Pharyngula

Tentacle Sex

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Doesn’t everyone just love cephalopods? I find them to be a fascinating example of a body plan radically different from our own, the closest thing to a truly alien large metazoan on our planet. I try to keep my eyes open for new papers on cephalopod development, but unfortunately, they are rather difficult to study and data is sadly thin and tantalizing.

I just ran across a pair of papers by Jantzen and Havenhand (2003a, b) on squid mating. That’s close enough to development for me!

First, let me explain a few general features of squid sex. Males produce elaborate spermatophores, illustrated to the left, which are complex packages of sperm. Huge numbers of sperm are stored centrally (1010 sperm, in some species), enclosed in a discharge mechanism that is triggered osmotically or mechanically—basically, it’s like those joke peanut cans that fling out a springy surprise when opened. Squid sex is a process of passing one of these clever novelty items to a female, where it will then go sproing when she lays some eggs.

Male squid do not have a penis. Instead, they have a pouch that opens into the mantle cavity, called Needham’s sac, where spermatophores are stored, and they have a specially modified tentacle, the hectocotylus, which is used to reach into the sac, scoop out a spermatophore, and and place it inside the buccal or mantle cavity of the female. In some cephalopods, the end of the hectocotylus snaps off and remains imbedded in the female.

Simple, hey? Of course, in the real world, it becomes much trickier, more exotic, and beautiful.

The first paper by Jantzen and Havenhand (2003a) describes the body patterns of squid courting and mating in their spawning grounds in South Australia. Cephalopods are famous for their ability to change color and pattern, and they give those capabilities a workout while trying to signal mates. They go through specific postural and chromatic activities that the authors describe; the body poetry of affectionate squid involves “rigid arms”, “upward curls”, and “peristaltic arm flares” while displaying “golden epaulettes” or “stitchwork fins” or “iridiscent sclera”. It’s lovely stuff. It makes my habit of picking out a clean shirt before going out on a date look rather pathetic—I’d have to take up ballet and gymnastics and start wearing luminescent make-up and glo-tubes if I want to keep up.

The second paper (Jantzen and Havenhand, 2003b) is more of a Kama Sutra of squid intercourse. Squid have a preferred position, illustrated below, in which the male swims upside-down above the female, and deftly scoops out a spermatophore which he deposits in the females buccal cavity, while the male is flashing “mantle margin stripe”, “dark arm stripes”, and “fin stripes”, and she is showing off “white dorsal stripes”, “golden epaulettes”, and “rigid arms”.

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Six-frame sequence of “male-upturned mating” behavior in Septoteuthis australis. The male (top) swims into position over the female (bottom, a). The male then rotates into the upside down position (b) and gathers spermatophores (Sp) from the funnel with the left 4th hectocotylized arm (c). The hectocotylized arm then moves down the right 4th arm that is positioned in the buccal area of the female (d) and and deposits spermatophores in this area (e). Copulation is complete, and the male rotates back to the normal swimming position (f). Total time elapsed = 3s.

Squid also like a little variety. With much lower frequency, they try head-to-head matings, or with the female on top (“male-parallel”).

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Percentage of all matings of each of the four mating types (male-upturned, head-to-head, male-parallel, or sneaker) identified in Sepioteuthis australis, with illustrations of the three mating types between paired individuals.

A particularly interesting case is sneaker mating. In these attempts, a male would coast up to a courting pair and attempt to flick in one of his spermatophores. Sometimes, while the sneaker was trying to make his deposit, he’d display the typical paired female body patterns of “dorsal white stripe”, “golden epaulettes”, and “rigid arms”; the females did not seem to appreciate these devious intrusions, and would most often jet away. The sneaker males were not only unpopular, but sloppy, and would splatter spermatophores onto the female’s head, arms, or mantle.

Some of the cool features of this animal system are the opportunities to study male competition and mating strategies. The fact that females are repulsed by sneaker males strongly suggests that female selection is important. And they are gorgeous to watch.


Jantzen TM and Havenhand JN (2003a) Reproductive behavior in the squid Septoteuthis australis from South Australia: Ethogram of reproductive body patterns. Biol. Bull 204:290-304.

