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Female impersonation as an alternative reproductive strategy

in giant cuttlefish
Mark D Norman, Julian Finn and Tom Tregenza

Proc. R. Soc. Lond. B 1999 266, doi: 10.1098/rspb.1999.0786, published 7 July 1999

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Female impersonation as an alternative

reproductive strategy in giant cuttlesh

Mark D. Norman*, Julian Finn{ and Tom Tregenza{

Department of Zoology, University of Melbourne, Parkville,Victoria 3052, Australia

Out of all the animals, the cephalopods possess an unrivalled ability to change their shape and body
patterns. Our observations of giant cuttlesh (Sepia apama) suggest this ability has allowed them to evolve
alternative mating strategies in which males can switch between the appearance of a female and that of a
male in order to foil the guarding attempts of larger males. At a mass breeding aggregation in South
Australia, we repeatedly observed single small males accompanying mating pairs. While doing so, the small
male assumed the body shape and patterns of a female. Such males were never attacked by the larger mate-
guarding male. On more than 20 occasions, when the larger male was distracted by another male intruder,
these small males, previously indistinguishable from a female, were observed to change body pattern and
behaviour to that of a male in mating display. These small males then attempted to mate with the female,
often with success. This potential for dynamic sexual mimicry may have played a part in driving the
evolution of the remarkable powers of colour and shape transformation which characterize the cephalopods.
Keywords: alternative mating strategy; cephalopod; giant cuttlesh; mimicry; Sepia apama; Spencer Gulf

undertaken into the biology, behaviour and reproduction of this

1. INTRODUCTION
cuttlesh. The species is sexually dimorphic with males posses-
Alternative male mating strategies have become the text- sing longer arms than females, these arms being fringed by
book example of evolutionarily stable strategies. Examples wide, banner-like webs o the ventral margins (gure 1a).
of dierent males employing dierent behaviours and/or Mating consists of males courting females with elaborate colour
life histories are known from many animal groups, displays (dark zebra stripes rapidly pulsing across the dorsal
including all vertebrate classes (Arak 1984) and a number mantle with extended white banner-like webs o the arms).
of invertebrates (Forsyth & Alcock 1990; Sauer et al. 1997). Copulation occurs by coupling head to head, with the male
A common situation has males which are either large and transferring sperm packets to a pouch below the beak of the
able to guard females or resources, or small and reliant on female (gure 1b). During most of this process, the female
`sneaky' matings (Taborsky 1998). One method by which displays a mottled body pattern of dark blotches on a white
sneaks escape detection by larger males is to impersonate a background (gure 1b). Following copulation, the female then
female, something which typically requires males to have a proceeds to lay large eggs singly, attaching them to the under-
life history that makes them physically similar to females. surface of rock crevices or boulders. Eggs are fertilized by being
Theoretical models (Owens & Hartley 1991) suggest that passed over the sperm receptacle below the mouth. The male
constraints on males' ability to vary their phenotype may remains in attendance, mate guarding the female from other
be necessary for `honest signalling' of male quality to suitors. In larger breeding aggregations of giant cuttlesh, males
evolve, giving opponents the opportunity to assess compe- frequently engage in ritualized display combat with other males.
titive ability. If males are able to change their appearance Disparate size typically results in the loser eeing without
facultatively, then the system will be less stable, increasing physical combat. In more even contests, battles can escalate to
the likelihood of an arms race between impersonators and seizing and biting opponents. Many males exhibit bite scars or
males attempting to avoid deception. missing arm tips.
In Spencer Gulf, South Australia, extensive soft sediment
substrates and limited rocky reefs have resulted in massive and
2. STUDY ANIMAL AND METHODS
unique breeding aggregations of giant cuttlesh. Every year
The giant cuttlesh (Sepia apama) lives in the shallow tempe- between April and July, these animals congregate in their thou-
rate waters of southern Australia, from southern Queensland to sands on small shallow rocky reefs in the region to spawn
north-west Western Australia. No detailed studies have been (Moran 1998). Breeding animals can be easily approached and
will mate, lay eggs, mate guard and ght within centimetres of
*
Author and address for correspondence: Marine Biology, James Cook observing divers.
University, Townsville, Queensland 4811, Australia
(mark.norman@jcu.edu.au).
{ Present address: Institute of Antarctic and Southern Ocean Studies, 3. RESULTS
University of Tasmania, Hobart, Tasmania 7001, Australia.
{ Present address: School of Biology, University of Leeds, Leeds While investigating male mate-guarding behaviour
LS2 9JT, UK. during spawning, we repeatedly observed male ^ female

Proc. R. Soc. Lond. B (1999) 266, 1347^1349 1347 & 1999 The Royal Society
Received 1 March 1999 Accepted 12 March 1999
 Downloaded from rspb.royalsocietypublishing.org on March 20, 2014

