Accumulation of calcium and phosphorus in pigeon (Columba livia) embryos

Summary Calcium and phosphorus were measured in the yolk and albumen of fertile pigeon (Columba livia) eggs incubated for 0–17 days, and in embryos and hatchlings. Shell provided most of the calcium for skeletal mineralization of the embryos, whereas phosphorus was derived from the yolk and albumen. Mobilization of calcium from the shell to the embryo commenced at approximately day 11 of incubation, accumulating both in the embryo and the yolk sac. There was 1.4 times more calcium in squab yolk sacs than that contained in newly laid egg yolks. The results suggest that whereas general patterns of calcium and phosphorus accumulation during embryogenesis in altricial birds closely resemble those of precocial birds, calcium mobilization from the shell begins later, proceeds at a slower rate and results in a less mineralized hatchling.CIDA/NSERC Visiting Research Associate Permanent address: Department of Animal Science, University of Peradeniya, Peradeniya, Sri Lanka     

Suction among pickers: jaw mechanics,dietary breadth and feeding behaviour in beach‐spawning Leuresthes spp. compared with their relatives

Jaw mechanics and dietary breadth in California grunion Leuresthes tenuis and Gulf grunion Leuresthes sardina were compared with three other members of the tribe Atherinopsini to test whether these two species have evolved a novel jaw protrusion that might be associated with feeding narrowly on abundant prey near spawning beaches. Quantitative comparison of cleared‐and‐stained specimens of five members of the atherinopsine clade showed that, compared with false grunion Colpichthys regis, topsmelt Atherinops affinis and jacksmelt Atherinopsis californiensis, L. tenuis and L. sardina have longer, more downwardly directed premaxillary protrusion, expanded dentary and premaxillary bones, greater lower jaw rotation and larger premaxilla–vomer separation. Leuresthes tenuis showed greater differences than L. sardina in these features. Comparison of the gut contents of L. tenuis and A. affinis with zooplankton samples collected simultaneously with these fishes in the water column within 1 km of shore showed that, as predicted, L. tenuis fed predominantly on mysid crustaceans and had a narrower diet than A. affinis. High‐speed video analysis showed that L. tenuis exhibits a mean time to maximum jaw protrusion c. 2·5 times shorter than that of A. affinis. The grunion sister species, especially L. tenuis, have evolved suction feeding that may allow efficient feeding on common, evasive prey near spawning sites. The morphological traits seen in both species of Leuresthes signify a marked difference from their closest relatives in prey capture and suggest a type of jaw protrusion not yet seen in cyprinodontiforms or perciforms.     

Early development of johnny darter,Etheostoma nigrum,and fantail darter,E. flabellare,with a discussion of its ecological and evolutionary aspects

Synopsis Fantail darters,Etheostoma flabellare, have larger eggs with greater yolk volume than johnny darters,E. nigrum, and have a longer embryo period. This longer embryo period is associated with accelerated finfold differentiation, producing a larger, better formed individual at the onset of exogenous feeding. Developmental differences among these two species and the rainbow darter,Etheostoma caeruleum, primarily in timing of ontogenetic events, are described in detail. These differences in timing are considered largely early developmental phenomena as they affect embryos, larvae, and aievins but apparently not juveniles or adults. Demographic aspects of early life history were assessed using data from studies of Ontario streams. Differences in early survival among species appear to play an important role in recruitment of mature females, but cannot be attributed to parental care or egg size differences.     

Geographic variation in offspring size of a widespread lizard (Takydromus septentrionalis): importance of maternal investment

