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Assessment of the mating history

of female pygmy octopuses and a
possible sperm competition
mechanism
ARTICLE in ANIMAL BEHAVIOUR FEBRUARY 1995
Impact Factor: 3.14 DOI: 10.1016/0003-3472(95)80218-5

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1 AUTHOR:
John Cigliano
Cedar Crest College
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Assessment of the mating history of female pygmy octopuses and a possible

sperm competition mechanism
Department

of Biology,

JOHN A. CIGLIANO
Boston University, 5 Curnrnington

Street, Boston, MA 023/S.

/IS. .4.

(Received
21 July IYY4: initial ncceptonce
14 August IYY4,
,$nal acceplance
17 October 1994: MS. nwnhu:
as-1081fci

Sperm precedence has been reported for a wide

range of taxa with internal fertilization
(see Smith
1984; Birkhead & Mnller 1992). For sperm precedence to occur, (1) females must be able to store
viable sperm for an extended period of time, (2)
there must be a delay between mating and fertilization, and (3) more than one male must mate
with the female during the delay (Waage, 1984).
Octopuses (Octopodidae:
Octopus) meet all three
criteria. Females store viable sperm in two oviducal glands for up to 10 months before laying
eggs, there is a considerable delay between mating
and egg laying, and females remain sexually receptive after mating (Mangold
1987). Moreover, males of some species exhibit prolonged
copulation,
transferring
several to many spermatophores (Wells & Wells 1972; personal observation). This has been termed sperm loading and
functions in some taxa as a sperm competition
mechanism to flush out or dilute the sperm of
previous males (Dickinson
1986; Birkhead
&
Hunter 1990).
Because of the evidence suggesting that sperm
precedence via sperm competition
might be occurring in octopuses, I examined the mating behaviour of the pygmy octopus (Octopodidae:
Octopus). I tested the prediction
that if sperm
competition
is occurring, a male will modify his
mating behaviour if he is mated to a recently
mated female, as observed in other taxa (e.g.
Corder0
1990). Specifically,
the second male
might transfer more sperm if sperm loading is
occurring, OF show a greater latency of spermatophore transfer if he is manually
displacing or
removing previously deposited sperm (Birkhead
& Hunter 1990).
Male octopuses transfer spermatophores
by
placing the ligula, the tip of the hectocotylus
0003%3472/95/030849+03

$08.00/O

(modified
third right arm), into the female:.
mantle cavity. After the oviduct is located. the
ligula is inserted and a spermatophore
is ejected
through the funnel. The spermatophore
is transported down the hectocotylus in the sperm groove
to the oviduct opening (Wells & Wells 1971). The
spermatophore
then goes through a spermatophoric reaction and free sperm are forced out
(Mann et al. 1966).
The pygmy octopus is a small (3040 g). benthic
octopus found from the northern Gulf of Mexico,
along the coast of Florida and in the northwestern
Caribbean Sea (Hanlon 1983). It has been referred
to incorrectly in the literature as Octopusjouhirzi
and is currently undescribed
(Forsythe & Toll
1991). The pygmy octopus was chosen because it
meets the three criteria for sperm precedence and
is one of the easier octopods to maintain
in
captivity (Hanlon 1983).
Ten female and five male octopuses were collected from St Joseph Bay, Florida and shipped to
Boston University, Boston, Massachusetts. I kept
the octopuses in isolation for at least 1 week
before the start of the experiment. Nine females
mated with two different males on consecutive
days (one re-mating attempt was unsuccessful). 1
chose males randomly
to be either the first or
second male to mate with that female. I concluded
the experiment (1) after the pair completed mating
(characterized
by separating and moving away
from each other) or (2) after 30 min had elapsed.
If no mating occurred, 1 chose another male
and placed it into the tank. This was repeated
until the female had mated. I made all observations under red light to simulate night, because
the pygmy octopus is nocturnal
(Mather 1978).
I recorded the following
data by sitting 1 m
from the tank and dictating observations into a

