K. Moriya

Ontogenetic study of thermoregulation in birds

Abstract We reviewed our ontogenetic studies of thermoregulatory capacity in avian embryos in relation to metabolic responses to egg cooling.Basic understanding of abrupt egg cooling and quasi-equilibrium state of cooling was discussed together with eggs thermal conductance and heat production.Two cooling tests, which were designed to minimize the rate of heat loss during cooling, were conducted to investigate a feeble compensatory metabolic response to cooling in precocial and altricial embryos, and models for early development of homeothermy in birds were suggested.Instantaneous heart rate (IHR) response to cooling was measured in chick embryos. The baseline of IHR rised and became oscillating. HR oscillation may be a phenomenon related to thermoregulation, which needs to be studied.

Development of cardiac rhythms in birds.

Heart rate (HR) in avian embryos developing inside an eggshell has been measured by various means while maintaining adequate gas exchange through the eggshell. This is an important requirement in order to avoid adverse effects of impeding gas exchange on the cardiac rhythms of developing embryos. The present report is a review of our ontogenetic study on embryonic HR, which was measured with fulfillment of the above requirement and also hatchling HR measured non-invasively. Firstly, we reviewed measurements of daily changes (developmental patterns) in embryonic mean heart rate (MHR), which were determined from a short-term measurement of HR once a day, in 34 species of altricial and precocial birds. The allometric relationship between the MHR during pipping in altricial birds and their fresh egg masses was the same as that between the MHR at 80% of incubation duration and fresh egg masses in pre-cocial birds. Secondly, we presented the developmental patterns of MHR in chick embryos and hatchlings, which were determined from long-term, continuous measurement of HR before, during and after hatching. The ultradian and circadian rhythms of HR were clearly shown in embryos and hatchlings, respectively. Thirdly, we summarized instantaneous HR fluctuations: HR variability and HR irregularities, in chick embryos and hatchlings. The distinctive patterns were shown in pre-pipped and pipped embryos and newly hatched chicks, individually, which were partly related to autonomic nervous functions and physiological functions.

Cardiac rhythms in developing chicks

Instantaneous heart rate (IHR) of chicks was determined by electrocardiogram measured non-invasively from the day of hatch to day 6 for continuity of investigation of HR fluctuations from embryos and for ascertainment of HR diurnal rhythms. In Experiment I, IHR was determined for 1-h periods twice a day, in daytime and at night, to investigate development of heart rate fluctuations (variability and irregularities). Chick IHR was substantially more arrhythmic than embryonic HR and spontaneous acceleration dominated HR fluctuations. Chick HR fluctuations were categorized into three types; [1] Type I as a widespread baseline HR (20-50 bpm) due to respiratory arrhythmia, with a mean oscillatory frequency of 0.74 Hz (range 0.4-1.2 Hz); [2] Type II as low frequency oscillations of baseline HR, at a mean of 0.07 Hz (range 0.04-0.10 Hz), and [3] Type III as non-cyclic irregularities, dominated by frequent transient accelerations. In Experiment II, continuous measurements of HR were made under conditions of a natural photoperiod, thermoneutrality and with feed available throughout the first week after hatching and circadian rhythms of HR were ascertained. HR was very variable in the daytime (250-500 bpm), due in part to feeding and activity, and decreased to a diurnal low (200-350 bpm) at night when mean HR was relatively stable. HR fluctuations persisted throughout the diurnal cycle.

Heart rate in developing ostrich embryos

1. A non-invasive condenser microphone was used to detect cardiogenic, acoustic pressure changes (acoustocardiogram, ACG) over the eggshell in order to determine embryonic heart rate (HR) of ostriches in a commercial hatchery. 2. HR measured for 36 eggs at 36.3C was maintained at about 185 bpm during the middle stage of development (days 19 to 23) and then decreased with embryonic development. 3. The daily changes in HR were not related to egg mass, but HR of high water vapour conductance (GspH2O) eggs was found to decrease less during the last stages of incubation relative to low and medium GspH2O groups. 4. The averaged HR at 80% of incubation period was close to the value predicted from the allometric equation determined previously for embryos of domesticated precocial birds.

Development of respiratory rhythms in perinatal chick embryos

In chick embryos, gas exchange takes place via the chorioallantoic membrane (CAM) and the lungs at approximately 1 day prior to hatching. The present study was designed to elucidate the development of respiratory rhythms in the chick embryo during the whole pipping (perinatal) period with a condenser-microphone measuring system. The microphone was hermetically attached on the eggshell over the air cell on day 18 of incubation. It first detected a cardiogenic signal (i.e. acoustocardiogram), and then beak clapping and breathing signals (acoustorespirogram, ARG). The first signals of lung ventilation appeared intermittently and irregularly approximately once per 5 s among the clapping signals after the embryo penetrated its beak into the air cell (internal pipping, IP). The respiratory rhythm then developed irregularly, with a subsequent more regular rate. The envelope pattern of breathing from the onset of IP through external pipping (EP) to hatching was constructed by a specially devised procedure, which eliminated external and internal noises. The envelope patterns indicated that the IP, EP and whole perinatal periods of 10 embryos were 14.1+/-6.4 (S.D.), 13.6+/-4.0 and 27.6+/-5.4 h, respectively. In addition, they also indicated the period of embryonic hatching activity (i.e. climax) which was 48+/-19 min. The development of respiratory rhythm was also shown by the instantaneous respiratory rate (IRR) which was designated as an inverse value of two adjacent ARG waves.