Geographic variation in offspring size is widespread, but the proximate causes of this variation have not yet been explicitly determined. We compared egg size and egg contents among five populations of a lizard (Takydromus septentrionalis, Günther, 1864) along a latitudinal gradient, and incubated eggs at two temperatures to determine the influence of maternal investment and incubation temperature on offspring size. The mean values for female size and egg size were both greater in the two northern populations (Chuzhou and Anji) than in the three southern populations (Lishui, Dongtou, and Ningde). The larger eggs were entirely attributable to the body size of females in the Anji population, but their increased size also stemmed from further enlargement of egg size relative to female body size in Chuzhou, the northernmost population sampled in this study. Eggs of the Chuzhou population contained more yolk and less water than those of southern populations. Despite the lower lipid content in the yolk, eggs from the Chuzhou population had higher energy contents than those from the two southern populations, owing to the larger egg size and increased volume of yolk. Hatchling size was not affected by incubation temperature, but differed significantly among populations, with hatchlings being larger in the Chuzhou population than in the other populations. Our data provide an inference that oviparous reptiles from cold climates may produce larger offspring, not only by increasing egg size but also by investing more energy into their eggs. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 59–67.     

Probable evolution of the coelacanth's reproductive style: lecithotrophy and orally feeding embryos in cichlid fishes and in Latimeria chalumnae

Synopsis The living coelacanth is a livebearer. Yolk seems to be the main source of nutrients and of oxygen to the embryo (fetus). Long before birth, young may also possibly feed orally on histotrophe secretion and egg debris. This type of reproduction evolved, as in most other fishes, from oviparity. The Carboniferous coelacanth Rhabdoderma exiguum had eggs of much lesser yolk volume and may represent an earlier form of oviparity with hiding, guarding or brooding type of parental care. The Jurassic coelacanth Holophagus (Undina) and the Cretaceous Axelrodichthys appear to have already evolved the internal-bearing style. Much of this evolutionary sequence is similar to that in cichlids. Ancestral cichlids are substrate tenders and nesters, with small eggs, little yolk and a feeding larva with indirect development. Mouthbrooding cichlids evolved a few, large eggs with denser yolk, direct development and, ultimately, orally feeding embryos while yolk is still in ample supply. Mixed feeding from yolk and orally ingested food in cichlids and in coelacanths is shown to be an enhanced mode of food delivery to the embryos over that from each source separately, in order to produce directly a better developed or larger young at the time of release, i.e. independence. Increase in egg size is regarded as an environmentally induced, altered pattern of yolk synthesis and an initial component of the epigenetic mechanism leading towards greater specialization. Carotenoids are incorporated within the yolk to assist the oxidative metabolism of the developing embryo.     

Parental food conditions affect sex-specific embryo mortality in the yellow-legged gull (Larus michahellis)

Different mortality of males and females during early post-hatching development in sexually size-dimorphic bird species is usually attributed to different nutritional requirements of the sexes, because mortality is mostly biassed toward the larger sex. We investigated whether sex-specific embryo mortality in the yellow-legged gull (Larus michahellis), a size-dimorphic seabird, depends on parental condition. To test this, we experimentally modified parental nutritional conditions by supplementary feeding of yellow-legged gulls during egg formation, to evaluate sex-biassed environmental sensitivity of gull embryos. We found that eggs were larger in supplemented clutches, but egg size did not affect embryo survival. Survival of male gull embryos was more related to parental food conditions than was survival of female embryos. Survival of male embryos in supplemented clutches was greater than in unsupplemented clutches whereas survival of female embryos was similar in both groups. Because size at hatching was similar in both sexes our results suggest that male phenotype disadvantage is not exclusively linked to the energy demands of size-dimorphic development at the embryo stage.     

Early development of marine catfishes (Ariidae): from mouth brooding to the release of juveniles in nursery habitats

The development and allometric growth patterns of the ariid catfishes Cathorops spixii and Cathorops agassizii were studied from neurula embryos to juveniles. The ontogenetic sequence revealed that prior to hatching, embryos of both species are well developed, and their axial and appendicular skeletons are well ossified. Embryos of both species grow slowly longitudinally, but positively allometric growth (growth coefficient, β₁ > 1) was observed in head width and eye diameter. It is hypothesized that these growth patterns might be related to functional priorities for the development of sensory organs, such as the inner ears (otoliths), the Weberian apparatus, eyes and nostrils, during the embryonic period. The first appearance of vertebrae and otoliths, as well as the ossification of otoliths and the Weberian apparatus, occur earlier in embryos of C. agassizii than in embryos of C. spixii. After hatching, mouth‐brooded free embryos of both species grow isometrically. Negatively allometric growth was observed in head width and eye diameter during the yolk‐sac period, which is expected given that the sensory organs are already formed. Free embryos of C. agassizii are distinguishable from those of C. spixii by their larger eyes, longer snouts, longer heads and heavier yolk sacs. The end of the yolk‐sac period is characterized by a direct change from free embryo to juvenile, without a true larval period. The juveniles of the two species can also be distinguished from each other by the larger eyes of C. agassizii compared with C. spixii, as in adult fishes.     

