Mating Behavior in Littorina planaxis Philippi.
Daniel G. Gibson, III
Hopkins Marine Station of Stanford University
Pacific Grove, California
The habitat of the grey periwinkle, Littorina planaxis
Philippi (1847), well above high water on rocky western North
American shores, exposes this snail to desiccating sun and
wind and high temperatures to a greater degree than most other
intertidal organisms (Ricketts and Calvin, 1952). This degree
of exposure presents several problems to the process of re-
production. Fertilization is internal, which requires that
males must have some means of locating females, recognizing
them as such, and mating with them. This paper will attempt
to explore the mating behavior of Littorina planaxis and ex-
plain its method of locating other individuals, differences
in the behavior of males and females, and the anatomy and
mechanics of copulation.
Studies were made at Hopkins Marine Station, Pacific
Grove, Calif., during April and May, 1964. Egg-laying and
copulating individuals were seen throughout this period.
Ricketts and Calvint (1952, p.13) state that some individuals
can be found copulating at any time of year, but spring and
summer seem to be the times for heavy occurrences of mating.
Locating of Mating Partners
All movement and any subsequent locating of mating
partners in Littorina planaxis occurs when the rocks on which
these winkles are living are moist. This may be at night or
at any time during the day, and may take place even in direct
sunlight. Tide height and wave action are two of the main
factors that govern rock wetness. Males and females follow
mucus trails of other individuals over moist rock, with ap-
parent disregard for the sex of the snail that laid down the
trail they are following, using their cephalic tentacles to
feel their way along (Peters, 1964). Such following of mucus
trails has selective advantage, since it leads winkles to other
winkles, which may be potential mating partners.
Pairing Behavior
Males differ from females in that they immediately climb
upon the shell of any other Littorina planaxis individual
they encounter, usually over the head end of the shell and
often after touching tentacles with the other snail. Once on
the shell, the male will migrate to the right side and insert
his penis into the mantle cavity of the snail beneath him,
assuming the the pairing position shown in Figure 1. This
position is necessary for copulation, since the genitalia in
both sexes are found on the right side, behind the head (for
a complete illustration of Littorine anatomy, see Fretter and
Graham, 1962, Chapter 2, pp. 14-48). When the animal below
is a female, copulation may ensue. However, it appears that
success or failure of the tip of the penis in contacting the
bursa copulatrix of the female mantle cavity is the only way
in which a male can tell whether he has encountered a female
or another male. A male exhibits no defensive reaction to
having his mantle cavity explored by the penis of another male,
but the male above will soon climb off and seek another mate
if his probings do not meet with success. Observations were
made of 32 males placed on a moist rock in the laboratory and
watched for an hour and a half. No females were present.
During this time, 12 pairs formed, and the length of time that
each remained in the pairing position was recorded. None of
the male-male pairs observed persisted for more than 8 minutes,
and more than half of them broke up in two minutes or less. Be-
canselof theiryshort duration, male-male pairseare nõt prevalent
indthetfield atcanyionentime.1 Paralleliobservations ofg 32 females
inathe absence ofmales under the above conditions yielded no
pairing or climbing on one another's shells.
This apparent trial-and-error methodcof finding a mate
could be of great selective advantage in the range where Lit
torina planaxis lives.
A male becomes aggressive if he comes into contact with
another male on the shell he is exploring or intending to
explore. Ten battles resulting from such circumstances have
been observed, lasting between 30 seconds and 3 minutes, con-
sisting of the males jerkily pushing each other with the head
ends of their shells until one is dislodged.. Figure 2. shows
such a battle in progress. In two cases, the snail the fighting
males were on was also a male, but they apparently did not
know it, for the victor in each case attempted copulation with
the snail beneath him.
Often a third snail will be found very close to or touching
two paired individuals. In 50 checks of the sex of this third
individual, 48 were males, 2 females. The proximity of the
second male to the pair might be due to the fact that he has
just been pushed off the female and has not yet left the area,
or it might suggest a chemo-attraction of males to the vicinity
of females.
Normal (heterosexual) pairs persist for quite some time
after formation, often spanning an entire moist-rock activity
period of 10 hours or more. A field study of pairiformation
and persistence over one activity period is shown in Figure 3.
Pairs are seen to form over a wide range of dark and daylight
—
12



