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Biology of Reproduction 62, 1452-1458 (2000)
© 2000 Society for the Study of Reproduction, Inc.

Articles

Circadian Rhythm of the Preovulatory Surge of Luteinizing Hormone and Its Relationships to Rhythms of Body Temperature and Locomotor Activity in Turkey Hens1

Jingying Yanga, James L.M. Morganb, John D. Kirbyb, David W. Longa, and and Wayne L. Bacon2,a

a Department of Animal Sciences, The Ohio State University, Ohio Agricultural Research and Development Center, Wooster, Ohio 44691 b Department of Poultry Science, University of Arkansas, Fayetteville, Arkansas 72701


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Simultaneous measurements of plasma LH, body temperature, and locomotor activity were made in laying turkey hens and are reported. Blood samples were remotely collected using a jugular cannula system, and body temperature and locomotor activity were remotely monitored using a radiotelemetry system in freely moving laying turkeys. Under a photoschedule of 14L:10D, the period for preovulatory surges of LH was 25.7 ± 0.4 h while the periods for peak body temperature and onset of sustained locomotor activity were 24.9 ± 0.4 and 25.7 ± 0.5 h, respectively. During exposure to constant light, the periods for preovulatory surges of LH, peak body temperature, and onset of sustained locomotor activity increased to 27.9 ± 0.9, 26.7 ± 0.7, and 27.4 ± 0.7 h, respectively. With the 14L:10D photoschedule, initiation of LH surges was restricted to the scotophase, but after 8 days of constant light, initiation of LH surges had dispersed throughout the 24-h subjective day and night. With constant light, the amplitude of the peak body temperature rhythm decreased, while the duration of the locomotor activity rhythm became broadened and, in some birds, disorganized. Peak body temperature and onset of locomotor activity rhythms and LH surges did not coincide, even though peak body temperature, onset of locomotor activity, and LH surges had similar periods. It is concluded that 1) the photoschedule influences the periods of the LH surge, peak body temperature, and onset of locomotor activity; and 2) a specific or direct relationship between the rhythms of LH surge, body temperature, and locomotor activity remains to be determined in laying turkey hens.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
All organisms exhibit daily rhythms in behavioral, physiological, and biochemical processes. Circadian rhythms are those rhythms that persist in the absence of clues external to the organism and have free-running periods close to 24 h under constant environmental conditions, such as continuous light. The periods of most circadian rhythms under constant conditions are slightly less than 24 h [1]. One physiological process that exhibits a circadian rhythm is body temperature [2]. The circadian rhythm of body temperature has been studied extensively using radiotelemetry in chickens [3–8] and Japanese quail [9, 10]. Kadono and coworkers [7] found that, under conditions of constant light, chicken hens selected for increased egg production (White Leghorn) had a body temperature circadian rhythm with a period of 25.3 h that was the same as the period for ovipositions. In laying Japanese quail under conditions of constant light, Underwood et al. [10] found that the period for the body temperature circadian rhythm was 26.7 h, but exposure of the hens to constant dark or ovariectomy, conditions that block or preclude egg-laying, resulted in a shortened circadian rhythm of 22.7 h. In both chickens [3, 4, 7] and quail [10], there was a spike in body temperature of 1–2 h duration associated with oviposition. It has not been reported if this oviposition-associated spike in body temperature is expressed in turkeys or other avian species.

In both mammals and birds, a preovulatory surge of LH is necessary to induce ovulation. In ewes [11], the LH surge takes place during the low body temperature portion of the daily temperature rhythm, but occurs only once each estrous cycle of 17–18 days. In birds, the relationship of body temperature rhythm and the approximately daily surges of LH or other diurnally cycling hormones has not been directly determined in a longitudinal study of several days duration. In the chicken, it is known that ovulation occurs about one-half hour before the temperature spike associated with ovulation [3, 8]. Ovulation of intra-sequence ova occurs 15–30 min after oviposition in turkey hens [12]. Ovulation occurs about 8 h after injection of LH in chicken hens [13]. Also, ovulation is blocked by hypophysectomy 4–6 h before expected ovulation in laying chicken hens [14] and Japanese quail [15]. Thus, surges of LH were predicted to occur 6–8 h before ovulation in two avian species. Later measurements of plasma LH by RIA confirmed this prediction of plasma LH surges 6 to 8 h before ovulation in chickens [16] and turkeys [17]. No investigations in any avian species have looked at the rhythms of both body temperature and ovulatory surges of LH and their possible interrelationships because of difficulties associated with remote collection of the necessary serial blood samples in avian species. In the present study, we have for the first time looked at the relationships of the rhythms of body temperature, ovulatory surges of LH, and locomotor activity in a freely moving laying bird, the domestic turkey.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Turkey Hens and Management

Laying turkey hens, 50 wk of age (E-line selected for increased egg production [18]), were supplied by the Turkey Research Center of the Ohio Agricultural Research and Development Center. A total of 8 hens with records of continuous egg production were caged (60 x 60 x 80 cm) individually, with wood shavings as litter, in a light-controlled room under a photoschedule of 14L:10D, lights-on at 0500 h. Regular laying hen ration and water were provided for ad libitum consumption.