Jantzen TM and Havenhand JN (2003b) Reproductive behavior in the squid Septoteuthis australis from South Australia: Interaction in the spawning grounds. Biol. Bull 204:305-317.

Comments

  1. #1 Lee Billings
    February 20, 2006

    Like listening to cetacean groans and whistles, cephalopod chromatophore displays always make me wonder what their significance is. What I’ve read concerning the intelligence of octopi, in particular, makes me think some of their dazzling chromatics approach language in terms of conveying symbolic information. Do you know if there’s been much research into this, PZ?

  2. #2 Corkscrew
    February 20, 2006

    Waitaminute, five Pharyngula posts in a row relating to tentacle sex? It’s Pharyngula so I’ve gotta read them… but be aware that you may be getting a bill from my shrink ten years down the line :-/

  3. #3 Monte Davis
    February 20, 2006

    “… a body plan radically different from our own, the closest thing to a truly alien large metazoan on our planet.”

    Analogous to my amateur fascination with coral reef ecology. While sunlight still matters to the algal symbionts, the layout is dictated at least as much by

    1) the need for firm attachment: hence acres of relatively barren sandy bottom, and then — with one small rock outcrop — corals growing on corals growing on corals

    2) access to goodies floating in the water (a 3D problem rather than the layered-2D problem of leaves competing for sun)

    So the, uhh, biome bauplan is very different from any forest on land. A reef (or a deep-sea vent with tubeworms etc.) is the closest to a truly alien landscape of life we can get.

  4. #4 Carlo
    February 20, 2006

    This entry is hilarious! I start cracking up when I try to imagine sneaker mating in human term.

  5. #5 Socialist Swine
    February 20, 2006

    Lee,

    I’m not a cephalopod expert by any means so I can’t really comment on the possibility that octopi might use their chromatophore displays as a sort of language but I used to have a pet O. bimaculoides and she would used to signal that she was hungry by approaching the glass, waving her tentacles and flash black. Or, perhaps I should say that I interpreted that behaviour as a request for food, she would only do it when I had forgotten to feed her for a day or two. I always found the display quite impressive, and it was effective for her as a means of getting a nice fresh mussel or a few shrimp.

  6. #6 Lee Billings
    February 20, 2006

    Swine,

    It’s funny – the “cephalopod experts” I’ve informally consulted about the issue say the same thing. They usually have a good anecdote or two and they definitely believe octopi are quite clever, but none as of yet have many answers about the content or complexity of the information conveyed by cromatophore displays. And understandably so – as far as I know there hasn’t been much research devoted to the topic.

    It’s definitely fascinating stuff, and I hope someone looks into it eventually (or directs me to those who already have!).

  7. #7 Socialist Swine
    February 20, 2006

    Lee,

    I think there’s the further issue is that when it comes to intelligence in other species people tend to treat animal behavaviour as an analogue to human behaviour. As PZ pointed out, cephalopods are quite alien, such being the case, I could understand how it would be rather difficult to say much about how their behaviour works in terms that would be easy to understand.

  8. #8 ekbworldwide
    February 27, 2006

    The sneaker males were not only unpopular, but sloppy, and would splatter spermatophores onto the female’s head, arms, or mantle.

    Well – who would like that?

  9. #9 Earthceuticals
    March 29, 2008

    I find myself being intrigued by these stories. Alien large metazoans… thats so true, we have the makings of science fiction movies right below our oceans. We really do need to explore here the oceans at home. Not that the search for space life isn’t equally intriguing, but we know for a fact there is life on our own planet we do not yet understand. And who knows where this research will go, maybe the next medical breakthrough will stem from research on deep sea organisms. Keep the interesting stuff coming in.

  10. #10 Nina
    April 24, 2008

    I was so excited by this post!! I LOVE cephalopods and always get a sneer from my friends for my enthusiasm whenever I see anything about octopuses, squids, or cuttle fish. I have a small collection of octopus paraphernalia so am glad when any new information comes out about them or their close relatives. May I again reiterate how excited this entry made me! yay for squid sex!

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