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A histological study of gametogenesis in captive red snapper Lutjanus campechanus
Aquaculture Research
Abstract
Gametogenesis was monitored histologically in wild-caught red snapper (Lutjanus campechanus, Poey) maintained in captivity under simulated nat-ural photothermal conditions. Gonads were col-lected every 2–3 weeks (average n = 14) for histology during the pre-spawning season (Febru-ary to May, temperature increasing from 16°C to 24°C). Primary vitellogenic oocytes were first observed in one female when temperature reached 20°C. Subsequent samples revealed females in pre-vitellogenesis or at early stages of vitellogenesis, although one female had tertiary vitellogenic (Vtg3) oocytes. The first histological signs of sper-matogenesis were observed when temperature reached 17°C. Spermatozoa were observed in tes-ticular lobules of all males sampled on 14 May (24°C) but little or no sperm was released during manual stripping. Ten males and 10 females were left in tanks and monitored for spawning. No egg release was observed during the monitoring period that encompassed the natural spawning season of wild red snapper. Ovarian biopsies taken during the late spawning season (16 July) revealed that four of eight sampled females had Vtg3 oocytes. Males were manually stripped but released no sperm. These results indicate that captive red snapper can complete gametogenesis in photother-mal controlled systems. Additional research is needed to develop procedures that will achieve reliable maturation and spawning.
... Previous research conducted on red snapper focused on describing the early larval stages as well as spawning induction techniques for wild-caught broodstock (Arnold et al., 1978;Bardon-Albaret et al., 2013;Hastey et al., 2013;Papanikos et al., 2008;Rabalais et al., 1980;Saillant et al., 2013;Williams et al., 2004). While providing the baseline for hatchery technology development for this species, much of this work was constrained by difficulties in obtaining volitional spawning in captivity and high mortalities during the early developmental stages associated with first feeding of the larvae. ...
... Bardon- Albaret, 2014;Bardon-Albaret et al., 2013;Bardon-Albaret & Saillant, 2017;Ogle & Lotz, 2006;Saillant et al., 2013;Williams et al., 2004). Such issues were not observed in the present study. ...
The red snapper (Lutjanus campechanus) has one of the most valued fisheries in the southeastern United States and has been largely studied for its aquaculture potential with varied results that revealed production challenges. This study focused on addressing challenges in larval rearing and juvenile production of this species. Broodstock fish were acclimated in a 60 m 3 tank equipped with recirculating aquaculture system (RAS) and temperature control. After 1 year in captivity, fish volitionally spawned and larval rearing trials were conducted in replicated flow-through seawater tanks ranging from 0.4 to 2.4 m 3 , at a temperature range of 24-26 C. Enriched s-strain rotifers, Brachionus rotundiformis (lorica length of 100-210 μm), were used for first feeding. Enriched Artemia sp. were gradually introduced after 18 days post hatch (DPH). The survival rate before metamorphosis (12 DPH) averaged 66.09 ± 0.08%. Survival rate from yolk-sac larvae to post-metamorphic early juvenile averaged 4.43 ± 0.01%. At 40 DPH, early red snapper juveniles averaged 0.35 ± 0.02 g in weight and 28.83 ± 0.60 mm in standard length. A total of 31,849 fully
... While collection of milt using the stripping procedure can result in a sufficient quality and quantity of sperm for many fish species [e.g., trout (Hajirezaee et al., 2009)], testicular sperm collection utilizing euthanization and testicular tissue collection is a viable alternative for species where sperm are in short supply and/or of less-than-desirable quality (Rurangwa et al., 2004;Kowalski et al., 2006). Importantly, testicular collection is superior to sperm collection using the stripping procedure in a large number of commercially valuable species [common snook (Centropomus undecimalis), African catfish (Clarias gariepinus), Japanese eel (Anguilla japonica), freshwater gobies (Rhinogobius sp), captive Red Snapper (Lutjanus cempechanus)] (Ohta et al., 1997;Viveiros et al., 2002;Tiersch et al., 2004;Yokoi et al., 2008;Bardon-Albaret et al., 2015). The results from these previous studies indicate that a large number of spermatozoa can be obtained from the testis that are not procured using the stripping procedure for sperm collection. ...
... In turbot, the structure of testes is lobular, with the germinal compartments converged toward the spermatic duct in the periphery of the organ. The testicular structure of most teleost is of this type (El-Sayed Ali et al. 2014;Bardon-Albaret et al. 2015). ...
