AMER. ZOOL., 23:495-506 (1983)
Photosensitivity of Chromatophores 1
WALTER WEBER
Zoological Institute, University of Cologne, 5000 Cologne, Wexertal 119,
Federal Republic oj Get many
SYNOPSIS. Almost all major phyla of invertebrates and lower vertebrates display a direct
sensitivity of their chromatophores to light by either dispersing or—in rare cases—aggregating the pigment granules within the cell. This '"primary response" of color change is
an accessory component of the "dermal light sense" and characterizes the chromatophores
as an independent receptor for light and effector of the chromomotor response. Photosensitivity does not seem to be restricted to certain parts of the pigment cell but is rather
supposed to be a ubiquitous property of the chromatophore. Experiments on partially
illuminated chromatophores show that the photopigment, whose chemical composition is
still unknown, is localised within the plasma membrane or the cytoplasmic ground substance. Threshold responses for a just visible reaction are much higher than for background responses and have for some pigment cells been determined to be in a range
between 0.2 and 0.5 erg/sec/cm 2 . The physiological significance of the photosensory
reaction is closely related with thermoregulation and the protection of underlying tissue
against harmful radiation. The chain of events involved in photosensory transduction
remains to be further studied and can at present be interpreted only on the basis of related
phenomena like retinal pigment migration and the light-sensitivity of simple non-pigmented contractile systems.
INTRODUCTION
In the animal kingdom photoreception
is not restricted to photoreceptor organs
or other related structures but may in
numerous invertebrates and lower vertebrates be mediated by a remarkable light
sensitivity of the body surface and the
underlying tissue. Such extraocular photoreception has been called the "dermal or
diffuse light sense" and originally denned
"as a widespread photic sense that is not
mediated by eyes or eyespots and in which
light does not directly act on an effector"
(Millott, 1968). In the light of recent advances in ultrastructural and electrophysiological research a further specification is
given by Yoshida (1979): reactions involving cellular elements that are structurally
related to photosensory cells should be
classified as "diffuse photosensitivity,"
whereas photobehavioral reactions evoked
by direct stimulation of nervous tissue or
photoexcitable neurons should be referred
to as "neural" or "neuronal photosensitivity" respectively.
The phenomenon of extraocular photosensitivity has been extensively summarised by Steven (1963), Millott (1968), and
Wolken and Mogus (1979) and is judged
by the behavior of the organism or—as far
as the nervous system is concerned—by
electrophysiological evidence. The specific
reaction found after illumination may be
restricted locally to special parts of the body
or to organs, but it may also concern the
behavior of the whole animal. According
to Steven (1963), the principal types of
response are: a) the shadow or withdrawal
reflex, which is a quick response to a sudden change in the intensity of illumination:
b) orientation by bending of the body to
the direction of the incident light; c) photokinetic control of locomotion and speed
regulation; d) the direct action of light on
the chromatophore system which causes
color and shade changes in the skin of the
animal. In this essay an attempt will bemade
to define the different morphological and
physiological aspects of light-sensitivity of
chromatophores and to elucidate common
functional principles.
PHYSIOLOCICAL COLOR CHANCE
1
From the Symposium on Chromatophores and Color
Changes presented at the Annual Meeting of the
American Society of Zoologists, 27-30 December
1981, at Dallas, Texas
Light-sensitivity of chromatophores as
an accessory component of the dermal light
sense is an integral part of the physiological
495
496
WALTER WEBER
PRIMARY RESPONSE
Light
Darkness
®
DISPERSION
AGGREGATION
B
Darkness
Light
FIG. 1. Schematic illustration of the "primary
response" of color change. A: Light-induced pigment
dispersion: B: Darkness-induced pigment dispersion
(; e , tail darkening reaction).
color change mechanism in a variety of
invertebrates and lower vertebrates (Parker, 1948: Fingerman, 1963, 1965: Waring, 1963: Bagnara and Hadley, 1973). The
term "physiological color change" signifies
the rapid alteration in color and shade of
the integument, manifested as dispersion
or aggregation of pigment granules within
a stellate shaped chromatophore. The distribution of the pigment within the cell is
usually staged according to the system proposed b) Hogben and Slome (1931).
