Effects of Photostimulatory Light Intensity on Ovarian Morphology and ...

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maturation on ovarian and carcass morphology at first oviposition [sexual maturity .... liver, oviduct, ovary, and stroma (ovary with LYF re- moved) were recorded.
Effects of Photostimulatory Light Intensity on Ovarian Morphology and Carcass Traits at Sexual Maturity in Modern and Antique Egg-Type Pullets R. A. Renema,* F. E. Robinson,*,1 H. H. Oosterhoff,* J.J.R. Feddes,* and J. L. Wilson† *Department of Agricultural, Food, and Nutritional Science, University of Alberta, Edmonton, AB, Canada, T6G 2P5 and †Department of Poultry Science, University of Georgia, Athens, Georgia, 30602 ABSTRACT The effects of light intensity during sexual maturation on ovarian and carcass morphology at first oviposition [sexual maturity (SM)] were examined in two Single Comb White Leghorn (SCWL) strains. A modern commercial layer strain (COMM; Shaver Starcross 288) and an antique randombred control strain (ANT) were used to compare the effects of changes in laying stock on their response to varying light intensities from photostimulation (PS) until SM. Two hundred pullets from each strain were reared following COMM breeder guidelines. At 18 wk of age, 32 COMM and 32 ANT pullets were individually caged in individually lit cages and photostimulated with light intensities of 1, 5, 50, and 500 lx. Each bird was processed when it reached SM, and carcass and ovarian morphology were assessed. The ANT birds came into production 9.1 d later than the COMM birds, on average. The ANT pullets consumed 7.0% more feed per day than COMM pullets but gained at a slower rate (ANT = 12.9 g/d; COMM = 15.0 g/d). The ANT birds reached SM at a greater weight and with a smaller ovary than did COMM birds. Although the number of large yellow follicles (LYF) was similar between strains (mean = 6.72), both LYF weight and first egg weight were lower in ANT birds than in COMM birds. The COMM layer strain was more growth efficient and had a greater emphasis on ovary maintenance.

Light intensity had no effect on the timing of SM or on BW at SM, indicating that all intensities used were effectively able to stimulate the sexual maturation process. However, ovary weight and number of LYF exhibited an increasing dose response to light intensity, particularly in the COMM birds. Overall, the birds photostimulated with 1 lx of light had reduced ovary development and were heavier than their counterparts exposed to 50 and 500 lx. Within the ANT strain, LYF numbers were not significantly affected by light intensities, whereas, within the COMM strain, LYF numbers were 4.88, 6.63, 7.88, and 8.13 for the 1-, 5-, 50-, and 500-lx intensity groups, respectively. Although light intensity did not affect the rate of sexual maturation, it altered ovarian morphology and carcass lipid stores. A light intensity of 1 lx was limiting to ovarian follicle formation and caused increased carcass weight compared with birds on higher light intensity treatments. The COMM birds were more negatively affected by low light intensity than were the ANT birds, indicating that light intensity may be a more critical environmental factor with modern, highly efficient SCWL strains than has previously been thought. Light intensity can affect the reproductive development and likely the associated egg production potential of modern layer stocks.

(Key words: egg-type hen, light intensity, sexual maturation, ovarian morphology, carcass composition) 2001 Poultry Science 80:47–56

creasing stimulus below 5 lx, to a minimum of 0.4 lx, which is equivalent to darkness (Morris, 1967). King (1962) demonstrated that pullets reared in darkness eventually became sexually mature, but they produced eggs at a lower rate (59%) than hens raised on 6 h of 5 to 8 lx of light with weekly day length increases of 15 min (73% average annual production). Other experimental results have demonstrated that light intensity can affect timing of sexual maturity (SM). Wilson et al. (1956) reported that light intensities below 4 lx retarded sexual maturation in caged pullets. Dorminey et al. (1970) reported that sexual maturity (SM) was delayed by 1 wk in pullets reared under 8 h of 1.1 lx (measured 15 cm above the pen floor) compared with pullets reared under 3.2, 5.4, 10.8, and 32.3 lx and about

INTRODUCTION The effect of light intensity on laying hens has typically been assessed through rate of egg production or age at first egg. Morris (1966), using light intensities of 0.2, 1, 5, and 25 lx, demonstrated a logarithmic linear decline in egg production as light intensities decreased. Maximum stimulus for the photoperiodic mechanism was proposed for light intensities above 5 lx, with de-

Received for publication February 25, 2000. Accepted for publication August 17, 2000. 1 To whom correspondence should be addressed: frank.robinson@ ualberta.ca.

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2 wk later than pullets reared under subdued natural light with longer day lengths. Morris (1967) demonstrated a dose-response increase in egg production for hens in three-tiered cages with light intensities of 0.2, 1, and 5 lx measured at the middle tier feed trough. The birds exposed to 0.2 lx reached maturity 9 and 12 d later than the birds exposed to 1 and 5 lx, respectively. In more recent studies using caged laying hens, no significant differences in egg production were observed with light intensity ranging from 2 to 45 lx (Hill et al., 1988), although they suggested that the range of intensities utilized might not have been extreme enough to produce a clear response. Similarly, Tucker and Charles (1993) found no consistent response to light intensities from 0.5 to 15 lx, which led those authors to suggest that modern prolific hybrid laying hens may be more tolerant of low light intensities than earlier stocks. Morris (1994) stated that the laying strains of the 1980s were less sensitive to light than those of the 1960s. However, when Lewis et al. (1999) compared the day of first egg data from their trial to similar treatments of Morris (1967), they concluded that the threshold intensity required to operate the photoperiodic mechanism has not likely been affected by genetic selection for egg production or early SM between 1960 and 1990. Although data are available that examine the effect of light intensity on age at SM and egg production, few published data exist examining the effect of light intensity on reproductive morphology in chickens. Robinson et al. (1998a,b) have demonstrated in broiler breeders that ovarian morphology is important, as an extra large yellow follicles (LYF) at SM is associated with a reduction in total egg production of 10.9 eggs. The primary objectives of this experiment were to investigate the effects of light intensity during sexual maturation on ovarian and carcass morphology at SM and to compare differences in response to light intensity at photostimulation (PS) between a modern commercial strain of Single Comb White Leghorn (SCWL) and an “antique” randombred control strain (ANT).

