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-It's known that rooster always crow in the morning sort of as an alarm clock, however roosters crow all throughout the day.
-A rooster's crow can be to show dominance over the hens or other roosters.
- However, crowing can also be due to being startled or scared by something in the environment.
-Roosters often times will also crow after mounting a hen.

The article below was a study done to show how crowing and dominance are related. Their results found that their is a hierarchy of dominance. The most dominant rooster crows first followed by the next in line for dominance and so on.

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Abstract

The "cock-a-doodle-doo" crowing of roosters, which symbolizes the break of dawn in many cultures, is controlled by the circadian clock. When one rooster announces the break of dawn, others in the vicinity immediately follow. Chickens are highly social animals, and they develop a linear and fixed hierarchy in small groups. We found that when chickens were housed in small groups, the top-ranking rooster determined the timing of predawn crowing. Specifically, the top-ranking rooster always started to crow first, followed by its subordinates, in descending order of social rank. When the top-ranking rooster was physically removed from a group, the second-ranking rooster initiated crowing. The presence of a dominant rooster significantly reduced the number of predawn crows in subordinates. However, the number of crows induced by external stimuli was independent of social rank, confirming that subordinates have the ability to crow. Although the timing of subordinates' predawn crowing was strongly dependent on that of the top-ranking rooster, free-running periods of body temperature rhythms differed among individuals, and crowing rhythm did not entrain to a crowing sound stimulus. These results indicate that in a group situation, the top-ranking rooster has priority to announce the break of dawn, and that subordinate roosters are patient enough to wait for the top-ranking rooster's first crow every morning and thus compromise their circadian clock for social reasons.

The crowing of roosters has informed human beings of the coming of morning since the Indus civilization (B.C. 2600-1800), and this sound symbolizes the break of dawn in many cultures. Previously, we showed that the timing of roosters' predawn crowing is regulated by the circadian clock, an internal biological clock with a period about 24 hours. Although external stimuli such as light and crowing by other individuals also induce crowing, the magnitude of this induction is also controlled by the circadian clock. Entrainment is synchronization of a circadian clock to environmental cycles. The ambient light-dark cycle serves as the most effective synchronizer for the circadian clock. However, once organisms are transferred to constant conditions (such as constant darkness), free-running rhythms can be observed. Interestingly, in some species, entrainment of circadian clock to social cues is observed in the absence of other time cues. For example, fruit flies exhibit more coherent group rhythms in constant darkness when housed together than when housed individually. This group synchronization is disrupted by the introduction of arrhythmic flies into the group. Such synchronization may facilitate tight group organization, effective hunting and foraging, and reproduction.

When one rooster breaks the dawn, others in the neighborhood have a higher probability of crowing. Chickens are highly social animals, and crowing is thought to be a means of advertising their territories, thus avoiding the risk of direct aggressive interactions. When the group size is small enough for each bird to recognize the others (generally, less than 10 individuals), chickens develop a linear and fixed hierarchy, also known as the "pecking order". In such groups, the behaviors of each rooster reflect the social hierarchy, and higher-ranking roosters have priority for food, mating, and resources in the pen such as nests and roosting places. Thus, the pecking order forms the basis of social behavior in chickens. Here, we show that the top-ranking rooster also has priority to determine the timing of predawn crowing, and that subordinates are obedient to the top-ranking rooster in a group situation.

Results

The top-ranking rooster announces the break of dawn

Four inbred roosters of the PNP strain were kept in a group cage in order to fix and determine the dominance hierarchy. Roosters were then introduced in groups of four into individual experimental cages in a light- and sound-tight room ( Supplementary Fig. S1a). A total of three groups were examined in each experiment. We analyzed the relationship between crowing behavior and social ranks under a 12-h light:12-h dim light (12L12dimL) condition for 14 days, and then under a constant dim light (dimLL) condition for 14 days. Consistent with the results of a previous study, anticipatory predawn crowing was observed approximately 2 hours (1.83 ± 0.23 h) before light onset under the 12L12dimL condition (). Simple linear and stable hierarchies were observed in all groups. Higher-ranking roosters tended to crow more than lower-ranking roosters under the 12L12dimL condition (). The top-ranking rooster almost always started to crow first every morning (97.6 ± 2.9%; ), followed by lower-ranking roosters in descending order of social rank (). When we looked at temporal changes in the incidence of predawn crowing in detail, subordinates followed the top-ranking rooster within a few tens of seconds (). We also confirmed that lower-ranking roosters crowed less than higher-ranking roosters over this short time scale (i.e., ~100 s) (). Even though the timing of first crowing by the top-ranking rooster varied each day (), the timing of subordinates' first crowing was strongly correlated with that of the top-ranking rooster (). These results suggested that the timing of lower-ranking roosters' crowing is dependent on that of the top-ranking rooster. Consistent results were also observed in free-running subjective predawn crowing under the dimLL condition ( Supplementary Fig. S1b-f).

Second-ranking rooster initiates crowing when the top-ranking rooster is removed

We next examined the effect of physical removal of the top-ranking rooster on subordinates' crowing behavior. When the top-ranking rooster was removed, the second ranking rooster started to crow first (92.7 ± 5.1%; ), and the third- and fourth-ranking roosters immediately followed the second-ranking rooster's crow (). In addition, lower-ranking roosters crowed less frequently (). As in the case of the groups of four (), the timing of first crowing of the second-ranking rooster and its subordinates were strongly correlated ().

Free-running periods of crowing rhythms coincide within a group

Because the timing of subordinates' crowing was closely related to that of the top-ranking rooster, we predicted that the crowing rhythms of subordinates would coincide with that of the top-ranking rooster. Indeed, periodogram analysis of crowing rhythms demonstrated such coincidence within groups (). In addition, when the top-ranking rooster was physically removed from groups, the free-running period of subordinates' crowing was altered (): after the removal of the top-ranking rooster, shortening of free-running rhythms was observed in two groups, and lengthening of the rhythm was observed in one group (). Although the top-ranking rooster always crowed first every morning, these results suggested that the free-running period of the top-ranking rooster is not always the shortest within a group.

All roosters have different free-running periods of body temperature rhythms

We next examined whether the circadian clocks of subordinates are entrained to the top ranking rooster's circadian clock. It is well established that the locomotor activity rhythms of galliform birds (i.e., chicken and quail) are not clear. To address this issue, we examined roosters' body temperature rhythms under dimLL conditions and fitted them to cosine curves. This analysis revealed that the free-running periods of body temperature rhythms differed among individuals kept within the same group (), even though the free-running periods of crowing rhythms appeared to be the same within groups ().

Anticipatory predawn crowing rhythm does not entrain to a timed crowing sound stimulus

Finally, we investigated whether free-running crowing rhythms can entrain to the crowing sound of other individuals under dimLL conditions. Although we observed induction of crowing by sound stimulus, anticipatory predawn crowing did not entrain to the timed sound stimulus ().

Discussion

In this study, we discovered that the highest-ranking rooster crows first every morning, followed by its subordinates in descending order of their social rank (). Although anticipatory predawn crowing was usually observed approximately 2 hours before light onset, the timing of the top-ranking rooster's first predawn crow varied to some extent (). Crowing order, which reflects social rank, is strictly conserved even when the timing of the top-ranking rooster's first crow is advanced or delayed each day (). We also observed that lower-ranking roosters crowed less than higher-ranking roosters (). Previous studies reported that the presence of a dominant rooster suppresses subordinates' crowing. By contrast, when we examined the effect of external stimuli (light stimulus or crowing sound stimulus) on crowing behavior, the percentage of first crowing ( Supplementary Fig. S2a,b) and the number of crows ( Supplementary Fig. S2c,d) were independent of social rank. These results suggested that although lower-ranking roosters do have the potential to crow, predawn crowing by subordinates is repressed by the presence of dominant roosters. This idea is also supported by the experiment in which we removed the top-ranking rooster. In the presence of the top-ranking rooster, the crowing of second ranking rooster was suppressed (). However, once the top-ranking rooster is physically removed from the group, the second-ranking rooster behaves as if he is the top-ranking rooster ().