Geographic variation in avian incubation periods and parental influences on embryonic temperature

Theory predicts shorter embryonic periods in species with greater embryo mortality risk and smaller body size. Field studies of 80 passerine species on three continents yielded data that largely conflicted with theory; incubation (embryonic) periods were longer rather than shorter in smaller species, and egg (embryo) mortality risk explained some variation within regions, but did not explain larger differences in incubation periods among geographic regions. Incubation behavior of parents seems to explain these discrepancies. Bird embryos are effectively ectothermic and depend on warmth provided by parents sitting on the eggs to attain proper temperatures for development. Parents of smaller species, plus tropical and southern hemisphere species, commonly exhibited lower nest attentiveness (percent of time spent on the nest incubating) than larger and northern hemisphere species. Lower nest attentiveness produced cooler minimum and average embryonic temperatures that were correlated with longer incubation periods independent of nest predation risk or body size. We experimentally tested this correlation by swapping eggs of species with cool incubation temperatures with eggs of species with warm incubation temperatures and similar egg mass. Incubation periods changed (shortened or lengthened) as expected and verified the importance of egg temperature on development rate. Slower development resulting from cooler temperatures may simply be a cost imposed on embryos by parents and may not enhance offspring quality. At the same time, incubation periods of transferred eggs did not match host species and reflect intrinsic differences among species that may result from nest predation and other selection pressures. Thus, geographic variation in embryonic development may reflect more complex interactions than previously recognized.     

Waiting for a sign: extended incubation postpones larval stage in the beach spawning California Grunion <Emphasis Type="Italic">Leuresthes tenuis</Emphasis> (Ayres)

Unlike most embryos that hatch on a predetermined timetable, California Grunion Leuresthes tenuis can prolong the embryonic period up to three times longer than the time required for hatching readiness. L. tenuis are teleosts that spawn tidally around the highest spring tides of spring and summer, incubating eggs above the water line. Embryos are competent to hatch in 10 days, however they do not hatch until triggered by an environmental cue, agitation in seawater, as the next spring tides rise. This study examined the growth and survival of L. tenuis embryos and larvae that were all fertilized on the same day, then triggered to hatch after different durations of incubation, up to 35 days post fertilization. L. tenuis embryos that survive extended incubation had decreased yolk reserves and did not advance appreciably in morphological development, even when incubation time was extended to its upper limit. After extended incubation, length of hatchlings was significantly longer than hatchlings from the primary incubation time. Regardless of the duration of incubation, larvae provided food ad libitum grew rapidly and were not significantly different in length at three weeks post hatch. Dry mass increased over time and was not significantly different between larval groups within any post-hatch age. Larval growth and survival after one additional tidal cycle of incubation are not adversely affected, but longer incubation significantly decreases embryonic and larval survival. Large reproductive output, environmentally cued hatching, and plasticity in incubation duration enable L. tenuis to reproduce successfully in the unpredictable sandy intertidal ecosystem.     