MATERIALS AND METHODS Stocks and Management A total of 200 commercial strain pullets (COMM; Shaver2 Starcross 288) and 200 ANT were selected from the University of Alberta replacement layer flock and rare-breed preservation flocks, respectively. Pullets were reared following COMM breeder guidelines in four floor pens (4.75 × 5.85 m) of 100 birds each. Rearing photoschedule was 8L (light):16D (dark) in a light-tight facility with an approximate light intensity of 3 to 5 lx. Feed

2 Shaver Poultry Breeding Farms Limited, Box 400, Cambridge, ON, Canada N1R 5V9. 3 Model LI-188; Licor Inc., Lincoln, NE 68504. 4 GE Lighting Canada, Mississauga, ON, Canada L5M 2E4.

and water were provided ad libitum. The ANT pullets originated from random-bred stock imported by Agriculture Canada in 1950 and maintained as a genetic resource to experimental farms and Universities. In 1974, the University of Saskatchewan acquired control of a foundation flock, and it became commonly known as the Saskatchewan Strain White Leghorn (R. D. Crawford, University of Saskatchewan, Saskatoon, Canada, S7N 0W0, 1997, personal communication). A second flock was established from the University of Saskatchewan at the University of Alberta Poultry Research Centre in 1990.

Experimental Design At 17 wk of age, 32 pullets from each strain were individually weighed, wing-banded, and randomly placed in individual, illuminated, standard wire laying cages (30 × 46 cm), alternating by strain. The portable cage units consisted of 16 cages arranged in two tiers of 8. Selected pullets of each strain were of average BW, and there was a similar BW variance for each strain. Light intensity for each battery cage unit was set to provide 1, 5, 50, or 500 lx at a height approximately 22 cm above the cage floor. The resulting experimental design was a 2 × 4 factorial design (strain × light intensity) with 32 birds per strain and 16 birds per light intensity. Each row of eight cages was provided with nine dimmable overhead incandescent bulbs located 21 cm above either the dividing walls of the middle cages or the side walls of the end cages (64 cm from cage floor). The lights above each set of eight cages were checked for consistency of light intensity and were controlled by a single, electronic dimmer. This arrangement allowed the provision of precise light intensities as well as ensuring that birds in end cages were exposed to similar light as those in middle cages. Lights were contained in clear, glass, waterproof fixtures. Lights were cleaned, and the intensities were adjusted using a Li-Cor Quantum/Radiometer/Photometer3 once per week. The 1- and 5-lx treatments were provided with 25 W soft white bulbs, and the 50- and 500-lx treatments used 100 W soft white bulbs.4 Different bulb types were used to limit the shift in the light spectrum that can occur with dimming incandescent bulbs. The cage units were placed in a large, light-tight room divided into four quadrants, including a central hallway, using an opaque black curtain constructed to prevent light transfer between treatments but maintaining adequate ventilation. Bright intensity treatments were on one side of the hallway, and dim intensity treatments were on the other side. The temperature of all treatment areas was maintained at approximately 20 C with the central heating and air-conditioning system. Recirculation fans were used to limit local temperature effects of the light bulbs. Manually recorded cage temperatures varied by less than 0.2 C with the computer-recorded room temperatures. Feed and water were provided ad libitum. The nutrient analyses and

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LIGHT INTENSITY EFFECTS ON SEXUAL MATURATION TABLE 1. Diet schedule and nutrient analyses Analyses

Starter 0–6 wk

Grower 1 6–12 wk

Grower 2 12–16 wk

Pre-lay 16–20 wk

Layer >20 wk

Crude protein (%) ME (kcal/kg) Linoleic acid (%) Methionine (%) Lysine (%) Calcium (%)

21 2,900 1.20 0.42 1.00 0.90

17 2,800 1.00 0.36 0.75 0.95

15 2,750 0.80 0.34 0.70 0.95

16 2,800 1.29 0.39 0.75 2.50

19 2,875 1.40 0.40 0.84 3.80

age of administration of the rations provided are listed in Table 1. At 18 wk, pullets were photostimulated with an initial increase in day length to 12L:12D, and subsequent single, weekly light period increases of 30 min to a maximum day length of 14L:10D at 22 wk. Individual BW and feed consumption data were recorded on a weekly basis. Blood samples were taken at 18, 20, and 22 wk of age for determination of plasma estradiol-17β concentration as described by Renema et al. (1999b). The experimental protocol was approved by the Animal Policy and Welfare Committee of the Faculty of Agriculture, Forestry, and Home Economics of the University of Alberta.

Carcass and Reproductive Traits at Sexual Maturity The weight of the first egg for each hen was recorded on the day of first oviposition, and feed was withdrawn overnight (12 to 20 h) to facilitate gut clearance. The following morning, that pullet was killed by cervical dislocation, and BW was recorded. Shank length (length of the tibiotarsus from the top of the hock joint to the middle of the footpad) was recorded as an indicator of frame size. The birds were dissected, and the weights of the breast muscle (Pectoralis major and minor), abdominal fat pad (including the fat surrounding the gizzard), liver, oviduct, ovary, and stroma (ovary with LYF removed) were recorded. The LYF were counted, sorted by size (with the largest follicle being the F1 follicle), and individually weighed. A follicle in the oviduct was considered the F1 follicle (most developed follicle) only prior to entry into the shell gland. The number of small yellow follicles (SYF; 5 to 10 mm in diameter) and postovulatory follicles (POF) on the stroma were recorded. Unexplained ovulations, defined as ovulations occurring prior to first oviposition, were calculated as described by Renema et al. (1999b) and adjusted for previous ovipositions and eggs in the oviduct. The carcasses were inspected for incidence of internal ovulation, internal oviposition, ovarian regression, and follicular atresia. Carcass components, except for the liver and oviduct, were returned to the carcass and stored at −15 C until analysis was performed. Each carcass was pressurecooked for 4 h and homogenized using an industrial blender. Duplicate 150-g samples were frozen, processed, and analyzed as described by Renema et al. (1999a). Carcass samples were analyzed in duplicate for

dry matter, ash, crude protein, and petroleum etherextractable lipid content. Livers and oviducts were frozen, freeze-dried, and ground. Total liver lipid content was determined by petroleum ether extraction. Oviduct samples were analyzed for crude protein. True liver lipid and oviduct protein content were calculated by adjusting recorded values to account for moisture loss during tissue preparation.

