Sex differences in embryo development periods and effects on avian hatching patterns

Competitive interactions among siblings are an important determinantof parental fitness. These are strongly influenced by relativeoffspring size and therefore also by the extent to which parentscan influence offspring size hierarchies. The temporal patternof hatching in an avian clutch has a large effect on size anddevelopmental disparities among chicks. Hatching spread is generallyassumed to be mainly determined by the onset of incubation inrelation to egg laying. However, the extent to which factorsother than incubation onset, such as development rate, alsoinfluence timing of hatching has received little empirical investigation.We compared incubation periods of male and female black guillemot(Cepphus grylle) embryos to ascertain whether the time takenfor an egg to hatch varies with embryo sex. Laying date andegg mass had no significant effect on incubation time, but maleembryos hatched on average a day sooner than did females. Theonset of incubation and hatching spread vary in black guillemots.However, in mixed-sexed clutches in which the first-laid embryois male, a faster development time of males should mean asynchronoushatching regardless of parental incubation regime. This wassupported by empirical investigation. These results demonstratethat factors other than incubation behavior can be importantin establishing avian hatching patterns. Whether these sex differencesin development rate are a result of constraints on the degreeof parental control, or an adaptive strategy to manipulate hatchingpatterns, remains to be established.     

Carotenoid plumage hue and chroma signal different aspects of individual and habitat quality in tits

We hypothesized that Blue Tits Cyanistes caeruleus and Great Tits Parus major from low quality habitat (small woods) would have less yellow ventral plumage than those from high quality habitat (large woods) because they moult faster and/or their diet contains fewer carotenoids. They moult faster because they moult later in the season and are subject to more rapidly shortening daylengths. We tested this using a database of the plumage coloration (chroma, hue and lightness) of birds breeding in woods of different sizes, by manipulating the speed of moult in captive Blue Tits, and by counting the abundance and size of caterpillars (the major source of dietary carotenoids) in the diet of nestlings. In accordance with our hypothesis, juveniles of both species (which moult about three weeks later than adults) were about 8% less saturated in colour (lower chroma) than adults, but there was no significant difference in chroma between habitats. However, both species did differ significantly in hue between large and small woods. Blue Tits forced to moult faster in captivity, at a rate similar to that caused by a month's delay in the start of moult, had yellow flank feathers that were 32% less saturated in colour than those allowed to moult more slowly. Blue Tit nestlings in large woods consumed 47% more caterpillar flesh (per gram of faecal material voided) than those in small woods, and Great Tit pulli 81% more. When habitat effects were controlled for in ANOVAs, Blue Tits mated assortatively on the basis of flank hue and Great Tits on the basis of flank lightness. Flank colour therefore has the capacity to provide information about the potential quality of both habitats, and individual birds, to potential colonists and sexual partners.     

Variation in maternal effects and embryonic development rates among passerine species

Embryonic development rates are reflected by the length of incubation period in birds, and these vary substantially among species within and among geographical regions. The incubation periods are consistently shorter in North America (Arizona study site) than in tropical (Venezuela) and subtropical (Argentina) South America based on the study of 83 passerine species in 17 clades. Parents, mothers in particular, may influence incubation periods and resulting offspring quality through proximate pathways, while variation in maternal strategies among species can result from selection by adult and offspring mortality. Parents of long-lived species, as is common in the tropics and subtropics, may be under selection to minimize costs to themselves during incubation. Indeed, time spent incubating is often lower in the tropical and subtropical species than the related north temperate species, causing cooler average egg temperatures in the southern regions. Decreased egg temperatures result in longer incubation periods and reflect a cost imposed on offspring by parents because energy cost to the embryo and risk of offspring predation are both increased. Mothers may adjust egg size and constituents as a means to partially offset such costs. For example, reduced androgen concentrations in egg yolks may slow development rates, but may enhance offspring quality through physiological trade-offs that may be particularly beneficial in longer-lived species, as in the tropics and subtropics. We provide initial data to show that yolks of tropical birds contain substantially lower concentrations of growth-promoting androgens than north temperate relatives. Thus, maternal (and parental) effects on embryonic development rates may include contrasting and complementary proximate influences on offspring quality and deserve further field study among species.     

