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Activation of thermoregulatory control elements in precocial birds during the prenatal period
ARTICLE IN PRESS
Journal of Thermal Biology 29 (2004) 621–627 www.elsevier.com/locate/jtherbio
Activation of thermoregulatory control elements in precocial birds during the prenatal period Martin Nichelmann Medical University of Minsk, Minsk, Republic of Belarus, formerly Humboldt University of Berlin
Abstract 1. Heat production (HP) and body core temperature (CT) were measured in the last third of incubation period in embryos of domestic fowl (Gallus gallus) as well as Muscovy ducks (Cairina moschata). Breathing activity and blood flow in the chorioallantoic membrane were simultaneously estimated after internal pipping. 2. The results revealed that ambient temperature (Ta) affected HP and CT, thus manifest endothermic responses starting on D18 of incubation in Gallus gallus and on D20 in Cairina moschata. 3. In comparison to HP heat loss mechanisms are well developed during the embryonic period. Panting occur after internal pipping. By this and by vasodilatation of the chorioallantoic vessels the heat loss to the environment may be increased at high Ta. Both factors may protect the organism against overheating during a relative long period. 4. Some general rules concerning the mechanism of functional embryonic development are formulated. r 2004 Elsevier Ltd. All rights reserved. Keywords: Muscovy duck; Chicken; Heat production; Endothermy; Panting; Heat loss mechanism
1. Introduction It is well known that newly hatched precocial birds are able to increase thermoregulatory heat production (HP) at ambient temperatures (Ta) lower than the thermoneutral temperature (Whittow and Tazawa, 1991). In previous experiments (Modrey and Nichelmann, 1992; Modrey, 1995), it was shown that in 1–10 day-old turkeys the relationships between Ta and HP may be described by parabola-like functions. Similar patterns can be found in avian (Nichelmann and Tzschentke, 2002).
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Nichelmann and Tzschentke (2002) have shown that the ontogeny of thermoregulation in precocial birds is characterised by three phases with different efficiencies. In the prenatal phase all control elements of the thermoregulatory system can function but the efficiency of the system is low. It is postulated that endothermic reactions during the prenatal period do not have a proximate (immediate) but rather have an ultimate (long-term) influence on the efficiency of thermoregulation. They may support adaptation to expected environmental conditions and may be involved in epigenetic adaptation processes. During the early postnatal phase the thermoregulatory system matures. Summit metabolism and resting metabolic rate, as well as the thermoregulatory set point, are increasing (Tzschentke and Nichelmann, 1999). During this period behavioural thermoregulatory mechanisms—such as the innate ability of ambient temperature preference are essential
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ARTICLE IN PRESS M. Nichelmann / Journal of Thermal Biology 29 (2004) 621–627
2. Material and methods Eggs of Muscovy duck (Cairina moschata) and domestic fowl (Gallus gallus) were incubated at 37.5 1C and a relative air humidity of 70% and turned automatically until the start of the experiment. During the experiments the eggs were not turned. Internal egg temperature, measured as the temperature of the allantoic fluid (Taf) was determined using miniature thermistor probes. The colonic temperature (Tc) of the embryos was measurable after internal pipping (days 20 or 21 in fowl embryos and days 33–35 in Muscovy duck embryos). After locating the tail feathers, the cloaca was easily identified and the thermoelements were inserted through the vent to a depth of 1–2 cm. Oxygen consumption was measured in single embryos using an oxygen-analyser based on the paramagnetic principle. During the experiments, the metabolic chambers were placed in a temperature-controlled water bath. Breathing activity after internal pipping led to measurable pressure fluctuation in the air cell. By installing a tube into the air cell, the periodical pressure fluctuations could be recorded using a Statham element (Hugo Sachs Elektronik KG, 79232 March, Germany) in combination with a Gould recorder (Gould Inc, Test
& Measurement Group, Valley View, Ohio 44125, USA). The recorded pressure fluctuations enabled the calculation of respiratory rate, relative tidal volume and relative respiratory minute volume. Peripheral blood flow was measured in the chorioallantoic membrane using the laser Doppler principle (MBF3, Moor Instrument Company, Ltd, Devon, EX13 5DT, England).
