Director of Poultry Research and Nutrition
North American Nutrition Companies, Inc.
Lewisburg, OH
U.S.A.
Artificial insemination in turkeys has long been obligatory. The method is practiced around the world and continues to make significant contributions to the genetic improvement of turkeys. A basic understanding of the physiology and anatomy of the female reproductive tract is essential to fully capitalize on this technique. High, persistent levels of fertility can be obtained as long as close attention is paid to such key factors as initial insemination, semen dose, timing of inseminations, and insemination intervals.
Avian follicular development involves a complex coordination of neuroendocrine, physiological and metabolic factors that are integrated by seasonal changes in day length. Maximum egg production is not achieved because too many follicles are being recruited early in lay while recruitment is deficient late in lay. A key objective is to modulate ovarian function and follicular development to create well established, clearly delineated follicular hierarchies.
Incubation behavior is one of the most costly management challenges in turkey breeding. It is induced by interactions of the environment and the endocrine system and is evident in all genotypes. Numerous management strategies have evolved to alleviate these detrimental effects that are otherwise, in nature, representative of a normal physiological state in turkeys.
Light is a very powerful management tool. As such, it integrates environmental cues that ultimately are translated and processed into hormonal signals that change reproduction, metabolism and behavior. Year-around production is only feasible when birds are relived of photo refractoriness before being exposed to long stimulatory days. Light stimulation, however, triggers a bimodal response. While it initiates reproductive activity it is, simultaneously, also responsible for the gradual cessation of egg production.
For the interested reader, the current paper aims to discuss some of the basic underlying physiological, endocrine, metabolic and anatomical principles in regards to the aforementioned topics. An effort is made to relate these scientific principles back to practical, field-type conditions, recommendations and/or solutions.
I. ARTIFICIAL INSEMINATION
Introduction
Artificial insemination (AI) in avian species was first conducted and documented by a Russian scientist named Ivanov (Jefferey, 1955). Although initial research utilized almost extensively the domestic chicken, the commercial exploitation in this species up to date has been very limited (Van Wambeke and Huyghebaert, 1989). In contrast, AI is obligatory in today's modern turkey breeding industry (Lake, 1994; Bakst, 1994) and is practiced on nearly all commercial turkey breeder farms throughout the world (Bakst, 1989). A cornerstone in AI technology constituted the development of a practical method for semen collection in turkeys that can be applied to chickens as well (Burrows and Quinn, 1937). As a result, geneticists continued to emphasize selection for growth and conformation in male line stock that also dramatically improved growth rate and white meat yield in commercial turkeys (Krueger, 1988). However, this development occurred at the expense of reproductive efficiency. Numerous negative correlations between fertility traits and growth characteristics have been documented (Krueger, 1990; Hammerstedt and Shultz, 1994).
Review of literature
Sperm storage tubules
Once semen is deposited into a hen's oviduct, sperm gradually disappears from the lumen of the oviduct (Compton et al., 1978) and it is accommodated in what is referred to as sperm storage tubules (SST). Historically, SST were first discovered by a Danish scientist named Tauber in 1875 and much later rediscovered as "sperm nests" by Van Drimmeln (1946). The SST are located in a 2 to 3 cm wide band between the posterior portion of the uterus and the anterior region of the vagina (Brillard and Bakst, 1990), an area commonly referred to as the uterovaginal junction (UVJ). The UVJ is the primary sperm storage site in avian species and it is the anatomical unit responsible for the prolonged storage of spermatozoa in birds (Christensen and Bagley, 1989). Sperm storage tubules are important in poultry because they eliminate the need for synchronization of copulation with ovulation that is essential to most mammalian species. Furthermore, they reduce the number of inseminations needed to obtain fertile eggs over one or more clutches. Sperm storage tubules provide the anatomical basis for sperm competition. Lastly, they protect or harbor the sperm from the descending effects of the daily ovulatory cycle (Bakst, 2001). Histological preparations have shown that SST are essentially blind-ended tubular glands that arise as invaginations of the uterovaginal mucosa (Zavaleta and Ogasawara, 1987). The glands are nonciliated, mostly unbranched tubules, approximately 70 um in diameter, and as deep as 250 um (Bakst, 1994). The SST are not true glands. Contrary to previous assumptions, histological evidence suggests that they have little secretory capacity (Bakst, 2001). A secondary sperm storage site has been localized between the posterior fallopian region of the infundibulum and the anterior portion of the magnum (Zavaleta and Ogasawara, 1987; Bakst, 1994). It is in this area where fertilization takes place.
More than eighty percent of all spermatozoa administrated during a regular insemination are already flushed out from the oviduct within 30 min after insemination (Howarth 1971), and only about 1 to 5% of the sperm cells in a single insemination dose of 150 million spermatozoa will eventually reside in the SST (Christensen, 1990; Brillard, 1993). Thus, sperm loss is considerable.
