In precocial birds including poultry, physiological

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1 Effect of hatching time on poultry behaviour: the impact of incubation environment during the last days of embryonic development On Humboldt-University of Berlin Institute of Biology, Perinatal Adaptation Philippstrasse 13, Berlin, Germany Introduction Stage of development of physiological functions during hatching time In precocial birds including poultry, physiological mechanisms are well developed during hatching time, which represents the last days of embryonic development (roughly from plateau phase until hatching). Peripheral and central nervous mechanisms, for instance, of the cardio-vascular-, respiratory-, and thermoregulatory system show characteristics, which are not very different from the post-hatching one. Most of the regulatory systems undergo a dramatic qualitative change from an open loop system without feed back mechanisms into a closed control system with feed back mechanisms (Tzschentke and Plagemann, 2006 Tzschentke, 2007; Tzschentke and Rumpf, 2011). In chicken embryos the hypothalamic-pitatury-thyroidal axis, for instance, is functional on embryonic day (E) 19 (Muchow et al., 2005). In this species, also the thermoregulatory system shows feed back reactions on acute temperature influences during the last days of embryonic development (Tzschentke and Plagemann, 2006 Tzschentke, 2007; Tzschentke and Rumpf, 2011). Sensory modalities in avian embryos develop in the following sequence: (1) nonvisual photic sensitivity, (2) tactile sensitivity, (3) vestibular sensitivity, (4) proprioception, (5) audition and (6) vision (after Gottlieb, 1968 and Vince, 1974). Hence, the sensory capacity for hearing and vision in bird embryos develops lastly, but both are functional during hatching time. During the last days before hatching the embryos may also activate behavioural mechanisms. The embryos are able to produce calls (Tuculescu and Griswold, 1983; Rumpf and Nichelmann, 1993; Brua, 2002). Embryonic motility is an important component of development and may be a precursor of post-hatching motor behaviour (Nechaeva et al., 2010). In chicken embryos first movements occur on E3.5, increase during development, and during final incubation possibly transforms into targeted hatching behaviour (Hamburger and Balaban, 1963; Hamburger et al., 1965; Oppenheim, 1966; Bradley, 1999; Bekoff, 1992; 2001; Nechaeva et al., 2010). Finally, the embryos have all prerequisites to react on environmental influences on physiological, neuroendocrine and with limits on behavioural level (e.g. acoustic communication, motility). Impact of environmental factors during embryonic development The major impact of prenatal and early postnatal environmental conditions for later development and performance in poultry is more and more accepted. Especially during critical periods the effect of the actual environment is long-lasting and may be even passed on the succeeding generations in an epigenetic fashion (Plagemann, 2004; Tzschentke and Plagemann, 2006). A critical period is a strict time window during which a certain experience necessarily must occur to enable development to proceed normally and permanently alters performance (Baily et al., 2001; Hensch, 2005). But it has to be considered that even within a species different physiological functions and mechanisms of the respective function may have different critical periods, which may arise in an earlier stage of embryonic development, during hatching time or the early post-hatching development or be overlapping (Harwerth et al., 1986; Tzschentke and Plagemann, 2006). In this context imprinting of body functions, which mostly occurs during perinatal critical developmental periods, is a basic mechanism and obviously a fundamental process 1

2 of life. In his classical studies on newly hatched goslings, Konrad Lorenz analysed the development of social binding, applying the term imprinting to describe this process (Lorenz, 1935). One of his major hypotheses was that imprinting occurs during limited and severely restricted critical periods in early life. Later, Günter Dörner, a pioneering developmental neuroendocrinologist, developed a general origination concept of the epigenetic perinatal programming of the lifetime function of fundamental regulatory systems (Dörner, 1974, 1975). Hormones as well as neurotransmitters and cytotokines (as immune cell hormones) play a central role in this concept. They act as carriers of environmental information to the genome. Ultimately, they too are acting as epigenetic factors with long-lasting effects particularly during critical developmental periods (Fig. 1). As an example, a critical period in the development of regulatory systems is the development of feed back mechanisms. In chick and Muscovy duck embryos first feed back control of the thermoregulatory system, for instance, was found during hatching time (Tzschentke and Plagemann, 2006). Imprinting of physiological conrol systems Developmental trajectory critical period environmental influences a later developmental stage. For instance, shortterm alterations in incubation temperature did not change embryonic motor activity in an early stage of incubation (E5 E14; Oppenheim and Levin, 1975; Nechaeva and Turpaev, 1991). But, a shortterm temperature increase or decrease modified embryonic motility in