Statistical Analysis The experiment was analyzed as a 2 × 4 factorial design. Sources of variation were strain, light intensity, and the interaction of strain by light intensity. All data were analyzed by two-way analyses of variance using the General Linear Models procedures of SAS (SAS Institute, 1996). When significant differences were determined for the main effects or their interaction, comparison among means were made using the Least Significant Difference procedure. Error variation was considered to be birds within a strain and light intensity. Unless otherwise stated, all statements of significance were assessed using P < 0.05.

RESULTS AND DISCUSSION Carcass Characteristics Age of SM was significantly lower in the COMM than in the ANT strain (Table 2); COMM birds reached SM 146.8 d after PS, on average, compared with 155.9 d for ANT birds. The 9.1-d difference in age of SM represented a 35.1% decrease in the interval between PS and SM in COMM compared with ANT birds. This decrease might have been due to a more efficient or uniform response of the COMM flock to PS or to some degree of sexual maturation prior to PS. The ANT pullets were less uniform in their response to PS, as only 62.5% of the flock reached SM within ±5% of the mean age of first oviposition, whereas 96.9% of the COMM strain were within this range. This reduced variation demonstrates the effectiveness of current selection and breeding programs in selecting for reproductive traits compared with randombred populations. Growth was more efficient in the COMM compared with the ANT strain, because, in addition to a higher daily gain between PS and SM, average daily feed intake was significantly lower for COMM than for ANT birds (ANT = 91.3 g/d; COMM = 85.3 g/d).

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TABLE 2. Age and BW at sexual maturity (SM); BW gain between photostimulation (PS) and SM; and breast muscle, abdominal fat pad, and liver weight, and liver lipid content at SM in females of two Single Comb White Leghorn strains subjected to various photostimulatory light intensities Source Strain2 ANT COMM SEM Light intensity (lx) 1 5 50 500 SEM

Age at SM

BW at SM

BW gain (PS to SM)

Breast muscle weight

Abdominal fat pad weight

Liver weight

Liver lipid content1

(d)

(g)

(g)

(% of BW)

(% of BW)

(g)

(%)

155.9a 146.8b 1.3

1,517 1,469 17

334a 252b 15

13.35b 14.27a 0.20

2.95a 1.92b 0.14

26.4 24.3 0.8

18.3a 12.8b 1.4

152.7 153.6 149.4 149.6 1.8

1,519 1,482 1,496 1,484 24

320 297 283 280 21

14.00 13.88 13.85 13.51 0.28

2.93a 2.21b 2.17b 2.43ab 0.19

27.3a 22.6b 24.9ab 26.6a 1.1

21.4a 10.1b 11.6b 18.3a 2.1

a,b

Means within a column and within a source with no common superscript differ significantly. Lipid percentage = liver lipid weight/liver weight × 100. 2 ANT = Randombred antique stock (University of Alberta); COMM = Shaver Starcross 288. 1

These data are evidence of effective selection pressure for both reduced age of first oviposition and feed efficiency of growth in modern strains of SCWL. At 18 wk of age, the BW of the COMM strain (1,217 g) was significantly higher than that of the ANT strain (1,183 g). However, by SM the relationship had reversed because of the increased time to SM in ANT birds. At SM, the ANT birds weighed 1,517 g on average compared with 1,469 g for COMM birds (P = 0.055) (Table 2). Shank length, an indicator of frame size, was similar between the strains, averaging 9.86 cm. The larger BW gain in ANT birds between PS and SM (Table 2) was not due to differences in growth rate because ANT birds gained at a rate of 12.9 g/d compared with 15.0 g/d for COMM birds. Breast muscle weight was not different on an absolute basis between the strains (data not shown). However, when compared relative to BW, the COMM birds had a larger proportion of breast muscle (14.27%) than did ANT birds (13.35%) (Table 2). This difference carried through to the carcass composition analysis, where COMM carcasses contained 23.9% crude protein compared with 21.9% in ANT carcasses (Table 3). The use of 1- to 500-lx light intensities between PS and SM had no significant effect on age at SM (Table 2). These results concur with those of Lewis et al. (1999), who monitored the effects of light intensity on age at first egg and concluded that the threshold intensity required by chickens for stimulation of a full response to an increase in photoperiod lies between 0.9 and 1.7 lx. The results differ from observations of Wilson et al. (1956) and Dorminey et al. (1970), who found that reduced light intensities of 4 and 1.1 lx, respectively, delayed SM. These differences may be related to differences in light delivery in these experiments or to the use of a step-up lighting schedule in the current study, which provided a lengthening day signal each week. The most important interpretation of the lack of light intensity effect on the timing of SM, however, is that all intensities were effectively able to stimulate the sexual maturation process. Light intensity also had no affect on BW at SM,

shank length (data not shown), or breast muscle weight (Table 2). The 1-lx intensity treatment provided enough light for normal feed and water access, as these birds maintained similar BW and sexual maturation patterns to birds in the brighter light intensity treatments. Feed intake between PS and SM was not affected by light intensity, averaging 88.3 g/d. Lewis and Morris (1999), based on regression analysis of six studies performed between 1946 and 1993, predicted that daily feed intake of production hens would decreased linearly by 0.2 g for each 10-lx increase in light intensity to 100 lx. No effect of light intensity from 54 to 324 lx was reported for the feed intake or feed efficiency of turkeys (Siopes, 1991). Although the current study uses a range of 1- to 500-lx light intensity with no effect on daily feed intake or growth efficiency, it may be that negative effects of higher light intensity on feed intake are not expressed until a later age. Abdominal fat pad weight was heavier in the ANT strain than in the COMM strain at SM on both an abso-