Practical implication
The UVJ is the primary sperm storage site. Although there is an abundance of SST, the vast majority of all sperm is flushed out after an insemination. The existence of SST allow sperm to be available whenever the hen decides to ovulate ultimately facilitating today's AI schedules.
Sperm competition
A sperm selection process takes place at the level of the SST in the UVJ (Ogasawara et al., 1966; Bakst, 1989). Fifty to 70% of the poults from hens inseminated with pooled semen from 12 to 15 males can be traced back to have originated from one or two toms (Bakst, 2001). Dead or "non-fit" spermatozoa are more prone to fail to enter the SST and less likely to traverse the oviduct to the site of fertilization than "fit" spermatozoa implying that sperm integrity and motility are essential to reach the primary storage sites (Brillard, 1993). Van Krey et al. (1966) deposited large quantities of spermatozoa directly into the magnum bypassing the uterovaginal SST. Fertility was high but so was early embryonic mortality. A direct cause-effect relationship could, however, not be established since a large number of spermatozoa surrounding the ova at the time of fertilization could have led to polyspermy, a known mortal factor in early embryonic development (Zavaleta and Ogasawara, 1987). For turkeys in production the maximum filling capacity of the SST is reached 2 days following insemination. Sperm cells can reside in the SST as long as 8 to 15 wks in turkeys (Brillard, 1993). It is assumed that spermatozoa sequestered within the SST are metabolically quiescent. They exhibit greatly reduced motility and their plasma lemma and the acrosomal membranes are stabilized (Bakst, 2001). The mechanism responsible for the release of spermatozoa from the SST is still poorly understood and presumptive and includes theories suggesting a passive escape of sperm while the hen is still in lay to a squeezing of sperm out of the SST as the egg mass descends through the UVJ (Bakst, 2001). Most recent data suggests that there may be also a neural mechanism involved since nerve innervations have been identified (Freedman et al., 2001). The precise underlying mechanism still needs to be elucidated.
Practical implication
It is of utmost importance to insure that those breeder toms that are selected to sire progeny are proven to be the heaviest birds with good conformation and walking ability. Only a very small number of all the breeder toms will provide the paternity for the fast majority of the hatched poults. Perhaps, future management strategies should consider whether or not toms should be selected on the basis of their fertilizing capacity.
Initial inseminations and semen dose
Among naturally mating turkeys the female initiates the mating process (Margolf et al., 1947). This behavioral response is known as squatting and indicates the hen's receptivity to be mated (Siopes, 1995). It is most intense shortly before laying commences (Smyth and Leighton 1953; Carte and Leighton, 1969) and affects the fertility of hatching eggs. If AI is performed in hens before egg production is initiated (days 14 and 17 post photo stimulation) then fertility is significantly improved over breeders that are already in production due to increases in the rate at which the SST are activated and filled with spermatozoa (McIntyre et al., 1982, McIntyre and Christensen, 1983; 1985; Bakst, 1993). A similar mechanism appears to be involved in the determination of the optimum number of spermatozoa needed for weekly consecutive inseminations. For example, McIntyre et al. (1986) used 20, 50, or 100 million sperm cells/insemination on a weekly basis and overall fertility was improved with every increment in sperm numbers per insemination. Commercial industry standards for concentration of sperm range, on average, between 200 to 240 million sperm cells per insemination throughout the production cycle.
Practical implication
The first insemination should take place before hens initiate egg production. Hens with intact membranes on the oviduct should not be inseminated. These turkeys should be released and inseminated during the second round of inseminations. Good synchronization of a flock's reproductive state cannot be achieved without placing strong emphasis on good flock uniformity. Low semen dosages cause marginal filling rates that translate into poor fertility and persistency.
Timing of AI and insemination interval
The presence of a hard-shelled egg in the uterus of the hen constitutes a physical barrier to the migratory sperm and, therefore, AI should not take place around the time of oviposition. Significantly better fertilities are obtained when the AI is performed either early in the morning or late at night (Christensen and Johnston, 1977; Brillard, 1993). The need to investigate the effect of insemination interval on fertility is derived from the fact that the rate of sperm release from the SST in old hens is about twice as much as that observed in young hens (Brillard, 1993). High levels of fertility could only be sustained by progressively increasing semen quantities throughout the later part of the breeding season (Christensen and Bagley, 1989; Krueger, 1990). Furthermore, inseminations on a weekly basis yielded higher levels of fertility than biweekly inseminations (Meyer et al., 1980; McIntyre and Christensen, 1985; Christensen, 1990) although egg production was better in some cases when hens were inseminated every other week (Meyer et al, 1980). Some flocks are inseminated on a biweekly basis through ten weeks of production followed by weekly insemination thereafter or are "doubled-up" between the 12th and 15th week of production (Krueger, 1990). It appears therefore, that the age related decline in fertility is not only due to a reduced capacity of the SST to accommodate sperm, but also due to an increased rate of sperm release and the failure of the SST to sequester spermatozoa not as effectively anymore as during the early parts of the laying cycle (Brillard, 1993).