With respect to the regulation of pigment movements, two principally different
mechanisms can be distinguished: a) the
"secondary response," mediated by the eyes
and controlled by neural and/or endocrine factors: b) the "primary response,"
in which the chromatophore reacts directh
in response to the intensity of the incident
light. In the latter reaction the chromatophore reacts as an independent receptor
and effector, transducing light energy into
the mechanical process of pigment trans-
location and thereby causing color and
shade changes in the skin.
The primary color response as first
observed by Babak (1910) in larvae of the
axolotl and later extensively studied by
Laurens (1915) was originally defined as
pigment dispersion under the influence of
light, which is reversible in darkness (Fig.
1). However, as will be shown below, more
recent observations made on crustaceans,
fish and amphibians have demonstrated
that illumination may also lead to a pigment concentration while darkness induces
pigment dispersion.
In most types of chromatophores the
movement of pigment granules in .situ takes
place without any substantial alteration of
the cell outline. The tight anchoring of the
cell within the collagenous connective tissue stabilizes its spacial integrity and during pigment aggregation allows at most a
flattening of the dendritic processes by
simultaneous upheaval of the cytocentre
(Wise, 1969: Schliwa and Bereiter-Hahn,
1973: Obika, 1975). Isolated and cultivated chromatophores offish and amphibians, however, show drastic transformations from a stellate to a more spherical
shape during transition from the dispersed
to the aggregated state (Obika, 1976: Seldenrijk et «/., 1980).
The chromatophores of the diadematid
sea urchins represent a special variety: they
float within the intercellular fluid of the
epithelium without having any firm contact with the surrounding tissue and change
their shape depending upon the intensity
of the incident light. In complete darkness,
they are round to ovoid; when subjected
to light, the\ stretch out and flatten due to
centrifugal movement of the cytoplasm
containing the membrane-bound pigment
granules. The fully dispersed cell covers
an area many times larger than its original
size (Weber and Dambach, 1972, 1974).
In vivo, the primary response occurs in
pigment cells of larval forms or in blinded
or eyeless animals which do lack the ability
to perform background adaptation either
at that stage or permanently. Doubtless the
primar\ response ontogeneticalK represents the original reaction which, during
PHOTOSEXSITIVITY OF CHROMATOPHORES
development of larval forms to adult animals, becomes disguised by the secondary
response. Evidence supporting this
assumption stems from observations on fish,
reptiles and amphibians which after acquisition of the secondary response revert to
the primary as soon as they have been
blinded (Parker, 1948). There is no evidence for a secondary response being
replaced by a primary. The onset of acquisition of the secondary response varies with
species (Laurens, 1915; Bagnara and Hadley, 1973).
EXPERIMENTAL PROCEDURE
The exact definition of a chromatophore as an independent receptor and
effector is influenced by the kind of preparation used and the possible influence of
material factors in the surrounding tissue.
More or less unambiguous results may be
expected from isolated or cultivated chromatophores kept in an adequate physiological medium. If isolated pieces of skin
or embryonal tissue of heterogenous composition are used, it cannot be excluded
that illumination releases active factors
from other tissue components which may
influence the reaction of the chromatophores (van der Lek, 1967). Likewise, a
local reflex mechanism, still functioning in
excised pieces of skin might be considered
(Wells, 1932; Kleinholz, 19386): a morphological proof for such an interaction
has, however, so far not been substantiated. Furthermore, if blinded but otherwise intact animals are used, then the influence of humoral or hormonal factors on
the reaction of the chromatophores cannot
be ruled out (Brown and Sandeen, 1948).