Population genetic structure of annual and perennial populations of Zostera marina L. along the Pacific coast of Baja California and the Gulf of California

The Baja California peninsula represents a biogeographical boundary contributing to regional differentiation among populations of marine animals. We investigated the genetic characteristics of perennial and annual populations of the marine angiosperm, Zostera marina, along the Pacific coast of Baja California and in the Gulf of California, respectively. Populations of Z. marina from five coastal lagoons along the Pacific coast and four sites in the Gulf of California were studied using nine microsatellite loci. Analyses of variance revealed significant interregional differentiation, but no subregional differentiation. Significant spatial differentiation, assessed using θ_ST values, was observed among all populations within the two regions. Z. marina populations along the Pacific coast are separated by more than 220 km and had the greatest θ_ST (0.13–0.28) values, suggesting restricted gene flow. In contrast, lower but still significant genetic differentiation was observed among populations within the Gulf of California (θ_ST = 0.04–0.18), even though populations are separated by more than 250 km. This suggests higher levels of gene flow among Gulf of California populations relative to Pacific coast populations. Direction of gene flow was predominantly southward among Pacific coast populations, whereas no dominant polarity in the Gulf of California populations was observed. The test for isolation by distance (IBD) showed a significant correlation between genetic and geographical distances in Gulf of California populations, but not in Pacific coast populations, perhaps because of shifts in currents during El Niño Southern Oscillation (ENSO) events along the Pacific coast.     

A morphometric comparison of dissimilar early development in sibling species of Platynereis (Annelida,Polychaeta)

Summary Early development of Platynereis massiliensis was studied in serial sections of fixed embryos and in living or fixed embryos whose nuclei had been made visible with a fluorescent label. The unfertilized egg is an ellipsoid with three axes of differing length. The longest axis corresponds to the dorsoventral axis of the developing embryo. Egg volume is ten times that in the sibling species, P. dumerilii, mainly due to increased yolk content. The timing and spatial pattern of cleavage were observed from first cleavage to the 62-cell stage. Volumes of the blastomeres, their nuclei, their yolk-free cytoplasm and their yolk were determined from serial sections up to the 29-cell stage. In the P. massiliensis embryo, cell cycles are on average 3.7 times longer than in P. dumerilii; volume proportions among the blastomeres also differ and the macromeres containing the bulk of yolk are particularly large, but otherwise the cleavage patterns, differential segregation of yolk and yolk-free cytoplasm, and the histogenetic fates of the blastomeres are the same as in P. dumerilii. This equivalence of cell lineage and of cytoplasmic segregation mechanisms in both species, maintained in spite of the different appearance of the embryos, suggests functional importance of and selective constraint on these developmental features. The relatively accelerated divisions of the 2d cell line in P. massiliensis may be interpreted as the precocious development of cell lines which give rise to adult structures. Several structures, obviously functional in developing P. dumerilii, have lost their function in P. massiliensis: the egg contains few cortical granules, giving rise to only a moderate egg jelly layer in the zygote; prototroch cells develop cilia, but the heavy embryo is unable to swim; the larva develops three pairs of parapodia but, unlike the corresponding stage in P. dumerilii, is not capable of coordinate locomotion. This loss of motility is related to the brooding habit of the species developing inside the parental tube and is explained as the result of a switch from pelagic to benthic, protected reproduction in P. massiliensis. Offprint requests to: A.W.C. Dorresteijn     

The embryonic development of the primitive moth,Neomicropteryx nipponensis Issiki (lepidoptera,micropterygidae): Morphogenesis of the embryo by external observation

The micropterygid moth Neomicropteryx nipponensis belongs to the most primitive suborder Zeugloptera of the Lepidoptera. During embryogenesis the small circular germ disk formed on the ventral egg surface invaginates deeply into the yolk. It finally separates from the egg periphery or rudimentary serosa, and becomes a sac-shaped germ rudiment. Its anterior part later develops into the germ band, while its posterior part is the future amnion. Just before revolution of the embryo, the embryo assumes a completely superficial position beneath the yolk. Neither amnion nor serosa rupture during revolution; by completion of dorsal closure they have been incorporated into the yolk to form the secondary dorsal organ. The formation of the germ rudiment and embryonic membranes in N. nipponensis resembles those of swift moths, Endoclyta (suborder Monotrysia) and of the caddisflies, Stenopsyche (Trichoptera), but differs from those of ditrysian Lepidoptera. The secondary dorsal organ has never been found in any other lepidopteran embryos; however, it is formed in N. nipponensis and in the Trichoptera. The results of the present study strongly support the general phylogenetic views that the Zeugloptera have a close affinity to the Trichoptera.     

