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Poult Sci 2007. 86:1025-1036
© 2007 Poultry Science Association
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SYMPOSIA: Managing the Embryo for Performance

Attainment of Thermoregulation as Affected by Environmental Factors1

B. Tzschentke2

Institute of Biology, Humboldt-University of Berlin, 10115, Germany

2 Corresponding author: barbara.tzschentke{at}rz.hu-berlin.de


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 SUMMARY AND CONCLUSIONS
 REFERENCES
 
The review addresses the development of thermoregulation in poultry embryos as well as the effect of acute and chronic changes of environmental factors on this process and the incubation temperature being the foremost. In poultry, the early development of adaptive body functions, like the thermoregulatory system, is characterized by the following peculiarities. First, the development of peripheral as well as central nervous thermoregulatory mechanisms start during the prenatal ontogeny. However, their maturity is attained during early postnatal development. In the perinatal period, environmental factors have a high effect on development of temperature regulation. Second, acute changes in the environmental conditions induce as a rule first uncoordinated and immediately nonadaptive reactions. Later, the uncoordinated nonadaptive reactions change into coordinated (adaptive) reactions. Prenatal environmental influences may have a training effect on the postnatal efficiency of the thermo-regulatory system. Third, functional systems of the organism develop from an open loop system without feedback control into a closed system controlled by a feedback mechanism. During this critical period, the actual environment modulates the development of the respective physiological control systems for the entire life period, especially by changes in neuroorganization and expression of related effector genes. Knowledge on these mechanisms might be specifically used to generate long-term adaptation of the organism to the postnatal climatic conditions (perinatal epigenetic temperature adaptation). In poultry, perinatal epigenetic temperature adaptation was developed by changes in the incubation temperature. When a comparison is made in birds, which were incubated at 37.5°C, a low incubation temperature induced postnatal cold adaptation, and warm incubation temperature induced postnatal heat adaptation. Perinatal epigenetic temperature adaptation exhibited changes in the neuronal thermosensitivity in the hypothalamus as well as in the peripheral thermoregulatory mechanisms. These alterations could be already found at the end of incubation. Further, temperature-experienced embryos have a lower c-fos expression than in the control after acute heat stress.

Key Words: thermoregulation • environmental factor • poultry embryo • imprinting • critical period


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 SUMMARY AND CONCLUSIONS
 REFERENCES
 
The development of body functions starts early during the embryonic phase in precocial birds, especially poultry. This early and very sensitive developmental phase is of high significance for the adaptability of the organism during later life.

In the hierarchy of regulatory systems, the thermoregulatory system is on a higher level. The goal of temperature regulation in homoeothermic animals in the postnatal developmental phase is the maintenance of a stable body core temperature under most conditions. To realize this, the thermoregulatory system employs all of the systems of the body and integrates their activities into appropriate and coordinated reactions. The prenatal development of thermoregulatory mechanisms in precocial animals is beneficial for the quick maturation of temperature regulation in the early posthatching phase, which is important for the performance of the whole organism.

From the results of our investigations and from related scientific literature, we postulated general rules for the development of physiological control systems, including the thermoregulatory system (Nichelmann et al., 1999, 2001; Tzschentke and Basta, 2002; Tzschentke et al., 2004):

  1. The development of peripheral as well as central nervous thermoregulatory mechanisms starts during the prenatal ontogeny.
  2. Acute changes in the environmental conditions induce as a rule first uncoordinated and immediately nonadaptive reactions. Later, the uncoordinated (immediately) nonadaptive reactions change into coordinated (adaptive) reactions.
  3. During critical developmental phases, a long-term adaptation to an actual environment occurs via epigenetic adaptation processes.

The review addresses the development of thermoregulation in poultry embryos as well as the effect of acute and chronic changes of environmental factors on this process, with incubation temperature being the foremost. Further, the fundamental process of imprinting of physiological control systems during critical periods of early ontogeny (Tzschentke and Plagemann, 2006) is described. The methods developed or adapted and used in my group are herewith briefly described.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 SUMMARY AND CONCLUSIONS
 REFERENCES
 
Incubation of Eggs
The experiments were carried out in Muscovy duck (Cairina moschata f. domestica) and in chicken (Gallus gallus f. domestica) embryos during the second half of incubation. Eggs of the Muscovy duck need a total incubation period of 35 d, and those of the chicken need 21 d. The eggs were incubated at 37.5°C and at a RH of 70% until the day at which the eggs were transferred into the hatcher, viz embryonic day (E) 28 in the Muscovy duck and E17 in the chicken. During this period, the eggs were subjected to automatic turning. In the hatcher, the eggs were incubated at 37.5°C and at a RH of 90%. For experiments on chronic influence of changes in incubation temperature on the development of thermoregulation, 1 group of eggs was incubated at 34.5°C (cold incubated group) and another group at 38.5°C (warm incubated group). After hatch, the birds were kept during the first 10 d either in the animal house at an ambient temperature of 25°C with additional infrared lamps (35°C) or in a temperature gradient channel (10 to 45°C). Food and water were given ad libitum.

Measurement of Body Temperature
Before internal pipping, embryonic temperature was measured in the allantoic fluid (Taf) near the embryo using a miniature thermistor probe (Figure 1Go). On the blunt side of the egg, a hole (2 x 2 mm) was drilled into the eggshell without damaging larger blood vessels. Through this hole, a thermocouple was inserted into the Taf to a depth of 2.5 cm between the chorioallantoic membrane and the embryo. After internal pipping (from E20 in chicken embryos and E33 in Muscovy duck embryos until hatching), it was also possible to measure the colonic temperature (Tc). After locating the tail feathers, the cloaca was easily identified, and the thermistor probe was inserted to a depth of 1 to 2 cm. Details of the method are described by Holland et al. (1998) and Nichelmann and Tzschentke (2003). Allantoic fluid as well as Tc were measured continuously during the entire period of experiments. In some embryos, both temperatures were measured simultaneously. There were only minor differences between Taf and Tc (ranging from 0.0 to 0.2°C) at constant incubation temperature. Under changing incubation temperature, the difference rose to a range of 0.1 to 0.4°C (Holland et al., 1998). After posthatch, the Tc was generally used for measurement of deep body temperature (Tzschentke and Nichelmann, 1999).


