Semi-altricial Species Research Articles

Maternal Buffering of Human Amygdala-Prefrontal Circuitry During Childhood but Not During Adolescence

Mature amygdala-prefrontal circuitry regulates affect in adulthood but shows protracted development. In altricial and semialtricial species, caregivers provide potent affect regulation when mature neurocircuitry is absent. The present investigation examined a potential mechanism through which caregivers provide regulatory influences in childhood. Children, but not adolescents, showed evidence of maternal buffering, such that maternal stimuli suppressed amygdala reactivity. In the absence of maternal stimuli, children exhibited immature amygdala-prefrontal connectivity. However, in the presence of maternal stimuli, children’s connectivity was more mature, resembling adolescents’ connectivity. Children showed improved affect-related regulation in the presence of their mothers. Individual differences emerged, with greater maternal influence on amygdala-prefrontal circuitry associated with stronger mother-child relationships and maternal modulation of behavioral regulation. These findings suggest a neural mechanism through which caregivers modulate children’s regulatory behavior by inducing more mature connectivity and buffering against heightened reactivity. Maternal buffering in childhood, but not adolescence, suggests that childhood may be a sensitive period for amygdala-prefrontal development.

Reversed hatching order, body condition and corticosterone levels in chicks of southern rockhopper penguins ( Eudyptes chrysocome chrysocome)

In altricial and semi-altricial species, asynchronous hatching gives the first chicks to hatch an initial advantage over other siblings and often leads to the elimination of the smallest chicks. Both baseline corticosterone and acute stress-induced corticosterone levels have been shown to be higher in food deprived chicks than in chicks fed ad libitum. However, first-hatched chicks have also been shown to exhibit higher corticosterone levels than last-hatched chicks, suggesting an influence of the initial differences between eggs on corticosterone levels. We subjected single-chicks of southern rockhopper penguins Eudyptes chrysocome chrysocome to a standardised capture-stress protocol. In this species having very dimorphic two-egg clutches, we examined whether corticosterone levels were different between the two chick categories and tested for the effect of body condition controlled by the chick category. Neither body sizes, nor corticosterone levels differed between A- and B-chicks at 18 days. In contrast to baseline corticosterone levels, acute stress-induced levels of corticosterone were negatively correlated to body condition: chicks with a good body condition had lower acute stress-induced levels of corticosterone than chicks with a poor condition, whatever the chick category. Our results do not support the idea that initial differences in egg characteristics could drive the difference in corticosterone levels between siblings. On the contrary, they show that the A-egg of rockhopper penguins has, when reared alone, the same intrinsic potential to develop into a fledged chick as the B-egg. Later differences in body condition appear to lead to variation in the acute stress-induced levels of corticosterone.

Age-related variation in the adrenocortical response to stress in nestling white storks ( Ciconia ciconia) supports the developmental hypothesis

The post-natal development of the adrenocortical response to stress was investigated in European white storks. Sixty wild nestlings aged 24–59 days old were subjected to a standardized capture and restraint protocol, and the time-course pattern of the response to stress was assessed through determination of circulating corticosterone in blood samples collected at five fixed times during the 45-min period following capture. The time course of the response was best fit to a third-order function of handling time, and showed a strong effect of age. Although age did not affect baseline titers and all birds showed a positive post-capture increase in circulating corticosterone, age had a positive effect on the relative increase from baseline titer, the recorded time to reach maximum level, and the acute concentration after 10 min following capture and restraint. While young nestlings displayed very little response to capture, the response near fledging resembled the typical adrenocortical pattern widely reported in fully developed birds. Our results concur with those found in altricial and semi-altricial species, and suggest that non-precocial birds follow a similar mode of development of the hypothalamic–pituitary–adrenal (HPA) axis. The fact that HPA sensitivity to stress is functional suggests that young storks gradually develop emergency responses of adaptive value and are able to overcome acute perturbations in spite of their parental dependence, at least during the last two-thirds of post-natal development. According to the Developmental Hypothesis, such gradual changes would allow nestlings to respond to perturbations as a function of the specific behavioral and physiological abilities of their age. The potential sources of stress that nestlings have to face during development (i.e., weather conditions, dietary restrictions, and social competition) are discussed according to developmental changes in behavioral and physiological abilities.