Because the timing of subordinates' crowing was closely related with that of the top-ranking rooster, it was reasonable to speculate that the crowing rhythms of subordinates were entrained to the crowing rhythm of the top-ranking rooster. Indeed, the free-running periods of subordinates' crowing were coincident with that of the top-ranking rooster under dimLL conditions (). When the top-ranking rooster was removed from groups, the second-ranking rooster took its place, and the free-running periods of the remaining three individuals were altered (). Notably, the lower-ranking rooster sometimes crowed first in this situation (), probably because the second-ranking rooster was not as able as the top-ranking rooster to repress lower-ranking roosters ( Supplementary Fig. S3). We then analyzed the free-running rhythms of body temperature rhythms, but found that they differed among individuals (). In addition, anticipatory predawn crowing did not entrain to the timed sound stimulus of other roosters' crowing (). This result was in marked contrast with the circadian clock of songbirds, which can entrain to a sound stimulus. All of these results suggested that the circadian clocks of subordinates are not entrained to that of the top-ranking rooster, and an identical free-running period observed within a group appeared to be a "masking response", i.e., a direct response to environmental stimuli.

Because the top-ranking rooster always started to crow first each morning (, , Supplementary Fig. S1), it was also reasonable to speculate that the free-running period of the top-ranking rooster is shorter than those of its subordinates, or that the rooster whose free-running period is the shortest would become the highest-ranking rooster. However, both of these hypotheses are unlikely to be true, because the top-ranking rooster did not always have the shortest free-running period (, ). However, interestingly, the top-ranking rooster showed similar free-running period in both crowing and body temperature (), which suggest that top-ranking rooster start crowing on his own timing. On the other hands, although the subordinate rooters also have their own free-running rhythm of body temperature, they appear to keep a pace with the top-ranking rooster. Taken together, the data suggest that subordinate roosters have the potential to crow, but they are patient enough to wait for the top-ranking rooster's first crow.

In summary, in this study, we demonstrated that the highest-ranking rooster has priority to announce the break of dawn, based on his own circadian clock, and that subordinate roosters compromise their clocks for social reason and wait for the top-ranking roosters' first crow every morning.

Methods

Animals and experimental environment

Inbred roosters of the PNP strain were used in this study. Each group consisted of four roosters. These four roosters were kept in four individual cages (44 cm × 39 cm × 74 cm) within a single light- and sound-tight room ( Supplementary Fig. S1a). A total of three groups were examined in each experiment using the same four cages and room. Fully matured 30-week-old roosters that exhibited crowing behavior were used for experiments. The room temperature was set at 20.0 °C. The roosters had ad libitum access to water and feed. Animals were treated in accordance with the guidelines of Nagoya University. All experimental protocols were approved by Nagoya University.

Dominance hierarchy

Four roosters were initially kept in a group cage in order to fix and determine the dominance hierarchy. For focal behavior observation, all roosters were individually marked using colored leg rings. Direct visual observation of aggression was conducted in the daytime. Aggressive behaviors (aggressive pecking, displacing, chasing, and threatening) were recorded, and both winner and loser were noted. From the record of the winners and losers of these aggressive interactions, we calculated the dominance value of individual roosters by using the index of Clutton-Brock (ICB), calculated using the following formula:

Dominant value

where B = number of roosters that an individual beat; Σ b = total number that they beat excluding the subject; L = number of roosters that the individual lost to; Σ l = total number that they lost to excluding the subject. This index takes into account the success of opponents, so that an individual's score is determined by the score of the individuals it dominated and of those that dominated that individual. The formula is especially effective in the case of a linear and fixed hierarchy, such as that of domestic chickens. We also calculated the linearity in each group, using Landau's index of linearity. Normalized index values (h) range from 0 (nonlinear) to 1 (perfectly linear), and h ≥ 0.9 would be a reasonable (although arbitrary) cutoff criterion for 'strong', nearly linear hierarchies. In this study, the mean (± SEM) index value of linearity (h) was 0.97 ± 0.02, confirming that the hierarchies were nearly linear. Therefore, we used the dominance values to identify the rank of each rooster: 7.4 ± 0.6 (1st rank), 2.2 ± 0.2 (2nd rank), 0.6 ± 0.1 (3rd rank), and 0.2 ± 0.0 (4th rank). The dominance values were differed significantly between ranks ( F 3,8 = 137.8, P  < 0.01, ANOVA, Tukey-Kramer's test). Consistent with previous reports, a simple linear hierarchy was observed in this study. After each experiment, we introduced the four roosters back into a group cage and confirmed that the social rank remained the same throughout the experiment by examining the aggressive interactions as described above.

Behavioral observation

Roosters were then introduced into individual experimental cages to record individual crowing behavior ( Supplementary Fig. S1a). This also helped to avoid reduction in the frequency of crowing by lower-ranking roosters due to aggressive pecking. All roosters were kept under 12L12dimL condition for 1 week to allow adaptation before the beginning of each experiment. The lighting was adjusted to give an intensity of 100 lux for regular light and <0.1 lux for dim light at the height of the roosters' heads. The crowing of roosters was recorded all day using an IC recorder (ICD-UX300F, Sony) and an HD recorder (DMR-XP200, Panasonic) connected to a digital video camera (HDR-XR550V, Sony) equipped with a near-infrared illuminator (K-Light, Keiyo Techno). Because roosters exhibit elevation and extension of the head prior to and during crowing, the crowing of each individual rooster could be easily distinguished from the sound and video recordings.

Sound and light stimuli

When we investigated the entrainment to the crowing sound (), 100 dB sound stimuli were given for 3 hours. Using Sound Forge Audio Studio v9.0 (Sony), the sound stimuli of a familiar rooster' crowing were edited as follows: six different crows/min (one crowing/10 sec) × 180 replicates (=3-h sound stimuli). The sound stimuli were presented using a speaker (SRS-T10PC, Sony) placed in front of the cage. To investigate the effect of light stimuli on the order of crowing ( Supplementary Fig. S2a,c), we counted the number of crows during a 30-min exposure to a 100 Lux light stimulus at light-onset. For the effect of sound stimuli ( Supplementary Fig. S2b, d), 100 dB sound stimuli were given for 30 min ³.

Body temperature recording

Body temperature was measured at 15 min interval using a temperature data logger (Thermochron iButtons, Maxim Integrated Products; temperature accuracy: ±0.5 °C), implanted subcutaneously on the neck under anesthesia.

Statistical analysis

Before the statistical tests mentioned below, we confirmed the normal distribution by test for difference of mean. When normality could not be confirmed, the data were arc-sin transformed for proportion data and square-root transformed for count data. One-way ANOVA was used to evaluate the effect of social rank. Significances of differences were evaluated by multiple comparisons using Tukey-Kramer's test. The back-transformed data are shown in the figures. Behavioral sequences of crowing between ranks were analyzed calculating z-scores and testing significance. Correlations between the timing of first crowing and social ranks were determined using Pearson's correlation after time values were transformed into serial values (e.g. 0:00, 12:00, and 24:00 were transformed into 0, 0.5, and 1.0, respectively). Free-running periods of crowing under dimLL conditions were calculated by Lomb-Scargle periodogram analysis using the ClockLab software v2.61 (Actimetrics). Free-running periods of body temperature were calculated by cosine curve fitting using the Prism software v4.03 (GraphPad Software). The number of crowing was counted for 100 sec after first crow.

