Reproductive biology of common snook Centropomus undecimalis (Perciformes: Centropomidae) in two tropical habitats

In Southeastern Mexico, Centropomus undecimalis is an important fish species of sport and commercial fisheries for coastal and riverine communities. Fisheries along rivers and coasts depend on migratory habits of this species, and these movements are probably related to reproduction. In spite of its economic importance, few studies have been conducted focusing on its reproductive biology, and this research aims to analyze these habits. Samples (fork length, somatic and gonads weight, and macroscopic maturity stages) were obtained from organisms collected by fishermen from the largest fishing cooperatives along the coastal and riverine areas of Tabasco, from July 2006 to March 2008. Fish size ranged from 34 to 112 cm fork length, with an average age of 6.42 years for males and 9.12 years for females. In riverine areas, fish sizes ranged from 30 to 85 cm and the average age was 5.5 years for males and 6.6 years for females. Significant differences were recorded between lengths of males and females from the two areas (Kruskal-Wallis, p < 0.05). The male:female ratio was 1:0.68 in the coast, and 1:0.16 in riverine areas. The length-weight relationship did not vary between both sexes among areas (ANCOVA, p > 0.05). A curve for eviscerated weight was calculated for both sexes, for coastal fishes SW = 0.0059 (FL)3.07, and the riverine ones SW = 0.0086 (FL) 2.98, with an isometric growth (b = 3). The period of maximum reproduction was from July to August, with temperatures of 28 to 30 degrees C. A significant correlation between the gonadosomatic index (GSI) and rainfall was recorded for samples of both males and females from coastal areas (r = 0.63, r = 0.70) whereas only one positive correlation was recorded for riverine females (r = 0.57). The size at first maturity (L50) was estimated at 60 cm and 80 cm (FL), corresponding to 5.5 and 8.5 years of age, for males and females, respectively. An important proportion of mature females of eight years and older, suggests that these ages contribute significantly to the reproductive biomass. The results indicate that due to changes in the exploitation period, we recommend to protect populations of the common snook.     

Effects of salinity on physiological conditions in juvenile common snook Centropomus undecimalis

This study describes the effects of different salinities on oxygen consumption, ammonia excretion, osmotic pressure, apparent heat increment, postprandial nitrogen excretion, and oxygen:nitrogen ratio in juvenile common snook Centropomus undecimalis. Oxygen consumption of fish fasting and fish feeding was statistically different in relation with salinity. Fish maintained at 0, 25, and 35 ppt invested more energy processing feed than fish maintained at 12 ppt. Fasting fish had lower ammonia excretion than feeding fish and excretion was reduced at high salinities. Snook can change the energetic substrate in function with salinity, from a mixture of protein and lipids and carbohydrates at 35 ppt to a more acute preference for proteins at lower salinities. This species changes osmotic plasma concentrations at extreme experimental salinities. The different salinities were the snook inhabits (0-36 ppt), have a direct effect on the physiology, inducing changes on the oxygen consumption, nitrogen excretion, changes on the energetic substrate and plasma osmotic pressure.     

Ontogeny of suction feeding capacity in snook, Centropomus undecimalis

The ontogeny of suction feeding performance, as measured by peak suction generating capacity, was studied in the common snook, Centropomus undecimalis. Suction pressure inside the buccal cavity is a function of the total expansive force exerted on the buccal cavity distributed across the projected area of the buccal cavity. Thus, the scaling exponent of peak suction pressure with fish standard length was predicted to be equal to the scaling exponent of sternohyoideus muscle cross-sectional area, found to be 1.991, minus the scaling exponent for the projected buccal cavity area, found to be 2.009, equal to -0.018. No scaling was found in peak suction pressure generated by 12 snook ranging from 94 to 314 mm SL, supporting the prediction from morphology. C. undecimalis are able to generate similar suction pressures throughout ontogeny.     