Figure 2. Mating battle;
Figure 1. Pairing position;
males push each other with
female from above, male from
head ends of shells until
left side. Part of male s
one is dislodged. X2.
foot visible. During pairing,
male's foot is entirely on
the other shell. X3.
KEY
Figure 3.
Field study of formation
-paired
and persistence of pairs
during a moist-rock ac-
tivity period. Pairs
formed
broke up
are seen to form over
=========== Same 9 wirh
-
—
a wide range of dark
new d
and daylight hours and
to persist for greatly
varying lengths of time.
Some animals paired more
than once (with dif-
ferent partners) during
the same activity period.
aaaaaaaa.
—

—
„-----
==
-
9AM
3AM
6 AM
-DAYLIGHT
hours, and are seen to persist for greatly varying lengths
of time. A certain percentage of snails are to be found
paired, with different partners, more than once during the same
activity period, as Figure 3. also shows.
The amount of pairing occurring at any time in the field
seems to be affected by the level of the tide. Figure 4. shows
two pairing frequency studies made over 25-hour tide cycles
a week apart, in order to show that the time shift in the tide
level causes a concomitant shift in the time of day that the
greatest and least numbers of individuals are paired. The
area observed was about 1 meter square in area, containing
about 100 Littorina planaxis individuals. Each hour the num-
ber of pairs and single winkles in the area was counted, the
percentage pairing calculated, and plotted. The second week,
as the tide came in later in the day, pairing percentage also
peaked later. In both studies, pairing percentage rose as
the tide came in, and then began to fall as the tide rose further.
An increasing amount of splash, capable of dislodging paired
snails, since in a pair only the female's foot is attached to
the substrate, may account for this.
MAA2
14
50



u 0
om
a
-7
6-
950
——
254



OL
Figure 4. Two 25-hour field studies of percentage pairing
in relation to tide level, made one week apart in order
to illustrate that a shift in the time of tide-level peaks
is accompanied by a time-shift in pairing peaks. Overall
drop in pairing the second week may have been due to ex-
tremely calm conditions, with little splash.