Additional Information

How to cite this article: Shimmura, T. et al. The highest-ranking rooster has priority to announce the break of dawn. Sci. Rep. 5, 11683; doi: 10.1038/srep11683 (2015).

Supplementary Material
Supplementary Information:
Acknowledgments

PNP strain roosters were provided by the Nagoya University Graduate School of Bioagricultural Sciences Avian Bioscience Research Center through the National Bio-Resource Project (NBRP) of MEXT, Japan. This work was supported in part by JSPS Grant-in-Aid for Research Activity Start-up 25892013 and for Young Scientist (B) 15K18802, and by the Uehara Memorial Foundation. WPI-ITbM is supported by the World Premier International Research Center Initiative (WPI), MEXT, Japan.

Footnotes

Author Contributions T.Y. and T.S. conceived and designed the research. T.S. and S.O. performed the research. T.Y. and T.S. wrote the manuscript.

References

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Wood-Gush D. G. M. The behaviour of the domestic fowl (Nimrod Press, 1971).

Collias N. E. & Collias E. C. Social organization of red jungle fowl, Gallus gallus, population related to evolution theory. Anim. Behav. 51, 1337-1354 (1996).

Menaker M. & Eskin A. Entrainment of circadian rhythms by sound in Passer domesticus. Science 154, 1580-1581 (1966).

Gwinner E. Periodicity of a circadian rhythm in birds by species-specific song cycles (Aves, Fringilli-dae: Carduelis spinus, serinus serinus). Experientia 22, 765-766 (1966).

Tadano R. et al. Molecular characterization reveals genetic uniformity in experimental chicken resources. Exp. Anim. 59, 511-514 (2010).

Clutton-Brock T. H., Albon S. D., Gibson R. M. & Guinness F. E. The logical stag: adaptive aspects of fighting in red deer (Cervus Elaphus L.). Anim. Behav. 27, 211-225 (1979).

Lehner P. N. Handbook of Ethological Methods (Cambridge University Press, 1996).

Quinn G. P. & Keough M. J. Experimental Design and Data Analysis for Biologists (Cambridge University Press, 2002).

Martin P. & Bateson P. Measuring Behaviour: An Introductory Guide (Cambridge University Press, 1993).

Bakeman R. & Gottman J. M. Observing interaction: an introduction to sequential analysis (Cambridge University Press, 1997).

Scott J. L. [et al. The evolutionary origins of ritualized acoustic signals in caterpillars. Nature Communications 1, 4 (2010).PMC free article]

# data[].attributes.attachment_link.title
The highest-ranking rooster has priority to announce the break of dawn

# data[].attributes.attachment_link.description
The "cock-a-doodle-doo" crowing of roosters, which symbolizes the break of dawn in many cultures, is controlled by the circadian clock. When one rooster announces the break of dawn, others in the vicinity immediately follow. Chickens are highly social animals, and they develop a linear and fixed hierarchy in small groups.

# data[].attributes.body
- Mature Male -Rooster or Cock
-Immature male- Cockeral
-Mature female- hen
-Immature female- pullet
-Castrated male-Capon

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-Hens do no need a rooster to produce an egg. Hens can have eggs on their own. However, those eggs are not fertilized and no chicks can come from them. Rooster are great for protecting the flock, fertilizing the eggs, and can even break up the hen fights that come about.
Some people choose not to have rooster because they can be aggressive themselves or can wear out the hens if there aren't enough hens for the rooster. There should be about 8-10 hens per rooster.

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-Many factors effect when she will lay her first egg including hormones, diet, breed, health, temperatures, the stress of the environment, and even lighting conditions.
-On average, the first egg could be laid between 5 and 6 months of age.
-Diet plays a huge part. When the pullet is 18 weeks old, her diet should consist of less protein and more calcium to produce a strong eggshell. If not enough calcium is available in the feed, the calcium will start being extracted from her bones which will be detrimental to her overall health.
-Access to clean water is also very important since eggs are 75% water.
-Egg laying will also happen sooner in a low stress environment.

http://www.the-chicken-chick.com/2013/02/when-will-hen-begin-laying-eggs-what-to.html

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-The hen will crouch low to the ground and show submissive behavior.
-Some females become more dominant in the flock and show more difficulty in being receptive toward males. When this happens, sometimes the over dominant hens will be separated or put into smaller flocks where there are less hens to show dominance over.

https://www.animalbehaviour.net/poultry/

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Behavior that Hen is About to lay her egg

# data[].attributes.subject
Behavior that Hen is About to lay her egg

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-Her comb will get larger and have a more reddish color than normal.
-She may go in and out of nesting boxes if they are present or find a place to nest in general.
-She will start to squat and become more vocal.
-The hen may be more aggressive toward the other hens to exhibit protectiveness.
-The vent will be moist and pink, and the pelvis will be widening.
-She may even lose some feathers because the body is focusing on going into labor.

https://www.mypetchicken.com/backyard-chickens/chicken-help/Are-there-signs-that-a-hen-may-be-laying-H93.aspx

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-Rooster will swing his tail to the side of the hen's tail and spread his feathers.
-This allows for his cloaca to come in contact with the females cloaca and semen is ejaculated directly into the females vagina once the male's rudimentary phallus passes through the female's cloaca.
This mating behavior is specifically referred to as Cloacal Contact. This contact happens for only about 1 second. A rooster will copulate nearly 30 times a day but not all of those copulations will have semen transfer.

(Principles & Applications of Domestic Animal Behavior)
The article below talks about how early experiences can effect development and behaviors later in life.

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Abstract

Early life experiences can be important in determining offspring phenotypes and may influence interaction with the environment and hence health, welfare, and productivity. The prenatal environment of poultry can be divided into the pre-lay environment and the egg storage/incubation environment, both of which can affect offspring outcomes. The ability to separate maternal and egg/incubation effects makes birds well suited to this type of research. There are many factors, including feeding and nutrition, environmental conditions, husbandry practices, housing system, social environment, infectious environment, and maternal health status, that can influence both the health and performance and behavior and cognition of the offspring. There are some aspects of the environments that can be changed to produce beneficial effects in the offspring, like addition of certain additives to feed or short changes in incubation temperatures, while other aspects should be avoided to reduce negative effects, such as unpredictable feeding and lighting regimens. Measures of offspring characteristics may prove to be a useful method of assessing parent stock welfare if known stressors result in predictable offspring outcomes. This has the advantage of assessing the parent environment without interfering with the animals and possibly affecting their responses and could lead to improved welfare for the animals.

INTRODUCTION

The early life (prenatal and neonatal) period has been found to be extremely important in shaping animal phenotypes throughout life. Examples of how variation in experience at the very start of life can impact upon lifetime biology have been seen across a wide range of different animal groups, including mammals, fish, and birds (reviewed by Rutherford et al., 2012). Similarly the human fetal environment has been shown to have lasting effects on offspring phenotype with correlations being found between low birth weight and later ill health (Barker, 2004). For farmed species it is becoming increasingly apparent that the early life environment may be critical in determining how well individual animals cope with their postnatal environment and has consequential effects on farm performance and individual animal health and welfare. In this paper, we will use the definition of welfare that refers to an animal's state in relation to its environment and its ability to cope in that environment. Animals that fail to cope or have difficulty coping in an environment are said to have poor welfare (Broom, 1991). As prenatal experiences determine how well an animal fits with its postnatal environment, prenatal experiences can affect welfare.