Figure 1
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  		Figure 1. Localization of thermistor probes for measurement of the temperature of the allantoic fluid (Taf) and colonic temperature (Tc), laser Doppler probe for estimation of the blood flow in the chorioallantoic membrane, and tube with pressure differential sensor for recording of breathing activity in the avian egg.

 
Measurement of Heat Production
Assuming a respiratory quotient of 0.72 (Decuypere, 1984), which corresponds to a caloric heat equivalent of J/mL of O2, heat production (HP) was calculated from O2 consumption, egg weight, and caloric heat equivalent, taking into account the actual gas flow. Oxygen consumption was continuously measured using an O2 analyzer based on the paramagnetic principle. For these measurements, single eggs were placed into the metabolic chambers, and the respective ambient (incubation) temperature was regulated by a temperature-controlled water bath. After a minimum of 2 h of acclimation of the embryos to the respective ambient temperature, O2 consumption and the ambient temperature (as well as Taf) were recorded for 1 h. For acute temperature stimulation of HP, the ambient temperature was increased (39.5°C) or decreased (34.5 to 31.5°C) from the normal level (37.5°C) for 3 h using another water bath. Detailed information on the methodology is published in Nichelmann et al. (1998, 2001) and Nichelmann and Tzschentke (2002, 2003). Post-hatching HP was obtained by a similar method (Tzschentke et al., 1996; Tzschentke and Nichelmann, 1999).

Recording of Respiratory Rate
Breathing by lung occurs after internal pipping. The breathing activity induces pressure fluctuations in the air cell of the egg. These pressure fluctuations can be registered using a Statham element in a tube, which was inserted in the air cell (Figure 1Go). The recordings gave information about the respiratory rate, the relative tidal volume, and relative respiratory minute volume (Nichelmann and Tzschentke, 2003).

Recording of the Blood Flow in the Chorioallantoic Membrane
Blood flow in the chorioallantoic membrane was measured by MBF3 laser Doppler instrument. The laser Doppler probe was placed directly on the egg membrane (Figure 1Go). Before positioning the probe, the egg was candled to find an area with many small blood vessels. Then a 5 x 5 mm piece of the eggshell was removed. The following parameters could be measured: mean red blood cell flux, the red blood cell concentration, and the mean red blood cell speed. Detailed information is furnished in Nichelmann and Tzschentke (2003).

Recordings of Neuronal Activity
Extracellular recordings of single-cell activity were carried out in brain slices (400 µm) from neurons of the preoptical area of the anterior hypothalamus (PO-AH). The slices were placed into a recording chamber (Schmid et al., 1993) and continuously perfused by artificial cerebrospinal fluid. From the beginning of the experiment, the bath temperature in the recording chamber was maintained at 39°C in the embryos or 40°C in the birds post-hatching and continuously controlled by a small thermocouple. This temperature approximately corresponds to the deep body temperature in poultry at a later stage of embryonic development if incubated at the normal 37.5°C (Janke et al., 2002) or during the first days posthatching (Tzschentke and Nichelmann, 1999). To identify the thermosensitivity of single neurons, the bath temperature was sinusoidally changed to a maximum of ±3°C and a velocity of about 0.02°C/s. The temperature response curve of each neuron was evaluated by relating firing rate to slice temperature and fitted to a piecewise, rectilinear, or both regression function (Vieht, 1989). The thermosensitivity of a neuron was defined by a temperature coefficient of greater than or equal to 0.6 impulse/s per degree Celsius (change in temperature) for warm-sensitive (WS) neurons and less than or equal to –0.6 impulse/s per degree Celsius for cold-sensitive (CS) neurons. All other neurons are named as temperature insensitive (TI) according to this definition (Nakashima et al., 1987). For characterization of the neuronal hypothalamic thermosensitivity, the proportion of WS, CS, and TI neurons in the PO-AH was determined in relation to all neurons investigated (Tzschentke and Basta, 2000). Further details of the methodology are described in Tzschentke and Basta (2002) and Tzschentke et al. (2004).

Investigation of c-fos Expression
On the last day of incubation, acute heat stress (42.5°C) for 90 min was applied before starting the experiment. Then, the extracted embryos were anesthetized and transcardial perfusion was performed. Brains were dissected, and 20-µm brain sections were made using a cryostat. In the PO-AH region of the slices, c-fos expression was detected by immunohistochemical method. Analysis was made by light microscopy and digital photography (magnification of 50-fold). The c-fos-positive neurons were counted in a standardized area of the PO-AH using a rectangle mask. Due to the lack of stereotaxic data of the brain of the chicken embryo, the width of the rectangle was set proportional to the brain of the adult chicken at 990 µm for all embryos. Stereotaxic data of the adult chicken brain were taken from Kuenzel and Masson (1988). For details, see Janke and Tzschentke (2006).

Determination of Preferred Ambient Temperature
Preferred ambient temperature was determined in a temperature gradient tunnel temperated between 10 and 45°C. Groups of 5 birds were kept for 10 d in the temperature gradient immediately after hatching. During this period, the chosen ambient temperatures were observed for 9 h every 10 min every day (Tzschentke and Nichelmann, 1999).


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
SUMMARY AND CONCLUSIONS
 REFERENCES
 
Development of Peripheral as well as Central Nervous Thermoregulatory Mechanisms in Poultry Embryos
The development of peripheral as well as central nervous thermoregulatory mechanisms in precocial birds starts during the prenatal ontogeny. However, their maturity is attained during early postnatal development (Nichelmann and Tzschentke, 2002).

Development of Endothermic Reactions.
The development of HP and body temperature (Taf) under normal incubation temperature (37.5°C) follows an exponential function (Nichelmann et al., 1998; Janke et al., 2002). Initially a continuous increase in HP is observed. In precocial birds after approximately 80% of incubation time, stagnation in HP occurs (plateau phase). At the end of the plateau phase, the embryo pierces the chorioallantoic and inner shell membrane (internal pipping) and starts respiration through the lungs (Tazawa and Whittow, 2000). From internal pipping until hatch, HP increases a lot. A similar developmental pattern of HP has been found in all precocial and altricial bird species investigated (Prinzinger and Dietz, 1995). It is interesting to note that Taf follows the developmental pattern of HP (Figure 2Go). The relationship between HP and Taf could be described by a highly significant linear correlation (Janke et al., 2002).