Analysis of the origin and development of hatching gland cells by transplantation of the embryonic shield in the fish, Oryzias latipes

Hatching gland cells of the medaka, Oryzias latipes, have been observed to differentiate from the anterior end of the hypoblast, which seems to first involute at the onset of gastrulation. These results suggest that the hatching gland cells of medaka originate from the embryonic shield, the putative organizer of this fish. The present study investigated whether hatching gland cells really originate from the embryonic shield in the medaka. Transplantation experiments with embryonic shield and in situ hybridization detection of hatching enzyme gene expression as a sign of terminal differentiation of the gland cells were carried out. The analysis was performed according to the following processes. First, identification and functional characterization of the embryonic shield region were made by determining the expression of medaka goosecoid gene and its organizer activity. Second, it was confirmed that the embryonic shield had an organizer activity, inducing a secondary embryo, and that the developmental patterns of hatching gland cells in primary and secondary embryos were identical. Finally, the hatching gland cells as identified by hatching enzyme gene expression were found to coincide with the dye-labeled progeny cells of the transplanted embryonic shield. In conclusion, it was determined that hatching gland cells were derived from the embryonic shield that functioned as the organizer in medaka.     

Mechanism and cost of synchronous hatching

1. Synchrony in the timing of births is thought to have evolved as a general predator avoidance strategy. In turtles, synchronous hatching may facilitate group emergence from the nest, which in turn, may limit predation by diluting an individual's risk of predation or by simply swamping predators upon emergence. However, synchronizing hatching should not be easily achieved in natural nests because of thermal gradients affecting developmental rates.
2. We evaluated pipping synchrony in the painted turtle ( Chrysemys picta ), where the drive to hatch synchronously may be reduced, because in many populations, hatching and emergence are dissociated through hatchlings overwintering within a nest.
3. We also assessed developmental mechanisms through which synchrony occurs and explored potential trade-offs between pipping synchrony and individual fitness by determining potential short and long-term neuromuscular developmental costs to hatching prematurely. These data were also used to develop a theoretical model to determine how differential embryonic maturation rates affect hatching synchrony.
4. Underdeveloped embryos pipped much earlier than expected and at similar times to their more advanced sibs. In addition, a trade-off between hatching synchronously and neuromuscular development (motility) was evident several days after hatching and up to 9 months later, after the overwintering period.
5. Synchronous hatching is an ancestral trait in turtles, but its relevance today is not solely for predator avoidance in all species.
6. Abiotic factors during incubation (e.g. temperature regime and moisture) have long-term effects on reptiles during ontogeny but it is also clear that incubation behaviour is major factor for the persistence of these developmental costs.     

Variation in incubation effort during egg laying in the Mountain Bluebird and its association with hatching asynchrony

Females in many bird species reportedly begin incubation prior to clutch completion, but the nature of such incubation and the degree to which it varies among females remains undescribed for almost all species. We used continuous recording of nest‐cup temperatures to document incubation effort during egg laying at 57 Mountain Bluebird (Sialia currucoides) nests in a high‐elevation Wyoming population. We then asked whether such effort predicted the degree to which eggs hatch asynchronously. Although substantial egg heating could begin abruptly late in laying (previously reported as the norm for this species) or even after clutch completion, we found that most (>90%) females began incubation gradually, engaging in a few (usually 1–8), brief (<10 min) bouts of heating on the day they laid their first or second egg. Thereafter, females varied markedly in when they increased incubation effort and by how much. The onset of nocturnal incubation also varied, with females beginning to incubate at night after laying their prepenultimate, penultimate, or last egg and not always initially incubating through the night. As an index of the total amount of heat applied to eggs during laying, we calculated the cumulative number of degrees by which nest‐cup temperatures exceeded the threshold temperature required for embryonic development. This value varied by more than 150‐fold between nests and explained >50% of the variation in hatching asynchrony. Our results thus provide strong support for the widely held, but rarely tested, assumption that parent birds can have substantial control over the degree of hatching asynchrony by varying the amount of incubation done prior to clutch completion.     