In the case of avian species, both pre-lay and egg storage/incubation (referred to subsequently as "incubation") periods can influence the post-hatch development and responses of individual birds. Factors in the prenatal environment have been shown to have lasting effects on how the offspring respond to their environment (reviewed by Lickliter, 2005; Henriksen et al., 2011). It has been demonstrated that in addition to genetic factors a range of maternal and early life environmental factors can influence development, physiology, and behavior of the progeny (e.g. Lickliter, 2005). For example, prenatal exposure to androgens can influence growth and activity levels in the chicks (e.g. Eisling et al., 2006) and incubator-hatched quail chicks respond selectively to the maternal calls of their own species and show attention biases that help lead them to the proximity of their mother (e.g. Heaton et al., 1978). This phenomenon has begun to receive more attention in the past few decades and has led to a variety of studies of the effects of prenatal environment on poultry.

Avian species' prenatal environments differ from that of mammals and can be divided into two phases: pre-lay and incubation. Consequently the maternal environment and the incubation/egg environment can have independent and lasting effects on the offspring (Mousseau and Fox, 1998; Lay and Wilson, 2002; Henriksen et al., 2011). This characteristic makes birds useful in the study of early life environment as influences directly from the mother (e.g. nutrition levels or antibody deposition) and the environment (e.g. temperature, day length) can be separated (Lickliter, 2005). The short generation intervals of some avian species such as chickens and quail also make them ideally suited for research. As a consequence, there are a number of studies designed to manipulate the pre-lay or incubating environment to assess subsequent effects on progeny. Thus the purpose of this paper is to review how stressors applied to the maternal parent and embryo affect the health and welfare of the offspring. There have been studies comparing the genetic contributions of the paternal parent on, e.g. offspring BW (Dottavio et al., 2005) or immunity (Li et al., 2008), but the effects of stressors applied to the sire on offspring outcomes have received little attention and will not be covered here. Due to the disparate nature of literature relating to this topic, and to ensure a transparent and repeatable selection process, a systematic review ( SR) approach was adopted (Arnott et al., 2012).

SR uses scientific review methods to minimize systematic and random errors (Cook et al., 1997) that may occur in a more traditional narrative review where the author may have pre-conceived opinions and biases regarding a topic (Sargeant et al., 2006). Specific search strategies and inclusion criteria are used in SR, eliminating selection bias and subjecting all studies to critical appraisal. Generally, SR uses a quantitative analysis approach, such as meta-analysis. However, as with the Arnott et al. ( 2012) review, this was considered unsuitable due to the broad nature of the review topic, and therefore a systematic, transparent search strategy that could be repeated by others and a protocol to identify suitable studies to include were developed. Once these studies were identified, a narrative approach was used due to the broad review questions that examined many outcomes and a relatively small number of appropriate studies to examine the results and formulate reasonable conclusions.

MATERIALS AND METHODS

Searches

The online database "ISI Web of Knowledge," which searches simultaneously ISI Web of Science (1970 to present), MEDLINE (1950 to present), and BIOSIS Previews (1969 to present), was used to examine the literature. The search terms were combinations of words relating to prenatal and incubation stress. The final search string is given below (asterisks indicate where the electronic database looked for words beginning with stated letters; for example, chicken* was used to find references relating to the words "chicken" and "chickens"):

(prenatal or maternal or perinatal or gestation*) and (stress or program* or nutrition* or effect*) and (poultry or chicken* or chick* or hen or bird* or avian)

Additionally, detailed searches of several relevant journals were conducted (e.g. Applied Animal Behavior Science, Poultry Science, Animal Welfare, British Poultry Science), and any articles deemed relevant but missed in the database search were included. This was all conducted as per the methods described in Arnott et al. ( 2012).

Search Results

The initial search was conducted in Web of Knowledge on 07 Dec 2009, with updates added after a repeated search using similar terms on 09 July 2011 and 16 Oct 2013. After removal of duplicates, the search yielded 3,165 references in both English and non-English languages. The references and any available abstracts were imported into the Reference Manager (Thomson Reuters, New York City, NY) bibliographic database for manipulation and were then classified as outlined below.

Classification of Results

A general overview of the result classifications will be presented here as the procedures and categories have been used in another publication (please refer to Arnott et al. (2012) for a detailed explanation).

Initially the references were screened for relevance and those that were clearly irrelevant or were review articles were removed (2,830 irrelevant papers were removed, leaving 335). The remaining papers were examined in more detail and classified according to whether they contained maternal outcomes only (i.e. with no progeny measures) or whether they investigated aspects of maternal nutrition or applied some form of stressor to the hen prior to ovulation or the egg during incubation and then investigated offspring outcomes. Stressor here refers to any form of non-nutritional challenge with impacts on hen biology.

As an aim of this review was to identify pre-hatch hazards that affect offspring health and welfare, studies were classified according to the early life treatment applied. Early life hazards were classified under the following headings: Feeding Method and Nutrition, Environmental Parameters, Artificial Parameters, Husbandry Parameters, Housing System, Social Environment, Infectious Environment, and Maternal Health Status.

Quality Assessment

A quality assessment of the studies was made as recommended by Sargeant et al., ( 2006), using the following protocol, which was largely adopted from the REFLECT statement (O'Connor et al., 2010). Any studies not meeting these standards were discarded (for full details see Arnott et al., 2012). The criteria used included:

1. Randomization: individuals randomly allocated to treatment groups

2. Treatment intervention: experimental treatment intervention clearly described

3. Control: use of a suitable control group

4. Sample size: use of a sample size of five experimental units or more (as recommended by Festings and Altmann, 2002)

5. Statistical methods: use of appropriate and clear statistical methods

6. Avoidance of data repetition: multiple publications reporting on same data

7. Exclusion of conference abstracts/proceedings

After quality assessment, one reference was identified as a conference proceeding and 5 references failed to pass sample size, statistical methods, and control criteria and were removed. In total, 108 articles proceeded to the final data extraction process of the SR.

RESULTS

Feeding Method and Nutrition

The nutritional status of the mother and of the egg during incubation can affect the health and growth rate of the embryo and in some cases may have lasting effects later in the animal's life (Couch and Ferguson, 1975; McCellan and Novak, 2001).

Effects on Offspring Health and Performance.

The majority of studies conducted in poultry were designed to test the effects of supplementing a basal feed (designed to meet the nutritional requirements of the animal) on offspring performance and health (28 out of 34 papers made up the Feeding Method and Nutrition hazard category, a subset of the total 108 papers). For example, carotenoids are thought to confer many benefits including prevention of some infections (Chew and Park, 2004), regulation of cell proliferation and differentiation (Livny et al., 2002), and enhanced antioxidant capacity (Stahl and Sies, 2003). In hens, carotenoids are deposited into the egg yolk and give the yolk its characteristic yellow-orange color (Surai, 2002) but they also provide other benefits to the chick: Feeding broiler breeders carotenoid-supplemented feed led to an increased concentration of carotenoid in the egg yolks (Karadas et al., 2005), improved hatching rates, and enhanced the antibacterial activity of the egg (Cucco et al., 2007), while the immune response in the hatchlings was significantly improved. (Haq et al., 1996).

