Paranatal oxygen consumption and respiratory frequency in the Laysan Albatross.

The oxygen consumption and respiratory frequency of Laysan Albatross eggs were measured during the different phases of pipping (paranatal period) and in hatchlings. The initial phase of pipping--penetration of the aircell of the egg by the embryonic beak--coincided with the beginning of pulmonary ventilation, the embryo rebreathing aircell gas, but it did not result in a statistically significant increase in oxygen consumption. The second phase of pipping--star-fracture of the shell (external pipping)--was the shortest (25 h) of the three phases of pipping, and it did not result in a significant increase in either oxygen consumption or respiratory frequency. The longest phase of pipping (65 h)--the pip-hole phase--represented 54% of the total duration of pipping, and it was accompanied by significant increases in oxygen consumption and respiratory frequency. When the eggs hatched, the oxygen consumption increased further but respiratory frequency diminished significantly. It was calculated that the paranatal period, which represented 7.9% of the total incubation period of the egg, accounted for 37.2% of the total oxygen consumption of the egg.

Simple, noninvasive system for measuring the heart rate of avian embryos and hatchlings by means of a piezoelectric film.

Using a flexible piezoelectric film, the authors developed a simple system to determine noninvasively the heart rate of chicken embryos and hatchlings. The film was piezoelectric polyvinylidene fluoride (PVDF), which is sensitive enough to detect cardiogenic ballistic movements of the egg (ballistocardiogram (BCG)) and precordial movements of the hatchling attributable to cardiac contractions (apexcardiogram (ACG)). The BCG could be detected, during the second half of incubation, by placing the egg on the PVDF film on a soft substrate. The detected signal was found to be a measure of movement velocity. The ACG could be measured when the hatchling's chest wall made contact with the PVDF film installed in a box in which the hatchling was confined. The heart rate was counted from the lag time of autocorrelation calculated for a certain time segment (e.g. 2 s) of the BCG and ACG recordings.

Metabolic responses of chicken embryos and hatchlings to altered O2 environments.

The oxygen consumption (MO2) response over a 4 h period of exposure to altered ambient O2 (air, 10, 15, 40, 60, 80 and 100%), helium (He) and sulfur hexafluoride (SF6) environments was determined for young (12 days old) and late (16 and 18 days old) embryos, externally pipped (EP) eggs and just hatched chicks (hatchlings) of the domestic fowl. The young embryos were insensitive to hyperoxic gas mixtures and to He exposure, while the late embryos increase their MO2 in hyperoxic environments, independently of O2 concentration, and also in a He atmosphere. Both the young and late embryos responded to SF6 exposure with decreasing MO2, as SF6 reduces O2 diffusivity through the eggshell. The MO2 of EP eggs and hatchlings in He and SF6 varied very widely, the effects of altered diffusivity being insignificant. In hypoxic environments in which the MO2 decreased, the fall of MO2 became smaller as embryos developed and particularly after they pipped the shell and hatched. In an atmosphere of 10% O2, the MO2 of all embryos in the egg before hatching decreased to below 10% of the control after 4 h, while in hatchlings the MO2 remained above 80% of the control. As all embryos in situ in the egg depend entirely or partly on diffusion in order to obtain O2, this emphasizes the limitation of the diffusive process. A 4 h exposure to 10% O2 was lethal for embryos in the egg even if they had pipped the shell and were breathing air with the lungs.

Embryonic oxygen consumption and organ growth in the wedge-tailed shearwater.

Embryonic oxygen consumption and organ growth were measured in the Wedge-tailed Shearwater (Puffinus pacificus), a tropical seabird characterized by slow embryonic growth and a prolonged pipping process prior to hatching. In most organs, growth in unpipped eggs could be represented by a linear regression of organ mass on whole-embryo mass. However, the slopes of the regression lines varied considerably between organs. The slope was steepest for the stomach and lowest in the heart and lungs. Oxygen consumption also increased linearly with embryo mass up to 25g in unpipped eggs, until just prior to pipping. In pipped eggs, however, there was a considerable increase in oxygen consumption, and acceleration of growth in some organs (eg. liver, intestine) while in others (eg. stomach, pectoral muscles, eyeballs) growth rates diminished. Comparison with the reported growth of other species revealed a number of similarities between the embryos of the semi-precocial shearwater and the precocial domestic fowl, together with several differences between the shearwater and the altricial pigeon embryo.

Comparative metabolic responses to prolonged cooling in precocial duck (Anas domestica) and altricial pigeon (Columba domestica) embryos.

1. Embryos and hatchlings of the duck and pigeon were exposed to a lowered temperature for 6 hr. The oxygen consumption (MO2) was measured before and after cooling and the ratio of the two was compared with that predicted for a temperature coefficient of 2 (Arrhenius value). 2. Late prenatal ducks kept the MO2 above the Arrhenius value at 28 degrees C, while the MO2 of pigeon hatchlings became the same as the Arrhenius value even at 32 degrees C. 3. Thus, incipient homeothermic ability appears in the duck during prenatal development, but it is not evident in the pigeon even after emergence from the shell. The precocial chicken and semi-precocial noddy previously studied are intermediate in their metabolic response between the duck and the pigeon.