Figure 2
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  		Figure 2. Development of heat production and body temperature (temperature of allantoic fluid) in Muscovy duck embryos from d 20 until d 34 of incubation at an incubation temperature of 37.5°C (modified from Janke et al., 2002).

 
The subject of investigations was if and at which stage of embryonic development poultry embryos change HP during acute alterations of ambient (incubation) temperature. In our investigations, we already found endothermic reactions before internal pipping in Muscovy duck and chicken embryos (Nichelmann et al., 1998). During an acute decrease in incubation temperature, Taf also shows a similar decrease with the difference in incubation temperature. But Taf is always higher than ambient temperature. On the other hand, HP only decreases moderately (Figure 3Go). A drop in body temperature, due to low incubation temperature, mostly causes a decrease of net HP, but the decrease is lower as assumed by the Van’t Hoff rule (Nichelmann et al., 2001). An endothermic counterreaction occurs, which can be determined using the Q10 method (Nichelmann et al., 1998). With increasing embryonic age, the cold load induced decrease in HP diminishes. Near hatching time, with decreasing Taf, in some embryos, a short-term increase in HP was observed. However, poultry embryos are not able to keep body temperature constant under cold load. The phase of full-blown homeothermy starts during the first days of posthatching (Tazawa and Rahn, 1987; Nichelmann and Tzschentke, 2002; Tazawa et al., 2004).


Figure 3
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  		Figure 3. Course of body temperature (temperature of allantoic fluid) and heat production before and during 3 h of cooling in a single Muscovy duck embryo on d 34 of incubation (Nichelmann and Tzschentke, 1999).

 
Altogether, in comparison with the heat loss mechanisms, efficiency of thermoregulatory HP is very low in embryos. Precocial bird embryos show a high thermal tolerance, which protects them to some extent from disturbances by cooling (Whittow and Tazawa, 1991; Tazawa and Whittow, 2000). The remarkable tolerance of precocial bird embryos to low body temperatures seems to be a part of their thermal strategy to save energy. An increase in high-energy, costly thermoregulatory HP to keep body temperature constant is, to a degree, not necessary for the survival of the bird embryos (Nichelmann and Tzschentke, 2001, 2002; Tzschentke, 2003).

Changes in the Blood Flow of the Chorioallantoic Membrane.
During the last third of incubation time, poultry embryos are able to react on changes in incubation temperature with changes in the blood flow of the chorioallantoic membrane (Figure 4Go). At end of the plateau phase, blood flow increases with increasing incubation temperature or decreases with decreasing ambient temperature. In chicken embryos, for instance, the body core temperature remains constant for more than 40 min after the beginning of the increase in ambient temperature by activating this heat loss mechanism (Nichelmann and Tzschentke, 2003).


Figure 4
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  		Figure 4. Influence of increase in incubation temperature [ambient temperature (Ta)] on the course of body temperature [colonic temperature (Tc)] and blood flow (measured in arbitrary units of flux) in the chorioallantoic membrane in a single chicken embryo after internal pipping (modified from Holland et al., 1998).

 
Changes in Respiration.
First, rhythmic contractions of the respiratory muscles start before internal pipping. These movements are without ventilation of the lung. One goal of this movement is to consolidate the morphology and function of the respiratory tract (Tazawa, 1987; Murzenok et al., 1997). After internal pipping, lung ventilation occurs. In Muscovy duck embryos between internal and external pipping, panting reactions were found when body core temperature increased. Like in adult birds (Arad and Marder, 1983), 2 phases of panting occurred in Muscovy duck embryos, too. At body core temperatures from 38.5 to 40.5°C, respiratory rate increased and the tidal volume decreased, and above 40.5°C, the second phase of panting started, which was characterized by a decrease in respiratory rate and an increase in tidal volume (Figure 5Go).


Figure 5
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  		Figure 5. Influence of colonic temperature (body temperature) on respiratory rate, tidal volume, and relative respiratory minute volume in a single Muscovy duck embryo on d 34 of incubation (Nichelmann and Tzschentke, 1999). Respiratory rate is given in number/minute; tidal volume and relative respiratory minute volume is given in arbitrary units.

 
Communication with the Environment.
After internal pipping, acoustic responses can be used by the bird embryo for protection of endothermic reactions (Nichelmann and Tzschentke, 1997). In a cold environment, the distress call rate increases. After rewarming, this rate decreases again. It is found in embryos of geese (Nichelmann and Tzschentke, 1997) and ring-billed gulls (Larus delawarensis; Evans et al., 1994). Under natural conditions, cold-induced vocalization is a signal of the need of the offspring for warmth from the incubating parents.

Another possibility for communication between the embryo and the incubating parents seem to be NO emission (Ifergan and Ar, 1999). Nitric oxide emission was found mainly via the chorioallantoic membrane in a study made on 18 bird species under cold conditions by Ar et al. (2004). Nitric oxide emission was increased under cold load. Ar et al. (2004) speculated that NO emission from eggs might carry a "message" from the embryo to the incubating parents and vice versa. It was suggested from the same group to use NO emission as a general marker for embryonic stress (Samuni and Ar, 2006).

Development of Central Nervous Thermoregulatory Mechanisms.
Just like peripheral mechanisms of thermo-regulation, central nervous thermoregulatory mechanisms are developed early and might show the same fundamental characteristics in the prenatal condition as experienced in the postnatal. During investigation in Muscovy duck embryos, Tzschentke and Basta (2000) found thermosensitive PO-AH neurons on E22 and E23 that showed characteristics similar to posthatching (Tzschentke and Basta, 2000), growing (unpublished data), and adult birds (Nakashima et al. 1987) as well as mammals (Schmid and Pierau, 1993). From d 28 of incubation until hatching, the proportion of CS, WS, and TI neurons in relation to all neurons investigated was very constant and not significantly different from that in hatchlings (Figure 6Go; Tzschentke and Basta, 2000, Tzschentke et al., 2004).


Figure 6
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  		Figure 6. Influence of age on proportion of warm-, cold-, and temperature-insensitive neurons in relation to all neurons investigated in their respective age groups in the preoptic area of the anterior hypothalamus of Muscovy ducks (modified from Tzschentke and Basta, 2000). Asterisks represent significance at the level of P < 0.05. E = embryonic day; d = day posthatching.

