Warning, super-esoteric: stumped on onychoteuthid mating behavior

[Tintenfisch]

OK, gang. Got a puzzle for you. I don't know the answer myself, and have spent a good long while mentally turning over the pieces without making any headway.

Males of the family Onychoteuthidae are known to mate by hydraulically implanting spermatophores (packets of sperm) into the mantle musculature of the female. In some genera, these spermatophores are implanted in rows, in longitudinal cuts that, we assume, are made by the male's hooks or beak.

While at the Smithsonian, I observed a spent female Onychoteuthis, with spermatophores implanted in ventral cuts in her mantle tissue, similar to those photographed near the bottom of this page on the Tree of Life. In the Smithsonian specimen, the cuts were longitudinal, but the strangest thing was the implanted spermatophores. They were implanted in bunches, with most of the spermatophore embedded in the tissue perpendicular to the cut, but the part of each spermatophore that remained protruding from the external surface of the female's tissue had a weird, hollow round bulb at the end of it (see attached photo). Now, I also observed several specimens of what I believe were males from the same species, and their spermatophores (un-discharged) did not have this structure. I have seen the same thing on a male/female pair from a different species of Onychoteuthis from Australia as well - the spent female has these bulb-tipped spermatophores implanted in cuts, while the male has very different spermatophores, in this case implanted in his own viscera, which I assume happened during capture. (Fairly common.)

Soooooo, anyone want to take a crack at what could be going on here??? Are the bulbs an artefact of the force with which the spermatophores are implanted? Why are they hollow? Why do they look like they exploded? Are they functional in some way? If they are an artefact of implantation, why didn't the male of the Australian species have them on the spermatophores embedded in his mantle?

Speculations are most welcome! The wilder the better! Welcome to an eensy-weensy but representative corner of my thesis.

 

[Steve O'Shea]

Hmmmmmmmmmmmmmmmmmmmmmm; I aint neva seen nuttin like that Kat!!

Surely they cannot be a copepod if you have seen this on several specimens, but it sure is most bizarre!

 

[cuttlegirl]

Which way do you think the spermatophores were implanted? Is the bulb at the end or the beginning???

When the spermatophore is implanted it turns itself inside out, right? I think the term is eversion... Do these squid spermatophores have a cement body?

Could it be an artifact of fixation/preservation? Could it be a fungus that grew after the animal died?

Just wildly guessing...

 

[Tintenfisch]

Unless the sperm are implanted from inside the mantle toward the outside, the bulb-end is the last thing to leave the male squid. If they are implanted from inside toward outside, I guess the bulb could be a socket for some kind of egg-tooth-type structure used to punch through the female's mantle and anchor the spermatophore... but the 'inner' end isn't protruding into the female's mantle cavity, it's embedded in the tissue, parallel between inner and outer surfaces.

 

[cuttlegirl]

Ok, so the male squid implants the spermatophore from the outside of the female squid's mantle, through the mantle wall and into the mantle cavity, right? Maybe it is a plug, so that the spermatophore is anchored in the mantle and he doesn't overshoot his target...

 

[monty]

Ok, so the male squid implants the spermatophore from the outside of the female squid's mantle, through the mantle wall and into the mantle cavity, right? Maybe it is a plug, so that the spermatophore is anchored in the mantle and he doesn't overshoot his target...

Maybe I'm misunderstanding, but I thought the male cuts a groove, and then implants the spermatophores into the side wall of the groove, so it's embedded in the flesh of the mantle, and never gets through to the mantle cavity... although that begs the question of how the sperm gets inside the mantle to fertilize the eggs... and that question begs my next question, which alternately seems like either insight or idiocy: If the spermatophore is embedded in the flesh of the mantle, maybe the bulbs are an artifact of the way the sperm is released to fertilize the eggs, so the reson the self-implanted ones in the male don't have the bulbs because they've never released their sperm. Perhaps the spermatophores sit there embedded until the eggs are ready, and then some hormone tells them to move all the sperm out of the protection of the "root" embedded in the mantle out into the protruding part, which expands as a bulb, and then, when the eggs are near or the female pokes them with an arm or something, they release the sperm, which is conveyed somehow to the eggs to fertilize them, leaving the hollow bulb. I suppose a way to test this would be to see if the spermatophores in the male's flesh have a bunch of sperm in them, while the ones in the female are pretty much empty... all, of course, assuming you squid reproduction experts don't my crackpot theory because everybody who's anybody knows it can't work that way...

This is a lot of free association, but maybe it'll help. Unfortunately, I need to be doing (my) real work, so I can't think on this too much...

As a last work-avoidance-behavior, I read the section of Nixon & Young (p.179) that has a description that seems to match what you've said, and describes a "head and neck" on the spermatophores:

More than 1000 Onychoteuthis banksi (Chaunoteuthis mollis) captured off Japan, had a 'sour' flesh when tasted and all were gravid females (Okutani and Ida 1986). These squids had cuts, 100mm long, on the left ventral side of the mantle with implanted spermatophores, and the tentacles reduced to stumps 5% of the mantle length. Spermatophores, with only the head and neck projecting, were embedded in the longitudinal cuts in the mantle tissue.

the reference is:

Okutani, T. and Ida, H. (1986). Rare and interesting squid in Japan-IX. A mass occurrence of Chaunoteuthis mollis Appellof, 1891 (Oegopsida:Onychoteuthidae) from off Japan. Venus, Japanese Journal of Malacology, 45, 53-60.