3. Results and discussion 3.1. Heat production After placing the glass vessel containing the embryo (within the eggshell) into the water bath at 31.5 or 35.5 1C, the measured temperatures and HP showed a typical time course: The temperature in the vessel decreased very rapidly and was after 30 min identical to the temperature of the surrounding water bath; the body core temperature (Taf) decreased more moderately and the heat production showed a nearly exponential but fluctuating decrease (Fig. 1). In domestic fowl, younger embryos from days 14–17 crossed the Q10-threshold of 2.0 at Taf below 36.6 1C. However, from day 18 onwards, values were below 2.0 at all Taf temperatures between 35.8 and 39.1 1C. When Ta was lowered to 31.5 1C, even a fowl embryo on day 21 reached Q10-values above 2.0 only at the end of a 3 h test (Taf=32.0 1C; HP=5.29 J g 1 h 1; Q10=2.1). Following the theoretical considerations, given by Nichelmann et al. (1998a, b), it can be postulated, that embryos of these ages show endothermic responses (Fig. 2). These disappear at core temperatures lower than 35.0–34.0 1C, perhaps because the activity of the thermosensitive neurones ceases at these temperatures. Tzschentke and Basta (2002) showed that Muscovy duck embryos aged 33 and 28 days have cold-, warm10.0
40.0
9.5
39.0
9.0
38.0
heat
8.5
37.0
production
8.0
temperature of allantoic fluid
7.5 7.0
35.0 34.0
6.5
33.0
ambient temperature
6.0 5.5 0.0
36.0
Temperature [˚C]
for maintenance of homeothermy because the autonomic mechanisms of temperature regulation are not fully developed (Tzschentke and Nichelmann, 1999). The phase of full-blown homeothermy is characterised by a typical activation order of thermoregulatory control elements (Nichelmann and Tzschentke, 1995). In contrary, information on the development of autonomic thermoregulatory control during the prenatal period is extremely rare: during a cold load, HP mostly decreases and seldom increases, respiratory rate seems to increase during heating the embryos (Dawes, 1979) and regularities in changes of blood flow in the chorioallantoic membrane are unknown. Some of the different results may be caused by different experimental conditions like the used species, modulation of Ta exposure and temperature experiences before the experiments. Because of these difficulties, standardised experiments in two avian species, one with a short incubation period (domestic fowl, Gallus gallus, 21 days) and another one with a long incubation period (Muscovy duck, Cairina moschata, 35 days), were carried out to study the activation of thermoregulatory control elements in embryos of precocial birds. First of all, it was necessary to develop an useful methodology to estimate the function of thermoregulatory control elements during the prenatal period. As this part is described comprehensively elsewhere (Nichelmann and Tzschentke, 1999, 2003), we present in this paper only a very short description.
Heat production [J*g-1*h-1]
622
32.0 1.0
2.0 Time [h]
3.0
31.0 4.0
Fig. 1. Time course of ambient temperature, temperature of the allantoic fluid, and heat production of a single 34 day old Muscovy duck embryo, incubated at 37.5 1C (1st h) and 31.5 1C thereafter (from Nichelmann and Tzschentke, 1999).
ARTICLE IN PRESS M. Nichelmann / Journal of Thermal Biology 29 (2004) 621–627
and temperature-insensitive neurones activated in a similar fashion as in 1–5 day-old ducklings. The results presented show that fowl embryos between 14–21 days of development and Muscovy ducklings starting at day 20 have a Q10o2.0 at body temperatures between 34 and 39 1C. It is postulated that embryos at these ages manifest endothermic responses (Table 1). The threshold temperature (Taf) of Q10=2.0, showing the transition to endothermic responses in all Muscovy duck and fowl embryos at all age groups, is presented in Table 1. At transient temperature changes between 37.5 and 31.5 1C it was between 34.0270.36 1C and
8.0
Q10
6.0
9.5 9.0
HP Q10
5.0
8.5
4.0
8.0
3.0
7.5
2.0
7.0
1.0
6.5
0.0 40.0
39.0 38.0 37.0 36.0 35.0 34.0 Temperature of the allantoic fluid [˚C]
Heat production [J*g-1*h-1]
10.0 y = -0.1132x 2+ 8.6348x - 155.65 R2 = 0.9069
7.0
6.0 33.0
Fig. 2. Effect of the temperature of the allantoic fluid (Taf) on heat production (HP) and Q10 in the same Muscovy duck embryo as shown in Fig. 1. For details of calculation see Nichelmann et al., (1998b).
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35.0370.65 1C for the fowl embryos and between 34.2470.61 1C and 35.8370.40 1C for Muscovy duck embryos, whereas at transient temperature changes between 37.5 and 34.5 1C it was between 36.277 0.35 1C and 37.4070.26 1C in fowl embryos and between 36.1070.42 1C and 37.7070.48 1C in Muscovy duck embryos. Table 1 shows that the rate of body temperature changes in Muscovy duck and fowl embryos have an effect on the threshold temperature for endothermy, and support the assumption that the dynamic component of central or peripheral thermosensors may be developed very early. The faster the core temperature changed the lower is the threshold temperature of endothermic responses. Janke et al. (2003) have published the following observation: when embryos were exposed to several high ambient temperatures (38.0, 38.5, 39.0, 39.5 1C) on the day before hatching, there was no rise of HP parallel to Taf, but a decrease below the level at normal Ta in same cases. At a Ta of 38.0 1C, embryos of Cairina moschata increased their HP by 5.4%. At 39.0 1C there was a small increase of 1.2%, followed by 8.2% increase at 39.5 1C. In Gallus gallus the course of HP was similar, but at a lower level, namely, a slight increase of HP by 0.2% at 38.0 1C was followed by a drop in HP of 5.2% at 38.5 1C. At the highest Ta tested (39.5 1C) HP increased by 3.5%. The results presented are in accordance with the literature data and allow the assumption that a second chemical thermoregulation in investigated precocial bird embryos may occur near hatching,
Table 1 Threshold temperature (Taf 1C) of Q10=2.0 (heat production) in fowl and Muscovy duck embryos Fowl embryo
Duck embryo
31.5 1C
34.5 1C
31.5 1C
34.5 1C
D1
n
Taf
n
Taf
D1
n
Taf
n
Taf
12 13 14 15 16 17 18 19 20 21
4 6 5 6 6 6 6 6 6 6
34.0270.36 34.9870.25 35.5870.28 35.4570.48 34.9370.67 35.0370.65 34.9570.54 35.4870.44 34.8770.59 34.4370.48
6 4 6 6 6 6 1 3 0 2
36.2770.35 36.8270.57 36.4370.89 37.2770.39 36.8370.24 37.2070.79 36.70 — 37.4070.26 — 37.1570.49
20 21 22 23 24 25 26 27 28 29 30 31 32 33 34
6 6 6 6 6 6 6 6 6 6 5 6 5 5 5
35.0870.50 35.6070.17 35.3370.37 35.8370.40 35.2070.27 35.0370.69 34.9070.29 35.0770.34 35.6770.32 34.9270.44 34.5670.76 34.3270.68 34.2470.61 34.8470.65 35.4070.28
5 4 5 5 4 3 4 3 2 3 5 3 1 2 4
36.4670.42 36.9770.73 36.4670.45 36.6270.39 36.3570.19 36.3770.32 36.3570.26 36.2770.32 36.1070.42 36.8370.11 36.6670.30 36.4370.40 36.40 — 36.6070.28 37.7070.48
Values are presented as means7standard error. D1=day of incubation.