 
In contrast to the growing and adult ducks, the neuronal hypothalamic thermosensitivity in embryos and ducklings during the first days of posthatching is characterized by a higher neuronal cold sensitivity. A qualitative change occurs from d 5 to 10 in the neuronal thermosensitivity of the PO-AH from the "juvenile" to the "adult" type (Tzschentke and Basta, 2000), which is characterized by a high warm sensitivity and a low cold sensitivity (Nakashima et al., 1987). A similar developmental pattern is also found in chicken during early postnatal development (Sallagundala et al., 2006).

In Muscovy duck embryos as well as in ducklings during the first 10 d of life (Tzschentke et al., 2000), thermo-sensitivity of PO-AH neurons can be modulated by the neuropeptide bombesin. Bombesin is one of the most investigated neuropeptides known to influence thermoregulation in ectothermic and endothermic vertebrates (Brown et al., 1977; Jansky et al., 1987; Schmid et al., 1993; Kozlovskii and Pastukhov, 1995; Leger and Mathieson, 1997). Further, temperature guardian neurons, which are temperature sensitive over a small temperature range not more than 1°C during the applied sinusoidal temperature range, have been found in Muscovy duck embryos on E28 (Tzschentke and Basta, 2000; Tzschentke et al., 2004). Such neurons were first described from my group in 10-d-old Muscovy ducklings (Basta et al., 1997). Temperature guardian neurons are exclusively sensitive to extreme low or high brain temperatures and may activate more effective thermoregulatory mechanisms if the normal regulatory range is exceeded.

Altogether, during late prenatal development, poultry embryos have all prerequisites (autonomic, behavioral, and central nervous mechanisms) to react on changes in incubation temperature. In bird embryos, especially studied in the Muscovy duck, mechanisms for central nervous control of temperature regulation are well developed. For early consolidation and maturation of body functions, sensory inputs are necessary. Environmental influences (e.g., temperature, light, acoustic signals) can stimulate this process (training effect). The typical reaction pattern of body functions, especially thermoregulatory mechanisms, on external stimuli during early ontogeny has been explained in detail in the following section.

Typical Reaction Pattern of Physiological Mechanisms on Acute and Chronic Environmental Stimulation during the Perinatal Period
Environmental manipulations during the prenatal or early postnatal phase first lead to uncoordinated and almost nonadaptive reactions of the respective physiological control systems. The theory is that during early ontogenesis of body functions, it seems not to be important for the organism that a distinct adaptable reaction on various environmental influences occurs, but rather that any reaction occurs seems to be important for the adaptability during later life (training effect). These proximate nonadaptive reactions become coordinated and adaptive during later development, probably with closing of the regulatory system. For instance, experiments at the end of incubation time in chicken embryos have revealed first proximate nonadaptive and later adaptive reactions with respect to the influence of cooling and warming on blood flow in the vessels of the chorioallantoic membrane (Nichelmann and Tzschentke, 2003). In chicken embryos, the blood flow increased or decreased while warming or cooling on E15 until E19 (proximate nonadaptive). After this period, the reaction became proximate adaptive; on E20 and E21, the blood flow in the chorioallantoic membrane increased during warming and decreased during cooling, as expected (Figure 7Go). Similar changes in the blood flow during cooling or warming have also been found in Muscovy duck embryos at the end of incubation (Tzschentke, 2002). Also in other systems (e.g. heart frequency; Höchel et al., 2002) and on cellular levels in the brain (e.g. neuronal hypothalamic thermosensitivity, mentioned in next paragraph), first proximate nonadaptive reaction on acute or chronic environmental stimulation was found during the perinatal period. As shown in Figure 7Go, in chicken embryos, E19 seems to be the critical day related to changes from proximate nonadaptive into adaptive reactions in the blood flow in the chorioallantoic membrane under both environmental conditions (cooling as well as warming). In Muscovy ducklings, this change after cooling and warming seems to occur on different days of incubation. It is similar with the early development of the primate visual system, in which for each specific visual function, different and partially overlapping critical periods were found (Harwerth et al., 1986).


Figure 7
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  		Figure 7. Influence of warming (38.5°C) and cooling (35.5°C) on blood flow in the chorioallantoic membrane of 15- to 21-d-old chicken and 26-to 34-d-old Muscovy duck embryos. Each column represents the reaction in 1 individual embryo, expressed in flux, which is given in arbitrary units. The blood flow was measured using the laser Doppler method (modified from Nichelmann and Tzschentke, 1999, 2003).

 
However, this characteristic reaction pattern could be a physiological tool, that helps to characterize a critical period of the respective system during early development, whereas regulatory systems develop from an open loop system without feedback into a closed control system with feedback (Tzschentke and Plagemann, 2006).

Imprinting of Physiological Control Systems during the Perinatal Period: Prenatal Epigenetic Temperature Adaptation
Basic Concept of Imprinting of Physiological Control Systems.
During critical developmental periods, a long-term adaptation to the actual environment occurs via epigenetic adaptation processes. Our hypothesis states that, during the perinatal period, imprinting of physiological control systems occur that is probably realized by both neural imprinting at the microstructural level (e.g., in terms of synaptic plasticity) as well as by lasting environment-induced modification of the genome (Tzschentke and Plagemann, 2006). Basically, most functional systems of the organism develop from open loop systems without feedback control into closed control systems regulated by feedback mechanisms. During critical periods, the actual level at which physiological parameters occur may predetermine the set point (set ranges) of the respective physiological control system during the entire life period, possibly through acquired changes in the expression of related effector genes. Determination of the set point depends on the environment experienced by the embryo and fetus during critical periods of development (first described as determination rule by Dörner, 1974). In general, in the etiological concept of epigenetic perinatal programming of the lifetime function of fundamental regulatory systems, developed by Dörner (1974), hormones play a decisive role as environment-dependent organizers of the neuroendocrine immune system, which finally regulates all fundamental processes of life (Dörner, 1975, 1976). During critical periods, hormones as well as neurotransmitters and cytotokines (as immune cell hormones) act as critical endogenous effectors that transmit environmental information (e.g., sensible input) to the genome. Finally, they thereby also act as epigenetic factors.

