Cuttlefish woos female and dupes male with split-personality skin

ByEd Yong
July 03, 2012
4 min read

Imagine trying to talk to two people at the same time. I don’t mean just talking to one and then the other – I mean simultaneously saying different things to both of them. And in one of those conversations, you’re pretending to be someone of the opposite sex. That’s exactly the exchange that Culum Brown from Macquarie University has witnessed off the east coast of Australia.

The speakers were mourning cuttlefish – relatives of octopus and squid, and masters of camouflage. By rapidly expanding and contracting sacs of pigment in their skin, cuttlefish can turn their entire bodies into living video displays. Colours appear and vanish. Mesmeric waves cascade across their flanks. They can even produce different patterns on the two halves of their bodies.

Brown saw a male cuttlefish swimming between a female and a rival male, and displaying different messages to both of them. On his left half, the one the female could see, he flashed zebra-stripe courtship colours to advertise his interest. But on his right half, facing the rival male, he flashed the mottled colours of a female. As far as the competitor was concerned, he was swimming next to two females, oblivious to the act of cross-dressing/seduction going on right next to him. The cheater, meanwhile, prospers.

This is the first time that both tactics – cross-dressing and dual-signalling – have been seen at the same time, but both are used by other species of cephalopods (cuttlefish and their kin). The Caribbean reef squid frequently sends mixed messages from either side of its body, but it usually sends seductive signals to a female and “Back off” messages to an adjacent male. Meanwhile, the giant cuttlefish has weedy “sneaker males” that mimic the appearance of females. So disguised, they actually creep into the middle of a courting couple, and deviously inseminate the female right under the more powerful male’s tentacles.

Mourning cuttlefish gather in groups with a surplus of males, so there’s intense competition for any females that are around. Brown spent six years watching these gatherings, and saw many males courting females with one half of their body, while deceiving rivals with the other half. He only ever spotted this behaviour when two males were swimming with a female, but the dual-signals appeared in 39 per cent of such triplets.

(A canny diver can see through the male’s subterfuge because males have longer arms than females, and one of their arms has a modified tip for dispensing sperm. Why the cuttlefish can’t do the same is another matter.)

Sometimes, the ruse works. On at least two occasions, Brown saw that the lying male was actually fertilising the female, right next to his rival. On other occasions, the deceptive male is rumbled, as in the video above. “His cover is blown,” says Brown. “The approaching male has realised he is using the deceptive signal and has moved in to challange him.”

To Brown, the tactic is testament to the intelligence of cuttlefish, because the males use it in very specific social situations, when exactly the right number of on-lookers is present. They don’t bother if there are two rival males nearby, because there’s a greater chance that their deception would be uncovered, and they would be attacked.  They also don’t bother if there is one rival male and two females around. Instead, they just tried to court both females, possibly because it’s too hard to point the right displays at all the watching parties.

Reference: Brown, Garwood & Williamson. 2012. It pays to cheat: tactical deception in a cephalopod social signalling system. Biology Letters. http://dx.doi.org/10.1098/rsbl.2012.0435w

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