Supplementing maternal diets with vitamin E (150 and 450 p.p.m.) 2 wk prior to an immune challenge (2 mL intramuscular injection of Brucella abortus and Freund's incomplete adjuvant in a 1:1 ratio) increased antibody levels in the plasma of chicks at 2 and 7 d of age; however offspring from hens fed 90, 300, and 900 p.p.m. vitamin E did not exhibit any response. This inconsistent relationship between vitamin E and antibody transfer also has been found in other species (Jackson et al., 1978). Additionally, vitamin E, as well as some minerals, can have beneficial effects on reproductive performance. Taiwan native breeder hens given 40 to 120 mg/kg vitamin E and broiler breeders given 0.5 mg/kg Se in their basal diet had increased fertility and hatchability of offspring (Tsai et al., 2008) and decreased embryonic mortality (Pappas et al., 2006). However, some supplements, like high concentrations of vitamin D ₃ (cholecalciferol) (2,500 to 5,000 μg/kg) or added fats (sunflower or fish oil), resulted in decreased fertility and hatchability compared to low (24 μg/kg) or unsupplemented concentrations (Ameenuddin et al., 1986; Pappas et al., 2006; Bozkurt et al., 2008). Similarly high concentrations of Zinc (150 μg/g) in laying hen diets may cause marginal immunosuppression in the chicks but does seem to affect their growth (Stahl et al., 1989).

Vitamin D ₃ given to broiler breeders can, however, improve leg health in the offspring by decreasing the incidence of tibial dyschondroplasia and decreasing rickets scores, while BW and feed intake increase with increasing supplementation (D ₃: up to 4000 IU/kg) (Atencio et al., 2005a, b; Driver et al., 2006). D ₃ supplementation also can lead to faster morphological gut maturity, and, as a result, function in the offspring when the hens are provided 4,000 IU/kg compared to a control diet of 1,000 IU/kg (Ding et al., 2011). Suboptimal nutrition of the hen and/or the developing embryo can also, unsurprisingly, affect the offspring. Malnutrition during incubation (achieved by removing quantities of albumen from the egg) can lead to raised corticosterone levels, brain sparing through the diversion of well oxygenated blood to the brain at the possible expense of other organs (measured by calculating the mean brain to BW ratio), low hatch rates in the chicks (Rodricks et al., 2004), and decreased post-hatch BW up to 7 d of age (Everaert et al., 2013). However, during the laying phase (18 to 55 wk of age) hens hatched from eggs that had partial albumen removal had higher BW than control and sham removal birds, but they also had reduced egg weights, laying rates, and egg mass and an increased number of second-grade eggs (Willems et al., 2013). Restricting Dwarf broiler breeders to 90% of what they would eat ad libitum resulted in decreased egg production, reduced hatchability, and decreased egg and chick weights compared to ad libitum fed birds (Triyuwanta and Nys, 1992); however when these birds were fed ad libitum, they had reduced fertility rates compared to restricted birds (Triyuwanta and Nys, 1990). A more severe feed restriction (or complete feed withdrawal) also can be used in forced molting to "reset" the reproductive system of birds and results in heavier eggs with better hatchability than the eggs being produced before the molt (Tona et al., 2002), although there is hen mortality and decreased immune function associated with this procedure (Patwardhan and King, 2011).

Effects on Offspring Behavior and Cognition.

Maternal nutrition can affect the behavior and cognition of the offspring. For example, laying partridges fed feed supplemented with higher concentrations of n-3 fatty acids (4.40 g/kg) had chicks that performed better in a memory retention task at one d of age than chicks from hens receiving a lower concentration of n-3 fatty acid (0.48 g/kg) (Fronte et al., 2008). Also, the method of feeding itself can have effects on the offspring. Laying hens that were exposed to an unpredictable food restriction schedule had chicks with longer tonic immobility durations, which is thought to be an indicator of fear, than ad libitum fed birds (Janczak et al., 2007a).

Thus there is good evidence that additional supplementation of the hen's feed above the recommended NRC standards with some vitamins or minerals can result in improved growth, development, and/or learning in the offspring. Restricting nutrients has mixed results on the offspring-hatched chicks may be smaller than those of ad libitum fed birds but free feeding of some strains, like broiler breeders, can lead to decreased fertility and hatchability. In addition, there are still a number of unresolved welfare issues surrounding feed restriction of parent stocks (see Decuypere et al., 2010).

Environmental Parameters

There are a number of environmental or climatic parameters that could affect the offspring, including the pre-lay environment of the hen and the environment that the embryo is exposed to between ovulation and hatching.

Effects on Offspring Health and Performance.

Incubation temperature or fluctuations in temperature can have both positive and negative influences on the hatched chicks. For example, increasing the incubation temperature from 37.8 to 39.5°C and the RH from 56 to 65% for 3 h a d during the second wk of incubation (d 8 to 10) increased chick hatchability compared to standard environmental parameters or periodically increasing the temperature and RH during the last wk of incubation (d 16 to 18) (Collin et al., 2007). Eggs exposed for short periods of time (3 h) to increased temperature (to 39.5 or 41°C) later in incubation still had chicks with increased hatchability compared to standard incubation parameters (Yahav et al., 2004). Periodic exposure to cold temperatures (30 min on d 18 and 2 30-min sessions on d 19 of incubation) was also beneficial, resulting in chicks hatching with higher BW than those not exposed to cold stress (Shinder et al., 2009). Embryos that were cooled for 6 h/d from d 15 to 18 also had enhanced thyroxine response to the thyrotrophin releasing hormone, which may help the chick cope with later stressors (Decuypere et al., 1988). However longer exposure to relative extremes of temperature (e.g. temperature reductions to 36.9 to 38°C for 6 h/d for the first 8 d of incubation) led to reductions in hatchability or chicks with decreased BW (Byerly, 1938 in Oppenheim and Levin, 1975; Yalcin and Siegel, 2003). Reduced temperatures (36.7°C) early in incubation also led to broiler chicks with reduced relative shank and femur weight and chicks with more leg problems than those incubated at standard temperatures (Oviedo-Rondon et al., 2009). Additionally, longer exposure to higher temperatures (38.9°C from d 7 of incubation onwards) led to chicks with 26% lower heart weights at hatch and higher overall levels of mortality and ascites-related mortalities (4.1 and 3.8% higher, respectively) than chicks from eggs incubated at the standard temperature of 37.8°C (Molenaar et al., 2011a). It is important to note that some of the temperatures referred to above are invariably the so-called set temperature (the temperature to which the incubator thermostat is set). Early on in incubation, the set temperature and embryo temperature will be similar if not identical; however, once past the mid-time point of incubation, metabolic heat output increases dramatically, meaning that the temperature experienced by the embryo is invariably greater than the set (or air) temperature. This does not alter, however, that there is an interaction between the age of the embryo, the duration of exposure, and the temperature to which the embryo is exposed, with the optimum conditions varying depending on the parameter selected.

In addition to incubation temperatures, the temperatures that the hens are housed at also influences offspring characteristics. Hens kept during wk 22 to 27 of life under standard thermal conditions (21°C) or warmer but within the thermotolerance range conditions (31°C) had similar laying rates. However, the hens raised in warmer temperatures had lighter eggs and higher concentrations of yolk progesterone, testosterone, and estradiol, and chicks hatched from these eggs had higher morphological quality scores (based on measures described in Tona et al., 2003) that varied from zero (very bad) to 40 (very good) and made fewer distress calls when exposed to a novel food. These findings may indicate a beneficial adaptive response as maternal environment can result in different offspring phenotypes that may be more suited to particular environmental conditions (Bertin et al., 2013).