older embryos (E15 E20; Oppenheim and Levin, 1975). Similar age dependent influence on motility was also found under hypoxia (Nechaeva et al., 2010; Nechaeva, 2011). Whether such short-term environmental influences on motor activity during the last third of incubation have also an effect on post-hatching motor behaviour needs further investigations. Finally, there are two possibilities regarding long-lasting effects of environmental factors during incubation on later development including behaviour. On one hand, the incubation environment is a basis for perinatal mal programming, which besides metabolic disorders and cardiovascular diseases also may cause behavioural disorders in birds during later life (Schwabl, 1996, 1997; Bock et al., 2005). On the other hand, knowledge and better understanding of the imprinting mechanisms might be specifically used to induce long-term adaptation of an organism, for instance, to the postnatal climatic conditions (epigenetic temperature adaptation; Nichelmann et al., 1994, 1999; Tzschentke and Basta, 2002), which includes also behavioural thermoregulation. 2 developing embryo/fetus pre-programmed by genetics instructions changes in hormone concentration transmitters/ neuropeptides cytokines Figure 1 - Imprinting of physiological control systems by environmental factors during critical periods of early development (modified from Tzschentke and Plagemann, 2006). Importance of prenatal environmental factors on behaviour Behaviour is an interaction between the organism (genes and physiological status/ homeostasis) and the environment (Tembrock, 1978). Prenatal environment may immediately influence the embryonic behaviour und may also induce longlasting behavioural alterations after hatching. Clear modifications of embryonic behaviour by environmental influences were mostly found in longlasting modification of the pre-determined adult phenotype via changes in gene expression Altogether, the long-lasting influence of incubation factors on post-hatching behaviour in poultry is not much investigated. The following presentation is focused on the influence of acoustic signals, light and temperature during hatching time on poultry behaviour. Acoustic signals, hatching synchronization and post-hatching behaviour Development of hearing, sound transmission Jones et al., (2006) proposed two periods of ontogeny of the hearing system in chick embryos. The first period is the so-called prehearing period

3 (about E12-E16). It is the period of endogenous cochlea (inner ear) signalling. It is important for the normal development of the central binaural processing pathway. In the second period (about E16-E19) the cochlea begins to detect and encode sound. In the late chick embryos between E18 and E 21 auditory structures and functions show an adultlike development in most respects (for details, see Rubel and Parks, 1988; Manley et al., 1991; Jones and Jones 1995a,b; Jones et al., 2006). Also in other poultry species exogenous acoustic signals are detectable at the beginning of the plateau phase of metabolism. In Muscovy ducks with an incubation time of 33 days, for instance, the acoustic-sensorycardiac axis is functional from embryonic day 27 and heart rate responses to acoustic stimulation were observed (Höchel et al., 2002). membrane a species-specific sound repertoire develops gradually. During the final prenatal period vocalization activity rises that as is especially evident in those bird species having a long period of prenatal vocal production. Fig. 2 shows the vocalization activity of the Muscovy duck (Rumpf and Nichelmann, 1993). The number of vocalization increased within the 3 days before hatching as studied in single and in paired embryos. Similar results of increasing vocalization activity are published for naturally incubated domestic chick embryos (Tuculescu and Griswold, 1983). Whether an embryo can hear only its neighbour or all the embryos in the clutch depends on sound transmission between the eggs. Rumpf and Tzschentke (2010) described measurements of sound transmission in Muscovy duck embryos at E32 before the outer eggshell was pipped (2-3 days before regular hatching) using an artificial sound emitter (broad band noise signal in the range of Hz, in the range of the embryos own sound production frequencies). The artificial sound was presented to the first egg and was measured on each of the 9 following eggs in 10 lengthwise or crosswise positioned eggs. Summarizing all measured frequencies, sound absorption in crosswise positioned eggs was by 5-10 db greater compared with that of lengthwise positioned eggs (Lauch, 1989). Above 3 khz no frequency dependence of sound absorption was measured. As sound absorption from the first to the 6th egg amounted to 10 db it can be assumed that embryos have mutual acoustic contact with all the other embryos in a clutch. Finally, sound transmission is based on a sound-conducting medium. In a clutch, sound is conducted via the eggshell, lengthwise and crosswise. In industrial or commercial incubators a metal grid or a metal setter tray may serve as a sound-conducting medium. Even in the case when embryos are connected via a metal grid, a nearly perfect sound conductance was measured (Lauch, 1989). Finally, we suppose that most sound within the prenatal period is bone-conducted and not airconducted (Rumpf and Tzschentke, 2010). Sound production (1) Vocalizations and its relevance for acoustic communication Beginning with penetrating the inner egg Figure 2 - Prenatal vocal activity of single (white columns) and paired embryos (black columns). Each column represents the mean value of three embryos (significant different, p<0.01 three days and one day before hatching, not significant different 2 days before hatching) from Rumpf and Tzschentke (2010), according to Rumpf and Nichelmann (1993). Higher acoustic activity might be regarded as non-specific mutual stimulation which is supported generally by the birds` own vocalization or other stimulation within the perinatal period. Vice versa, a disruption of mutual vocal communication in the pre-hatching period led to lower acoustic postnatal activity and also damaged postnatal acoustic communication (Lauch, 1989). Pekin ducks, for instance, need embryonic experiences of a wide range of repetition rates of their contactcontentment call to develop a preference for maternal calls (Gottlieb, 1985). Also recent studies in domestic chicken (Kauser et al., 2011) and the bobwhite quail (Harshaw and Lickliter, 2011) have shown that prenatal auditory stimulation with either species-specific or complex rhythmic music sounds bias postnatal responsiveness to social stimuli, facilitates spatial learning and influences memory. 3

4 4 Up to now it is not known if and how the embryos receive the acoustic signals of the breeding parent. But it is likely that the breeding parent receives the acoustic signals of the embryos. Vocalizations of the embryos may affect the behaviour of the parent (Tschanz,1968; Lauch, 1989) for instance eggturning, nest building or the amount of time parents spend on the nest. Embryonic vocalizations might also serve as caresoliciting signals concerning temperature regulation. Cold induced vocalization (distress calls; Fig. 3) may help to restore normal incubation temperature (Evans, 1989; 1990; Brua et al., 1996; Nichelmann and Tzschentke, 1997). Under natural conditions it may be a signal of the offspring s need for warmth from the incubating parents. For the full review to this topic see Rumpf and Tzschentke (2010). Figure 3 - Distress call rate of Muscovy duck embryos before (min -5 to 1) and after a cold stimulus of 20 to 22 C (min1 to 19) from Nichelmann and Tzschentke (1997). (2) Clicking sounds and its relevance for hatching synchronization Accompanying with the development of breathing the embryos begin to regularly produce so-called clicking sounds (Vince and Salter, 1967), clicks or clicking noises. Prenatal clicks are accompanying noises of respiration and not a real vocalization, controlled by the syrinx. In the Muscovy duck first clicking sounds were observed once the inner eggshell was penetrated (Lauch et al., 1988). The clicking rate (number of clicks per minute) corresponded with the audible respiration frequency. The development of the clicking rate of one Muscovy duck embryo from the first clicks to the hatching is shown in Fig. 4. Investigations on the development of prenatal clicking rate are only available for Muscovy ducks (Lauch et al., 1988; Lauch, 1989) and quails (Vince and Salter, 1967). Since the investigations by Vince on quails (1964a,b) it is known that the acoustic communication by clicking sounds is an essential factor for hatching synchronization. Vince discovered that the development and hatching time of quail embryos could be accelerated or decelerated, by clicking sounds (Vince,1966a,b; Vince 1968a,b; Vince and Cheng, 1970; Vince et al., 1984). In the Muscovy duck synchronization starts, when the second embryo within a clutch begins to click. Within certain, species-specific range embryos adapt their clicking rates to those of others. The result is a common rhythm. Muscovy duck embryos need about a minute to achieve this common rhythm (or beat). Normally, embryos try to synchronize their rhythms 1:1. Then the resulting clicking rate is the same in both or in all of the embryos. If the lung respiration is not sufficiently developed and the embryo cannot follow the given rhythm over a long time, the embryo initially follows the clicking beat irregularly (with breaks). Towards hatching, embryos click more and more regularly. Usually, the Muscovy duck embryos in a clutch were able to synchronize their clicking rates (Fig. 5 A, B) if the surrounding sound level does not exceed about 80 db as measured in industrial incubators (Nichelmann et al., 1990). However, if Figure 4 - Prenatal clicking rate of a single embryo (measured every 30 minutes); method described by Lauch et al., (1988). A- External pipping; B- Cutting (pipping while rotating); C- Hatch. Figure from Rumpf and Tzschentke (2010), according to Lauch et al., (1988).