On one hand, this mechanism seems to be a possible basis for perinatal malprogramming, which causes metabolic disorders and cardiovascular diseases as well as behavioural disorders during later life in mammals including man (Plagemann, 2004) as well as in birds (Schwabl, 1996, 1997; Ruitenbeek et al., 2000). On the other hand, knowledge and better understanding of these mechanisms might be specifically used to induce long-term adaptation of an organism, for instance, to postnatal climatic conditions (epigenetic temperature adaptation). Figure 8Go summarizes this conceptional approach.


Figure 8
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  		Figure 8. Induction of epigenetic perinatal malprogramming or epigenetic adaptation processes such as epigenetic temperature adaptation by environmental factors during the critical period of early development; basic concept (Tzschentke and Plagemann, 2006).

 
Epigenetic Temperature Adaptation.
Knowledge on imprinting of physiological control systems might be specifically used to induce long-term adaptation of an organism, for instance, to the postnatal climatic conditions. For an imprinting like that of the thermoregulatory system, the term epigenetic (temperature) adaptation was introduced (Nichelmann et al., 1994, 1999; Tzschentke and Basta, 2002; Tzschentke et al., 2004). In chicken and other precocial birds, epigenetic temperature adaptation can be induced by changes in incubation temperature at the end of embryonic development (Decuypere, 1984; Minne and Decuypere, 1984; Nichelmann et al., 1994; Tzschentke and Nichelmann, 1997; Tzschentke and Basta, 2002; Loh et al., 2004) as well as by thermal conditioning during the first days after hatching (Yahav and Plavnik, 1999; Yahav, 2000). Altogether, prenatal temperature experiences induce postnatal warm or cold adaptation (Tzschentke et al., 2004). The change in the levels of HP in differentially incubated birds occur already before hatching (Figure 9Go; Loh et al., 2004).


Figure 9
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  		Figure 9. Heat production of cold-, warm-, and normal-incubated chicken embryos on the last day of incubation investigated at 37.5°C (left panel) and at different incubation temperatures when the embryos were adapted (right panel). Results presented in boxplots are based on median and quartiles. Compared with all investigated groups, cold-incubated embryos have a significantly (P < 0.05) higher heat production when investigated at 37.5°C. The heat production in warm-incubated embryos is significantly (P < 0.05) higher when investigated at the respective adaptation temperature (modified from Loh et al., 2004); c = cold-incubated/cold temperature (34.5°C); n = normal-incubated/normal temperature (37.5°C); w = warm-incubated/warm temperature (38.5°C); the first letter indicates the incubation group and the second the incubation temperature at which the experiments were carried out.

 
On the last day of incubation, the cold-experienced chicken embryos had a significant higher HP when measured at 37.5°C. When investigations were made at 34.5°C, cold-incubated embryos did not show lower HP compared with the control (incubated at 37.5°C), even though the incubation temperature as well as Taf were at 3°C lower than in the control (Figure 10Go). The interesting aspect is that warm incubation seems to stimulate HP as well. However, to explain changes in HP in poultry embryos due to prenatal temperature experiences, it should be taken into consideration that temperature-dependent alterations in physiological processes can be caused by the Q10 effect related to the Van’t Hoff rule (Precht et al., 1973), by epigenetic mechanisms, or both. As described in the previous paragraph, further, proximate nonadaptive reactions on external stimuli can occur during the early development of body functions.


Figure 10
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  		Figure 10. Influence of incubation temperature on embryonic temperature (temperature of allantoic fluid) in warm- (ww; 38.5°C), cold- (cc; 34.5°C), and normal- (nn; 37.5°C) incubated chicken embryos from d 18 of incubation until hatch (Loh et al., 2004). Results presented in boxplots are based on median and quartiles (* is an extreme value). Note: In the present experiments, the first day of incubation is d 1 (in practice, it is d 0). In cold-incubated embryos, the development is delayed. These birds hatch 2 d later than the other groups. n = number of birds investigated.

 
On the first day posthatching, Muscovy ducklings incubated at lower temperatures than normal, for instance, having a 56% higher HP and a higher deep body temperature under cold load as compared with controls (1 h at 10°C). Cold-incubated birds are able to control their actual deep body temperature at their set point, in contrast to those incubated at 37.5°C, which display a lower HP (Nichelmann et al., 1994; Tzschentke et al., 2004). Minne and Decuypere (1984) found that cold-incubated chicken had a higher HP over a range of ambient temperatures up to 8 wk of posthatching. The higher HP was accompanied with higher triiodothyronine and thyroxine levels. In a temperature gradient, Muscovy ducklings incubated at a low temperature preferred a significantly lower temperature than birds incubated at the normal incubation temperature during the first 10 d of posthatching. This supports the hypothesis that avian prenatal cold experience leads to a downward shift of the thermoregulatory set point (Tzschentke and Nichelmann, 1999). On the other hand, the preferred ambient temperature in 1- to 10-d-old turkeys is higher after a prenatal heat load (38.5°C) than in birds incubated at the normal temperature (37.5°C). This indicates an elevation of the thermoregulatory set point after prenatal heat load.

Prerequisites for the changes in the thermoregulatory set point are the changes that occur in prenatal body temperature during critical periods of early development (as mentioned under "Basic Concept of Imprinting of Physiological Control Systems"). In our experiments, we found a strong influence of chronic changes in incubation temperature at the end of embryonic development on body temperature (Taf) of chicken as well as Muscovy duck embryos (Figure 10Go). If there occurs a critical period at the end of the embryonic development of the thermo-regulatory system, the lower Taf under cold conditions and the higher Taf under warm conditions is related with the lower and higher posthatching set points.

Our basic concept of imprinting of physiological control systems (Tzschentke and Plagemann, 2006) states that on one hand this process is probably realized via neural imprinting at the microstructural level (e.g., in terms of synaptic plasticity). In our experiments, changes in the neuronal thermosensitivity of the hypothalamic control center of the thermoregulatory system reflect the changes in peripheral thermoregulatory mechanisms after prenatal temperature experiences. Prenatal cold experience increases on d 10 of posthatching; the neuronal hypothalamic warm sensitivity and prenatal heat experiences increase neuronal hypothalamic cold sensitivity. Changes in neuronal hypothalamic thermosensitivity start at the end of incubation. On the last day of incubation, changes in neuronal hypothalamic thermosensitivity are not significant, but they become significant on d 1, 5, and 10 posthatching. From the last day of incubation until d 5 of posthatching, the changes are independent of the temperature experienced within the prenatal period (proximate nonadaptive). On d 10 of life, the changes are proximate adaptive (Figure 11Go). During the early ontogeny, such strong changes in the neuronal network that control specific body functions, like thermoregulation, could be related to the development of synaptic contacts. At the beginning of this procedure, the number of synaptic contacts increases, whereas later their number decreases (Brown et al., 2004). For both steps of the development of synaptic contacts, sensory stimulation is essential. Only those contacts remain that are necessary to maintain homeostasis under the respective surroundings and that repeatedly receive sensory input (Bock et al., 2003).