r 1995 The Association for the Study of Animal Behav~our

849

850

Animal

Behaviour,

microcassette recorder: duration of mating (from

insertion of hectocotylus to completion), latency
in spermatophore transfer (from insertion to
transfer of first spermatophore), and number of
spermatophores transferred.
I analysed paired observations for each female
(first male to mate and second male to mate)
using the Wilcoxon matched-pairs signed-ranks
test. A one-tailed test was used based on the
hypothesis that, if sperm competition is occurring,
the second male to mate would increase either the
number of spermatophores transferred or the
latency in spermatophore transfer.
Mating duration was 180.11 rt 80.7 s (x* SE)
and consisted of three distinct stages. During
Stage I (59.78 & 15.9 s), intromission occurred
but no spermatophores were transferred. Stage
II (39.80 f 16.0 s) began with arching and
pumping movements (Wells & Wells 1972) followed by spermatophores being transferred
(1.67 f 0.4 spermatophores). Stage III (83.90 %
16.3 s) lasted until the completion of the mating.
Stages I and III were similar in that the ligula
was inserted but no spermatophores were transferred. Males mated longer when they were the
second male to mate (103.67 f 13.0 versus
263.22 & 75.8 s; T=5.0, N=9, P=O.O2). This
increasewas not becausesecond males transferred
more spermatophores (2.10 f 0.4 versus 1.88 f
0.3; T= 13.0, N=9, NS) but becausethey more than
doubled the duration of Stage I (34.67 * 7.3
versus 84.89 * 29.3 s; Tx7.0, N=9, P=OM).
When males mated on consecutive days as a
second male, mating durations did not differ
(F, ,4= 0.04, P= 0.85: single classification ANOVA,
data were log-transformed). Also, a male that
mated as a first male, then as a second male on
consecutivedays, decreased the duration of Stage
I on the second day (52 versus 7 s). Becausemales
that mated on consecutive days did not increase
the duration of Stage I regardless of whether they
were a first or second male, spermatophore
depletion is an unlikely cause of the increase
in Stage I. Second males also tended to increase
the duration of Stage III (36.33 f 5.4 versus
13144 i 44.6 s; T=9.0, N=9, P=OO6).
Male pygmy octopuses were able to determine
the mating history of females, as indicated by the
increase in mating duration when mating with
recently mated females. Male octopuses possibly
used the presence/absenceof sperm to determine
whether females had recently mated. When a

49, 3

female pygmy octopus mated for the first time in

this study, she previously had not mated for at
least 1 week. It is likely that any remaining sperm
had migrated to the oviducal glands and would be
undetectable by the male. Recently mated females
(within 24 h), would still have sperm in the distal
oviduct because sperm takes at least 1 day to
migrate from the distal oviducts to the oviducal
gland (Jo11 1976). The sperm could therefore be
detectable by males. Corder0 (1990) found that
male damselflies, Ischnura graellsi, mated longer
with non-virgins and suggested that males
modified their behaviour because they were able
to detect the presence of sperm.
When females mate with multiple males, males
are expected to modify their behaviour to ensure
that their sperm fertilizes the majority of the
females eggs (Parker 1970). The dramatic increase in mating duration reported here strongly
suggests such a sperm competition function.
Duration was not extended by increasing the
number of spermatophores transferred (Stage II)
as would be expected if sperm loading is occurring
(Birkhead & Hunter 1990). Second males, however, did more than double the duration of Stage
I. This increase might occur because males are
either removing or displacing previously deposited
sperm from the females oviduct. Sperm removal
is widespread among dragonflies (Siva-Jothy &
Tsubaki 1989) and also occurs in damselflies
(Waage 1986). The amount of sperm removed is
related to the length of copulation (Corder0 &
Miller 1992). Sperm displacement by repositioning previously deposited sperm has been observed
in dragonflies, Crocothemis erythraea (Siva-Jothy
1984). Male pygmy octopuses place the ligula in
the distal portion of the oviduct and so are in a
position to manipulate previously deposited
sperm. The ligula is spoon shaped and may
function to scoop out sperm instead of to place
the spermatophore into the oviduct as has been
traditionally thought.
In conclusion, male pygmy octopuses seem to
be able to assessthe mating history of a female. If
the female has mated within 24 h, males increase
the duration of Stage I, suggesting that they are
removing or displacing previously deposited
sperm.
I thank Liza Bowman, Lauren Rader and
Dr Fred Wasserman for their help during this
study. I also thank Karen Cigliano for all her
support.

Short Communications
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