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similar than in adult birds and mammals (Janke et al., 2003). The mechanism of down-regulation of heat production was speculated elsewhere (Janke et al., 2002). In the rat, a centre in the midbrain reticular formation was found that tonically inhibits HP (Shibata et al., 1999). It cannot be excluded that this centre inhibits HP during slight hyperthermia in mammals and birds in general, including the examined bird embryos. 3.2. Heat loss mechanism In addition to the low efficiency of the endothermic responses during embryonic development, the prenatal efficiency of embryonic heat loss mechanisms seems to be higher than that of the HP mechanisms as respiration movements occur before internal pipping (Vince and Tolhurst, 1975; Pettit and Whittow, 1982; Tazawa, 1987; Murzenok et al., 1997). Panting responses (Fig. 3) were found in Muscovy duck embryos between the internal and the external pipping (Nichelmann et al., 1997a,b); at the same time, Respiratory rate 150 100 50 0 37.5
38.5 39.5 40.5 Colonic temperature (˚C)
41.5
Tidal volume 2000 1500 1000 500 37.5
38.5 39.5 40.5 Colonic temperature (˚C)
41.5
Temperature (˚C)
Respiratory minute volume 25500 20500 15500 10500 5500 500 37.5
38.5 39.5 40.5 Colonic temperature (˚C)
there are changes in blood flow in the chorio-allantoic membrane at different Ta’s (Holland et al., 1998). After Ta was increased to 40.5 1C, Taf increased soon and in parallel to Ta and was after a few minutes higher than Ta and Tc (Fig. 4). The Tc, however, was kept constant for more than 40 min after the initial Ta increase and was higher than Taf only before heating and after Ta had reached a new stable level at the 150th min of the experiment. In our previous studies (Nichelmann et al., 2001a, b), we have postulated a general rule—that the activity of organ functions occurs during embryonic development even before this function is ultimately needed to ensure the survival of the embryo. It can be postulated that endothermic responses during the prenatal period have an ultimate but not a proximate (immediate) effect on the efficiency of thermoregulation. They have a training effect on the control systems and support adaptation to expected environmental conditions. It may be that they have an effect on epigenetic adaptation mechanisms. Thus, in the adaptation process, environmental factors during gestation of mammals or during incubation of birds have an effect on gene expression in embryos. The effect of altered environmental conditions during the prenatal period on the later development of physiological control systems in birds and mammals has been previously described, e.g. for reproductive system and glucose metabolism (Do¨rner et al., 1984), growth processes (Widdowson, 1980), thyroid hormones and metabolism (Decuypere, 1984; Minne and Decuypere, 1986) and the arginine-vasotocin system (Kisliuk and Grossmann, 1993). Tzschentke et al. (2001) and Tzschentke and Basta (2002) provided more general aspects of epigenetic adaptation including epigenetic temperature adaptation. They have shown, that in birds, incubation at a lower than normal temperatures induced postnatal cold
41.5
Fig. 3. Influence of colonic temperature on respiration rate, tidal volume and relatively respiratory minute volume of one Muscovy duck embryo after internal pipping on D34 of incubation. The respiration rate is given in n*min 1, the tidal volume and the relatively respiratory volume in arbitrary units (Nichelmann et al., 1998b).
41.5 41.0
360 320
40.5 40.0 39.5
280 240 200
Tc Taf
39.0 38.5 38.0
Tc Ta Taf Flux
Flux
37.5 37.0
Ta 0
60
120
160 120 80
Flux
624
40 0 180
Time (min)
Fig. 4. Time course of ambient temperature (Ta) temperature of the allantoic fluid (Taf), colonic temperature (Tc) and blood flow in the chorioallantoic membrane (flux) during a typical experiment in a chicken embryo after internal pipping (from Holland et al., 1998; Nichelmann and Tzschentke, 1999).
