Indian 10urnal of Experimental Biology

Vol. 37, November 1999, pp . 1053- 1064

Review Article

Light sensitivity of the photoperiodic response system in higher

vertebrates: Wavelength and intensity effects
Vinod Kumar & Sangeeta Rani
Department of Zoology, University of Lucknow, Lucknow 226 007 , India
Most species use daily li ght in one way or the other in regulation of their short and/ or long term activities. Li ght is
perceived by pigment(s) present in the retinal (RP) and/ or extra-retinal photoreceptors (ERPs). ERPs may be located at
vari ous sites in the body but in non-mammalian vertebrates they are found predominantl y in the pineal body and hypoth alamic region of the brain ,- Li gh t radiations directly penetrate brain ti ssues to reach and stimul atc the hypothalami c (dcepbrain) photoreceptors. How does li ght information fin all y reach to the clock is not fully understood in man y ve rtebrate
groups? In mammals, however, the light informati on from the retina to the clock (the hypoth alami c suprachiasmatic nu cl ei,
SeN) is rel ayed throu gh the retino-hypothalamic tract (RHT) which ori ginates from the retinal gangli on cell s, and th rough
the geniculo-hypothalami c tract (G HT) which origi nates from the photically respon sive cells of a porti on of the lat eral genicul ate nucleus (LGN), called the intergeni cu late leanet (lGL).
A response to light (the photoperiodic respo nse) is the result of the interpretation of li ght information by the photoperiodic system. Apart from the duration , the animals use the gradual shi fts in the intensity and wavelength of daily li ght to
regu late thei r photoperiodic clock system. The wavelengths to which photoreceptors are maximall y sensiti ve or the wavelengths which have greater access to the photoreceptors can induce a maximal response. There can also be differenti al effects of wavelength and intensit y of light on circadian proc es s (e~) involved in the entrainment and induction of the photoperiodic clock. This may have some adapti ve implicat ion s. Entrainment to dail y light-dark (LD) cyc le may be achieved at
dawn or dusk , depending whether the animal is day- or night-acti ve, when there is relatively low inten sity of li ght. By CO Il tras t, photoperiodic inducti on in many speci es occurs durin g long days of spri ng and summer when plent y of da yli ght at
hi gher inten sity is avail able later in the day.

The thru st of evolutionary bio logy is that the changes

in nature produce biological stresses that lead to either adaptation or ex tin ction of a gi ven species .
Adaptive advantage is the key to synchroni zati on of
physiological and behavioural activities to environmental factors such that these occur at the most favourable time of the year. Natural selec ti on ensures
that th e organi sms choose environmental cue(s) th at
is(are) predi ctable and that help them anti cipate th e
"appropriate season" . At a given latitude, the annual
variation in daily light (day length , photoperiod ) is
extremely predictable and used by Illost species in
one way or the other in regulation of their short and/
or long term activities. Apart from the durati on, oth er
important characteri stics of dai ly li ght are its quantity
(light intensity) and quali ty (colour, spectra l composition). The gradua l al terati ons in th e intensit y an d
wave length of li ght that occur in natural cond itions
can also provide reliabl e informati on about th e timeof-day and/or the ti me-of- year. The intensity refers to
the amount of photons avai lab le in the li ght source,
and the co lour is the sensat ion ex peri enced as a resul t
of activati on of certain classes of photoreceptors by

selected wave lengths of visible li ght spectrum (380 to

760 nm ; commonly expressed as VIBGYOR wh ere
violet to blue corres pond to sh ort wave lengths, gree n
and yell ow to mid wave lengths and red to long
wavelengths) .
It is important that day length is percei ved and
measui'ed correctly before it is transduced to effect an
appropriate photoperiod -induced chan ge. Thus, th e
photoperiodic inducti on (for example, gonada l
growth, bod y fatt ening etc.) is the res ult of li ghtind uced effects on th e wh ole photoperi od ic machi nery (the photoperi odic response sys tem) of an ani ma l
that can be very specific depend ing upon th e wavelengt h (spectrum, colour) and intensity o r li ght. In
thi s arti cl e, we aim to summarize bri efl y th e prog ress
of research th at has been mad e in stud yin g th e effects
of wavelength and intensity of li ght on photoperi odic
regu lati on of ph ys iological fun cti ons, based on studies in hi gher vertebrates with spec ial emphasis placed
on birds and mammals. In particul ar, we wil l restrict
ourselves to two photoperi od ic e\'ents , th e photorece ption and th e photoperi odi c time measurement , in
thi s communication . At th e end , we gtve a brief ac-

1054

INDIAN J EXP BIOL, NOVEMB ER 1999

count of light effects on other (non-reproductive) circadian functions as an overview of light sensitivity of
the circadian system in organisms.