TABLE 3. Carcass protein, lipid, ash, and water content at sexual maturity, in females of two Single Comb White Leghorn strains subjected to various photostimulatory light intensities Source

Carcass protein

Carcass lipid

Carcass ash

Carcass water

(% of BW) Strain1 ANT COMM SEM Light intensity (lx) 1 5 50 500 SEM

21.9b 23.9a 0.2

16.9a 12.5b 0.5

3.6b 3.8a 0.1

56.3b 58.4a 0.3

22.2b 23.2a 22.8ab 23.4a 0.3

16.2a 13.5b 14.0b 15.3ab 0.7

3.4 3.8 3.8 3.8 0.1

56.8bc 58.2a 58.1ab 56.4c 0.5

a–c Means within a column and within a source with no common superscript differ significantly. 1 ANT = Randombred antique stock (University of Alberta); COMM = Shaver Starcross 288.

LIGHT INTENSITY EFFECTS ON SEXUAL MATURATION

lute basis (ANT = 42.2 g; COMM = 26.4 g) and when expressed relative to BW (ANT = 2.95%; COMM = 1.92%) (Table 2). The relative weights are similar to the values of 2.5, 1.7, and 1.9% reported by Robinson et al. (1996b) in pullets photostimulated at 16, 18, and 20 wk, respectively. An increased liver lipid content in ANT (18.3%) compared with COMM livers (12.8%) further demonstrated the increased fatness of ANT birds (Table 2) , as did an increased relative carcass lipid content (Table 3). The reduced proportion of water in ANT compared with COMM birds (Table 3) is consistent with previous observations on the inverse relationship between carcass lipid and water content (Yu et al., 1992a). The differences in lipid content at various sites provide explanation for the increased growth efficiency of the COMM strain compared with the ANT strain and clearly demonstrate how the growth patterns of these birds have changed because of genetic selection programs. It has been suggested that there is a BW or body composition threshold for the onset of sexual maturation (Brody et al., 1980, 1984). The delay in SM for ANT birds appears to fit the threshold concept, as these initially smaller birds reached a BW similar to that of the COMM strain by SM. However, the increased abdominal fat pad size and carcass lipid content of ANT birds indicate that the delayed SM in the ANT strain was not limited by a lipid content threshold as proposed by Bornstein et al. (1984). Renema et al. (1999a) found the relationship between reproductive development and carcass parameters in broiler breeders to also be inconsistent and concluded that the actual internal signal for initiating reproductive development was more likely a metabolic one. Although the lipid content threshold might have been significantly reduced in the COMM strain by genetic selection for earlier SM and feed efficiency, a more accurate explanation may be that it is due to changes in photoperiodic drive. Eitan and Soller (1993) examined birds with high and low BW thresholds for reproduction and found that the low line birds commenced lay sooner and at a lower BW than high line birds. They hypothesized the differences to be due to a decreased photoperiodic drive in the high line birds relative to the low line birds. In the current study, the above hypothesis would mean that the COMM birds are more responsive to light than are their ANT counterparts. Alternatively, the hypothalamic maturity of the COMM birds may be earlier, allowing them to respond to the increasing photoperiod more quickly. These strains might also have differing involvement of the pineal gland in the measurement of day length. It has been suggested that the pineal gland is able to perceive light and transform photic information into a measure of day length (Nakahara et al., 1997), as indicated by the circadian pattern of melatonin release. Although light intensity did not affect BW or breast muscle weight at SM, it did alter abdominal fat pad weight and total carcass lipids. Abdominal fat pad weight, expressed as percentage of BW, was 2.93% in birds exposed to 1-lx light compared with 2.21 and 2.17% in birds exposed to 5- and 50-lx , respectively (Table 2).

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Livers of birds exposed to 1-lx light were 20.7% heavier than those of birds exposed to 5-lx light, and their liver lipid content was 21.4% compared with a mean of 10.9% in birds exposed to 5 and 50-lx light (Table 2). Liver weight and lipid content of birds exposed to 500-lx light were similar to those of birds exposed to 1-lx light. Abdominal fat pad proportion for birds exposed to 500-lx light was intermediate to those for birds exposed to 1 lx of light compared with birds exposed to the 5- and 50-lx treatments, however. This relationship was also present in the proportion of carcass lipids: birds on the 1-, 5-, 50-, and 500-lx treatments contained 16.2, 13.5, 14.0, and 15.3% lipid, respectively (Table 3). The carcass lipid content of birds exposed to 1 lx of light was greater than that of birds exposed to 5 and 50 lx of light, whereas the 500-lx value was intermediate. Liver lipid content was significantly increased in birds exposed to 500 lx of light, with a level of 18.3% in these birds compared with a mean of 10.7% in birds exposed to 5 and 50 lx of light (Table 2). Increased light intensity may have a stimulatory effect on lipogenesis, possibly through the influence of estrogen. The proportion of carcass protein was reduced in birds exposed to 1 lx of light compared with those exposed to 5 and 500 lx of light. Absolute carcass protein weights did not differ (data not shown), which likely relates to the elevated lipid content of birds exposed to 1 lx of light. Above 1 lx, fat content and liver weight appear to increase in a dose-response manner to the 5-, 50-, and 500-lx light intensities. A contributing factor to the increased fatness of birds on the 1-lx treatment may be decreased pullet activity caused by the dim conditions. Reduced bird activity and decreased maintenance levels of energy required permitted a greater proportion of energy to be allocated to lipid depots, whereas increasing light intensity above 5 lx increased lipogenesis by the liver. Liver lipid content was significantly increased in birds on the 500-lx treatment, with a level of 18.3% in these birds compared with a mean of 10.7% in birds on the 5 and 50-lx treatments (Table 2).

