Egg size and larval development in Central Amazonian fish

The relationship between larval development and egg size was studied in 14 species of Central Amazonian fish (seven characiforms, five cichlids and two siluriforms). Egg size was measured as yolk dry weight at activation (egg minus chorion). Larval development was measured as larva] dry weight and age (h from activation) at the developmental stages. Egg size explained most of the variability of larval body weight and total larval weight at hatching, pectoral bud formation, eye pigmentation, jaw formation, swimbladder inflation, onset of swimming, first feeding and maximum weight attained with exclusively endogenous feeding. Larval ages at these developmental stages were poorly related to egg size. Other variables, such as the weight-specific yolk caloric content of the eggs (cal mg⁻¹), spawning site (river or lake) and phyletic relationships had no effect on the remaining variance. These results suggest that the developmental stages considered were conservative among the species examined and that a sequence of stages occurs in the larval development of Amazonian larval fish. The resistance of the larvae to starvation was not related to egg size.     

Embryogenesis and larval development of migratory matrinchã Brycon orthotaenia Günther 1864 (Characiformes: Bryconidae)

The present study aimed to characterize the embryogenesis and larval development of matrinchã (Brycon orthotaenia), through the analysis of egg and larval morphology. Fertilized eggs had a mean diameter of 1.17 mm, with yolk occupying most of the egg (1.06 mm). Embryogenesis lasted for 15 hr at an average temperature of 27°C. At hatching, yolk-sac larvae measured 3.67 mm in mean standard length (SL). Pre-flexion, flexion and post-flexion larva had 5.01, 8.24 and 11.88 mm mean SL, respectively, with significant increases observed particularly in head length, head height, and eye diameter. The yolk persisted in the yolk-sac and pre-flexion stages (5.96 mm SL). The mouth opening could first be observed 13 hr after hatching, and cannibalism was observed 29 hr after hatching in pre-flexion larvae after absorption of the yolk sac; in such cases, the larvae had already developed teeth and a complete digestive tract. For an endangered species such as matrinchã, early life history studies are important because they provide researchers with a better understanding of critical stages of development and thus enhance captive management by rearing and restocking of the species.     

Functional morphology of embryonic development in the Port Jackson shark Heterodontus portusjacksoni (Meyer)

The oviparous Port Jackson shark Heterodontus portusjacksoni embryo has a long incubation of 10–11 months during which it undergoes major morphological changes. Initially the egg capsule is sealed from the external environment by mucous plugs in either end of the capsule. Four months into incubation, the egg capsule opens to the surrounding sea water. Fifteen stages of development are defined for this species, the first 10 occur within the sealed capsule, the remaining five after capsule opening to hatching. The functional significance of major definitive characters such as circulation within the yolk membrane and embryo, rhythmic lateral movement of the embryo, external gill filaments, heart activity, internal yolk supplies, egg jelly and the significance of the opening of the egg capsule are described. The egg jelly in the sealed capsule functions to mechanically protect the embryo during early development, however, it eventually creates a hypoxic environment to the embryo as the available oxygen is used up. This generates several physiological challenges to the developing embryo. It is able to overcome these problems by morphological changes such as increasing the effective surface area for gaseous exchange with the development of external gill filaments, fins and extensive circulation in both the embryo and attached external yolk sac. These adaptations become limiting as the embryo grows and respiratory needs outweigh the available oxygen. At this time, the mucous plugs dissolve and the capsule becomes open to the external environment.     