Isolation and characterization of 27 polymorphic microsatellite loci for the common snook,Centropomus undecimalis

Here we describe 32 di‐, tri‐ and tetranucleotide microsatellite loci isolated by PIMA, a polymerase chain reaction (PCR)‐based procedure, for the common snook (Centropomus undecimalis). Five loci were monomorphic, and the remaining loci averaged 6.7 alleles per locus in a sample of 45 common snook. For polymorphic loci, expected heterozygosities ranged from 0.02 to 0.91 (mean = 0.538). Significant departures from Hardy–Weinberg equilibrium expectations occurred in two loci. Exact tests for genotype disequilibrium gave evidence for linkage at one pair of loci. Many cross‐species primer assays yielded PCR fragments of the expected size for 11 species of Centropomus and two species of the confamilial genus Lates.     

Maturation of female common snook Centropomus undecimalis: implications for managing protandrous fishes

The assumption for hermaphroditic fish species that mature individuals of the terminal sex arise directly from mature individuals of the primary sex has led to the use of sex ratios as a proxy for age at maturity (A₅₀). The timing of transition and deficient energy reserves, however, can result in a delay between transition and spawning. To test the assumption of female maturity and investigate the relationship between maturation and energy reserves, common snook, Centropomus undecimalis, a protandrous hermaphrodite, were collected from rivers, estuaries, inlets and offshore habitats on the east coast of Florida during 2010–2015. Immature females were observed every month, with lowest proportions during the peak spawning months of July and August. When calculated based on sex ratio, A₅₀ (8.1 years) overestimated the age at which 50% of the female population was, in fact, mature (4.1–4.9 years). Best-fit models indicate that mesenteric fat index (I_F) and hepato-somatic index (I_H) were significantly affected by gonad phase, month and size and weakly by habitat. In post hoc analysis, immature female I_F did not differ significantly from developing and regenerating females, but immature female I_H was significantly lower than that for all mature phases except animals in the regressing phase. Although immature females may have sufficient energy in terms of fat, it appears that energy is not allocated to reproductive processes, as evidenced by lower I_H. Nonetheless, approximately 95% of females were spawning-capable during peak spawning months, suggesting that the energy threshold at which immature females reach maturity is met by most females each spawning cycle.     

Development and fate of the postovulatory follicle complex,postovulatory follicle,and observations on folliculogenesis and oocyte atresia in ovulated common snook,Centropomus undecimalis (Bloch, 1792)

The common snook, Centropomus undecimalis , was induced to ovulate using a time‐release, GnRH analogue. Ovulation occurred the afternoon or evening the day after hormone administration. The time of ovulation was established within half an hour. At ovulation, three fish per time‐group were divided into 0, 6, 12, 18 hr and one thru five days post‐ovulation to study changes in the postovulatory follicle complex (POC). Histology of the ovaries revealed changes in the POC, postovulatory follicle (POF) and oocyte atresia through five days post‐ovulation. Within 24 hr, nuclei of the POF cells lost their initial spherical or oval configuration, and by four days the basement membrane within the POC had fragmented. There was a temporal separation between ovulation and post‐ovulation folliculogenesis; that is, in that the formation of new follicles commenced within the germinal epithelium between 12–48 hrs after ovulation. Morphology of the POC was best revealed with the reticulin stain; it is composed of the POF and postovulatory theca (POT). These are separated by a basement membrane, reflecting the origin of a follicle from a germinal epithelium while the theca is derived from stroma. The POF is composed of the former follicle cells that surrounded and contacted the oocyte during its development; the follicle is composed of the oocyte and its surrounding follicle cells. The POC is composed of a prominent basement membrane separating the POT from the POF. The reticulin stain clearly defines compartmentation in the ovary and supports redefinition of the POF as the follicle cells that formerly surrounded the oocyte prior to ovulation. J. Morphol. 278:547–562, 2017. © 2017 Wiley Periodicals, Inc.     

Early gonadal differentiation in the Mexican snook Centropomus poeyi (Centropomidae,Perciformes, Teleostei) suggests protandric hermaphroditism

ABSTRACT

This study describes for the first time the early gonadal morphogenesis and raises the possibility of occurrence of protandric hermaphroditism in the Mexican snook (Centropomus poeyi). To achieve this, histological analysis of early gonadal differentiation was performed in 105 juvenile specimens ranging from 136 to 367 days post-hatching (dph). The early gonadal differentiation of the Mexican snook started at 178–213 dph and was completed at 355–367 dph. Active spermatogenesis was observed at 355–367 dph, once the compartmentalization of testis in germinal and interstitial compartments was accomplished. Our study demonstrates that in the Mexican snook, early gonadal differentiation is directed to produce 100% males, implying protandric hermaphroditism and showed the presence of a long-lasting period of gonadal differentiation, which makes this species highly sensitive to environmental cues.     