1348 M. D. Norman and others Female impersonation in giant cuttlesh

Figure 1. (a) Male giant cuttlesh in typical courtship display, characterized by extended banner-like web margins o the arms
and fast-moving, black zebra stripes across the mantle. (b) Mating couple with female (left) showing mottled body pattern.
(c) Satellite male (right) with retracted web banners and mottled body pattern in attendance with large mate-guarding male and
egg-laying female. (d) Mottled satellite male (left) attempting to mate with guarded female while larger males are in display
combat. As this combat escalated to physical attacks between the larger males, the satellite male went on to mate successfully
with the female.

pairs being shadowed at close proximity by what

4. DISCUSSION
appeared to be a second female (on the basis of short
arms without banners and the mottled body pattern Due to the remote location of this breeding aggrega-
typical of females; gure 1c). However, on occasions when tion, its exposure to adverse weather conditions and the
the large male of the pair was engaged in display or limited breeding season of giant cuttlesh (April^June),
physical combat with other large males, the satellite indi- the authors have not yet been able to undertake detailed
vidual frequently moved towards the female and quantitative surveys of the behaviour described. At this
attempted to mate with the female (gure 1d), often with stage, information on dynamic female mimicry in giant
success. In approaching the female and during mating, cuttlesh remains qualitative. However, our direct obser-
the behaviour of smaller males varied, with some vations and video footage noted more than 20 examples
showing male displays of banners and moving stripes and of such mimicry in satellite males, suggesting that the
others remaining in female guise. Returning large males behaviour is relatively widespread in this large breeding
had varied responses ranging from ignoring the mating aggregation and possibly within the species as a whole.
couple to aggressive separation of the pair. On separation, As there is no information on ageing in S. apama, it
satellite male behaviour varied from attempts to mate remains unclear whether the behaviour observed in the
guard the female (using typical male displays and smaller males is a strategy of younger males or is an alter-
extended web banners) to repeated female impersonation. native strategy for undersized males of equivalent age to
The satellite male typically remained close to the large their larger competitors.
male and female. When the satellite male donned the Few studies have examined cephalopod mating beha-
mottled body pattern (gure 1c), agonistic behaviour of viour in the wild (see the summary in Hanlon &
the large male immediately ceased. In contrast, large Messenger (1997)). None of these studies have reported
males would chase displaying males considerable female impersonation as a mating strategy. However, the
distances away from the female they were guarding. In paucity of such studies means that it is entirely possible
the absence of rivals, males previously observed that similar behaviour occurs in other cephalopods, parti-
mimicking females displayed typical male body patterns cularly shallow and clear-water species.
and shape and courted females in identical fashion to Cephalopods are less constrained in their ability to
larger males. vary their physical appearance than perhaps any other

Proc. R. Soc. Lond. B (1999)

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Female impersonation in giant cuttlesh M. D. Norman and others 1349

group. It is likely that pressure from visual predators and Forsyth, A. & Alcock, J. 1990 Female mimicry and resource
the need to avoid detection by visual prey were the defense polygyny by males of a tropical rove beetle,
primary driving forces in the evolution of cephalopod Leistotrophus versicolor (Coleoptera, Staphylinidae). Behav. Ecol.
skin. The sexual mimicry behaviour reported here may Sociobiol. 26, 325^330.
Hanlon, R. & Messenger, J. 1997 Cephalopod behaviour.
make `honest signalling' less likely (Owens & Hartley
Cambridge University Press.
1991), raising the intriguing possibility that the benets of Moran, P. A. G. 1998 Live fast and die young: the story of the
dynamic sexual mimicry may also have contributed to giant Australian cuttlesh. Aust. Geogr. 51, 70^87.
the evolution of these transformation abilities, particu- Owens, I. P. F. & Hartley, I. R. 1991 Trojan sparrows evolu-
larly in the most dramatic colour-changing groups such tionary consequences of dishonest invasion for the badges-of-
as the cuttlesh. status model. Am. Nat. 138, 1187^1207.
Sauer, W. H. H., Roberts, M. J., Lipinski, M. R., Smale, M. J.,
Hanlon, R.T.,Webber, D. M. & Odor, R. K.1997 Choreography
REFERENCES
of the squid's`nuptial dance'. Biol. Bull. 192, 203^207.
Arak, A.1984 Sneaky breeders. In Producers and scroungers (ed. Taborsky, M. 1998 Sperm competition in sh: `bourgeois' males
C. J. Barnard), pp. 154^194. London: Croom Helm. and parasitic spawning. Trends Ecol. Evol. 13, 222^227.

Proc. R. Soc. Lond. B (1999)

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