HOTOTAXIS AND PHOTOKINESES
LITTORINA PLANAXIS
Ecker
May 30, 1964
Recent investigations havereported some interesting, species-
specific differences in the phototactic and photokinetic responses
of British Littorina (Newell, 1958; Charles, 1961). It was decided
to study these reactions in one of the two Littorines common to

the American west coast. L. planaxis was chosen because of its
greater size and availability. The following observationsare a
selection of many that were made during the period April 25 to
oh The
May 28, 1964 at Hopkins Marine Station in central California. Coes
RESPONSES TO SUNLIGHT
L. planaxis collected from horizontal rock surfaces and
placed on a damp glass plate in direct sunlight invariably begin
to crawl in one of two general directions. The paths of 79 snails
were recorded and measured to the nearest 5 (grh 1). Since the
surface of the glass is featureless, this suggests that the snails
are orienting in some way to the sun itself. To test this supposi-
tion the glass plate upon which a snail was actively crawling toward
the sun was rotated 180. The snail also proceeded to turn 180
and again moved in the same direction as before rotation. The
same experiment was then repeated with snails moving in various
directions and in each case the snail turned 180 and moved in a
direction approximately parallel to its original one.
It has been suggested that this orientation is due to a type
of "light compass reaction" in which certain directions along the
24
guve
rays of the sun are prefered (Newell, 1945). However, L. planaxis
from horizontal surfaces tested in the laboratory by illumination
from the side proved to be entirely photonegative. Of the more than
50 snails tested, not one was observed to move toward the light
for more than a short distance before turning. Thus while a limited
light compass reaction may be responsible for the orientation of
L. littorea, where each snail can be either photopositive or photo-
negative, it does not explain the observed distribution of the
ntirely photonegative species, L. planaxis.
Mitsukuri (1901) reported that the Japanese snail, L. exigus
was also photonegative under normal conditions and that this effect
would serve to drive the snails away from the sea. To test this,
the tracks of 23 snails were measured on a glass plate placed
at the water's edge on beaches facing in two different directions
from the sun. The observations (figures 2,3) are admittedly insuf-
ficient to state conclusively whether the snails are orienting
to the sun or to the sea, but an obvious predominance in the direction
away from the se, as would be expected from Mitsukuri's explanation,
was not observed.
There remained the possibility that L. plansxis was orienting
in some way to the polarized light in the sky. This type of orienta-
tion has already been described for L. littorea, L. saxatalis, L.
littoralis, and L. neritodies, where it was shown that these snails
can orient to polsrized light by means of the intensity differences
based upon Fresnel's laws of refraction. Photonegative snails were
observed to orient slong the plane of polarization, and photopositive
r
Fiqure

snsils at right angles to it (Charles, 1961). To test this, light
from a 150 watt spotlight placed horizontally was reflected down-
ward by a mirror and the trails of 20 snails recorded and measured
to the nearest 2 under this arrangement. Examination with a polariged
filter showed weak but definite polarization of the reflected light.
The results are plotted on a polar graph with the 0-180 axis
figure
describing the plane of polsrization (gråph 4). L. planaxis, being
photonegative, oriented as would be expected along the plane of polari-
zation. The two snails that were crawling at right angles to this
plane were then tested with artificial light from the side. They
were photonegative. The control group of 20 snails was tested with
nonpolarized light from above adjusted to the same intensity (500 fc).
These snails did not move in any one direction long enough to enable
the determination of a prefered orientation.
Though a great many more snails would have to be tested in order
to fully establish the nature of this orientation, one other experiment
also indicated a sensitivity to polarized light. L. planaxis anesthe-
tized in an isotonic MgCl, solution for one hour and then unilaterally
blinded by the cauterization of the right eye invariably went into
"circus movement" (Fraenkel and Gunn, 1940) toward the blinded
side when illuminated by artificial light from above. Similar
treatment brought no effect upon snail illuminated from above by
light shining through a polaroid filter. The same lack of circus
movement in polarized light has also been recorded in L. littoralis.
(Charles, 1961).
27
Egten