Figure 11
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  		Figure 11. Proportion of warm-, cold-, and temperature-insensitive hypothalamic neurons in relation to all neurons investigated in Muscovy duck embryos and ducklings incubated at 34.5, 37.5 (control group), and 38.5°C [modified from Loh et al., 2004 (embryos) and Tzschentke and Basta, 2002 (ducklings)]. Total number of investigated neurons in embryos was 81 (cold-incubated group), 74 (control group), and 87 (warm-incubated group). In 1-, 5-, and 10-d-old ducklings, the total number was 80 neurons for each incubation temperature. Asterisks represent significance at the level of *P < 0.05, **P < 0.01, and ***P < 0.001.

 
On the other hand, the basic concept of imprinting of physiological control systems states that this process is realized by lasting environment-induced modification of the genome (Tzschentke and Plagemann, 2006). Initial studies on hypothalamic c-fos expression (Janke and Tzschentke, 2006) related to prenatal temperature changes as well as expression of brain-derived neurotrophic factor (Katz and Meiri, 2006) and R-Ras3 gene (Labunskay and Mairi, 2006) related to postnatal thermal conditioning could show changes on the level of gene regulation. In our experiments (Janke and Tzschentke, 2006), we used the transcription factor and early immediate gene c-fos as stress markers to detect acute heat stress in chicken embryos on the last day of incubation adapted to different incubation temperatures (34.5, 37.5, and 38.5°C). Heat stress evoked c-fos expression in the PO-AH in all embryos but not in the unstressed control. Even the differences between the groups were not significant, trends that show that temperature-experienced embryos have a lower c-fos expression than in the control after acute heat stress. These proximate nonadaptive changes (in this study related to the cold-incubated group) are in accordance with the previously described results from electrophysiological (Tzschentke and Basta, 2002; Tzschentke et al., 2004) and metabolic (Loh et al., 2004) investigations in temperature-experienced poultry embryos. After thermal conditioning on d 3, posthatching changes in the R-Ras3 gene expression are found in the PO-AH with a 10-fold peak after 12 h of heat conditioning and a 4-fold increase after 6 h of cold conditioning (Labunskay and Meiri, 2006). Similar changes were found in the brain-derived neurotrophic factor induction in both heat-and cold-exposed birds. A main question that needs to be addressed during further investigations is if these changes in the central nervous network and also in the periphery are long-lasting (Yahav and Tzschentke, 2006).


   SUMMARY AND CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 SUMMARY AND CONCLUSIONS
REFERENCES
 
At the end of prenatal development, poultry embryos have all prerequisites (autonomic, behavioral, and central nervous mechanisms) to react on changes in incubation temperature, even though the thermoregulatory system is not mature. The level of full maturity is attained in the posthatching period. In comparison with the heat loss mechanisms, in embryos efficiency of thermoregulatory HP is very low. Mechanisms for central nervous control of temperature regulation seem to be well developed.

For early consolidation and maturation of body functions, sensory inputs (e.g., environmental influences) are essential and can stimulate this process (training effect). The typical reaction pattern of thermoregulatory mechanisms on external stimuli during early ontogeny has been first an uncoordinated and proximate nonadaptive reaction that changes during later development into a proximate adaptive one. The early training of body functions (e.g., by environmental stimulation) can improve the development of central as well as peripheral physiological mechanisms. This might also be a basis for postnatal health, welfare, and productivity in poultry.

During critical developmental periods, a long-term adaptation to the actual environment occurs via epigenetic adaptation processes. During the perinatal period, imprinting of physiological control systems, like the thermo-regulatory system, occurs. Imprinting is realized by both the changes of synaptic plasticity as well as by lasting environment-induced modification of the genome. Perinatal epigenetic temperature adaptation could be a tool to adapt poultry embryos or hatchlings to later climatic conditions. For the specific use of perinatal epigenetic temperature adaptation in practice, more investigations on the basic mechanisms of imprinting of physiological control systems and on the problem of critical periods are necessary.


   ACKNOWLEDGMENTS
 
Research projects carried out in my working group, Perinatal Adapation, were supported by grants of the Deutsche Forschungsgemeinschaft (Ni 336/3-1; TZ 6/2-1, 6/2-2, 6/6-4, 6/10).


   FOOTNOTES
 
1 Presented as part of the Embryo Symposium: Managing the Embryo for Performance, July 19, 2006, at the Poultry Science Association Annual Meeting, Edmonton, Alberta, Canada. Back

Received for publication November 9, 2006. Accepted for publication November 19, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 SUMMARY AND CONCLUSIONS
 REFERENCES
 
Ar, A., O. Ifergen, A. Feldman, L. Zelik, and A. Reizis. 2004. Possible role of nitric oxide emission from bird embryos. Avian Poult. Biol. Rev. 15:105–106.

Arad, Z., and J. Marder. 1983. Acid-based regulation during thermal panting in the fowl (Gallus domesticus): Comparison between breeds. Comp. Biochem. Physiol. A 74:125–130.

Basta, D., B. Tzschentke, and M. Nichelmann. 1997. Temperature guardian neurons in the preoptic area of the hypothalamus. Brain Res. 767:361–362.[ISI][Medline]

Bock, J., C. Helmeke, W. Ovtscharoff Jr., M. Gruss, and K. Braun. 2003. Frühkindliche emotionale Erfahrungen beeinflussen die funktionelle Entwicklung des Gehirns. Neuroforum 2:51–55.

Brown, M., R. Keynes, and A. Lumsden. 2004. The developing brain. Oxford Univ. Press, Oxford, UK.

