Extraretinal Photoreception. Proceedings of the Symposium and Extraretinal Photoreception in Circadian Rhythms and Related Phenomena

91 Pages·1976·24.846 MB·English

by  Michael Menaker

EXTRARETINAL P H O T O R E C E P T I ON
Proceedings of the Symposium and Extraretinal Photoreception
in Circadian R h y t h ms and Related Phenomena
Held at:
The 2nd Annual Meeting of the
American Society of Photobiology
July 22-26 1974, Vancouver, Canada
Chairman and Guest Editor: Michael Menaker
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THE PROCEEDINGS OF THE SYMPOSIUM
HELD AT THE 2ND ANNUAL MEETING OF THE
American Society for Photohiology IN
VANCOUVER, CANADA, ON 22-26 JULY 1974
AND PUBLISHED AS A SPECIAL ISSUE OF
Photochemistry and Photohiology
VOLUME 23, NUMBER 4 1976,
AND SUPPLIED TO SUBSCRIBERS AS PART OF THEIR SUBSCRIPTION.
ALSO AVAILABLE TO NON-SUBSCRIBERS.
Printed in Great Britain by A. Wheaton & Co. Ltd., Exeter, Devon
Photochemistry and Photohiology, 1976, Vol. 23, p. 213. Pergamon Press. Printed in Great Britain
INTRODUCTION*
Although it has been known for over fifty years that of recent work on either single species (Aplysia, cray­
some organisms with complex image forming eyes fish), a group of closely related species (lizards), or
have, in addition, other less highly structured photo­ an entire class (insects, amphibians, birds). We hope
receptors, it is only recently that the phenomenon of in this way at least to introduce a reasonably broad
extraretinal photoreception has emerged as more than perspective without sacrificing the richness of specific
a curiosity. The new interest in the subject has been detail which provides the core of any exciting field.
generated by several discoveries that have occurred As well as containing a great deal of specific infor­
during the past 7 or 8 years: extraretinal photorecep­ mation, the papers in this Symposium, taken as a
tion has now been demonstrated in a large number group, emphasize how much remains to be learned.
of invertebrates and in at least some members of all In particular, although both the sensitivity and the
5 classes of vertebrates; although precise anatomical wide distribution of extraretinal photoreception
localization of the receptors involved has still not argues forcefully that it is adaptively significant, it
been accomplished in most cases, the available evi­ is not yet evident of what that significance might con­
dence indicates that most are located in the brain sist. What do organisms gain by partitioning photo­
or other central nervous system structures; despite sensitivity among several discrete receptors with the
their "deep" location many extraretinal photorecep­ attendent problems of then reintegrating the informa­
tors are sensitive to very low levels of ambient illu­ tion obtained, as against making multiple usage of
mination; and finally, extraretinal photoreceptors the eye which they must in any case employ in the
have been shown to mediate the effects of light on perception of images? The fact that adult mammals
physiological responses which have themselves and some insects apparently do employ the eyes in
become more interesting to students of biological this way simply makes the question more difficult.
organization in recent years—in particular circadian Finally it should be emphasized that as far as extrare­
rhythms and associated phenomena such as reproduc­ tinal photoreception is concerned, we do not as yet
tive cycling and even celestial orientation. have any complete cases. Either we have identified
In this Symposium we have attempted to draw and studied the physiology of such receptors but have
together much of the work which has led to the no clear idea of their function (e.g. the pineals of the
renewed interest in the subject. Limitations of time Poikilothermie vertebrates, the 6th abdominal gang­
and space have prevented us from including all well lion receptor of crayfish), or we have identified extra-
documented cases of extraretinal photoreception— retinally-mediated functions (e.g. the entrainment of
indeed the Symposium is in no sense intended as an circadian rhythms) without knowing where the recep­
exhaustive review. Rather we have focused our atten­ tors are or much about how they work. Further pro­
tion on those cases in which there is a good deal gress clearly depends on bringing these two kinds of
information together in as many different organisms
*Editor's note: The papers presented in this Symposium as possible.