Figure
VARIATION IN RATE OF CRAWLING AND
TURNING IN DIFFERENT LICHT INTENSITIES
Individual snails collected from horizontal rocks and dark-
adapted for 24 hours were tested on a glass plate for rate of turning
under varying light intensities. The light source consisted of two
150 watt spotlights from above shining through a 3" water filter.
The position of the snail was marked on the glass plate itself at
one-half minute intervals and the rate of change in direction determined
upon later examination of the mucus trails by measuring the angle
of deviation from the snail's proceeding straight path. Both right
and left turns were assigned positive values. The results are
summarized in Table 1. While the threshold for increased rate of
turning seems to vary (see results at 350 fc), all show a greatly
increased rate of turning at 1000 fc.
The same apparatus was now modified by the addition of a
25 watt light at one end of the glass plate. The snails would now
immediately move in the opposite direction. The speed of each snail
was recorded at one minute intervals by marking the glass itself. The
overhead light was switched on at 8 minutes; (see Table 2 below.)
The average speed of all 10 snails is presented for each
minute in graph 1. Immediately after the overhead light was turned
on, there was an initial reduction in the rate of crawl between 8
and 9 minutes, and a rapid increase between 9 and 10 minutes. This
reaction was consistent in 9 out of the 10 snails tested. There
wes
seemed te be no tendency to return to the original speed after
the first few minutes of higher light intensity.
Gogalor
Snail
9
Rafe
She/
Tatle
Vesor-ly
10 P.c.
56
20
35
Table
Crow
10
17
L
4
e
2.0
2.8
28
2.
2.7
2-1
2. 3
2.
Regrees
Tateasy
380
fe.
41
9 2°
71
32
Em
per
Minnle
Per
Re.
1000
131
2 51
570
71
mihu Te
1000
3./
3. 2
3.
3.
3. 3
3.7
3.0
3. 7
4. 0
47
a
f
20
20
t
one

To test whether an active incresse or decrease of light
intensity is necessary for a change in rate of orawl, fifty snails
were dark-adapted for 24 hours and then divided into two groups of
25 each. One group was tested in the laboratory, the other in bright
sunlight. The results are summarized in Table 3.
Thus it can be seen that L. planaxis behaves orthokinetically,
increasing both its rate of forward crawling and rate of turning at
higher light intensities. This reaction may be partly responsible
for the clustering effect noted in both L. littorea (Newell, 1956
and L. planaxis (Miyemoto, 1964) unpublished).
As pointed out by Fraenkel and Gunn (1940), the eventu-
result of any orthokinetic and klinokinetic movement serves toking
the animal to an area of lower light intensity.
It is interesting to note that L. planaxis moves at less than
one-half the rate reported for L. littorea. Under no conditions was
observed
and
a snail/to move faster than 4 cm. per minute,, This rate was only
approached by one snail at maximum light intensity.
TENTACLE WITHDRAWAL RESPONSE
Both L. planaxis and L. scutulata respond to a sudden dacrease
in light intensity by a rapid but comparatively short withdrawal
into their shell. Upon closer examination it was observed that
this withdrawal is only partial, the foot remaining in contact with
the substrate. Parker (1911) reported that locomotion in several
types of gastropods is accomplished by two separate mechanisms;
simple adhesion of mucus during forward motion, and actual suction
when any force is exerted on the shell. To test whether this with-
drawal reponse involves a change from one mechanism to another,
snail was placed on a plexiglass plate with a minute hole filled
with water drilled in it. As the snail erawled over the hole, a
bright light from above was switched off. Air bubbles were now
observed to rise in the hole, indicating an increase in suction as
the tentacles and head retracted. This was observed only for a
sudden but relatively small decrease in light intensity. Rapid
increases in light intensity brought no similar reaction, although
the sharp decrease in the rate of crawling as an overhead light
is switched on (see graph 1) indicates that the snail is not entirel,
unaffected by sharp increases in light intensity.
SENSITIVITY TO VARTOUS WAVE LENGTHS
While the tentacle withdrawal response to decreased light
is consistent with newly collected snails, the response quickly-
diminishes upon repeated trial. This rate of fatigue or adaptation
was used to test the color sensitivity of the L. planaxis eye,
or at least the color specificity of this response. Snails were
illuminated from below by a 150 watt spotlight controlled by a
rheostat. The snail was allowed to crawl on a glass plate placed
over Corning glass filter. Light was focused on the filter by a
water lens also serving as a heat filter. A second rheostat controlled
25 watt bulb also placed below the filter. This supplied enough
light to observe the snail's reaction as the main light source
was switched off.
One red, one green, and two blue filters were tested, as
well as a "control" with normal white light. In every case the
intensities were equilibrated by varying the intensitjes of the
150 watt light source as measured through the filter by a thermopile
and galvonometer.
The light was switched off every 15 seconds and turned on 7/
seconds later. When the snail showed no reaction, in three consecutive
decreasing
/light trials, it was considered "adapted." No snail was used for
any two trials, thus a total of 50 snails was tested. The results
o
are given in Table 4.

