Comprehensive Physiology Wiley Online Library

Daily and Seasonal Rhythms

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Daily Rhythms
1.1 Models and Mechanisms
2 Circadian Pacemaking Systems in Invertebrates
2.1 Pacemakers in the Arthropod Brain
2.2 Circadian Pacemakers Outside the Nervous System in Insects
2.3 Pacemakers in the Gastropod Retina
2.4 Multioscillator Organization
2.5 Identification of Output Pathways
3 Circadian Pacemaking Systems in Vertebrates
3.1 The Mammalian SCN
3.2 Other Circadian Oscillators in Mammals
3.3 Hypothalamic Regulation of Circadian Function in Nonmammalian Vertebrates
3.4 The Pineal Organ
3.5 Eyes as Clocks
4 Photoreceptor Localization and Mechanisms of Entrainment in Invertebrates
4.1 Photoreceptive Input: Invertebrates
4.2 Mechanisms of Regulation of Pacemaker Phase
5 Photoreceptor Localization and Mechanisms of Entrainment in Vertebrates
5.1 Identification of Photoreceptors
5.2 Mechanisms of Regulation of Pacemaker Phase
6 Seasonality in Invertebrates
6.1 Modes of Seasonality
6.2 Timing of Seasonal Cycles
6.3 Photoperiodic Time Measurement
6.4 Mechanisms of Photoperiodic Time Measurement
6.5 The Photoperiodic Timer
6.6 The Photoperiodic Counter
6.7 Anatomical Location of Timers and Counters
6.8 Photoreceptors
6.9 Circannual Rhythms
7 Seasonality in Vertebrates
7.1 Photoperiodic Time Measurement: Models and Experimental Validation
8 Physiological Mechanisms
8.1 The Pineal and Melatonin: Mammals
8.2 Mechanisms of Pineal Action
8.3 The Pineal and Melatonin: Nonmammalian Vertebrates
8.4 Photoreceptive Inputs: Mammalian
8.5 Photoreceptive Inputs: Nonmammalian
8.6 Maternal–Fetal Transfer of Photoperiodic Information
9 Circannual Rhythms
9.1 Physiological Mechanisms
10 Concluding Comments
Figure 1. Figure 1.

Effects on locomotor activity of optic lobe transplantation between groups of cockroaches raised in LD 11:11 or LD 13:13. A: Locomotor activity records showing restoration of rhythmicity after transplantation (exchange). The record begins with the animals free‐running in DD. After 4 weeks, optic lobes were exchanged, and after several weeks of low activity, rhythmicity returned in both cases. B: Plots of free‐running period of the activity rhythm after transplantation vs. period of the donor animal before surgery. Diagonal line shows values expected if pre‐ and postoperative periods were identical; CST, central standard time.

data from Page []
Figure 2. Figure 2.

Data from animals treated with localized low‐temperature pulses. Solid circles, time of activity onset for each day; open circles, projected phases of rhythms before and after pulse; lines are linear regressions; PST, Pacific standard time. Pulses were 6 h in duration and began at activity onset (CT12). In A, the intact optic lobe of an animal with one sectioned optic tract was cooled to 7°C while the isolated lobe was maintained at 25°C, and in B, the isolated lobe was cooled. Cooling the intact lobe caused a large phase‐delay, while cooling the isolated lobe had no effect. C and D illustrate the effects of a low‐temperature pulse to one lobe on the rhythm driven by the opposite lobe. C : The optic tract of the treated lobe was cut 4 days after pulse, and the subsequent rhythm, driven by the untreated lobe, was phase‐delayed by several hours. D: The optic tract of the treated lobe was sectioned 0.5 h after pulse, preventing the phase shift of the rhythm. CP, cold pulse; OTX, optic tract section.

from Page []
Figure 3. Figure 3.