Embryonic growth and mobilization of energy and material during incubation in the checkered keelback snake, Xenochrophis piscator

We collected 20 checkered keelback snakes (Xenochrophis piscator) to study embryonic growth and mobilization of energy and material during incubation. Females laid eggs between late May and late June. The eggs were incubated at 27 degrees C (+/-0.3). One egg from each clutch was dissected at five-day intervals starting at oviposition. The mean incubation length at 27 degrees C was 48.9 days. We identified three phases of embryonic growth or yolk depletion in X. piscator. Phase 1, between oviposition and Day 20, was one of minimal transfer of energy and material from yolk to embryo. Phase 2, between Day 20 and Day 39-40, was characterized by increasingly rapid embryonic growth or yolk depletion. Phase 3, between Day 39-40 and hatching, was characterized by reduced embryonic growth or yolk depletion. Approximately 71% of dry mass, 53% of non-polar lipids and 66% of energy were transferred from the egg contents to the hatchling during incubation. Our data confirm that oviposition is not timed to coincide with the onset of rapid embryonic growth in oviparous squamate reptiles. The greater conversion efficiencies of energy and material from egg to hatchling in snakes can be attributed to their lower energetic costs of embryonic development and greater residual yolk sizes.     

Embryonic growth and mobilization of energy and material in oviposited eggs of the red-necked keelback snake, Rhabdophis tigrinus lateralis

We used the red-necked keelback (Rhabdophis tigrinus lateralis) as a model animal to study embryonic growth and mobilization of energy and material in oviposited snake eggs. Females (N=12) laid eggs between late May and early June. Eggs were incubated at 30 (+/-0.3) degrees C. One egg from each clutch was dissected at five-day intervals starting at oviposition. Incubation length averaged 27.9 days. Three phases of embryonic growth or yolk depletion could be detected in this study. The first phase, between oviposition and Day 10, was one of minimal transfer of energy and material from yolk to embryo. The second phase, between Day 10 and Day 22-23, was characterized by increasingly rapid embryonic growth and yolk depletion. The third phase, between Day 22-23 and hatching, was characterized by a gradual reduction in embryonic growth and yolk depletion. Approximately 73.6% of dry mass, 50.0% of non-polar lipids and 57.8% of energy were transferred from egg to embryo during incubation. Embryos withdrew mineral from the eggshell mainly during the last quarter of incubation. Our data show that oviposition does not coincide with the onset of rapid embryonic growth in oviparous species of squamate reptiles that are positioned midway within the oviparity-viviparity continuum, and that the greater conversion efficiencies of energy and material from egg to hatchling in snakes can be mainly attributed to their lower energetic costs of embryonic development and greater residual yolk sizes.     

Availability of avidin-bound biotin to the chicken embryo.

Avidin, an exceptionally stable protein in egg white, binds the vitamin biotin with very high affinity and can induce biotin deficiency when fed to animals. To determine if biotin bound to avidin is available to the chicken embryo, the fate of [3H]biotin complexed to avidin was monitored during embryonic development. The majority (greater than 85%) of the [3H]biotin was extraembryonic until the day before hatching, when embryos swallow egg white and withdraw the yolk sac into their abdomen. Thus, biotin in the egg white of chicken eggs contributes little to the biotin status of the chick prior to hatching. After hatching, much of the [3H]biotin was assimilated. About 30% of the total was found in the liver and kidneys by 4 days of age. The biotin in liver was associated with large proteins and not with avidin. In a separate experiment, biotin injected into the egg white of biotin-deficient eggs failed to increase embryonic development or hatchability. Both experiments suggest that biotin in egg yolk is the primary and virtually sole source of biotin for the chicken embryo.     

Developmental consequences of association with a photosynthetic substrate for encapsulated embryos of an intertidal gastropod

Aggregation of embryos in clutches that lack internal circulation can increase the risk of hypoxia by limiting gas exchange. As a result, limits on oxygen solubility and diffusion in water can constrain the size and embryo concentration of aquatic egg clutches. Hypoxia in egg masses can slow embryo development, increase mortality, and reduce size at hatching. The risk of hypoxia for embryos, however, can be reduced by association with photosynthetic organisms. We examined whether embryo development in egg ribbons of the cephalaspidean mollusk Haminoea vesicula is significantly influenced by oviposition on eelgrass (Zostera marina). Association with the photosynthetic substrate had marked effects on development relative to association with non-photosynthetic substrates, and the direction of these effects was mediated by light conditions. Under intermediate and high light levels, association with eelgrass accelerated embryo development, while under dim light, the presence of the macrophyte increased development rate and reduced hatchling shell size. Benefits of association with eelgrass at higher light levels likely result from oxygen production by eelgrass photosynthesis, while we attribute costs under low light to oxygen depletion by eelgrass respiration. Association with Z. marina also limited microphyte growth in egg ribbons of H. vesicula. In the field, measurements of light attenuation within an eelgrass bed showed that conditions under which benefits accrue to embryos are ecologically relevant and correspond to spatial patterns of oviposition on eelgrass in the field. The choice of a photosynthetic oviposition substrate under appropriate light conditions can improve embryo fitness by accelerating embryo development without compromising hatchling size and by reducing the potential for excessive and harmful fouling by microphytes.     