Reproductive Morphology Layer strain primarily affected the weight of the oviduct, ovary, and ovarian follicles. Oviducts of COMM birds were 10.0% larger than those of ANT birds and had a 17.5% protein content compared with 19.2% in ANT birds, suggesting that the lower oviduct weight in ANT pullets was not simply a function of lean tissue growth (Table 4). The ability of the infundibulum to capture the first ovulation may relate to oviduct maturity and motility rather than simply size. Internal ovulation at SM has been proposed to result from a lack of synchrony between the maturation of the oviduct and the ovary (Robinson et al., 1996a; Melnychuk et al., 1997). Postovulatory follicles that are not reconcilable with confirmed ovulations or ovipositions at SM provide a numeric indication of internal ovulation and the degree of oviductal incompetence upon the onset of ovulation. In

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RENEMA ET AL. TABLE 4. Oviduct weight and protein content and ovary weight at sexual maturity in females of two Single Comb White Leghorn strains subjected to various photostimulatory light intensities Oviduct Source Strain3 ANT COMM SEM Light intensity (lx) 1 5 50 500 SEM

Ovary 1

2

Weight

Percentage

Protein

Weight

Percentage1

(g)

(%)

(%)

(g)

(%)

42.8b 47.1a 0.9

3.02b 3.44a 0.05

19.2a 17.5b 0.3

30.7 35.5 1.8

2.15b 2.59a 0.12

42.8 44.8 45.7 46.3 1.3

3.04b 3.26a 3.29a 3.33a 0.08

19.4a 18.4ab 17.7b 17.9b 0.5

26.9b 31.9ab 36.1a 37.4a 2.6

1.87b 2.32ab 2.59a 2.70a 0.17

a,b

Means within a column and within a source with no common superscript differ significantly. Oviduct percentage = oviduct weight/BW × 100. 2 Oviduct protein = oviduct protein weight/oviduct weight × 100. 3 ANT = Randombred antique stock (University of Alberta); COMM = Shaver Starcross 288. 1

the current study, the ANT strain demonstrated a higher number of unexplained POF (ANT = 1.16; COMM = 0.09) (Table 5). When internal ovulation or other follicle losses occur, first oviposition does not accurately represent the age at which the pullet has first ovulated. For the ANT strain, the age of first ovulation might have been 1 to 3 d prior to the reported age of first oviposition. Renema et al. (1995) and Melnychuk et al. (1997) have previously observed that a high incidence of unexplained POF at

SM contributed to reproductive inefficiency in turkey hens. Genetic selection for reproductive efficiency in modern SCWL appears to have greatly reduced the potential for the incidence of internal ovulation at SM. Relative oviduct weight increased in response to each logarithmic increase in light intensity at PS; a significant difference was observed between oviducts of birds receiving 1or 500 lx of light (Table 4). The absolute oviduct weight was numerically, but not significantly, affected

TABLE 5. Unexplained postovulatory follicle (POF), ovarian follicle numbers, and stroma weight at sexual maturity in females of two Single Comb White Leghorn strains subjected to various photostimulatory light intensities

Source Strain4 ANT COMM SEM Light intensity (lx) 1 5 50 500 SEM Interaction ANT-1 ANT-5 ANT-50 ANT-500 COMM-1 COMM-5 COMM-50 COMM-500 SEM

Ovarian follicles2

Unexplained POF1

LYF

SYF

Stroma weight3

(no.)

(no.)

(no.)

(g)

1.16a 0.09b 0.13

6.56 6.88 0.34

3.91 3.63 0.33

3.92 3.54 0.19

1.06a 0.75ab 0.44b 0.25b 0.18

5.50b 6.56ab 7.31a 7.50a 0.48

4.13 3.06 4.56 3.31 0.46

3.37 3.60 3.91 4.04 0.30

2.00a 1.25ab 0.88b 0.50b 0.13 0.25 0.00 0.00 0.26

6.13 6.50 6.75 6.88 4.88b 6.63ab 7.88a 8.13a 0.68

5.63a 2.75b 4.25ab 3.00b

4.25 3.44 3.91 4.07

2.63b 3.38ab 4.88a 3.63ab 0.65

2.49b 3.75a 3.91a 4.01a 0.38

a,b Means within a column and within a source with no common superscript differ significantly. Interaction means are compared within a strain. 1 POF not accounted for by eggs laid or by yolks or eggs in oviduct. 2 LYF = Large yellow follicles (>10 mm diameter); SYF = small yellow follicles (5 to 10 mm diameter). 3 Stroma = Ovary with the LYF removed. 4 ANT = Randombred antique stock (University of Alberta); COMM = Shaver Starcross 288.

LIGHT INTENSITY EFFECTS ON SEXUAL MATURATION

(P < 0.10) in a similar fashion. Oviduct protein content also differed; the oviducts of birds on the 1-lx treatment consisted of 19.4% protein compared with an average of 17.8% in birds exposed to 50 and 500 lx of light (Table 4). The quantity of irreconcilable POF was highest in the pullets photostimulated with 1 lx of light intensity and decreased as light intensity increased (Table 5). The strain × light intensity interaction means suggest that the majority of unexplained POF were associated with ANT birds; values were near zero for most light intensities with COMM birds (Table 5). Greater values were associated with low light intensities in both strains. As previously discussed, internal ovulation may be the result of an immature oviduct that is unable to capture the first ovulated follicles. Light intensity affected the growth of the oviduct, particularly factors pertaining to the attainment of its functional maturity. A light intensity of 1 lx does not produce the same degree of oviduct development as higher light intensities. The increased number of unexplained POF in ANT birds exposed to low light intensity suggests that control of ovulation may be compromised. Ovary weight was 35.5 g in COMM birds compared with 30.7 g in ANT birds. Although this difference was not significant (P = 0.08), there was a significant strain effect on the relative ovary weight (Table 4). There was no effect of strain on stroma weight (ovary weight without LYF), however, and the number of LYF and SYF were also similar (Table 5). The total LYF weight (ovary weight — stroma weight) and average LYF weight were higher in the COMM strain than in the ANT strain (Table 6). Therefore, although number of LYF did not differ, the size of each LYF was larger in the modern COMM strain, which was further evidenced by the heavier F1 follicle weight (ANT = 7.4 g; COMM = 8.7 g) and initial egg weight (ANT = 37.0 g; COMM = 42.6 g) in COMM

