zooplankton or benthic organisms such as copepods and amphipods.

It is important to mention that in this work no individuals were analyzed in the adult stage, and the diet could not be compared with larger individuals. On the other hand, there are reports of Eucinostomus melanopterus, Gerres cinereus, and Diapterus rhombeus in this lagoon (Vega-Cendejas & Hernández de Santillana, 2004; Peralta-Meixueiro & Vega-Cendejas, 2011), they were not included in the analyzes by its low capture frequency.

With these results, it can be inferred that mojarras species use the same food resources. However, it is a fact that these resources are exploited in different situations, reducing the overlap or competition between them, being a reflection of the feeding strategies as well as the availability of food (Xie et al., 2000). On the other hand, these fish in their first sizes are omnivorous and generalist, but as they increase in size, they become more selective and specialized, as observed in the works of Aguirre-León & Díaz-Ruiz (2000); Franco-López et al. (2011) or Pineda-Peralta et al. (2016). For this reason, these ontogenetic changes in juvenile fish are essential for understanding the ecology of fish (Schreck & Moyle, 1990).

ACKNOWLEDGMENTS

To Mirella Hernández de Santillana for her valuable help in the collection and identification of the samples, Alex Acosta for his technical support in the laboratory. Finally, we would like to express our thanks to the anonymous group of reviewers for their comments and suggestions on the document. The captures made during the study were from the project "Contribution to the ichthyofaunal wealth of the reserve of Ría Lagartos, Yucatán”, with reference number BK026, financed by CONABIO.

REFERENCES

Abascal-Monroy, I.M., M.J. Zetina-Rejón, F. Escobar-Toledo, G.A. López-Ibarra, A. Sosa-López & A. Tripp-Valdez. 2016. Functional and structural food web comparison of Términos Lagoon, Mexico in three periods (1980, 1998, and 2011). Estuar. Coast., 39: 1282-1293. [ Links ]

Aguirre-León, A. & S. Díaz-Ruiz. 2000. Population structure, gonadal maturity and feeding habits of Eugerres plumieri (Gerreidae) in the Pom-Atasta fluvial-deltaic system, Mexico. Cienc. Mar., 26: 253-273. [ Links ]

Aguirre-León, A. & S. Díaz-Ruiz. 2006. Size structure, gonadic development and diet of the fish Diapterus rhombeus (Gerreidae) in the Pom-Atasta fluvial-deltaic system, Campeche, Mexico. Rev. Biol. Trop., 54: 599-611. [ Links ]

Aguirre-León, A. & A. Yáñez-Arancibia. 1986. Las mojarras de la Laguna de Términos, Campeche: taxonomía, biología, ecología y dinámica trófica (Pisces: Gerreidae). An. Centro Cienc. Mar. Limnol. UNAM, 13: 366-444. [ Links ]

Almeida, J.R., C. Gravato & L. Guilhermino. 2014. Effects of temperature in juvenile seabass (Dicentrarchus labrax) biomarker responses and behaviour: implications for environmental monitoring. Estuar. Coast., 38: 45-55. [ Links ]

Almeida-Silva, P., R.A. Tubino, L.C. Zambrano, D.A. Hunder, S.R. Garritano & C. Monteiro-Neto. 2015. Trophic ecology and food consumption of fishes in a hypersaline tropical lagoon. J. Fish Biol., 86: 1781-1795. [ Links ]

Amos, W.H. & S.H. Amos. 1985. Atlantic and gulf coasts. The Audubon Society Nature Guides, Alfred A. Knopf, New York, 670 pp. [ Links ]

Araújo, F.G. & A.C. Santos. 1999. Distribution and recruitment of mojarras (Perciformes, Gerreidae) in the continental margin of Sepetiba Bay, Brazil. Bull. Mar. Sci., 65: 431-439. [ Links ]

Arceo-Carranza, D., M.E. Vega-Cendejas & M.J. Hernández de Santillana. 2013. Day and night trophic variations of dominant fish species in a lagoon influenced by freshwater seeps. J. Fish Biol., 82: 54-68. [ Links ]