Karyotypic characterization in mitosis and meiosis of the common snook Centropomus undecimalls (Pisces: Centropomidae)

The common snook Centropomus undecimalis inhabits marine, brackish and freshwater habitats in the Western Central Atlantic Ocean, including the Gulf of Mexico. Common snook is an economically important fish in many localities, nevertheless the number of studies on its biology and genetics are still few. The present study attempts to establish the cytogenetic profiles of the specimens collected in Paraiso Municipality Tabasco, Mexico. Tissue of five females and eight male organisms were processed by conventional cytological techniques to obtain chromosome slides of high quality in order to assemble the karyotype. The results from the kidney tissue analysis showed that 85.1% of 288 mitosis had a 2n = 48 chromosomes, and 52.8% of 104 meiosis exhibited the haploid number 1n = 24. The diploid karyotype showed 48 monoarmed chromosomes of the telocentric (T) type. There was no chromosome heteromorphism between females and males. The diploid karyotype was very similar to that observed in the majority of marine fishes.     

Development of the germinal epithelium and early folliculogenesis during ovarian morphogenesis in the cichlid fish Cichlasoma dimerus (Teleostei,Perciformes)

Formation of the germinal epithelium and folliculogenesis during ovarian development in Cichlasoma dimerus were described at the light‐ and electron‐microscopic levels. Prior to gonadal differentiation, germ cells and enveloping support cells reside within an inpocketing of the coelomic epithelium. Separation of the germinal and interstitial compartments of the gonad by a basement membrane is apparent from early gonadal development. Upon ovarian differentiation, oogonia undergo cyst‐forming divisions leading to the formation of clusters of interconnected cystocytes that synchronously enter meiosis, becoming oocytes. At the pachytene step, each oocyte becomes individualized by cytoplasmic extensions of prefollicle cells, thereby developing as an ovarian follicle. Subsequent somatic reorganization leads to the formation of the ovarian lumen in a cephalo‐caudal gradient. As a result, the germinal epithelium becomes internalized and lines the ovarian lumen. As defined by its origin from the germinal epithelium, the ovarian follicle is composed of an oocyte and the surrounding follicle cells. Thecal cells derived from the stroma encompass the basement membrane outside the follicle, thus forming a follicle complex. A common basement membrane is shared by the germinal epithelium and the follicle complex along a small portion of its surface. This point of attachment represents the site at which the oocyte would be released to the ovarian lumen during ovulation.     

Lack of genetic differentiation in the fat snook Centropomus parallelus (Teleostei: Centropomidae) along the Brazilian coast

The patterns of genetic variation in a fragment of the cytochrome b mtDNA gene in 130 individuals of the fat snook (Centropomus parallelus) did not show evidence of genetic differentiation along the Brazilian coast as shown in F‐statistics and AMOVA analyses, indicating the existence of high gene flow among the studied populations. In addition, the study of the evolutionary demography of the species using mismatch distribution analysis and statistical tests such as Tajima’s D and Fu’s F indicate that it experienced a pattern of population expansion during its recent evolutionary history.     

Acute toxicity of nitrite in fat snook (Centropomus parallelus)

Oxidative stress and hypoxia responses in Centropomus parallelus exposed to three different concentrations of nitrite (0, 0.5, and 10 mg L^?1) were evaluated. To determinate toxicity, we used enzymatic analyses and quantifications of oxygen consumption and opercular beats under conditions of normoxia and hypoxia. There was no significant difference in GST, CAT, or GPx enzymes in the liver or in GPx in the gills. Levels of GST were altered at a concentration of 10 mg L^?1 in experiment I. Experiment II displayed alterations for GST and CAT in the liver at the same concentration, indicating that exposure to nitrite does not generate differentiated activation in the body’s defense system by the production of oxidative stress enzymes. When nitrite was associated with hypoxia, there was a significant increase in both enzymatic activity and opercular beating under hypoxia in the group exposed to 10 mg L^?1 nitrite compared to the control.     