Factors such as the age of the parent flock will affect the offspring. Generally younger birds have smaller eggs that result in lighter offspring, chick weights in poultry species typically being approximately 70% of the total egg weight. For example, broiler chicks hatched from young parents (27 or 32 wk of age) had lower BW than chicks hatched from older parents (57, 42, or 65 wk old) (Nelson et al., 1992; Yalcin et al., 2008), and quail chicks from younger parents (11 wk of age) were lighter than chicks from older parents (37 wk of age) at hatch (Guibert et al., 2012). Additionally, eggs from younger (24 wk of age) hens had higher yolk levels of antibody Immunoglobulin Y ( IgY) than birds from 36- and 82-week-old hens (Barua et al., 2000), which may have implications for disease control programs. However, broiler breeders just coming into lay (about 23 wk old) had lower egg fertility and hatchability and higher embryo mortality, indicating that there is a lower limit to the benefits of incubating eggs from young-parent birds (Pappas et al., 2006).

Egg storage times before incubation also can have effects on the subsequent offspring. Fertilized eggs are typically stored for approximately 7 d before being incubated. Eggs stored for longer periods (18 d before incubation) had delayed hatching and an increase in triiodothyronine ( T3) most likely due to higher concentrations of corticosterone between internal pipping and hatching and which may indicate a more stressful hatching event compared to embryos hatching from eggs stored for 3 d (Tona et al., 2003). Embryos stressed due to hypoxia (O ₂ decreased below physiological concentrations) and anoxia (total depletion of O ₂) also resulted in increased plasma corticosterone levels in newly hatched chicks and had an increased number of adverse conditions such as a delay in righting response (Rodricks et al., 2008), impaired development of thermogenesis (Azzam et al., 2007), and lower BW for up to 10 d post-hatch (Camm et al., 2001) compared to embryos that did not experience hypoxia during incubation. Chicks exposed to high O ₂ levels (25%) during d 9 to 19 of incubation also had decreased residual yolk weight at hatch and higher yolk-free weights and longer chick body lengths than chicks incubated with lower (21%) O ₂ concentrations (Lourens et al., 2007). Yolk-free body mass at d 18 of incubation was also higher with higher O ₂ levels, although differences between high and normal O ₂ concentration treatments disappeared by 48 h after hatch (Molenaar et al., 2011b). Fertile eggs exposed for 24 h to 6% CO ₂ and either 10 or 20% O ₂ during the first 10 d of incubation had increased cardiac and non-cardiac malformations, such as thickening of the inter-atrial septum demonstrating that increased CO ₂ levels can be teratogenic; however, newly hatched chicks were also 10% heavier than in the control groups (Haring et al., 1970).

Exposure to environmental toxins, which would be more prevalent among wild or farmed birds with access to range, or which could contaminate crops that are made into feeds for farmed animals, usually had negative effects in the offspring. 2,3.7,8-tetrachlorodibenzo-p-dioxin ( TCDD) is a toxin known to cause, among other symptoms, wasting syndrome, carcinogenicity, and immunotoxicity (Poland and Knutson, 1982). It can get into the environment through combustion and incineration and chemical and biological processes. Poultry were used as a model for wild turkeys to determine the risks of exposure. Chicks from eggs injected with the toxin showed suppressed B-cell proliferation and catalytic enzyme production (Peden-Adams et al., 1998). One-time exposure of Japanese quail embryos to dichlorodiphenyldichloroethylene ( DDE) resulted in female offspring with accelerated puberty onset and male offspring with reduced reproductive performance (e.g. mount attempts); however, reproductive physiology in adults appeared to be unaffected (Quinn et al., 2008). This means there may be immune and neurological risks for the offspring of wild or farmed birds that come into contact with the external environment or that are fed contaminated feedstuffs, especially if exposure occurs when young.

Effects on Offspring Behavior and Cognition.

Increasing incubation temperature also can have positive behavioral effects: Chicks from eggs exposed to 24 h of 40.6°C incubating temperature on d 16 showed less aggressive pecking to conspecifics at 21 wk of age than those from eggs incubated under standard conditions, although it is not clear exactly what the mechanism behind this difference in behavior was (Lay and Wilson, 2002). However, chicks from eggs exposed to hypoxic conditions (24 h of 14% O ₂) on d 10 or d 14 of incubation had impaired short-term memory but this was not consolidated into long-term memory impairment (Gibbs et al., 2009). Additionally, chicks from eggs that were incubated with decreased O ₂ levels during d 10 to 14 were less successful in an avoidance discrimination task (exposed to 2 different color beads: one had an aversive taste; the other did not) than birds hatched from control eggs (Rodricks et al., 2004), and chicks from eggs partially wrapped in a membrane during incubation also had reduced success in an object avoidance test 60 and 120 min after being taught the task (Camm et al., 2001).

Offspring from eggs exposed to 2 h of pulsing bright lights (750 to 1,000 lux) on d 18 of incubation, feather pecked more on d 7, 14, and 21 after hatch (Riedstra and Groothuis, 2004). The authors hypothesized that this was due to light exposure influencing lateralization of the brain, thereby decreasing the ability of the birds to discriminate between familiar and unfamiliar birds whom they would "explore" by pecking. Conversely, embryos incubated with a 12L:12D light schedule had better retention of a passive avoidance and discrimination task after hatch compared to dark-incubated only chicks (Sui and Rose, 1997). Occasional exposure to sounds in the incubation environment (15 min/h from d 10 to hatching), using both natural, species-specific noises and artificial noises (sitar music) increased hippocampal function (Chaudhury et al., 2009), which may facilitate learning and memory, and influenced postnatal auditory preferences (Jain et al., 2004); however, only high-decibel music (110 dB) positively modulated spatial orientation, learning, and memory when compared with noise (non-patterned or rhythmic) of the same decibel levels (Sanyal et al., 2013). Maternal age also can influence offspring characteristics: Chicks from 37-week-old Japanese quail were less reactive when encountering a novel environment, but they were more stressed by social isolation than chicks from 11-week-old quail (Guibert et al., 2012).

Stress also can affect the offspring through inherited epigenetic modifications and this process may have been favored by domestication: White Leghorn and Red Junglefowl hens undergoing stress in the form of unpredictable light:dark rhythms showed decreased ability to perform a spatial learning task; however, this effect was greater in the White Leghorn hens. These White Leghorns also had offspring with reduced spatial learning abilities that were more competitive and that grew faster than offspring from non-stressed hens, whereas offspring from the Red Junglefowl hens exposed to the same stressors did not exhibit this reduction in spatial learning (Lindqvist et al., 2007).

Thus, small environmental manipulations, such as short increases or decreases in incubation temperature can have beneficial effects on the offspring while young to middle-aged parent flocks tend to have more successful offspring than very young or old parent flocks. Irrespective of the age of the parent bird, storage times that exceed 7 d (e.g. 18 vs. 7 d storage), varied lighting schedules, restricted gas exchange across the egg shell, and exposure to toxins may lead to detrimental effects on the offspring and should be avoided when possible.

Artificial Parameters

Artificially manipulating the concentration of stress hormones in the individual or their offspring can give an insight into the potential effects of any related stressor.

Effects on Offspring Health and Performance.

