Ontogenetic variability of maternal effects in an iteroparous fish

Maternal effects have been observed to interact with genotypic and environmental influences to structure offspring phenotypes across a wide variety of taxa. In fishes, maternal effects may be especially important due to their potential influence on development and survival during early ontogeny – a period with high potential for population regulation. While previous studies have confirmed that maternal effects on offspring phenotype are common in fishes, the consistency with which they positively affect offspring fitness throughout early ontogeny remains largely unknown. We examined maternal effects on offspring fitness by quantifying relationships between maternal (length, mass and age), egg (diameter, mass and density) and larval traits (length, yolk‐sac volume and survival) in yellow perch (Perca flavescens). Consistent with several past studies, positive relationships among maternal and egg traits were evident. While egg mass was positively related to larval size at hatching, direct relationships between maternal and larval metrics were not apparent. Larval survival appeared to have two critical periods; in contrast with expectations, survival in the first 5 days posthatch was strongly negatively related to female size and age, while survival over the following 9 days was unrelated to maternal traits. Throughout the study, survival was positively related to yolk‐sac volume. Our unexpected observation of a negative relationship between maternal size and age and initial larval survival indicates that maternal effects may not be consistent throughout larval ontogeny. In fact, maternal effects appear to be dynamic influences on offspring fitness, and may have complex effects on individual‐ and population‐level reproductive success.     

Bigger is not always better: egg size influences survival throughout incubation in brown trout (Salmo trutta)

Classical optimality models for the evolution of egg size predict a single optimal investment for females inferior to the optimal investment for offspring because of the egg size–fecundity trade‐off and the assumption that ‘bigger is better’ for offspring fitness. Such models do not satisfactorily represent observed within‐population variation in egg size. We measured the influence of maternal investment in egg size on offspring survival in brown trout. Individual measures of egg size, metabolism and survival at different temperatures throughout ontogeny were carried out. We then developed a survival model with regard to egg size, incubation temperature and observed metabolic rate. Small eggs were found to survive at higher rates than large eggs, and the egg size–survival relationship was found to differ among females in accordance with average metabolic rate measured at hatching. These results provide insights for the understanding of the evolutionary significance of egg size variations within a population.     

Brown trout spawning habitat selection and its effects on egg survival

Salmonid females invest heavily in reproduction, through gamete production, habitat selection and maternal care. Habitat selection and maternal care are expected to provide shelter for eggs against scouring and predators. However, females also tend to produce variable egg sizes, and this trait may interact with habitat quality to influence the survival of offspring. In this study, we aimed at evaluating the role of female habitat selection on egg survival conditional on individual egg size and female body size. We monitored female reproductive activity in two natural rivers for 3 years, in order to relate nest characteristics to female body size. Bigger females dug deeper nests at lower shear stress force. Right after the end of nest construction, we sampled a part of the eggs laid by each female, measured them individually, and placed them back using capsules within their original position in the nest. At time of hatching, the capsules within the nest were collected and individual egg mortality was assessed. Our results indicate that scouring was the main driver for mortality (75%) and that nest burial depth and shear stress force above the nest both influenced scouring. However, subsequent survival was influenced by neither nest characteristics, individual egg size, nor the interaction between both. It is therefore expected that traits or tactics that reduce nest scouring probability should be under strong selection.     

Impact of a new artificial shelter on Arctic charr (Salvelinus alpinus, L.) behaviour and culture performance during the endogenous feeding period