Reproductive biology of the fat snook Centropomus parallelus Poey, 1860 (Teleostei,Centropomidae) and implications for its management in the southern Atlantic Ocean

The reproductive biology of Centropomus parallelus was described from 589 individuals captured in estuarine and coastal waters in Southern Brazil. Length-frequency distribution showed the dominance of males in smaller length-classes (132–290 mm L_T), whereas females were dominant in larger length-classes (>290 mm L_T). Total length at maturity (L₅₀) was 180 mm L_T and corresponded to 29% of the maximum length recorded. Histological sections revealed one hermaphrodite (205 mm L_T) and few immature females. Life history traits provided herein can contribute to sustainable fisheries management practices.     

Life‐history traits of the common snook Centropomus undecimalis in a Caribbean estuary and large‐scale biogeographic patterns relevant to management

The ecology of common snook Centropomus undecimalis in Amatique Bay, a tropical estuary in eastern Guatemala, was investigated and life‐history traits were used to conduct a meta‐analysis of the species from Florida to Brazil. The reproduction cycle of C. undecimalis in Amatique was strongly related to the precipitation cycle, with a lag of 2 months. Spawning occurred from April to November with a peak spawning after the onset of the summer rains. Protandric sex reversal occurred early in the dry season (December) before somatic recovery from spawning. The growth cycle preceded that of body condition by c. 1 month, and was out of phase with the reproductive cycle. Growth was fast, as many individuals reached >70% of the maximum observed total length (L_T, 102 cm) after 3 years. Sex transition occurred within a relatively narrow L_T range (70–79 cm), but over a wide range of ages, indicating plasticity in this respect. The meta‐analysis indicated a latitudinal‐temperature gradient in life‐history traits, as well as different seasonal patterns relative to temperature and hydrographical cycles. Centropomus undecimalis from cooler winter waters (e.g. Florida) reach larger maximum L_T and L_T at sex change, as well as greater gonado‐somatic indices and longer life spans. Further, increased fishing mortality results in younger age at sex reversal and male predominance in the populations compared. Recognition of large‐scale biogeographic patterns in this important, but little studied, fish species helps in the formulation of management advice in other areas of its occurrence.     

Energetics of Swimming in Juvenile Common Snook, Centropomus undecimalis

Little research has been devoted to the investigation of swimming energetics and performance in lie-in-wait predators. This study evaluated activity metabolism and swimming performance in juvenile snook, Centropomus undecimalis, a lie-in-wait predator, by determining oxygen uptake in a tunnel respirometer. Compared to previously reported results for more actively foraging species (i.e., white crappie, rainbow trout), snook exhibited lower maintenance metabolism (58.6ml O₂kg^–1WMh^–1) and greater metabolic expansibility (6.5). Relative critical swimming speeds decreased isometrically with length, implying that small snook are capable of prolonged swimming in velocity regimes similar to those experienced by larger individuals. Swimming was most efficient at the transition between pectoral (low-speed) and caudal (high-speed) propulsion. The results of this study support previous speculation that maintenance costs may be reduced in lie-in-wait predators compared to other fishes.     

Cytochemical, immunocytochemical and ultrastructural observations on leukocytes and thrombocytes of fat snook (Centropomus parallelus)

