*Dirección para correspondencia

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Abstract

Most studies on Eugerres mexicanus ]]> E. mexicanus, based on 30 embryos and 30 larvae sampled by induced spawning of breeders, taken in February 2009 from the Usumacinta River in Tenosique, Tabasco, Mexico. All descriptions of the embryonic development were based on morphometric and meristic data and followed standard methods. Eggs, recovered at the gastrula stage, had an average diameter of 1.17mm (SD=0.08). The bud stage appeared during the first ]]> E. mexicanus were typical for the Gerreidae group. However, their morphometric characters were slightly ]]> E. mexicanus were olive and yellow on the margin of the notochord, which differs from those reported for other species. This is the first recorded report on the reproductive biology and early life development of this species.

Key words: reproduction, induction, embryo, larva, Eugerres mexicanus, Tabasco.

Resumen

La ontogenia se basó en 30 ]]> E. ]]> son típicas del período de desarrollo de los peces de la familia Gerreidae, en particular en el caso de las especies E. brasilianus y E. lineatus que habitan en ambientes marinos. Sin embargo, sus caracteres morfométricos son diferentes con respecto al diámetro y el tamaño de los huevos y de la gota de aceite, ya que en E. mexicanus son más grandes que los de las especies ]]> respecto a la pigmentación, la larva con saco de E. mexicanus presenta un olor olivo y amarillo sobre el margen del notocordio, lo cual difiere a lo reportado para E. lineatus,ya que en esta muestra un grupo de ]]>

Palabras clave: reproducción, inducción, embrión, larva, Eugerres mexicanus, Tabasco.

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Although Gerreidae are mostly marine fish, they are frequently found in estuaries, particularly near mangroves, and occasionally in continental environments (Castro et al. 1999). At least one species, Eugerres mexicanus, is confined to the freshwater environments of Southeastern Mexico and Northern Guatemala (González 2005, Miller et al. 2005, González & Rodiles 2007, González et al. 2007). Commonly known as White Mojarra, it is distributed throughout the Atlantic watershed of Southern Mexico in the Coatzacoalcos and Usumacinta river basins and in ]]> et al. 2002). It is a tropical freshwater demersal species found in neotropical ecosystems (Deckert & Greenfield 1987) and caught in the Usumacinta River, especially in the municipality of Tenosique in Tabasco, Mexico, where it is an important food source sold as a fresh or frozen product. Its body is relatively high, with a slightly high convex pre-dorsal profile, ascending softly up to the first dorsal spine. Its dorsal fin has a concave posterior profile. It also has a wide inter-orbital space, a groove or maxillary process without scales, an oval central depression, and big eyes. Its ]]>

Studies on E. mexicanus have focused on systematic and biogeographic aspects (González 2005), ]]> & Greenfield 1987, Gilmore et al. 2002). However, few studies have been carried out on the reproduction of the species from the genus Eugerres, in contrast with the number of studies on E. lineatus and E. brasilianus, as well as on Diapterus peruvianus (Álvarez et al. 1996, Jiménez et al. ]]> et al. 2008). The embryonic and larval development of several species of this genus is unknown. Considering the fishery and ecological importance of E. mexicanus, this study was designed to describe its embryonic and larval development, in order to increase knowledge about the species and provide useful data for future research.

Materials and methods

Study site: This study was carried out in February 2009 at the Recreo locality (17°28’52’’ N and 91°25’17’’ W) on the Usumacinta River. Five females and two males of the species E. mexicanus were collected with a seine net with a mesh size of 1x1cm, 50m long and 3m wide. The specimens were transported to ]]>

All specimens were measured, and weighed on a Torrey digital scale (capacity 0.4 to 20 000g). Pasteur ]]>

Spawning induction: Spawning was induced with human chorionic gonadotropin hormone (CGH) Pregnyl using 5 ]]>