issue are based on Symposium VI: Extraretinal Photore­
ception in Circadian Rhythms and Related Phenomena,
held at the 2nd Annual Meeting of the American Society MICHAEL MENAKER
for Photohiology, Vancouver, Canada, July 22-26, 1974. Symposium Chairman and Guest Editor
213
Photochemistry and Photoh\ology\ 1976, Vol. 23, pp. 215-225. Pergamon Press. Printed in Great Britain
EXTRARETINAL PHOTORECEPTION IN INSECTS
JAMES W. TRUMAN
Department of Zoology, University of Washington, Seattle, WA 98195, U.S.A.
[Received 30 September 1975; accepted 10 October 1975)
Abstract—Extraretinal photoreceptors are widespread among insects and function in the photoperiodic
control of development and in the entrainment of circadian rhythms. The effects of light on the daily
and seasonal regulation of brain neuroendocrine activity are mediated solely through extraretinal photo­
receptors. In primitive insects, the eyes participate in the entrainment of nonendocrine circadian rhythms
such as the locomotor rhythm. In more advanced forms, however, extraretinal pathways appear to
be the only pathway for the entrainment of all rhythms thus far examined. But even in this latter
case, the eyes sometimes effect a masking of the expression of the overt rhythm. An exact localization
of the extraretinal receptors has not been accomplished, but in all studies to date they appear to
be associated with the cerebral lobe region of the brain. Action spectra for photoperiodic responses
have been determined for a number of insects. In general the responses are maximally sensitive in
the blue with a marked decline in the red although exceptions do exist. Complete action spectra
for circadian responses have been determined only for two insects. In both cases a plateau of sensitivity
extends through the blue with a steep drop at longer wavelengths. From the action spectra data,
the extraretinal receptors appear to have a threshold sensitivity less than 3 χ 10~^ J/m^. The pigment
nature of the receptor is unknown although it appears not to be a carotenoid derivative.
INTRODUCTION earliest evidence that indicated the involvement of
It has long been known that insects are equipped with extraretinal photoreception in this response was the
two types of retinal photoreceptors. Adult insects demonstration that the discrimination of daylength
typically have two prominent compound eyes and continued even after occlusion or removal of the eyes.
from 0 to 3 medially placed simple eyes or ocelli. This was true not only for larval insects (Tanaka,
Larvae of forms having incomplete metamorphosis 1950; Belov, 1951; cited in Danilevski, 1965), but also
usually have the same arrangement as the adult. In for adults as well (de Wilde, 1958).
insects that show complete metamorphosis, the larvae Geispits (1957) attempted to localize the site of
always lack both the compound eyes and medial photoperiodic sensitivity in larvae of the pine moth,
ocelli, but may have laterally positioned simple Dendrolimus pini. Cateφillars were exposed to con­
eyes—the stemmata. stant light, but one-half of each animal was hooded
In 1950, Tanaka showed that larvae of the oak silk- over for 12 h each day. Consequently, one-half of the
moth, Antheraea pernyi, could detect differences in larva was exposed to a LD12 :12, whereas the other
day-length, even after removal of their stemmata. half was in LL. Her results indicated that the anterior
These results first indicated that insects also used end was photosensitive but she then went on to con­
extraretinal photoreception. During the 25 years since clude that the larval eyes were the receptor in ques­
Tanaka's report, there have been numerous confirma­ tion. This conclusion was based on similarities
tions of extraretinal photoreception in insects, a capa­ between the spectral sensitivities of the photoperiodic
city which now appears to be almost universal in this and the phototactic responses. But, it must be ques­
group. This photoreceptive system is totally separate tioned in light of her other results which showed that
from the eyes and typically plays the major role in discrimination of day-length continued, albeit in a
the coordination of physiological and behavioral pro­ somewhat modified form, after the stemmata were
cesses with daily and seasonal photoperiod cycles. covered with black paint.