The cytochemical, immunocytochemical and ultrastructural characteristics of leukocytes and thrombocytes in the peripheral blood of the fat snook (Centropomus paralellus) - a fish occurring in Brazil - were investigated. The cytochemical methods were performed to demonstrate four enzymatic reactions - o-toluidine-hydrogen peroxide, naphtol AS-MX phosphate, naphtol AS-BI phosphate and alpha-naphtil acetate to detect myeloperoxidase (MPO), alkaline phosphatase (ALP), acid phosphatase (ACP) and non-specific esterase (α-NAE), respectively - and two non-enzymatic ones - Periodic-Acid Schiff (PAS) and Sudan black B (SBB) to detect the occurrence of glycogen and phospholipids, respectively. Immunocytochemical method utilizing polyclonal rabbit antibody against mammal metalloproteinases (MMPs) 2 and 9 were done. Standard method for Electron Microscopy (EM) was applied for the ultrastructural study. The cytochemical reactions were positive in neutrophils for MPO, ACP, α-NAE, glycogen and phospholipids; in lymphocytes for ACP and α-NAE; in monocytes for ACP and α-NAE and in thrombocytes for ACP, α-NAE and glycogen. Only neutrophils were positive for MMPs 2 and 9, and none of the cells studied were positive for ALP. Ultrastructurally: 1) neutrophil showed a spherical shape with a spherical, indented or lobulated euchromatic nucleus, and cytoplasm containing granules of varied sizes and mitochondria of varied shapes and sizes. The nucleus/cytoplasm relation and the size of granules suggest neutrophil maturation in peripheral blood; 2) lymphocytes showed partially heterochromatic nucleus and minimal cytoplasm; 3) monocytes had long cytoplasmic projections, an indented nucleus, evident nucleolus and cytoplasm with granules of varied sizes and vacuoles; 4) thrombocytes were predominantly elliptical or roughly spherical in shape, had a partially heterochromatic nucleus and cytoplasm containing electron-dense granules, intricate canalicular system and vacuoles occasionally holding phagocytic material.     

Ionregulation in juvenile swordspine snook (Centropomus ensiferus,Poey, 1860) in relation to environmental salinity

Ninety‐nine swordspine snook Centropomus ensiferus (9.80 ± 0.3 g, mean ± SE) were studied in order to evaluate the influence of salinity on physiological properties under rearing conditions. Growth performance, survival rates, and ion concentrations (Na⁺, K⁺, Cl^?) as well proximal composition were measured over 76 days. Fish were exposed to three experimental salinities (0, 10, 20 ‰ , three replicates per treatment) and maintained in plastic tanks with a recirculation system equipped with flow‐through aquaria pumps (533 L per tank). Fish were fed twice daily to apparent satiation; at the end of the experiment the weight of fish kept in 10 ‰ was higher than that of fish kept in 0 and 20 ‰ , however no significant differences (P > 0.05) were observed among the experimental salinities. Survival was significantly lower in 10 ‰ salinity than in fish kept in 20 and 0 ‰ salinities. No significant differences (P > 0.05) were found in the Condition factor (K), specific growth rate (SGR), or in plasma Na⁺, K⁺, or Cl^? concentrations among treatments. Salinities also did not affect body composition (P > 0.05), but were significantly lower (P < 0.05) than at the start of the experiment. However, towards the end of the experiment a large accumulation of visceral fat in fish farmed in the three salinities (VFI > 4%) was observed. Water quality was within the optimum range (T: 28.7 ± 0.1°C; O2: 5.6 ± 0.1 mg L^?1; ammonia: 0.2 mg L^?1) for the growth of swordspine snook. Data indicates that C. ensiferus is an ionoregulator fish and able to cultivate successfully in various osmotic conditions, and in turn, maintain high levels of survival in captivity.     

Germinal epithelium, folliculogenesis, and postovulatory follicles in ovaries of rainbow trout, Oncorhynchus mykiss (Walbaum, 1792) (Teleostei, protacanthopterygii, salmoniformes)

The rainbow trout, Oncorhynchus mykiss (Walbaum, 1792), is a salmoniform fish that spawns once per year. Ripe females that had ovulated naturally, and those induced to ovulate using salmon gonadotropin-releasing hormone, were studied to determine whether follicles were forming at the time of spawning and to describe the process of folliculogenesis. After ovulation, the ovaries of postspawned rainbow trout were examined histologically, using the periodic acid-Schiff procedure, to stain basement membranes that subtend the germinal epithelium and to interpret and define the activity of the germinal epithelium. After spawning, the ovary contained a few ripe oocytes that did not ovulate, numerous primary growth oocytes including oocytes with cortical alveoli, and postovulatory follicles. The germinal epithelium was active in postspawned rainbow trout, as determined by the presence of numerous cell nests, composed of oogonia, mitotic oogonia, early diplotene oocytes, and prefollicle cells. Cell nests were separated from the stroma by a basement membrane continuous with that subtending the germinal epithelium. Furthermore, follicles containing primary growth oocytes were connected to the germinal epithelium; the basement membrane surrounding the follicle joined that of the germinal epithelium. After ovulation, the basement membrane of the postovulatory follicle was continuous with that of the germinal epithelium. We observed consistent separation of the follicle, composed of an oocyte and surrounding follicle cells, from the ovarian stroma by a basement membrane. The follicle is derived from the germinal epithelium. As with the germinal epithelium, follicle cells derived from it never contact those of the connective tissue stroma. As with epithelia, they are always separated from connective tissue by a basement membrane.     