In teleost, sex steroid hormones are critical for reproduction. Progestin is known to promote spermiation. To further understand the functions of progestin via its receptors during the annual reproductive cycle in male turbot (Scophthalmus maximus), we observed testicular development, quantified several sex steroid hormones, detected the expression of progestin receptors, and measured various sperm parameters. Results showed that the turbot testicular structure was of the lobular type. During breeding season, a number of spermatocytes (stage III) developed into spermatids (stage IV), then differentiated into sperm during spermiogenesis (stage V), and finally regressed to spermatocytes (stage VI). Concomitant with testicular development, serum progesterone (P4) and 17α,20β-dihydroxy-4-pregnen-3-one (DHP) exhibited higher levels from stage IV to V than other stages. Furthermore, males with higher motility sperm showed higher levels of P4 and DHP compared with fish with lower motility sperm. These results indicated that P4 and DHP might induce spermatogenesis due to seasonal changes. Concurrently, in testes, the nuclear progesterone receptor (pgr) was expressed throughout the reproductive cycle and its level peaked during spermiogenesis while expression of membrane progestin receptor alpha (mPRα) did not change significantly. However, in sperm, mPRα expression was higher than in testes and had a significant positive correlation with curvilinear velocities (VCL), sperm motility, and motility duration. In conclusion, progestin appears to exert a direct pgr-mediated effect on spermiogenesis and improve sperm motility characteristics depending on the abundance of mPRα protein in sperm during spermiation.
... Thus, initial research efforts on red snapper have focused mainly on controlling reproduction (Phelps et al., 2009). While spermiation is inhibited in red snapper males reared in captivity, most red snapper female broodstock initiate oogenesis (Bardon-Albaret et al., 2015); however, oocyte maturation is infrequent and spontaneous spawns in tanks are scarce and typically unfertilized (Phelps et al., 2009). Volitional tank spawning is expected to lead to a better fry quality (Mylonas and Zohar, 2001;Papanikos et al., 2003). ...
The quality of red snapper eggs is highly variable and unpredictable in aquaculture, leading to high mortality during early larval rearing. In this work, the viability of red snapper eggs was monitored from fertilization until unfed larvae expired because of exhaustion of vitelline reserves to determine egg quality traits in this species. The spawns were obtained via strip spawning wild-caught females following hormonal induction with chorionic gonadotropin. Females were induced immediately after capture (wild group, n=17) or held captive for the entire maturation period prior to induction (captive group, n=7). Candidate predictors of egg quality measured on the female parent at the time of induction or on the spawn at ovulation were evaluated using correlation and multiple regression analysis. The fertilization rate, the hatching rate, and the duration of survival of unfed larvae post hatch were weakly correlated to each other (-0.23<r<−0.08), revealing occurrence of distinct and independent components of egg quality. Spawns from captive females were characterized by a longer latency interval between hormonal induction and ovulation, lower fecundity, and lower hatching rates, as compared to those from wild females. Among the wild brood fish, a positive correlation was observed between the age of the female and the hatching rate. The best model optimized during stepwise multiple regression analysis of hatching rate data only explained 34% of the variance for this trait and no model could be optimized for the prediction of fertilization rate or the duration of survival post hatch. These results highlight the need to develop alternative egg quality measures to predict the viability of fry with confidence.
Red snapper (Lutjanus campechanus) is a popular marine sportfish and is a significant part of the commercial fisheries in the Gulf of Mexico. It can be reproduced under hatchery conditions by induced spawning of wild-caught adults or by conditioning wild-caught adults to spawn naturally under controlled conditions. Mature females (Gondosomatic Index ω 1) occur in the northern Gulf of Mexico from May to September. When such females were collected off the Alabama coast and induced to spawn with HCG, 56 ± 17.3% of the females ovulated. Fecundity (ovulated floating eggs) varies, for 60 spawns averaged 197,212 ± 173,349 eggs/kg female. Percent hatch averaged 42.1 ± 3.44%. Wild-caught adult red snapper can be held in confinement and natural spawning obtained when temperature and photoperiod are controlled. Adult snapper held in 13.2-m3 tanks (8–10 fish/tank), where photoperiod and temperatures were adjusted, spawned naturally 63 times over a 105-day period, with a mean egg production/tank of 4.2 million eggs. Mean fertilization rate, hatch rate, and survival at 36–40 hph were 90.5%, 83%, and 49%, respectively. Natural spawns produce better quality seed, but the occurrence of fertilized spawns is unpredictable. Hormone-induced spawns are easier to schedule but egg quality can be variable.