497
erythrophores are reported to react to
light. A light-dependent dispersion which
Chicewicz (1956) observed in vivo in xanthophores of the shrimp Crangon crangon
cannot be interpreted clearly. In most cases
the light stimulus causes pigment dispersion irrespective of the kind of preparation
used. Special attention however should be
given to those experiments in which the
reverse effect, a light-induced aggregation
of pigment, is shown. The physiological
mechanism of this deviating reaction to
light and darkness is obscure. An interpretation can—at least in some cases—be given
on the basis of methodical or functional
peculiarities: In isolated scales of F undid us
heteroclitus, exposure to ultraviolet light
within a range of 185-290 nm leads to a
rapid pigment aggregation in melanophores (Spaeth, 1913). This chromomotor
response is reversible under conditions of
visible light. The pigment aggregation of
melanophores in isolated skin pieces of
Amb\stoma larvae illuminated by light from
an arc lamp is also attributed to the ultraviolet component (Laurens, 1915). Cultured melanophores of embryonic tissue of
Xiphophorus macidatus and of young animals also exhibit a light-dependent aggregation of pigment which, however, does
not begin until 2 days after the start of the
culture and occurs in no more than 50%
of the cells (Wakamatsu, 1978). In isolated
integuments of the embryos and the young
fish melanophores are in the dispersed state
and do not react any longer to changes of
light intensity, which may be due to surrounding substances or structures that prevent them from responding to light (Wakamatsu, 1978).
Another special feature, originally
observed in Xenopus larvae by Bagnara
(1957), is the "tail darkening reaction.'" In
In Table 1 a compilation is given of the contrast to the melanophores of the head,
most important results concerning light- trunk and myotome region which show
sensitivity of chromatophores and their background response, tail fin melanoubiquitous occurrence in different species phores react independently to local illuof invertebrates and lower vertebrates. mination with pigment aggregation and to
Apart from the brown chromatophores of darkening with pigment dispersion (van der
Hirudinea and Echinoderms, among the Lek, 1967). Cultured tail fin melanophores
four classical categories of pigment cells, of Xenopus laevis are also about 40% lightmelanophores, irido-leucophores and sensitive and react in the same way (SelOCCURRENCE OF PHOTOSENSITIVE
CHROMATOPHORES
498
TABLE 1. Occurrence of light-sensitive pigment cells.
Species
L.eec hfs
CAossiphonui lomplanata
Piumila geometra
I'luunla geometra
Type of cell
M
M
M
Direction
of
response
Nature
of
stimulus
whole animal
whole animal
excised pieces
D
D
D
V
V
Preparation used for
determination of response
V
References
Wells, 1932
Janzen, 1932
Weber and Molleken (unpublished)
Si'.i urchins
Ihailcma \eto\um
Ci'iitrostejihanus longiipinw.
red-brown
red-brown
skin pieces
skin pieces
D
D
V
V
Cenhnstef>hanu\ longispinus
red-brown
isolated cells
D
V
isolated cells
eyestalkless animal
eyestalkless animal
eyestalkless animal
D
D
D
V
V
V
V
('uistatca
I'altumoii \eirtitu\
Ftiltii'inini serratus
Sf,aima reticulation
Palaemonetei sp.
L
L/E
M
L/E
D
Yoshida, 1957
Kleinholz, 1938: Dambach
andjochum, 1968
Weber and Dambach, 1974
Knowles, 1940
Stephenson, 1934
Fingerman el al., 1960
r
H
Fingerman and Tinkle, 1956;
50
D
D
D
D
D
A
V
V
V
V
V
V
E
M
zoea/eyestalkless animal
eyestalkless animal
isolated legs
zoea
eyestalkless animal
eyestalkless animal/isolated
dactyli
excised pieces
blinded animals
Pasteur-Humbert, 1962
Rao, 1967, 1968
Brown and Sandeen, 1948
Coohill el al., 1970
Pautsch, 1953
Kleinholzand Welsh, 1937
Burgers, 1958
A
D
V
V
Noel, 1979
Smith, 1938
\iphophnnt\ maculatu\
M
M
isolated scales
cultured cells
A
A
uv
V
.\niijitichlh\s jonlnni
M
isolated scales
D
V
Spaeth, 1913
Wakamatsu, 1978: Wakamatsu
etal., 1980
Burgers, 1958
M
tail (in
A
V
Bagnara, 1957: Iga and
()c\l>i>de inacroceia
I iu pugilator
leu jiugilator
Ciaiigou craiigon
Htj)pnl\te variant
Manopijuts xrrnalis
I'rmewa eduli\
I-igia oceanica
L
L/M
M
L/M
L/M
E/M
hsh
Fttiiilulus heteroclitus
Amphibia
Xenojiu* laei'is
m
03
PI
JO
TABLE 1. Continued
Species
Type of cell
Preparation used for
determination of response
Direction
Nalure
response
stimulus
of
of
Xenojnts laevn
XenofiUi larva
Agalxchnii dacniiolor
Agalxrhnis darnicolor
Xciiojni.\ larvis
M
M
M
M
M
tail fin
tail fin
tail fin
partly covered (adult)
neural crest
A
A
A
D
D
V/nUV
liana escnlenta
liana esrulrnla
liana jnjnen.s
Amb\.\loma ligrnium
Ambxstoina lignnn in
M
M
M
M
M
neural crest
excised skin pieces
neural crest
local illumination
excised skin pieces
D
D
D
D
A
V
V
V
V
nUV
M
local illumination
V
D
M
M
local illumination
with denervation
isolated skin pieces
V
D
V
D
Reptiles
Chameleo sp.
