Pharyngula

When male squid get together with their female friends, they have a couple of nuptial options: they can go ahead and use their charm to court the female, or they can just start poking her with tentacles full of sperm in mating frenzy. Now some of you guys might be thinking the latter option sounds good (what's the point of living the life of a squid if you can't be selfish and uninhibited, right?), while the ladies and gentlemen here might think the former is better. A study of the mating behavior of squid close-up and in the lab suggests that it's true: taking one's time and mating cooperatively is much more likely to get the sperm in the right place and improve the likelihood of reproductive success. And as a bonus it's got some lovely photos of squid caught in flagrante.

Here are the two most commonly observed patterns of squid mating observed. On the left is male-parallel (MP) mating, and on the right is male-upturned (MU) mating.

MP mating occurs as part of courtship, and males typically guarded their mates, fending off any other approaching males. The activity was also only carried out during the egg-laying period of the female. Males move to the ventral side of the female, and reaches up to caress her mantle with his right arm IV, and then inserts right arm IV into her mantle opening. He then ejaculates sperm packets onto his left arm IV (his hectocotyl arm), and inserts that arm into her mantle, depositing the spermatophores. The whole process takes on average about 15 romantic seconds, and the male completes everything successfully 95% of the time. The pair also stay together, and may repeat the mating at approximately half hour intervals. Here's the action in a closeup:

MU mating was more abrupt. Males got behind the female, and flipped upside down. Then, while holding her in place with arms I and II, he scoops up some spermatophores with his hectocotyl arm and inserts them into her buccal cavity. Average mating time was about 8 seconds, and was successful only about 44% of the time—females tried to escape!

There's another advantage to courtship and MP mating: it gets the sperm to exactly the right place, and maximizes the probability of paternity. The authors opened up a few females to analyze where the sperm packets were planted, and the diagram of the squid reproductive tract shows the result: instead of getting sperm all over her face in the MU mating, he has put it right outside her oviduct.

One of the results of the study, though, was the discovery that MP mating was a privilege of the larger males. The smaller, and presumably less desirable males, were the ones who resorted to MU mating. Although squid appear rather promiscuous, what this suggests is that there is also a significant component of female mate choice.

Wada T, Takegaki T, Mori T, Natsukari Y (2005) Alternative mating behaviors dependent on relative body size in captive oval squid, Sepioteuthis lessoniana (Cephalopoda, Loliginidae). Zoological Science 22:645-651.