Photoreception
The environmental illumination useful for animal
physiology is perceived by at least two forms of
photoreceptor: visual and non-visual photoreceptors.
Whereas visual photoreceptors function as image detectors, non-visual photoreceptors detect photoperiod
and sync hronize physiology with respect to environmental time. Thus, the two divergent sensory tasks
seem to have led to the evolution of specialized photoreceptor systems I . In contrast to visual, our understanding of anatomy, physiology and biochemistry of
the non-visual photoreceptor system is poor. Here, we
briefly focus upon the non-visual photoreceptor
which are important for the photoperiodic timing.
In vertebrates, light used to synchronize physiology with respect to environmental time is perceived
by pigment(s) in the photoreceptors present in the eye
(retinal photoreceptors, RP), pineal and/or extraretinal (extrapinea l) structures (extra-retinal photoreceptors, ERPs). In general, photopigments can be
characterized by their biochemi stry and by the
physiological responses they medi ate. All vertebrate
photopigments characterized so far are remarkabl y
similar in consisting of an opsin protein coupl ed to a
chromophore derived from a n II-cis form of vita min
A retinaldehyde 2a .b .c .
In non-mammalian vertebrates, the pinea l organ is
an important photorece ptive system. Th e pineal complex of many fish and amphibi ans contain pinealocytes which have ultrastructural prope rti es th at resemble retinal photo rece ptors and show li ght depend ent e lectri ca l act ivity, and thu s act as ph otoreceptors
(see revi e w by Dodt and M e iss l'). In reptiles, pinealocytes act photoreceptors, and it has been show n in
the isolated pinea l o f Ano/is li zard s th at me latonin
production can be e ntrain ed to the li ght:dark (LD)
4
cycle . Spec tra l sens itivity of pin eal ph otoreceptor
may be spec ies specific but, in gene ral, the peak sensitivities o f most ph otoreceptors ran ge in between
520-530 nm .
Ph otoreception with respect to light regulated
phys io logical func ti ons has bee n ex te nsive ly stud ied
in birds. As is tru e of mam ma ls, retinal ill umination
in birds reac hing the putative cloc k site in th e hypoth alamu s is re layed through th e re ti no-h ypoth ala mi c
tract (RHT)5 , a [rac t of nerve f ibe rs ori bain at in ba fro m

the retinal ganglion cells . The prec ise rol e o f RHTmediated photic information in avian photope riodism
is unclear given the fact that photi c e ffect s onto re67
productive axis survive in the enucleated birds . The
pineal in birds differ from visual ph otoreceptors and
the pineal photoreceptors of the lowe r verte brates in
lacking the ordered cytoplasmic laminae and pe r0
forms photoreceptive and c lock functions s. . Chicken
pineal is the most studied photoreceptive system . It
contains a photoreceptive molecule that receives e nvironmental light signal and transmit s this signal to
the oscillator. This photoreceptive molecule is suggested to be rhodopsin like, although the action spectrum of this molecule as obtained by inhibitory effects of light on the N-acetyl transferase (NAT), th e
enzyme involved in the melatonin synth esis, was
broader in shape (maximum at 500520 nm) than that
of the absorpt ion spectrum of rhodopsin . Immunohistochemical studies show rhodops in-like immunoreactivity in bird pineal cell s (e. g . in the chicken
and quail), but the identity of pineal pigme nt is still
lO
unclear. Recent molecular studies (for exampl e see )
have identified pinopsin (a major pigment ) and iodopsin (a minor pigment) as the pinea l pigme nt , and
still the existence of a third or more photorecepti ve
molecule cannot be ruled out. Take n toge th e r, vari ous
lines of e vide nce seem to sugges t th at th e p in eal and
retinal photoreceptors may ha ve ph oto-transdu cti on
(re lay of photic information) cascades similar to eac h
othe r, although the y may not have iden tical path ways .
Apart from the retina and pin eal , th e brain in nonmammali a n ve rtebrates contains photorece pto rs that
are involved in transfer of li ght information to the
photoperi odi c res ponse syste m. ERPs are s ituated in
the brain (call ed encephalic ph otorece ptors or dee pbrain ph otoreceptors, DBPs) , parti c ularl y in th e hypothalami c regions. Avail abl e data ra ise th e poss ib il ity th at th e re a rc se ve ral types o f ph otorece pt or ph otopi gme nt s (cone-like, rod-like or diffe re nt fro m
both), and de pendin g on speci es at leas t two types o f
photoreceptor ce ll : CSF-containing ne uron s (found in
larval lamprey, re ptil es and bird s) a nd c lass ica l ne urosecretory neurons within th e nu c le us magnoce llu lari s preoptic us (NMPO; fi sh an d a mphibian s) (for
more deta il s see l I) .
ERPs have bee n imp li ca ted in scve ra l d iffe rc nt a reas of ph ysi o logy but , in ali species ex ami ned. they
pl ay a c riti ca l role in the regul ati on o f c ircadia n an d
re produ cti ve responses to li ght. In re ptiles, they ha ve
been show n medi atin g ex c lu s ive ly th e c ircad ia n c n-

KUM AR & RANI; WAV ELENGTH AN D INTENSITY EFFECTS

trainment since blinded, pinealectomi zed and parietal

eye (if present) removed lizards are readily entrainab le to light:dark cycle ' 2 . ERPs are qu ite sensitive
since lizards can be entrained to light as dim as I
lux ' 3 . A more detailed study of ex traretinal photoreception has been done on AnaUs lizards (A nalis caroIinensis)14 . In this spec ies, Cerebrospinal fluid (CSF)contacting neurons in th e septal area of th e brain represent the ERPs and bind to anti-opsin anti serum.
Further, the anti-opsin antibodies recogn ized a 40 kD
protein in ocul ar, pineal and onl y in septa l brain areas, and the anterior brain of Anolis contai ned specific retinoids ( II-cis and all-trans-retinoids) associated with phototransduction. In birds, ERPs have
been suggested to be located in the CSF-contacting
neurons within the septal and tuberal areas of the
brain 's.
The following table summarizes the important
characteristics of retinal and ex traretinal photoreceptor cell s measured in terms of light sense of these receptorsl 6:
Characteri sti cs