Practical implication
Inseminations should either be performed early in the morning or late in the evening. The number of hens per insemination crew should be chosen in such a manner to accommodate for these circumstances. Increases in sperm concentration will help to sustain good fertility rates in older breeder flocks.
Concluding remarks
Management approaches alone cannot alleviate all of the detrimental effects of genetic selection in breeders. Management for "fitness" of spermatozoa in conjunction with proper executed AI will be very important to obtain high and persistent levels of fertility. Specific attention must be given to selection of toms since only very few toms sire the majority of the progeny. Timely initial inseminations and carefully adjusted semen doses provide the basis for good fertility rates.
II. FOLLICULAR DEVELOPMENT
Introduction
Generally, avian reproduction involves a rather complex coordination of neuroendocrine, physiological, and nutritional factors that are integrated by seasonal changes in day length. However, over the years, unidirectional selection for growth has pushed an intrinsically functional and relatively efficient reproductive system out of balance.
Today, meat-type poultry production is associated with poor reproductive capacity (Siegel and Dunnington, 1985). Genetic inheritance, which favors rapid protein anabolism, also favors rapid formation and deposition of an ovarian follicular precursor called lipoprotein (Jaap 1969). Increased synthesis of this hepatic precursor leads to an increase in number and size of ovarian follicles in broiler breeders (Van Middelkoop, 1971; Zelenka et al., 1986a; Yu et al., 1992b), turkeys (Nestor et al., 1970; 1980), and ducks (Hocking, 1990). As a result, double hierarchies with pairs of two or more follicles of similar size develop, culminating in multiple ovulations, erratic ovipositions, and defective eggs (Hocking et al., 1987; Decuypere et al., 1994).
A major constraint in understanding the underlying mechanism is a lack of knowledge as to how the "normal" form and function of the hypothalamic-pituitary-gondola axis can be influenced by body weight, body composition, feed intake and the interactions among them in order to successfully regulate and modulate ovarian function and follicular development.
Review of literature
Puberty and ovarian follicular function
Reproductive activity commences with the onset of puberty. While the classical "gonadostat" hypothesis is based on the existence of a negative feedback mechanism (estradiol), the "open loop" theory suggests instead an age dependent central inhibition of the GnRH pulse-generator (Ramirez and McCann, 1963; Plant, 1994).
The timing of sexual maturity is influenced by BW and age at photostimulation (Brody et al., 1980; Dunnington and Siegel, 1984), body fat content (Bornstein et al., 1984), rate of food intake (Kennedy and Mitra (1963), growth rate (Glass et al., 1976), lean tissue mass (Soller et al., 1984), absolute quantity of breast tissue mass (Zelenka et al., 1986b) as well as interactions among these factors (Foster and Rayan, 1979). The minimum day length required to stimulate gonadotropin release in chickens and turkeys is between 10-12 h (Sharp, 1989). Delaying the onset of sexual maturity by delaying photostimulation improves reproductive efficiency. Eggs that are laid have better shells, are usually larger, and the birds show a better persistency in production (Hocking, 1992a,b).
Practical implication
One of the main objectives of rearing and "black-out" is to delay the onset of sexual maturation, to synchronize the reproductive state of the birds in a flock, and to dissipate the effects of juvenile photorefractoriness. Photoperiods prior to "black-out" should be kept at or below 12 h a day after the initial brooding phase.
Photoperiodic-neuroendocrine control of reproduction
The eye and the pineal gland are not essential in birds in the transduction of photoperiodic cues to stimulate gonadal development (Sharp, 1993). In fact, chickens (Wilson and Woodward, 1958) and turkeys (Siopes, 1991) will eventually lay eggs even when kept in complete darkness assuming that they were correctly photosensitized. Instead, it is believed that extra-retinal photoreceptors are imbedded in the encephalic region of the brain (Kuenzel, 1993). They provide inputs to the biological clock (suprachiasmatic nucleus), which is essential for the establishment of a circadian rhythm (Moore, 1983) that divides a 24 h day into a light and dark phase. GnRH neuronal cell bodies originate in the hypothalamus and have projections ending in the median eminence where they, upon stimulation, discharge FSH/LH-RF (Sharp, 1993). A relative increase in the ratio of facilitatory over inhibitory hypothalamic inputs on GnRH neuronal terminals is essential for the genesis of a preovulatory LH surge (Contijoch et al., 1992). The ratio appears to be modulated by the steroid environment of the bird (Wilson and Sharp, 1976) and decreases during the egg producing life of the hen.