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adaptation and incubation at higher than normal temperature induced heat adaptation. Their conclusions were supported by some experiments of Modrey (1995), carried out in turkeys incubated at a normal temperature of 37.5 1C and at a low temperature of 34.5 1C. At Ta between 5 and 40 1C, the birds incubated at the lower Ta have had a higher HP than the normally incubated controls during the first 10 days after hatching (Nichelmann, 2004).
4. General conclusions Apart from the specific remarks, some general rules concerning the mechanisms of functional embryonic development could be formulated using the results from the literature and the own experiments cited in this paper and elsewhere (Nichelmann and Tzschentke, 2003). Firstly, during the ontogenesis adaptive body functions are developed even before they are needed for the survival of the organism. For example, contractions of heart muscle cells occur in chicken embryos at D2, before morphological differentiation into atrium and ventricle exists and before blood transport is possible, and before sympathetic innervation of the heart is fully developed before D24 in ducklings (Ho¨chel, 1998) and at D16 in chicken embryos (Ho¨chel et al., 1998). In eggs of precocial birds the first rhythmic contractions of the respiratory muscles occur before internal pipping (Murzenok et al., 1997). Respiratory movements start before perforation of the chorioallantoic and internal egg membrane. Three periods and three types of respiratory movements could be differentiated in respect to frequency, amplitude and morphological signs of the respiratory movements. Before regular respiratory movements occurred, an increase in the low amplitude movements was observed. It is assumed that these movements occur without ventilation and have the function of consolidating the morphology and function of the respiratory tract. Regular respiration movements occur immediately after internal pipping and show a typical order of events. The respiration rate increases at a normal incubation temperature (37.5 1C) from about 20–40 during the first hours to between 40 and 60 for the next 3 h. There are large fluctuations (between 10 and 90 breaths per minute) in the middle of the pipping period. Three hours before hatching, the fluctuations are diminished. Because of the low efficiency of the thermoregulatory effector systems in avian embryos it could be argued that the thermoregulatory mechanisms are not necessary in avian embryos, given that (1) the embryos are kept warm by the incubating parent in most birds, for most of the time and (2) the thermal tolerance of the embryos
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protects them to some extent from overheating and cooling (Whittow and Tazawa, 1991). Secondly, the development of the physiological control systems starts with non-coordinated and proximately non-adaptive responses. As it could be shown above, training effects may occur during the development of body functions and control systems. They are necessary for the development of body functions. Another point of view is that the development of the physiological control systems starts with non-coordinated and non-specific responses which have no proximate adaptive effects but are necessary for the ultimate adaptation. The first indication for these relationships was found more than 20 years ago in own experiments carried out in new born piglets (Nichelmann, 1977; Nichelmann and Barnick, 1982). In older birds and mammals the control elements of the thermoregulatory system will be activated in a typical order. Firstly, with increasing ambient temperature the evaporative heat loss will be activated, and thereafter, the threshold temperature for conductance changes occur. At higher temperatures, the biological optimum temperatures is reached and finally, the thermoneutral temperature—the threshold temperature for HP—are established (Nichelmann and Tzschentke, 1995). In piglets (Nichelmann and Barnick, 1982), during the first days after birth, the control elements will be activated in a non-coordinated fashion, but only at the 9th day of life the normal activation modus occurs. Thus, not the direction of changes seems to be most important for the organism but only the fact that a change occurs. Thirdly, apart the genetically determined adaptation of the organism to the environment epigenetic adaptation processes occur. Without adaptation to the environment survival in birds and mammals is impossible. Following the Glossary of terms for Thermal Physiology (2001), ‘‘adaptation is a change which reduces the physiological strain produced by stressful components of the total environment’’. This means that the reaction to a special stimulus before the adaptation is qualitatively and/or quantitatively different from the reaction after the adaptation. This change in the type of response may take place within the lifespan of an organism (phenotypic adaptation) or maybe the result of genetic selection in a species or subspecies (genotypic adaptation). Whereas the phenotypic adaptation is a precise adjustment to a special environment, the epigenetic adaptation is an adaptation to an expected environment. The accuracy of the epigenetic adaptation is situated between those of genetic and phenotypic adaptation. Mostly, the epigenetic adaptation is innate but not genetically fixed. More detail are given elsewhere (Nichelmann, 2004).
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5. Summary The goal of this paper is to describe the prenatal developmental processes of the thermoregulatory system that occurs during the last third of the embryogenesis in precocial birds and its effect on the postnatal efficiency of thermoregulatory control elements. For this, the internal core temperature, the heat production and oxygen consumption, the respiration rate after internal pipping, the peripheral blood flow in the chorioallantoic membrane were measured and the Q10 for heat production was calculated in embryos of the domestic chicken (Gallus gallus) and Muscovy duck (Cairina moschata). The experiments show that (1) avian embryos manifest endothermic reactions; (2) hyperthermia causes a down-regulation of heat production in precocial avian embryos; (3) in contrast to heat production, the efficiency of heat loss is high in precocial embryos; and (4) the development of physiological control systems starts with non-coordinated and proximate (immediate) non-adaptive reactions. It is concluded, that strategies of avian embryos in relation to temperature regulation are developed optimally. Endothermic responses occur very early during the embryonic development but their efficiency is limited.
Acknowledgements The research was supported by grants of Deutsche Forschungsgemeinschaft (Ni 336/2-1,1-2,3-1). Part of the experiments were carried out by Dr. Sven Holland and Dr. Oliver Janke.