This review deals only with cases of extraretinal pho­ A more exact localization of an extraretinal recep­
toreception that are related to insect photoperiodism tor came with the studies by Lees (1960, 1964) on
and circadian rhythms. For much of the background the aphid Megoura viciae. In this insect, the produc­
to the non-photoreceptive aspects of these two pheno­ tion of the sexual, egg laying morph vs the asexual,
mena, the reader should consult the recent reviews parthenogenetic morph is controlled by day-length.
by Brady (1974) and Saunders (1974). Lees exposed female aphids to a short day regimen
(LOM'AO) and, by means of light guides and light-
conducting filaments, provided an additional 2 h illu­
Extraretinal photoreception and photoperiodism
mination to selected regions of the aphid. As seen
The ability to use changes in day-length to cue cer­ in Fig. 1, a long-day response was obtained only
tain developmental events is widespread among the when the head was included in the area of supplemen­
insects (Danilevskii, 1965). As mentioned above, the tal illumination. Moreover, the area most sensitive
215
216 JAMES W. TRUMAN
Figure 1. The resuhs obtained by selectively illuminating various regions of Megoura viciae. The de­
nominator in each "fraction" indicates the number of aphids treated, the numerator is the number
responding positively to supplementary illumination. Areas illuminated denoted by circles (from Lees,
1964).
Photoreception and circadian rhythms
to light v^as the dorsomedial region of the head, di­
rectly over the brain. In only a few individuals was There are two main ways by which light can affect
light directed at the eyes effective. These experiments the overt expression of a rhythm (Aschoff, 1960). It
provided strong evidence that the brain was the pri­ can act as a Zeitgeber to entrain the circadian clock
mary receptive site mediating the photoperiodic re­ and, thereby, determine the phase of the rhythm rela­
sponse. The few positive responses seen when light tive to environmental light cycles. Light can also exert
was directed to the compound eyes presumably were a "masking effect" such that the rhythmic output of
due to scattered light that reached the brain. the clock is modified by the effects of exogenous light
The photosensitivity of the insect brain was conclu­ (or darkness). The present section considers photo­
sively shown by the experiments of Wilhams and receptors involved in the first function—^that of
Adkisson (1964) on the termination of pupal diapause entrainment of the circadian clock.
in A. pernyi. By exposing the two ends of diapausing There has been considerable confusion and contro­
pupae to different photoperiod regimens, they estab­ versy regarding the identity of the photoreceptors that
lished that the anterior end was photosensitive. They mediate the entrainment of insect rhythms. In large
then transplanted the brain to the tip of the abdomen part, this has been due to the use of inadequate tech­
in another series of pupae and inserted the animals niques and the failure to apply rigorous criteria to
into holes bored into wooden blocks. One-half of the analysis of the results. The most abused technique
each insect was exposed to DD (which is partially is that of shielding a receptor with an opaque mater­
inductive in this species) and the other half to an ial. If the insect continues to show entrained activity
inhibitory short-day regimen. The pupae that had after this procedure, it is usually concluded that the
their brainless anterior ends exposed to short-day and covered area is not required for entraiimient of the
their abdomens (with the brain implant) in DD res­ rhythm. Aside from the fact that the covering may
ponded by initiating development, whereas those in be incomplete, often the incident light intensities are
the reversed condition (i.e. abdomens in short-day) too great. Consequently, light penetrates the cuticle
remained in diapause. Indeed, both groups of pupae and sufficient scattered light reaches the receptor un­
responded to the photoperiod to which the abdomen der the paint. A better method involves the ablation
was exposed, thereby indicating that the site of photo­ of the receptor, but even then, the result that the in­
sensitivity had been transferred to the abdomen with sect continues to entrain can only be inteφreted as
the brain. Claret (1966) also showed that photo­ showing that the ablated structure was not the sole
periodic sensitivity could be transferred to another receptor responsible for entrainment. The strongest
region of Pieris brassicae larvae by transplantation evidence for the involvement of a particular receptor
of the brain. is the demonstration that after the receptor is
Insect extraretinal photoreception 217
removed or masked, the rhythm then free-runs in a the eyes and the ocelli were covered over with black
photoperiod regimen that is of an intensity sufficient wax. But Loher (1972), working with the stridulatory
to entrain the intact animal. rhythm of another cricket, Teleogryllus commodus,
A good example of the above problems is seen in showed that entrainment occurred only via the com­
the studies of the locomotor rhythm of the cockroach. pound eyes. After removal of these structures and
On the basis of painting experiments, Cloudsley- their replacement with transparent cups, the crickets
Thompson (1953) reported that the locomotor rhythm showed a free-running rhythm of stridulation even
was entrained by light perceived by both the ocelli under a photoperiod and even though the ocelli were
and the compound eyes. Harker (1956), also relying intact. In light of these experiments on Teleogryllus
primarily on covering receptors, then claimed that the and the extensive literature on cockroaches, the role
ocelli, but not the compound eyes, mediated entrain­ of the ocelli in the entrainment of the locomotor
ment. However, her data show that after the ocelh rhythm in Acheta should be reexamined.