Extraretinal

Retinal

Image analys is
Ontogeny
Mode of transdu ct ion
Refractory periods
Cave dwelling
Function

poor or absent
early
neural and humoral
well establi shes
survival
orientati on in time

prominent
late
ne ural (humoral ?)
absent
degeneration
orientation in space

It is probable that extraretinal photoreception existed prior to the evolution of lateral eyes since the
most primitive eyeless organisms definitely utilized
the daily LD cycle as an entraining stimulus. Imageforming vision needs a specialised structure like an
eye, irradiance detection for the photoentrainment
does not require any such specialised structure.
Rather, these irradiance detecting encephalic photoreceptors could be closely associated with their effector
system within the brain. The fact that most primitive
vertebrate brain of lampreys contains di stinct population of photoreceptors which are associated with different behavioural and physiological functions but all
they are labelled by one or more of the anti-opsin antibodies 2b (indicating the presence of opsin, VA opsin
(vertebrate ancient opsin), photopigment) favour for
early evolution of encephalic photoreceptors. The
eyes were "wired" into the photoreceptive system
when they evolved . There may be some selective advantages for having extraretinal photoreception since
ERPs survived even after evolution of eyes in major-

1055

ity of vertebrates. It appears th at retin al and extra

photoreceptors ex tract different kinds of informati on
from the light envi ronment, e.g. parametri c (co nti nuous action occ urrin g throughout li ght phase of an LD
cycle) versus non-parametri c (disco ntinuous acti on
occurring at LD or DL tran siti ons . Alternatively, it
may be th at ERPs are integral part of th e timin g device (c lock) itself and therefore evo luti onary conserved as its cell component: These considerat ions
however raise an important questi on: wh y mammals
apparentl y do not possess ERPs? There is no convincing explanation for thi s riddl e, but there can be
some speculations. One of these co uld be th at mammal s apparently evolved from ni ght acti ve mammallike reptiles which natura ll y hid durin g th e day in
dark places, and thus, the developing brain of these
animals probably did not ex peri ence sufficie nt ligh t
during critical periods of its ontogeny. The abse nce of
specific stimuli during critical peri od of ontogeny can
result the loss of function that has to be induced by
the stimuli . ERPs which deve lop early in ontogeny
degenerated whereas RP cells which develop late in
ontogeny survived since they probably rece ived sufficient light. RPs took over visual function in a reshaped visual system and photic control of endogenous rhythmicity.
In mammals, photoreception occurs exc lusively
through the eyes (the retina). However, one recent
study by Campbell and Murph yl 7" suggests that ex traocular exposure (behind the knee) may cau se
phase-shifts of the circadian clock in human s. Thi s
important result which challenged the belief that adu lt
mammal s are incapable of using ERPs for th e circadian phototransduction , however, could not be
proved by another similar study of Lockley el al. 17b
in wh ich extraocular exposure (be hind the knee) of
human.s to light failed to suppress the circadian
rhythm of melatonin secretion , a direct function of th e
circadian system. So, unless replicated by ot he,' laboratories, the extraocular circadian phototransduction
in mammals is to be considered with a lot of caution.
At present, retinal phototransduction remains only
effective pathway for photic regulation of circadian
system in mammals. The exact ocular (ret inal) photoreceptors involved are not known since ve ry recentl y
Lucas et 01.1 8 found that the mice which had no rods
or cones (rdlrd cl mi ce, the strain of mice that had
combined the rd mutation and a transgeni c ablation of
cones) showed normal suppress ion of pineal melatonin in response to monochromat ic li ght of wave-

1056

INDI A N J EXP BIOL, NOVEMBER 1999

length 509 nm; thi s finding clearl y suggests that

mammals have additi onal ocu lar photoreceptors
whic h they use in the regulati on of their photoperi od ic timing. The photic informati on from eyes to the
suprachiasmatic nucleus (SeN), the important clock
site in mammals that is located in the anterior hypothalamus is conveyed through RHT which is composed of very thinly mye linated ret inal ganglion cell
axons th at emerge from the chiasma to terminate in
l9
the ventral SeN in rats and th e entire SeN in Syrian
2o
hamster . The second photic pathway reaching SeN
is the genicul c-hypothalamic tract (GHT) which
ori gi nates in photically responsive cell s in a porti on
of the lateral gen icu late nucleus (LGN) ca lled th e
intergenicu late leaflet (IGL)21. Treep et a/. 22 clearly
de monstrated that stimul ati on in the IGL region antidromically activates a retinal projection that reaches
both the IGL and the SeN via co ll ateral fibers. The
relay of light is medi ated chemicall y by synaptic release of glutamate and other excitatory amino ac ids
(EAA) which act through specific EAA receptors (see
Kumar et at. 2J for details) as well as of a host of neurotransmitters like neuropeptide Y (NPY), enkephaline (ENK) etc .. A simple schematic di agram of how
photic information is relayed to the clock components
in mammal s is shown in Fig. I.
Action spectrum studies help in characterization of
pineal and ERPs. All opsin and I I-cis retinaldehyde
based photopigme nts have a characteristic shape to
their absorbance and action spectra even th ough they
may have a very different wavelength of maximum
sensitivity. An action spect rur.l for ERPs in Japanese
quail was similar to the acti on spectra of pineal responses although the receptors in vo lved were clearly
not in the pineal24 . It may be noted however th at the
studies on action spectra of light provide a basis for