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Journal of Thermal Biology 29 (2004) 621–627 www.elsevier.com/locate/jtherbio
Activation of thermoregulatory control elements in precocial birds during the prenatal period Martin Nichelmann Medical University of Minsk, Minsk, Republic of Belarus, formerly Humboldt University of Berlin
Abstract 1. Heat production (HP) and body core temperature (CT) were measured in the last third of incubation period in embryos of domestic fowl (Gallus gallus) as well as Muscovy ducks (Cairina moschata). Breathing activity and blood flow in the chorioallantoic membrane were simultaneously estimated after internal pipping. 2. The results revealed that ambient temperature (Ta) affected HP and CT, thus manifest endothermic responses starting on D18 of incubation in Gallus gallus and on D20 in Cairina moschata. 3. In comparison to HP heat loss mechanisms are well developed during the embryonic period. Panting occur after internal pipping. By this and by vasodilatation of the chorioallantoic vessels the heat loss to the environment may be increased at high Ta. Both factors may protect the organism against overheating during a relative long period. 4. Some general rules concerning the mechanism of functional embryonic development are formulated. r 2004 Elsevier Ltd. All rights reserved. Keywords: Muscovy duck; Chicken; Heat production; Endothermy; Panting; Heat loss mechanism
1. Introduction It is well known that newly hatched precocial birds are able to increase thermoregulatory heat production (HP) at ambient temperatures (Ta) lower than the thermoneutral temperature (Whittow and Tazawa, 1991). In previous experiments (Modrey and Nichelmann, 1992; Modrey, 1995), it was shown that in 1–10 day-old turkeys the relationships between Ta and HP may be described by parabola-like functions. Similar patterns can be found in avian (Nichelmann and Tzschentke, 2002).
Corresponding author. Pestalozzistrasse 1B, Berlin 13187,
Germany. Tel.:/fax: 49-30-4856801. E-mail address: [email protected] (M. Nichelmann).
Nichelmann and Tzschentke (2002) have shown that the ontogeny of thermoregulation in precocial birds is characterised by three phases with different efficiencies. In the prenatal phase all control elements of the thermoregulatory system can function but the efficiency of the system is low. It is postulated that endothermic reactions during the prenatal period do not have a proximate (immediate) but rather have an ultimate (long-term) influence on the efficiency of thermoregulation. They may support adaptation to expected environmental conditions and may be involved in epigenetic adaptation processes. During the early postnatal phase the thermoregulatory system matures. Summit metabolism and resting metabolic rate, as well as the thermoregulatory set point, are increasing (Tzschentke and Nichelmann, 1999). During this period behavioural thermoregulatory mechanisms—such as the innate ability of ambient temperature preference are essential
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2. Material and methods Eggs of Muscovy duck (Cairina moschata) and domestic fowl (Gallus gallus) were incubated at 37.5 1C and a relative air humidity of 70% and turned automatically until the start of the experiment. During the experiments the eggs were not turned. Internal egg temperature, measured as the temperature of the allantoic fluid (Taf) was determined using miniature thermistor probes. The colonic temperature (Tc) of the embryos was measurable after internal pipping (days 20 or 21 in fowl embryos and days 33–35 in Muscovy duck embryos). After locating the tail feathers, the cloaca was easily identified and the thermoelements were inserted through the vent to a depth of 1–2 cm. Oxygen consumption was measured in single embryos using an oxygen-analyser based on the paramagnetic principle. During the experiments, the metabolic chambers were placed in a temperature-controlled water bath. Breathing activity after internal pipping led to measurable pressure fluctuation in the air cell. By installing a tube into the air cell, the periodical pressure fluctuations could be recorded using a Statham element (Hugo Sachs Elektronik KG, 79232 March, Germany) in combination with a Gould recorder (Gould Inc, Test
& Measurement Group, Valley View, Ohio 44125, USA). The recorded pressure fluctuations enabled the calculation of respiratory rate, relative tidal volume and relative respiratory minute volume. Peripheral blood flow was measured in the chorioallantoic membrane using the laser Doppler principle (MBF3, Moor Instrument Company, Ltd, Devon, EX13 5DT, England).
3. Results and discussion 3.1. Heat production After placing the glass vessel containing the embryo (within the eggshell) into the water bath at 31.5 or 35.5 1C, the measured temperatures and HP showed a typical time course: The temperature in the vessel decreased very rapidly and was after 30 min identical to the temperature of the surrounding water bath; the body core temperature (Taf) decreased more moderately and the heat production showed a nearly exponential but fluctuating decrease (Fig. 1). In domestic fowl, younger embryos from days 14–17 crossed the Q10-threshold of 2.0 at Taf below 36.6 1C. However, from day 18 onwards, values were below 2.0 at all Taf temperatures between 35.8 and 39.1 1C. When Ta was lowered to 31.5 1C, even a fowl embryo on day 21 reached Q10-values above 2.0 only at the end of a 3 h test (Taf=32.0 1C; HP=5.29 J g 1 h 1; Q10=2.1). Following the theoretical considerations, given by Nichelmann et al. (1998a, b), it can be postulated, that embryos of these ages show endothermic responses (Fig. 2). These disappear at core temperatures lower than 35.0–34.0 1C, perhaps because the activity of the thermosensitive neurones ceases at these temperatures. Tzschentke and Basta (2002) showed that Muscovy duck embryos aged 33 and 28 days have cold-, warm10.0
40.0
9.5
39.0
9.0
38.0
heat
8.5
37.0
production
8.0
temperature of allantoic fluid
7.5 7.0
35.0 34.0
6.5
33.0
ambient temperature
6.0 5.5 0.0
36.0
Temperature [˚C]
for maintenance of homeothermy because the autonomic mechanisms of temperature regulation are not fully developed (Tzschentke and Nichelmann, 1999). The phase of full-blown homeothermy is characterised by a typical activation order of thermoregulatory control elements (Nichelmann and Tzschentke, 1995). In contrary, information on the development of autonomic thermoregulatory control during the prenatal period is extremely rare: during a cold load, HP mostly decreases and seldom increases, respiratory rate seems to increase during heating the embryos (Dawes, 1979) and regularities in changes of blood flow in the chorioallantoic membrane are unknown. Some of the different results may be caused by different experimental conditions like the used species, modulation of Ta exposure and temperature experiences before the experiments. Because of these difficulties, standardised experiments in two avian species, one with a short incubation period (domestic fowl, Gallus gallus, 21 days) and another one with a long incubation period (Muscovy duck, Cairina moschata, 35 days), were carried out to study the activation of thermoregulatory control elements in embryos of precocial birds. First of all, it was necessary to develop an useful methodology to estimate the function of thermoregulatory control elements during the prenatal period. As this part is described comprehensively elsewhere (Nichelmann and Tzschentke, 1999, 2003), we present in this paper only a very short description.
Heat production [J*g-1*h-1]
622
32.0 1.0
2.0 Time [h]
3.0
31.0 4.0
Fig. 1. Time course of ambient temperature, temperature of the allantoic fluid, and heat production of a single 34 day old Muscovy duck embryo, incubated at 37.5 1C (1st h) and 31.5 1C thereafter (from Nichelmann and Tzschentke, 1999).
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and temperature-insensitive neurones activated in a similar fashion as in 1–5 day-old ducklings. The results presented show that fowl embryos between 14–21 days of development and Muscovy ducklings starting at day 20 have a Q10o2.0 at body temperatures between 34 and 39 1C. It is postulated that embryos at these ages manifest endothermic responses (Table 1). The threshold temperature (Taf) of Q10=2.0, showing the transition to endothermic responses in all Muscovy duck and fowl embryos at all age groups, is presented in Table 1. At transient temperature changes between 37.5 and 31.5 1C it was between 34.0270.36 1C and
8.0
Q10
6.0
9.5 9.0
HP Q10
5.0
8.5
4.0
8.0
3.0
7.5
2.0
7.0
1.0
6.5
0.0 40.0
39.0 38.0 37.0 36.0 35.0 34.0 Temperature of the allantoic fluid [˚C]
Heat production [J*g-1*h-1]
10.0 y = -0.1132x 2+ 8.6348x - 155.65 R2 = 0.9069
7.0
6.0 33.0
Fig. 2. Effect of the temperature of the allantoic fluid (Taf) on heat production (HP) and Q10 in the same Muscovy duck embryo as shown in Fig. 1. For details of calculation see Nichelmann et al., (1998b).
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35.0370.65 1C for the fowl embryos and between 34.2470.61 1C and 35.8370.40 1C for Muscovy duck embryos, whereas at transient temperature changes between 37.5 and 34.5 1C it was between 36.277 0.35 1C and 37.4070.26 1C in fowl embryos and between 36.1070.42 1C and 37.7070.48 1C in Muscovy duck embryos. Table 1 shows that the rate of body temperature changes in Muscovy duck and fowl embryos have an effect on the threshold temperature for endothermy, and support the assumption that the dynamic component of central or peripheral thermosensors may be developed very early. The faster the core temperature changed the lower is the threshold temperature of endothermic responses. Janke et al. (2003) have published the following observation: when embryos were exposed to several high ambient temperatures (38.0, 38.5, 39.0, 39.5 1C) on the day before hatching, there was no rise of HP parallel to Taf, but a decrease below the level at normal Ta in same cases. At a Ta of 38.0 1C, embryos of Cairina moschata increased their HP by 5.4%. At 39.0 1C there was a small increase of 1.2%, followed by 8.2% increase at 39.5 1C. In Gallus gallus the course of HP was similar, but at a lower level, namely, a slight increase of HP by 0.2% at 38.0 1C was followed by a drop in HP of 5.2% at 38.5 1C. At the highest Ta tested (39.5 1C) HP increased by 3.5%. The results presented are in accordance with the literature data and allow the assumption that a second chemical thermoregulation in investigated precocial bird embryos may occur near hatching,
Table 1 Threshold temperature (Taf 1C) of Q10=2.0 (heat production) in fowl and Muscovy duck embryos Fowl embryo
Duck embryo
31.5 1C
34.5 1C
31.5 1C
34.5 1C
D1
n
Taf
n
Taf
D1
n
Taf
n
Taf
12 13 14 15 16 17 18 19 20 21
4 6 5 6 6 6 6 6 6 6
34.0270.36 34.9870.25 35.5870.28 35.4570.48 34.9370.67 35.0370.65 34.9570.54 35.4870.44 34.8770.59 34.4370.48
6 4 6 6 6 6 1 3 0 2
36.2770.35 36.8270.57 36.4370.89 37.2770.39 36.8370.24 37.2070.79 36.70 — 37.4070.26 — 37.1570.49
20 21 22 23 24 25 26 27 28 29 30 31 32 33 34
6 6 6 6 6 6 6 6 6 6 5 6 5 5 5
35.0870.50 35.6070.17 35.3370.37 35.8370.40 35.2070.27 35.0370.69 34.9070.29 35.0770.34 35.6770.32 34.9270.44 34.5670.76 34.3270.68 34.2470.61 34.8470.65 35.4070.28
5 4 5 5 4 3 4 3 2 3 5 3 1 2 4
36.4670.42 36.9770.73 36.4670.45 36.6270.39 36.3570.19 36.3770.32 36.3570.26 36.2770.32 36.1070.42 36.8370.11 36.6670.30 36.4370.40 36.40 — 36.6070.28 37.7070.48
Values are presented as means7standard error. D1=day of incubation.