Only long days are photoperiodically active and transduce both stimulatory and inhibitory inputs to the GnRH neurons. This principle is generally referred to as the "second clock" which shuts off the neuro-endocrine control mechanism (Sharp, 1993). Furthermore, stress-related inputs, like feed restriction (intentional or accidental), can cause an increase in dopaminergic inhibitory inputs on LHRH terminals resulting in ovulatory failure (Advis and Contijoch, 1993). Prolonged exposure to long days is associated with decreased pituitary responsiveness to GnRH, decreased pituitary LH content, decreased plasma LH concentration, and decreased egg production, which, taken together, result in photorefractoriness (Sharp, 1993). Photorefractoriness refers to the bird's loss of sensitivity to respond to stimulatory light.
The turkey industry uses "black-out" programs to expose birds to short photoperiods in order to regain this sensitivity. It is important to have an appreciation of the photoperiodic-neuroendocrine control in birds because it is a dynamic - not a static system - that undergoes changes in sensitivity as the animal progresses through the reproductive season and/or laying cycle.
Practical implication
Light stimulation (transfer to long photo schedules) not only activates the mechanism for commencement of reproductive activity it also, concurrently, triggers the gradual cessation of it. Upper limits for photostimulation need to be chosen carefully. The duration of the photophase is inversely related to the onset of photorefractoriness.
Follicular maturation and recruitment into hierarchy
According to Johnston (1993), ovarian follicles can be classified into at least four stages of development; these include small white resting (months or years) follicles (< 2 mm), the slow-growing white follicles (2 to 6 mm), the stage of recruitment into the follicular hierarchy (small, yellow), and the final differentiation (large, yellow). The exact physiological mechanism(s) that regulate growth and order of the ovarian hierarchy is not well understood. The endocrine control involves hormones from the hypothalamus and the pituitary (Etches, 1990), as well as the coordinated function of several physiological compartments within the ovary as described in the classical two-cell model for ovarian steroidogenesis (Tilly et al., 1990; Johnson, 1990). The follicles of the chicken and turkey ovary proliferate very little during the first 15 weeks of life (Etches, 1990). The minimum day length required to stimulate gonadotropin release in chickens and turkeys is between 10 to 12 h (Sharp, 1989). Ovarian growth and function are mediated by a rise in plasma LH and FSH concentrations within 2 to 3 days post photostimulation (El Halawani et al., 1984). As follicles mature, they grow from less than 1 mm to approximately 35 mm in diameter (Etches, 1990). The average ovary of a commercial layer has a hierarchy consisting of 6 to 8 large follicles (Zakaria et al., 1984). Nine and 12.4 follicles, respectively have been counted in dwarf versus normal broiler breeders ( Hocking, 1987). Usually, follicles require 11-13 days to grow from an eight mm follicle to an ovulable mature size (Bacon and Cherms, 1968; Hocking et al, 1988b) but this increases with age (Bacon and Cherms, 1968).
Recruitment of follicles into the hierarchy occurs preferentially at the level of the white-yolky stage by a process of differential atresia (Gilbert and Wells, 1984; Hocking et al., 1988a). In this content, genetic comparisons of lines selected for growth or feed conversion indicate that selection for improved feed conversion (leanness) reduces incidence of atresia and maintains a larger population of small white follicles available for subsequent recruitment (Hocking and Whitehead, 1990). Conversely, increased rates of atresia and a decreased recruitment in follicular numbers (Palmer and Bahr, 1992) as well as slowed follicular maturation per-se, and shortening of the duration of the "open period" (Robinson et al., 1990), have been associated with the decreased ovulation rates observed in aging hens. Considering the fact that forced molted hens have initially a higher ovulation rate than first cycle hens at the end of their production cycle complicate the picture even further. One could speculate and, perhaps, relate it back to a function of follicular maturation rates and longer open periods and revitalized sensitivity to the action of GnRH. Nonetheless, follicles that are recruited into the hierarchy are destined to ovulate (Etches, 1990). Atresia at this point in development is rare but can be induced by metabolic disorders like starvation (Gilbert et al., 1983). Thus, the ovarian follicular hierarchy is already established before the follicles are filled with yellow yolk.
Practical implication
Control over follicular recruitment and maturation in breeders is very important. To achieve this, early maturation of the hypothalamus in the brain needs to be delayed. This is accomplished practically by placing hens on short days. A clear understanding of the underlying physiological and endocrine mechanisms is required to successfully design and optimize lighting programs.