Shelter is of major importance in many species of fish both in the wild and in aquaculture. Sheltering behaviour of Arctic charr has been poorly studied in aquaculture. A new type of shelter made of PVC agricultural drain cut in half was tested on culture performance and behaviour during the endogenous feeding period. This device offered grooves where alevins could position themselves and lie in a vertical position. A first experiment compared fish with and without shelter in incubator compartments. All fish were measured at 122, 158, and 190 days post fertilization (dpf) and observed at 126, 139 and 157 dpf. Fish provided with shelter showed better growth performances, lower mortality and started first exogenous feeding about six days later compared to fish without shelter. These effects from shelter provision were also associated with much less mobility in fish provided with shelter. At 126 dpf, all fish provided with shelter were immobile while other fish displayed horizontal stationary body movement (86%) or swam against the water current (7%). At 157 dpf, 85% of fish without shelter were immobile compared to 95% in fish provided with shelter. Both categories displayed stationary body movements. In most cases, there was one single fish per groove and a stable average value of 2.4 grooves was maintained between two successive fish throughout the study. The second experiment was a preference test where the fish were placed in similar compartments but occupied by a half shelter. We found that 61% of the fish were located under the shelter at 122 dpf while at 157 dpf, 58% were on the shelter and 42% out of the shelter. The present results revealed Arctic charr behavioural characteristics in the presence of a new type of artificial shelter at very early stages of development. This shelter enables the fish to stabilize in a vertical position without producing any movement and to choose by itself its favorite location throughout development. This device could be used to improve Arctic charr growth, performance and fish welfare during the endogenous feeding period.     

Individual variation in progeny size and quality in rainbow trout, Oncorhynchus mykiss (Walbaum)

Early life history traits of fish are very variable as a result of both genetic and environmental factors. In this study, we examine individual variation in early life history traits in progeny of seven females crossed with one male rainbow trout, Oncorhynchus mykiss (Walbaum). Individual eggs were followed from fertilization through hatching until death of the larvae by starvation. Larvae and yolksac size (size was shown to be a good indicator of energy content) increased with increasing egg size, but there were still differences between families after variation in egg size was accounted for. Incubation time was not correlated with egg size, and did not differ between families. The progeny from the different families utilized the available energy differently, as both longevity and growth-rate without food was independent of yolk-sac size, but strongly dependent on family. The observed between-family differences in early life history traits in rainbow trout were mainly caused by genetically based effects; egg size and thus probably egg quality, which differed strongly bet ween females, could not adequately explain these differences.     

Effects of LHRHa treatments upon the timing of ovulation and upon egg and offspring quality in Arctic charr, Salvelinus alpinus (L.)

Abstract Five groups of Arctic charr, Salvelinus alpinus (L.), were studied, each group consisting of 13 females. The fish in four of the groups received a single intramuscular (IM) injection: three groups were injected with LHRHa in various forms and dosages, and one was injected with saline (control). The females in the fifth group were implanted with controlled-diffusion implants containing LHRH analogue. Ovulation in two of the treatment groups (30μg/kg D-Ala⁶ LHRH and 150μg/kg D-Trp⁶ LHRH) occurred earlier, and was better synchronized, than in the control group. The treatments did not significantly affect (1) the weight of eggs released from each female; (2) egg size, weight, or chemical composition; (3) mortality rates; (4) hatching times or the length of alevins. The fertilization rate in one of the treatment groups (150 μg/kg D-Trp⁶) was significantly lower than in the control group.     

Predicting egg size across temperatures in marine teleost fishes

Marine teleost fish species in colder environments generally produce larger eggs than those in warmer environments. This pattern is thought to reflect changes in the optimal strategy of allocation to offspring size and number across temperatures, yet quantitative assessments of this hypothesis are lacking. Here, we model optimal offspring size across temperatures in marine teleost fishes based on the trade‐off between offspring survivorship and number. In doing so, we derive quantitative predictions for the relationship of optimal egg size to temperature based on the size and temperature dependences of the growth and mortality, and hence survivorship, of eggs and larvae. Our model shows that smaller eggs are favoured at warmer temperatures largely because egg survivorship declines with both egg size and temperature. The predictions of our model (egg mass in grams = 0.013*e^{?0.11*T ºC}) were comparable to the observed interspecific relationship (0.0029*e^{?0.09*T ºC}; N = 221 spp.). Thus, our results provide insights into how temperature shapes the evolution of egg size in marine teleost fishes.     