Analysis of heart rate in developing bird embryos: effects of developmental mode and mass

Bird embryos may be regarded as developing in their thermo-neutral zone, at rest, and stay in the egg for a fixed period of time until hatching. It is therefore interesting to investigate if they follow the same ‘rule’ set for adult homeotherms, which states that, within a taxonomically or functionally defined category such as mammals or birds, the number of heart beats throughout the life span ( s L) is more or less constant. This rule stems from the allometric relationships between heart rate ( f H) and body mass ( m B) and between s L and m B. As a step towards understanding the general allometric nature of avian embryonic physiology we analyzed the f H values of avian embryos in relation to their incubation span ( s I). Data from 30 species were selected from the scientific literature for the analyses. Values obtained from invasive methods which were judged to grossly alter natural incubation conditions, or from undefined or unmatched temperature conditions were not used. These include most values obtained below the first 30% of the incubation. Also, data obtained after internal pipping were discarded since hatching activity influences them. Values for s I and egg mass ( m E) as representatives of embryonic mass were also collected. Embryonic f H was normalized to 70.1–80% s I. At 20.1–30% s I it was only 85% of the value at 70.1–80% s I and increased to a plateau at about 50.1–60% s I. It was almost constant among species between 50.1 and 60% s I and pre-internal pipping (PIP) time and thus, the mean f H value between 50.1 and 60% s I and between 90.1 and 100% excluding pipped eggs ( f̄ H) was taken as a representative value for each given species. The f̄ H (min −1) and the corresponding s I (days) values for the 30 species, scaled with m E (g) as follows: f̄ H=371.1 · m E −0.112 and: s I=12.29 · m E +0.209. Both powers were significantly different from 0. The product of f̄ H and s I ( f̄ H · s I), representing the total number of heartbeats throughout the incubation, scaled with m E for the entire data set as follows: f̄ H · s I=6.565 · 10 +6 · m E +0.096, where the +0.096 power is significantly different from 0. Values for f̄ H · s I from embryos of altricial birds tended to concentrate at the low m E end of the plot while those of the precocial ones tended towards the high end. Separate analyses showed that the m E power for the combined altricial and semi-altricial species (ASA), and the combined precocial and semi precocial species (PSP), of log f̄ H · s I against log m E regressions, were both insignificantly different from 0. Thus, means of f̄ H · s I for ASA and PSP were calculated. The mean ASA value of 7.27 · 10 +6 heartbeats for f̄ H · s I, was significantly different from the mean PSP value of 10.93 · 10 +6. The difference of 3.66 · 10 +6 (33.5%) heartbeats can be attributed to either the more advanced stage of the PSP hatchlings at hatch, to the larger m E values of these hatchlings, to the difference in water fraction of the hatchlings or all. The result of a linear regression of f̄ H · s I against the rate of s I completion (the inverse of incubation span, f I; day −1) was: f̄ H · 10 −6=0.205+3.940 · s I −1. Thus, the faster is the average rate of development accomplished per day (shorter incubation) the higher is daily heart rate. Data tended to cluster such that large eggs, mostly of the PSP type with relatively low f̄ H, complete 2–4% of their incubation per day, while small, ASA type eggs with relatively high f̄ H, complete 6–8% of their incubation time per day. We conclude that, at this stage of knowledge, the data is insufficient to resolve whether the different modes of hatch stage alone can explain differences in the total number of heartbeats throughout embryonic life among all bird species, or egg mass and water content differences contribute variability. This should be investigated on a larger sample of species in more depth.

Embryological Development of Oxygen Consumption and Egg Parameters in the Semi-altricial Australian Diamond Dove, Geopelia cuneata

Diamond dove eggs show characteristics typical of semi-altricial birds. All egg parameters that we examined were within the expected range for semi-altricial birds; only the relative portion of lipid content (7·9% of egg mass) was different from (25% higher) the mean value for comparable-sized eggs of semi- altricial birds. The embryonic development of oxygen consumption shows a clear plateau phase with values within the expected range for semi-altricial species. The plateau occurs at 83·0 ± 6·0% of incubation, and is about 1 day in duration; the oxygen consumption per egg is 42·2 ± 3·14 mL per day and 0·80 ± 0·06 mL per g per h, respectively.

Strategies of mass change in breeding birds

Birds experience strikingly different patterns of mass change during breeding. In some species with uniparental incubation, the incubating parents (mostly females) lose mass and attain their lowest point when the chicks hatch (Incubatory mass loss strategy = IML). In species with shared incubation, or with intense incubation feeding, the incubating parents maintain or increase in body mass without reducing attentiveness levels (Incubatory mass constancy = IMC). In other species, uniparental incubation with IMC is associated with reduced levels of attentiveness. The mobilization of fat stores or its preservation are involved in the two strategies. IML leads to mass increases after hatching of the young, while the opposite is true for IMC. The non-incubating sex in uniparental species does not experience significant mass changes during breeding. Fasting endurance, predation risk and mode of development are proposed as the main selective factors determining strategy. Latitude, climate, diet and food availability interact with the main factors. From a revision of the literature we can deduce that IML is mainly found among large birds with precocial development, while IMC is typical of smaller species with altricial development. Proportional mass losses are positively correlated with body mass in IML-species, as well as in precocial species, where body mass explains more than 70% of the variation in proportional mass change. Incubation periods increase with body mass in uniparental IMC-species, but not in IML-species. IML is thus associated to fast embryonic growth in large species. Successful raising of highly-dependent young in altricial and semialtricial species apparently depends on one of the parents retaining reserves until hatching. Subsequent mass losses may be necessary to maintain the brooding parent through a period when nestlings require heat, insulation and food. Patterns of mass change are not mere consequences of reproductive stress but the outcome of adaptive compromises between different selective factors and constitute an important aspect of the breeding biology and life history of birds.