were painted, the cockroaches shifted to diurnal ac­ In their lack of extraretinal receptors, cockroaches
tivity, but they did not then show a free-running and crickets are in contrast to all other insects that
rhythm of locomotion. Roberts (1965) subsequently have been studied. In the walking stick photorecep­
demonstrated that only the compound eyes mediated tion continues after removal of the compound eyes
entrainment. Surgical ablation of the ocelli did not (Eidmann, 1956; Godden and Goldsmith, 1972). Simi­
affect entrainment to photoperiod cycles, but painting larly, in the grasshopper, Chorthippus curtipennis
over the compound eyes produced animals that (Loher and Chandrashekaran, 1970) and the "long-
showed a free-running rhythm even under a photo­ horn" grasshopper, Ephippiger (Dumortier, 1972)
period regimen. These results were later confirmed entrainment of the oviposition and stridulatory
by Nishiitsutsuji-Uwo and Pittendrigh (1968), who rhythms respectively occur after removal of all exter­
also showed that transection of the optic nerves simi­ nal photoreceptors. In Chorthippus, the extraretinal
larly produced a free-running animal irrespective of receptor was reported to be extracephalic. This con­
the conditions of illumination. These workers further clusion was based on the fact that grasshoppers that
demonstrated that if light was allowed direct access had their head covered with black paint, nevertheless,
to the brain through a transparent "window" pos­ entrained to a light-dark regimen. The high intensity
itioned over the brain, then entrainment still did not of illumination [1500-2000 Ix (/m/m^)] coupled with
occur after the optic nerves were severed. Thus, they the extreme sensitivity of some insect extraretinal
concluded that in the cockroach there is no extra- receptors (see below) makes it likely that sufficient
retinal receptor associated with entrainment of the scattered light could have penetrated into the head
locomotor rhythm, at least, at the low levels [40 to have caused entrainment.
lx(/m/m^)] incident illumination used. Recent exper­
In Ephippiger (Dumortier, 1972) experiments in­
iments by Driskill (1974) on Leucophoea maderiae and
volving the selective exposure of the head or the re­
Periplaneta americana have confirmed the above
mainder of the body of eyeless and ocelli-less animals
results and have shown that eyeless animals with plas­
to 40 Ix photoperiods showed that an extraretinal
tic windows over their brain will not entrain even
receptor was located in the head. Attempts to localize
to intensities as high as 22,700 be. Thus, the absence
the site of sensitivity within the head by directing light
of extraretinal photoreception in cockroaches with re­
through fiber optics to the brain or subesophageal
spect to the locomotor rhythm is well established.