Phtxnoioma blainviilii
Anal is srqneitrii
V
V
V
V
Reference
Bagnara, 1976
van der Lek, 1967
Seldenri|k el al.. 1979
Bagnara, 1974
Iga and Bagnara, 1975
Kulemann, I960; Obika and
Bagnara, 1963; Bagnara and
Obika, 1967; MacMillan, 1977
Bagnara and Obika, 1967
Zettner, 1956
Bagnara and Obika, 1967
Laurens, 1915
Laurens, 1915
Briicke, 1982: Zoond and
Eyre, 1934
Redfield, 1918; Parker, 1938
13
X
0
o
z
in
o
X
0
2
o
"0
X
o
70
Smith, 1929; Hadey, 1931;
Kleinhol/., 1938
M: Melanophores. L: Irido-leucophores. E: F.rythrophores. V: Visible light. nUV: Near ultraviolet light. D: Dispersion of pigment. A; Aggregation of
pigment.
ID
500
WALTER WEBER
denrijk el ai, 1979). Indeed, the reaction
can, as a result of possible dedifFerentiation
during the maintenance period be reversed
in pigment aggregation by darkness and
pigment dispersion by application of higher
light intensities. The concept of a reaction
pattern that deviates under the influence
of the surrounding medium is also supported by the observation of Bagnara
(1960), that after regeneration of excised
tail fins, the migrating melanophores
acquire photosensitivity only after reaching their definite positions in the tissue.
Recent observations have shown, that the
"tail darkening reaction" is not restricted
to Xenopus, a representative of the Pipidae,
but also occurs in tail fins of the taxonomically remote phyllomedusine frog Agalychnis dacnicolor (Bagnara, 1974: Iga and Bagnara, 1975). They both are filter feeders
and suspend themselves in water by rapid
undulating movements of the tail tip.
PARTIAL IRRADIATION OF SINGLE
CHROMATOPHORES AND LOCALISATION
OF PHOTOPIGMENT
The reaction of the pigment cell to light
raises the question of whether all regions
of the cell are equally light-sensitive or
whether the light stimulus is only perceived in specific light-sensitive areas and
then transmitted to other cell regions.
Experimental investigations into this problem have so far been conducted on only
two pigment cell types that respond to light
in opposite ways:
elicited even in small cell fragments. Moreover, partial illumination or darkening of
pigment cells causes locally varied and
appropriate pigment movements in the
individual cell (Gras, 1981). Since a differential sensitivity of both peripheral or centrally located parts of the cell was not ascertained, the assumption seems to be justified
that light sensitivity constitutes a common
and ubiquitous property of this pigment
cell. Possible candidates for structural correlates of light-sensitivity might be the cell
membrane, the cytoplasmic ground substance and/or the pigment granules. An
experimental approach has been performed by Gras (1981) with isolated cells
which, in the dark-adapted state, display
long pigment free filopodia protruding
from the pigmented cell body. Local illumination of a filopodium with a light spot
measuring 3 to 5 /urn in diameter, at a distance of ca. 25 tim from the edge of the
central pigment body, leads to a centrifugal migration of pigment granules and filling of the illuminated filopodium only.