不同温度对三叶虫萤卵孵化和初孵幼虫发育的影响

本文研究了三叶虫萤Emeia pseudosauteri在不同恒温设置和室内变温条件下卵孵化率和初孵幼虫存活率,并通过直接最优法和直线回归法计算出了三叶虫萤卵的发育起点温度和有效积温。结果表明:12~30℃恒温条件下,卵的孵化率随着温度升高显著下降(P<0.05),且均低于室内变温条件(P<0.05)下的孵化率;初孵幼虫在恒温15℃下的存活率最高,为73.13%;低于12℃和高于30℃恒温中初孵幼虫均无法存活;在恒温条件12~30℃下,卵的发育历期随温度升高而缩短,其中恒温12℃下最长,发育历期为42.96 d(n=3),恒温30℃下最短,发育历期仅12.75 d(n=3)。通过直接最优法计算出三叶虫萤卵的发育起点温度为3.52℃,有效积温分别为382.20 d·℃。上述结果为三叶虫萤的人工繁育提供了参考。     

Egg development time in the Zebra Finch Taeniopygia guttata varies with laying order and clutch size

As female birds are able to lay no more than a single egg each day, in those species producing larger clutches the first laid eggs may get a developmental head‐start over later eggs in the clutch. All other things being equal, the differential pattern of development across the clutch may contribute to hatching asynchrony and subsequent inequity in the competition between brood mates, and ultimately increase variance in the quality and fitness of first‐ and last‐laid offspring. It has been suggested that females might allocate resources differently across the laying sequence to moderate the developmental rate and hatching time of different embryos. We tested this theory in the Zebra Finch Taeniopygia guttata, a common model species for investigating maternal effects in birds. We removed 758 eggs from 160 nests shortly after they were laid and used artificial incubators to control for parental effects and monitor hatching times. Eggs from larger clutches consistently hatched sooner than those from average‐sized clutches, demonstrating that the intrinsic properties of an egg can alter the developmental time of embryos. There were also differences in the development time of eggs across the laying sequence, but these patterns were weaker, inconsistent and unrelated to sequential investment across the laying sequence in a straightforward way. This study indicates that maternal resource allocation to eggs across the laying sequence and across clutch sizes can influence development times and play a potentially important role in determining the competitive dynamics of broods.     

Abiotic factors influencing embryonic development, egg hatching, and larval orientation in the reindeer warble fly, Hypoderma tarandi

Wild-caught, tethered females of the reindeer warble fly, Hypoderma tarandi (L.) (= Oedemagena tarandi (L.)), (Diptera, Oestridae) were stimulated to oviposit on hairs of a reindeer hide. Newly laid eggs incubated at constant temperatures and relative humidities hatched within 3 days to 2 weeks, depending on the experimental conditions. Over a range of 7-40 degrees C, hatching only occurred between 20 and 37 degrees C. Eggs held at 100% relative humidity had lower hatchability and longer time to hatch relative to eggs held at 77% relative humidity. The average number of degree-days for hatching was 50.35. Between 20 and 33 degrees C there was a temperature-dependent linear trend in developmental rate, and the proportion of eggs hatching was highest, and least variable, at the mid-temperature ranges. The temperature range found in the natural host micro-habitat where H. tarandi commonly affix their eggs (close to the skin at the base of a host hair) was consistent with the experimental temperature treatments that produced the highest hatching rate. Newly emerged larvae displayed positive thermotaxis, while showing no phototaxic or geotaxic behaviour. Results indicate that constraints of the host environment, coupled with temperature-dependent hatching success, may impose a selective pressure on oviposition behaviour.     

The role of partial incubation and egg repositioning within the clutch in hatching asynchrony and subsequent effects on breeding success

The main mechanism to achieve hatching asynchrony (HA) for incubating birds is to start heating the eggs before clutch completion. This might be achieved through partial incubation and/or early incubation. Even in the absence of incubation behaviour during the laying phase, clutches still experience a certain degree of asynchrony. Recent studies have shown that eggs located in the centre of the nest receive more heat than peripheral ones during incubation. As eggs receiving more heat would develop faster, we hypothesized that HA should be shorter in nests where eggs were moved homogeneously along the centre–periphery space during incubation than in those nests where eggs repeatedly remained in the same locations, either centrally or peripherally. We explored the relative roles of egg repositioning and partial incubation in determining HA in wild birds by (1) removing eggs from 20 Great Tit Parus major nests on the day of laying and replacing them with fake eggs to avoid partial incubation, and returning them when full incubation began; (2) monitoring twice a day the position of each individually marked egg relative to the clutch centre during incubation, and estimating the coefficient of variation of the distances; and (3) determining HA in each nest. Preventing partial incubation reduced HA by 51% days in experimental nests. It also caused negative effects for the incubating females (lengthening the full incubation period) and positive effects for the brood (increasing fledging success). However, our hypothesis about the role of egg repositioning on HA was not supported: all the females moved the eggs with remarkable consistency, generally attaining a coefficient of variation of the distances around 33%, and it was not related to the HA experienced. We therefore conclude that partial incubation is an important factor regulating HA, and females compensate for the potential effects of differential heating by moving the eggs homogeneously within the clutch.     