ganglion were inconclusive. Direct illumination of
Ball (1972) and Ball and Chaudhury (1973) working these structures in intact animals typically resulted
with Blaberus craniifer and Periplaneta americana in entrainment, but when eyeless insects were treated
have recently challenged this conclusion. They in the same manner none entrained. These results are
showed that cockroaches with occluded heads will peφlexing because they appear to rule out the exist­
entrain to a photoperiod if a plastic window is in­ ence of an extraretinal receptor in the head, whereas,
serted in the head. They claim that these results the former experiments indicate its presence. Dumor­
demonstrated the photosensitivity of the brain, but tier (1972) suggests that the light from the fiber optic
this technique also allows light to reach the retinal was too bright, but it appears more likely that the
elements of the eyes. Their experiments have been ex­ extraretinal receptor is less sensitive than the eyes in
tensively criticized by Roberts (1974) and the details Ephippiger and that the light was too dim. The data
need not be repeated here. Suffice it to say that ques­ on this insect indicate that the stridulatory rhythm
tionable experimental techniques coupled with the is entrained through both retinal and extraretinal
lack of proper controls cast serious doubt upon these pathways but the location of the latter is uncertain.
new findings. They do not stand against the strong The localization of an extraretinal photoreceptor
body of careful experimentation presented above. to the insect brain has been demonstrated for the
The cricket appears similar to the cockroach with rhythm of adult eclosión. Using an eyeless mutant
respect to retinal entrainment of its locomotor of Drosophila melanogaster, Engelmann and Honegger
rhythm. Nowosielski and Patton (1963), using only (1966) showed that entrainment of the eclosión
opaquing techniques, claimed that individuals of rhythm continues in the absence of the compound
Acheta domesticus became arrhythmic only after both eyes and ocelli. By painting over the anterior or the
218 JAMES W. TRUMAN
posterior ends of fly puparia, Zimmerman and Ives
(1971) then restricted the site of photosenstivity to
the anterior end. The fact that the brain contained
the extraretinal receptor for the eclosión rhythm was
then shown by experiments with the giant silkmoths,
A. pernyi and Hyalophora cecropia (Truman and Rid-
diford, 1970; Truman, 1972a, b). In these insects eclo
sión is controlled by a brain-centered clock. When
the brain is removed from animals early in adult de
Figure 3. Drawing of the brain of an adult silkmoth. The
velopment, the resulting moths show eclosions that
cross-hatched area may be removed without interferring
are randomly distributed throughout the photo with photoreception. OL, optic lobes; CL, cerebral lobes;
period. Implantation of the brain into the abdomen AN, antennal nerve; CC circumesophageal connective. The
of a debrained animal restores the ability of the ani location of the medial and lateral neurosecretory cell
groups are indicated.
mal to synchronize its eclosión with the photoperiod
and to emerge during the time of day characteristic
for that species. Moreover, transfer of brains between although it does abolish a noncircadian lights-on re
two species that show different emergence times sponse. Even in photoperiods that have an incident
serves to transfer the species-speciñc time of emer intensity of only 1 Ix, eyeless moths show good
gence (Truman and Riddiford, 1970). entrainment. Therefore, as with eclosión, the flight
The location of the eclosión photoreceptor was rhythm of these moths is presumably entrained
determined by experiments similar to those employed through an extraretinal receptor in the brain.