5 the embryos had a big developmental difference to the next sibling, this embryo hatched considerably earlier or later (one example in Fig. 5 B). It can be hypothesized that small differences between the embryos as caused by, e.g., temperature can be compensated. For hatching synchronization in the Muscovy duck the mutual acoustic contact between the embryos was necessary during the whole prenatal clicking period (Lauch, 1989). As already given before, clicking sound communication is different from communication by vocalization (Rumpf and Tzschentke, 2010). In laboratory experiments using white noise in combination with low pass and high pass filters respectively, it was possible to eliminate clicking sound communication and allow communication by vocalization on the one hand, and to allow clicking sound communication but exclude communication by vocalization on the other hand (Lauch et al., 1988). Clicking rates and hatching synchronization were measured under different sound levels (steps of 5 db). Over a sound level of 80 db (white noise low pass filter) clicking sound communication was disturbed and Muscovy duck embryos hatched asynchronously (Fig. 5 C, D). Hatching interval under desynchronizing conditions (80 db) was significantly, on average 4 times longer, than under synchronizing conditions (Lauch et al., 1988). Commercial incubation conditions seem to be more similar to desynchronized laboratory conditions (Nichelmann et al., 1990). Summarizing all findings there is evidence that prenatal clicking sounds in contrast to other acoustic signals play an important role for hatching synchronization at least in quails and Muscovy ducks. For the full review to this topic see Rumpf and Tzschentke (2010). Light, brain development and post-hatching behaviour In precocial birds light stimulation during embryogenesis is very important for normal brain development. Especially the specialization of the avian hemispheres (brain lateralization) depends on light exposure of the embryo during hatching time. The influence of light during the last days before hatching on the brain lateralization is related to Figure 5 - Synchronization of prenatal clicking rates of 8 (A) and 12 (B) Muscovy duck embryos under a sound pressure level in the laboratory incubator of 50 db and desynchronization of prenatal clicking rates of 7 (C) and 12 (D) Muscovy duck embryos under a sound pressure level in the laboratory incubator of 80 db, from Rumpf and Tzschentke (2010), according to Lauch 1989). (broken line=eggshell pipped, mutual eggshell contact, white noise low-pass-filter<2khz ). 5

6 6 the body position of the embryo in the egg; the left eye is covered by the body and the right eye is near the light-transmissive egg shell, which was already observed in chick embryos by Kuo (1932). Lateralization of the brain is fundamental for the post-hatching behaviour (Rogers, 2011). For investigations of brain lateralization and behaviour, it is important to know, that the visual information from each eye is processed to the opposite hemisphere (left eye to right hemisphere, right eye to left hemisphere). The left eye-right hemisphere preferentially controls behaviour, which is important under emergency or stressful conditions (e.g. attention to novel objects, predators, fear response). In chicken the right hemisphere is also involved in copulation behaviour (Roger et al., 1985) and different aspects of social learning (Daisley et al., 2009), which includes, e.g., the maintenance of social hierarchy (Hogue et al., 1996) and recognition of face-like stimuli (Daisley et al., 2009). The main functions, which are preferentially controlled by the right eye-left hemisphere, are learnt and routine behaviour under nonstressful situations. The ability to learn to distinguish between different objects (e.g. between food grains and pebbles, Mench and Andrew, 1986), for instance, is a feature of the left hemisphere. Another example, which is controlled by the left hemisphere, is the ability to focus attention on training cues in an experiment (Roger et al., 2008). In dark incubated chicken and other bird species no or weakly developed anatomical and functional brain asymmetries were found (Dharmaretnam and Rogers, 2005; Rogers, 2011). During the first posthatching weeks limitations or losses in behavioural abilities (e.g. learning, social behaviour) are typical. Whether these behavioural changes are persistent needs further validation. In comparison with light incubated chicks, dark incubated chicks develop, for instance, less stable social hierarchies (Roger and Workman, 1989). They are unable to discriminate between different conditions (Chiandetti and Vallortigara, 2009) and produce more distress calls, followed by a higher fearfulness (Dharmaretnam and Rogers, 2005). Finally, dark incubated birds are more vulnerable to post-hatching stress. To reduce this negative effect, bird embryos need light exposure, which can be an important contribution to life-long welfare (Rogers, 2011). Incubation temperature and behaviour Investigations on the influence of incubation temperature on post-hatching behaviour in birds are rare. In Wood ducks (Aix sponsa) it was shown that already mild changes in incubation temperature have a significant influence on locomotion in the offsprings (Hopkins et al., 2011). In Wood ducks the natural incubation temperature varies between 34.8 and 37.8 C, so that also the incubation length differs from 30 to 37 days (Hepp et al., 2006). Locomotor activity of Wood ducks incubated at three different ecologically relevant temperatures (35 C, 35.9 C and 37 C) was tested at 15 and 20 days posthatching. Ducklings, which were incubated at the lowest temperature, showed a significantly reduced aquatic swim velocity compared with the ducklings, which were incubated at both higher temperatures (Hopkins et al., 2011). The authors suggest that the lower aquatic swim velocity at the lowest incubation temperature is a sign for reduced fitness, because locomotor activity might be important for survival under