If you haven't read that, maybe you should dig it up! (Of course, it may be in Japanese...) And there's supposed to be an umlaut over the o in Appellof, but I can't figure out how to insert one...

 

[Clem]

Hello Monty,

Yeah, I'm with you on this one. My notion was that the spermatophores might react chemically to the female's tissue and swell above the implantation site, either to release the sperm or to facilitate location and manipulation by the female: the bulbs would be a kind of sperm pull-tab, allowing the female to pluck them out and move them where they need to go. Your idea could explain why auto-injection (or a bad case of "wrong team") in the males doesn't yield the tell-tale bulb: wrong hormones in the implantation site.

Or something.

Cheers,
Clem

 

[Tintenfisch]

A ha, should have checked my list of refs more carefully - I knew I had that one, but this explains why I couldn't find it under 'Kubodera.'

Monty, I also wondered whether the spermatophores were rupturing on the outside rather than inside - maybe to release the sperm directly to the surface of an egg-mass, for example. This could be in response to some hormone/chemical associated with the eggs, or as you suggest, in response to some physical rupturing from the female.

The grooves photographed in the article look very similar to the ones I observed, although of course there is no photo or drawing enlarging the spermatophore 'heads and necks.' This is what Golfingia looks like (the worm Nesis (1970) said resembled the spermatophores). Mayyyybe...

In Moroteuthis, at least in the two species I have seen with implanted spermatophores, the sperm reservoirs actually do eventually break through into the interior of the mantle cavity and presumably fertilize the eggs before they are extruded. But that doesn't have to be the case in all onychoteuthid genera.

Ongoing thought required!

 

[Tintenfisch]

One additional thought: the 'bulbs' are

 

[Steve O'Shea]

And there's supposed to be an umlaut over the o in Appellof, but I can't figure out how to insert one...

Have mine .... ö

 

[monty]

Have mine .... ö

mmm. Tasty Germanic goodness. Thanks, Dr. Ö'Shea!

 

[OB]

Urrr, what about requesting the Smithsonian one (assumed?) spermatophore for (microscopic) section?

 

[cuttlegirl]

Tree of Life has a computer animation of a spermatophore, I have no idea if it is correct, but here it is...

http://tolweb.org/accessory/Spermatophore_Terminology?acc_id=1972

You probably have this reference, but just in case...it is from the Journal of Morphology

Takahama, H., Kinoshita, T., Sato, M. and F. Sasakim, 1991,
Fine structure of the spermatophores and their ejaculated forms, sperm reservoirs, of the Japanese common squid, Todarodes pacificus,
Journal of Morphology 207(3), 241-251.

*Correspondence to Fumie Sasaki, Department of Biology, School of Dental Medicine, Tsurumi University, 2-1-3 Tsurumi, Tsurumi-ku, Yokohama 230, Japan

Abstract
Spermatophores in a squid, Todarodes pacificus, were observed by light and electron microscopy and were further analyzed by X-ray microanalysis (XMA) of frozen thin sections. Each spermatophore consists of a sperm mass, a cement body, an ejaculatory apparatus, and some fluid materials, all of which are covered by an outer tunic. The outer tunic consists of about 20 membranous layers, each containing straight, parallel microgrooves. Each layer's microgroove pattern is roughly in an orthogonal arrangement with respect to the next layer's pattern. The sperm mass, which is the only cellular component, consists of a sperm rope which is coiled more than 500 times. Most of the spermatozoa in the rope are arranged regularly and are enveloped in materials which are well-stained by Alcian blue. The cement body is located between the sperm mass and ejaculatory apparatus and has a hard outer shell with an arrowhead-like structure, presumably for penetration into the tissue of the female. Calcium and phosphorus are present in the shell of the cement body, which also has an affinity for alizarin red. The ejaculatory apparatus consists of two tubes, designated as the inner tunic and the inner membrane.
After the spermatophoric reaction, a sperm reservoir is formed at the anterior end of the extruded and inverted ejaculatory apparatus. The sperm reservoir, which encases the sperm mass, is composed of the cement body at the anterior end and the inner tunic of the ejaculatory apparatus at the posterior end.

 

[main_board]

A bit late, but I'm inclined to agree with the previously stated theory that the sperm are release out into the water instead of into the mantle. That is what I was thinking as I read your inital post, Kat, only to find that others had come to the same conclusion.

And as far as the release factor goes, I prefer the chemical signal idea instead of direct manipulation. The chemical signals could come from the female, but I think it would be more likely to come from the eggs/egg mass. If the female signalled for the sperm to be released, the timing would have to be exceptional as she has to release the eggs and manipulate them towards the spermatophores before the sperm is released. Hormones released into the blood would take time to reach the spermatophores, and I don't think she wants to be caught mid-way through the procedure by a sperm whale. Instead, I think that she lays her eggs, mixes them with the jelly to make the egg mass and then places that near the spermatophores. The chemical signals are received due to proximity to the egg mas and it is showered with sperm. However, I'm not sure if sperm would be able to find the eggs to fertilize them through the jelly. Hmmmm...

Oh, do Onychoteuthids lay pelagic egg masses?

Definitely a good mental work-out. Thanks Kat!

Cheers!

 

[chrono_war01]

...I've been rereading the whole read and the only thing I could think of was "What?"

And as Main_board said: Definitely a good mental work-out."