Sexual cannibalism by Octopus cyanea on a Pacific coral reef

Transcription

Downloaded By: [Hanlon, Roger T.] At: 14:48 7 April 2008
Marine and Freshwater Behaviour and Physiology
Vol. 41, No. 1, March 2008, 19–28
Sexual cannibalism by Octopus cyanea on a Pacific coral reef
Roger T. Hanlona* and John W. Forsytheb
a
Marine Biological Laboratory, Woods Hole, MA 02543, USA; bMarine Biomedical Institute,
University of Texas Medical Branch, Galveston, TX 77555-1163, USA
(Received 3 April 2007; final version received 30 July 2007)
Sexual cannibalism is rare in the animal kingdom. Although cannibalism is not
uncommon in cephalopods, here we report the first documented case of sexual
cannibalism. A large female Octopus cyanea was observed continuously for
2.5 days in Palau, Micronesia, when she was out of her den. On the second day, a
small male followed and mated her 13 times during 3.5 h while she continued to
forage over 70 m distance. After the 12th mating, she aggressively chased a
different small octopus that barely escaped by jetting, inking and swimming
upwards. Shortly thereafter, the original small male mated her a 13th time, but
subsequently she attacked and suffocated him and spent 2 days cannibalizing him
in her den. This sort of intraspecific aggression helps to explain several reports of
octopuses mating out in the open, a behaviour that may serve to allow the smaller
mate to escape cannibalism.
Keywords: Cephalopod; sexual selection; behaviour; mating system; reproduction;
mate choice
Introduction
Sexual cannibalism is a taxonomically rare phenomenon, having been documented only
in arachnids, insects (Polis 1981) and amphipods (Dick 1995), although anecdotal
evidence suggests its existence in copepods (marine crustaceans) and gastropod molluscs
(Elgar 1992). Sexual cannibalism can be defined as the killing and consumption of an
actual or potential mate before, during or after copulation, but always in the context of
courtship or mating (Elgar 1992), although the relationship between mate choice and
sexual cannibalism remains unclear (Prenter et al. 2006). In this study, we report a rare
case of sexual cannibalism in cephalopods during ethological studies (Forsythe and
Hanlon 1997; Hanlon et al. 1999) of foraging and reproductive behaviour of Octopus
cyanea Gray, 1849.
Mating systems of octopuses are poorly understood (reviewed by Hanlon and
Messenger 1996). However, the following general features are thought to be characteristic
of most species for which information is available: (i) individuals are solitary throughout
most or all of their brief lives (about 1 year; Boyle 1983); (ii) there is little or no courtship;
(iii) there is usually no obvious sexual dimorphism, except body size in some species;
(iv) males do not fight among themselves for females and thus no dominance hierarchy
*Corresponding author. Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543
USA. Tel: 508 289-7700. Fax: 508 289 7900. Email: rhanlon@mbl.edu
ISSN 1023–6244 print/ISSN 1029–0362 online
! 2008 Taylor & Francis
DOI: 10.1080/10236240701661123
http://www.informaworld.com
20
R.T. Hanlon and J.W. Forsythe
exists for access to females; (v) both sexes seem promiscuous and mating pairs are not
formed; (vi) mating periods are long, often in the order of 1 h; (vii) fertilization is internal,
females can store sperm for long periods and thus sperm competition is probable; and (viii)
there is no parental care for the young, although females brood the eggs (Hanlon and
Messenger 1996). In particular, little is known about sexual selection or sperm competition
in any octopus species.
As a generalization, each individual octopus’ strategy might be hypothesized to be
‘‘mate – or attempt to mate – with any conspecific octopus you meet, because you may not
meet another one.’’ Nevertheless, there are likely to be slightly different strategies for
males and females, particularly in habitats or populations in which individuals encounter
conspecifics more often or where the operational sex ratio is not 1 : 1. One such species is
the large, diurnally active O. cyanea Gray, 1849, in which several individuals can be found
in proximity to or near coral reefs in the tropical Indo-Pacific from Hawaii to East Africa
(Van Heukelem 1983; Forsythe and Hanlon 1997; Hanlon et al. 1999; Norman 2000). Near
Tahiti, occupied octopus dens were spaced ca. 30 m apart (range 14–98 m) (Forsythe and
Hanlon 1997) and their daily feeding forages covered a distance of 15–120 m; thus,
sometimes they would encounter another octopus.