Effects of oxygen,carbon dioxide,and nitrogen on hatching behavior and hatching time in the katydid,Eobiana engelhardti subtropica Bey-Bienko (Orthoptera: Tettigoniidae)

The trigger for the hatching behavior and determination of hatching time of the katydids, Eobiana engelhardti subtropica (Orthoptera: Tettigoniidae) have been shown to be influenced by light–dark signals or temperature. In this study, I investigated the effects of oxygen, carbon dioxide, and nitrogen on the hatching behavior and hatching time of the katydid. Eggs rarely hatched under a constant temperature of 25°C and hatched sporadically at a constant temperature of 15°C under continuous light in the air. However, when eggs were exposed to 100% oxygen or a mixture of oxygen and nitrogen (2:1 or 1:1), hatching occurred within a few seconds. Hatching behavior was directly triggered by high concentrations of oxygen. It was inhibited by exposure to 100% carbon dioxide, 100% nitrogen, or a mixture of oxygen and nitrogen (1:2). The hatching time, determined by the temperature fall (transfer from 25°C to 15°C), was delayed by these gases, and was reset by the transfer back of eggs to the air. This suggests the existence of a time-measuring mechanism that is triggered by the transfer of eggs to the air. These results, indicating that hatching behavior was directly triggered by high concentrations of oxygen and that hatching time was set by the transfer from carbon dioxide or nitrogen to the air, are new findings to the best of my knowledge.     

Quantitative staging of embryonic development of the tobacco hawkmoth,Manduca sexta

Summary A complete timetable of embryonic development of the tobacco hawkmoth,Manduca sexta (Lepidoptera: Sphingidae), is presented. Using living embryos, 20 developmental stages from oviposition to hatching are described with respect to their morphological and physiological maturation. This staging series provides a simple method to identify the stage ofManduca development during all phases of embryogenesis.     

Investigation of hatching and early post‐embryonic life of freshwater crayfish by in vitro culture,behavioral analysis,and light and electron microscopy

The late embryonic and early post‐embryonic life period of freshwater crayfish, which is the main time period of organogenesis, is poorly investigated because of the protective brooding behavior of crayfish mothers. A combination of in vitro culture, behavioral observations, and microscopic investigations of organs involved in hatching, attachment, exploration of the environment, and searching and processing of food yielded deeper insights in this important period of life. Experiments were performed with the robust parthenogenetic marbled crayfish. The following results were obtained: (1) Marbled crayfish can be raised in simple in vitro systems from 80% embryonic development to juvenile Stage 4 with up to 100% survival; (2) Hatching is prepared by chemical weakening of the egg shell and completed by levering actions of the hatchling's appendages; (3) The telson thread, a safety line that keeps the hatchling secured to the mother, is formed by secretions from the telson and the detaching inner layer of the egg case; (4) Molting Stage‐1 juveniles are secured by an anal thread that results from delayed molting of the hindgut; (5) Active attachment of the hatchlings to the maternal pleopods with their 1st pereiopods is achieved by an innate fixed action pattern; (6) In vitro, juveniles are motile from Stage 2 despite incomplete development of their balance controlling statocysts. Movement pattern and social behavior vary greatly among individuals; and (7) Feeding starts in Stage 3, when the mouthparts and the gastric mill are fully developed. Onset of feeding is innate and does not require maternal contributions. In vitro culture of the isogenic marbled crayfish is recommended for broader use in research because it enables not only time and stage‐specific sampling but also precisely timed experimental manipulations. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

Length of herring larvae in relation to age and time of hatching

The lengths of newly hatched herring Clupea harengus larvae were generally larger than the lengths of embryos released from eggs on the same day. Over subsequent days, the daily increase in length was higher in groups that were released from the eggs as opposed to groups that hatched naturally. Thus by the end of the hatching period (18 days after fertilization) there were no significant differences in mean lengths.