by Williams and Adkisson (1964). Developing aduhs
Localization of insect extraretinal photoreceptors
of H. cecropia were ñtted midway through holes that
were drilled in an opaque partition. The partition was All of the evidence to date strongly indicates that
then used to separate two chambers of a photoperiod the brain is the location of the extraretinal photo
box that were programmed suchuhat the two ends receptors that mediate photoperiodism and circadian
of each animal received reciprocal schedules of illu rhythms. There are other putative extraretinal recep
mination (Fig. 2). One group of animals had the brain tors in insects, e.g. the abdominal ganglion (Ball,
transplanted to the tip of the abdomen, whereas those 1965) and para-ocellor organs and tegumentary
of the other group had the brain removed from the photoreceptors (Brousse-Gaury, 1967, 1968, 1969) of
head and then reimplanted back into the head. As cockroaches. These, however, appear to have no role
seen in Fig. 2, the site of photosensitivity shifted from in the phenomena of interest here. One exception is
the anterior to the posterior end in those moths that the circadian rhythm of chitin lamellogenesis by the
had their brains implanted into their abdomens (Tru epidermis of the locust which appears to be mediated
man and Riddiford, 1970; Truman, 1972a). through direct reception of light by the epidermal
Extraretinal photoreception is also involved in the cells (Neville, 1967). Thysanura (Pipa, Nishioka and
flight rhythm of silkmoths (Truman, 1974). Surgical Bern, 1964) and some moths (Eaton, 1971) have been
removal of the compound eyes and ocelli does not reported to have internal ocelli. The latter are of spe
interfere with the entrainment of the flight rhythm cial interest because of their occurrence in the adults
of the giant silkmoths. Their participation in photo
reception for the flight and eclosión rhythms has not
been rigorously excluded, but it is unlikely that these
delicate structures would have routinely survived the
mainpulations involved in brain transplantation de
scribed above (Truman, 1972a).
Experknents involving the implantation of various
parts of the brain into a debrained host have shown
that the optic lobes are not required for the entrain
ment of the eclosión rhythm of silkmoths (Truman,
1972a). Similarly, the photoperiodic response of A.
pernyi pupae continues after excision of the optic
lobes (Williams, 1969). Experiments on the aphid
?l 09 21
(Lees, 1964), Carasius (Eidmann, 1956), and Ephip-
Time. EST
piger (Dumortier, 1972) likewise implicate the cerebral
Figure 2. The eclosión of two groups of "loose-brain"
lobe area of the brain as the probable site of the
moths which differed only in the site of brain implantation.
The anterior and posterior halves of the developing moths photoreceptor. Indeed, in every case that has been
were exposed to the photoperiod regimens indicated by examined thus far, extraretinal photoreception is
the square and circle, respectively. The mean and standard
associated with the cerebral lobes (Fig. 3). Attempts
deviation of each group is given; square, brain implanted
to localize further the site of photosensitivity have
into head; circle, brain implanted into tip of abdomen
(from Truman, 1972a). been inconclusive (Williams, 1969; Truman, 1972a).
Insect extraretinal photoreception 219
Or
(a) (b)
> -:
Λ
\
^ -4|
-5h
400 500 600 400 500 600
Wavelength, nm
Figure 4. Spectral sensitivity of the compound eye (a) and the circadian rhythm (b) in white-eye
(open circles, dotted arrows) and wild-type (closed circles, solid arrows) Drosophila pseudoobscura.
Ordinate: log reciprocal of the relative number of quanta required for a constant response (photorecep­
tive cells in compound eye: 5 mV corneal negative wave; rhythm: phase shift on day 2). In b, circles
denote light energies giving 40-60% phase shift on day 2, upward pointing arrows more than 60%,
and downward pointing arrows less than 40% (from Zimmerman and Ives, 1971). Reproduced with
permission of the National Academy of Sciences.
Relationship between retinal and extraretinal pathways show free-running activity rhythms even though the
eyes are exposed to the dim-light regimen. Thus,
In Ephippiger light perceived through both retinal
shielding the brain from light while allowing the eyes
and extraretinal pathways is apparently effective in
to see the photoperiod does not allow entrainment
entraining the clock that controls stridulatory activity
(Truman, 1974). Consequentíy, in the silkmoths, as
(Dumortier, 1972). However, the existence of both
in Drosophila, retinal pathways do not participate in
retinal and extraretinal inputs to a photo­
the entrainment of circadian rhythms.
periodic or a circadian clock is not the general rule
Even in cases where the eyes are not involved in
in insects. This was first indicated by the fact that
the entrainment of a rhythm, they may still mediate
in Megoura light perceived only by the eyes was not
the masking effects of light. In the night rhythm of
effective in eliciting a photoperiodic response (Fig. 1)
male Hyalophora cecropia, removal of the eyes does
(Lees, 1964). The same light positioned over the brain
not affect the circadian components of the rhythm
was fully effective.