Since many octopus species are known to be cannibalistic (see reviews in Boletzky and
Hanlon 1983; Boyle 1983; Huffard 2007), it is worth considering this fact as it relates to the
mating system. Hanlon and Wolterding (1989) suggested that octopuses, which generally
remain hidden in dens or stay cryptic when foraging (Hanlon et al. 1999), may mate in the
open because of the danger of cannibalism from the larger mate. Their suggestion stems
from the observation of a female Octopus briareus in a Bahamian saltwater lake (Aronson
1986) that was found in her den consuming a smaller male (the initial act of cannibalism
was not observed), then ca. 1 h later was mated by a small male (53 mm mantle length
versus her 85 mm mantle length) out in the open.
The most detailed account of octopus mating behaviour came from the laboratory
study of Wells and Wells (1972), who observed 46 and 141 matings of O. cyanea and
O. vulgaris, respectively. In this study, we observed and filmed 21 matings of O. cyanea in
their natural habitat. We used the technique of long-term daily focal sampling of female
octopuses and we were fortunate to capture on video a case of sexual cannibalism.
Materials and methods
We observed the natural behaviour of six O. cyanea Gray on the shallow coral reefs
(1–5 m) near Turtle Cove in the southern portion of the Palau Archipeligo, in western
Micronesia (latitude 7! 150 N, longitude 134! 300 E), although results are presented only on
the focal samples of a single male/female pair. The habitat is best described as coral rubble
and large stone boulders in the backreef; there were sporadic stands of live coral. From
midday 18 April 1995 to midday 21 April 1995, octopuses were observed continually
during daylight hours (ca. 05:30–19:00 h) by paired SCUBA divers (totally 14 divers) who
videotaped their behaviour while the octopuses foraged during the day. Several octopuses
were identifiable because of their size and from marks in the skin and they were never
touched or harassed in any way, rather divers remained at a distance to facilitate and
maintain habituation. The den of a large female octopus, which was conspicuous by its
large size (ca. 1–2 kg) and skin markings, was marked with a buoy and checked regularly
for 2.5 days (19, 20 and half of 21 April 1995), including spot checks at night to assess her
general activity period. The males were approximately 500–700 g.
21
We define mating as the act during which the male extends his third right arm (the
hectocotylus; modified with a groove along its length and a flat, cup-like tip) towards
the female and inserts it into her mantle cavity, where the arm tip is inserted into one of her
paired oviducts. Octopuses mate in two positions: one in which the male mounts
the female and the other in which he remains ‘‘at a distance’’ and extends his arm to her
mantle cavity. Octopus cyanea, like many octopuses, uses both positions but only the latter
was observed in this study. Two other male behaviours that are common are: the arch and
pump (Wells and Wells 1972). Spermatophores (each 2–3 cm long) are extruded from the
penis to the base of the hectocotylized arm with an ‘‘arched’’ posture followed by an
explosive ‘‘pump’’ action that sends the spermatophore down the grooved arm to the tip,
placing it into the oviduct (Wells and Wells 1972).
Results
The octopuses habituated to divers quickly and were observed and videotaped from
a distance of several meters; often the octopuses moved very close to the divers and seemed
oblivious to them.
Fourteen matings by one female were videotaped for analyses: 13 on 20 April and one
on 21 April (7 others were observed without video on 18 April and 19 April). Mating
durations (in minutes) for the 13 matings on 20 April, all with the same small male, were:
1, 2, 0.5, 1.5, 14, 5, 7, 1, 23, 12, 5, 5 and 2. All matings were ‘‘at a distance,’’ with the male
remaining separated from the female and extending his third right hectocotylized arm and
inserting it into the female’s mantle cavity, presumably into the oviduct (Figure 1). Arches
and Pumps, which are a proxy for spermatophore transfer by the male, were not visible in
the long-distance video. In all but one case, the males were smaller than the females and in
all the cases, the male initiated mating. No specific body patterns were associated with the
males; most were in a camouflaged pattern although they were sometimes a bit darker than
the surroundings. No behaviour that could be categorized as courtship was seen. Nor did
we see the bold striped pattern shown occasionally in this species (Van Heukelem 1983;
Forsythe and Hanlon 1997). All matings were out in the open except the 21st mating seen
on the last day.