Mechanisms controlling the ovulatory cycle
The ovulatory cycle in birds is basically controlled by two asynchronous and independent systems. The first system refers to the ability of the large follicles to acquire a functional steroidogenic system (Robinson et al., 1993). The second factor is the "open period" for LH release (as mentioned earlier) which constrains the release of gonadotropins to an approximately 8 to 10 h period within the photophase each day. While FSH concentrations peak 16 to 14 h before ovulation, maximum LH concentrations are reached 7 to 4 h before an ovum is released (Kawashima et al., 1992b). Progesterone is produced by the vascular granulosa cells in all of the five largest preovulatory follicles. However, under normal physiological conditions, only the largest preovulatory F-1 follicle secretes progesterone into the systemic circulation (Johnson et al., 1988). The remaining lower ranking follicles utilize progesterone as an intermediate for the synthesis of androstenedione (Etches, 1990; Yu et al., 1992a). The increased plasma progesterone secretion of the F-1 follicle acts as a positive feedback stimulation on the hypothalamus, which responds with an increased GnRH secretion into the hypothalamic pituitary portal system. At the pituitary, GnRH binds to receptors and enhances LH secretion, which augments the progesterone production in the F-1 follicle thereby completing the positive feedback loop (Etches, 1990). The pituitary binding capacity for GnRH is significantly greater in laying than nonlaying hens. Furthermore, the induction of the receptors is enhanced by the presence of the ovarian steroids (Kawashima et al., 1992a ).
Practical implication
The mechanism controlling the ovulatory cycle consists of a complex hormonal system that is superseded by the effects of the photoperiod again emphasizing the importance of light in breeders.
The oviposition/ovulation sequence
As mentioned before, the occurrence of oviposition and subsequent ovulation for the next egg in the domestic hen, duck, quail, and turkey is normally restricted to an 8 to 10 h "open period" that is part of a regular 24 h light/dark cycle (Fraps, 1955; Morris, 1973). The timing and the regulation of the open period is entrained principally by the dusk signal (the longest dark period) of the previous scotophase (Sharp et al.,1981; Wilson and Cunningham, 1984). Uterine contractions at the time of oviposition are induced by prostaglandins (Hester and Newlon, 1991). Regardless of photoschedule, oviposition precedes ovulation for the next egg in a sequence by approximately 0.5 to 1.0 h (Etches, 1990; Bakst, 2001). When ovulation does not fall into the open period, the hen will delay ovulation until the next morning and "skip" laying an egg for that particular day. The occurrence increases with the length of the laying cycle and is most noticeable in older hens.
Practical implication
The fact that turkey hens skip laying an egg is a result of normal physiological and endocrine constraints. The frequency increases as rate of follicular maturation and duration of the open period decrease with increased length of egg production.
Concluding remarks
A more precise understanding of the factors involved in ovarian follicular function would certainly aid in improving the poor reproductive efficiency in turkeys. There are essentially two areas of concern. These relate to early production and late production. While loss in egg production arises due to too many follicles early in lay there is no sufficient recruitment and maturation of large follicles late in lay to sustain egg production at high rates.
III. INCUBATION BEHAVIOR
Introduction
Turkey breeder hens have a natural propensity towards early cessation of egg laying. This is due to the hen's intrinsic desire to incubate a clutch of eggs to ensure survival of the species (El Halawani and Rozenboim, 1993). The term "incubation" describes the behavior and the physiological state associated with the maternal care of the unhatched egg. Incubation behavior (IB) is not unique to turkeys. It persists also to various degrees in broiler breeders (dwarf-gene) and ducks but not in White Leghorns.
The expression of IB, or broodiness, remains a significant source of economic loss for the turkey industry (Guemene, 1992) due to a potentially substantial loss in egg production and increased labor cost for identification and treatment of broody hens. Studies conducted under commercial conditions have indicated that daily, on average, more than one percent of the hens in a flock became broody throughout the laying cycle (Guemene and Etches, 1990).
Review of literature
Behavioral, morphological and metabolic adaptations associated with incubation behavior
According to Guemene (1992) for hens with access to a nest, initiation of IB manifests itself by a progressive increase in frequency and duration of nest visits. Initially, nest visits increase during the night first if the hen is allowed to do so because prolactin levels are highest at the end of the scotophase (Proudmann, 1998). Subsequently, increased nest visits will then take place during both, the scoto- and photophase. At the end of this intermediate period, the incubating hen will spent more than 90% of her time on the nest. If approached, the hen exhibits some characteristics of defensive nest behavior. She gathers and moves around the eggs, emits a characteristic vocalization (hissing) and she may ruffle her feathers (Guemene, 1992). Feed and water intake are greatly reduced (Bedecarrate et al., 1997). Hens displaying IB are known to undergo substantial weight losses of up to 30%. The mobilized tissue reserves are used as energy sources to sustain metabolic and physiological functions. If untreated, a regression of the entire reproductive tract is common. Birds in littered floor pens either housed individually or collectively have significantly higher prolactin levels than turkeys housed in cages. The highest prolactin levels have been measured in collective floor pens (Bedecarrate et al., 1997). One should mention, however, that a "normal" degree of nesting/ incubation behavior is highly desirable. It begins just before an egg is laid and enables the bird to anticipate the forthcoming event and to be at her chosen nest site rather than laying eggs randomly on the floor (Sharp, 1997).