Time of eclosion of Hyalophora cecropia and Antheraea pernyi moths in LD 17:7, showing effects of brain removal, transplantation of brain to abdomen, and interchange of brains between the two species. After brain exchange, the host emerges at the eclosion time characteristic of the donor species.

from Truman []
Figure 4. Figure 4.

Rhythm of sperm movement in intact gypsy moths, Lymantria dispar, (A) or in testis–upper vas deferens (UVD)–seminal vesicle complexes isolated in vitro at times indicated by arrows (B, C). In A and B, preparations were exposed to LD 16:8 (illustrated by bars at the bottom of each record), while in C, the complex was released in DD.

from Giebultowicz et al. []
Figure 5. Figure 5.

Frequency of spontaneous compound action potentials (CAPs) recorded in DD from optic nerves of Bulla gouldiana. The two eyes and attached central ganglia were isolated in vitro in artificial seawater. On the third day of the record, the two eyes were uncoupled by severing the cerebral and pedal connectives (CX). Uncoupling the two ocular pacemakers had little or no effect on the free‐running period, amplitude, or persistence of the rhythm. FASW, filtered artificial sewater.

from Page and Nalovic []
Figure 6. Figure 6.

Locomotor activity record from the cricket Teleogryllus commodus. Prior to the beginning of the experiment, one optic nerve was cut, isolating one optic lobe pacemaker from input from its compound eye (see schematic in inset). After 14 days, the animal was placed in LL. Treatment lengthens the period of the optic lobe pacemaker still attached to its eye, desynchronizing its component of activity. On day 40, that optic lobe is removed (LOBX), eliminating the long period component.

from Wiedenmann []
Figure 7. Figure 7.

Rhythms in electroretinogram (ERG) amplitude and efferent impulse activity in optic nerve of the horseshoe crab Limulus polyphemus. On the left is a schematic of the experimental arrangement. The ERG in response to a brief light pulse delivered via the light pipe was recorded from the left eye, while an electrode placed on the right optic nerve recorded efferent impulse activity. ERG amplitude (top) and efferent impulse frequency (bottom) show strongly correlated circadian rhythms.

from Barlow []
Figure 8. Figure 8.

In vitro rhythmicity in SCN explants. Upper panel: time histogram of firing frequency in a single SCN neuron. Lower panel: circadian oscillation of vasopressin release. (Upper figure; lower figure.)

adapted from Bos and Mirmiran [] adapted from Murakami et al. []
Figure 9. Figure 9.

Transplantation of SCN tissue restores rhythmicity in SCN‐lesioned hosts, and the restored rhythm bears the period of the donor. Left panel shows the effect of transplanting SCN tissues from a 20 h period mutant donor into an SCN‐lesioned wild‐type host. Right panel shows the effect of transplanting SCN tissue from a wild‐type donor (period = 24 h) into an SCN‐lesioned heterozygote mutant host. Data in the left panel have been plotted at 20 h intervals to help visualize rhythmicity. SCNX, suprachiasmatic nucleus lesion; T, transplantation.

from Ralph et al. []
Figure 10. Figure 10.

Metabolic pathway describing pineal indoleamine derivatives of tryptophan. Enzymes: (1) tryptophan hydroxylase, (2) aromatic L‐amino acid decarboxylase, (3) N‐acetyltransferase, (4) monoamine oxidase, (5) aldehyde dehydrogenase, (6) hydroxyindole‐O‐methyltransferase.

Figure 11. Figure 11.

Schema of activity patterns showing effects of pinealectomy in three classes of vertebrate. Top panel: Columba livia (pigeon), Passer domesticus (house sparrow), Sturnus vulgaris (starling). Middle panel: Sceloporus olivaceus (Texas spiny lizard), Anolis carolinensis (green anole), Sceloporus occidentalis (Western fence lizard). Lower panel: Catostomus commersoni (white sucker), Heteropneustes fossilis (catfish), Lota lota (burbot). P, pinealectomized.

Figure 12. Figure 12.