Seasonal and interannual components of intrapopulation variation in clutch size and egg size of a darter

Abstract –  Previous studies have offered suggestive but sometimes conflicting glimpses at the range and patterns of seasonal and interannual variation in female darter life-history traits. The present study examined clutch-size and egg-size variation from a single Mississippi population of brighteye darters (Etheostoma lynceum ), collected at regular intervals over four sequential spawning seasons. Both life-history traits were significantly correlated with body size, and they both showed significant variation within and among breeding seasons. The overall intraseasonal trends in these traits involved an increase in clutch size (CS) and a decrease in egg size from early to late periods of the spawning season. Clutch size and egg size showed a weak but significant negative correlation, which was indicative of a trade-off between the two clutch parameters. Seasonal changes in temperature appear to be related to differing patterns of seasonal variation in egg size reported in the literature for darters. Inverse seasonal shifts in egg size and CS in the brighteye darter may represent adaptive phenotypic plasticity that allows females to produce larger, competitively superior offspring early in the reproductive season when there is low supply of food for them (parental investment hypothesis) or to produce larger eggs early in the reproductive season to ensure that each egg is adequately provisioned in the face of uncertainty (bet-hedging hypothesis) if the food available for the young is unpredictable early in the season. Consistent with theoretical predictions, egg size showed less phenotypic variability than CS.     

Otolith size differences during early life of dwarf and cannibal Arctic char (Salvelinus alpinus)

In Arctic and alpine lakes, Arctic char [Salvelinus alpinus (L.)] often form two distinct morphs: invertebrate feeders (‘dwarfs’) and piscivores (‘giant or cannibals’). Here, we test for early life history growth variation in dimorphic Arctic char as a proximate explanation for the observed life history variation between the two forms. Char were sampled in 11 alpine and Arctic Norwegian lakes. Dwarfs (defined as sexually mature char less than 15 cm long; N = 304) had a mean total length of 105 mm, whereas the typical cannibal (body length above 20 cm; N = 153) was 388 mm long. A positive correlation between egg size and otolith hatching ring were ascertained in a separate hatching experiment with brown trout (Salmo trutta) and it is assumed that this relationship also is valid for Arctic char, and otolith size was used as a proxy for length. Otolith hatching ring from Arctic char cannibals was larger (mean ± SD; 187 ± 24 μm) than those from dwarfs (mean ± SD; 164 ± 23 μm). There were only minor size differences between dwarfs and cannibals during the next three years, after which dwarfs usually matured. Two mutually nonexclusive, proximate explanations for the differentiation into separate morphs (dwarfs and cannibals) are therefore maternal effects and/or genetic based differentiation. The high catchability of large piscivorous char and low production in alpine and Arctic lake ecosystems may make these stocks particularly vulnerable to overexploitation.     

Dietary fatty acid enrichment during the spawning season increases egg viability and quality in Hippocampus hippocampus

Control of the reproductive cycle is essential to achieve a successful aquaculture industry. Seahorse reared in captivity often shows eggs of poor quality and low offspring survival due to unsuitable rearing and nutritional protocols. This study aimed to evaluate the effect of dietary enrichment, added exclusively during the spawning season, on the egg quality of Hippocampus hippocampus. The effect of enriching mysis throughout the spawning season was analysed in terms of female fecundity, egg viability, egg size and fatty acid profile. The results showed that fecundity was not affected by the enrichment of the diet, but egg viability was increased when females were fed the enriched mysis (84.9 ± 4.1% compared to 62.2 ± 9.4%). Moreover, the content of several PUFA (20:4n‐6, 18:2n‐6, 22:5n‐3, 22:5n‐6, sum of n‐6) decreased throughout the spawning season, especially in the last clutch, in eggs originated from females fed non‐enriched mysis. Eggs from females fed the enriched diet maintained the fatty acid profile throughout the spawning season. In conclusion, enrichment of the diet of H. hippocampus improved egg viability and avoided a decrease in the quality of eggs by maintaining PUFA content in the last clutches of the spawning season.     

Egg yolk nutritional constituents as indicators of egg quality in Atlantic halibut (Hippoglossus hippoglossus L.)