]]> Parameter records: Spawning was carried out maintaining an average temperature of 30.5°C; (SD=1.9), an electric conductivity of 0.29μS (SD=0.40); pH at 8.1 (SD=0.10); dissolved oxygen at 6.8m/L (SD=4.8), total chlorine at 0.15mg/L (SD=0.30); nitrite at 0.70mg/L (SD=0.40) and nitrate at 0.0mg/L. During the incubation stage, parameters were maintained at 28.6°C (3.1); 0.55μS (0.10); 8.2 (0.10); 2.7mg/L (4.8); 0.10 mg/L (0.00), without nitrite and nitrate. At larval stage, parameters were at 27.1°C (1.90): 0.55μS (0.10); 7.9 (1.2); 5.30mg/L (2.1); 0.05mg/L (0.01), ]]>

Measurement of embryos and larvae: A total of 30 eggs with embryos and 30 larvae were extracted every three hours. They were observed with a Motic BA300 binocular microscope, photographed with a Digitan Moticam 2 300 digital camera, ]]> number of spines and rays on the fins during the larval development (Rosas et al. 2008).

Results

The specimens collected in the wild presented viable sexual products. Females presented oocytes in the ]]>

Embryonic development: Fertilized eggs were recovered in the gastrula stage with an average diameter of 1.17mm (SD=0.08). They were adhered to the substrate and presented a ]]> Fig. 1, Table 1 and 3).

On the first day following fertilization, the early embryo stage was observed three hours post-gastrula, with an average diameter of 1.19 (0.04). The caudal region was adhered to the vitellus, where Kupffer´s vesicle was visible, and the cephalic region had an ovoid projection (Fig. 2A, Table 1). The free tail stage occurred six hours after fertilization, and the developing optical vesicles could be observed in the head  and the heart. The heart presented contractions that generated beats (Fig. 2B, Table 1). After nine hours, the embryo increased in size, mainly around the caudal region, with the myomeres or segments of the developed muscles becoming visible (Fig. 2C, Table 1). Twelve hours post-fertilization, the embryo exhibited vibrating movements in the caudal region, where vesicles or ear plaques appeared, and a developed notochord could also be observed (Fig. 2D, Table 1).

Fifteen hours post-fertilization, the embryo occupied 90% of the egg space, and the somites or primitive segmentation could be seen (Fig. 2E, Table 1). The final stage of the embryonic development was reached after 18 hours, and 100% of the vitelline space was occupied. Also visible were the chromatophores, or pigment cells responsible for the skin color of the embryo, along the dorsal and caudal regions of the body. The chorion membrane was broken by the frequent vibrating movements, and hatching began (Fig. 2F, Table 1).

Recently hatched larvae: The posthatching yolk-sac larvae were light brown in color, had an average total length of 2.94mm (SD=0.7) and a width of 0.79 (0.10). The notochord had an average length of 2.74mm (0.80). They showed a longitudinally oval vitellum with an average length of 0.98mm (0.20) and a width of 0.59 (0.20). An average big drop of oil could be seen, measuring 0.49mm (0.10) long and 0.49 (0.10) wide (Fig. 3). The larvae on day one, specifically eight hours post-hatching, had an average total length of 4.02mm (0.26) and a width of 0.79 (0.07). The head and the notochord were 0.56mm (0.05) and 3.85mm (0.24) long, respectively. The vitellum had an average length of 0.99mm (0.12) and width of 0.61 (0.09), and was in the process of re-absorption. The drop of oil measured an average of 0.48mm (0.09) long and 0.47 (0.08) wide. On the second day (hour 20) a pair of ear plaques could be seen in the cephalic region, together with dark pigmented spots or melanophores on the body, and the mouth was open. The completely pigmented eyes of the larvae were an average of 0.24mm (0.02) long and 0.22 (0.01) wide. The orbital circle was an average of 0.26mm (0.02) long and 0.31 (0.38) wide, and the average orbital fossa was 0.29mm (0.18) long and 0.28 (0.01) wide. The larvae had an average pre-anal length of 1.44mm (0.23) and a post-anal length of 2.00mm (0.28) (Table 4).