natural conditions. In poultry chronic and short-term changes in incubation temperature during the last days until hatch have different effects on the post-hatching performance and adaptability to the environment (Tzschentke and Halle, 2009; Halle and Tzschentke, 2011). The impact of these changes in incubation temperature on the post-hatching behaviour is not so much investigated. Some examples are given in the next paragraphs. Epigenetic temperature adaptation and post-hatching thermoregulatory behaviour Birds and mammals attain effective thermoregulation by physiological as well as behavioural mechanisms (Schmidt, 1984). Precocial birds are able to use thermoregulatory behaviour, like the innate ability for temperature preference, shortly after hatching. During the first days post-hatching behavioural temperature regulation is essential to maintain a stable body temperature, because the physiological mechanisms are not completely developed. Further, behavioural thermoregulation is not so much energy consuming like physiological thermoregulation. Finally, to regulate body temperature by behavioural mechanisms is an effective energy saving mechanism. During the first 10 days of life we found for different poultry species, for instance, a close relationship between the preferred ambient temperature for resting

7 behaviour and thermoneutral temperature (Fig. 6). Resting under thermoneutral condititons is an effective energy saving mechanism. In this way, high-energy costly thermoregulatory heat production is to a large degree not necessary to keep body temperature constant (Tzschentke, 2003; Tzschentke and Nichelmann, 2003). At the 10 th day post-hatching cold experience during the last days until hatching elevated the total neuronal hypothalamic warm-sensitivity through an increased proportion of warm-sensitive neurons and a reduced proportion of cold-sensitive neurons in comparison with the control group. Exposure to the warmer temperature during the prenatal period induced the opposite effect. This change in neuronal hypothalamic thermosensitivity after exposure to various incubation temperatures may be caused through a down or upward shift in the range in which the respective neurons are sensitive to temperature changes. Figure 6 - Preferred ambient temperature (PT) for resting behaviour (R) and thermo-neutral temperature (TNT) in 9 days old turkeys (from Tzschentke & Nichelmann, 2003). Temperature experiences during hatching-time significantly influenced postnatal temperature preference. We carried out experiments in Muscovy ducks and turkey, which were chronically incubated at lower or higher temperatures than usual (37.5 C) during the last days until hatching. Preferred ambient temperature was determined in a temperature gradient tunnel temperated between 10 and 45 C. During this period, every day the chosen ambient temperatures were observed for 9 hours every 10 min (Tzschentke and Nichelmann, 1999). With increasing age Muscovy ducklings incubated at a low temperature (34.5 C) preferred a significant lower temperature than birds incubated at the normal incubation temperature (37.5 C) during the first 10 days post-hatching (Fig. 7). 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-day-old turkeys (Fig. 8) is higher after a prenatal heat load (38.5 C) than in birds incubated under normal temperature (37.5 C). This indicates an elevation of the thermoregulatory set-point after prenatal heat load (Tzschentke and Nichelmann, 1999). These findings were supported by our study on the influence of prenatal temperature experiences on neuronal activity of the thermoregulatory centre in the hypothalamus (Tzschentke and Basta, 2002). Figure 7 - Influence of incubation temperature (34.5 C, 37.5 C) on preferred ambient temperature in 1-, 5- and 10-d-old Muscovy ducklings (n=15 in each experimental group). Figure 8 - Influence of incubation temperature (IT: 38.5 C, 37.5 C) on preferred ambient temperature in 1- to 10-days-old turkeys (n=15 in each experimental group) from Tzschentke and Nichelmann (1997). In the last days until hatching, body temperature of chicken and Muscovy duck embryos was strong influenced by chronic changes in incubation temperature (Fig. 9; Loh et al., 2004). We assume a critical period in the development of the 7

8 normal incubated group (Halle and Tzschentke, 2011). 8 Figure 9 - Temperature of allantoic fluid as measure for embryonic body temperature in warm (ww, 38.5 C), cold (cc, 34.5 C) and normal (nn, 37.5 C) incubated chicken embryos on different days of incubation (* and o are extreme values). For each incubation group, the first letter indicates incubation temperature during the last days until hatching and the second letter refers to the temperature conditions during 1h of measurement (in this experiment similar with the respective incubation temperature) from Loh et al., (2004). thermoregulatory system at the end of the embryonic development. Therefore the lower embryonic temperatures under cold incubation condition and the higher one under warm incubation condition are prerequisites for changes in the thermoregulatory set-point. The above-described changes in the thermoregulatory behaviour were observed during the first 10 days post-hatching. We assume that these changes are persistent, because we found long-lasting changes in different physiological parameters. Heat induced c-fos-expression