Über die Entwicklung der Eikapselvolumina bei verschiedenen Opisthobranchier-Arten (Mollusca,Gastropoda)

An attempt has been made to estimate the volumes of eggs and egg-capsules employing the formula for the rotation-ellipsoid, first after oviposition, second for the capsules during different stages of embryonic development until hatching. The results of the calculations permitted analysis of: (a) the relationship between egg-case volume and egg volume immediately after oviposition; (b) the size of capsules during development until hatching; (c) the relationship of the capsule volume at hatching in comparison to that after oviposition (enlargement-factor).Placida dendritica shows no increase in capsule volume during development.Gonidoris nodosa, Rostanga rufescens, Trinchesia viridis, Acanthadoris pilosa, Archidoris pseudoargus, Tritonia hombergi andAeolidia papillosa show a distinct increase in capsule volume at the time of velarcilia appearance. The degree of egg-case enlargement and the time of its beginning reveal interspecific differences; within some of the species, both also depend on the number of larvae present in the egg-case. The reasons for such behaviour are not yet known; some possible explanations are discussed.     

Embryo developmental events and the egg case of the Aleutian skate Bathyraja aleutica (Gilbert) and the Alaska skate Bathyraja parmifera (Bean)

Embryo development events were correlated with egg-case changes for the Aleutian skate Bathyraja aleutica and the Alaska skate Bathyraja parmifera . Yolk absorption underwent two phases: that of steady absorption during early development and that of rapid yolk absorption during the final development stages. Total length ( L _T) for 50% of the pre-hatching embryos egg-case jelly disappearance was 92·04 mm (range 81–102 mm) and 99·36 mm (range 81–100 mm) for B. aleutica and B. parmifera , respectively, allowing the inner chamber to open to seawater flow. The tail filament underwent three phases of growth: rapid elongation during early development (<100 mm embryo L _T), stasis of tail filament length during the remainder of embryo development and rapid absorption soon after hatching. Complete tail filament development coincided with the disappearance of egg-case jelly. Clasper buds first developed at embryos >70 mm L _T for both species and the sex ratio was 1:1 well before hatching. Egg cases that were devoid of an ova or developing embryo were c. 5·0 and 6·5% of the egg cases examined for B. aleutica and B. parmifera , respectively. Measurements showed that egg cases containing only egg jelly were smaller in both width and length than those possessing an ova. Embryo stages were punctuated with distinct events that correlated with egg case changes controlling the internal environment of the developing embryo.     

Seasonal variation in dry weight and elemental composition of the early developmental stages of Petrolisthes laevigatus (Guérin, 1835) (Decapoda: Porcellanidae) in the Seno de Reloncaví, southern Chile