As the number of fish reproduction studies has proliferated, so has the number of gonadal classification schemes and terms. This hasmade it difficult for both scientists and resourcemanagers to communicate and for comparisons to be made among studies.We propose the adoption of a simple, universal terminology for the phases in the reproductive cycle, which can be applied to all male and female elasmobranch and teleost fishes. These phases were chosen because they define key milestones in the reproductive cycle; the phases include immature, developing, spawning capable, regressing, and regenerating. Although the temporal sequence of events during gamete development in each phase may vary among species, each phase has specific histological and physiologicalmarkers and is conceptually universal. The immature phase can occur only once. The developing phase signals entry into the gonadotropin-dependent stage of oogenesis and spermatogenesis and ultimately results in gonadal growth. The spawning capable phase includes (1) those fish with gamete development that is sufficiently advanced to allow for spawning within the current reproductive cycle and (2) batch-spawning females that show signs of previous spawns (i.e., postovulatory follicle complex) and that are also capable of additional spawns during the current cycle. Within the spawning capable phase, an actively spawning subphase is defined that corresponds to hydration and ovulation in females and spermiation in males. The regressing phase indicates completion of the reproductive cycle and, formany fish, completion of the spawning season. Fish in the regenerating phase are sexually mature but reproductively inactive. Species-specific histological criteria or classes can be incorporated within each of the universal phases, allowing for more specific divisions (subphases).
Marine stock enhancement is a set of management approaches involving the release of cultured organisms to enhance or restore fisheries. Such practices, including sea ranching, stock enhancement, and restocking, are widespread, of variable success, and often controversial. A set of principles aimed at promoting responsible development of restocking, stock enhancement, and sea ranching has been proposed by Blankenship and Leber [American Fisheries Society Symposia 15: 167–175 (1995)], and has gained widespread acceptance as the 'Responsible Approach'. Fisheries science and management, in general, and many aspects of fisheries enhancement have developed rapidly since the responsible approach was first formulated. Here we provide an update to the Responsible Approach in light of these developments. The updated approach emphasizes the need for taking a broad and integrated view of the role of enhancements within fisheries management systems; using a stakeholder participatory and scientifically informed, accountable planning process; and assessing the potential contribution of enhancement and alternative or additional measures to fisheries management goals early on in the development or reform process. Progress in fisheries assessment methods applicable to enhancements and in fisheries governance provides the means for practical implementation of the updated approach.
Almost all fish reared in captivity exhibit some form of reproductive dysfunction. In females, there is often failure to undergo final oocyte maturation, ovulation and spawning; while in males milt production may be reduced and of low quality. These dysfunctions are due to the fact that fish in captivity do not experience the conditions of the spawning grounds, and as a result there is a failure of the pituitary to release the maturational gonadotropin, luteinizing hormone (LH). Reproductive hormones have been utilized since the 1930s to stimulate reproductive processes and induce ovulation/spermiation and spawning. The first methods employed freshly ground pituitaries collected from reproductively mature fish, which contained gonadotropins (mainly LH) and induced steroidogenesis and gonadal maturation. Eventually, purified gonadotropins became available, both of piscine and mammalian origin, e.g., carp or salmon gonadotropin, and human chorionic gonadotropin. In the 1970s, spawning induction methods begun employing the newly discovered gonadotropin-releasing hormone (GnRH), which induces the secretion of the fish's own gonadotropin from the pituitary, thereby overcoming the endocrine failure observed in captive broodstocks. Development of highly potent, synthetic agonists of GnRH (GnRHa) constituted the next generation of hormonal manipulation therapies, and created a surge in the use of hormones to control reproductive processes in aquaculture. The most recent development is the incorporation of GnRHa into polymeric sustained-release delivery systems, which release the hormone over a period of days to weeks. These delivery systems alleviate the need for multiple treatments and induce (a) long-term elevation in sperm production and (b) multiple spawning in fish with asynchronous or multiple-batch group-synchronous ovarian physiology. Based on the recent discovery of GnRH multiplicity in fish and the increasing understanding of its functional significance, new GnRH agonists can be designed for more potent, affordable and physiologically-compatible spawning induction therapies. Future strategies for improved spawning manipulations will be based on understanding the captivity-induced alterations in the GnRH system, and on new approaches for their repair at the level of GnRH gene expression and release.
Ovaries of red snapper Lutjanus campechanus were examined histologically to determine rates of oocyte maturation, diel spawning periodicity and whether lunar cycle influenced spawning rhythm. Hydration of red snapper oocytes began during the mid‐morning hours; c. 5 h was necessary for oocytes to become fully hydrated and ovulation occurred no more than 5 h after oocytes attained full hydration. Appearance of fresh postovulatory follicles after 1330 hours and the absence of hydrated oocytes after 1830 hours signified that red snapper spawning occurred during this 5 h period. In addition, evidence of a peak in spawning was seen near 1600 hours. Postovulatory follicles degenerated within a 24 h time period. A lunar spawning cycle was not evident.
