Circadian Ovulatory Rhythms in Japanese Quail: Role of Ocular and Extraocular Pacemakers

Abstract

Previous studies have shown that the circadian system of Japanese quail is composed of multiple photic inputs and multiple oscillators. Among these are extraretinal photoreceptors that mediate both circadian and photoperiodic responses and circadian pacemakers in the eyes that, via neural and hormonal outputs, help to maintain rhythmicity of central circadian clocks (presumably located in the suprachiasmatic area of the hypothalamus). Furthermore, a component of the central circadian system is influenced by reproductive hormones. Under certain conditions, the circadian system of female quail can be induced to split into two circadian components: one driven by ocular pacemakers and one driven by feedback from reproductive hormones. Importantly, ovulation is either inhibited or permitted as these two oscillators (or sets of oscillators) constantly change internal phase relationships with each other, suggesting an "internal coincidence" mechanism in the control of ovulation. The oviposition patterns of quail in light-dark (LD) cycles also support an internal coincidence mechanism. The authors tested the hypothesis that the ocular pacemakers are an important component of an internal coincidence mechanism controlling ovulation by examinig the effects of blinding by complete eye removal (EX), and the effects of eye-patching, on the body temperature and oviposition patterns of quail exposed to 24-h LD cycles. They also examined the effects of EX on quail exposed to continuous light (LL) and to continuous darkness (DD). Neither EX nor eye-patching affected the oviposition patterns of birds in LD. Furthermore, robust body temperature and oviposition rhythms continued in EX birds in LL, but body temperature became arrhythmic in DD with the cessation of ovulation. The results do not show a role for ocular pacemakers in the control of ovulation, but they do support the hypotheses that (1) entrainment of the central oscillators by extraretinally perceived light is sufficient to preserve a normal ovulatory pattern in LD in the absence of the ocular pacemakers, and (2) in LL, feedback of reproductive hormones onto the central oscillators is sufficient to organize the circadian system even in the absence of the ocular pacemakers. Whether or not the ocular pacemakers are normally involved in the control of ovulation is still an open question.

Extended Laying Interval of Ultimate Eggs of the Eastern Bluebird

“…the period is determined proximately by photoperiod (Opel 1966, Phillips et al 1985, Zivkovic et al 2000 and perhaps ultimately by diel patterns of food availability, predation, or weather (Wiebe and Martin 1995). If females have trouble acquiring resources for an egg, then the egg takes longer to travel down the oviduct, and if that delay pushes its laying out of the open period then ovulation for a subsequent egg will not be stimulated.…”

“…If a last-laid egg is experimentally removed, it is possible that a female will not be able to lay another the next day because she will not have ovulated, may have moved out of the permissive zone, and/or her oviduct may already be regressing (Williams and Ames 2004). If she does replace the egg, it might be after a delay, extending the laying period (Zivkovic et al 2000). Therefore, identifying a clutch as complete on a basis other than hindsight could facilitate field experiments aimed at reducing clutch size, extending the laying period, or generating gaps in laying (i.e., attempting to generate embryos/young of different ages).…”

“…For example, many Passeriformes generally lay in the early morning, while some Galliformes (e.g., quail) lay in the afternoon (Wiebe andMartin 1995, Zivkovic et al 2000). Yet, on closer examination, interspecific variation in laying intervals and the time of day of laying have been evident (Watson et al1993, Wiebe andMartin 1995), and, in intraspecific studies, it is possible to manipulate laying intervals and subsequent clutch size, as through food supplementation (Aparicio 1994) and changes in photoperiod in the laboratory (Zivkovic et al 2000).…”

“…The response of birds to removal/addition experiments has been described as some species laying to achieve a particular clutch size (indeterminate layer) and others laying a particular number of eggs (determinate layer). Although phylogenetic constraints play a role in the determination of clutch size (Yom-Tov 1987, Postma andvan Noordwijk 2005), the termination of laying has been attributed to (1) extrinsic cues that trigger the cessation of laying (e.g., the tactile stimulation of the brood patch; Haywood 1993a, b), (2) nutrient limitations on egg production (Houston et al 2007), and (3) hormonal and circadian regulation of clutch size (Haywood 1993a, b, Zivkovic et al 2000. If any of these mechanisms play proximate roles in…”

“…The sequential pattern of egg formation and laying can result in variation in parental allocations among embryos (Lipar et al 1999), size differences among offspring (Clotfelter et al 2000), determining clutch size in wild birds, detailed patterns of laying may complement insights gained from egg-removal and addition experiments. For example, discerning the potential role of the permissive zone (Opel 1966, Zivkovic et al 2000 in the termination of egg laying requires, among other things, specifics on the time of day of egg laying. We used video cameras to examine the time of laying during the day and intervals between eggs in the Eastern Bluebird (Sialia sialis).…”