The cannula system, previously described by Chapman et al. [19], was used to withdraw 1.0-ml blood samples every hour. Briefly, a medical-grade silicone tubing cannula was percutaneously inserted approximately 10 cm into the right jugular vein, sutured to the bird's skin at the site of percutaneous puncture, passed to a small back harness, then threaded through a stainless steel spring tether to a fluid swivel mounted at the top of the cage. An extension cannula then extended outside of the animal room. This system allowed hens free-movement and access to feed and water within the individual cages. Remote blood withdrawal operations were performed outside the animal room so as not to disturb the birds or alter their behavior when serial blood samples were collected during photophases and scotophases.

Body temperature and locomotor activity were continuously recorded using a radiotransmitter (VM-FH, 5 cm; Mini-Mitter, Sunriver, OR) and radio receiver (TR-3000; Mini-Mitter) radiotelemetry system. Hens were anesthetized with Isoflurane (Rhone-Poulenc, Collegeville, PA), and transmitters were implanted between internal and external oblique abdominal muscles. Radio receivers were positioned directly under the hens and connected to a computer and software program (VitalView; Mini-Mitter) that logged body temperature and total locomotor activity in 2.5-min increments.

Experimental Protocol

The 8 laying turkey hens, maintained on a lighting schedule of 14L:10D, were cannulated for serial bleeding and implanted with radiotransmitters two days later. Radiotelemetry monitoring of body temperature and relative activity started immediately after hens were returned to their individual cages. After overnight recovery, serial blood samples (1.0 ml) were collected hourly for 4 days, using 5 mg sodium citrate per milliliter of blood as an anticoagulant. The hens were then placed on a constant light photoschedule (24L:0D) for 8 days. Serial blood samples were collected hourly for the last 4 days (4 of 8 days) on constant light. Next the birds were returned to the 14L:10D lighting schedule, and serial blood samples continued for an additional 4 days (Table 1). Plasmas were separated from blood cells by centrifugation at 4°C and harvested. The blood cells were reconstituted with sterile saline to the original volume and returned to the hen of origin approximately every 3 h to guard against hemodilution. The presence or absence of eggs was recorded approximately every 4 h during photophases, but not at the same time each day, to randomize effects on behavior that might affect the rhythmic processes being monitored. This method of egg collection did not allow the direct comparison of body temperature to precise time of oviposition, but it allowed us to mark oviposition time within an approximate 4-h window within photophases.


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  		TABLE 1. Lighting and blood sampling schedules