K
4
6
Fig. 5a. Male ex¬
5b. Beginning of in-
5c. Penis deep in mantle
tending penis prior
sertion. Front edge
cavity of female, as during
to copulation. It
is pushed forward and
sperm transfer. Longest
elongates downward and
in first, tip of penis
time penis observed remained
backward, becoming en-
trails behind. Fretter
inserted: 15 mins. Female
gorged with blood. Fe-
& Graham (1962) state
in Fig. 5c waving foot
male shown while attach
that mammaliform glands
about in an attempt to
ing foot to glass plate,
on leading edge of penis
right herself.
illustrating hows
may yield secretions
spreading of foot blocks
which help hold penis in
view.
place during copulation.
Copulation
The trial-and-error behavior displayed by male Littorina
planaxis in finding females suggests that copulation is the
first purpose of pairing, and probably occurs immediately
upon finding the female's genital opening. Figures 5a, b, & c
illustrate insertion of the penis. It is first extended
downward and backward, becoming engorged with blood and
elongating (5a.); as it continues to elongate, the front edge
is pushed into the mantle cavity (5b.); the tip trails in after
the front edge and is eventually inserted in the bursa copu-
latrix (5c.). Involuntary cilia in the penis cause a very
rapid flow of sperm and prostatic secretions down the seminal
groove that can be observed with a dissecting microscope.
The rate of flow here makes it very unlikely that copulation
takes very long, and it has been observed that sperm transfer
is not always occurring during the entire time the penis is
inserted. Of ten cases of copulation observed without disruption,
the longest time the penis remained inserted was 15 minutes,
more usually 4 or 5. The technique of observation was thelcol-
lection of dry, closed pairs stuck together with mucus which
were then placed under seawater with the female on her back.
Under these conditions the snails soon extended themselves,
and the male usually attempted to insert the penis. The only
drawback to this method of observation is occasional dis-
ruption of copulation as the female swings her foot around.
trying to find a substrate in order to right herself. An at-
tempt was made to remedy this problem by allowing the female
to contact a glass plate with her foot while upside down;
however, contact with the plate was followed by a spreading
and flattening of the foot which obscured the view of the penis
and the female's mantle cavity.
When the female is righted, the positionpofithe male
shell during pairing completely obstructs the view of the penis.
Since it is impossible to tell by male shell orientation whether
or not the pair is copulating, field studies of duration or
frequency of copulation are practically impossible. Disruption
of 100 active (extended) pairs in the field revealed only 17 in
which the male's penis was extended, so paired snails cannot
be regarded as always copulating.
Size Ratios in Male-Female Pairs.
A question arises as to what size males will be found with
pairediwithewhätssize females in the field, and whether any
selection for size of mate occurs. Figure 6 is a scattergram
of allothefpairseofttwoidifferent Littorina planaxis popula-
tions taken from two different areas, in which the size of
each female is plotted against the size of the male she was
paired with. The method of measurement used for both Figures
10
6 and 7 is shown in Figure 6a. All symbols between the diverging
slope lines in Figure 6 represent pairs in which the smaller
member is at least 2/3 the size of the larger. This suggests
itself to be the practical limit in size disproportion in pairs
found in the field. An overall survey of populations in which
only the most disproportionate pairs were selected yielded only
4 out of 84 pairs taken that failed to fall within the suggested
limits. A few of these limit-defining pairs are also recorded
on the scattergram.
A breakdown of size frequency by sex of the two scattergram
populations is presented in Figure 7. Here is suggested one
reason why more disproportionate pairs are not found: very
large males and females are not found in the same populations
with very small individuals. Therefore, in addition to the me-
chanical problems of copulation between Littorina planaxis in-
dividuals with grossly disproportionate genitalia, there are
undoubtedly many ecological pressures involved which keep large
and small snails apartiin nature, such as size as a factor in
withstanding wave shock, desiccation, etc. However, laboratory
experiments in which large males were kept isolated with small
females, and conversely, for two weeks yielded only one pair, out-
side the 2/3 limit but not significantly so, while control in-
dividuals under the same environmental conditions paired readily.
Figure 6. Scatter-
gram of all pairs of
two different field
papulations, plus
14
eral of the most
disproportionate
pairs found.any-
where, all illustra-
ting a practical
limit of disproportion
in pairs found in the
field: All symbols 9
between the diverging
slope lines represent
pairs in which the
smaller member is
at least 2/3 as large
as the larger member.
- pop. 41 (61 pairs)
x- pop. 2 (72 pairs)
o- pairs selected for
their disproportion
20-
54
210
6


4
8
m
at
mn
11
r „ *
14
16

Figure 6a. Method of
measurement used in
figs. 687. Across shell
aperture, from center of
lip to widest part of
whorl.
Figure 7. Breakdown of
size frequency by sex for
the two scattergram popu-
lations, showing that the
largest and smallest indi-
viduals do not occur in the
same areas.
Every half-millimeter
is plotted as a category,
i.e., 7.0-7.5 mm contains
25 females.
— pop. 1 2 (93)
— — - pop. 1  (126)
—— - pop. 2 ? (96)
- - - - - pop. 2 d' (120
Sex Ratio
As Figure 7 indicates, there are generally more males
than females in the population. A survey of 1000 unpaired
individuals yielded a ratioof two males to each female;
however, when the population as a whole and the large number
of snails that are pairing at any one time are considered,
the balance between the sexes is such that there is probably
little or no significance in the greater number of males
present.
Literature Cited
Fretter, Vera, and Graham, Alastair.
1962. British Prosobranch Molluscs. London: The Ray
Society. xvi755pp.; 310 figures.
Peters, Ronald.
1964. Function of the Cephalic Tentacles in Littorina
planaxis. Hopkins Marine Station of Stanford University,
Pacific Grove, California. unpublished.
Ricketts, Edward F., and Calvin, Jack.
1952. Between Pacific Tides; an account of the habits
and habitats of some five hundred of the common, con-
spicuous seashore invertebrates of the Pacific Coast
between Sitka, Alaska, and northern Mexico. Stanford,
California: Stanford University Press. xii-502 pp.;
134 figures.