A Corning Blue 4553 filter was substituted for the original
sccua
4503 when analysis with a hand spectrometer showed that this first
filter allowed a considerable amount of green light to pass. The
slight sensitivity to red light can probably be explained by the
small amount of orange or white light not absorbed by this filter.
The reactions to red light consisted at best of a slight jerk of
both tentacles. Thus the tentacle withdrawal response is specific only
A
for light in the graen portion of the spectrum. This is consistent
with the findings on L. littorea, which orient only to polarized
light in the blue-green portions of the spectrum (Charles, 1961).
Snails retested up to 2 hours after their first adaption
showed only partial and sporadic withdrawal. However, snails left
on the filter at full light intensity for up to 30 minutes showed
no appreciable difference in response from that of freshly collected
e
snails. This wouid indicate that the tentacle withdrawal response
and adaptation is due to a nervous function rather than the bleaching
of any specific pigment in the eye.
Rafe
Table
o
erew!
Indoot5
Ouldeer)
Dlnt mive
7.14
Tuhle
Vanber
8lu
213
whTe
5n
12
12
10
1.5
5. 8
Wverafe
W114
Goelys
filler
loved
some

Cm
Rale
2.0 enfmin
enfmi
2.85
Reatlens
B/ue
Green
3
33
21
21
35
27
3/
20
28
33
30
25.2
a
showed
Perlaene
14.7
re5
hreen
171
per
19.
Vumber
20
2 1
50
Rel
a7
74.5
20
TAXIS AFTER EXTENDED PERTODS
PHC
LIGHT AND DARK ADAPTTON
In the area from which the test snails were obtained, L. plana
can be found both on dry rocks anditidepools. To test for any
difference in phototaxis samples collected from both locations
were kept in toth constant light and dark conditions for periods
up to four weeks. All tests were conducted under approximately one
foot of water in a standard l'x2' aquarium. A suspension of India
ink was added to the sea water in the tank and a 200 watt bulb
and rheostat at one end provided the light source. These conditions
esteblished a good light gradient ranging from 10 fcp at the bright
end to lfop in the middle. For each test 10 snails were placed
facing random directions in the center of the tank. After two hour-
the tank was drained and the direction of crawling established by
examining the carbon-dyed mucus trail. In each case 10 snails were
tested, however only the paths of the active snails are reporte
here.
Snails from tidepools. Of the snails tested immediately after
au were
collection, 7 were photopositive, 2 relatively indifferent (see Fig. 5).
After 24 hours of constant light conditioning, both the light- and
dark-adapted snails were photopositive without exception (see Fig. 6).
Both light- and dark-adapted snails were tested every 48 hours and
were, without exception, photopositive. On the 18th day, five of
the dark-conditioned snails suddenly became photonegative, one re-
mained photopositive. Of the light-conditioned snails, all 7 active
snails were photonegative. Both the light- and dark-adapted groups
had been entirely photopositive when tested on the löth day. Both
groups remained photonegative until the experiment was terminated
10 days later.
Snails from drx rocks. 20 k. planaris were collected from
dry rocks and immediately tested. 14 of these were photonegative,
3 were relatively insensitive. After 24 hours of either light-
or dark-adaption all were found to be photonegative. There is now
further evidence that 24 hoursjconstant environment not only "stabilizes