TABLE 6. Large yellow follicle (LYF) weight parameters at sexual maturity and first egg weight in females of two Single Comb White Leghorn strains subjected to various photostimulatory light intensities LYF Parameters Source

Total weight

Mean weight

F1 weight1

(g) Strain2 ANT COMM SEM Light intensity (lx) 1 5 50 500 SEM

First egg weight (g)

29.0b 37.3a 1.9

4.43b 5.27a 0.16

7.4b 8.7a 0.3

37.0b 42.6a 1.0

25.3b 33.0a 36.3a 38.2a 2.6

4.29b 5.02a 5.00a 5.08a 0.22

7.3 8.0 8.4 8.4 0.4

39.6 41.2 38.9 39.4 1.4

a,b Means within a column and within a source with no common superscript differ significantly. 1 F1 = Protein percentage = protein weight/oviduct weight × 100. 2 ANT = Randombred antique stock (University of Alberta); COMM = Shaver Starcross 288.

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birds compared with ANT birds (Table 6). Despite BW that were similar to those of COMM birds at SM and despite increased fatness, the initial egg size of ANT birds remained 15.1% less than that of COMM birds. Yolk size (F1 weight) related to egg size in this study and, if incubated, chick size would also likely relate (Shanaway, 1984). Ovary weight, expressed in both absolute terms and relative to BW (Table 4), and ovarian LYF number (Table 5) exhibited an increasing dose response to light intensity. The ovaries of birds on the 1-lx treatment were significantly smaller than those of birds on the 50- and 500-lx treatments. The LYF means for the light intensity groups varied from 5.50 in the 1-lx group to 7.50 in the 500-lx group (Table 5). However, the effects of light intensity were primarily associated with the COMM strain. The LYF means for ANT birds under different intensities did not differ from each other, whereas, within the COMM strain, LYF numbers were 4.88, 6.63, 7.88, and 8.13 for the 1-, 5-, 50-, and 500-lx treatment groups, respectively. A range of six to eight LYF is typical for high producing layer strains (Williams and Sharp, 1978). The reduced quantity of LYF under low light intensities suggests that potential egg production may be compromised. This finding is in agreement with previous observations of reduced egg production under very low light intensities (Morris, 1966, 1967), but does not agree with those of Dorminey et al. (1970), Hill et al. (1988) and Tucker and Charles (1993), who reported no difference in egg production as a result of light intensities ranging from 1.1 to 34 lx. Hill et al. (1988) suggested that the range of intensities that they utilized might not have been extreme enough to produce a clear response. In a broiler breeder study in which the dietary treatments were associated with a 1.1 difference in LYF numbers (Robinson et al., 1998a), there was ultimately a 10.9 egg difference in total egg production (Robinson et al., 1998b). However, in the same study, a 0.9 LYF difference caused by photoperiod treatments did not result in a difference in egg production. Although the 3.25 difference in LYF numbers in the COMM birds caused by light intensity was not a feed-based difference, it was large enough that long-term effects on egg production would be expected. Unlike the situation with broiler breeders, for which excess LYF production is of concern because of production of unsettable eggs (Yu et al., 1992b), here the limiting factor may be follicular insufficiency in the 1-lx light intensity group. Renema et al. (1999a) found that a 1.2 follicle reduction in LYF numbers in low BW feed-restricted birds compared with target or higher BW feed-restricted birds was associated with increased rates of small follicle atresia. They theorized that as LYF numbers decline with age, the combination of reduced LYF number with elevated rates of atresia would likely limit egg production. Atresia of the small follicles was not examined in the current study, however. Ovarian stroma weight and SYF number of COMM birds was affected in a similar fashion to ovary weight and LYF number; the birds exposed to 1 lx of

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light had significantly lower values than some of the birds in higher light intensity groups (Table 5). Light intensity had very little effect on the ovarian morphology of the ANT birds. Examination of the LYF parameters showed that birds exposed to 1 lx of light produced a smaller total LYF mass (25.3 g) than did in any of the birds on the higher intensity treatments (mean total weight = 35.8 g) (Table 6). The mean weight of the individual LYF was 14.8% smaller in birds exposed to 1 lx of light, on average, than that of birds on any other light intensity treatment. Egg weight was not affected by light intensity, however, and F1 weight demonstrated only numerical reductions for birds exposed to 1-lx light compared with the other birds. These observations demonstrate that a light intensity of 5 lx is adequate for production of fully formed LYF, whereas 1 lx was insufficient for adequate yolk deposition. The limited yolk deposition in birds exposed to 1 lx of light is not believed to be due to insufficient light and dark contrast, limiting the photostimulatory effect. Morris and Bhatti (1978) reported that the light intensity of the photophase must be at least 10 times greater than the intensity of the scotophase for chickens to normally entrain oviposition rhythms. The facility used in the current study had no exterior doors in the bird areas and had light-tight ceiling ventilation units. Meyer et al. (1988) found that a bird’s photoperiodic history did not influence its likelihood of photostimulation with dim light and that the photophase contrast was more important than the absolute light intensity. In the strain and light intensity comparisons, the groups producing fewer or smaller LYF also had the highest measures of fatness (ANT and 1-lx treatments). In these birds, there was a shift in nutrient allocation from yolk formation to lipid storage. Genetic changes in growth and laying efficiency can adequately explain differences between the strains. Although all light intensities provided adequate stimulation to operate the photoperiodic mechanism, follicle formation and yolk deposition were occurring at a reduced rate in birds exposed to 1 lx of light compared with those on higher light intensity treatments. This effect may originate with changes to the structure of the very low density lipoprotein (VLDL) particles transporting lipid from the liver. Plasma estrogen, for example, stimulates hepatic fatty acid and triglyceride synthesis and stimulates the formation of phospholipids and proteins to package the characteristically smaller VLDL particles destined for ovarian uptake (Walzem, 1996). Birds emphasizing yolk deposition will have an increased proportion of VLDL particles in the 22- to 51-nm range rather than larger sizes, which are indicative of poorer egg production rates (Walzem et al., 1994; Walzem, 1996) and increased lipid deposition. Hormonal impulses for both reproductive development and growth are both expressed, in part, at the liver level. If light intensity provides inadequate stimulation for normal ovarian and oviduct development, excess