findin g the pigment(s) res ponsibl e for a spec ific

photoresponse, but they do not necessarily te ll ho w
many photoreceptors are in volved. Bra in pholoreceptors were discovered more than five decades ago
by Benoit and hi s colleagues but the acti on spect ra
for the photoperiodic responses have bee n studied
on ly for a few species as yet (see espec iall /'ls).
In non-mammalian vertebrates, the retina and pi neal organ may have both photorecepti ve and ti memeasurin g capabilities. Whether pho torecepti on by
these two structures is meant for the entrainment of
their own osc illator or th ey furth er re la y the photi c
informati on to the brain (hypothalami c) pacemaker is
uncl ear. This is important in view of th e fact that
enucleated (both eyes surgica lIy removed) house
sparrows respo nd fu ll y to stimul atory effects (e.g .
photoinduced gonadal growth) of light , and circadian
locomotor acti vit y rhythms in blind sparrows ca n entrain to LD cyc les . Also, pinealectomy does not impair photoperiodi c inductio n in many species (see
review29 .3o) and pinea lectomi zed birds show onl y
gradual loss of circad ian rh yt hmi ci ty of locomotor
activity (see review~ I ). These clear y argue for th e
principal ro le of hypoth alam ic photorece ptors in the
circad ian photoresponse system at least in bird s.
Furthermore, whether th ese different orga ns of photorecepti on work synerges ti call y or work independen tl y
remains an open questi on. A co nservat ive exp lanati on
at the moment could be that the photorecepti on by th e
pineal and eye (retina) pl aya modul ating ro le on th e
circadian pacemaking system located e lsewhere in the
brain which may include the photoreceptor, the clock
or both.
How do DBPs communicate with the photoperiodic machinery is not absolutely clear') In birds , however, DBPs co-express prote ins characteri st ics of

Fig. I-A schematic diagram of photic relay from the retina to the clock components in mammals. EAA - excilatory am in o acids ; E l K enkephaline; LGN - lateral genicu late nucleus; NPY - neuro peptide Y ; SeN - suprach ias matic nu cle us

1057

KUMAR & RANI: WAVELE NGTH AND INTENSITY EFFECTS

retinal photoreceptors, as we ll as vasoactive-intestinal

polypeptide (VIP)! ). These putative opsi n-ex press ing
DBP have fibers lying in c lose appos ition wit h go nadotropin releasing hormone (GnRH)-expressing cell s
which mi ght mean that they communicate with GnRH
neurons, and vice ve rsa. There is also ev idence of
seasonal variation in these brain peptides: ex press ion
of VIP-like immunoreactivity is highest in photorefractory an imals while GnRH-li ke immunoreactivity
is hi ghest in photosensitive birds . Also, expression of
these brain peptides is correlated wit h changes in
plasma prolact in and lutei ni zing hormone (LH) . All
this might be taken to suggest th at putative DBP are
in vo lved someho w in med iating the photoperiodinduced seasonal cyclicity. How is the relay of light
information from photoreceptors to the clock components done, which is so crucial for the measurement
of day length, is not known ? The issue may be more
clear once the definiti ve clock sites in av ian brain
become known.
The direct effect s of light intensity on vertebrate
photoreceptors have not been monitored. A large
number of studies have however investigated the intensity affects on reprodu cti ve and non-reproducti ve
functions that are mediated by photoreceptors. The
spectrum of light intensity effects includes the effects
on food and feeding, reproduction , immune system to
general health 32 .J3 . Both low and high light inten siti es
can cause con vulsions and death in the African
weaver finch 34 . Since the demonstration of the role of
light intensity in the manipUlation of starling's reproductive response to day length 3), the effects of intensity on photosexual response has been studied in
ds, b0 bwh'Ite qual'1 ''6 , ] apanese quat'1,7.,9
some bIr
- - , d0 .
k
40 d
.
d
k4!
h
mestlc tur ey , omestlc uc , ouse sparrow 42-4';-,
white-crowned sparrow46 . Of these, the studies on
house sparrow are most comprehensive.
A photoperiodic response is maximally induced by
the wavelength(s) at which photoreceptor(s) mediating such effect is most sensitive or by wavelengths
which have greater access to the photoreceptors.
Photoreceptors seem to have precise spectral sensitivity. When blackheaded bunting were su bj ected to a
stimulatory day length of 13L: I I D in white, green
(528 nm) and red (654 nm) colours at 100 lux intensity, photostimulation (weight gain and testis growth)
occurred in all groups but the tes tes were significantl y
larger in birds that were ex posed to red light (Fi g. 2).
Similar respon ses occur in other bird species (see
Oishi and Lauber37 for detail s). In mammals too, the

wave length - and intensity-depende nt photoperi odic

inducti on has been reported. In th e hamster. I hr
pulse of green, blue or near ultrav iolet light. but not
red or yellow li ght, presented to animals during dark
period bl ocked the co llapse of the reprodu ct ive system. Also, at equal irrad iances diffe rent bandwidth s
of light have different effects on short phot operi od
induced collapse of th e hamster reproductive system47 .48. The effects of light spectrum have been reported in lower ve rtebrates as we ll. Jos hi and
Udaykumar49 found that th e effects on ovari an follicul ar kin eti cs in th e fro g, Raila cY({llophlyclis , were
max imum of red ligh t, foll owed by ye ll ow and gree n
li ght.
Photoperiodic t.ime measurement (PTM , the photoperiodic clock)
The precision with which seasonal res ponses are
temporally organized clearl y suggests that th ey are
regu lated by a clock mec hani sm that is fine-tuned by
the light environment. Expe rimen tal ev idence conclude that endogenous circa-rhythms , sy nchroni zed to
time-of-day (circadian rh ythm ; circa - about , dies day) and/ or time-of-year (ci rcannual rhythm ; circa about, annum - year), help measure th e length of th e
day. It is believed that the entrainment and induct ion
of the circadian rh ythm of photoperi odi c ph otosens i100