Metabolic responses of chicken embryos to graded, prolonged alterations in ambient temperature.

1. Chicken embryos aged 12, 16, 18 and 20 (externally pipped) days of incubation were exposed to graded reductions (2 degrees C) in ambient temperature from 38 to 28 degrees C, exposure to each temperature lasting up to 9 hr. 2. Oxygen uptake was measured first at 38 degrees C and then in the quasi-equilibrium state at lowered temperatures. The temperature coefficient (Q10) was calculated for each egg. 3. For mild cooling (32 degrees C), the Q10 in 18-day-old embryos was about 1.5, while 12- and 16-day-old embryos had a Q10 value of about 2, indicating that a feeble homeothermic metabolic response to cooling appears in late prenatal embryos. It became more marked in externally pipped embryos and further augmented in hatchlings.

Metabolic responses to gradual cooling in chicken eggs treated with thiourea and oxygen.

1. Late prenatal chicken embryos in eggs injected with saline showed a feeble homeothermic metabolic response to gradual cooling. This response was absent in thiourea-treated eggs. This suggests that the incipient homeothermic metabolic response before paranatal life may be attributed to thyroid development. 2. The compensatory metabolic response disappeared in embryos exposed to a hypoxic environment, while it was augmented in eggs in pure O2, decreasing as ambient temperature fell. 3. These results may indicate that the homeothermic metabolic response in late embryos is O2-conductance-limited and power-limited as previously suggested.

Oxygen consumption of brown noddy (Anous stolidus) embryos in a quasiequilibrium state at lowered ambient temperatures.

1. The oxygen consumption (MO2) of the semi-precocial Brown Noddy embryos at different stages of development was measured at 36 degrees C and again after 5-hr exposure to lowered ambient temperatures (30 and 32 degrees C). 2. The MO2 measured in a quasiequilibrium state was equal to the value predicted by a temperature coefficient of 2. 3. In contrast to precocial chickens, the semi-precocial Noddy had no apparent metabolic response to cooling before hatching.

Short-term effects of altered shell conductance on oxygen uptake and hematological variables of late chicken embryos.

The preceding report on the O2 uptake (MO2) of chicken embryos whose shell conductance (GO2) was altered from the beginning of incubation showed that the MO2 was decreased despite increased GO2 [Okuda, A. and H. Tazawa (1988) Respir. Physiol. 74: 187-198]. This was attributed to an excess water loss which reduced the growth of the embryos. The present study was designed to investigate the short-term effects of altered GO2, obviating the effect of excess water loss, on the MO2 and simultaneously on the hematological variables of embryos on days 16-17 and days 18-19 of incubation. The MO2 measured 5 h after increasing the GO2 was neither decreased nor increased significantly. The diffusing capacity of the chorio-allantoic membrane, which was estimated using the Bohr integration procedure, decreased as the GO2 was increased. When the GO2 was decreased, on the other hand, the decrease in MO2 was not so large as expected from the decrease in GO2, for both 16- and 18-day-old embryos. The effect of reduced GO2 on MO2 was more prominent in 18-day-old embryos than 16-day-old embryos. One-day-long hypoxia due to decreased GO2 induced erythropoiesis in 18-19-day embryos, but did not do so in 16-17-day embryos. The increase in hematocrit value of the latter group of embryos was attributed to an increase in cell volume due to concurrent hypercapnia.

Incubation energetics of the Laysan Albatross.

The energy expenditure of incubating and foraging Laysan Albatross (Diomedea immutabilis, mean body weight 3.07 kg) was estimated by means of the doubly-labelled water technique. During incubation, the energy expenditure was similar to that of resting birds that were not incubating an egg. The energy expenditure of foraging albatross (2072 kJ/day) was 2.6 times that of resting birds. It was concluded that the energy expenditure of the tropical Laysan Albatross was not less than that of species foraging over cold, high-latitude oceans. An energy budget compiled for an incubating pair of albatross revealed that the energy expenditure of the female was greater than that of the male bird, during the incubation period.

Metabolic cost of incubation in the Laysan albatross and Bonin petrel.

1. Oxygen consumption and carbon dioxide production were measured in resting and incubating Laysan albatrosses and Bonin petrels on Midway Atoll in the north central Pacific Ocean. 2. Incubation metabolism within the thermal neutral zone is less than or equal to resting metabolism in the albatross and petrel. 3. The respiratory quotients (0.64-0.72) during the long fasts indicate fat metabolism. 4. The estimated fractional water content of the albatross and petrel do not change during incubation fasts because water loss is balanced by metabolic water production.

The initiation of pulmonary respiration in a bird embryo: tidal volume and frequency.