but it abolishes the brief burst of night activity that
Zimmerman and Ives (1971) compared the spectral
occurs at light-on (Truman, 1974). A shnilar pheno-
sensitivities of the compound eyes and the eclosión
monon is also seen in the eclosión response of this
rhythm in Drosophila pseudoobscura. As seen in Fig.
species. The emergence of H. cecropia under a LD
4, the action spectrum of the eclosión rhythm shows
17 :1 photoperiod shows a pronounced skew toward
a sharp decline in sensitivity at wavelengths longer
lights-on (Fig. 6). Severence of the optic nerves reduce
than 500 nm. But the spectral sensitivity of the eye
this rapid response to lights-on, and implantation of
(based on the electroretinogram response) extends
the brain into the abdomen abolishes it completely.
beyond 600 nm. Thus, the compound eye is sensitive
In the latter case, eclosión still occurs synchronously
to certain wavelengths of light to which the eclosión
but somewhat removed from the lights-on signal. The
rhythm will not respond. Moreover, the white eye
light-on response can be reestablished in a "loose-
mutant of Drosophila shows an ERG response that
brain" animal by transplanting in the pupal stage the
is 1000 times more sensitive than wild type, but both
brain with the attached eye imaginal discs. The im­
mutant and wild type show equal sensitivity in their
plants subsequently metamorphose to form brains
circadian response (Zimmerman and Ives, 1971).
with attached compound eyes. In these animals the
A different technique was used to show that the
eclosión response is shifted back towards lights-on
compound eyes do not participate in the entrainment
(Truman, 1972a). Thus, in the silkmoths, the entrain­
of the silkmoth activity rhythm. As mentioned above,
ment of the rhythm by light is mediated through a
intact and eyeless silkmoths entrain to a dim (1 lux)
brain-centered receptor, whereas the masking effects
photoperiod. The complete covering of the head of
of light are accomplished through the compound eyes.
the moth with black wax yields an insect that shows
a free-running rhythm of night activity under these
photoperiod conditions. Fig. 5 shows the result of Spectral sensitivity of extraretinal receptors
covering the head except for the compound eyes. A knowledge of the relative contribution of retinal
Males of H. cecropia and Samia cynthia so treated pathways to a circadian or a photoperiodic response
220 JAMES W. TRUMAN
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Figure 5. Example of the effect of covering over the entire head of a silkmoth with black wax except
for the compound eyes, a-d shows four different S. cynihia males. The data for each mdividual are
shown in the form of the event recorder records and of histograms. The moths were exposed to
1 Ix photoperiods (from Truman, 1974).
is important when considering the spectral sensitivity in the beetles, Anthonomus granáis (Harris et ai,
of such a response. In most instances, since responses 1969; Mangum, Earle, and Newsom, 1968) and Lep-
include no retinal components, spectral data reflect tinotarsa decemlineata (de Wilde and Bonga, 1958),
the sensitivity of the extraretinal receptor modified the homopterans, Euscelis (Muller, 1964) and
by the screening properties of the overlying tissues Megoura viciae (Lees, 1966), the dipteran, Chaoborus
and cuticle. In many small insects the screening effect (Bradshaw, 1972), and a wide variety of Lepidoptera,
is minimal because there is little tissue to filter the Bombyx mori (Kogure, 1933, as cited in Danilevskii,
light before it reaches the pigment. Other insects, such 1965), Pieris rapae (Barker et α/., 1964), Α. pernyi
as A. pernyi pupae (Shakhbazov, 1961; Williams and (Williams et ai, 1965; Norris et al, 1969), Laspeyresia
Adkisson, 1964) have transparent patches that overlie pomonella (Norris et al, 1969), L. molesta (Dickson,
the brain; others (e.g. larvae of Chaoborus) are totally 1949), Pectinophora gossypiella (Pittendrigh et al,
transparent. 1970), Pieris brassicae (Gespits, 1957; Bünning and
The spectral sensitivity of the photoperiodic re­ Joerrens, 1960), Dendrolimus pini and Acronycta
sponse has been examined for a number of insects: rumiéis (Gespits, 1957).