nutrients will be available for deposition or catabolism at other sites. Although reduced follicle stimulating hormone and luteinizing hormone release may limit follicle formation and estrogen release, plasma estradiol-17β concentration did not significantly differ between light intensity groups (data not shown). Thyroid hormone is known to be elevated during conditions of chronic positive energy balance (Simon, 1989) and can inhibit gene expression of an estrogen-stimulated apoprotein (Akiba et al., 1982) that is important to the formation of VLDL specific to yolk deposition (Schneider et al., 1990). Clearly both strain and light intensity effects on lipid allocation are complex and may involve interaction on multiple levels. Light intensity had a greater effect on LYF numbers in the COMM strain than in the ANT strain (Table 5). Tucker and Charles (1993) stated that modern prolific hybrid laying hens may be more tolerant of low light intensities than earlier stocks. Morris (1994) suggested that laying strains of the 1980s were less sensitive to light intensity than those of the 1960s because more recent studies with modern strains had not shown the same light intensity effects on rate of lay as earlier studies. However, when Lewis et al. (1999) compared the day of first egg data from their trial with similar treatments groups from Morris (1967), they concluded that the threshold intensity required to stimulate the photoperiodic mechanism appears to have been unchanged by genetic selection for egg production traits since the 1960s. The results of the current study demonstrate that a modern COMM strain of SCWL responds to PS and reaches SM at an earlier age than the ANT strain. Modern commercial strains of SCWL are the product of genetic selection and breeding programs that have been successful at developing very reproductively efficient birds. Modern birds exhibit decreased age at first oviposition and changes in reproductive morphology. This study also demonstrates that birds have differential responses to lighting, as it is affected by both the history of the strain and by light intensity. The use of 1- to 500-lx light intensities did not affect the timing of SM, which concurred with other recent results monitoring age at SM (Lewis et al., 1999). However, it has not previously been demonstrated that light intensity affects reproductive and carcass morphology at SM. Although the 1-lx treatment stimulated sexual maturation following PS, it was not a full response. Ovary and oviduct weights were reduced, and lipid stores were increased, relative to the higher intensity groups, indicating inadequate PS. In birds exposed to the 500-lx treatment, numerically increased weights of all lipid measures and numerically higher values for most ovarian morphology measures, including estradiol-17β concentration (data not shown), suggest the potential for overstimulated sexual development. If follicle stimulating hormone, luteinizing hormone, and estrogen concentrations were further elevated at very high light intensities, there may be reason for concern about overstimulation of ovary

LIGHT INTENSITY EFFECTS ON SEXUAL MATURATION

development, leading to similar reproductive problems as found in overweight broiler breeder hens (Robinson et al., 1991, 1993; Yu et al., 1992b). The threshold light intensity for a complete morphological response to PS in this study was between 1 and 5 lx. A 1-lx intensity resulted in inferior ovary development, particularly in the COMM birds. The COMM birds were more negatively affected by low light intensity than were ANT birds, indicating that light intensity may be a more critical environmental factor with modern, highly efficient SCWL strains than has been previously shown. With the development of highly specific genetic strains, it will be increasingly important to match the environmental management practices to the particular strain of hens.

ACKNOWLEDGMENTS This project was funded by the Alberta Agricultural Research Institute and Shaver Poultry Breeding Farms, Ltd. Infrastructure support was provided by the University of Alberta Poultry Research Centre through funding provided by the University of Alberta, Alberta Agriculture, Food, and Rural Development and the four Alberta Poultry Producer Boards.

REFERENCES Akiba, Y., L. S. Jenson, C. R. Barb, and R. R. Kraeling, 1982. Plasma estradiol, thyroid hormones, and liver lipid content in laying hens fed different isocaloric diets. J. Nutr. 112:299–308. Bornstein, S., I. Plavnik, and Y. Lev, 1984. Body weight and/ or fatness as potential determinants of the onset of egg production in broiler breeder hens. Br. Poult. Sci. 25:323– 341. Brody, T., Y. Eitan, M. Soller, I. Nir, and Z. Nitsan, 1980. Compensatory growth and sexual maturity in broiler females reared under severe food restriction from day of hatching. Br. Poult. Sci. 21:437–446. Brody, T. B., P. B. Siegel, and J. A. Cherry, 1984. Age, body weight, and body composition requirements for the onset of sexual maturity of dwarf and normal chickens. Br. Poult. Sci. 25:245–252. Dorminey, R. W., J. E. Parker, and W. H. McClusky, 1970. Effect of light intensity on leghorn pullets during the development and laying periods. Poultry Sci. 49:1657–1661. Eitan, Y., and M. Soller, 1993. Two-way selection for threshold body weight at first egg in broiler strain females. 3. Reproductive performance under various levels of feed restriction. Poultry Sci. 72:1813–1822. Hill, J. A., D. R. Charles, H. H. Spechter, R. A. Bailey, and A. J. Ballantyne, 1988. Effects of multiple environmental and nutritional factors on laying hens. Br. Poult. Sci 29:499–511. King, D. F., 1962. Egg production of chickens raised and kept in darkness. Poultry Sci. 41:1499–1503. Lewis, P. D., and T. R. Morris, 1999. Light intensity and performance of domestic pullets. World’s Poult. Sci. J. 55:241–250. Lewis, P. D., T. R. Morris, and G. C. Perry, 1999. Light intensity and age at first egg in pullets. Poultry Sci. 78:1227–1231. Melnychuk, V. L., F. E. Robinson, R. A. Renema, R. T. Hardin, D. A. Emmerson, and L. G. Bagley, 1997. Carcass traits and reproductive development at the onset of lay in two lines of female turkeys. Poultry Sci. 76:1197–1204. Meyer, W. E., J. R. Millam, and F. A. Bradley, 1988. Photostimulation of Japanese quail by dim light depends upon pho-