negative phototaxis, but actually strengthens it. Snails collected
in the field and negativejgeotactic will crawl slowly upwards even
when illuminated from above. After 24 hours of dark-adaption the
same snail will crawl downward, although their negative geotaxis
has not changed (Klabunde, 1964) unpubitsheu). Both the light- and
lark-adapted snails were then tested every 48 hours and no reversal
of phototaxis was observed. All remained nagatively phototacti-
for the three weeks the tests were continued.
In only one case were L. planaxis collected from dry rocks
esifvely
ever observed to be phototactic. 10 snails were kept entirely
submerged in sea water under normal light conditions in the labors-
tory. Tested after four weeks of submersion, 7 were photopositive
and 3 moved across the beam of light. None were photonegative.
Aekios
This is approximately the disteibutien that would be expected from
snails found in tidepools.
The same apparatus was also used to test phototaxis of uni-
laterally and totally blinded snails. 8 L. planaxis from a tidepoo.
and 6 from thre dry rocks were dark-adapted for 24 hours and anesthetized
-10-
ingisotonic solution of MgCl, for one hour. The right eyes were then
cauterized with a hot needle and the anesthetized snail immediately
placed in a test tank. The mucus trails showed that the snails
had moved and prececded in the expected direction, dry L. planaxis
frem
awayl and tidepool L. planaxis toward the light, with no abnormal
deviation from the course. (See Fig. 7) Totally blinded snails,
operated upon and tested in the same manner, proved to be totally
insensitive to light and proceeded on a path closely resembling that
of an unoperated snail in total darkness (Fig. 8).
S.
Littorina planaxis crawling on glass plates in the sunlight
orient themselves primarily along the sun's rays. A response to
the plane of polarization of the sunlight is the probable mechanism
involved.
ct
L. planaxis behaves ertkokinetically, increasing both its
rate of turning and its rate of forward crawling at higher light
intensities.
The Rittorine eye, as tested by the tentacle jerk response,
is sensitive only to green light.n Kante 9  vke pad
Snails found on dry rocks were always photonegative. Those
found in tidepools were primarily photopositive. In either case,
censTen!
the response is strengthened by 24 hours of either light or darkness.
Tratt

ot
Figure

Ejure

unilaTer ly
Soe
hormelt
ad
Vorae
she
Bided
phelopes.Tive
Dark
Snel
adeg sed
Sahl:2
Figute


—
Frute
Te1.Hy
Oladet
Sa
ITERATURE CITED
larles, G.H. 1961. The orientation of Littorina species to polarized
light. Jour. Exp. Biol. 223:189.
Fraenkel, F.S. and Gunn, D.L. 1940. The Orientation of Animals:
Kineses, Taxes and Compass Reactions. Oxford.
Fretter, V. and Graham, A. British Prosobranch Molluscs. Published
for the Ray Society; Abelard and Son, Limited, Bartholomew
Press, Dorking, England. 1962.
itsukuri, K. 1901. Negative phototaxis and other properties of
Littorina as factors in determining its habitat. Annot.
Zool. Japan. 4 (1):1-19.
Newell, G.E. 1958. An experimental analysis of the behavior of
Littorina littorea (L.) under natural conditions and in the
laboratory. J. mar. biol. Ass. U.K. 37:241-266.
Newell, G.E. 1958. The behavior of Littorina littorea (L.) under
natural conditions and its relation to position on the shore.
:229-239.
J. mar. biol. Ass. U.K.
Parker, G.H. 1911. The mechanism of locomotion in gastropods.
Journ. of Morph. 22: 155-170.