Ovarian folliculogenesis in collared peccary, Pecari tajacu (Artiodactyla: Tayassuidae)

The sustainability and production of collared peccary (Pecari tajacu) has been studied in the last few years; however, further information on its reproduction is necessary for breeding systems success. Understanding folliculogenesis aspects will contribute to effective reproductive biotechniques, which are useful in the preservation and production of wildlife. The aim of this study was-to evaluate the ovarian folliculogenesis in collared peccary. Ovaries from six adult females of collared peccary were obtained through ovariectomy and analyzed. These were fixed in aqueous Bouin's solution and sectioned into 7 microm slices, stained with hematoxilin-eosin and analyzed by light microscopy. The number of pre-antral and antral follicles per ovary was estimated using the Fractionator Method. The follicles, oocytes and oocyte nuclei were measured using an ocular micrometer. Results showed that the length, width, thickness, weight, and the gross anatomy of the right and left ovaries were not significantly different. However, the mean number of corpora lutea was different between the phases of the estrous cycle (p<0.05), with the highest mean in the luteal phase. Primordial follicles were found in the cortex; the oocytes were enveloped by a single layer of flattened follicular cells. In the primary follicles, proliferation of the follicular cells gave rise to cuboidal cells (granulosa cells). The secondary follicle was characterized by two or more concentric layers of cuboidal cells (granulosa), beginning of antrum formation, and the presence of pellucid zone and theca cells. Antral follicles were characterized by a central cavity (antrum), the presence of cumulus oophorus and theca layers (interna and externa). In the right ovary, the values of the primordial and primary follicles were similar, but significantly different from the secondary ones (p<0.05). In the left ovary, significant differences were observed between all follicles in the follicular phase (p<0.05); the mean number of primordial and primary follicles was similar in the luteal phase. The mean number of pre-antral follicles and antral follicles in the follicular phase was higher in the left ovary (p<0.05). The mean number of antral follicles in the luteal phase was similar in both ovaries. We also found significant differences in mean diameter of preantral follicles, oocyte, granulosa layer and oocyte nucleus during the estrous cycle. In the antral follicles a significant difference was observed only in follicular diameter (p<0.05). The predominance of active primordial and primary follicles was found in both phases; otherwise the secondary follicles and antral follicles showed a high degree of degeneration. The results obtained in the present work will strengthen the development of biotechnology programs to improve the productive potential and conservation of the collared peccary.     

Morphocytochemical, immunohistochemical and ultrastructural characterization of the head kidney of fat snook Centropomus parallelus

This study characterized the structure and the morphocytochemical, immunohistochemical and ultrastructural aspects of the head kidney (HK) of the fat snook Centropomus parallelus. The HK is enclosed by a thin capsule of connective tissue, from which fine trabeculae originate and branch into the interior of organ. In the parenchyma, there are aggregates of lymphoid cells containing populations of lymphocytes T immunopositive for CDRO45, in a nodular arrangement, around blood vessels and melano-macrophage centres. Among the cells that constituted these aggregates and surrounded them, were macrophages and monocytes, and their precursors, with strong immunopositivity for CD68, along with cells of the granulocytic lineage in various phases of maturation positive for lysozyme and PAS. Macrophages and chromaffin and interrenal cells are also present. Ultrastructurally, the HK comprises a reticulum-endothelial stroma consisting of endothelial cells, reticulocytes of the fibroblast type and macrophage type and a parenchyma with increased cellularity, principally blood cells of the erythrocytic, granulocytic, lymphocytic, monocytic and thrombocytic series.