Egg and larval quality of red snapper, Lutjanus campechanus from natural spawns of domesticated brooders and hormone-induced spawns of wild fish were compared. Eggs and larvae from natural spawns were found to be more viable in terms of fertilization, hatching and survival rate. Also, eggs from natural spawns were larger, and eggs and recently hatched larvae had larger oil-globule. These findings indicate that natural spawning of red snapper can be a sustainable and reliable source of good quality eggs.
Red snapper, Lutjanus campechanus, were induced to ovulate following injections of Human Chorionic Gonadotropin (HCG). Females were injected initially with 1.1 IU/g body weight. When subsequent injections were necessary, 0.55 IU/g of body weight was used. Ovulation occurred between 42 and 56 h following injection. Eggs were wet stripped and fertilized simultaneously with sperm from two males. Initial mitosis was detected 30 min post fertilization. Hatching occurred in 20 h at 27°C.
Sex ratio, size at maturity, reproductive periodicity, ovarian development pattern, and spawning ground data for red snapper Lutjanus campechanus from the southern Gulf of Mexico were analyzed to understand this species' reproductive biology throughout its geographical distribution. Red snapper were sampled in 1999 and 2000 from commercial fishery catches taken on Campeche Bank at depths ranging from 43 to 130 m. Overall sex ratio (male: female) and sex ratios by size-class did not differ significantly from a 1:1 ratio. First maturity was at a slightly smaller size in males (24.2 cm total length [TL]) than in females (28.3 cm TL), and maximum length percentages at first maturity were 28% for males and 34% for females. The length at which maturity was attained in 50% of females (L50) was 31.4 cm TL. The Campeche Bank red snapper stock had a protracted spawning period from February to November, with a spawning peak occurring in early fall. Vitellogenic oocytes were continually recruited from previtellogenic oocytes during the entire spawning season, with no gap between each oocyte development stage. This means that red snapper ovaries are asynchronous and that the species can be considered a heterochronal (batch) spawner with indeterminate annual fecundity. Females in spawning condition were collected from both the northeastern and northwestern areas of Campeche Bank, near submerged or emergent coral reef structures, and at depths between 48 and 117 m. These results generally agreed with those for red snapper stocks in others regions of the Gulf of Mexico and the Atlantic Ocean off the southeastern United States. However, reproductive periodicity in the Campeche Bank red snapper stock apparently displayed more of an insular pattern of extended spawning in comparison with the typical continental pattern of restricted spawning reported for other regions. The latitudinal differences observed in red snapper spawning seasons could also reflect a latitudinal gradient in the intensity of seasonal environmental constraints.
Red snapper (Lutjanus campechanus) spawned in captivity when held at temperatures and photoperiods which approximated normal conditions in the Texas Gulf of Mexico region. Multiple spawns were observed in May and June, 1978.
Two experiments addressed the spontaneous spawning of red snapper, Lutjanus campechanus, under controlled temperatures and photoperiods and the effect of broodstock diets supplemented with oils rich in polyunsaturated fatty acids. In Experiment 1, broodfish were fed a standard diet (ST1) and one enriched with menhaden oil (ER1) over a 355-d period. ER1-influenced egg fatty acid profile, however, did not positively influence egg production. Both diets produced highly viable eggs and larvae but results varied within treatments. In Experiment 2, broodfish were fed either a standard diet (ST2) or one supplemented with oils (ER2) rich in docosahexaenoic and arachidonic acid using a 203-d cycle. Both treatments produced eggs but fertilization rates ranged 0–10%. There was no clear influence of the diets on egg fatty acid profiles. These results indicate that red snapper can spawn spontaneously in tanks under controlled environmental conditions and produce viable eggs and larvae when fed diets based on squid, shrimp, and fish. The fatty acid composition of the diets was reflected in the eggs to some degree, but the oil enrichments did not further enhance the reproductive performance and egg quality under the conditions of this study.