Hormone Assay and Data Analysis

Concentrations of plasma LH in turkey hens were measured by RIA [20]. The LH RIA used reagents provided by John Proudman (USDA, Beltsville, MD). The intraassay and interassay coefficients of variability were 6.9% and 9.8%, respectively. The PULSAR algorithm [21] was used to determine pulses of LH (the preovulatory surge). The G values used in the PULSAR algorithm were G(1)=3.80, G(2)=2.60, G(3)=1.90, G(4)=1.50, G(5)=1.20. The assay standard deviation (SD) values used in the PULSAR analyses were (6.87 X + 6.87)/100, where X is the concentration of LH measured in an individual sample. The rhythmicity (period) of LH surges was determined by calculating the intervals between peaks (highest values within pulses identified by PULSAR analysis) of consecutive LH pulses (surges) within a sequence of eggs. Because consecutive data were available for only 4 days on any particular photoperiod, period lengths for body temperature and locomotor activity were determined by visual inspection of double-plotted actograms of individual hens using RhythmWatch (Mini-Mitter). Using the cursor line function of RhythmWatch, a best-fit line was drawn on the actograms between several consecutive activity or temperature peaks. The program used the best fit line to calculate the period. Statistical significance of periods of the LH surge, body temperature, and locomotor activity between lighting treatments were tested with Duncan's multiple-range test after repeated-measures ANOVA, with lighting treatment as the main effect.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The first LH surges of sequences under the 14L:10D lighting schedule were initiated during the early or middle portions of scotophases and terminated late during scotophases. Many of the intrasequence LH surges occurring under the 14L:10D lighting schedule were initiated late during scotophases and terminated early during photophases. A very few LH surges were initiated at the scotophase-to-photophase transition under the 14L:10D lighting schedule (Fig. 1a). The peak of the first LH surge in a sequence generally occurred before lights-on, and the peak of subsequent LH surges occurred later each day, with a lag of 0–3 h for each successive peak (Table 2, Fig. 1a). Several hens had intervals of >40 h with no LH surge, with both the 14L:10D (birds A-10, C-3, and H-14; Fig. 1a) and the 24L:0D photoschedules (birds A-10 and E-5), while the majority of LH surges had intervals of 24–30 h in all hens. The surges of LH with intervals of >40 h were associated with pause days between sequences of eggs, while the surges of LH with intervals of 24–30 h were associated with intra-sequence surges of LH. After the turkey hens were switched to constant light for 8 days, peaks of LH surges were dispersed throughout most of the 24-h subjective day and night (Table 2, Fig. 1b). The average period between consecutive surges of LH in sequences of 2 or more eggs under 14L:10D lighting increased under constant (24L:0D) lighting (Table 3). After the switch back to 14L:10D from 24L:0D, peaks of LH surges in all birds were synchronized to a window of 5 h during the late portion of the second scotophase (Table 2; Fig. 1b). Mean durations of the LH surges were not different between the 14L:10D (6.5 ± 1.4 h) and 24L:0D (6.2 ± 1.3 h) lighting schedules. The rising phase of LH surges was more rapid, accounting for about one-third of the total duration of surges, than the declining phase, accounting for the remaining two-thirds of the duration of LH surges. Also, there were no apparent changes in baseline levels of LH secretion between the 14L:10D (1.29 ± 0.31 ng/ml) and the 24L:0D (1.25 ± 0.32 ng/ml) photoschedules.



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  		FIG. 1. Preovulatory surges of LH in the 8 laying turkey hens. a) Preovulatory LH surges were initiated only during scotophases or at the scotophase/photophase interfaces when the hens were maintained on the 14L:10D photoschedule. b) After being maintained for 4 days on constant light (24L:0D), preovulatory surges of LH were initiated throughout the subjective day/night. After the hens were returned to the 14L:10D photoschedule, preovulatory surges of LH were initiated only during scotophases. N, 14L:10D scotophases; SN, subjective scotophases while the hens were exposed to the 24L:0D photoschedule, aligned with the 14L:10D scotophases. Shadowed bars indicate the scotophases (darker continuous bars) or subjective scotophases(lighter discontinuous bars), and the discontinuous bar height within each hen represents 3 ng/ml of LH. Blank parts in data lines indicate missing samples


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  		TABLE 2. Times of preovulatory LH surges in individual turkey hens exposed to different photoschedules.a


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  		TABLE 3. Periods of the preovulatory surges of LH, body temperature, and locomotor activity in turkey hens exposed to diurnal (14L:10D) or continuous light (24L:0D) photoschedules

In hens entrained to 14L:10D, body temperature started to increase about 1–3 h before lights-on, gradually increased to its highest level 1–3 h before lights-off, and then dropped quickly before lights-off (Fig. 2, a and b). As expected, this rhythm had a period of about 24 h (Fig. 2, a and b). In four birds, a second rhythm of body temperature was detected, with a supplementary spike in body temperature with an average period of 24.9 h (Table 3). When hens were placed on constant light, a peak in body temperature with an average period of 26.7 h was detected in 6 of the 8 birds. These body temperature spikes with periods of 24.9 h under 14L:10D photoperiod and 26.7 h when the turkeys were on constant light were not different from the periods observed for LH surges with these respective photoschedules. In constant light, the body temperature rhythms were less robust when detected (Fig. 2,a and b), and in 2 hens body temperature rhythms were disrupted and not apparent.



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  		FIG. 2. Comparison of the rhythms of plasma LH, body temperature, and locomotor activity in 2 laying turkey hens (a: C-3 and b: H-14) during 14L:10D and 24L:0D photoschedules. There was no increase in body temperature or locomotor activity that occurred coordinately with the preovulatory LH surges or ovipositions. As expected, body temperatures and locomotor activity rhythms peaked during photophases and decreased during the scotophases while the hens were exposed to the 14L:10D photoschedule. The hens exhibited more arrhythmic patterns of locomotor activity and body temperature while exposed to constant light (24L:0D). Returning the birds to the 14L:10D photoschedule after eight days of constant light restored rhythmicity to the changes in body temperature and locomotor activity. N, 14L:10D scotophases; SN, subjective scotophases aligned with the preceding 14L:10D scotophases while the hens were exposed to the 24L:0D photoschedule. Bars indicate the scotophases (dark bars) or subjective scotophases (light bars)