Low-frequency oscillation of instantaneous heart rate in newly hatched chicks.

Instantaneous heart rate (IHR) of chickens began to fluctuate on days 13-14 of incubation and heart rate (HR) fluctuations became augmented towards hatching and increased further after hatching. IHR fluctuations of newly hatched chicks have been categorized into three types: type I HR variability (HRV), which is high-frequency oscillation; type II HRV, which is low-frequency oscillation; and type III HR irregularities (HRI), which are irregular HR accelerations. The present experiment was carried out to investigate the origin of type II HR oscillations. Following previous evidence, we assumed that the low-frequency oscillation of HR in newly hatched chicks was related to thermoregulation and changed by environmental temperature. Eventually, type II HRV was produced or augmented by exposure of hatchlings to lowered ambient temperature and was abolished by exposure to elevated environmental temperature. The hatchlings that were exposed to large temperature decreases tended to increase their HR more than those exposed to small temperature decreases, and vice versa. The HR oscillation accompanied by an elevation of HR baseline in response to cooling may be a phenomenon related to thermoregulation in chick hatchlings.

Cardiac rhythms in prenatal and perinatal emu embryos

Emu eggs weigh approximately 600 g and have an incubation duration (ID) of approximately 50 days. The egg mass is approximately 10-fold heavier than the chicken egg and the ID is approximately 2.5-fold longer. Daily changes in mean heart rate (MHR) of emu embryos were previously determined, but further measurement was needed to investigate the species-specific behavior of cardiac rhythm for comparison with other species. In the present study, we continuously measured the electrocardiogram of emu embryos while maintaining adequate gas exchange through the eggshell and determined instantaneous heart rate (IHR) during the last 2-7 days of incubation until hatching or death. The MHR over 1-min intervals was calculated from IHR data in order to present continuous developmental patterns of heart rate (HR) in a single graph and 24-h recordings of HR in a single panel, showing the HR trend over a prolonged period. However, neither circadian nor ultradian rhythms of HR were shown in these figures or by power spectrum analysis. The IHR distinctively fluctuated and the fluctuations were mainly comprised of three patterns of irregular HR accelerations in embryos that hatched. Respiratory sinus arrhythmia also occurred in perinatal embryos. During the final stages of the perinatal period, short-term, repeated, large accelerations of IHR appeared, which signaled imminent hatching and has been reported for chick embryos. IHR fluctuations in embryos that failed to hatch tended to become inactive towards death.

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

Abstract 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.

Embryonic heart rate measurements during artificial incubation of emu eggs

1. Daily changes in embryonic heart rate (HR) of emu were determined non-invasively at 36°C by acoustocardiography (ACG) during the last 30% of artificial incubation (predicted incubation time is 50 d). 2. The pattern of daily changes in mean HR of hatched embryos decreased from about 175 bpm to about 140 bpm towards the end of incubation. 3. The mean HR at 80% of incubation (ca. 170 bpm) was close to the value predicted from an allometric equation reported previously for precocial domesticated birds. 4. ACG could measure embryonic HR even during the external pipping period. 5. If the artificial external pipping procedure is timed correctly after internal pipping, it might aid the embryos in hatching. However, further investigation into this aspect is needed.

Cardiac rhythms in developing emu hatchlings

Six emu hatchlings were non-invasively measured for electrocardiogram (ECG) from their chest wall using flexible electrodes, and the instantaneous heart rate (IHR) was determined from ECG throughout the first week of post-hatching life. Although the baseline heart rate (HR) was low, approximately 100-200 beats per min (bpm), compared with chick hatchlings, the IHR fluctuated markedly. The fluctuation of IHR comprised HR variability and irregularities that were designated as types I, II and III in chick hatchlings and additional large accelerations distinctive of emu hatchlings. Type I was HR oscillation with a mean frequency of 0.37 Hz (range 0.2-0.7 Hz), i.e. respiratory sinus arrhythmia (RSA). From RSA, breathing frequency in emu hatchlings was estimated to be approximately half of that in chickens. Type II HR oscillation was also found in the emu; the frequency ranged from approximately 0.04 to 0.1 with a mean of 0.06 Hz, and the magnitude tended to be large compared with that of chickens. In addition to type III HRI, which was designated in chickens, large, irregular HR accelerations were characteristic of emu hatchlings. From IHR data, developmental patterns of mean heart rate (MHR) were constructed and plotted on a single graph to inspect the diurnal rhythm of MHR by visual inspection and power spectrum analysis. A circadian rhythm was not clear in the emu hatchlings, in contrast to chick hatchlings, which showed a dominant diurnal rhythm.