80

M
E

.s 60
QJ

E
:::l

~ 40

:;:;
I/)

CIl

I-

20

O~------------+-~~~~

35

Days
Fig. 2-Testicular re~po n sc of th c photoscll siti \ 'C blackheaded
bunting (ElI1beriza lIleln ll OCefJhala) cxposed to a I()ng photopel iod
( 13L: lID : L: 100 Ix. D: 0 Ix) of while (w). green (g). and red (r)
ligh t. The un stimul ated birds werc maintained und er sha n days
ensurin g their sensitivity to light. Note that red li ght group indi cates significantl y larger response cOlllpared with white ( w )
and/or green (g) li ght group (red rawn from KUlllar and Rani ")

1058

INDIAN J EXP BIOL, NOVEMBER 1999

tivity (CRPP) by photoperiod are key to the timekeeping process. Intensity and wavelength are the
characteristics of 24 hr daily cycle of illumination
that are important to the photoperiodic entrainment
and induction of CRPP.
The models
Pittendrigh 50 has summarized in theoretical model s
how could the circadian organization be involved in
PTM 50-52 . Bri efl y, a photoperiodic clock is circadian
and operates as if there is coincidence between phases
of the photoperiodic oscillator and th e light:dark (LD)
cycle - the external coincidence, or there is interaction between two or more independent oscillators as a
result of expos ure to LD cycle- the internal coincidence (Fig. 3). The central feature of the external coincidence model, as originally conceived by Erwin
Buenning53 and later widely used to explain the photoperiodic phenomena, is that light exerts phasecontrol over the circadian osci llation to enable its
dual actions, of phasing th e oscillation and of effecting the photoperiodic induction by extending (or not
extending) into the photoinducible phase (<I>i), located early in the subjective night. Remarkably, so
much experimental effort has gone into testing the
Buenning hypothesis without making any significant
achievement in unraveling the mechanism how light
exerts phase control over CRPP. Furthermore, there
can be species variation in the ability of <I>i to free-

run in constant condition (e.g. constant darkn ess. DD)

and such differences raise th e qu estion as to wheth er
the photoperi odic clocks are gen uin e ly and qual itatively different between the speci es. C learly, in species like AlIa/is li zards and Japanese quail the circadian system drivin g <I>i is weak ly se lf-s ustaining,
but in species like golden hamste r, white-crowned
sparrow and blackheaded bunting the c ircad ian system driving <l>i is strongly se lf-susta ining. These aspects of the photoperiodic clock ha ve been discussed
in detail by Kumar and Follett:>".
CRPP: Phasic effects
Relati ve ly less is known concern ing spectral se nsi tivity of phasic components of circad ian effec ts of
light. Indirect ev idence from a few spec ies noneth eless show that light intens ity at a threshold is required
for the photoperiodic entrainment and induction of
the photoperi od ic clock mediating full go nadal
growth and develop ment. In the bunting (ElIlberi-:,{{
melanocephala and Emberiza brulliceps) held in a
skeleton photoschedul e, the rate of gonadal growth is
very slow in 100 lux li gh t intensity 55.56 . Also. in
Japanese quail I hr ni gh t-interrupti on at an intensity
of 850 lux stimulates significan tly large r (P<0.02)
testes than those exposed to at 250 lux.1,} There is
strong evidence supporting the role of li ght intensity
as synchronizer of clock-regulated long term seasonal
responses . At equater where the change in day lengt h
Long day

External
coincidence

Internal
. coincidence

Days

Days

Fig. 3-Models of mechanis m(s) involved in the photope riodic time - measureme nt in lon g day a nim als. In th e external coincidence
model (A), coincidence of light with the photo indu ci ble ph ase (<I>i ), which fa il s early in the night, leads to a photope riodic respon se under long days . In internal coincidence, photoperiodic stimUlation under long days occurs due to changes in the phase relationship (and
thereby coincidence) between two circadian oscillators (B). Non -stimulation under short days is due to non- coincidence of li ght with th e
<I>i (external coineidence- Fig. 3A), or due to a different relationship between two or more circadian oscillators (in te rnal coincidencc54
Fig. 3 B) (redrawn from Kumar and Follett ).