Physiology of incubation behavior
The development of IB is induced by interactions between the environment, genotype and the endocrine system (Sharp, 1997). There is a gradual progression in the intensity of nesting behavior in turkeys after photostimulation for a few weeks (Proudmann, 1998). On a comparative basis, wild turkeys become broody after laying a clutch of nearly 20 eggs (Guemene, 1992). Commercial turkeys appear to have moderately high base-line levels of prolactin and get broody just after peak egg production which is at approximately three to four weeks of lay (Nixey, 1978.) If no action is taken, broodiness reaches a second maximum between the eighth and tenth week of lay and may persist throughout the remainder of the laying cycle (Guemene, 1990). Even when treated, the same birds often become broody two or more times at intervals of 3 to 4 weeks (Nixey, 1978).
A significant factor in the induction of incubation behavior is tactile stimulation via the brood patch on the ventral abdominal area of the bird (Guemene, 1992). The brood patch is highly vascularized and blood flow is greatly increased during incubation. Furthermore, vasodilatation and vasoconstriction constitute physiological means to main temperatures in well- defined parameters suitable to promote embryonic development (Brummermann and Reinertsen, 1992). A stimulus may originate from sitting on eggs or merely through the exposure to a littered floor (Sharp, 1997). If the nerves supplying the brood patch are cut, broodiness will not develop (Brook et al., 1991). Tactile stimulation from the brood patch appears to stimulate prolactin secretion since removal of a broody hen from its nest or transfer into a cage results in an immediate and rapid decrease in plasma prolactin levels (El Halawani et al., 1980).
Endocrine control of incubation behavior
The neuroendocrine mechanism controlling broodiness is not completely understood (El Halawani et al., 2000). Nesting behavior and exposure to long daily photostimulation of as little as one day stimulate prolactin secretion (Bedecarrats et al., 1997). The secretion of prolactin from the anterior pituitary gland is controlled by the prolactin releasing hormone produced in the median eminence of the hypothalamus and is released into the portal blood system (El Halawani et al., 1997). The releasing factor has been identified as vasoactive intestinal polypeptide (VIP), a 28 amino acid neuropeptide first isolated from the gut, (Sharp et al., 1989). Base-line prolactin levels increase gradually beginning at about 10 d prior to the onset of IB. Concurrently, luteinizing hormone and progesterone levels decline during the same period (Proudmann, 1998). Egg production generally remains high during this period and nesting frequency increases sharply just prior to oviposition of the last egg. Immunization against VIP suppresses prolactin secretion and inhibits the development of broodiness while maintaining high levels of egg production (Sharp, 1997; El Halawani et al., 2000). Once broodiness is established it no longer depends on the presence of estrogens and progesterone, and is maintained by the high levels of prolactin in the blood (Zadworny and Etches, 1987). High levels of circulating prolactin suppress secretion of gonadotropins, which are directly responsible for the regression of the ovary, the decrease in plasma ovarian steroids and, ultimately, cessation of egg production (Sharp, 1997). Good layers have moderate base-line prolactin levels throughout egg production. A daily rhythm for prolactin secretion has been reported suggesting highest levels to be observed at the end of the scotophase (Proudmann, 1998).
Prevention and treatment of incubation behavior at the flock level
All known management procedures to prevent and treat IB and to improve egg production to date are based on lowering baseline prolactin levels (El Halawani et al., 2000). The technique most widely used involves moving potentially incubating hens from its familiar pen or barn section to different surrounds (barn rotation) or a less comfortable area (broody pen) without nests (Nestor et al., 1986). All strategies must aim at removing eggs from the nest and/or floor as frequently as possible (Sharp, 1997) without promoting floor laying. This technique eliminates tactile information from the brood patch (Brook et al., 1991) thereby resulting in an immediate and rapid decrease in circulating prolactin levels. Implementation of uniform lighting systems will discourage nesting in dim corners. High barn temperatures, slow and insufficient ventilation rates, inappropriate flock densities relative to housing design, ventilation capacity and time of year need to be avoided (Nixey, 1973; El Halawani et al., 1983). Manual and automatic egg collection systems must be fully operational, closed at night, and sufficient for the number of birds housed. There must be an appreciation for the physiological and environmental factors that have been shown to influence expression of IB (Guemene, 1992). Specifically, the existence of a threshold of environmental stimuli in conjunction with a threshold for a physiological state within the hen needs to be thoroughly understood, clearly communicated with employees, and carefully considered if the aim is prevention of IB. Training of employees in correctly recognizing incubation behavior is not easy, yet a critical priority. Presently, there is no good, reliable tool to forecast IB in a field situation other than depending on the "eye of the farm manager". Some computerized systems in conjunction with mechanical nests can help detect nesting frequency.