Restoration of rhythmicity by transplantation of a pineal into the eye of a pinealectomized house sparrow. Donors' light cycles are diagrammed at the top of their respective records. Pinealectomized recipients were in DD.

from Zimmerman and Menaker []
Figure 13. Figure 13.

In vitro patterns of melatonin secretion from individual pineal glands of the chicken Gallus domesticus, the green anole Anolis carolinensis, the desert iguana Dipsosaurus dorsalis, the pike Esox lucius, and the trout Salmo gairdneri. Left panels show melatonin patterns expressed under 24 h LD cycles and right panels show patterns expressed in DD.

adapted from Takahashi et al. [] adapted from Menaker and Wisner [] adapted from Janik and Menaker [] adapted from Falcon et al. [] adapted from Gern and Greenhouse []
Figure 14. Figure 14.

Melatonin infusion cycles with a period of 24.4 h entrain the feeding rhythm of a pinealectomized pigeon. The bird was held in DD and given 10 h of continuous melatonin (M) every 24.4 h.

from Chabot [])
Figure 15. Figure 15.

Both light and temperature affect the pineal melatonin rhythm of reptiles. A: Annual changes in the daily rhythm of pineal melatonin content in the tortoise Testudo hermanni held under natural conditions of photoperiod and temperature (adapted from Vivien‐Roels et al. []). B : Effects of amplitude reduction of a 24 h temprature cycle on the phase of the pineal melatonin rhythm of green anoles (Anolis carolinensis). Anoles were exposed to a temperature cycle in which the cool phase occurred during either day (left panel) or night (right panels). Pineal melatonin rhythm is entrained by the temperature cycle if the cycle is of high amplitude (32°/20°) but by the light cycle if the cycle is of low amplitude (32°/30°).

from Underwood []
Figure 16. Figure 16.

Circadian rhythms of melatonin release from individual eyecups of the African clawed frog Xenopus laevis can be reset by light. Control eyecups (dashed lines) were held in DD and experimental eyecups (solid lines) were exposed to a 6 h pulse of white light during the times indicated at the top of each figure. Light pulses presented during the subjective day were without effect, pulses during the early part of the subjective night caused a delay in the phase of the rhythm, and pulses presented during the late subjective night caused an advance in the phase of the rhythm.

Adapted from Cahill and Besharse []
Figure 17. Figure 17.

Blinding by enucleation (EX) disrupts the circadian body temperature rhythm of Japanese quail. Actogram record (left panel) shows the body temperature rhythm of a blinded quail. The bird was rhythmic when held under LD 12:12 (diagrammed at the top of the figure) but became arrhythmic after being placed into DD. Right panels show results of F‐periodogram analysis of body temperature during LD (top) or DD (bottom): the bird was rhythmic under LD but arrhythmic under DD. By contrast, unoperated birds remained rhythmic in DD .

Figure 18. Figure 18.

Extraretinal photoreceptors mediate entrainment in nonmammalian vertebrates. A: Entrainment of perch‐hopping activity of a blinded house sparrow to an LD 12:12 light cycle. At the point marked 1, the phase of the LD cycle was shifted, and at the point marked 2, the bird was exposed to DD (from Menaker []). B: Entertainment of a blinded Texas spiny lizard to an LD 12:12 light cycle.

from Underwood []
Figure 19. Figure 19.

Models of mammalian (A) and nonmammalian (B) circadian systems. LGN, lateral geniculate nucleus; SCN, suprachiasmatic nucleus; RH, retinohypothalamic; ERR, extraretinal receptor.

Figure 20. Figure 20.

Activity feedback affects the circadian pacemaker of mammals. A: Representative activity records from hamsters free‐running in LL and given pulses of induced wheel‐running (between triangles) (from Reebs et al. []. B: Phase response curves for 30 min social interaction (top panel), cage changing (middle panel), and 2 h of novelty‐induced wheel‐running in hamsters.

adapted from Mrosovsky et al. []
Figure 21. Figure 21.