Arenas-Granados, A. & P. Acero. 1992. Organización trófica de las mojarras (Pisces: Gerreidae) de la ciénaga Grande de Santa Marta (Caribe colombiano). Rev. Biol. Trop., 40: 325-334. [ Links ]

Bacha, M. & R. Amara. 2009. Spatial, temporal and ontogenetic variation in diet of anchovy (Engraulis encrasicolus) on the Algerian coast (SW Mediterranean). Estuar. Coast. Shelf Sci., 85: 257-264. [ Links ]

Beukema, J.J. & E.C. Flach. 1995. Factors controlling the upper and lower limits of the intertidal distribution of two Corophium species in the Wadden Sea. Mar. Ecol. Prog. Ser., 125: 117-126. [ Links ]

Bondavalli, C. & A. Bodini. 2014. How interaction strength affects the role of functional and redundant connections in food webs. Ecol. Complex., 20: 97-106. [ Links ]

Bouchereau, J.L. & J. Chantrel. 2009. Régime alimentaire de trois gerreidés et d'un sciaenidé dans une lagune à mangrove antillaise. Cybium, 33: 179-191. [ Links ]

Braga, R.R., H. Bornatowski & J.R.S. Vitule. 2012. Feeding ecology of fishes: an overview of worldwide publications. Rev. Fish. Biol. Fish., 22: 915-929. [ Links ]

Branco, C.W., T. Aguiaro, F.A. Esteves & E.P. Caramaschi. 1997. Food sources of the teleost Eucinostomus argenteus in two coastal lagoons of Brazil. Stud. Neotrop. Fauna Environ., 32: 33-40. [ Links ]

Bray, J.R. & J.T. Curtis. 1957. An ordination of the upland forest communities of southern Wisconsin. Ecol. Monogr., 27: 325-349. [ Links ]

Carpenter, K.E. 2002. The living marine resources of the western Central Atlantic. Volume 3: Bony fishes. Part 2 (Opistognathidae to Molidae), sea turtles and marine mammals. Food and Agriculture Organization, Rome, 2127 pp. [ Links ]

Chavance, P., D. Flores-Hernández, A. Yáñez-Arancibia & F. Amezcua-Linares. 1983. Ecología, biología y dinamica de las poblaciones de Bairdiella chrysoura en la laguna de Términos, sur del Golfo de México. (Pisces: Sciaenidae). An. Centro Cienc. Mar. Limnol. UNAM, 11: 123-162. [ Links ]

Chi-Espínola, A.A. & M.E. Vega-Cendejas. 2013. Hábitos alimenticios de Sphoeroides testudineus (Perciformes: Tetraodontidae) en el sistema lagunar de Ría Lagartos, Yucatán, México. Rev. Biol. Trop., 61: 849-858. [ Links ]

Chi-Espínola, A.A. & M.E. Vega-Cendejas. 2016. Food resources of Eucinostomus (Perciformes: Gerreidae) in a hyperhaline lagoon: Yucatan Peninsula, Mexico. Rev. Biol. Mar. Oceanogr., 51: 395-406. [ Links ]

Clark, F.J. & A.L.M. Pessanha. 2014. Diet and ontogenetic shift in habitat use by Rhinosardinia bahiensis in a tropical semi-arid estuary, north-eastern Brazil. J. Mar. Biol. Assoc. U.K., 1-9. [ Links ]

Cyrus, D.P. & S.J. Blaber. 1982. Mouthpart structure and function and the feeding mechanisms of Gerres (Teleostei). S. Afr. J. Zool., 17: 117-121. [ Links ]

Denadai, M.R., F.B. Santos, E. Bessa, W.S. Fernandez, C.C. Paschoal & A. Turra. 2012. Diets of Eucinostomus argenteus (Baird & Girard, 1855) and Diapterus rhombeus (Cuvier, 1829) (Perciformes: Gerreidae) in Caraguatatuba Bay, southeastern Brazil. Panam. J. Aquat. Sci., 7: 143-155. [ Links ]

Elliott, M. & K.L. Hemingway. 2002. Fishes in estuaries. Blackwell Science, Oxford, 636 pp. [ Links ]

Franco-López, J., L.G. Abarca-Arenas, H. Barrera-Escorcia, C.M. Bedia-Sánchez & V. Rivera-Félix. 2011. Seasonal patterns of food and length-weight relationship of three species of the family Gerreidae in the Alvarado Lagoon, Veracruz, México. Res. J. Fish. Hydrobiol., 6: 59-68. [ Links ]

Gning, N., G. Vidy & O.T. Thiaw. 2008. Feeding ecology and ontogenic diet shifts of juvenile fish species in an inverse estuary: the Sine-Saloum, Senegal. Estuar. Coast. Shelf Sci., 76: 395-403. [ Links ]

Gning, N., F. Le Loc'h, O.T. Thiaw, C. Aliaume & G. Vidy. 2010. Estuarine resources use by juvenile Flagfin mojarra (Eucinostomus melanopterus) in an inverse tropical estuary (Sine Saloum, Senegal). Estuar. Coast. Shelf Sci., 86: 683-691. [ Links ]

González-Acosta, A.F., J. De la Cruz-Agüero & J.L. Castro-Aguirre. 2007. A review of the marine western Atlantic species of the genus Eugerres (Perciformes: Gerreidae). Bull. Mar. Sci., 80: 109-124. [ Links ]

Griffiths, S.D. 1975. Prey availability and food of predators. Ecology, 56: 1209-1215. [ Links ]

Hammer, Ø., D.A. Harper & P.D. Ryan. 2001. PAST: Paleontological Statistics Software Package for Education and Data Analysis [Online] Electronic paleontology. [http://palaeo-electronica.org/2001_1/past/issue1_01.htm]. Reviewed: 26 May 2017. [ Links ]

Hammerschlag, N., D. Ovando & J.E. Serafy. 2010. Seasonal diet and feeding habits of juvenile fishes foraging along a subtropical marine ecotone. Aquat. Biol., 9: 279-290. [ Links ]

Herrera-Silveira, J.A. & J. Ramírez-Ramírez. 1997. Salinity and nutrients in the coastal lagoon of Yucatan, México. Verh. Internat. Verein Limnol., 6: 1473-1478. [ Links ]

Herrera-Moreno, A. 2000. Clasificación numérica y su aplicación en la ecología. Instituto Tecnológico de Santo Domingo, República Dominicana, 91 pp. [ Links ]

Hoese, H.D. & R.H. Moore. 1998. Fishes of the Gulf of Mexico, Texas, Louisiana, and Adjacent Waters. Texas A and M University Press, College Station, Texas, 422 pp. [ Links ]

Hofling, J.C., L.I. Ferreira, F.B. Neto, A.M. Filho, P.A. Lima & T.E. Gibin. 1998. Fish alimentation of the Gerreidae family of the estuarine lagoon complex in Cananeia, São Paulo, Brazil. Rev. Bioikos, 12: 7-18. [ Links ]

Instituto Nacional de Ecología (INE). 1999. Programa de manejo de la reserva de la biosfera de Ría Lagartos. Instituto Nacional de Ecología SEMARNAP, Yucatán, 203 pp. [ Links ]

Kudo, R.R. 1980. Protozoología. Compañía Editorial Continental, México D.F., 905 pp. [ Links ]

Kuk-Dzul, J.G., G. Gold-Bouchot & P.L. Ardisson. 2012. Benthic infauna variability in relation to environmental factors and organic pollutants in tropical coastal lagoons from the northern Yucatan Peninsula. Mar. Pollut. Bull., 64: 2725-2733. [ Links ]

Kupschus, S. & D. Tremain. 2001. Associations between fish assemblages and environmental factors in nearshore habitats of a subtropical estuary. J. Fish Biol., 58: 1383-1403. [ Links ]

Laegdsgaard, P. & C. Johnson. 2001. Why do juvenile fish utilize mangrove habitats? J. Exp. Mar. Biol. Ecol., 257: 229-253. [ Links ]

Littler, D.S. & M.M. Littler. 2009. Caribbean reef plants. An identification guide to the reef plants of the Caribbean, Bahamas. Florida and the Gulf of México. Offshore Graphics, Washington, 542 pp. [ Links ]

