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« Give me creaturely over preacherly any day | Main | Squid nuptial dances »

Tentacle Sex

Category: DevelopmentOrganismsReproduction
Posted on: February 20, 2006 9:41 AM, by PZ Myers

old pharyngula
squidspermatophore.jpg

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".

sepioteuthis2.jpg
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").

sepioteuthis1.jpg
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.

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Comments

#1

Posted by: Lee Billings | February 20, 2006 10:10 AM

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

Posted by: Corkscrew Author Profile Page | February 20, 2006 10:20 AM

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

Posted by: Monte Davis | February 20, 2006 11:25 AM

"... 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

Posted by: Carlo | February 20, 2006 11:46 AM

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

#5

Posted by: Socialist Swine | February 20, 2006 12:28 PM

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

Posted by: Lee Billings | February 20, 2006 1:44 PM

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

Posted by: Socialist Swine | February 20, 2006 5:07 PM

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

Posted by: ekbworldwide | February 27, 2006 1:45 AM

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

Posted by: Earthceuticals | March 29, 2008 8:09 PM

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

Posted by: Nina | April 24, 2008 10:24 AM

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!

#11

Posted by: AdultGamer | November 8, 2009 3:50 AM

Actually, I surfed this site looking for Japanese Tentacle Porn.

I am very interested in Giant Squids myself; but, rely on Television Programming for information.

The story about the Octopus flashing black makes me think that she was expressing anger. Her approaching the glass and waving of her tentacles may have been her attempt at getting your attention.

As a cat person, I do know that Domestic Cats do communicate ideas with their various meows.

On one occasion, my barnyard cat while we lived in a city apartment community, captured a pigeon that had Mockingbird Wing Stripes. My cat captured it in the early morning hours for me took at; but, because it was too early for me to get up, she de-winged the pigeon. After presenting the pigeon to me, she went into a lengthy meow session telling me about her hunting and capturing the bird and asking me to identify it (I assume). My cat had no other interest in the bird...as a toy or as food.

While living in those same apartments, there was a time period that I had no money and no food; and, my barnyard cat captured Field Mice and Mockingbirds for me to eat.

Once, she even caught a large rat to feed her babies, as her means of weening them.

While living at my current residence, a 5 acre "booneyville" lot with a forest, there used to be White Mice with Grey Crescent Moons on their hind hips on the property. One day, when she returned from her hunting session, she gave me a lengthy meow session describing her search for the White Mice; but, couldn't find any (I assume).

My cat also "ka-ka-ka" to birds...the only time I hear her make that sound. I have never heard another cat make that vocal sound.

My barnyard cat died in 1999.

I have another cat that meows to me for food, to play with her, et cetera.

Each of these requests has a specific meow. Movement issues like "Don't step on me" or "Here I come" are variations of Reowrs.

It is intersting that our dogs don't have the same vocal speech range as cats do; although, certain species of dogs have specific accents of barks, growls, and howls.

#12

Posted by: AdultGamer | November 8, 2009 3:57 AM

Actually, I surfed this site looking for Japanese Tentacle Porn.

I am very interested in Giant Squids myself; but, rely on Television Programming for information.

The story about the Octopus flashing black makes me think that she was expressing anger. Her approaching the glass and waving of her tentacles may have been her attempt at getting your attention.

As a cat person, I do know that Domestic Cats do communicate ideas with their various meows.

Once, my barnyard cat while we lived in a city apartment community, captured a pigeon that had Mockingbird Wing Stripes. My cat captured it in the early morning hours; but, because it was too early for me to get up, she de-winged the pigeon. After presenting the pigeon to me, she went into a lengthy meow session telling me about her hunting and capturing the bird and asking me to identify it (I assume). My cat had no other interest in the bird...as a toy or as food.

While living at my current residence, a 5 acre "Booneyville" lot with a forest, there used to be White Mice with Grey Crescent Moons on their hind hips on the property. One day, when she returned from her hunting session, muy cat gave me a lengthy meow session describing her search for the White Mice; but, couldn't find any (I assume).

My cat also "ka-ka-ka" to birds...the only time I hear her make that sound. I have never heard another cat make that vocal sound.

My barnyard cat died in 1999.

Presently, I have another cat that meows to me for food, to play with her, et cetera.

Movement issues like "Don't step on me" or "Here I come" are variations of rowrs, not meows.

It is intersting that dogs don't have the same vocal speech range as cats do; although, each species of dog has a specific accent for barks, growls, and howls.

#13

Posted by: Hayley | November 21, 2009 3:10 PM

Prof. Myers,

I love your posts on cephalopods. I'm an English major, thus science is not my natural habitat, but biology is filled with such amazing writing material, I'm continually awe-struck by the information out there. My current writing project deals with cephalopods, and I'd love to see more entries on our tentacled friends. I know this blog entry is years old, but I hope for more! Thanks for writing!

Hayley

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