Figure 1. Mating O. cyanea, with the smaller male (left) extending his specialized third right arm
(hectocotylus) towards the female and inserting it into her oviduct.
22
On 20 April, the large female octopus became alert at the front of her den at 05:30 h
and at 06:00 h began to slowly forage over the reef. At 07:00 h, a small male (ca. half her
weight, as calculated from his mantle length versus hers; see Aronson 1982) then followed
her for the next 3.5 h as she foraged more than 70 m away from her den. During this time,
he mated her 13 times ‘‘at a distance.’’ Matings 1, 2, 3, 4 and 13 (mean duration 1.2 min)
occurred while the female continued to forage; matings 5 and 12 (mean duration 9 min)
were stationary. Only twice did the female move away (i.e., reject him) when he extended
his arm to her. On 13 occasions, the male suddenly ‘‘jumped back’’ 0.5–2.0 m in brief
retreat, apparently sensing aggression by the female. In eight cases, the jump back
occurred after the female moved even slightly towards the male. In five cases, she showed
only a subtle head bob and a faint darkening of her body pattern. On five occasions, the
male blanched white briefly. In each case, he then cautiously approached the female again.
During the 11th mating, the female suddenly terminated the mating and swam at first
slowly and then very quickly for more than 20 m chasing another small octopus that was
zig-zagging around the reef trying to evade her. In this aggressive act of apparent
attempted cannibalism, the female nearly caught the octopus (Figure 2a–d) that escaped
by inking and jetting very swiftly towards the surface. It was noteworthy that this octopus
produced a continuous stream of ink for ca. 3 m as it jetted away.
Within 2 min, the original small male approached her, but backed off quickly 2 m as if
sensing aggression. He then extended his hectocotylus and inserted it into her mantle
(Figure 3a) for the 13th mating in the morning, while she continued to forage for 70 s. At
10:25 h, she moved slowly towards him (Figure 3b), then suddenly swept an arm towards
his head and forcibly knocked him backwards over the ledge of coral as he inked
profusely (Figure 3c and d). She quickly pounced and engulfed him in her arms and web
(Figure 3e–g) and then swam off with him (Figure 3h and i) "20 m into a cavity under
a coral. Thirty minutes later, the female moved to the top of the coral and a large amount
of ink was released (Figure 3j); we presume that the male was still alive and inking, but it is
possible that he was dead and the female had bitten into the ink sac or squeezed the mantle
tightly. She then swam back to the same den which she had occupied all the 3 days and
spent the next 24 h there without foraging while she continued to consume the male.
The next morning (21 April) after sexual cannibalization, another small male
approached her den very slowly (with apparent caution) and, without ever seeing the
female, extended his hectocotylized arm around a rock and into her den and mated her for
nearly 3 h. The female was receptive to mating without ever seeing him. Arching and
(a)
(b)
(c)
(d)
Figure 2. Attempted cannibalism of a presumed small male by a large female (ca. 1–2 kg). In video
print (a) the female has swum swiftly to the male, who inked and is jetting quickly upwards. In video
print (b), the female pursues him and extends an arm unsuccessfully to grab him. In video print
(c), the female ceases pursuit as the male. In video print (d), the female stops inking and vigorously
continues to jet towards the surface of the water.
(g)
(b)
(h)
(c)
(i)
(d)
(j)
(e)
Figure 3. Sexual cannibalism by the large female (a, bottom) on a small male who is ca. 0.5 m away. In (b), the female slowly swims towards him and
extends an arm to him (c) and forcefully pushes him backwards over a ledge (d) and engulfs him completely within her web and arms (e) as he then
struggles and inks (f, g). The female swims away with him (h, i) for 20 m. Thirty minutes later he is still alive and inking (j).
(f)
(a)
23
24
Pumping actions of the hectocotylized arm were conspicuous and occurred very often,
sometimes only 2–3 min apart. The study was concluded at this point due to prior
scheduling of the dive boat.
Discussion
Smaller male O. cyanea are at great risk of cannibalism when mating larger females. This
may help explain the previously ‘‘odd’’ observations of other octopuses mating out in the
open, exposed to predation (Hanlon and Wolterding 1989; Hanlon and Messenger 1996).
The risk of cannibalism to small male O. cyanea may be comparable to the risk of
predation.
The female O. cyanea in Palau continued to forage even during the act of copulation.