Daily feeding entrains a circadian oscillator in rats. The rat was fed for 2 h (marked with arrows) under LD 14:10, then placed into DD and presented with periods of feeding ad libitum (F) or food deprivation (N). The food‐associated rhythm persists in DD and can be discerned during periods of food deprivation but not during a libitum feeding.

adapted from Clarke and Coleman []
Figure 22. Figure 22.

Sample photoperiodic response curves: (A) pupal diapause of Yponomeuta vigintipunctatus ; (B) egg diapause of Aedes atropalpus ; (C) adult diapause of Stenocranus minutus ; (D) larval diapause of Carposina niponensis .

Figure 23. Figure 23.

Effect of latitude (A) and temperature (B) on induction of larval diapause of Acronycta rumicis. The latitude from which the strain was collected and the temperature at which the experiment was conducted are given next to the appropriate photoperiodic response curve .

Figure 24. Figure 24.

Bünning's model for the photoperiodic clock. The photoperiodic time‐measuring system oscillates between periods of sensitivity (filled in part of the curve) and insensitivity to light. Upper panel depicts the rhythm free‐running under constant conditions and the two lower panels show the effects of a short day (middle panel) and a long day (bottom panel). If the days are long enough, they extend into the sensitive phase of the rhythm and a photoperiodic response is initiated.

adapted from Bünning []
Figure 25. Figure 25.

Positive and negative responses to the Nanda‐Hamner protocol. Various scotophases are combined with an 8 h photophase. Experimental LD cycles shown on bottom of figure. Positive response (dotted line) for diapause induction of the red spider mite Tetranychus urticae . Note the periodic maxima approximately 24 h apart. Negative response (solid line) for virginopara production of Megoura viciae .

Figure 26. Figure 26.

Positive and negative responses to the night‐break protocol. A short photophase (8 or 12 h) is combined with a 64 h scotophase and 1 h light break during the extended night. Experimental LD cycles shown on bottom of figure. Positive response (dotted line) for Tetranychus urticae . Note the periodic maxima approximately 24 h apart. Negative response (solid line) for Megoura viciae .

Figure 27. Figure 27.

Effects of transferring developing larvae of two species from long (L) to short (S) photoperiods, or short to long, at different stages of development. Numbers on abscissa refer to the instar during which the transfer was made. Note that the sensitive period appears to comprise the entire period of larval development and that the diapause‐averting effects of long days are greater than the diapause‐promoting effects of short days. Data for Antberaea pernyi from Tanaka and those for Ostrinia nubilalis from Beck .

Figure 28. Figure 28.

Effect of temperature on induction of pupal diapause in Sarcophaga argyrostoma at LD 10:14, showing interaction between the sensitive period and the required day number. Polygons show the proportion of each batch of larvae forming puparia each day; shaded portions of polygons represent larvae which became diapausing pupae. Note that the sensitive period and the required day number have different temperature coefficients. At high temperatures (26° and 24°C), the sensitive period is shorter than the required day number and few, if any, of the pupae enter diapause, whereas the opposite is true at lower temperatures (14° and 16°C). Inset: Effect of temperature on proportion of diapause pupae at LD 10:14. Figure and legend from Saunders .

Figure 29. Figure 29.

Gonadal response and activity patterns of Syrian hamsters exposed to resonance and T‐experiment lighting protocols. A: Upper panel shows wheel‐running patterns of hamsters entrained to four different resonance light cycles; lower panel, testicular response to these light cycles. Cycles in which light impinged on the animals' subjective night were inductive (LD 6:30, LD 6:54), whereas cycles in which light impinged only on the subjective day (LD 6:18, LD 6:42) were not (from Elliott et al. []). B: Upper panel shows wheel‐running activity of hamsters entrained to three different light cycles using 1 h light pulses. Line connects midpoints of 1 h light pulses. Lower panel shows testicular response to various T‐cycles (1 h light pulses). Photoperiodic stimulation of testicular growth is dependent on the position of the 1 h light pulse relative to the circadian system. Testicular growth occurs only if the light pulse entrains the circadian system such that light falls during subjective night (that is, the sensitive phase of Bünning's rhythm).

from Elliott []
Figure 30. Figure 30.