Corticosterone is the most frequently studied stress hormone in poultry but other hormones (such as noradrenaline) or lines of birds selected for low or high stress levels are also studied. For example, quail selected for high plasma corticosterone laid eggs with higher yolk corticosterone (Hayward et al., 2005) and had lower egg fertility (Schmidt et al., 2009b) than birds selected for low plasma corticosterone. The offspring from "high stress" quail had greater size differences between their left and right tibia and middle toe lengths, indicating that developmental instabilities like increased stress can lead to greater fluctuating asymmetry in the offspring (Satterlee et al., 2008). Raised corticosterone levels in hens (achieved by corticosterone implants or injections) also decreased growth rates and increased mortality in their chicks compared to hens with non-functional implants or injected with saline (Hayward and Wingfield, 2004; Hayward et al., 2006; Satterlee et al., 2007; Wall and Cockram, 2010), and eggs with increased corticosterone, e.g. from corticosterone injections, led to increased mortality and decreased BW in the chicks for up to 77 d post-hatch (Eriksen et al., 2003; Janczak et al., 2006, 2007b). Quail subjected to corticosterone injections in ovo showed higher corticosterone concentrations when stressed at 64 d of age by being placed individually in an opaque box than quail subjected to sham injections or post-natal corticosterone injections, demonstrating the potentially longer-lasting effects of early stressors (Marasco et al., 2012). Corticosterone also can be raised by subjecting the birds to unpredictable stressors. Japanese quail hens were exposed to mild stressors (unpredictability in the environment and sudden movements) 3 times a d for 24 consecutive d and compared with hens in which no stressors were applied. Stressed hens had heavier eggs, contained more albumen, hatched earlier, and were heavier at hatching than non-stressed hens' eggs (Guibert et al., 2011). Even the physiology of the parent birds can affect corticosterone levels in the offspring, with chicks hatched from a standard heavy broiler breeder line having higher corticosterone levels than an experimental lighter broiler breeder line (Tona et al., 2004).

Other hormones affect offspring development as well. So, for example, quail eggs injected with testosterone had a lower hatchability and cell mediated immunity than eggs not injected or injected with the carrier only (Daisley et al., 2005; Cucco et al., 2008), although these offspring did have higher growth rates (Cucco et al., 2008). However the negative effects of testosterone supplementation were found to be reduced when chicks were supplemented with carotenoids in their feed (Cucco et al., 2008). Additionally, eggs injected with noradrenaline to increase the basal concentration produced chicks with raised levels of circulating corticosterone (Gibbs et al., 2009).

Effects on Offspring Behavior and Cognition.

Early exposure to stress hormones can affect fear behavior. Hens selected for "low stress" had offspring that took longer to induce tonic immobility ( TI: an indicator of stress or fear, Davis, 2008), and chicks from eggs injected with testosterone had longer TI durations than chicks from eggs that weren't injected with testosterone during incubation (Okuliarova et al., 2007). Eggs injected with corticosterone before incubation resulted in: chicks that had higher latencies in a human-approach test and fewer chicks that would cross a barrier to reach food (Janczak et al., 2006); chicks that had raised basal plasma corticosterone during a beak-trimming stress test (Lay and Wilson, 2002; Rodricks et al., 2006); and chicks that performed more aggressive pecking to their conspecifics (Lay and Wilson, 2002). Chicks from quail exposed to unpredictable mild stressors, such as sudden movements or noises, had higher reactivity when introduced to a novel environment and they reacted more strongly to social isolation (Guibert et al., 2011). However, quail chicks from eggs injected with testosterone had reduced numbers of total calls and a greater latency to call in open field tests, took less time and had a shorter latency to approach novel objects, and had lower fecal corticosterone after a 90-min isolation test than offspring from control eggs (Daisley et al., 2005). Male quail injected with testosterone in ovo showed increased food competitiveness and had a more female-like phenotype than sham treated males, suggesting that maternal androgens interact with sexual differentiation of the brain and behavior and development of secondary sex characteristics (Riedstra et al., 2013).

Corticosterone injections in eggs also influenced learning ability, with chicks from eggs injected with larger doses (0.3 nmol/egg) performing worse in an object discrimination task than those injected with very small doses (0.01 nmol/egg) (Rodricks et al., 2006). Quail chicks injected with noradrenaline and exposed to a maternal call during incubation did not show a preference for the call while chicks exposed only to the call during incubation did (Markham et al., 2006). Similarly, chicks injected with corticosterone during incubation and exposed to an imprinting stimulus (another chick) did not prefer the stimulus, while the control chicks did (Nordgreen et al., 2006).

Thus, there is good evidence indicating that early life exposure to increased stress levels can have a later effect on chick mortality, development, stress sensitivity, and behavior, and this has implications for the management of captive breeder birds and potentially also wild birds. Although stress levels were raised artificially in these studies, other aspects of the production environment can lead to increased stress levels (e.g. Parsons, 1990) and this could affect production and bird welfare.

Husbandry Parameters

There was only a small sample of studies that examined the effects of husbandry procedures on the offspring.

Effects on Offspring Health and Performance.

One study involved the practice of forced molting, a method still practiced in many countries like the United States but is illegal in the United Kingdom and can involve withdrawing food completely from the hens until they have ceased laying for a few d resulting in a wk or more without food (Patwardhan and King, 2011). This practice is stressful for the hens and leads to increased concentrations of antibodies, such as levels of IgY, in the yolks of their eggs for at least 10 d after the hens begin to re-lay, which could have beneficial effects for the early immune function of fertilized eggs (Barua et al., 2001). Even non-invasive procedures such as habituating quail to humans by increased exposure to humans, gentle handling, and food rewards and then exposing habituated and non-habituated quail to human disturbances had significant effects. Eggs had more yolk, lighter shells, increased progesterone, and decreased androgen levels, and the chicks hatched earlier and weighed more than non-habituated quail eggs (Bertin et al., 2008).

Effects on Offspring Behavior and Cognition.

Chicks from quail habituated to humans had a greater fear response as measured by tonic immobility tests (reduced number of inductions) and showed more fear behavior when exposed to the experimenter and a novel environment. It was postulated that the habituation process may have been stressful for the hens and may have led to higher stress hormone levels being transferred to the eggs (Bertin et al., 2008). There were also social effects of the habituation treatments as offspring from non-habituated quail spent less time near conspecifics and males showed less crowing and courtship behavior toward females than offspring from habituated quail (Bertin et al., 2009).

The egg quality and social and sexual changes in the offspring have implications not only for birds hatched in production systems but also when interacting with wild species during conservation efforts.

Other Parameters

Other parameters, such as social environment, housing conditions, and the infectious environment and maternal health status may influence factors in the offspring.

Effects on Offspring Health and Performance.

Dominant hens allocate more testosterone to male eggs than female eggs, while subordinate hens allocate more testosterone to female eggs (Muller et al., 2002). Housing environment also can influence the hormones allocated to eggs. Hens housed in floor pens laid eggs with yolks higher in androstenedione and estradiol while caged hens had eggs with higher concentrations of estradiol in the albumen (Janczak et al., 2009).

Vaccination of the hens before they begin to lay can lead to long-lasting maternal antibodies being passed into the egg and offspring. For example, pre-lay hens vaccinated against Salmonella led to long-lasting Salmonella-specific antibodies found in the egg yolk as Immunoglobulin G (I gG) and in the offspring as IgG in the serum and IgA in the intestinal fluid. Chicks from vaccinated hens also had higher antibody response when orally infected with Salmonella strains than non-vaccinated hen offspring (Hassan and Curtis, 1996). Vaccinating adult birds and the use of chicks from vaccinated hens are helping to control and reduce infections in the birds from bacteria that can be found in a production environment.

Effects on Offspring Behavior and Cognition.