Visual inspection of locomotor actograms from birds on a 14L:10D light schedule indicated the presence of two different rhythms. All 8 hens increased their level of locomotor activity during the photophase under 14L:10D lighting, and this rhythm had a period of about 24 h. There was also a period of intense locomotor activity with a period that had the same length as that found for surges of LH with both lighting schedules (Table 3).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Longitudinal studies over several ovulatory surges of LH in undisturbed laying birds have not been reported previously, because of lack of suitable procedures for the collection of serial blood samples over several consecutive days. By modifying the previously reported procedure of Chapman et al. [19] to collect hourly blood samples, we collected serial blood samples of sufficient volume to monitor LH surges over at least 8 consecutive days, and over 12 of 16 consecutive days while switching photoschedules. The hens remained in egg production throughout the 16 days of the experiment. Thus, this is the first relatively detailed longitudinal examination of the rhythm of the preovulatory surges of LH and the relationship of this rhythm to the rhythms of body temperature and locomotor activity in an avian species. The data also allow us to examine for the first time some possible relationships between ovulatory surges of LH and sequence position in laying domestic turkey hens. Because the physiological measurements and blood sample collections were made remotely, and all hens continued ovipositions immediately after radiotransmitter implantation and throughout the periods of blood collection, we are confident that these experimental birds were only minimally stressed by the experimental procedures.

As expected, our data support the requirement of a surge of LH to induce ovulation and subsequent oviposition in the turkey hen. In the present study, no oviposition occurred without a prior surge of LH. Surges of LH did not occur in a tightly controlled rhythm, however, with equally spaced intervals between all the LH surges. With both the 14L:10D (Fig. 1a) and the 24L:0D photoschedules (Fig. 1b), some of the hens had intervals between LH surges of >40 h, while the majority of LH surges were 24–30 h apart in all hens. The surges of LH with intervals of >40 h were associated with pause days between sequences of eggs, while the surges of LH with intervals of 24–30 h were associated with intra-sequence surges of LH [22]. These data support the mathematical representation model of Etches and Schoch [23] for timing of ovulation/oviposition cycles in the chicken hen. In this model, the chicken hen ovulatory cycle is considered not to be inherently circadian, but the result of the interaction of two systems, one of which is regulated by the circadian clock either directly or indirectly, and the second by the maturation of ovarian follicles. Follicular maturation in sexually mature hens was suggested to be initiated by the previous ovulatory surge of LH [23]. For hens reaching puberty and ovulating for the first time, an alternative inducer of follicular maturation would need to be incorporated into the model, to prime the system.

In the current study, ovulatory surges of LH were the dominant event determining plasma LH levels in laying hens. No evidence for crepuscular peaks of LH, the small peaks associated with initiation of scotophases in laying chicken hens [24–26], were found in any of the 8 laying turkey hens and the over 80 ovulatory surges of LH examined in the current study. The pattern of the preovulatory surges of LH was similar to that previously determined in turkey hens sampled every 10 min [19] instead of every hour, and had a duration of about 7 h, in agreement with Chapman et al. [19].

In the current investigation, more than 80 LH surges were detected and used to examine the period of LH surges. The first LH surge in a sequence (clutch) occurred early in the scotophase, and most subsequent surges occurred with a delay of 0–3 h. This delay (or lag) occurred under both the 14L:10D and the 24L:0D photoschedules. The mechanism and anatomical location of the oscillator system, possibly associated with follicular maturation [23], that generates the rhythm with a period of approximately 26 h (14L:10D) or 28 h (24L:0D) remains to be determined.

The presence of alternating periods of light and dark affected the frequency of LH surges in two ways. First, the period between intra-sequence surges was 25.7 h on a 14L:10D lighting schedule, but it was 27.9 h on constant light. The interval between LH surges is in general agreement with Pyrzak and Siopes [27], who reported intrasequence oviposition intervals ranging between 25.7 and 27.6 h in commercial laying turkey hens throughout a production period of 160 days. Second, re-entrainment of laying turkeys to a 14L:10D lighting schedule synchronized LH surges in 7 of 8 hens (the exception being bird C-3, Fig. 1b) by the second scotophase, and in all 8 hens by the third scotophase. This re-entrainment occurred without associated pauses between sequences in 7 of 8 hens, (the exception being bird C-3, Fig. 1b). Thus, pauses may or may not be associated with re-entrainment and were not a requirement for re-entrainment.