of hypothalamic neurons, for instance, was significantly different between chronic warm- and cold-incubated chickens even after 8 weeks posthatching (Janke and Tzschentke, 2010). Warm growing conditions (32 C) induce decrease in feed intake and body weight. We found that under this growing condition chronic warm incubated male broiler chicks had a much lower feed consumption than the normal incubated group. Moreover, the final body weight (d 35) in this group was significant lower, too. The stronger reduction of feed intake in chronic warm incubated male chickens lead to a stronger decrease in body heat production, which significantly minimized the warm induced thermal strain of these birds in comparison to the Prenatal temperature training, robustness and behaviour In contrast to chronic warm incubation, short-term warm stimulation ( temperature training ) during hatching time induces different effects on post-hatching performance under standard growing conditions (Tzschentke and Halle, 2009; Halle and Tzschentke, 2011). In comparison to the usual incubation temperature, chronic warm incubation (1 C over standard) had no effects on hatchability and later performance. But, short-term warm stimulation improves hatchability, feed intake, feed conversion, and body weight at slaughter, especially in male broilers (Tzschentke and Halle, 2009). Further, in this study the ratio of hatched female to male chicks shifted in favour of the male chicks. During temperature stimulation the embryos show a decrease in heat production and, finally, a lower embryonic temperature befor hatching compared with the non-stimulated group. The idea is that shortterm temperature training during the last days of embryonic development might improve robustness of the broiler chickens. Thus, changes in behaviour during later life might result. In our first study on the influence of short-term warm stimulation on post-hatching locomotion we found no difference between the warm-stimulated and the normal incubated group. However, this topic is still under investigation. Conclusion For optimal development poultry embryos need environmental stimulation during the last days of incubation. During this time-window physiological mechanisms are well developed. Its further maturation will be improved by environmental inputs, like temperature variations, light-dark cycle, and acoustic signals. Light, for instance is very important for the normal brain development, especially the brain lateralization. Besides improvement of robustness and performance, environmental influences could also have a long lasting influence on post-hatching behaviour. Dark

9 incubated poultry embryos, for instance, show reduced cognitive abilities. Commercial incubation programmes should include environmental stimulation, with temperature and light as the foremost and more silent environment to realize mutual acoustic communication between the embryos. Such conditions are near to the nature and will address also the animal welfare aspect. References BAILY, D.B., BRUER, J.T., SYMONS, F.J. and LICHTMAN, J.W. (2001) Critical thinking about critical periods. P H Brookes Publishing Co. BEKOFF, A. (1992) Neuroethological approaches to the study of motor development in chicks: achievements and challenges. Journal of Neurobiology 23: BEKOFF, A. (2001) Spontaneous embryonic motility: an enduring legacy. International Journal of Developmental Neuroscience 19: BOCK, J., THODE, C., HANNEMANN, O., BRAUN, K. and DARLISON, M.G. (2005) Early socio-emotional experience induces expression of the immediate-early gene ARC/ARG3. 1 (activity-regulated cytoskeletonassociated protein/activity-regulated gene) in learning-relevant brain regions of the newborn chick. Neuroscience 133: BRADLEY, N. (1999) Transformations in embryonic motility in chick: kinematic correlates of type I and II motility at E9 and E12. Journal of Neurophysiology 81: BRUA, R.B. (2002) Parent-offspring interactions. In: DEEMING D.C., (Ed)., Avian incubation: behaviour, environment and evolution. Oxford: University Press: Oxford UK. BRUA, R.B., NUECHTERLEIN, G.L. and BUITRON, D. (1996) Vocal response of eared grebe embryos to egg cooling and egg turning. Auk 113: CHIANDETTI, C. and VALLORTIGARA, G. (2009) Effects of embryonic light stimulation on the ability to discriminate left from right in the domestic chick. Behavioural Brain Research 198: DAISLEY, J.N., MASCALZONI, E., ROSA-SALVA-O., RUGANI, R. and REGOLIN, L. (2009) Lateralization of social cognition in the domestic chicken (Gallus gallus). Philosophical Transactions of the Royal Society Biological Science 364: DHARMARETNAM, M. and ROGERS, L.J. (2005) Hemispheric specialization and dual processing in strongly versus weakly lateralized chicks. Behavioral Brain Research 162: DÖRNER, G. (1974) Environment-dependent brain differentiation and fundamental processes of life. Acta Biologica et Medica Germanica 33: DÖRNER, G. (1975) Perinatal hormone levels and brain organization. Anat. Neuroendocrinology 1: EVANS, R.M. (1989) Egg temperature and parental behavior during the transition from incubation to brooding in the american white pelican. Auk 106: EVANS, R.M. (1990) Vocal regulation of temperature by avian embryos: a laboratory study with pipped eggs of the american white pelican. Animal Behaviour 40: GOTTLIEB, G. (1968) Prenatal behaviour of birds. Quartely Review of Biology 43: GOTTLIEB, G. (1985) Development of species identification in ducklings: XI. Embryonic critical period for speciestypical perception in hatchling. Animal Behaviour 33: HALLE, I. and TZSCHENTKE, B. (2011) Influence of temperature manipulation during the last 4 days of incubation on hatching results, post-hatching performance and adaptability to warm growing conditions in broiler chickens. Poultry Science 48: HAMBURGER, V. and BALABAN, M. (1963) Observation and experiments on spontaneous rhythmical behavior in the chick embryo. Developmental Biology 7: HAMBURGER, V., BALABAN, M., OPPENHEIM, R. and WENGER, E. (1965) Periodic motility of normal and spinal chick embryos between 8 and 17 days of incubation. Journal of Experimental Zoology, 159:1-14. HARSHAW, C. and LICKLITER, R. (2011) Biased embryos: Prenatal experience alters the postnatal malleability of auditory preferences in bobwhite quail. Developmental Psychobiology 53: HARWERTH, R.S., SMITH, E.L., DUNCAN, G.C., CRAWFORD, M.L., and VON NOORDEN, G.K. (1986) Multiple sensitive periods in the development of primate visual system. Science 232: HENSCH, T.K. (2005) Critical period plasticiy in local cortical circuits. Nature Reviews Neuroscience 6: HEPP, G.R., KENNAMER, R.A. and JOHNSON, M.H. (2006) Maternal effects in Wood ducks: incubation temperature influences incubation period and neonate phenotype. Functional Ecology 20: HÖCHEL, J., PIROW, R. and NICHELMANN, M. (2002) Development of heart rate responses to acoustic stimuli in Muscovy duck embryos. Comparative Biochemistry and Physiology A-Physiology 131A: HOGUE, M.E., BEAUGRAND, J.P. and LAGUE, P.C. (1996) Coherent use of information by hen observing their former dominant defeating or being defeated by a stranger. Behavioural Processes 38: HOPKINS, B.C., DURANT, S.E., HEPP, G.R. and HOPKINS, W.A. (2011) Incubation temperature influences locomotor performance in young Wood ducks (Aix sponsa). Journal of Experimental Zoology 315: JANKE, O. and TZSCHENTKE, B. (2010) Long-lasting effect of changes in incubation temperature on heat stress 9

10 10 induced neuronal hypothalamic c-fos expression in chickens. Special Issue: Early development and epigenetic programming of body functions in birds (Ed. Tzschentke, B.). The Open Ornithology Journal 3: JONES, S.M. and JONES, T.A. (1995a) Neural tuning characteristics of auditory primary afferents in the chicken embryo. Hearing Research 82: JONES, S.M. and JONES, T.A. (1995b) The tonotopic map in the embyronic chick cochlea. Hearing Research 82: JONES, T.A., JONES, S.M. and PAGGETT, K.C. (2006) Emergence of Hearing in the Chicken Embryo. Journal Neurophysiology 96: KAUSER, H., ROY, S., PAL, A., SREENIVAS, V., MATHUR, R., WADHWA, S. and JAIN, S. (2011) Prenatal complex rhythmic music sound stimulation facilitates postnatal spatial learning but transiently impairs memory in the domestic chick. Developmental Neuroscience 33: KUO, Z.Y. (1932) Ontogeny of embryonic behavior in aves. III. The structural and environmental factors in embryonic behavior. Journal of Comparative Psychology 13: LAUCH, M. (1989) Prä- und perinatale akustische Kommunikation bei der Moschusente (Cairina moschata). PhD Theses, Humboldt-University: Berlin. LAUCH, M., NICHELMANN, M. and WALLSCHLÄGER, D. (1988) Pränatale akustische Kommunikation bei der Moschusente (Cairina moschata). Mh. Vet. Med. 43: LOH, B., MAIER, I., WINAR, A., JANKE, O. and TZSCHENTKE, B. (2004) Prenatal development of epigenetic adaptation processes in poultry: changes in metabolic and neuronal thermoregulatory mechanisms. Avian and Poultry Biology Reviews 15(3/4): LORENZ, K. (1935) Der Kumpan in der Umwelt des Vogels. Journal fur Ornithologie 83: MANLEY, G.A., KAISER, A., BRIX, J. and GLEICH, O. (1991) Activity patterns of primary auditory-nerve fibres in chickens: development of fundamental properties. Hearing Research 57:1-15. MENCH, J.A. and ANDREW, R.J. (1986) Lateralization of a food search task in the domestic chick. Behavioral and Neural Biology 46: MUCHOW, M., BOSSIS, I. and PORTER, T.E. (2005) Ontogeny of pituitary thyrotrophs and regulation by endogenous thyroid hormone feedback in the chick embryo. Journal of Endocrinology 184: NECHAEVA, M. (2011) Physiological responses to acute changes in temperature and oxygenation in bird and reptile embryos. Respiratory Physiology Neurobiology 178: NECHAEVA, M. and TURPAEV, T.M. (1991) The effect of temperature on the motor activity of the chick embryo and amnion at 5-14 days of development. Zhurnal Evoliutsionnoi Biokhimii i Fiziologii 27: NECHAEVA, M., VLADIMIROVA, I. and ALEXEEVA, T. (2010) Effect of acute hypoxia on the motor activity and heart rate of the 10- and 14-day chick embryo. The Open Ornithology Journal 3: NICHELMANN, M. and TZSCHENTKE, B. (1997) Ontogeny of thermoregulation during the prenatal period in birds. Annals of the New York Academy of Sciences 813: NICHELMANN, M., LANGBEIN, J. and LAUCH, M. (1990) Bedeutung und Mechanismen des perinatalen Verhaltens. Aktuelle Arbeiten zur artgemäßen Tierhaltung KTBL-Schrift 342; Landwirtschaftsverlag Münster-Hiltrup, Germany. NICHELMANN, M., LANGE, B., PIROW, R., LANGBEIN, J. and HERRMANN, S. (1994) Avian thermoregulation during the perinatal period. In: ZEISBERGER, E., SCHÖNBAUM, E. and LOMAX, P. (Eds) Thermal Balance in Health and Disease. Advances in Pharmacological Science, Birkhäuser Verlag, Basel. NICHELMANN, M., HÖCHEL, J. and