Preflexion: This stage was reached eight days post-hatching and presented an average larvae length of 4.67mm (SD=0.50) and width of 0.70 (0.11). Morphologic characters are shown in Table 2. Upon reaching hour 182, larvae exhibited a developing digestive tract ending at the anal orifice and a yolk-sack in process of re-absorption. Over the caudal region and posterior to the anus were 15 spots or melanophores. At hour 289 post-hatching, the head was free of the yolk-sack and the optical vesicles were completely pigmented. Pelvic fins were an average of 0.27mm (0.03) long and 0.27 (0.06) wide, while pectoral fins were an average of 0.35mm  (0.01) long and 0.27 (0.05) wide (Fig. 3).

Flexion: This developmental stage started 16 days (372 hours) post-hatching, when flexion of the notochord was observed in the region of the caudal fin of the embryo. A swim bladder could also be seen over the intestinal region and the intestine showed food in the process of decomposition. The primordium of the dorsal fin and a rudimentary anal fin could also be seen, together with small developing rays (Fig. 3, Table 2).

Postflexion: Larvae reached this stage 24 days post-hatching, with an average total length of 10.33mm (SD=1.45) and a total width of 1.73 (0.51) (Table 2 and 4). Aftermetamorphosis, the caudal fin was observed to be forked, with 17 fin rays, each with six segments. The length of the larvae to the fork varied 9.17 (0.44). At hour 578 post-hatching, the larvae presented small canine teeth on the maxilla and mandible in the mouth, measuring an average of 0.35mm (0.09) long and 0.03 (0.01) wide (Fig. 3). The complementary morphometric characters are shown in Table 2. Likewise, these larvae presented totally formed dorsal, anal, pelvic and caudal fins. By hour 692 post-hatching, the dorsal fin measured an average of 2.0mm (0.40) long and 0.62 (0.13) wide and presented IX spines: the first smaller than the others measuring an average of 0.25 (0.22), the second 0.32 (0.16), the third 0.37 (0.20), the fourth 0.31 (0.24), and the fifth 0.18 (0.13), with 10 rays. The anal fin was an average of 1.99mm (0.35) long and 0.47 (0.16) wide and presented III spines, the first small with an average length of 0.55mm (0.35) and the second one with an average length of 0.34mm (0.11) long. Eight rays were also observed measuring an average of 1.08mm (0.60) long. The pectoral and pelvic (n=5) fins were 0.35mm and 0.50mm long, respectively (Fig. 3, Table 5). ]]>

Prejuveniles: This phase started 33 days (792 hours) post-hatching, with an average total length of 14.3mm (SD=0.93) and a width of 3.12 (0.21). The mouth-fork length was 12.83mm (0.76). The dorsal fin measured 1.28mm long and 0.08mm wide and presented IX spines and 10 rays. The first spine measured an average of 0.30mm (SD=0.04) long, the second 1.23mm (0.09), the third 1.40mm ]]> ( Fig. 3, Table 5).

Juveniles: This stage occurred 45 days (1 080 hours) post-hatching with an average total length of 28.16mm (SD=1.93, n=5), a width of 30.1 (36.8, 5.0) and an average weight of 4.75g (SD=1.49, n=5) ( Table 5).

Pigmentation: The exceptional pigmentation during the larval with sack stage and before preflexion showed two lines of olive and yellow colors in the margin of the notochord. Dark pigmentation was noticed on the body, the posterior side of the head and on the base of the pectoral fin. Five post-anal melanophores were also displayed on myomere five and six. During ]]>

During flexion, pigmentation had a notorious silver color in the intestine. The myomerehad a beige coloration going from ]]> turned to a brownish olive color with black margins. The lateral line of the body had yellowish pigmentation from the later part of the operculum to the caudal peduncle, which is a characteristic trait of the species (González 2005). In juveniles the same pigmentation pattern ]]>

Discussion

The descriptive characteristics of the embryonic stage of E. mexicanus are typical of this developmental ]]> E. brasilianus and E. lineatus that inhabit marine environments (Álvarez et al. 1996, Ortíz et al. 2008). However, their morphometric characters are different with respect to the diameter and size of the oil drop, as E. mexicanus eggs are bigger than those of marine species, being similar to those of freshwater fish (Fuiman 2002).

The incubation period in hours is similar to that of marine species of the genus Eugerres and the incubation temperature is also similar to that reported for E. brasilianus, but greater than the one recorded during the incubation ]]> E. lineatus. Regarding the recently hatched larvae, E. mexicanus were bigger (average length of 2.94mm) than E. brasilianus (average length of 1.43mm). This may be observed through the average length of the vitelline sack of E. mexicanus and E. brasilianus measuring 0.98mm and 0.70mm, respectively, and the notochord length of E. lineatus (1.05mm) in ]]> E. mexicanus (2.74mm) (Álvarez et al. 1996, Ortíz et al. 2008).

Following the classification of pre-flexion, flexion and post-flexion established to determine the development of larvae, the E. ]]> larvae were bigger than the la rvae of the species E. brasilianus and E. lineatus of the same genus and the marine larvae of D. peruvianus (Álvarez et al. 1996, Jiménez et al. 2003, Ortíz et al. 2008).

It must be noted that Fuiman (2002) ]]> E. mexicanus prejuveniles of E. mexicanus measured 13.25mm to 15.00mm in length, similar to D. peruvianus (8.72 to 15.00mm) and E. lineatus prejuveniles (13.00mm to 18.00mm). On the other hand, E. mexicanus juveniles were bigger in length (28.16mm) than that recorded for E. ]]> (17.30mm) and D. peruvianus (17.00mm to 24.00mm) (Jiménez et al. 2003, Ortíz et al. 2008) (Table 5). With respect to the meristic characters, the fins of E. lineatus and D. peruvianus presented a different number of spines and rays during the ]]> E. mexicanus, as described by Deckert & Greenfield (1987) and González (2005).

Regarding pigmentation, the colors of the larva with sack for Eugerres mexicanus wereolive and yellow on the ]]> E. lineatus since in this sample there is a group of melanophores between myomere 9 to 13 as the main characteristic, and for Diapturus peruvianus because of the three spots displayed in the dorsal margin of the intestines from the insertion of the pectoral fin to the anus (Jiménez et al. 2003, Ortíz et al. 2008). E. mexicanus larvae during flexion ]]> E. lineatus, since the latter continues with a similar pigmentation during pre-flexion and flexion, in which only the first melanophores are accentuated. Nevertheless, although E. mexicanus shows similar post-anal spots from 13 to 16 as D. peruvianus, it differs in that one or two of those spots are where the caudal fin will be (Jiménez et al. 2003, Ortíz et al. 2008).

Three spots were observed in the caps, and dark spots remained in the margin of the dorsal fin, which differs from E. peruvianus since in E. mexicanus two groups of four opercular pigments are present and there is little pigmentation toward the corners of the dorsal fin while in D. peruvianus fins turn yellow and the body line is covered with silver flakes (Jiménez et al. 2003, Ortíz et al. 2008). In E. mexicanus prejuveniles brown pigmentation was observed in the cephalic region, the dark margins of the dorsal and anal fins, and the base of the tail, while pigmentation was yellow in the lateral line. ]]> E. peruvianus since in E. mexicanus two groups of four operculum pigments are present and there is little pigmentation towards the vertices of the dorsal fin, while in D. peruvianus fins turn yellow and the line of the body is covered with silver flakes (Jiménez et al. 2003, ]]> et al. 2008).

Physicochemical parameters played an important role during white mojarra  reproduction, as was the case of temperature that was favorable during the spawning and hatching stages. However, it varied from 25.6 to 28.4°C during the larval stage, which may have contributed to the high mortality recorded during this stage (99%). Álvarez et ]]> (1996) stated that a temperature of 20°C increased mortality in the case of E. brasilianus and also recorded a pH of 7.5 to 8.2 and values of dissolved oxygen of 5.5 to 7.1mg/L, similar to the pH and dissolved oxygen values required for E. mexicanus of 7.5 to 8.4 and 3.8 to 6.7mg/L,  respectively. The nitrogen compounds recorded in the present study showed low levels and were considered non-toxic for the fish. Conductivity was low and varied from 0.51 to 0.56μS/cm. The ]]> et al. (1996) provided the green alga Nannochloropsis oculata to E. brasilianus larvae ]]> Artemia sp. nauplii and copepods, obtaining a 50% survival.

Eugerres mexicanus specimens spawned after a single dose of 50UI/100g/fish of human chorionic ]]> E. brasilianus used 6-10UI/g/fish distributed over two and three doses (Álvarez et al. 1996). In other cases, doses of 3.4-6.3 UI/g/fish were applied to females of Lutjanus griseus (Cabrera et al. 1997), and three doses of hormones were used at concentrations of 3.00, 1.00 and 0.5UI/g/fish for ]]> Haemulon bonarinense (Cuartas et al. 2003), with the doses of 0.50 (females) and 0.25 (males) producing the most viable sexual products. Only the 0.50 dose presented similar results to those obtained for E. mexicanus. Álvarez & Hernández (2001) determined that a period of 10 hours for spawning is relatively short in the case of tropical species, and related this to the short physiological action of the ]]> E. brasilianus, which equaled to an average 87% success rate (range=60-100%) (Álvarez et al. 1996). Records of other fish species include Lutjanus griseus with 36% and 86% with the ]]> et al. 1997) and Haemulon donariense with 90% (Cuartas et al. 2003). Other authors used the synthetic analogue of the luteinizing hormone releasing hormone (LHRHA) and obtained 85% for Orthopristis ruber (Mata et al. 2004) and 90% for Centropomus parallelus (Álvarez et ]]> 2002).

The results of this study are the first recorded for this species and generated information on several aspects of its reproductive biology and early life development. These results have also made it possible to establish a technique for manipulation in captivity, which may be adopted for aquaculture development of this species.
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Acknowledgments

The authors acknowledge the CONACYT Fund and the government of the State of Tabasco for financing study TAB-2007-C09-73534.

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*Correspondencia:
Raúl E. Hernández: Ingeniería en Acuacultura, División Académica Multidisciplinaria de los Ríos, Universidad Juárez Autónoma de Tabasco, km 1 carretera Tenosique-Estapilla, Tenosique, Tabasco, México. CP 86901; raul.hernandez@ujat.mx
Martha A. Perera: Ingeniería en Acuacultura, División Académica Multidisciplinaria de los Ríos, Universidad Juárez Autónoma de Tabasco, km 1 carretera Tenosique-Estapilla, Tenosique, Tabasco, México. CP 86901.
Alfonso Castillo: Ingeniería en Acuacultura, División Académica Multidisciplinaria de los Ríos, Universidad Juárez Autónoma de Tabasco, km 1 carretera Tenosique-Estapilla, Tenosique, Tabasco, México. CP 86901.
Emiliano Luna H:Ingeniería en Acuacultura, División Académica Multidisciplinaria de los Ríos, Universidad Juárez Autónoma de Tabasco, km 1 carretera Tenosique-Estapilla, Tenosique, Tabasco, México. CP 86901.
José A. de la Cruz:Ingeniería en Acuacultura, División Académica Multidisciplinaria de los Ríos, Universidad Juárez Autónoma de Tabasco, km 1 carretera Tenosique-Estapilla, Tenosique, Tabasco, México. CP 86901.
Luis M. Gómez: División Académica de Ciencias Agropecuarias, Universidad Juárez Autónoma de Tabasco; luisgomezdd@gmail.com.mx
José Valdez Zenil: Facultad de Biología de Ciencias Biológicas y Agropecuarias, Universidad Veracruzana, carretera Tuxpan-Tampico, Tuxpan, Veracruz; josevaldezz@yahoo.com.mx ]]>
1. Ingeniería en Acuacultura, División Académica Multidisciplinaria de los Ríos, Universidad Juárez Autónoma de Tabasco, km 1 carretera Tenosique-Estapilla, Tenosique, Tabasco, México. CP 86901; raul.hernandez@ujat.mx
2. División Académica de Ciencias Agropecuarias, Universidad Juárez Autónoma de Tabasco; luisgomezdd@gmail.com.mx
3. Facultad de Biología de Ciencias Biológicas y Agropecuarias, Universidad Veracruzana, carretera Tuxpan-Tampico, Tuxpan, Veracruz; josevaldezz@yahoo.com.mx