López-López, E., M. Salgado-Mejía & A. Guzmán-Del Próo. 1991. Un análisis estacional de la ictiofauna de la laguna de Tampamachoco, Veracruz y sus hábitos alimentarios. An. Esc. Nac. Cienc. Biol. UNAM, 34: 81-107. [ Links ]

Mouillot, D., O. Dumay & J.A. Tomasini. 2007. Limiting similarity, niche filtering, and functional diversity in coastal lagoon fish communities. Estuar. Coast. Shelf Sci., 71: 443-456. [ Links ]

Nelson, J.S. 2006. Fishes of the world. John Wiley & Sons, New York, 601 pp. [ Links ]

Nicolaidou, A., K. Petrou, K. Kormas & S. Reizopoulou. 2006. Inter-annual variability of soft bottom macrofaunal communities in two Ionian Sea lagoons. In: K. Martens, H. Queiroga, M.R. Cunha, A. Cunha, M.H. Moreira, V. Quintino, A.M. Rodrigues, J. Seroôdio & R.M. Warwick (eds.). Marine biodiversity, developments in hydrobiology. Springer, Netherlands, 183: 89-98. [ Links ]

Odum, W.E. & E.J. Heald. 1972. Trophic analyses of an estuarine mangrove community. Bull. Mar. Sci., 22: 671-738. [ Links ]

Pech, D., P.L. Ardisson & N. Hernández-Guevara. 2007. Benthic community response to habitat variation: a case of study from a natural protected area, the Celestun coastal lagoon. Cont. Shelf Res., 27: 2523-2533. [ Links ]

Peralta-Meixueiro, M.A. & M.E. Vega-Cendejas. 2011. Spatial and temporal structure of fish assemblages in a hyperhaline coastal system: Ría Lagartos, México. Neotrop. Ichthyol., 9: 673-682. [ Links ]

Pereira, C.C., W.S. Smith & E.L. Espíndola. 2004. Hábitos alimenticios de nueve especies de peces del embalse de Tres Irmãos, São Paulo, Brasil. Univ. Cienc., 1: 33-38. [ Links ]

Pessanha, A.L. & F.G. Araújo. 2014. Shifts of the feeding niche along the size dimension of three juvenile fish species in a tidal mudflat in southeastern Brazil. Mar. Biol., 161: 543-550. [ Links ]

Pessanha, A.L. & F.G. Araújo. 2012. Spatial and size feeding niche partitioning of the rhomboid mojarra Diapterus rhombeus (Cuvier, 1829) in a tropical Brazilian Bay. Mar. Biol. Res., 8: 273-283. [ Links ]

Pineda-Peralta, A., J. Ramos-Miranda, M. Castillo Rivera & F. Arreguín-Sánchez. 2016. Cambios en la dieta de dos especies de mojarras (Gerreidae) en la laguna de Términos, Campeche, México. Rev. Biol. Ocenogr., 51: 385-394. [ Links ]

Pinkas, L., M.S. Oliphant & L.K. Iverson. 1971. Food habits of albacore bluefin, tuna, and bonito in California waters. Calif. Fish Game, Fish Bull., 152: 1-105. [ Links ]

Prado, P., C. Ibáñez, N. Caiola & E. Reyes. 2013. Evaluation of seasonal variability in the food-web properties of coastal lagoons subjected to contrasting salinity gradients using network analyses. Ecol. Modell., 265: 180-193. [ Links ]

Ramos, J.A., M. Barletta, D.V. Dantas, A.R. Lima & M.F. Costa. 2014. Trophic niche and habitat shifts of sympatric Gerreidae. J. Fish Biol., 85: 1446-1469. [ Links ]

Rueda, M. 2001. Spatial distribution of fish species in a tropical estuarine lagoon: a geostatistical appraisal Marine. Ecol. Prog. Ser., 222: 217-226. [ Links ]

Ruppert, E.E. & R.D. Barnes. 1996. Zoología de los invertebrados. Interamericana S.A., México D.F., 776 pp. [ Links ]

Salcido-Guevara, L.A. & F. Arreguín-Sánchez. 2014. Effects of biomass changes in the supply-demand balance of energy in aquatic food webs. Ecol. Modell., 276: 64-79. [ Links ]