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similar than in adult birds and mammals (Janke et al., 2003). The mechanism of down-regulation of heat production was speculated elsewhere (Janke et al., 2002). In the rat, a centre in the midbrain reticular formation was found that tonically inhibits HP (Shibata et al., 1999). It cannot be excluded that this centre inhibits HP during slight hyperthermia in mammals and birds in general, including the examined bird embryos. 3.2. Heat loss mechanism In addition to the low efficiency of the endothermic responses during embryonic development, the prenatal efficiency of embryonic heat loss mechanisms seems to be higher than that of the HP mechanisms as respiration movements occur before internal pipping (Vince and Tolhurst, 1975; Pettit and Whittow, 1982; Tazawa, 1987; Murzenok et al., 1997). Panting responses (Fig. 3) were found in Muscovy duck embryos between the internal and the external pipping (Nichelmann et al., 1997a,b); at the same time, Respiratory rate 150 100 50 0 37.5
38.5 39.5 40.5 Colonic temperature (˚C)
41.5
Tidal volume 2000 1500 1000 500 37.5
38.5 39.5 40.5 Colonic temperature (˚C)
41.5
Temperature (˚C)
Respiratory minute volume 25500 20500 15500 10500 5500 500 37.5
38.5 39.5 40.5 Colonic temperature (˚C)
there are changes in blood flow in the chorio-allantoic membrane at different Ta’s (Holland et al., 1998). After Ta was increased to 40.5 1C, Taf increased soon and in parallel to Ta and was after a few minutes higher than Ta and Tc (Fig. 4). The Tc, however, was kept constant for more than 40 min after the initial Ta increase and was higher than Taf only before heating and after Ta had reached a new stable level at the 150th min of the experiment. In our previous studies (Nichelmann et al., 2001a, b), we have postulated a general rule—that the activity of organ functions occurs during embryonic development even before this function is ultimately needed to ensure the survival of the embryo. It can be postulated that endothermic responses during the prenatal period have an ultimate but not a proximate (immediate) effect on the efficiency of thermoregulation. They have a training effect on the control systems and support adaptation to expected environmental conditions. It may be that they have an effect on epigenetic adaptation mechanisms. Thus, in the adaptation process, environmental factors during gestation of mammals or during incubation of birds have an effect on gene expression in embryos. The effect of altered environmental conditions during the prenatal period on the later development of physiological control systems in birds and mammals has been previously described, e.g. for reproductive system and glucose metabolism (Do¨rner et al., 1984), growth processes (Widdowson, 1980), thyroid hormones and metabolism (Decuypere, 1984; Minne and Decuypere, 1986) and the arginine-vasotocin system (Kisliuk and Grossmann, 1993). Tzschentke et al. (2001) and Tzschentke and Basta (2002) provided more general aspects of epigenetic adaptation including epigenetic temperature adaptation. They have shown, that in birds, incubation at a lower than normal temperatures induced postnatal cold
41.5
Fig. 3. Influence of colonic temperature on respiration rate, tidal volume and relatively respiratory minute volume of one Muscovy duck embryo after internal pipping on D34 of incubation. The respiration rate is given in n*min 1, the tidal volume and the relatively respiratory volume in arbitrary units (Nichelmann et al., 1998b).
41.5 41.0
360 320
40.5 40.0 39.5
280 240 200
Tc Taf
39.0 38.5 38.0
Tc Ta Taf Flux
Flux
37.5 37.0
Ta 0
60
120
160 120 80
Flux
624
40 0 180
Time (min)
Fig. 4. Time course of ambient temperature (Ta) temperature of the allantoic fluid (Taf), colonic temperature (Tc) and blood flow in the chorioallantoic membrane (flux) during a typical experiment in a chicken embryo after internal pipping (from Holland et al., 1998; Nichelmann and Tzschentke, 1999).
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adaptation and incubation at higher than normal temperature induced heat adaptation. Their conclusions were supported by some experiments of Modrey (1995), carried out in turkeys incubated at a normal temperature of 37.5 1C and at a low temperature of 34.5 1C. At Ta between 5 and 40 1C, the birds incubated at the lower Ta have had a higher HP than the normally incubated controls during the first 10 days after hatching (Nichelmann, 2004).