Brown, M., J. Rivier, and W. Vale. 1977. Bombesin: Potent effects on thermoregulation in the rat. Science 196:998–1000.[Abstract/Free Full Text]

Decuypere, E. 1984. Incubation temperature in relation to post-natal performance in chickens. Arch. Exp. Veterinarmed. 38:439–449.[ISI][Medline]

Dörner, G. 1974. Environment-dependent brain differentation and fundamental processes of life. Acta Biol. Med. Ger. 33:129–148.[ISI][Medline]

Dörner, G. 1975. Perinatal hormone levels and brain organization. Anat. Neuroendocrinol. 1:245–252.

Dörner, G. 1976. Hormones and Brain Differentiation. Elsevier, Amsterdam, the Netherlands.

Evans, R. M., A. Whitaker, and M. O. Wiebe. 1994. Development of vocal regulation of temperature by embryos in pipped eggs of ring-billed gills. Auk 111:596–604.[ISI]

Harwerth, R. S., E. L. Smith, G. C. Duncan, M. L. Crawford, and G. K. von Noorden. 1986. Multiple sensitive periods in the development of the primate visual system. Science 232:235–238.[Abstract/Free Full Text]

Höchel, J., R. Pirow, and M. Nichelmann. 2002. Development of heart rate responses to acoustic stimuli in Muscovy duck embryos. Comp. Biochem. Physiol. A 131:805–816.[Medline]

Holland, S., J. Höchel, A. Burmeister, O. Janke, and M. Nichelmann. 1998. A method for measuring deep body temperature in avian embryos. J. Therm. Biol. 23:123–129.[ISI]

Ifergan, O., and A. Ar. 1999. Embryo-incubating bird communication: Yes or no? Isr. J. Zool. 45:309–310.

Janke, O., and B. Tzschentke. 2006. Hypothalamic c-fos expression of temperature experienced chicken embryos after acute heat exposure. Pages 109–115 in New Insights into Fundamental Physiology and Perinatal Adaptation in Domestic Fowl. S. Yahar and B. Tzschentke, ed. Nottingham Univ. Press, UK.

Janke, O., B. Tzschentke, J. Höchel, and M. Nichelmann. 2002. Metabolic responses of chicken and Muscovy duck embryos to high incubation temperatures. Comp. Biochem. Physiol. A 131:741–750.[Medline]

Jansky, L., W. Riedel, E. Simon, C. Simon-Oppermann, and S. Vybiral. 1987. Effect of bombesin on thermoregulation of the rabbit. Pflügers Arch. 409:318–322.[ISI][Medline]

Katz, A., and N. Meiri. 2006. Brain-derived neurotrophic factor is critically involved in thermal-experience-dependent developmental plasticity. J. Neurosci. 26:3899–3907.[Abstract/Free Full Text]

Kozlovskii, S. V., and Y. F. Pastukhov. 1995. Effect of the fish hypobiosis peptide and bombesin-14 on thermoregulatory behaviour of the goldfish Carassius auratus. J. Evol. Biochem. Physiol. (translated from Zh. Evol. Biohim. Fiziol.) 31:161–164.

Kuenzel, W. J., and M. Masson. 1988. A stereotaxic atlas of the brain of the chick (Gallus domesticus). John Hopkins Univ. Press, Baltimore, MD.

Labunskay, G., and N. Meiri. 2006. R-Ras3/(M-Ras) is involved in thermal adaptation in the critical period of thermal control establishment. J. Neurobiol. 66:56–70.[ISI][Medline]

Leger, J. P., and W. B. Mathieson. 1997. Effect of bombesin on behavioural thermoregulation in the bullfrog. Brain Behav. Evol. 50:304–312.[ISI][Medline]

Loh, B., I. Maier, A. Winar, O. Janke, and B. Tzschentke. 2004. Prenatal development of epigenetic adaptation processes in poultry: Changes in metabolic and neuronal thermoregulatory mechanisms. Avian Poult. Biol. Rev. 15:119–128.

Minne, B., and E. Decuypere. 1984. Effects of late prenatal temperatures on some thermoregulatory aspects in young chickens. Arch. Exp. Veterinarmed 38:374–383.[ISI][Medline]

Murzenok, P., S. Holland, and M. Nichelmann. 1997. Study of development of respiration in chicken embryos during internal pipping. Pages 167–172 in Proc. III. Int. Workshop Invest. Perinat. Dev. Birds. H. Tönhardt and R. Lewin, ed. Inst. Vet.-Physiol., Freie Univ. Berlin, Germany.

Nakashima, T., F. K. Pierau, E. Simon, and T. Hori. 1987. Comparison between hypothalamic thermoresponsive neurons from duck and rat slices. Pfluegers Arch. 409:236–243.[ISI][Medline]

Nichelmann, M., A. Burmeister, O. Janke, J. Höchel, and B. Tzschentke. 1998. Avian embryonic thermoregulation: Role of Q10 in interpretation of endothermic reactions. J. Therm. Biol. 23:369–376.[ISI]

Nichelmann, M., J. Höchel, and B. Tzschentke. 1999. Biological rhythms in birds—development, insights and perspectives. Comp. Biochem. Physiol. A 124:429–437.[Medline]

Nichelmann, M., O. Janke, J. Höchel, and B. Tzschentke. 2001. Development of physiological control systems in avian embryos. News Biomed. Sci. 1:15–25.

Nichelmann, M., B. Lange, R. Pirow, J. Langbein, and S. Herrmann. 1994. Avian thermoregulation during the perinatal period. Pages 167–173 in Thermal Balance in Health and Disease. Advances in Pharmacological Science. E. Zeisberger, E. Schönbaum, and P. Lomax, ed. Birkhäuser Verlag, Basel, Switzerland.

Nichelmann, M., and B. Tzschentke. 1997. Ontogeny of thermo-regulation during the prenatal period in birds. Ann. N. Y. Acad. Sci. 813:78–86.[Medline]

Nichelmann, M., and B. Tzschentke. 1999. Thermoregulatory heat production in precocial avian embryos. Ornis Fenn. 76:177–187.

Nichelmann, M., and B. Tzschentke. 2001. Efficiency of thermo-regulation in precocial avian species during the prenatal period. J. Therm. Biol. 26:273–280.[ISI]

Nichelmann, M., and B. Tzschentke. 2002. Ontogeny of thermo-regulation in precocial birds. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 131:751–763.[Medline]

Nichelmann, M., and B. Tzschentke. 2003. Efficiency of thermo-regulatory control elements in precocial avian embryos (Review). Avian Poult. Biol. Rev. 14:1–19.