Action spectrum for the extraretinal photoreceptors mediating the photoperiodic response in Japanese quail; LH, luteinizing hormone.

adapted from Foster et al. []
Figure 31. Figure 31.

Maternal transfer of photoperiodic information to pups in utero. Figures show paired testes weights of Djungarian hamsters gestated and raised on the indicated photoperiods. The postnatal photoperiod is stimulatory or not depending on the photoperiod experienced by the mother during pregnancy.

adapted from Stetson et al. []
Figure 32. Figure 32.

Effects of pinealectomy and melatonin infusion on the annual reproductive cycle of sheep. Timing of high luteinizing hormone stages (horizontal solid bars) becomes uncoupled from the environment after pinealectomy (left panel), but short‐day (SD Mel, batched vertical box) and long‐day (LD Mel, open box) melatonin infusions entrain the reproductive cycle of pinealectomized ewes

adapted from Woodfill et al. []


Figure 1.

Effects on locomotor activity of optic lobe transplantation between groups of cockroaches raised in LD 11:11 or LD 13:13. A: Locomotor activity records showing restoration of rhythmicity after transplantation (exchange). The record begins with the animals free‐running in DD. After 4 weeks, optic lobes were exchanged, and after several weeks of low activity, rhythmicity returned in both cases. B: Plots of free‐running period of the activity rhythm after transplantation vs. period of the donor animal before surgery. Diagonal line shows values expected if pre‐ and postoperative periods were identical; CST, central standard time.

data from Page []


Figure 2.

Data from animals treated with localized low‐temperature pulses. Solid circles, time of activity onset for each day; open circles, projected phases of rhythms before and after pulse; lines are linear regressions; PST, Pacific standard time. Pulses were 6 h in duration and began at activity onset (CT12). In A, the intact optic lobe of an animal with one sectioned optic tract was cooled to 7°C while the isolated lobe was maintained at 25°C, and in B, the isolated lobe was cooled. Cooling the intact lobe caused a large phase‐delay, while cooling the isolated lobe had no effect. C and D illustrate the effects of a low‐temperature pulse to one lobe on the rhythm driven by the opposite lobe. C : The optic tract of the treated lobe was cut 4 days after pulse, and the subsequent rhythm, driven by the untreated lobe, was phase‐delayed by several hours. D: The optic tract of the treated lobe was sectioned 0.5 h after pulse, preventing the phase shift of the rhythm. CP, cold pulse; OTX, optic tract section.

from Page []


Figure 3.

Time of eclosion of Hyalophora cecropia and Antheraea pernyi moths in LD 17:7, showing effects of brain removal, transplantation of brain to abdomen, and interchange of brains between the two species. After brain exchange, the host emerges at the eclosion time characteristic of the donor species.

from Truman []


Figure 4.

Rhythm of sperm movement in intact gypsy moths, Lymantria dispar, (A) or in testis–upper vas deferens (UVD)–seminal vesicle complexes isolated in vitro at times indicated by arrows (B, C). In A and B, preparations were exposed to LD 16:8 (illustrated by bars at the bottom of each record), while in C, the complex was released in DD.

from Giebultowicz et al. []


Figure 5.

Frequency of spontaneous compound action potentials (CAPs) recorded in DD from optic nerves of Bulla gouldiana. The two eyes and attached central ganglia were isolated in vitro in artificial seawater. On the third day of the record, the two eyes were uncoupled by severing the cerebral and pedal connectives (CX). Uncoupling the two ocular pacemakers had little or no effect on the free‐running period, amplitude, or persistence of the rhythm. FASW, filtered artificial sewater.

from Page and Nalovic []


Figure 6.