Termination of spot illumination leads to
a centripetal movement of the pigment
granules. From this experiment the visible
pigment granules which have not been
irradiated may be excluded as candidates
for light perception as this is probably
located within the cell membrane and/or
the cytoplasm.
Tail Jin melanophores (Xenopus laevis)
van der Lek (1967) succeeded in demonstrating that illumination of tail fin melaSea urchin chromatophores
nophores with single light spots (diameter
Evidence for a local response was first 125 fim) and narrow light strips (width 7
obtained with a Japanese species Diadema nm) causes aggregation of pigment. When
2
setosum (Yoshida, 1956). If a non-pigment- low light energies (e.g., 4 erg/sec/cm ) are
ed area of a dark-adapted piece of epider- applied, aggregation is confined to the illumal surface was illuminated by a small light minated area. Upon stimulation with
spot 3 ^m in diameter, pigment granules radiation of2 higher intensities (e.g., 250
lying near the light spot moved in the erg/sec/cm ) pigment aggregation in the
direction of the spot and finally covered it, irradiated part is followed by aggregation
while the main cell bodies remained in the in adjacent, non-irradiated parts after a
dark-adapted aggregated state. Working time lag of 2 to 10 min between the onset
with isolated pigment cells of the mediter- of the local response and that of the
ranean diadematid Cenlrostephanus longispi- response in non-irradiated parts. As irranits Gras and Weber (1977) showed that diation of pigment granules is not required
light-induced pigment dispersion mav be for stimulation it is concluded bv the author
PHOTOSENSITIVITY OF CHROMATOPHORES
that the perception of the radiation occurs
either in the cytoplasm or in or near the
cell membrane.
501
sensitivity falls steeply, but is still clearly
measurable close to the UV range. The
correspondence of the action spectrum of
these chromatophores with the spectral
SPECTRAL SENSITIVITY OF
absorption of a reddish naphthaquinone
CHROMATOPHORES
pigment extracted from spines and soft tisThe most widespread photopigments in sue of Diadema antdlarum (Millott, 1957)
the visual system belong to a group ofhap- does for many reasons not justify the
locarotenoid proteins, which through their assumption that this pigment is involved in
linear structure as well as their cis-trans- photoreception (Millott, 1975).
isomeric form appear to be specially suited
The action spectrum of the tail fin melafor absorption of light quanta and trans- nophores of Xenopus hievis (van der Lek,
duction of light energy. Their accumula- 1967) was measured with respect to threshtion in membrane structures of the eye old response and shows a clear peak at 425
facilitates their isolation and chemical nm and a second shoulder at 450 nm. The
identification. Less frequently occurring curve closely resembles that of flavoxanphotopigments, found in visual systems as thin (Goodwin, 1955) which has peaks at
well as in neural light sense include the 421 and 450 nm. The relative high sensiflavins and haemoproteins (Wolken and tivity of the tail fin preparation in the UV
Mogus, 1979).
range with peaks at 265, 285 and 366 nm
The diffuse photosensitivity of chro- suggests absorption by pterine (van der Lek,
matophores, not being bound to any known 1967) whose widespread occurrence as a
specific organelle, makes localisation and pigment in insects and lower vertebrates
biochemical analysis of possible photore- has been summarised by Matsumoto et al.
ceptor molecules almost impossible and (1971). In the skin offish and amphibians
allows only indirect analysis through mea- Ziegler-Giinder (1956c/, b) found photolasurement of the spectral sensitivity of the bile pterines which are transformed by light
light reaction. Findings to date are sparse into pterinecarbonate showing two absorpand, due to the variety of methods tion peaks at 260 and 365 nm which equal
employed, of limited value as experimental those values measured by van der Lek
evidence. As shown in Table 2 the various (1967). Wakamatsu et al. (1980) also conchromatophores display measurable sen- cluded that the spectral sensitivity curve of
sitivity over a wide range (300-600 nm). Xiphophorus melanophores was that of a
A quantitative comparison between them pterine. However, despite the manifold
is however not possible, because the avail- biochemical role played by pterines in bioable data are mostly recorded without logical systems, it remains doubtful if they
regard to relative energy levels in different participate in a photoreacting system or
even as photoreceptive pigments in reguregions of the spectrum.
The first exact determination of the lating the chromomotor response.
spectral sensitivity of chromatophores with
In the shore living crab L'ca pugilalor.
respect to the relative threshold energy was near-UV between 300 and 400 nm is more
performed on skin pieces of the sea urchin than 100 times as effective as visible light
Diadema setosum by Yoshida (1957). These (400-700 nm) in eliciting pigment disperpigment cells show a distinct sensitivity sion up to a melanophore index of 3 (Coowithin a range of 450-500 nm with a peak hill et al., 1970). Larvae of the shrimp
at 470 nm. In isolated chromatophores of Crangon crangon do not adapt to backthe diadematid Centrostephanus longispinus, ground but also react upon illumination
which were measured under similar exper- with near-UV and violet (300-450 nm) with
imental conditions, the maximum relative a much more pronounced pigment disperspectral sensitivity is shifted into the blue sion than under conditions of illumination
region and shows a peak between 430 and with blue light, 450-500 nm (Pautsch,
440 nm (Gras, 1979). Below 430 nm the 1953).
TABLE 2.
Species
SIM ur< hins
Ihudemn selosum
Type of cell
Spectral sensitivity of chromatophores.
Preparation used for
determination of response
Direction
of response
Wave length
of maximal
sensitivity
(nm)
Reference
red-brown
red-brown
skin pieces
isolated cells
D
D
470
430-440
Yoshida, 1957
Gras, 1979
i ra jittgilator
M
isolated legs
M
F.
zoea
skin pieces
300-400
400-700
('.rattgon craiigon
I'rmewti edulis
D
(D)*
D
M
M
M
M
Crustacea
Fish
linululus heteroditus
Xtplwphotus maculatw
A
370-540
Coohill and Fingerman, 1976
Coohill and Fingerman, 1976
Pautsch, 1953
Noel, 1979
isolated scales
cultured cells
A
A
185-290
410
Spaeth, 1913
Wakamatsu el a/., 1980
skin pieces
tail (in
D
A
600
425
265,285,366
550-450
tu
Amphibia
liaiiii esmlenta
Xetwpus
r
For explanation of abbreviations, see 'Fable 1.
* Weak response.
Zettner, 1956
van der Lek, 1967
PHOTOSENSITIVITY OF CHROMATOPHORES
503
tional component of the dermal light sense
establishes
this phenomenon as more than
The statement of Steven (1963) that dermal light reactions are many times less sen- just an evolutionary relic (Millott, 1968).
sitive than optical light reactions is also true In some Crustacea the primary response
for the primary response of chromato- seems to be intimately associated with therphores. This is understandable given the moregulation and protection of body tissue
essentially sparser distribution of photo- against deleterious radiation (Fingerman,
pigment in chromatophores as opposed to 1965). Eyestalkless fiddler crabs disperse
structured photoreceptors. However, there their white pigment at temperatures above
is little quantitative data about the energy 20°C hereby increasing the heat- and lightlevels required to initiate a given degree dissipating area, while the melanophores
of dispersion in primary and/or secondary at temperatures above 15°C tend to aggreresponse. Recent quantitative experiments gate their pigment and thereby diminish
by Coohill el al. (1970) on Uca pugilator the surface area that absorbs light (Brown
show that a 100-fold higher degree of illu- and Sandeen, 1948). The greater sensitivmination, expressed in juj/cm2, is required ity of Uca melanophores to near-UV light
to produce pigment dispersion in mela- than to visible light is also consistent with
nophores of eyestalkless animals than that the hypothesis of a protective function for
effective in intact animals. Cultured mela- the underlying tissue (Coohill el al., 1970).
nophores of Xiphophorus maculalus are A thermoregulatory function of chroshown to have individual thresholds (Wa- matophores in lower vertebrates has been
kamatsu, 1978). The dose-response rela- extensively discussed by Bauer (1914) and
tionship between light-intensity and time Kruger and Kern (1924).
for full aggregation seems to fit the BunFor the darkness-induced tail darkening
sen-Roscoe law. In tail fin melanophores reaction in Xenopus larvae, the physiologof Xenopus laevis (van der Lek, 1967) the ical significance has been explained as a
intensity for a just visible threshold protective coloring in the tail tip which is
response, measured from the blue-green transparent in daytime. At night the melaregion of the spectrum, varies between 0.5 nophores with their pigment dispersed
and 2.0 erg/sec/cm 2 which corresponds to might prevent the reflection of stray light
a value of about 10"' to 4 X 10"' lux. This rays from the refractive iridophore layer
value is in accordance with the threshold (Bles, 1905: van der Lek, 1967).
sensitivity for most photokinetic responses
In diadematid sea urchins a protective
(Steven, 1963). Melanophores subjected to function has also been attributed to the
light flashes also show a reciprocal time- chromatophore system which, by very preintensity relationship within a low intensity cisely graded responses, may control the
range (van der Lek, 1967). In skin pieces sensitivity level of the underlying light-senof the sea urchin Centroslephanus longispi- sitive nervous plexus (Yoshida and Millott,
nus graded responses dependent upon the 1959: Millott, 1975: Yoshida, 1979). Moreintensity of the incident light were shown over, this is a fine example of the close
by Dambach (1969). Isolated pigment cells relationship between primary response and
of the same animal have individual thresh- neural photosensitivity in these animals.
olds for dispersion, the lowest measured at
440 nm in a range of less than 5 X 10'°
TRANSDUCING MECHANISM OF
light quanta/sec/cm 2 which is equivalent
LIGHT SENSITIVITY
2
to 0.2 erg/sec/cm . They also react to sinIn contrast to hormonally and neurongle light flashes of different duration and
intensity with graded pigment dispersion ally regulated pigment translocation in
and upon short time darkness with graded chromatophores, little is known about the
photosensory transduction and the chain
aggregation of pigment (Gras, 1979).
of events leading to the chromomotor
response. Theoretical models of this conPHYSIOLOGICAL SIGNIFICANCE
nection are loosely substantiated by findThe widespread occurrence of photo- ings about light-sensitivity of non-pigsensitivity of chromatophores as a func- mented cells like amoebae (Grebecki,
THRESHOLD RESPONSES
504
WALTER WEBER
1981), by experiments on retinal pigment
migration of arthropods (Hamdorf and
Hoglund, 1981), and by the assumption that
they display a common physiological mechanism.
In the special case of the "tail darkening
reaction" of Xenopus, the initiating signal
has been proved to be temporally independent of the subsequent pigment dispersion
(Iga and Bagnara, 1976). The reaction is
inhibited in O2-free medium but will reoccur after some delay in the presence of
light, when oxygen is returned to the
medium.
In describing a simple working model of
photosensory transduction, it could be
assumed that through illumination of a
membrane-bound photoreceptor molecule
and its concomitant conformational change
the intracellular concentration of specific
ions will be raised by changes in membrane
permeability and/or by release from internal stores. Ca++ could be a suitable candidate as a transducing agent between the
primary photoprocess and pigment migration, as it seems to play an important role
by modulating the function of cytoskeletal
elements in chromatophores (Schliwa and
Bereiter-Hahn, 1973: Byers and Porter,
1977) and retinula cells (Kirschfeld and
Vogt, 1980). A noteworthy finding concerning the problem of phototransduction
was recently presented by Wakamatsu el al.
(1980), working on cultivated fish melanophores: The light-induced pigment
aggregation is arrested in a dose-dependent fashion by theoph)lline, an inhibitor
of phosphodiesterase, as well as b\ cAMP.
From this result it is concluded that light
ma\ direct 1\ activate phosphodiesterase
thereby decreasing the intracellular cAMPlevel which regulates melanosome movement in pigment cells of poikilothermic
vertebrates (Bitensky and Burnstein, 1965:
Novales and Fujii, 1970: Schliwa and Bereiter-Hahn, 1974). Light-induced actuation of this enzyme, as also revealed in rod
outer segments of amphibia and mammals
(Bitensky rl al.. 1975) and the light-sensi-
ACKNOWLEDGMENTS
Financial support was granted by the
Deutsche Forschungsgemeinschaft.
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