In the Seno de Reloncaví, southern Chile, seasonal changes in dry weight (DW) and elemental composition (CHN) were studied in embryo (initial embryonic stage), newly hatched zoeae, and newly settled megalopae of a porcelain crab, Petrolisthes laevigatus. Samples were taken throughout the seasons of egg laying (March-December), hatching (August-February), and settlement (October–February). Values of DW and CHN per embryo or larva, respectively, were consistently minimum in the middle of each season and maximum near its beginning and end. Patterns of seasonal variation in early embryonic biomass may thus be carried over to larvae at hatching and, possibly, to the settlement stage. Such carry-over effects may be selectively advantageous, as zoeae released at the beginning or near the end of the hatching season face conditions of poor planktonic food availability in combination with low winter temperatures or decreasing temperatures at the end of summer (enforcing long development duration). Hence, an enhanced female energy allocation into egg production may subsequently translate to enhanced yolk reserves remaining at hatching, allowing for a larval development under unfavourable winter conditions. In summer, by contrast, plankton productivity and temperatures are generally high, allowing for fast larval growth and development. This coincides with minimal biomass and energy contents both at hatching and settlement. In conclusion, our data suggest that seasonal patterns in the biomass of early developmental stages of P. laevigatus may reflect phenotypic variability as an adaptive response to predictable variations in environmental conditions, allowing this species to reproduce in temperate regions with marked seasonality in water temperature and plankton productivity.     

Comparison of early life‐stage strategies in temperate freshwater fish species: trade‐offs are directed towards first feeding of larvae in spring and early summer

Based on the analysis of 12 egg and larval variables and temperature of 65 temperate freshwater fish species, the possible relationships between oocyte diameter, larval size at hatch, time and temperature were reassessed and the main early life‐stage strategies were described and compared. Time and degree‐days required to reach hatching and mixed feeding were weakly related to oocyte diameter and strongly to temperature. These results are chiefly because oocyte diameter and yolk reserves are weakly related and temperature strongly increases tissue differentiation rate, activity of hatching glands and embryo motility. Strong positive relationships were found between larval size and oocyte diameter and degree‐days for incubation. No relationship was found between larval size and degree‐days from hatching to mixed feeding and between degree‐days for incubation and degree‐days from hatching to mixed feeding. These last two results are chiefly because the developmental stages at hatching and at the onset of exogenous feeding are not fixed in ontogeny and are not directly related to either larval size or degree‐days for incubation, but more probably are species specific. Whatever the spawning season, which can occur almost all year long, the different trade‐offs at the early life‐stages ensure that most larvae are first feeding during spring, when food size and abundance are the most appropriate.     

Comparative approach to developmental analysis: the case of the dalyellid flatworm, Gieysztoria superba

Dalyellida represents a taxon of small rhabdocoel flatworms that occur in freshwater habitats all over the world. Combining histology and electron microscopy we have analyzed the embryonic development of a new dalyellid species, Gieysztoria superba, in order to obtain more comparative data pertaining to morphogenesis and organogenesis in flatworms. We have used a morphological staging system that we recently introduced for another rhabdocoel, Mesostoma lingua (Younossi-Hartenstein et al., 2000). Our data show that in many fundamental respects, such as the irregular cleavage, mesenchymal embryonic primordium, and lack of gastrulation movements, Gieysztoria is highly similar to Mesostoma. During cleavage (stages 1 and 2) the embryo is located in the center of the egg where it is surrounded by a layer of yolk cells. Cleavage leads up to a solid, disc shaped cell cluster. During stage 3, the embryo migrates to the ventral side of the egg and acquires bilateral symmetry. Stages 4/5 sees the emergence of the first organ primordia, the brain, epidermis and pharynx. A peculiar invagination of the epidermal layer pushes the embryo back into the center of the yolk ("embryonic invagination"). Organogenesis takes place during stages 5 and 6 while the embryo is invaginated. A junctional complex, consisting initially of small septate junctions, followed later by a more apically located zonula adherens, is formed in all epithelial tissues, including epidermis, protonephridia, and pharynx. During late stages (6-8), Gieysztoria embryos evert back to the surface where the epidermal primordium expands and grows around the yolk to close dorsally. During this phase of development cytodifferentiation of the different organ systems takes place. Stage 7 is characterized by the appearance of eye pigmentation, brain condensation and spindle shaped myocytes. Stage 8 describes the fully dorsally closed and differentiated embryo. In comparison to other rhabdocoels, including Mesostoma, Gieysztoria exhibits a precocious differentiation of an intestinal epithelium and male genital apparatus. In Mesostoma, these structures are formed post hatching.     