Metabolism of Barn Owl Eggs

The metabolism of barn owl (7Tto alba) eggs was examined during the incubation period. Until day 10 of incubation, 02 consumption was 1.4-2.8 ml 02/hr, and 02 consumption reached a plateau of 13 ml 02/hr at day 27 of incubation. The metabolism pattern leveled off near the end of the incubation period, which is not in agreement with the egg metabolism of an altricial species or the plateau level of a precocial species. The intermediate metabolism pattern exhibited by the barn owl egg warrants a designation. The barn owl has asynchronous hatching. Young nestlings will be present during the latter part of the incubation period and thus can provide additional heat for egg development. INTRODUCTION Nice (1962) classified avian eggs according to their developmental maturity at hatching (altricial and precocial). Ontogeny of metabolism is not similar in all avian eggs, but alters with the type of development of the embryo (Vleck et al., 1980). Variations in patterns of metabolism of eggs would not be surprising when one observes the phenotypic characteristics of hatched chicks. For example, altricial chicks are relatively naked, have closed eyes, and are restricted to the nest for parental assistance (i.e., feeding and warmth). (Nice, 1962; Vleck et al., 1980). Precocial chicks are covered with down, have open eyes, and are capable of locomotion, thermoregulation and foraging for themselves (Vleck et al., 1980). As Vleck et al. (1980) state, intermediates of the two classes described above are common; however, altricial and precocial species are extremes in the gamut of development modes, and their eggs can be easily separated on the basis of different patterns in the ontogeny of metabolism. Since Nice's (1962) classification, Vleck et al. (1979, 1980) and others have keyed their research efforts toward documenting the patterns of metabolism and growth of avian embryos of both altricial and precocial species. Eggs of altricial birds increase 02 consumption exponentially throughout embryonic development with a substantial increase at hatching (Vleck et al., 1979). Metabolism of eggs from precocial birds initially increases 02 consumption exponentially; however, this rate reaches a plateau approximately 75-80% of the way through the incubation period (Drent, 1970; Rahn et al., 1974; Vleck et al., 1980). Vleck et al. (1980) suggest that semi-altricial species [this is where Nice places the barn owl (7jto alba) ] would follow a pattern similar to an altricial species. However, there appears to be recent uncertainty as to the placement of eggs of the barn owl in Nice's (1962) scheme. Ar and Rahn (1980) included barn owl eggs in the altricial category on the basis of mean mass and water percentage of contents of fresh eggs and hatching chicks. However, Carey et al. (1980) placed these eggs in the semi-altricial-2 group on the basis of egg mass, content mass and yolk mass. Neither Ar and Rahn (1980) nor Carey et al. (1980) examined the metabolism of barn owl eggs in an effort to categorize this species' mode of metabolism. In the present study I address the following questions: (1) What is the pattern of metabolism of barn owl eggs? (2) How does this egg metabolism pattern compare with other egg patterns? (3) Lastly, what importance might such a metabolism pattern play in the heat production requirements of the incubating bird? 'Present address: Department of Physiology and Biophysics, University of Texas Medical Branch, Galveston 77550.

Parrot Eggs, Embryos, and Nestlings: Patterns and Energetics of Growth and Development

The Psittaciformes constitute a distinct and homogeneous order, members of which lay multiple egg clutches of relatively small eggs that have prolonged incubation periods. The chicks are altricial but nevertheless grow comparatively slowly. The contents of parrot eggs contain more solids (19.4%) than is typical for altricial or semialtricial species. The rate of embryonic oxygen consumption increases throughout incubation. The relative rate of increase in V̇o2 (percent per day) and the relative growth rate of the embryo decrease throughout incubation. The relative growth rate continues to decrease after hatching. In the six parrot species I studied, total embryonic energy metabolism is greater than predicted for altricial species owing to the prolonged incubation periods. Pre-pipping and hatching levels of oxygen consumption are lower than in the same size eggs of precocial species. In Agapornis roseicollis, mass-specific metabolism decreases through the first 15 days of incubation, then is relatively constant until immediately prior to hatching, increases sharply for about 4 days after hatching, becomes relatively constant for about 6 days, and then begins decreasing. This pattern reflects (1) changing maintenance costs due to increasing size and changes in maturational state and (2) changing growth costs which reflect the decreasing relative growth rate throughout the incubation and nestling periods.