Van Heukelem (1983) reported one such similar observation on a Hawaiian coral reef.
Thus, while the female was gaining food and spermatophores, the male was foregoing food
to remain vigilant towards the female as he followed and then mated her. The overall tactic
of the males was to mate multiple times, in the day and at a distance, to maximize the
chance of (i) gaining fertilization and (ii) escaping an aggressive female. Yarnall (1969)
reported a single mating of a male with a smaller female; the male followed her to her den
and mated her, then dug himself a hole within touching distance. Van Heukelem (1966)
noted that such ‘‘double homes’’ are not uncommon on the Hawaiian reefs during the
breeding season and stated that males and females tend to be of comparable size.
Photographer Fred Bavendam (pers. comm., 2005) observed a single pair denning nearby
and mating over a 9-day period in November 2003 in Bali; many of the matings were out in
the open although in a few, the male approached the female near enough to extend his arm
into her den. Mate guarding has not been described in O. cyanea, although it was recently
described in Octopus abdopus (Huffard 2003). In their laboratory study, Wells and Wells
(1972) always paired a male with a smaller female, and they nearly always placed a male in
the aquaria for at least 12 h before introducing the female. ‘‘In a few cases’’ (op. cit.) the
female was placed in the aquarium first. Under such conditions, using smaller females,
Wells and Wells (1972) were unlikely to see cannibalism upon males.
Octopuses have two mating positions: at a distance or with the male mounting the
female (reviewed by Mangold 1989; Hanlon and Messenger 1996). Octopus cyanea is not
an exception. Wells and Wells (1972) saw both the mating positions, but in Palau, we saw
mating only at a distance. This is possibly a function of the size of the animals involved:
when comparably sized, or with the males larger, the mounting position may be most
common (e.g. Wells and Wells 1972); yet, this remains to be demonstrated. When the male
is smaller (as in our observations), mating at a distance is likely safer for the male because
it facilitates escape. Conversely, females much smaller than males may also be at risk of
cannibalism. Field biologists could provide data for this idea. Experimental trials with
selective mate pairings could test the idea that relative size of partners correlates with
mating position.
Ecological conditions could influence mating behaviour as well. In Palau, the large
female as well as the numerous small males were quite conspicuous and did not use
camouflage very often, especially compared to O. cyanea studied near Tahiti (Hanlon et al.
1999). Low predator density and the relatively large size of octopuses may lead to more
matings ‘‘in the open field of view.’’
Wells and Wells (1972) also noted that females often (48 times in 84 opportunities)
approached and touched males, with the result that the inactive males were ‘‘nearly always
25
stirred into sexual activity, so that he came out, pursued and mated with the female.’’ We
did not see the female initiate touching of males, but collectively as females moved about
the reef, males were attracted to females from distances as great as 10 m. In contrast to the
lab trials of Wells and Wells (1972), in all cases it was the male that approached and
touched the female. Our observations – limited as they are – indicate that the female was
more concentrated on foraging than mating over the 4 days of observation. Overall, these
two studies indicate that there is considerable variability in the mating behaviours of
O. cyanea.
Small males often ‘‘jumped back’’ defensively from females but this did not always
occur after a conspicuous movement of the female, which suggests that perhaps the female
was putting out a signal (chemical?) of non-receptivity or aggression and that the males
were able to perceive this communication. Recent work has shown that chemical signals
are used by some cephalopods in the context of reproductive behaviour (Boal and Marsh
1998; Basil et al. 2002; Buresch et al. 2003, 2004; Hanlon and Shashar 2003; King et al.
2003). The last mating that was observed – by a new small male – was with the female in
her den as she continued to consume the small male that she cannibalized the previous day.
This male approached carefully as well, but his mating was very different: Arches and
Pumps were observed every 2–3 min, and the mating lasted nearly 3 h. Such a change in
behaviour by the female is hard to explain; yet, it could be due to the satiated or
nutritional state of the female.
Sexual recognition has not been demonstrated unequivocally in octopuses (Boal 2006).