Locomotor activity record from the cricket Teleogryllus commodus. Prior to the beginning of the experiment, one optic nerve was cut, isolating one optic lobe pacemaker from input from its compound eye (see schematic in inset). After 14 days, the animal was placed in LL. Treatment lengthens the period of the optic lobe pacemaker still attached to its eye, desynchronizing its component of activity. On day 40, that optic lobe is removed (LOBX), eliminating the long period component.

from Wiedenmann []


Figure 7.

Rhythms in electroretinogram (ERG) amplitude and efferent impulse activity in optic nerve of the horseshoe crab Limulus polyphemus. On the left is a schematic of the experimental arrangement. The ERG in response to a brief light pulse delivered via the light pipe was recorded from the left eye, while an electrode placed on the right optic nerve recorded efferent impulse activity. ERG amplitude (top) and efferent impulse frequency (bottom) show strongly correlated circadian rhythms.

from Barlow []


Figure 8.

In vitro rhythmicity in SCN explants. Upper panel: time histogram of firing frequency in a single SCN neuron. Lower panel: circadian oscillation of vasopressin release. (Upper figure; lower figure.)

adapted from Bos and Mirmiran [] adapted from Murakami et al. []


Figure 9.

Transplantation of SCN tissue restores rhythmicity in SCN‐lesioned hosts, and the restored rhythm bears the period of the donor. Left panel shows the effect of transplanting SCN tissues from a 20 h period mutant donor into an SCN‐lesioned wild‐type host. Right panel shows the effect of transplanting SCN tissue from a wild‐type donor (period = 24 h) into an SCN‐lesioned heterozygote mutant host. Data in the left panel have been plotted at 20 h intervals to help visualize rhythmicity. SCNX, suprachiasmatic nucleus lesion; T, transplantation.

from Ralph et al. []


Figure 10.

Metabolic pathway describing pineal indoleamine derivatives of tryptophan. Enzymes: (1) tryptophan hydroxylase, (2) aromatic L‐amino acid decarboxylase, (3) N‐acetyltransferase, (4) monoamine oxidase, (5) aldehyde dehydrogenase, (6) hydroxyindole‐O‐methyltransferase.



Figure 11.

Schema of activity patterns showing effects of pinealectomy in three classes of vertebrate. Top panel: Columba livia (pigeon), Passer domesticus (house sparrow), Sturnus vulgaris (starling). Middle panel: Sceloporus olivaceus (Texas spiny lizard), Anolis carolinensis (green anole), Sceloporus occidentalis (Western fence lizard). Lower panel: Catostomus commersoni (white sucker), Heteropneustes fossilis (catfish), Lota lota (burbot). P, pinealectomized.



Figure 12.

Restoration of rhythmicity by transplantation of a pineal into the eye of a pinealectomized house sparrow. Donors' light cycles are diagrammed at the top of their respective records. Pinealectomized recipients were in DD.

from Zimmerman and Menaker []


Figure 13.

In vitro patterns of melatonin secretion from individual pineal glands of the chicken Gallus domesticus, the green anole Anolis carolinensis, the desert iguana Dipsosaurus dorsalis, the pike Esox lucius, and the trout Salmo gairdneri. Left panels show melatonin patterns expressed under 24 h LD cycles and right panels show patterns expressed in DD.

adapted from Takahashi et al. [] adapted from Menaker and Wisner [] adapted from Janik and Menaker [] adapted from Falcon et al. [] adapted from Gern and Greenhouse []


Figure 14.

Melatonin infusion cycles with a period of 24.4 h entrain the feeding rhythm of a pinealectomized pigeon. The bird was held in DD and given 10 h of continuous melatonin (M) every 24.4 h.

from Chabot [])


Figure 15.