The embryo pancreas is a source of increased yolk amylase in the fertilized eggs of domestic fowls.

The amylases were studied in the yolk of fertilized eggs and in the pancreases of the embryos of domestic fowls. The amylase activity in the yolk increased markedly from 13 days of incubation until hatching, but the activity decreased when the embryos were taken out of the eggs. The isoamylases in the yolk and in the pancreas of the embryo were identical electrophoretically. The amylase occurs mainly in the pancreas of the embryo. We think that the increase in amylase activity in the yolk of fertilized eggs during incubation depends upon the accumulation of pancreatic amylase synthesized by the developing embryo in the egg.     

The beach‐spawning California grunion Leuresthes tenuis eats and digests conspecific eggs

Apparent egg cannibalism was investigated in the beach‐spawning California grunion Leuresthes tenuis. Three hypotheses were tested to determine whether L. tenuis regularly consumes and efficiently digests conspecific eggs. First, examination of the gut contents of adults collected at four spawning sites over two seasons showed that the intestines of most fish from all the sites (57–87%, n ≥ 30, each site) contained L. tenuis eggs. The two other hypotheses focused on digestion of the eggs. First, the force required to crush cannibalized eggs was significantly less than that for uncannibalized eggs (fertilized or unfertilized), indicating that ingestion weakens the egg chorions. Second, conspecific eggs fed to fish held in the laboratory visibly degraded as they passed through the gut. The eggs lost c. half of their protein content and about two‐thirds of their lipid content as they passed from proximal to distal regions of the gut, indicating that digestion occurred. Digestive enzyme activities of the gut further confirmed that L. tenuis can break down the contents of ingested eggs. Trypsin activity decreased and aminopeptidase activity increased posteriorly along the gut, whereas amylase and lipase activities exhibited less clear patterns by gut region. As far as is known, this study is the first to show that L. tenuis is an egg cannibal.     

Yolk androgens and embryo sex: maternal effects or confounding factors?

Maternal effects occur when offspring phenotype is affected by environmental factors experienced by the mother and, in egg-laying species, are often mediated via egg resources. There is currently great interest among behavioural ecologists in maternally allocated yolk androgens, especially their relationship with offspring sex and development. Such studies need embryonic tissue for sexing, however, requiring eggs to be incubated (usually for 3 days). Therefore, there are concerns about whether the androgen concentrations assayed reflect those allocated by the mother. In addition, studies showing sex biases in maternal allocation of androgens could be confounded if male and female embryos uptake or metabolise androgens at different rates. We ran a series of experiments using zebra finch (Taeniopygia guttata) eggs to address these potential confounding factors. First we showed, using eggs naturally incubated for up to 5 days, that eggs containing embryos had lower yolk androgen concentrations than eggs that had failed to form embryos. We then tested various hypotheses for this difference using controlled incubation treatments. Our results suggested that (a) embryo development causes the yolk to become progressively more diluted with albumin; and (b) between 3 and 5 days of incubation embryos start uptaking or metabolising androgens. Crucially, we found no decline in yolk androgen concentration at 3 days incubation, and no evidence for sex-specific rates of uptake or metabolism of androgens. This strongly suggests that yolk androgen levels up to 3 days incubation do reflect those allocated by the mother, and that studies of sex biased maternal allocation of yolk androgens are not confounded by sex differences in embryo development.     

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.     

Eggshell characteristics and yolk composition in the common cuckoo Cuculus canorus: are they adapted to brood parasitism?