Either indirect selection against IB or direct selection for improved egg production is part of most primary breeders genetics program. This has resulted in slow but significant improvements over time (Nestor et al., 1980; Sharp, 1997).
Considerations for designing and managing a broody pen
If persistent nesting behavior is identified at an early stage, the development of full broody behavior can be prevented without serious loss of egg production by transferring birds to a "broody pen" for three to six days (Sharp, 1997). Despite lowered levels of prolactin, readiness to incubate persists for another two to three days after nest deprivation. (El Halawani, 1980). Therefore, broody treatments must be carried out long enough to be effective.
Housing broody turkeys on raised wired floors has been reported many times to be very effective. Obviously, in today's large-scale turkey industry this does not prove to be practical and economically viable. Nonetheless, the objective of the broody pen design is not to just make it uncomfortable for the hen. The objective is to prevent the hen from sitting down as much as possible (lowering prolactin) and to keep her surrounding environment fairly cool (lowering prolactin). Bright continued lighting for the first 24 h supports the objective of lowering prolactin and stimulates the release of gonadotropins. The birds should not be crowded in the broody pen. "Huddling" and/or grouping of birds in the barn and in the broody pen should be avoided (lowering prolactin). Fresh feed and water should be provided at all times. Broody treatments that stress the birds excessively will terminate reproductive activity.
Concluding remarks
Incubation behavior is still a common occurrence in turkey breeder hens. Yet highly undesirable from an economic perspective, it is still normal from an evolutionary and physiological point of view. Expression of IB is influenced by genotype, environmental factors, and the endocrine state of the hen as well as interactions thereof. Correct identification of IB is a very difficult task. All remedial strategies need to aim at lowering prolactin levels.
IV. PRINCIPLES OF LIGHTING
Introduction
Light, natural or supplemental, has three principle effects on birds. Firstly, it is the medium of illumination that makes sight possible. This is achieved by conversion of images that have been formed on the retina to complex electrical signals that are transmitted via the optic nerve to the brain. Secondly, patterns of "light" and "darkness" reach various extra retinal photoreceptors in the brain and provide the bird with information on day length and/or seasonal changes. Thirdly, patterns of light energy that reach the hypothalamic region of the brain, either via the optic nerve or directly through the skull and tissue, control the secretion of gonadotropins (Lewis and Morris, 2000), which in turn stimulate the pituitary gland to release luteinizing and follicle stimulating hormone (LH and FSH).
In commercial poultry production periods of light and dark are usually combined in either a conventional, intermittent, or in an ahemeral lighting schedule. The most common photoschedule in turkeys is a conventional light regime consisting of a single scotophase (dark) and a single photophase (light) within a 24 h daylength (Etches, 1996).
Review of literature
Physiology of light and lighting programs
Changes in daylength influence the activity of the reproductive hormones (gonadotropins) by a neural pathway that does not directly involve the eyes. These changes in daylength are detected by extraretinal photoreceptors (Sharp, 1989). Since brain tissues are penetrated about 30 times faster by red (~ 650 nm wavelength) than by green (~ 500 nm) light (Lewis and Morris, 2000) it is not surprising that turkeys can be more readily stimulated into reproductive activity with the longer wavelengths of the visible spectrum (Jones et al., 1982). The amount of light a turkey requires for inducing egg production as well as maximum photostimulation for superior overall egg production cannot be defined without reference to the spectrum of the light source (Sharp, 1989).
Siopes (1984) compared the proportion of light energy in the red spectrum (600-700 nm) in incandescent and full-spectrum fluorescent lamps and found it to be 43 and 27%, respectively. As a consequence, birds exposed to 76 lux of incandescent or full spectrum fluorescent light, received a net exposure of 20.8 and 8.3 lux of red light. It is of utmost importance to realize that most colored lamps despite producing one visible color and, therefore, believed to be monochromatic, have often times broad spectrum emissions. (Lewis and Morris, 2000).