Pulmonary ventilation in embryos and hatchlings of the Wedge-tailed Shearwater (Puffinus pacificus), measured with a barometric plethysmograph, revealed a progressive rise in tidal volume (VT) and minute volume (VE) during the paranatal period to achieve hatchling levels. VT and VE in internally pipped eggs (penetration of air cell) was 0.06 ml +/- 0.03 (SD) and 3.11 ml . min-1 +/- 1.80, respectively. Ventilation was significantly higher (P less than 0.05) in eggs with pip-holes (VT = 0.15 ml +/- 0.04 and VE = 7.09 ml . min-1 +/- 2.76). A significant difference (P less than 0.05) was also obtained for VT and VE between embryos and hatchling chicks. The respiratory frequency (f) was approximately 47 breaths . min-1 for both embryos and chicks. Acute changes in ventilation were examined in response to 2% CO2, 5% CO2, and 10% CO2 in air. For embryos, VT increased significantly (P less than 0.05) only with 10% CO2 and was accompanied by a significant decrease (P less than 0.05) in f. Hatchling VT increased significantly (P less than 0.05) with each test gas and VE increased significantly (P less than 0.05) with acute exposure to 5% CO2, from 16.5 ml . min-1 +/- 2.0 in normoxic air to 53.9 ml . min-1 +/- 8.6. The shearwater embryo is relatively insensitive to high levels of CO2, suggesting a respiratory adaptation to naturally inspired air cell gas concentrations during the internal pipping phase and rebreathing.

The initiation of pulmonary respiration in a bird embryo: blood and air cell gas tensions.

The gaseous stimuli for pipping and the initiation of pulmonary respiration were examined in th Wedge-tailed Shearwater (Puffinus pacificus) by measuring blood gas tensions in the chorioallantoic vein and air cell gas tensions (Pao2 and Paco2) prior to and during the pipping process. External pipping (shell fracture) was the first observed pipping event and preceded internal pipping (penetration of air cell and initiation of pulmonary ventilation). This sequence of cracking the eggshell prior to the initiation of pulmonary respiration resulted in higher Pao2 and lower Paco2 values than the pre-pip air cell gas tensions. Pip-cracks in the shell allow greater diffusion than could normally be obtained across the intact eggshell. This also favors the establishment of large partial pressure gradients of O2 and CO2 across the chorioallantois, thereby improving gas exchange across the inner resistance barrier. The gaseous stimuli for pipping may be attenuated and thus favor the 5-6 day pip-to-hatch interval in this species.

Embryonic oxygen consumption and growth of Laysan and black-footed albatross.

The constraints placed on diffusive gas exchange by the eggshell and the adaptive features of embryonic respiration and metabolism in large Laysan and black-footed albatross eggs (300 g) during prolonged incubation (65 days) were examined in naturally incubated eggs on Sand Island, Midway, in the Northwestern Hawaiian Islands. A low eggshell gas conductance and slow growth rate were associated with a relatively low oxygen consumption (MO2) throughout incubation. Just prior to internal pipping (IP) of the inner shell membrane and penetration of the air space, the MO2 (pre-IP MO2) was approximately 1,250 ml O2 (STPD).day-1 for both species, resulting in air cell O2 and CO2 tensions of 106 and 40 Torr, respectively. During the 4- to 5-day pipping-to-hatching interval, O2 uptake increases rapidly as pulmonary respiration is initiated. Hatchling O2 consumption averaged 3,700 ml O2 (STPD).day-1 or about three times the pre-IP MO2. Data support the hypothesis that embryonic metabolism among Procellariiformes is related to the extent to which the incubation period deviates from the expected value based on initial egg mass.

Thyroid activity in a hypometabolic primate, the owl monkey (Aotus trivirgatus).

Serum levels of triiodothyronine (T3) and tetraiodothyronine (T4) were significantly lower in owl monkeys than in long-tailed macaques. These observations were considered to be consistent with the lower metabolic rate of the owl monkey. However, the absence of a significant difference in the levels of thyroid stimulating hormone (TSH) between the two species suggested a lower thyroid sensitivity to TSH in the owl monkeys. There was an inverse relation between levels of T3 and TSH in the owl monkeys at night and during the day.

Temperature regulation in a hypometabolic primate, the slow loris (Nycticebus coucang).

Six slow loris were exposed to air temperatures between 10 degrees C and 40 degrees C. Rectal temperature was stable (mean, 34.8 degrees C) at air temperatures between 17 degrees C and 31 degrees C; at higher air temperatures, the animals became hyperthermic. Oxygen consumption was minimal at air temperatures of 31.4-36.6 degrees C; the mean value (0.250 ml O2 g-1 h-1) was only 36% of the expected level for a eutherian Mammal. The slow loris increased its heat production at lower air temperatures. Thermal polypnea occurred in response to heat, and some of the animals were able to dissipate their entire metabolic heat production at lower air temperatures. Thermal polypnea occurred in response to heat, and some of the animals were able the combined thermal conductance of the tissues and haircoat was 73% of the predicted values. It was concluded that, in spite of its low metabolic rate, the slow loris had effective responses to moderate cold, and that, in addition, it was well adapted to a hot climate.