External sexual dimorphism hardly exists (but see Packard 1961; Voigt 1991), so visual
discrimination of sex is not likely. There is laboratory evidence suggesting that Octopus
bimaculoides can distinguish same sex from the opposite sex by odour, as measured by
changes in ventilation (Jean Boal, pers. comm., 2006). In any event, octopuses apparently
must get close or touch each other to distinguish sex, thus the small male O. cyanea in this
study were at risk of cannibalism due to the large size of the female. Male blue-ringed
octopus approach and mate female and male conspecifics equally often (Cheng and
Caldwell 2000), further suggesting lack of visual discrimination of sex.
Sperm competition is not documented in octopuses, but there are various suggestions
that it occurs, particularly the facts that octopuses have multiple mates and females have
two oviducal glands that store sperm (Cigliano 1995; Hanlon and Messenger 1996). There
is one report of a ‘‘sneaker male’’ O. cyanea mimicking a female but there are not sufficient
data or details to verify this possibility (Tsuchiya and Uzu 1997).
There is a general trend in which large females cannibalize smaller males in many
spider species (e.g. Buskirk et al. 1984; Elgar 1992; Andrade 1996; Persons and Uetz 2005).
Potential benefits to the female include nutritional gains and control of insemination
(Johns and Maxwell 1997; Schneider and Elgar 2001). Sexual cannibalism in various taxa
may occur before, during or after copulation, and the timing is thought to be related to the
fitness benefits/costs as well as to the intensity and direction of selection acting on male
traits (op. cit.). In O. cyanea reported here, cannibalism occurred after a mating attempt,
although many matings occurred beforehand with the same male. The female also
aggressively chased another small octopus (possibly a male) for 20 m and nearly caught it
(Figure 2). These limited observations suggest that sexual cannibalism in octopus can
occur in immediate association with sperm transfer or in its absence. There are no known
male octopus traits that function in sexual displays, except perhaps enlarged suckers or
ligula displayed in a few species (Packard 1961; Voight 1991; Hanlon and Messenger 1996;
Cheng and Caldwell 2000), but none are known in O. cyanea.
26
One ‘‘rule of thumb’’ found for wolf spiders (Persons and Uetz 2005) appeared to be:
‘‘if the male is not suitable as a mate, attack and eat him.’’ In our observations of
O. cyanea, the male had been mating the female throughout the morning, but with very
short durations and no obvious Arches and Pumps. If he was not successful in passing
spermatophores, the female may have decided that he was not suitable as a mate, and
thus she attacked and ate him. Concurrently, the female’s foraging success or failure may
have affected her state of hunger and influenced her decision to cannibalize the male.
Some male spiders are thought less likely to be cannibalized if they court and mate
females after the females have captured prey (Prenter et al. 1994; Fromhage and
Schneider 2004); in praying mantids, males preferentially mount well-fed females
(Maxwell 1999). In O. cyanea, this might help explain two things: that the males were
mainly mating females that were actively foraging (they capture small prey most of the
time; Forsythe and Hanlon 1997) and that the last mating we observed on 21 April
occurred when the female was in her den eating the male, a procedure that took at least
a day. This last event suggests that the male could sense that the female was well fed and
thus more approachable. Field observations of sexual cannibalism are difficult to
encounter in any species and a good deal more information is required before its role in
cephalopods can be addressed.
Acknowledgements
Fourteen volunteers from the organization CEDAM (Conservation, Education, Diving, Archeology
and Museums) helped with the observations and videotaping and their assistance was essential in
monitoring the behaviour of the octopuses continually; in particular, we appreciate the astute
performance of Susan Sammon and Collette Cody in capturing the cannibalism on video. Jean Boal
and Michael Maxwell kindly reviewed a late draft. We are grateful to the Marine Biomedical
Institute for providing travel funds.
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Sexual cannibalism by Octopus cyanea on a Pacific
coral reef
Roger T. Hanlon a; John W. Forsythe b
a
Marine Biological Laboratory, Woods Hole, MA 02543, USA
b
Marine Biomedical Institute, University of Texas Medical Branch, Galveston, TX
77555-1163, USA
Online Publication Date: 01 March 2008
To cite this Article: Hanlon, Roger T. and Forsythe, John W. (2008) 'Sexual
cannibalism by Octopus cyanea on a Pacific coral reef', Marine and Freshwater
Behaviour and Physiology, 41:1, 19 - 28
To link to this article: DOI: 10.1080/10236240701661123
URL: http://dx.doi.org/10.1080/10236240701661123
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Sexual cannibalism by Octopus cyanea on a Pacific coral reef

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