1059

KUM AR & RAN I: WAVELENGTH AND INTENS ITY EFFECTS

over the season is so small that it cannot be used as a

reliable photoperiodic index of the changing season,
animals seem to rely on the change in light intensity
over the season to regulate their responses. Simulating high and low intensity cycle of the nature, Gwin57
ner and Scheuerlein have demon strated that light
intensity could reliably be used by an equatorial avian
species in synchronizing its annual reproductive cycle.
We have for the first time attempted elucidating
the phasic effects on CRPP of light intensity and light
spectrum in birds using a skeleton paradigm. Inductive effects of I hr light pulse in a skeleton photoperiod (6L:6D: I L: liD) were intensity- and spectrumdependent. At 50- and 100 lux intensities of two different wavelengths (green - 528 nm, and red - 654
nm) , 1 hr light pulses induced fattening and gonadal
growth in the blackheaded bunting only under red
55
light . At a given intensity, red light is more effective
than white light and white light is more effective than
green light. In other words, the short wavelengths of
light are less effective than the long wavelengths in
stimulation of av ian photone uroendocrine (PNE)system.

Induction VS . entrainment
Differential responses to LD cycles that contain
same inductive but varyin g intensity and wave lengt h
of entraining pul se, or vice-versa, indicate the wavelength- and intensity-dependent entrainment of CRPP.
The threshold li ght intensity for entrainment seems to
be lower than that for induction. In the migratory
bunting, a 20 lux entrainin g or inducing li ght pul se
fail to induce full testis growth . Al so, there can be
differences in li ght intensity thres holds between entraini ng and inducing li ght pu lses.'i5. 56 . Cou ld it be that
the entrainment and induct ion of photoperiod ic responses are two separate phenomena? In any case, it
may be much eas ier to entrain the c ircadi an system
than to convert the photoinductive e ffects into a ne uroendoc rine event such as the lipogenes is (body fat.teni ng) and the gametogenes is (testi cular growth). It
remains however unclear whethe r the difference is at
the leve l of endocrin e system or at photoperi odic
c lock or of both. Furth erm ore, whether the photoperiodi c entrai nment and inducti on are mediated by differe nt classes of photorece pto rs is not known. The
phase-spec ific sensiti vity (e ntrainment by low and
induction by hi gh li ght intens ities) of ph otoperiodi c
clock to li ght intensity may however have some

adaptive implicat ions. For ex ample, entrainment to

daily LD cycle may be achi eved by ph as ic effects of
light at re lati vely low intensity durin g dail y twili ght
hours (dawn and dusk) . By contrast, photoperi odic
induction in a long day species like bunting occurs
during long day length s of spring and summer when
plenty of day light at higher intens ity is avail ab le .
There can al so be differential effects depending
how light is applied. Li ght in wide range of wavelengths is stimulatory when applied direc tl y on to
brain areas, thus directly illuminating ERPs, but not
when applied from outside. In the duck, E RPs th at
mediate light effects respond to both ' blue and red
lights when light is introduced through a qu artz rod
directly into the brain41. ERPs in qu ail also respond to
both blue (455 nm) and orange-ye ll ow (5 75 nm) li ght
when radioluminescent pa int was implanted directl y
25
in specific brain areas .
All observations from spectral studi es are consistent with the idea that the difference in photoperiodic
effects at a given intensity by different li ght wavelengths is due to the difference in number of ph otons
3.0

c, 2.0

.s
J:

..J

G>

..
U

g'1.0

s::.

C
0L-_________________________________

24

40

56

72

96

Circadian time (h)

Fig. 4-S hows th e importance of pos ition -dependent ill uminati on

of the photoinducible phase (<I)i ) in the blac kh eaded Imllfill g.l
(Em beriza melall ocephala). The photoinductive elTec t of Shr ligh t
pul se. given at vario us intervals during 88 hr constant da rk ness
( ~O ) on plasma concentratio ns of LH in bun tings. Hori zo nta l bar
at the bott om indicate time of Sh li ght pu lses. A grou p was maintained on short days and received an Hhr pu lsc at CT Ii - 19: thus
served as contro l (C) . denoted by open symbol. left ill body ot the
graph . The graph shows th e change in LH as determin cd by subtracting . th e pre- pul se pl asma Ll i pro lil e from thc post-pulse
pl asma pro fil es (redrawn from Ku nwr ('/ (I I. 1116)

1060

INDIAN J EXP BIOL, NOVEMBER 1999

received by the photoreceptors s8. At equal energy

levels, the number of photons emitted is larger in red
light than in green or blue light and the penetration to
brain tissues, thereby access to the photoreceptors
(capture of large number of photons by the photopigments), of red light (long wavelengths) is far more
faster and deeper th an of blue or green light (short
wavelengths)24,28)5)7,41. Thi s is although inconsistent
with the fact the deep brain photopigments in birds
which are known to med iate the photoperiodic effects
are not be maximall y sensitive to red light, rather they
are maximally sensitive to green li ght24, but they respond greater to red light since red light has greater
access to them because of being dominant in th e light
environment and having greater penetrance through
the brain ti ssues.