4. General conclusions Apart from the specific remarks, some general rules concerning the mechanisms of functional embryonic development could be formulated using the results from the literature and the own experiments cited in this paper and elsewhere (Nichelmann and Tzschentke, 2003). Firstly, during the ontogenesis adaptive body functions are developed even before they are needed for the survival of the organism. For example, contractions of heart muscle cells occur in chicken embryos at D2, before morphological differentiation into atrium and ventricle exists and before blood transport is possible, and before sympathetic innervation of the heart is fully developed before D24 in ducklings (Ho¨chel, 1998) and at D16 in chicken embryos (Ho¨chel et al., 1998). In eggs of precocial birds the first rhythmic contractions of the respiratory muscles occur before internal pipping (Murzenok et al., 1997). Respiratory movements start before perforation of the chorioallantoic and internal egg membrane. Three periods and three types of respiratory movements could be differentiated in respect to frequency, amplitude and morphological signs of the respiratory movements. Before regular respiratory movements occurred, an increase in the low amplitude movements was observed. It is assumed that these movements occur without ventilation and have the function of consolidating the morphology and function of the respiratory tract. Regular respiration movements occur immediately after internal pipping and show a typical order of events. The respiration rate increases at a normal incubation temperature (37.5 1C) from about 20–40 during the first hours to between 40 and 60 for the next 3 h. There are large fluctuations (between 10 and 90 breaths per minute) in the middle of the pipping period. Three hours before hatching, the fluctuations are diminished. Because of the low efficiency of the thermoregulatory effector systems in avian embryos it could be argued that the thermoregulatory mechanisms are not necessary in avian embryos, given that (1) the embryos are kept warm by the incubating parent in most birds, for most of the time and (2) the thermal tolerance of the embryos
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protects them to some extent from overheating and cooling (Whittow and Tazawa, 1991). Secondly, the development of the physiological control systems starts with non-coordinated and proximately non-adaptive responses. As it could be shown above, training effects may occur during the development of body functions and control systems. They are necessary for the development of body functions. Another point of view is that the development of the physiological control systems starts with non-coordinated and non-specific responses which have no proximate adaptive effects but are necessary for the ultimate adaptation. The first indication for these relationships was found more than 20 years ago in own experiments carried out in new born piglets (Nichelmann, 1977; Nichelmann and Barnick, 1982). In older birds and mammals the control elements of the thermoregulatory system will be activated in a typical order. Firstly, with increasing ambient temperature the evaporative heat loss will be activated, and thereafter, the threshold temperature for conductance changes occur. At higher temperatures, the biological optimum temperatures is reached and finally, the thermoneutral temperature—the threshold temperature for HP—are established (Nichelmann and Tzschentke, 1995). In piglets (Nichelmann and Barnick, 1982), during the first days after birth, the control elements will be activated in a non-coordinated fashion, but only at the 9th day of life the normal activation modus occurs. Thus, not the direction of changes seems to be most important for the organism but only the fact that a change occurs. Thirdly, apart the genetically determined adaptation of the organism to the environment epigenetic adaptation processes occur. Without adaptation to the environment survival in birds and mammals is impossible. Following the Glossary of terms for Thermal Physiology (2001), ‘‘adaptation is a change which reduces the physiological strain produced by stressful components of the total environment’’. This means that the reaction to a special stimulus before the adaptation is qualitatively and/or quantitatively different from the reaction after the adaptation. This change in the type of response may take place within the lifespan of an organism (phenotypic adaptation) or maybe the result of genetic selection in a species or subspecies (genotypic adaptation). Whereas the phenotypic adaptation is a precise adjustment to a special environment, the epigenetic adaptation is an adaptation to an expected environment. The accuracy of the epigenetic adaptation is situated between those of genetic and phenotypic adaptation. Mostly, the epigenetic adaptation is innate but not genetically fixed. More detail are given elsewhere (Nichelmann, 2004).
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5. Summary The goal of this paper is to describe the prenatal developmental processes of the thermoregulatory system that occurs during the last third of the embryogenesis in precocial birds and its effect on the postnatal efficiency of thermoregulatory control elements. For this, the internal core temperature, the heat production and oxygen consumption, the respiration rate after internal pipping, the peripheral blood flow in the chorioallantoic membrane were measured and the Q10 for heat production was calculated in embryos of the domestic chicken (Gallus gallus) and Muscovy duck (Cairina moschata). The experiments show that (1) avian embryos manifest endothermic reactions; (2) hyperthermia causes a down-regulation of heat production in precocial avian embryos; (3) in contrast to heat production, the efficiency of heat loss is high in precocial embryos; and (4) the development of physiological control systems starts with non-coordinated and proximate (immediate) non-adaptive reactions. It is concluded, that strategies of avian embryos in relation to temperature regulation are developed optimally. Endothermic responses occur very early during the embryonic development but their efficiency is limited.
Acknowledgements The research was supported by grants of Deutsche Forschungsgemeinschaft (Ni 336/2-1,1-2,3-1). Part of the experiments were carried out by Dr. Sven Holland and Dr. Oliver Janke.
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