Domesticated male striped bass were selected as high cortisol stress responders (HCR) or low cortisol stress responders (LCR) by ranking mean 1-h post-stress plasma cortisol levels following a 2-min standardized net challenge once per month for four consecutive months. During the selection period, HCR and LCR fish maintained a significant divergence in post-stress cortisol levels, but these differences were abolished coincident with the onset of sexual maturation. LCR fish stressed monthly during gonadal maturation and weekly during the spawning season had plasma testosterone (T) and 11-ketotestosterone (11-KT) levels 3-5 times lower than stressed HCR fish. During the simulated spawning season, plasma cortisol and glucose levels were moderately elevated but similar in HCR and LCR fish. There were no differences in sperm quality between HCR and LCR males; however, more HCR fish began spermiating earlier and maintained a spermiation response longer than LCR fish. There were no significant differences in weight, length or coefficient of condition, but HCR fish had a significantly greater specific growth rate on two sample intervals when compared to LCR fish. These results show that male striped bass selected for low cortisol stress responsiveness and exposed to repeated stress have diminished circulating levels of T and 11-KT associated with a shorter duration spermiation response when compared to males selected for high cortisol stress responsiveness. The data suggest that LCR male striped bass subjected to significant stress during maturation and spawning may have impaired reproductive performance. (c) 2005 Elsevier B.V. All rights reserved.
This paper is a review of the effects of stress on reproduction in fishes. I hope to further the development of the concepts of allostasis and hormesis as relevant to understanding reproduction in general and in fish in particular. The main contentions I derive in this review are the following: Stressors affect fish reproduction in a variety of ways depending on the nature and severity of the stressor. The effects are transduced through a hormonal cascade initiated by perception of the stressor and involving the hypothalamus–pituitary–interrenal axis, the catecholamines, and also cytokines. Mounting a stress response and resisting a stressor is an energetically costly process, including costs associated with allostasis, attempting to reset homeostatic norms. Responses in emergency situations (e.g., being chased by a predator or a net) can be different from those where fish can cope (e.g., being in a more crowded environment) with a stressor, but both situations involve energy re-budgeting. Emergency responses happen in concert with the onset of energy limitations (e.g., the fish may not eat), while coping with allostatic overload can happen in a more energy-rich environment (e.g., the fish can continue to eat). Low levels of stress may have a positive effect on reproductive processes while greater stress has negative effects on fish reproduction. The concept of hormesis is a useful way to think about the effect of stressors on fish reproduction since responses can be nonmonotonal, often biphasic.
Control of reproductive function in captivity is essential for the sustainability of commercial aquaculture production, and in many fishes it can be achieved by manipulating photoperiod, water temperature or spawning substrate. The fish reproductive cycle is separated in the growth (gametogenesis) and maturation phase (oocyte maturation and spermiation), both controlled by the reproductive hormones of the brain, pituitary and gonad. Although the growth phase of reproductive development is concluded in captivity in most fishes-the major exemption being the freshwater eel (Anguilla spp.), oocyte maturation (OM) and ovulation in females, and spermiation in males may require exogenous hormonal therapies. In some fishes, these hormonal manipulations are used only as a management tool to enhance the efficiency of egg production and facilitate hatchery operations, but in others exogenous hormones are the only way to produce fertilized eggs reliably. Hormonal manipulations of reproductive function in cultured fishes have focused on the use of either exogenous luteinizing hormone (LH) preparations that act directly at the level of the gonad, or synthetic agonists of gonadotropin-releasing hormone (GnRHa) that act at the level of the pituitary to induce release of the endogenous LH stores, which, in turn act at the level of the gonad to induce steroidogenesis and the process of OM and spermiation. After hormonal induction of maturation, broodstock should spawn spontaneously in their rearing enclosures, however, the natural breeding behavior followed by spontaneous spawning may be lost in aquaculture conditions. Therefore, for many species it is also necessary to employ artificial gamete collection and fertilization. Finally, a common question in regards to hormonal therapies is their effect on gamete quality, compared to naturally maturing or spawning broodfish. The main factors that may have significant consequences on gamete quality-mainly on eggs-and should be considered when choosing a spawning induction procedure include (a) the developmental stage of the gonads at the time the hormonal therapy is applied, (b) the type of hormonal therapy, (c) the possible stress induced by the manipulation necessary for the hormone administration and (d) in the case of artificial insemination, the latency period between hormonal stimulation and stripping for in vitro fertilization.
Endocrine manipulations of spawning in cultured fish: from hormones to genes–8 8 Red snapper gametogenesis in captivity A Bardon-Albaret et al
- Y Zohar
- C Mylonas
Zohar Y. & Mylonas C. (2001) Endocrine manipulations of spawning in cultured fish: from hormones to genes. Aquaculture 197, 99–136. © 2013 John Wiley & Sons Ltd, Aquaculture Research, 1–8 8 Red snapper gametogenesis in captivity A Bardon-Albaret et al.Aquaculture Research, 2013, 1–8
Stock assessment of Red Snapper in the Gulf of Mexico – SEDAR update assessment report. Miami FL P. 224 Available at http://www. sefsc.noaa.gov/sedar/Sedar_Workshops
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