Santos, A.C. & F.G. Araújo. 1997. Hábitos alimentares de três espécies de Gerreidae (Osteichthyes: Perciformes) na Baía de Septiba, R.J. Braz. Arch. Biol. Tecnol., 40: 359-368. [ Links ]

Schreck, C.B. & P.B. Moyle. 1990. Methods of fish biology. Am. Fish. Soc. Maryland, 704 pp. [ Links ]

Specziár, A. & T. Eros. 2014. Dietary variability in fishes: the roles of taxonomic, spatial, temporal and ontogenetic factors. Hydrobiologia, 1: 109-125. [ Links ]

Sturges, H.A. 1926. The choice of a class-interval. J. Am. Stat. Assoc., 21: 65-66. [ Links ]

Ter Braak, C.J. & P. Smilauer. 2002. CANOCO reference manual and CanoDraw for Windows user's guide: software for canonical community ordination (version 4.5). Microcomputer Power, New York, 500 pp. [ Links ]

Tresierra-Aguilar, A.E. & Z.G. Culquichicón-Malpica. 1995. Biología pesquera. Editorial Libertad, Trujillo, 432 pp. [ Links ]

Valdés-Lozano, D.S. & E. Real-De León. 2004. Nitrogen and phosphorous in water and sediments at Ría Lagartos coastal lagoon, Yucatán, Gulf of México. Indian J. Mar. Sci., 33: 338-345. [ Links ]

Vega-Cendejas, M.E. & M.J. Hernández de Santillana. 2004. Fish community structure and dynamics in a costal hypersaline lagoon: Rio Lagartos, Yucatan, México. Estuar. Coast. Shelf Sci., 60: 285-299. [ Links ]

Vega-Cendejas, M.E., M.J. Hernández de Santillana & D. Arceo-Carranza. 2012. Length-weight relationships for selected fish species from a coastal lagoon influences by freshwater seeps Yucatan peninsula, Mexico. J. Appl. Ichthyol., 28: 140-142. [ Links ]

Vinagre, C., S. França, M.J. Costa & H.N. Cabral. 2005. Niche overlap between juvenile flatfishes, Platichthys flesus, and Solea solea, in a southern European estuary and adjacent coastal waters. J. Appl. Ichthyol., 21: 114-120. [ Links ]

Vinyard, W.C. 1979. Diatoms of North America. Mad River Press, California, 120 pp. [ Links ]

Whitehouse, G., T. Buckley & S. Danielson. 2017. Diet compositions and trophic guilds structure of the easter Chuckchi Sea demersal fish community. Deep-Sea Res. II, 135: 95-110. [ Links ]

Wootton, R.J. 1990. Ecology of teleost fishes. Chapman & Hall, London, 392 pp. [ Links ]

Xie, S., Y. Cui, T. Zhang & Z. Li. 2000. Seasonal patterns in feeding ecology of three small fishes in the Biandantang Lake, China. J. Fish Biol., 57: 867-880. [ Links ]

Yáñez-Arancibia, A., J. Curiel-Gómez & V.L. de Yañez. 1976. Prospección biológica y ecológica del bagre marino Galeichthyes caerulescens (Gunther) en el sistema lagunar costero de Guerrero, México. (Pisces: Ariidae). An. Centro Cienc. Mar Limnol. UNAM, 3: 125-180. [ Links ]

Yáñez-Arancibia, A., A. Lara-Domínguez, A. Aguirre-León, S. Díaz-Ruiz, F. Amezcua-Linares, D. Flores-Hernández & P. Chavance. 1985. Ecología de poblaciones de peces dominantes en estuarios tropicales: factores ambientales que regulan las estrategias biológicas y la producción. In: A. Yáñez-Arancibia (ed.). Ecología de comunidades de peces en estuarios y lagunas costeras. UNAM, México D.F., pp. 311-365. [ Links ]

Received: October 07, 2017; Accepted: July 30, 2018

Corresponding author: Ariel Adriano Chi Espínola (kain_ex@hotmail.com)

Corresponding editor: Guido Plaza

Creative Commons License This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License, which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.