Temporal photosensiti vity

Intensity and spectrum of li ght are not the onl y
factors that induce seasonal res ponses in birds. If th at
was the case, regard less of the photoperi odi c schedul e, the light illuminatio n at given spectrum and intens ity should evoke si milar physiological effects but
it does not: Light pul ses given at different times in the
photosensi ti ve phase of CRPP induces differential
response (Fig. 4). This supports th e view th at an "appropriate" photoperiod is a far more impo rtant facto r,
of course after when the light intensity threshold is
at tained , In oth er words, a hi gher inte nsity or a longe r
wave length of light cannot act as a substi tute for a
"long" photoperiod. The st udy of BurgerS') clea rly
shows th at regardl ess of the increase or decrease in
light intensity, a photoperiod of I0.5L: 13.50 (a nonstimulatory photoperiod p er se) did not st imul ate
spermatogenesis in male sta rli ngs. However, recentl y,
Bentl ey et 01.60 have shown th at th e decrease in light
intensity alters the percepti on of day length in starlings : when groups of starlin gs were kept on 18L:60
at 3-, 13-,45- and 108- lu x li gh t int ensities, th e photoperiodic responses observed in these groups were
comparab le to those exposed to different photoperiods, viz. II L: 130, 13L: I: D, 16L:80 and 18L:60,
respecti ve ly , Thu s, there can be a fasc inating poss ibility that to a certain ex tent light intensity and photoperi od may have synerg isti c effec ts. We are working on th e poss ibility if wavelengt h of li ght could also
prod uce synergisti c effects along wi th li ght in tensity
and photoperiod .

Non-reproductive circadian functions

It is beyond the sco pe of thi s arti c le to summari ze
light effects on the circadian fun ctions, other than
reproduction, known so ex tensive ly but we intend to
cite a .few important findin gs that wi ll indicate the
spectrum of such studi es. It is speculated th at li ght
information that is so unique in twi light times when
th ere are large changes in irradiance as well as very
precise changes in light spectrum is utili zed by ani mals to regulate their ci rcadian ti ming system. Fresh
water alga Chlamydol11onos6 1 and th e marine alga
62
Gonyaulax are good examples of how spect ral informat ion is used by th e circadi an system in organisms with simple organization. A number of findin gs
on verteb rates also sugges t th at the spectral changes
of li ght affect the circadian system. Blue li ght increments are more effec ti ve in advancing the start of activity than blue decrements and ye llo w decrements
are more effecti ve than ye ll ow increment s(" in the
evening-acti ve wild rabbits. In go lde n hamste r, th e
sensitivity of th e circadian system to li gh t spectrum
was maxi mum near 500 nm and is sim il ar to th e absorption spectrum for rh odopsi n 6~ . In th e bat reti na ,
Joshi and Chandrasheka ran6s suggest the ex istcnce of
two classes of photoreceptors: S photoreceptors th at
have max imu m sensiti vity at th e wave length 430 nm
and mediate delay phase shifts, and M ph otoreceptors
whic h have maximum sensiti vity at the wave lengih
520 nm and mediate adva nce phase s hift ~ . However,
such li ght-spectrum based regu larion of ci rcad ian
system in vertebrates has not bee n th oro ughl y studi ed.
For ins tance, we do kn ow that the circadian system of
mouse 66 is sensi ti ve to both gree n li ght and near-UV
irradiance, but we do not know how th e signal s from
th ese different spectral chann e ls are uti li zed by th e
mammalian circad ian system.
The intensity of li ght acts as dom inant cxtcrnal
time cue (entra ining age nt, Zeilgehn - a German
word, Zeit- time, geher - giver) fo r the entrainment or
the clock in most organi sms , as shown in majorit y of
cascs by its effects on th e circadi an rhythm in locomotor ac ti vity . Even uncleI' constant concliti on:-- ,
li ghting can have important effec ts on rh ythms that
prov ide clues as to how th e sy nchroni zation can happen. The leve l of constant illumin at ion to whi ch an
anima l is ex posed affects th e ex pressed period (represented ' by the Greek letter, tau 1) of th e frcc nlll nin g
rhythm (freerun is a chronobiol ogica l jargon that denotes the express ion of a rh yth m with its peri od Linder
co nstant co nditions) . These effec ts were first sumlll(J-

KUMAR & RANI: WAVELENGTH AND INTENSITY EFFECTS

rized more than three decades ago by J. Aschoff in

what became known as "Asc hoff' s Rule" (for details
see67 ). This rule states that as constant light intensity
increases, 't lengthens for nocturnal species and shortens for diurnal species. With other regularities of the
effects of lighting on the circadian system, like the
effects on activity (represented by Greek letter alpha,
a) and rest (represented by Greek letter rho, p) of the
daily activity rhythm, added to Aschoff's Rule, they
became known as "Circadian Rul e". This then states
that as constant light intensity increases, tau shortens,
activity level increases, and the ratio of active phase
to rest phase (a : p) increases for diurnal animals.
The opposite effects are true of nocturn al animals.
This rule holds pretty well for most groups of vertebrates that have been studied : fi sh, reptiles, amphibians, birds and nocturnal mammals. The rul e is less
successful with most invertebrates , curi ously seems
not to apply to diurn al mammals, many of which respond as if they were, in fact, nocturn al.
The light effects are clearly seen in regulati on of
rhythm in melatonin sec retion th at occ urs in ni ght
regardless of the nature of animals, diurnal , nocturnal
or crepuscular. In starlings (Kumar et al., unpublished), daytime light intensity had some effec ts on
the circadian pattern of plasma melatonin. There was
also difference in the phasing of the melatonin
rhythm: peak melatonin levels tended to occur earli er
in LDdim ( I: 0.2 lux) th an in LDbright (500 : 0.2 lux).
The relationship between the li ght intensity at day
and/or ni ght and th e pattern of pl as ma melatonin and/
or enzymes in vo lved in th e melatonin synthes is has
been studi ed also in a few mammalian spec ies 6R-n .
Besides reproducti ve and circad ian fun ctions, viz.
rhythms in locomotor acti vity and melatonin secretion , the light of differe nt illuminance and wavelength
influence a variety of ot her responses in birds.
Wiltschko and hi s co ll eagu esn7~ have in vesti gated
the effects of I ight wave length on magnetorecepti on
in the avian mi grants (e.g. Tasmanian sil ver eyes,
Zosterops I. haeralis). They have found th at th ese
mi gran ts were well oriented in their appropriate migratory direction under 'wh ite' (full spectrum), blue
and green li ght but were disori ented under 633 nm
li ght in th e red region of th e light spec trum 7ns .
Light illuminance and wavelength also affect
growth of birds76-80 . When large white turkey hens at
the age of 30 weeks were exposed to blue, green and
red or incandescent light equalized at a photon out-