Both light and temperature affect the pineal melatonin rhythm of reptiles. A: Annual changes in the daily rhythm of pineal melatonin content in the tortoise Testudo hermanni held under natural conditions of photoperiod and temperature (adapted from Vivien‐Roels et al. []). B : Effects of amplitude reduction of a 24 h temprature cycle on the phase of the pineal melatonin rhythm of green anoles (Anolis carolinensis). Anoles were exposed to a temperature cycle in which the cool phase occurred during either day (left panel) or night (right panels). Pineal melatonin rhythm is entrained by the temperature cycle if the cycle is of high amplitude (32°/20°) but by the light cycle if the cycle is of low amplitude (32°/30°).

from Underwood []


Figure 16.

Circadian rhythms of melatonin release from individual eyecups of the African clawed frog Xenopus laevis can be reset by light. Control eyecups (dashed lines) were held in DD and experimental eyecups (solid lines) were exposed to a 6 h pulse of white light during the times indicated at the top of each figure. Light pulses presented during the subjective day were without effect, pulses during the early part of the subjective night caused a delay in the phase of the rhythm, and pulses presented during the late subjective night caused an advance in the phase of the rhythm.

Adapted from Cahill and Besharse []


Figure 17.

Blinding by enucleation (EX) disrupts the circadian body temperature rhythm of Japanese quail. Actogram record (left panel) shows the body temperature rhythm of a blinded quail. The bird was rhythmic when held under LD 12:12 (diagrammed at the top of the figure) but became arrhythmic after being placed into DD. Right panels show results of F‐periodogram analysis of body temperature during LD (top) or DD (bottom): the bird was rhythmic under LD but arrhythmic under DD. By contrast, unoperated birds remained rhythmic in DD .



Figure 18.

Extraretinal photoreceptors mediate entrainment in nonmammalian vertebrates. A: Entrainment of perch‐hopping activity of a blinded house sparrow to an LD 12:12 light cycle. At the point marked 1, the phase of the LD cycle was shifted, and at the point marked 2, the bird was exposed to DD (from Menaker []). B: Entertainment of a blinded Texas spiny lizard to an LD 12:12 light cycle.

from Underwood []


Figure 19.

Models of mammalian (A) and nonmammalian (B) circadian systems. LGN, lateral geniculate nucleus; SCN, suprachiasmatic nucleus; RH, retinohypothalamic; ERR, extraretinal receptor.



Figure 20.

Activity feedback affects the circadian pacemaker of mammals. A: Representative activity records from hamsters free‐running in LL and given pulses of induced wheel‐running (between triangles) (from Reebs et al. []. B: Phase response curves for 30 min social interaction (top panel), cage changing (middle panel), and 2 h of novelty‐induced wheel‐running in hamsters.

adapted from Mrosovsky et al. []


Figure 21.

Daily feeding entrains a circadian oscillator in rats. The rat was fed for 2 h (marked with arrows) under LD 14:10, then placed into DD and presented with periods of feeding ad libitum (F) or food deprivation (N). The food‐associated rhythm persists in DD and can be discerned during periods of food deprivation but not during a libitum feeding.

adapted from Clarke and Coleman []


Figure 22.

Sample photoperiodic response curves: (A) pupal diapause of Yponomeuta vigintipunctatus ; (B) egg diapause of Aedes atropalpus ; (C) adult diapause of Stenocranus minutus ; (D) larval diapause of Carposina niponensis .



Figure 23.

Effect of latitude (A) and temperature (B) on induction of larval diapause of Acronycta rumicis. The latitude from which the strain was collected and the temperature at which the experiment was conducted are given next to the appropriate photoperiodic response curve .



Figure 24.

Bünning's model for the photoperiodic clock. The photoperiodic time‐measuring system oscillates between periods of sensitivity (filled in part of the curve) and insensitivity to light. Upper panel depicts the rhythm free‐running under constant conditions and the two lower panels show the effects of a short day (middle panel) and a long day (bottom panel). If the days are long enough, they extend into the sensitive phase of the rhythm and a photoperiodic response is initiated.

adapted from Bünning []


Figure 25.