Effects of long days during the growing period on subsequent egg production are remarkably persistent and suggest that longer periods of short-day treatments are necessary to ensure complete dissipation of juvenile photorefractory (Sharp, 1989). Conversely, it has long been known that the time required for photorefractoriness to develop is inversely related to the duration of the daily photophase (Sharp, 1983). Recently, Siopes (2002) suggested that not only stimulatory long days are required but also the presence of thyroid hormones shortly before and after photostimulation for initiation and maintenance of photorefractoriness. Thyroxine (T4) seemed to play a greater role than triiodothyronine (T3). The critical minimum daylength required to induce egg production is 10 to 12 h per day (Siopes, 1998). This may vary somewhat by strain of turkey and, certainly, by lighting history of the same birds during black-out (Sharp, 1989). The critical minimum daylength required to induce photorefractory is 12 h regardless of season (Siopes, 1998). The absolute degree of darkness required during light restriction (black-out) to effectively terminate photorefractoriness and to reestablish photosensitivity in turkey hens is less than 0.5 lux. (Siopes, 1991). Although the eye has been shown not to be essential for a photosexual response, it may still be the primary site of light reception at low intensities and, as a consequence, be relevant in poultry houses where low illuminance is frequently used to control an undesirable bird behavior ( Lewis and Morris, 2000).
Production facilities using light restrictions at higher light intensities (intentional or accidental) are commonly referred to as "brown-out" complexes. This management strategy can have significant repercussions on subsequent levels of egg production for "out of season" breeder candidates.
Design and execution of lighting regimes
Interestingly, according to Etches (1996) the choice and design of lighting regimes should be determined based upon the prevailing barn conditions at hand. It is generally accepted that light proof facilities allow better control over reproductive development than do curtain-sided facilities. Conversely, not all light controlled facilities are equally effective in preventing light from entering into a facility. A carefully implemented lighting program specifies light source, duration, distribution and light intensity. The light intensity of the photophase should be at least ten times more than the light intensity of the scotophase. If the ratio between photo- and scotophase is less than ten, some hens in a flock will perceive the lighting program as if they were exposed to continuous illumination (Etches, 1996).
For verification of exact implementation of a lighting program, the use of a light meter placed at bird level is mandatory. Obtained readings will have to be adjusted for the type of light source being used. Variables such as cleanliness of light bulbs, dust build-up, new light leaks, etc. may lower light intensity and negatively alter the ratio between photo- and scotophase over time (Hybrid Turkeys, 2002). The first hour of darkness should always be given at the same time to allow the birds to anticipate the transition from "lights on" to "lights off". As a fundamental physiological rule in an effort to optimize reproductive capacity, a short, non-stimulatory lighting regime should be given throughout rearing (Etches, 1996). "Stepping down" lighting programs help to overcome the adverse effects of light leaks and minimize the occurrence of premature squatting. Additions in supplemental light must always be given in the morning only. As birds are stimulated for commencement of egg laying, empirical data suggests that the frequency of vaginal prolapse is reduced when "step-up" lighting programs are used. Extensions of the photoperiod by 15 min per week until an 18 h photophase is reached may delay the onset of photorefractoriness and may help improving egg production during the later part of the egg laying cycle (Etches, 1996). Once photostimulated, daylength must never be decreased in order to sustain a continuous release of reproductive hormones.
The performance of a lighting program in general, as well as the consistency of the responses during lay between flocks over time, is influenced by the quality and consistency of the light management during rearing and black-out (Investment Phase). The importance of photoperiodic history is readily recognized when it comes to designing lighting programs for open-sided houses or houses with poor light control.
Lighting errors
Continuous illumination is one of the most common types of lighting errors. They can principally occur at any time, however they are most significant during "black-out" or following photostimulation. Exposure to continuous lighting during lay, particularly early in lay, accelerates the induction of photorefractoriness and as a result shortens the reproductive life-span of a flock (Etches, 1997). Furthermore, continuous lighting does not provide a clear cue to the hypothalamus to set the circadian rhythm. This has major implications for normal hormone release stimulation (GnRH) and may alter the egg laying pattern. For older hens in lay, the detrimental effect of continuous illumination is difficult to overcome since the capacity to reestablish a normal hormone balance for reproduction is greatly diminished due to a progressive vanishing in sensitivity to correctly applied stimulatory light.
The magnitude of the detrimental effects of continuous illumination during black-out is, like in case for the laying hen, time dependent. The purpose of exposing hens to a short daylength is to disrupt juvenile photorefractory and to synchronize the reproductive state of the vast majority of the hens in a flock and thereby establishing the ability to respond to stimulatory light upon transfer into the laying barn. In essence, depending on the degree of residual photorefractory at the time of the error, egg production will be more or less impaired.
Concluding remarks
Manipulation of photoperiods of turkey breeders is one of the most sensitive and most powerful management tools available to the turkey operation. Malfunctioning light equipment and incorrectly selected or poorly executed lighting programs and treatments will have profound impacts on performance. Conversely, comprehension of the physiological mechanisms, appreciation of the implications, good communication along with theoretical and practical training can lead to very rewarding results.
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From Proceedings of the "Midwest Poultry Federation Convention", St. Paul, Minnesota, U.S.A.