Maternal androgens increase competitiveness in the nestling and aggression and growth rate in the juvenile (Schwabl, 1993, 1996; Eising et al., 2001). These hormones may be a way for the hen to signal the state of the environment to her offspring and subsequently affect their development and phenotype. Also, prenatal sensory experience has a role in the lateralized postnatal visual discrimination in birds. During the hatching process, the chick embryo has its left eye blocked by its body and yolk sac but the right eye is exposed to light coming through the shell, leading to a 90% left side turning bias found in domestic chicks (Rogers, 1991). However, when both eyes are prenatally exposed to light or when the left eye is exposed and the right eye is blocked from light, the turning bias disappears, while birds who experimentally had their right eyes exposed and left eyes blocked from light prenatally still maintained the turning bias (Casey and Karpinski, 1999). Thus treatment of incubating and hatching eggs can have long lasting effects on the brain and behavior of avian offspring.

DISCUSSION

There are numerous factors that can have an influence on the hen and the incubating egg that will result in lasting effects on the phenotype of the offspring. These can range from the supplements provided in the feed (e.g. Atencio et al., 2005a, b) or even the amount of feed provided (e.g. Triyuwanta and Nys, 1992), the temperature and relative humidity during incubation (e.g. Collin et al., 2007), to age of the parent flock (e.g. Yalcin et al., 2008), levels of stress hormones in the hen (e.g. Schmidt et al., 2009a, b), habituation of the parents to humans (e.g. Bertin et al., 2009) to the dominance status of the hen (e.g. Muller et al., 2002). Some factors can result in benefits to the offspring, such as supplementing vitamin D ₃ in broiler breeder feed (Driver et al., 2006) while others may have detrimental effects, such as stress in the parents, leading to a reduction in memory and learning in the offspring (Rodricks et al., 2006).

The presence of some factors, like exposure to environmental toxins (e.g. Quinn et al., 2008), is unlikely to occur in current commercial poultry production where the birds are housed, although the trend to move towards extensive systems has the potential to increase the risks (Schoeters and Hoogenboom, 2006). However there is a risk that farmed poultry may be fed feed made with crops exposed to environmental toxins (van Barneveld, 1999). Other factors, like restricted feeding in broiler breeders, are standard practice (e.g. Triyuwanta and Nys, 1992). The most prevalent result of the different hazards found in production systems is likely to be increased stress leading to increased concentrations of circulating corticosterone. Increased stress could be caused by parasitic infections, pathologies, feed deprivation, social stress, exposure to novelty, and noise and behavioral restrictions (e.g. Parsons, 1990), meaning that the standard housing of poultry could be contributing to raised corticosterone levels compared to less intensively reared or wild fowl. This increased stress could lead to offspring with decreased weights, increased mortality, learning impairments, and increased stress sensitivity (e.g. Hayward and Wingfield, 2004). However more research is needed to determine how stressful current systems are in terms of, for example, elevated concentrations of corticosterone. Flock age is an ongoing concern in poultry production, as breeder birds may be placed in systems pre-lay and continue producing for well over a yr. Older flocks have chicks with higher BW, but they also have higher chick mortality (Yalcin et al., 2008) and lower yolk antibodies (Barua et al., 2000), which can have implications for the total number of viable offspring produced. Some deleterious effects are commonly encountered, such as reduced porosity in eggs from young breeding birds, whereas stressors such as bright pulsing lights during incubation would occur only in accident or emergency situations and should not present a regular problem for poultry welfare.

However, some hazards, like periods of increased or decreased temperatures during incubation, can be beneficial and may more closely mimic a hen brooding a clutch of eggs who takes breaks from sitting (White and Kinney, 1974). Supplementing poultry feed is a relatively easy way to provide additional protection to the offspring, e.g. vitamin D ₃ given to broiler breeders resulted in chicks with better leg health (Atencio et al., 2005a, b) but dosages should be monitored to prevent any negative effects, e.g. high levels of zinc being supplemented to hens acted as a mild immunosuppressant in the chicks (Stahl et al., 1989), although it should be noted that the studies examining these effects have been fairly small-scale experimental trials to date. On-farm studies would be useful to confirm that the same positive effects occur on a much larger scale and that changing the factors, such as incubation temperatures, is practically and economically feasible.

In terms of poultry welfare measures, offspring condition could reflect the suitability of the parent environment. For example, it has been suggested that fluctuating asymmetry in chicks be used as a proxy measure for chronic stress in the hens as asymmetries increase with increased stress (Satterlee et al., 2000). So hens in one environment producing chicks with larger asymmetries than hens from another environment may be more stressed and have poorer welfare. The differences in the 2 environments can then be compared to attempt to improve conditions for the more stressed hens. Other measures such as comparing chick mortality, growth rate, leg conditions, etc., from hens being housed and managed in different ways could also be used to assess suitability of the hen environment. Using offspring to assess parent environment has the advantage that the animals in the environment under question are not interfered with; however, more research and validation studies using this method compared to other generally accepted welfare measures are needed before offspring measures become a widespread parent welfare measurement.

In conclusion, the maternal environment includes many factors such as feeding method and nutrition, environmental parameters, artificial challenges, husbandry, housing system, social environment, infectious environment, and maternal health status, and these all can influence the development, physiology, and behavior of the offspring. As the conditions we keep commercial poultry in are quite artificial compared to their wild ancestors, they have the potential to be stressful, which could negatively affect the offspring. The literature strongly suggests that maternal conditions prior to lay, or conditions during incubation could have important effects on poultry health, welfare, and productivity. Consideration of how potential negative prenatal effects can be avoided may benefit poultry production. Additionally, we also have the potential to provide factors to the hen that will benefit the offspring and help improve their welfare. Using the offspring to help assess suitability of parent environment is a promising welfare assessment tool but it requires further study and validation against current welfare measures before becoming a widespread method.

The authors thank the UK Department for the Environment, Food and Rural Affairs (Defra, Project AW0509: Early environment effects on animal welfare, health, and productivity) for its support of this work. SRUC receives grant-in-aid from the Scottish Government. Thanks to Gareth Arnott for conducting the initial literature searches.

REFERENCES

Maternal Effects and Adaptations

Natural antioxidants in avian nutrition and reproduction

Nottingham University Press

# data[].attributes.attachment_link.title
Early experiences matter: a review of the effects of prenatal environment on offspring characteristics in poultry | Poultry Science | Oxford Academic

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Early life experiences can be important in determining offspring phenotypes and may influence interaction with the environment and hence health, welfare, and productivity. The prenatal environment of poultry can be divided into the pre-lay environment and the egg storage/incubation environment, both of which can affect offspring outcomes.

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-Hens only have one functioning ovary, usually the left ovary.
-The oviduct is connected to the ovary and functions to produce albumin (egg white), the shell membrane, and shell around the yolk.
-The uterus houses the egg while it is finishing development and also determines the color of the shell.
-The vagina releases the egg and regulates the timing of egg production.
-The egg also passes through the cloaca.
-Hens also have a vent which is an exterior opening where the digestive, reproductive, and urinary tracts all meet.

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-The rooster's testes are located inside the body.
-The ductus deferens, also known as vas deferens connects the testes to the phallus and is the tube that transports semen.
-Roosters do not have a penis. The rudimentary phallus is a projection that acts as a penis in poultry.
-Cloaca- structure located at the end of the digestive tract that will release feces and urine. This is present in birds, amphibians, and reptiles.

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The Rooster begins with a "wing drag." This is where he drags his wing on the ground to fan out his feathers so the female can see the size of them and all the colors. The Rooster will also raise the feathers on his neck for added effect. The Rooster also adds a dance where he circles around the front of the female and around to the back where he gets ready for mounting. Sometimes the wing drag and dance are left out and the rooster goes directly to mounting. Once the rooster mounts the female, he latches onto her comb, neck feathers, and skin on the back of the hen's neck as a way of holding on while mounting. Once the rooster is secured on the female, the last behavior involves the rooster slightly moving his feet back and forth on the hen's back.