The developmental rate of cuckoo embryos and their hatching size is greater than that of host species, which may require more nutrient resources in the egg and more intensive gas exchange during development. In the present study, we compared various egg characteristics of a brood parasite, the common cuckoo Cuculus canorus, and its frequent host, the great reed warbler Acrocephalus arundinaceus. As maternally‐derived testosterone is known to enhance growth rate of embryos and hatchlings, cuckoo eggs are expected to contain higher concentration of testosterone than host eggs. In addition, we expected higher concentration of antioxidants in cuckoo eggs to protect embryos from oxidative stress associated with accelerated growth. Our results showed that cuckoo eggs had thicker shells and higher pore density than great reed warbler eggs. Yolk was significantly heavier in cuckoo eggs and contained higher concentrations of carotenoids and vitamin E, however, yolk androgen and immunoglobulin concentrations were lower in cuckoo eggs as compared to great reed warbler eggs. We also examined whether eggshell colour was associated to egg quality, and detected a positive association between blue‐green chroma and yolk antioxidant concentration in both species, suggesting that eggshell colour reflects the antioxidant investment of the female into the eggs. Our results suggest that cuckoo females increase the size, growth rate and competitive ability of their young by providing them with more nutrients and more dietary antioxidants for embryonic development, and not through elevated yolk testosterone or antibody levels. In addition, increased porosity of cuckoo eggshells may allow embryos to develop more rapidly because of a greater capacity of gas exchange.     

Effect of algal diet and temperature on the embryonic development time of the rotifer Brachionus plicatilis in culture

The embryonic development times of two strains of Brachionus plicatilis (Bs and S-1) cultured on three different algal diets (Nannochloris oculata, N. maculata and Nannochloropsis gaditana), have been determined at 20°C, 25°C and 30°C. As expected, the embryonic development times decreased with increasing temperature in all cases. However, embryos from adults fed on N. gaditana tended to develop more slowly than those of individuals fed on the other algal species. Mean egg volume was also affected by diet, larger eggs being produced by females fed on N. gaditana. No obvious relationship between egg size and temperature was detected.Two principal factors seemed to affect the embryonic development time. The first was temperature which acts through its well known effect on metabolic rates. The second was maternal diet which probably affects development time through its effect on yolk content, as reflected in the size of the egg.     

Development and regulation of heart rate in embryos and hatchlings of gulls (Larus schistisagus and Larus crassirostris) in relation to growth

We compared the developmental patterns of mean heart rate in Larus crassirostris and L. schistisagus embryos and chicks with other avian species of different hatchling developmental modes. We proposed that, since mean heart rate is inversely related to fresh egg mass in all birds, larger species reached a higher fraction of their hatchling mean heart rate by the end of the early phase of incubation and that heart rate contributions to supplying the increasing metabolic demands during mid and late incubation phases were less important than in smaller avian species. Mean heart rate was essentially independent of age throughout the mid-incubation phase (33% of normalised incubation until pipping), but increased with time during early (L. schistisagus only investigated) and late-incubation phases in both species. The O₂ pulse of L. schistisagus embryos and chicks increased linearly with yolk-free body mass (log-log) after the early-phase of incubation until shortly before pipping, but was independent of body mass in the periods before and after. We conclude that a high heart rate in this first period is probably more important for increasing the circulation of nutrients to the embryo at a stage when extra-embryonic circulation to the yolk sac is limited by the size of the growing area vaculosa. Furthermore, large increases in mean heart rate during the late-incubation phase are probably important for increasing the cardiac output to hatching levels with onset of endothermy. However, mean heart rate is stable over the mid-incubation while O₂ pulse increases, suggesting that increases in stroke volume and other circulatory adjustments may be entirely responsible for the largest increases in O₂ transport during incubation of large avian species. Accepted: 18 May 2000     

Ontogenetic change in the response of the Gulf of California grunion, Leuresthes sardina (Jenkins & Evermann), to a salinity gradient

Larval and juvenile Gulf of California grunion, Leuresthes sardina (Jenkins & Evermann), hatched and reared in the laboratory, were subjected to salinity gradients in a Staaland salinity gradient device to determine their locomotive responses. Newly hatched prolarvae selected salinities in the range 15–24‰, while late postlarvae and juveniles preferred salinities in the range 45–54‰. Early postlarvae exhibited a bimodal preference, indicating that the behavioral change was in progress at that age. These behavioral responses may serve several functions in the physiological and behavioral ecology of the Gulf grunion.