Under long-day photoschedules such as the 14L:10D photoschedule used in the present study, it appears that the transition between the photophase and scotophase is an important signal for timing the initiation of the first LH surge in a sequence, with timing of subsequent ovulatory surges of LH determined by an interaction of the photoschedule and presence of a mature follicle in the ovarian hierarchy of laying chicken hens [23]. Since most surges of LH were initiated during scotophases, the switch from the scotophase to the photophase under the 14L:10D photoschedule appears to be associated with the initiation of LH surges during the photoperiod. In laying turkey hens, however, this restraint may be quite variable in comparison to that of laying egg-type chicken hens. Laying domestic turkey hens have been reported to have considerable variation in the 24-h distribution of ovipositions with a photoschedule of 16L:8D [27]. Some hens showed a "dispersed" pattern in the frequency distribution of ovipositions, and other hens showed a "clustered" pattern in the frequency distribution of ovipositions. The hens maintained the clustered or dispersed pattern in the frequency distribution of ovipositions throughout the 160-day production cycle [27]. This is in contrast to the domestic chicken selected for egg production, in which most of the ovipositions are clustered [22, 28]. Data on body temperature and activity rhythms were not reported by Pyrzak and Siopes [27].

Before the present investigation, no detailed studies in unrestrained birds of any species had been done to determine the profile of LH during an ovulatory cycle and its relationship to peak body temperature and onset of locomotor activity. Although the periods of the rhythms for surges of LH, peak body temperature, and onset of locomotor activity were similar, even in birds exposed to constant light, no coordinate and direct relationship between the LH surge, body temperature rhythm, and onset of locomotor activity was apparent in the turkey hens. Unlike the case of the quail [10] and the chicken [3–5, 7], no short duration spike in body temperature was associated with oviposition. There was a peak in body temperature and locomotor activity that exhibited a period similar to that of the LH surge, but the time that the peaks occurred did not coincide with surges of LH or with oviposition.

Circadian rhythms of body temperature have been investigated in chickens [3, 4, 7] quail [7–10, 29], and many other species [2]. Turkey hens are similar to other diurnal animals—exhibiting increased temperature and locomotor activity during the photophase. The periods of the locomotor activity and body temperature rhythms in the majority of the laying turkey hens exposed to constant light free-ran with a period that was greater than 24 h and that was close to the period of the preovulatory surge of LH, 27.9 h. This is similar to the period of the free-running body temperature rhythm observed under constant light conditions in laying chickens (25.2 h [7]) and in laying quail (26.7 h [10]). In these avian species, it was observed that the period of the free-running rhythms of body temperature and locomotor activity in laying hens was the same as the period of oviposition. In the present study, the free-running period of locomotor activity was estimated to be the same as the period for LH secretion. Underwood and coworkers [10] have suggested that in laying quail, dual oscillator systems (one with a relatively short free-running period of slightly less than 24 h and one with a relatively long free-running period of about 26 h) are collectively responsible for regulating body temperature and oviposition rhythms in laying hens. Ovipositions occurred only when the oscillator system with the relatively long period controlled the rhythm for body temperature. When the oscillator systems split and were both expressed in the body temperature rhythm, no eggs were oviposited until the oscillator systems became re-entrained. Under constant darkness, the body temperature rhythm free-ran with a period <24 h, and no eggs were laid. Both the eyes and the ovary were necessary to maintain free-running body temperature rhythms during constant light conditions. The data in the current study are consistent with the idea that the ovary of the laying turkey hen is an important determinant of the periods for the free-running rhythms of body temperature and locomotor activity [10]. From the present study, it is concluded that 1) the photoschedule influences the periods of the LH surge, peak body temperature, and onset of locomotor activity; and 2) a specific or direct relationship between the rhythms of LH surge, body temperature, and locomotor activity remains to be determined in laying turkey hens.


   ACKNOWLEDGMENTS
 
The authors thank Dr. John Proudman, USDA, Beltsville, MD, for donation of LH assay reagents.


   FOOTNOTES
 
First decision: 8 November 1999.

1 Salaries and research support provided by State and Federal funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University. Also supported by USDA grant 95–37203–2702, Arkansas Agricultural Experiment Station. Back

2 Correspondence: Wayne L. Bacon, Department of Animal Sciences, OARDC, 1680 Madison Ave, Wooster, OH 44691. FAX: 330 263 3949; bacon.2{at}osu.edu Back

Accepted: December 28, 1999.

Received: October 7, 1999.


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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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Biol Reprod, April 1, 2002; 66(4): 1068 - 1075.
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