Positive and negative responses to the Nanda‐Hamner protocol. Various scotophases are combined with an 8 h photophase. Experimental LD cycles shown on bottom of figure. Positive response (dotted line) for diapause induction of the red spider mite Tetranychus urticae . Note the periodic maxima approximately 24 h apart. Negative response (solid line) for virginopara production of Megoura viciae .



Figure 26.

Positive and negative responses to the night‐break protocol. A short photophase (8 or 12 h) is combined with a 64 h scotophase and 1 h light break during the extended night. Experimental LD cycles shown on bottom of figure. Positive response (dotted line) for Tetranychus urticae . Note the periodic maxima approximately 24 h apart. Negative response (solid line) for Megoura viciae .



Figure 27.

Effects of transferring developing larvae of two species from long (L) to short (S) photoperiods, or short to long, at different stages of development. Numbers on abscissa refer to the instar during which the transfer was made. Note that the sensitive period appears to comprise the entire period of larval development and that the diapause‐averting effects of long days are greater than the diapause‐promoting effects of short days. Data for Antberaea pernyi from Tanaka and those for Ostrinia nubilalis from Beck .



Figure 28.

Effect of temperature on induction of pupal diapause in Sarcophaga argyrostoma at LD 10:14, showing interaction between the sensitive period and the required day number. Polygons show the proportion of each batch of larvae forming puparia each day; shaded portions of polygons represent larvae which became diapausing pupae. Note that the sensitive period and the required day number have different temperature coefficients. At high temperatures (26° and 24°C), the sensitive period is shorter than the required day number and few, if any, of the pupae enter diapause, whereas the opposite is true at lower temperatures (14° and 16°C). Inset: Effect of temperature on proportion of diapause pupae at LD 10:14. Figure and legend from Saunders .



Figure 29.

Gonadal response and activity patterns of Syrian hamsters exposed to resonance and T‐experiment lighting protocols. A: Upper panel shows wheel‐running patterns of hamsters entrained to four different resonance light cycles; lower panel, testicular response to these light cycles. Cycles in which light impinged on the animals' subjective night were inductive (LD 6:30, LD 6:54), whereas cycles in which light impinged only on the subjective day (LD 6:18, LD 6:42) were not (from Elliott et al. []). B: Upper panel shows wheel‐running activity of hamsters entrained to three different light cycles using 1 h light pulses. Line connects midpoints of 1 h light pulses. Lower panel shows testicular response to various T‐cycles (1 h light pulses). Photoperiodic stimulation of testicular growth is dependent on the position of the 1 h light pulse relative to the circadian system. Testicular growth occurs only if the light pulse entrains the circadian system such that light falls during subjective night (that is, the sensitive phase of Bünning's rhythm).

from Elliott []


Figure 30.

Action spectrum for the extraretinal photoreceptors mediating the photoperiodic response in Japanese quail; LH, luteinizing hormone.

adapted from Foster et al. []


Figure 31.

Maternal transfer of photoperiodic information to pups in utero. Figures show paired testes weights of Djungarian hamsters gestated and raised on the indicated photoperiods. The postnatal photoperiod is stimulatory or not depending on the photoperiod experienced by the mother during pregnancy.

adapted from Stetson et al. []


Figure 32.

Effects of pinealectomy and melatonin infusion on the annual reproductive cycle of sheep. Timing of high luteinizing hormone stages (horizontal solid bars) becomes uncoupled from the environment after pinealectomy (left panel), but short‐day (SD Mel, batched vertical box) and long‐day (LD Mel, open box) melatonin infusions entrain the reproductive cycle of pinealectomized ewes

adapted from Woodfill et al. []
References
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Herbert A. Underwood, Gary T. Wassmer, Terry L. Page. Daily and Seasonal Rhythms. Compr Physiol 2011, Supplement 30: Handbook of Physiology, Comparative Physiology: 1653-1763. First published in print 1997. doi: 10.1002/cphy.cp130224