1061

put, a colour-dependent effect of li ght was found on

the cellular and humoral immune responses but not on
stress status33 . The light colour has also been found to
affect body temperature, kidney fun ction, sex ual
function, adrenal function and pituitary fun cti on in
32
birds .
Light-dependent compass ori entati on has also bee n
s1
reported in other vertebrates, such as fishes , am' 8?-.81" reptl'1 es 84 and mammals K'' althou gh
PhI'b lans
wavelength dependence seems to differ from th at or
birds. In primitive chordate like ri ver lamprey, LOll/p etra japonica, neuronal activity see ms to be influenced by the light colour. It was inhibited by the li ght
of short wavelengths and excited by middle to long
wavelengths ; the maximum sensiti viti es of th e inhibitory and excitatory responses were at about 380
and 540 nm, respectively. Since environmental li ght
contains both inhibitory and exc itatory compo nents,
th e neurons would keep both sensitiviti es during daytime and could measure th e variati on in th e spectral
6
composition. Tosini and Aver/ ha ve reported that
the spectral co mposition of I ight mi ght be an important variable in mediatin g the thermoregul atory processes in lizards.
The circadian literature is full of references
wherein a li ght pul se given at different times in th e
circadian cycle evokes differenti al res ponses, measured in the context of circadian loco motor rh yt hms as
phase shifts . A graphi cal represent ati on of such phase
shift induced in the oscillator by li ght pulses is kn ow n
as the phase res ponse curve (PRC). PRCs obtained by
the light pul se of varying intensity and/ or durati on
(few seconds to few hours) as we ll as va rying co lours
are available for a number of orga nisms includin g
plants. A few exampl es are: circad ian rh ythm or
K7
mating reacti on in Param ecillll1 hllr.\(/ rio , of CO 2
output of B ryophy llum fedlsch ellko / K, of ec los ion
rhythm in Drosophila ~'i-'i l , of petal movement s in
92
Kalanch oe and of ac ti vity rh yt hm in Ra II 11.1' e. l'lI91
lans . Three well-document ed in sta nces are th ose of
the sporulati on rhythm of the fun gus, Pi/obo /IIS'i~, the
ec los ion rh ythm of th e Drosophi/(/'is and th e circad ian
rh ythm of fli ght activity in the bat. Hipp osideros
96
speoris all of which respo nd with phase shi fts to
ex tremely short li ght fla shes of just 0.5 msec. Li ght
fl as hes of different durati ons (0.063 - 3.33 msec .)
phase shifts the circadian rh ythm in fli ght act ivit y in
the bat, Hipposideros speori.I96 Kl ante and Stei nlec hner97 report in Djungari an hamster that a single
weak red light pul se given 2 h before regular " li ghts

1062

INDIAN J EXP BIOL, NOVEMBER 1999

on" had acute and long term effects persistIng for

several days following exposure ; this indicates high
sensitivity of circadian system to red light pul ses
during later part of the night.
As yet, it has been difficult to produce a PRC for
the photoperi odi c oscillator because it cannot be
monitored directl y. Formal analyses of th e photoperiodic clock are done employing various LD cycle
paradigms54 and exa mining their effects on the
physiological and/ or behavi oural markers of the
clock system, assuming th at th ese markers faithfully
predict the photosensitive phase of the circadian
photoperiodic c1ock'J8.'J'J. However, recent studies on
few species including Japanese quail which show dissociation of photoperiodi c responses (LH rise) from
oth er circadian locomotor acti vit y rh ythm, qu estion if
the properties of photoperiodi c osc ill ator can be
st udi ed using any other marker of th e circadian system I OO- I 02

A final remark
It is intriguing that CRPP res ponsible for photoin-

duction of reproductive responses is stimulated at

such a hi gh li ght intensity when other circadi an systems are known to be affec ted by very low intensities
of light. A further co nundrum in the photoperi odi c
literature is that while red light is th e most effect ive
agent for the stimulation of PNE-system in bird s, it is
considered as "safe li ght" (i.e. non-ind ucti ve) for th e
stimulation of PNE-system in mammals. Is it because
of the differences in the sensiti vity of photorece ptors
or because of th e di ffe rences in th e deg ree of penetration of red li ght throu gh brain ti ssues overlying
photoreceptors in two verteb rate c lasses? It is more
puzzling when basic characteri sti cs of th e photoreceptors amo ng birds and mammals have great similarity with each other. For ex ampl e, although th e
anatomy of their eyes differs, the cones of human and
fow l are both tri chromat ic l03 and th e relative spectral
luminositi es of chicken , pigeon and man are th e
same I04 ,10., .

Acknowledgement
Resources from CSIR research gra nt to YK were
utilized in preparat ion of thi s rev iew paper.
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