Plagemann, A. 2004. ‘Fetal programming’ and ‘functional teratogenesis’: On epigenetic mechanisms and prevention of perinatally acquired lasting health risks. J. Perinat. Med. 32:297–305.[ISI][Medline]

Precht, H., J. Christopherson, H. Hensel, and W. Larcher. 1973. Temperature and Life. Springer-Verlag, Berlin, Germany.

Prinzinger, R., and V. Dietz. 1995. Qualitative course of embryonic O2-consumption in altricial and precocial birds. Resp. Physiol. 100:289–294.[ISI][Medline]

Ruitenbeek, K., F. A. Le Noble, G. M. Janssen, C. G. Kessels, G. E. Fazzi, C. E. Blanco, and J. G. De Mey. 2000. Chronic hypoxia stimulates periarterial sympathetic nerve development in the chicken embryo. Circulation 102:2892–2897.[Abstract/Free Full Text]

Sallagundala, N., K. Yakimova, and B. Tzschentke. 2006. Characterization of neuronal hypothalamic plasticity in chicken: A comparative analysis. Pages 99–108 in New Insights into Fundamental Physiology and Perinatal Adaptation in Domestic Fowl. Y. Yahav and B. Tzschentke, ed. Nottingham Univ. Press, UK.

Samuni, M., and A. Ar. 2006. Can nitric oxide emitted from incubated eggs be used to indicate stress? Int. Hatch. Pract. 20:29. (Abstr.)

Schmid, A. H., L. Jansky, and Fr.-K. Pierau. 1993. Temperature sensitivity of neurons in slices of the rat PO/AH area: Effect of bombesin and substance P. Am. J. Physiol. 264:R449–R455.[ISI][Medline]

Schmid, H. A., and Fr.-K. Pierau. 1993. Temperature sensitivity of neurons in slices of the rat PO/AH hypothalamic area: Effect of calcium. Am. J. Physiol. 264:R440–R448.[ISI][Medline]

Schwabl, H. 1996. Maternal testosterone in avian egg enhances postnatal growth. Comp. Biochem. Physiol. A Physiol. 114:271–276.[Medline]

Schwabl, H. 1997. Maternal steroid hormones in the egg. Pages 3–13 in Perspectives in Avian Endocrinology. S. Harvey and R. J. Etches, ed. Soc. Endocrinol., Bristol, UK.

Tazawa, H. 1987. Embryonic respiration. Pages 4–41 in Bird Respiration. T. J. Seller, ed. CRC Press. Inc., Boca Raton, FL.

Tazawa, H., Y. Chiba, A. H. Khandoker, E. M. Dzialowski, and W. W. Burggren. 2004. Early development of thermoregulatory competence in chickens: Responses of heart rate and oxygen uptake to altered ambient temperatures. Avian Poult. Biol. Rev. 15:166–176.

Tazawa, H. and H. Rahn. 1987. Temperature and metabolism of chick embryos and hatchlings after prolonged cooling. J. Exp. Zool. (Suppl. 1):105–109.

Tazawa, H., and G. C. Whittow. 2000. Incubation physiology. Pages 617–634 in Sturkey’s Avian Physiology. 5th ed. Acad. Press, New York, NY.

Tzschentke, B. 2002. Stimulate body functions of embryos and get them used to the post-hatch environment. World. Poult. 10:22–25.

Tzschentke, B. 2003. Energy saving mechanisms during the early ontogeny in precocial birds. News Biomed. Sci. 1:12–16.

Tzschentke, B., and D. Basta. 2000. Development of hypothalamic neuronal thermosensitivity in birds during the perinatal period. J. Therm. Biol. 25:119–123.[ISI]

Tzschentke, B., and D. Basta. 2002. Early development of neuronal hypothalamic thermosensitivity in birds: Influence of epigenetic temperature adaptation. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 131:825–832.[Medline]

Tzschentke, B., D. Basta, A. V. Gourine, and V. N. Gourine. 2000. Influence of bombesin on neuronal hypothalamic thermosensitivity during the early postnatal period in the Muscovy duck (Cairina moschata). Regul. Pept. 88:33–39.[ISI][Medline]

Tzschentke, B., D. Basta, O. Janke, and I. Maier. 2004. Characteristics of early development of body functions and epigenetic adaptation to the environment in poultry: Focused on development of central nervous mechanisms. Avian Poult. Biol. Rev. 15:107–118.

Tzschentke, B., and M. Nichelmann. 1997. Influence of prenatal and postnatal acclimation on nervous and peripheral thermo-regulation. Ann. N. Y. Acad. Sci. 813:87–94.[Medline]

Tzschentke, B., and M. Nichelmann. 1999. Development of avian thermoregulatory system during the early postnatal period: Development of the thermoregulatory set-point. Ornis Fenn. 76:189–198.

Tzschentke, B., M. Nichelmann, and T. Postel. 1996. Effects of ambient temperature, age and wind speed on the thermal balance of layer strain fowls. Br. Poult. Sci. 37:501–520.[ISI][Medline]

Tzschentke, B., and A. Plagemann. 2006. Imprinting and critical periods in early development. World’s Poult. Sci. J. 62:626–638.[ISI]

Vieht, E. 1989. Fitting piecewise linear regression functions to biological responses. J. Appl. Physiol. 67:390–396.[Abstract/Free Full Text]

Whittow, G. C., and H. Tazawa. 1991. The early development of thermoregulation in birds. Physiol. Zool. 64:1371–1390.

Yahav, S. 2000. Domestic fowl—strategies to confront environmental conditions. Avian Poult. Biol. Rev. 11:81–95.

Yahav, S., and I. Plavnik. 1999. Effects of early-age thermal conditioning and food restriction on performance and thermotolerance of male broiler fowl. Br. Poult. Sci. 40:120–126.[ISI][Medline]

Yahav, S., and B. Tzschentke. 2006. Perinatal thermal manipulations in poultry, does it cause long-lasting thermoregulatory memory? Proc. EPC, Verona, Italy. WPSA, Italian Branch, Verona.





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