55

tophase contrast, not light intensity. Biol. Reprod. 38:536– 543. Morris, T. R., 1966. Light intensity for growing and laying pullets. World’s Poult. Sci. J. 22:156–157. Morris, T. R., 1967. The effect of light intensity on growing and laying pullets. World’s Poult. Sci. J. 23:246–252. Morris, T. R., 1994. Lighting for layers: What we know and what we need to know. World’s Poult. Sci. J. 50:283–287. Morris, T. R., and B. M. Bhatti, 1978. Entrainment of oviposition in the fowl using bright and dim light cycles. Br. Poult. Sci. 19:341–348. Nakahara, K., N. Murakami, T. Nasu, H. Kuroda, and T. Murakami, 1997. Individual pineal cells in chick possess photoreceptive, circadian clock and melatonin-synthesizing capacities in vitro. Brain Res. 774:242–245. Renema, R. A., F. E. Robinson, V. L. Melnychuk, R. T. Hardin, L. G. Bagley, D. A. Emmerson, and J. R. Blackman, 1995. The use of feed restriction for improving reproductive traits in male-line large white turkey hens. 2. Ovary morphology and laying trait characteristics. Poultry Sci. 73:1724–1738. Renema, R. A., F. E. Robinson, M. Newcombe, and R. I. McKay, 1999a. Effects of body weight and feed allocation during sexual maturation in broiler breeder hens: 1. Growth and carcass characteristics. Poultry Sci. 78:619–628. Renema, R. A., F. E. Robinson, J. A. Proudman, M. Newcombe, and R. I. McKay, 1999b. Effects of body weight and feed allocation during sexual maturation in broiler breeder hens: 2. Ovarian morphology and plasma hormone profiles. Poultry Sci. 78:629–639. Roberts, J., and J. S. Carver, 1941. Electric light for egg production. Agric. Eng. 22:357–360, 364. Robinson, F. E., V. L. Melnychuk, L. D. Muller, H. H. Oosterhoff, T. A. Wautier, and J. L. Wilson, 1996a. Sexual maturation in female domestic poultry as influenced by photostimulation program. Pages 110–122 in: Proceedings of 45th Annual National Breeders Round Table Meeting, St. Louis, MO. Robinson, F. E., R. A. Renema, L. Bouvier, J.J.R. Feddes, J. L. Wilson, M. Newcombe, and R. I. McKay, 1998a. Effects of photostimulatory lighting and feed allocation in female boiler breeders 1. Reproductive development. Can. J. Anim. Sci. 78:603–613. Robinson, F. E., R. A. Renema, L. Bouvier, J.J.R. Feddes, M. J. Zuidhof, J. L. Wilson, M. Newcombe, and R. I. McKay, 1998b. Effects of photostimulatory lighting and feed allocation in female boiler breeders. 2. Egg and chick production. Can. J. Anim. Sci. 78:615–623. Robinson, F. E., N. A. Robinson, and T. A. Scott, 1991. Reproductive performance, growth rate, and body composition of full-fed versus feed-restricted broiler breeder hens. Can. J. Anim. Sci. 71:549–556. Robinson, F. E., T. A. Wautier, R. T. Hardin, J. L. Wilson, M. Newcombe, and R. I. McKay, 1996b. Effects of age at photostimulation on reproductive efficiency and carcass characteristics. 2. Egg-type hens. Can. J. Anim. Sci. 76:283–288. Robinson, F. E., J. L. Wilson, M. W. Yu, G. M. Fasenko, and R. T. Hardin, 1993. The relationship between body weight and reproductive efficiency in meat-type chickens. Poultry Sci. 72:912–922. SAS Institute, 1996. The SAS威 System for Windows. Release 6.12. SAS Inst., Inc., Cary, NC. Schneider, W. J., R. Carroll, D. L. Severson, and J. Nimpf, 1990. Apolipoprotein VLDL-II inhibits lipolysis of triglyceriderich lipoproteins in the laying hens. J. Lipid Res. 31:507–513. Shanaway, M. M., 1984. Inter-relationship between egg weight, parental age and embryonic development. Br. Poult. Sci. 59:159–163. Simon, J., 1989. Chicken as a useful species for the comprehension of insulin action. CRC Crit. Rev. Poult. Biol. 2:121–148.

56

RENEMA ET AL.

Siopes, T. D., 1991. Light intensity effects on reproductive performance of turkey breeder hens. Poultry Sci. 70:2049–2054. Tucker, S. A., and D. R. Charles, 1993. Light intensity, intermittent lighting and feeding regimen during rearing as affecting egg production and egg quality. Br. Poult. Sci. 34:255–266. Walzem, R. L., 1996. Lipoproteins and the laying hen: Form follows function. Poult. Avian Biol. Rev. 7(1):31–64. Walzem, R. L., P. A. Davis, and R. J. Hansen, 1994. Overfeeding increases very low density lipoprotein diameter and casus the appearance of a unique lipoprotein particle in association with failed yolk deposition. J. Lipid Res. 35:1354–1366. Williams, J. B., and P. J. Sharp, 1978. Ovarian morpology and rates of ovarian follicular development in laying broiler

breeders and commercial egg producing hens. Br. Poult. Sci. 19:387–395. Wilson, W. O., A. E. Woodard, and H. Abplanalp, 1956. The effect and after-effect of varied exposure to light on chicken development. Biol. Bull. 111:415–422. Yu, M. W., F. E. Robinson, R. G. Charles, and R. Weingardt, 1992a. Effect of feed allowance during rearing and breeding on female broiler breeders. 1. Growth and carcass characteristics. Poultry Sci. 71:1739–1749. Yu, M. W., F. E. Robinson, R. G. Charles, and R. Weingardt, 1992b. Effect of feed allowance during rearing and breeding on female broiler breeders. 2. Ovarian morphology and production. Poultry Sci. 71:1750–1761.