Insect extraretinal photoreception 221
the ultraviolet (Fig. 7a). Lees (1971) later determined
the action spectrum for the effectiveness of an inter­
ruption late in the night (Fig. 7b). As with the early
interruption, maximum sensitivity ranged from ap­
proximately 450-475 nm. However, during the late
night sensitivity extended to 600 nm and also towards
the shorter wavelengths. The striking differences in
the two spectra indicate that distinct biochemical
events are occurring during the early and late por­
tions of the night. Different photopigments may also
be involved.
Action spectra have also been obtained for Las-
07 13
E.S.T. peyresia pomonella, A. pernyi (Norris et al, 1969) and
Time of eclosión,
for Chaoborus americanus (Bradshaw, 1972). These
Figure 6. The influence of the eyes in the emergence of
H. cecropia moths: a, Normal moths; b, brain transplanted spectra were obtained by adding a 4 or 6 h period
to abdomen; c, brain with attached eye imaginal discs of monochromatic light to the beginning or the end
transplanted to abdomen (from Truman, 1972a). of a short night. Thus, if the monochromatic light
was perceived, then the overall regimen was inter­
preted as an inductive long day, whereas, if it was
In general, species tend to be most sensitive to the not perceived, the photoperiod was taken as a short
blue and very insensitive to the red wavelengths, but day. The two moths showed a maximum sensitivity
this is by no means universal. At least one species, at about 450 nm, whereas peak sensitivity was at 550
Chaoborus, has a peak sensitivity at 550 rmi (Brad- nm in Chaoborus. In this last species, a comparison
shaw, 1972), and a number of insects show an exten­ of the effectiveness of light periods given before or
sion of sensitivity out beyond 600 nm. after the night showed that the Chaoborus photo­
The first complete action spectrum was obtained periodic system was approximately 10-fold more sen­
by Lees (1966) for Megoura. A LD Í3.5:10.5 photo­ sitive at dawn as compared to dusk (Bradshaw, 1972).
period is interpreted by the aphid as a short-day However, unlike the aphid, the two spectra are quali­
regimen. The insertion of a 1 h light pulse beginning tatively similar.
1.5 h after the onset of darkness causes a reversal Only a few insects have been examined with respect
in response in that the regimen is now inteφreted to the spectral sensitivity of their circadian rhythms.
as a long-day. Lees exposed aphids to this interrupted The hatching rhythm of larval A. pernyi is sensitive
night regimen but used monochromatic light during to blue but not to red light (Riddiford and Johnson,
the 1 hour pulse. The action spectrum for the effect­ 1971). The same is true for the hatching, oviposition,
iveness of the early night interruption shows a peak and eclosión rhythms of Pectinophora gossypiella (Pit­
sensitivity at 450 to 475 nm with a steep drop-off" tendrigh et α/., 1970). Complete action spectra have
in sensitivity at longer wavelengths and also towards been obtained for 2 species. Frank and Zimmerman
10.5h lO.S^h
100 (a) 1.5, I.0L,8.0D,I3.5L ' 75D,0.5L,2.5D,I3.5L
460
21.0
10.0
4.6
.37^53 3^0.^0^^ .43 .30
2.1
1.0
0.46
0.21
•0.5 .0
0.1
365 400 450 500 550 600 365 400 450 500 550 600
Wavelength, μτη
Figure 7. The action spectra for the effectiveness of near-monochromatic light pulses (indicated by
the symbol ®) in inducing viginopara-production in the aphid Megoura viciae. a., a 1 h light pulse
applied in the early night, 1.5 h after the beginning of the 10.5 h dark period, b., a 0.5 h light pulse
applied in the late night, 7.5 h after the beginning of darkness. The curve is drawn through the approxi­
mate 50% points (from Lees, 1971). Reproduced with permission of the National Academy of Sciences.