Variation in oocyte quality affects sustainability of finfish aquaculture products including Atlantic halibut (Hippoglossus hippoglossus L.). To have an insight into role of major egg yolk constituents in the oocyte quality, egg fatty acid (FA), amino acid (AA) and folate contents were related to normal blastomere symmetry, and fertilization and hatching success. Significant correlations were found between dihomo‐γ‐linolenic acid (DGLA, 20:3n6), palmitic acid (PA, 16:00) and docosapentaenoic acid (DPA, 22:5n3), and normal blastomere symmetry and survival success. Egg concentrations of myristic acid (MA, 14:0), oleic acid (OA, 18:1n9), stearidonic acid (SA, 18:4n3) and eicosadienoic acid (EDA, 20:2n6) explained 56 % variation in fertilization success. OA and EDA explained 70 % of variation in blastomere symmetry. Palmitoleic acid (POA, 16:1n7) and linolenic acid (LNA, 18:3n3) concentrations explained 57% of variation in hatching success. Egg valine concentrations correlated with fertilization rates, and aspartic acid and leucine correlated with normal blastomere symmetry. Alanine and valine concentrations explained together 45% of variation in fertilization. Glutamic acid and tyrosine concentrations explained 68% of variation in normal blastomere symmetry while serine, arginine and valine explained 36% of variation in hatching. These FAs and AAa may be potential indicators of oocyte quality in Atlantic halibut.     

Can timing of spawning explain the increase in egg size with female size in salmonid fish?

A common observation is that egg size increases with maternal size within populations. Several hypotheses have been proposed to explain this phenomenon. Most recently, it was suggested that the optimal egg size depends on female size due to correlations between (i) breeding time and egg size selection and (ii) female size and breeding time, and as such, the positive egg size–maternal size relationship represents an adaptive strategy. Here, we test the second of these two premises in two salmonid species, Atlantic salmon (Salmo salar) and coho salmon (Oncorhynchus kisutch) for which we have detailed breeding and egg size data. The body size of spawning females decreased throughout the season in coho salmon, but not in Atlantic salmon. Furthermore, we did not find a direct correlation between egg size and breeding time, which would also be expected if this premise was correct. Accordingly, breeding date does not appear to be as important as other factors in shaping among female differences in egg size.     

Disentangling density‐dependent effects on egg production and survival from egg to recruitment in fish

Understanding of density‐dependent effects is key to achieving sustainable management of self‐regulating biological resources such as fish stocks. Traditionally, density‐dependent effects on population abundance in fish have been considered to occur from hatching to recruitment, based on the paradigm of proportionality between spawning stock biomass and total egg production. Here, we demonstrate how the existence of intraspecific and interspecific density dependence in egg production changes the current understanding of density‐dependent processes in the life history of fish, by disentangling density‐dependent effects on egg production and survival from egg to recruitment, using sardine (Sardinops melanostictus, Clupeidae) and anchovy (Engraulis japonicus, Engraulidae) as model species. For sardine, strong intraspecific density‐dependent effects occurred in egg production, but no density‐dependent effects occurred or if any they were weak enough to be masked by environmental factors from hatching to recruitment. In contrast, for anchovy, interspecific density‐dependent effects occurred in egg production. In the survival after hatching, anchovy experienced stronger intraspecific density‐dependent effects than currently recognized. This analysis could overturn the current understanding of density‐dependent effects in the life history, highlighting contrasts between the effects on individual quality and population abundance and between the model species. We propose to reconsider the basis of fisheries management and recruitment studies based on the revised understanding of density‐dependent effects in the life history of the respective species.     

Comparative growth study of wild- and hatchery-produced Arctic charr (Salvelinus alpinus L.) in a coldwater recirculation system

The growth performance of Arctic charr of wild (W) and hatchery (H) origin was compared in a commercial coldwater recirculation system (Villmarksfisk, Bardu, 68°N, 19°E, Norway). The initial individual body mass was 115 g and similar between groups. The rearing temperature was 9.2 °C and the fish were held under continuous light (24:0 L:D). At the end of the experiment (day 240), the average body mass of the H fish was 451 g compared to 231 g in the W fish. The accumulated mortality of wild Arctic charr was about 40%; 10 times higher than the mortality of hatchery-produced Arctic charr (4%). The difference in growth performance and survival rate impose a great disadvantage of using this wild caught fish as compared to commercially available hatchery-produced Arctic charr in coldwater recirculation system. However, further improvements in the production chain (catching, live transport, quarantine, size grading, etc.) may still make production of wild caught Arctic charr profitable, especially as it demands a higher price in niche markets.     

A reference growth curve for nutritional experiments in zebrafish (<Emphasis Type="Italic">Danio rerio</Emphasis>) and changes in whole body proteome during development

Zebrafish is one of the most used vertebrate model organisms in molecular and developmental biology, recently gaining popularity also in medical research. However, very little work has been done to assess zebrafish as a model species in nutritional studies in aquaculture in order to utilize the methodological toolbox that this species represents. As a starting point to acquire some baseline data for further nutritional studies, growth of a population of zebrafish was followed for 15 weeks. Furthermore, whole body proteome was screened during development by means of bi-dimensional gel electrophoresis and mass spectrometry. Fish were reared under best practice laboratory conditions from hatching until 103 days post-fertilization (dpf) and regularly fed ad libitum with Artemia nauplii from 12 dpf. A growth burst occurred within 9–51 dpf, reaching a plateau after 65 dpf. Fork length and body weight were significantly lower in males than in females from 58 dpf onwards. Proteomics analysis showed 28 spot proteins differently expressed through development and according to sex. Of these proteins, 20 were successfully identified revealing proteins involved in energy production, muscle development, eye lens differentiation, and sexual maturation. In summary, zebrafish exhibited a rapid growth until approximately 50 dpf, when most individuals started to allocate part of the dietary energy intake for sexual maturation. However, proteomic analysis revealed that some individuals reached sexual maturity earlier and already from 30 dpf onwards. Thus, in order to design nutritional studies with zebrafish fed Artemia nauplii, it is recommended to select a period between 20 and 40 dpf, when fish allocate most of the ingested energy for non-reproductive growth purposes.     

Influence of egg size on the growth,onset of feeding,point-of-no-return,and survival of unfed Oreochromis mossambicus fry

The variation in egg size within and between egg clutches of O. mossambicus, and the subsequent influence of mean egg size on growth, feeding incidence and survival of unfed fry were investigated.The individual egg sizes within 90% of the egg clutches examined were normally distributed and the coefficient of variation of egg size within clutches ranged from 7.4% to 15.4%. Fry emerging from the small, medium and large egg size groups reached their maximum length and weight at 9, 9 and 12 days after hatching, respectively. Maximum attainable fry length and weight were significantly correlated with egg size (r = 0.885 and 0.947, respectively, with P < 0.01).Egg size had little influence on the onset of feeding. Fry were capable of exogenous feeding within 6 to 7 days of hatching. Fry originating from small and medium egg size classes reached the point-of-no-return at 15–16 days after hatching compared to 21 days for fry from the large egg size class. The mean survival time (ST₅₀) of fry on their yolk reserves was significantly correlated (r = 0.923; P < 0.01) with their original mean egg weight and ranged from 9.5 days for fry hatching from 0.91-mg eggs to 21 days for fry from 1.93-mg eggs.     

Minimally invasive surgical technique for egg collection from the Persian sturgeon, Acipenser persicus

A minimally invasive surgical technique (MIST) for the removal of ovulated eggs from Persian sturgeon Acipenser persicus was tested on broodstocks caught from the wild to determine whether it affected fecundity or hatching rates compared with the traditional stripping method of killing and removing the eggs (commonly used in hatchery). Morphological parameters of females, germinal vesicle (GV) position, weight of obtained egg, number of eggs/gram, fertilization rate, and percentage of hatching during incubation were not significantly different between the MIST and traditional stripping methods. Obtained ova were 4.8 ± 0.4 kg female⁻¹ in the MIST and 4.6 ± 0.5 kg female⁻¹ in traditional stripped groups, respectively; the fertilization rate was 83.4 ± 11.2% and 80.0 ± 7.2% in groups, respectively. The results of this study showed that the minimally invasive surgical technique approach is efficient, practical, and less stressful to Persian sturgeon broodstocks during artificial propagation than other reported egg collection procedures.     

Effect of hybridization on reproductive performance of Oreochromis karongae,Oreochromis shiranus and Oreochromis mossambicus

The study assessed the effect of hybridization on reproductive performance of Oreochromis karongae, Oreochromis shiranus and Oreochromis mossambicus for a period of 120 days. Number of eggs per batch, number of females spawned, relative fecundity, egg size, hatching period, hatchability and hatchling survival were assessed. The results revealed higher number of eggs per batch and relative fecundity in the crosses where O. shiranus and O. mossambicus were females than female O. karongae. The results also revealed that egg size, hatching period, hatchability and hatchling survival were species specific. Significant differences were noted for number of eggs and larvae produced by the three species (p < .05). Interspecific and pure crosses for the same female species did not differ significantly for the number of eggs per batch, relative fecundity, egg size, hatching period, hatchability and hatchling survival. However, number of female spawned was found to be higher in the interspecific crosses of female O. karongae than in pure cross of O. karongae. Findings from this study suggest that hybridization can be used to improve reproductive performance of O. karongae as the females spawned increased, and it is a value addition in aquaculture management of indigenous species.     

Improvement of common carp artificial reproduction using enzyme for elimination of egg stickiness

This study summarizes optimization of techniques for common carp artificial propagation including improvements of activation solution (AS), the process of insemination, and elimination of egg stickiness. The optimum gamete ratio for good fertilization and hatching rate ranged from 8490 to 23 672 spermatozoa per egg, when dechlorinated tap water was used. Optimal ratio between eggs (weight in g) and AS (in ml) was defined as 1:1 to 1:2. Different concentrations of AS such as NaCl from 0 to 34 mM (0–68 mOsmol kg^–1) did not change fertilization and hatching rates. An AS adopted for carp spermatozoa (45 mM NaCl, 5 mM KCl, 30 mM Tris–HCl, pH 8) was compared with other saline AS; only the 51 mM (102 mOsmol kg^–1) NaCl solution decreased fertilization and hatching rate. The AS containing 20 mM Tris–HCl at pH 9 increased fertilization and hatching rates compared to dechlorinated tap water of pH 7 or to AS of pH 6 and 7. Adhesiveness from the eggs was successfully removed by incubation in Alcalase DX (PLN 04715) using two successive steps with different enzyme concentrations. The first step with an enzyme concentration of 2 ml l^–1 was applied from 8 to 20 min after fertilization. Later in a second step, the best time for application of alcalase enzyme at a concentration of 20 ml l^–1 was for 45 and 60 s at 20 min after fertilization leading to fertilization and hatching rates of 80–87%. The α-Chymotrypsin (EC 3.4.21.1. Merck) was also found effective for elimination of stickiness. Results with α-Chymotrypsin enzyme indicate that the response to success in elimination of stickiness is highly variable mainly due to differences in the environment, quality of water and carp strains.     

Investigation of the temporal effects of spawning season and maternal and paternal differences on egg quality in Atlantic cod Gadus morhua L. broodstock

A better understanding of the parameters affecting egg quality and larval survival is of importance for continued development of cod broodstock and efficient husbandry practices. Decision tree analysis (DTA) was applied to analyse 3 years of egg quality data in an effort to extract the most important variables (i.e. predictors) in explaining differences in egg quality. The effect of three predictors (spawning time, maternal and paternal differences) has been studied on early cleavage pattern parameters, egg diameters, fertilization and hatching rates and has shown that females are the dominant variable and that time has a limited and inconsistent impact on the data. When using maternal, paternal differences and batch number (instead of spawning time) as predictors, the results confirm that no particular relationship is found between batch order (i.e. order in time) and egg quality. Moreover, batches with a higher egg quality show a consistency in the parameters assessed (i.e. batches with higher rates of normality in any parameter tend to be normal for other parameters). This is confirmed by the significant correlations found between cleavage parameters. Our results highlight that spawning time is of less importance than female parent contribution in ensuring high rates of fertilization and larval hatch, and maximizing general egg quality.