Spawn and development of the olivid gastropod Olivancillaria carcellesi from north Patagonia,Argentina

Olivancillaria carcellesi occurs in shallow sandy shores from north Patagonia, in intertidal and subtidal sandy bottoms. Females of O. carcellesi exhibited a remarkable specificity for spawning on the shells of living males and females, indiscriminately, of the buccinanopsid Buccinastrum deforme, measuring 26.9 ± 4.7 mm in shell length. The egg capsule was semispherical and attached to B. deforme shells by a small elliptical and wide base. The capsule was translucid when spawned, with a thick and semirigid wall and a hatching aperture of 1.8 ± 0.1 mm (n = 111) in diameter. Each egg capsule contained a single egg that measured 1367 ± 34 μm (n = 5) in diameter before cleavage. The embryo developed a small bilobed velum and an operculum, which were both lost before hatching as a crawling juvenile of 1762 ± 47 μm (n = 28) in shell length. As in other species in the genus, the eggs of O. carcellesi are among the largest in the caenogastropods with direct development. The time from oviposition to hatching is estimated to be approximately 6 months.     

Vibration analysis on incubating eggs and its relation to embryonic development

Coucke (1998) was the first to use acoustic resonance analysis to monitor embryo development in chicken eggs. He remarked that at around 100 hours of incubation, the course of the resonant frequency and damping changed abruptly in the case of fertile eggs. He also showed that these changes were related to a physiologic event during early embryonic development. The objective of our study is to monitor the course of the vibration parameters during the early incubation of chicken eggs and to relate these changes to egg and embryo characteristics. A total of 72 Hybro eggs were incubated vertically in a small incubator at standard conditions. Several egg parameters were measured before incubation. During the early stages of incubation the vibration behavior of these eggs was monitored. The time at which the damping of the vibration suddenly changed, the diameter of the eggs and their interaction were found to be significant explanatory variables in order to predict hatching time. A correlation coefficient r of 0.72 was obtained.     

Metabolic fate of yolk fatty acids in the developing king penguin embryo

This study examines the metabolic fate of total and individual yolk fatty acids (FA) during the embryonic development of the king penguin, a seabird characterized by prolonged incubation (53 days) and hatching (3 days) periods, and a high n-3/n-6 polyunsaturated FA ratio in the egg. Of the approximately 15 g of total FA initially present in the egg lipid, 87% was transferred to the embryo by the time of hatching, the remaining 13% being present in the internalized yolk sac of the chick. During the whole incubation, 83% of the transferred FA was oxidized for energy, with only 17% incorporated into embryo lipids. Prehatching (days 0-49), the fat stores (triacylglycerol) accounted for 58% of the total FA incorporated into embryo lipid. During hatching (days 49-53), 40% of the FA of the fat stores was mobilized, the mobilization of individual FA being nonselective. At hatch, 53% of the arachidonic acid (20:4n-6) of the initial yolk had been incorporated into embryo lipid compared with only 15% of the total FA and 17-24% of the various n-3 polyunsaturated FA. Similarly, only 32% of the yolk's initial content of 20:4n-6 was oxidized for energy during development compared with 72% of the total FA and 58-66% of the n-3 polyunsaturated FA. The high partitioning of yolk FA toward oxidization and the intense mobilization of fat store FA during hatching most likely reflect the high energy cost of the long incubation and hatching periods of the king penguin. The preferential partitioning of 20:4n-6 into the structural lipid of the embryo in the face of its low content in the yolk may reflect the important roles of this FA in tissue function.     

Growth and uptake of mineral by embryos of the direct-developing frog Eleutherodactylus coqui

Embryos of the direct-developing frog Eleutherodactylus coqui take up small quantities of yolk and yolk mineral early in incubation but increase their uptake of yolk reserves at later stages of development. Growth and accumulation of calcium and magnesium by embryos also occur slowly at first and at a higher rate later. Accumulation of calcium and magnesium by embryos is largely a function of variation in size of embryos, but uptake of phosphorus is unrelated to size. Althrough patterns of growth and uptake of mineral by embryonic coquis resemble those for embryos of oviparous amniotes, embryonic coquis do not deplete the yolk of its nutrients to the same degree. Thus, residual yolk of coqui hatchlings contains a high percentage of the nutrient reserves originally present in the egg. This difference between embryonic coquis and embryos of oviparous amniotes may indicate that transfer of nutrients from yolk to embryo becomes limiting during the grwoth phase. Alternatively, some aspects of the neurologic system are so poorly developed at hatching that coqui may not be able to find prey effectively. A large nutrient reserve could sustain hatchling while the neurologic system continues to mature.     

西藏巨须裂腹鱼早期发育特征

巨须裂腹鱼(Schizothorax macropogon)隶属裂腹鱼亚科, 裂腹鱼属, 是西藏特有经济鱼类, 因过度捕捞, 其种群数量和分布面积下降, 在2009年中国红色名录评为“濒危”等级。研究通过研究巨须裂腹鱼早期发育特征, 旨在为该鱼的科学养护提供技术支撑。结果表明: 巨须裂腹鱼受精卵直径3.0—3.2 mm, 遇水开始具有微黏性, 随后脱黏, 经过准备卵裂阶段、卵裂阶段、囊胚阶段、原肠胚阶段、神经胚阶段、器官分化阶段、 孵化阶段, 在水温10℃的条件下, 经过460.67h孵化出来。初孵仔鱼体长9.9—1.1 mm, 心率48—50次/min, 鳃盖骨清晰可见, 下颌原基、尾鳍下骨原基可见。第2天鼻凹出现; 第3天肝胰脏原基出现; 第4天鳃耙、肩带原基出现; 第6天仔鱼上下颌开始张合; 第7天心血管分化结束, 仔鱼开始进入混合营养期; 第14天鳔一室和体侧色素带形成; 第26天肋骨原基出现; 第35天鳔二室出现, 卵黄囊耗尽; 第63天背鳍分化结束; 第83天臀鳍分化结束。巨须裂腹鱼胚胎具有独特的发育时序: 体节的出现先于胚孔封闭, 是对高原环境的一种适应和进化。     

Yolk sac development in lizards (Lacertilia: Scincidae): New perspectives on the egg of amniotes

Embryos of oviparous reptiles develop on the surface of a large mass of yolk, which they metabolize to become relatively large hatchlings. Access to the yolk is provided by tissues growing outward from the embryo to cover the surface of the yolk. A key feature of yolk sac development is a dedicated blood vascular system to communicate with the embryo. The best known model for yolk sac development and function of oviparous amniotes is based on numerous studies of birds, primarily domestic chickens. In this model, the vascular yolk sac forms the perimeter of the large yolk mass and is lined by a specialized epithelium, which takes up, processes and transports yolk nutrients to the yolk sac blood vessels. Studies of lizard yolk sac development, dating to more than 100 years ago, report characteristics inconsistent with this model. We compared development of the yolk sac from oviposition to near hatching in embryonic series of three species of oviparous scincid lizards to consider congruence with the pattern described for birds. Our findings reinforce results of prior studies indicating that squamate reptiles mobilize and metabolize the large yolk reserves in their eggs through a process unknown in other amniotes. Development of the yolk sac of lizards differs from birds in four primary characteristics, migration of mesoderm, proliferation of endoderm, vascular development and cellular diversity within the yolk sac cavity. Notably, all of the yolk is incorporated into cells relatively early in development and endodermal cells within the yolk sac cavity align along blood vessels which course throughout the yolk sac cavity. The pattern of uptake of yolk by endodermal cells indicates that the mechanism of yolk metabolism differs between lizards and birds and that the evolution of a fundamental characteristic of embryonic nutrition diverged in these two lineages. Attributes of the yolk sac of squamates reveal the existence of phylogenetic diversity among amniote lineages and raise new questions concerning the evolution of the amniotic egg. J. Morphol. 278:574–591, 2017. © 2017 Wiley Periodicals, Inc.