TZSCHENTKE, B. (1999) Biological rhythms in birds development, insights and perspectives. Comparative Biochemistry and Physiology A-Physiology 124A: OPPENHEIM, R.W. (1966) Amniotic contraction and embryonic motility in the chick embryo. Science 152: OPPENHEIM, R.W. and LEWIN, H.L. (1975) Short-term changes in incubation temperature: behavioural and physiological effects in chick embryo from 6 to 20 days. Developmental Psychobiology 8: PLAGEMANN, A. (2004) Fetal Programming and functional teratogenesis : on epigenetic mechanisms and prevention of perinatally acquired lasting health risks. Journal of Perinatal Medicine 32: ROGERS, L.J. (2011) The two hemispheres of the avian brain: their differing roles in perceptual processing and the expression of behaviour. Journal of Ornithology, DOI /s z. ROGER, L.J. and WORKMAN, L. (1989) Light exposure during incubation affects competitive behaviour in domestic chicks. Applied Animal Behaviour Science 23: ROGER, L.J., ZAPPIA, J.V. and BULLOCK, S.P. (1985) Testosterone and eye-brain asymmetry for copulation in chickens. Experientia 41: ROGER, L.J., MUNRO, U., FREIRE, R., WILTSCHKO, R. and WILTSCHKO, W. (2008) Lateralization response of chicks to magnetic cues. Behavioural Brain Research 186: RUBEL, E.W. and PARKS, T.N. (1988) The organization and development of the avian brain-stem auditory system. In: EDELMAN, G.M., GALL, W.E., COWAN, W.M. (Eds) Auditory function, New York: Wiley. RUMPF, M. and NICHELMANN, M. (1993) Development of prenatal acoustic interaction in the muscovy duck (Cairina moschata). British Poultry Science 34: RUMPF, M. And TZSCHENTKE, B. (2010) Perinatal acoustic communication in birds: why do birds vocalize in the egg? Special Issue: Early development and epigenetic programming of body functions in birds

11 (Ed. Tzschentke, B.). The Open Ornithology Journal 3: SCHMIDT, I. (1984) Interaction of behavioral and autonomic thermoregulation. In: HALES, J.R.S., (Ed) Thermal Physiology, New York: Raven Press. SCHWABL, H. (1996) Maternal testosterone in avian egg enhances postnatal growth. Comparative Biochemistry and Physiology A-Physiology 114A: SCHWABL, H. (1997) Maternal steroid hormones in the egg. In: HARVEY, S., ETCHES, R.J. (Eds) Perspectives in avian endocrinology. Bristol; Society for Endocrinology. TEMBROCK, G. (1978) Wörterbücher der Biologie. Verhaltensbiologie. VEB Gustav Fischer Verlag Jena. TSCHANZ, B. (1968) Die Entstehung der persönlichen Beziehung zwischen Jungvogel und Eltern. Berlin und Hamburg: Paul Parey. TUCULESCU, R.A. and GRISWOLD, J.G. (1983) Prehatching interactions in domestic chicken. Animal Behaviour 31:1-10. TZSCHENTKE, B. (2003) Energy saving mechanisms during the early ontogeny in precocial birds (Minireview). News Biomedical Science 1: TZSCHENTKE, B. (2007) Attainment of thermoregulation as affected by environmental factors. Poultry Science 86: TZSCHENTKE, B. and NICHELMANN, M. (1997) Influence of prenatal and postnatal acclimation on nervous and peripheral thermoregulation. Annals of the New York Academy of Sciences 813: TZSCHENTKE, B. and NICHELMANN, M. (1999) Development of avian thermoregulatory system during the early postnatal period: development of the thermoregulatory set-point. Ornis Fennica 76: TZSCHENTKE, B. and BASTA, D. (2002) Early development of neuronal hypothalamic thermosensitivity in birds: influence of epigenetic temperature adaptation. Comparative Biochemistry and Physiology A-Physiology 131A: TZSCHENTKE, B. and NICHELMANN, M. (2003) Temperature preference in turkeys and other poultry species: importance for keeping during the first days after hatching. In: HAFEZ, H.M. (Ed.), Proceedings 4 th International Symposium on Turkey diseases, Berlin, Verlag der DVG Service GmbH, Giessen. TZSCHENTKE, B. and PLAGEMANN, A. (2006) Imprinting and critical periods in early development. World s Poultry Science Journal 62: TZSCHENTKE, B. and HALLE, I. (2009) Influence of temperature stimulation during the last 4 days of incubation on secondary sex ratio and later performance in male and female broiler chickens. British Poultry Science 50: TZSCHENTKE, B. and RUMPF, M. (2011) Embryonic development of endothermy. Respiratory Physiology & Neurobiology 178: VINCE, M.A. (1964a) Synchronisation of hatching in american bobwhite quail (Colinus virgineanus). Nature 203: VINCE, M.A. (1964b): Social facilitation of hatching in the bobwhite quail. Animal Behaviour 12: VINCE, M.A. (1966a) Potential stimulation produced by avian embryos. Animal Behaviour 14: VINCE, M.A. (1966b) Artificial acceleration of hatching in quail embryos. Animal Behaviour 14: VINCE, M.A. (1968a) Retardation as a factor in the synchronisation of hatching. Animal Behaviour 16: VINCE, M.A. (1968b) Effect of rate of stimulation on hatching in Japanese quail. British Poultry Science 9: VINCE, M.A. (1974) Development of the avian embryo. Part I: Behaviour. In: B.M. FREEMAN, B.M., VINCE, M.A., (Eds) Development of the avian embryo. A behavioural and physiological study, Chapmann and Hall, London. VINCE, M.A. and SALTER, S.H. (1967) Respiration and clicking in quail embryos. Nature 216: VINCE, M.A. and CHENG, R.CH. (1970) The retardation of hatching in Japanese quail. Animal Behaviour 18: VINCE, M.A., OCKLEFORD, E. and READER, M. (1984) The synchronisation of hatching in quail embryos: aspects of development affected by a retarding stimulus. Journal of Experimental Zoology 229: