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Architeuthis (Giant Squid) reproduction

Architeuthis (Giant Squid) reproduction, with notes on basic anatomy and behavior

By Dr. Steve O'Shea

Last updated: 03/28/03

Note: Steve welcomes discussion in the Physiology & Biology forum.


Architeuthis
Architeuthis

Architeuthis
Architeuthis (Fig. 1, left) is basically an eating and breeding machine. A look inside the cut-open mantle (Fig. 2 and Fig. 3, right) revels a large stomach, and both spiral and digestive (or stomach) caeca, in addition to a substantial investment in the reproductive tissues of ovary, oviducts and oviducal and nidamental glands. There's not a lot else in there.

Submature to mature male and female Architeuthis are most-often trawled in New Zealand waters off Banks Peninsula, East Coast South Island during the austral summer, and off Hokitika Canyon, West Coast South Island during the austral winter. As Architeuthis has not been trawled outside of these two time periods (over the last decade), and juveniles have never been trawled here, it is unlikely that it is a full-time resident of New Zealand waters; it probably spends most of its post-larval life outside of New Zealand waters. To the contrary, we have ontogenetic series of specimens of many other fast-swimming oceanic and deep-sea squid species found in New Zealand waters, indicating that they do reside in New Zealand waters throughout their entire life cycle (suggesting that the absence of juvenile Architeuthis from collections is no artefact of collection effort or net evasion).

The regularity of mated or otherwise fully to near-fully mature male and female Architeuthis off these two areas, Hokitika Canyon and Banks Peninsula, suggests that these are breeding grounds, and that the adult squid have migrated into them. Unless pheromones are involved (squid perfumes), both male and female (or male/male and female/female) probably just bump into each other in the dark. After a moment of panic, sixteen arms and four tentacles entangle and the giants go beak to beak.

The relatively long terminal organ (penis) of a mature male is almost the length of its mantle, from which it projects freely, through the funnel, for a considerable portion of the organ's length. Species with such long organs presumably use them directly to implant spermatophores hydraulically into the female, and as a rule lack modification of either ventral arm (hectocotylus) for spermatophore transfer. Architeuthis lacks a hectocotylus.

Architeuthis sperm injection
His metre+-long penis presumably injects numerous spermatophores directly into the female's arms (Fig. 4, left). The two animals then separate, the male swimming away, probably a bit beat up (possibly having lost parts of his arms and tentacles in the violent struggle; see cannibalism thread), but none the wiser likely repeats this affair with another female (should the opportunity arise). His spermatophores remain embedded in each female's arms - possibly burrowing even deeper into their flesh.

Copulation is likely to accelerate maturity of the female. Eggs soon funnel from her large, terminally positioned ovary into long, convoluted proximal oviducts (Fig. 5). From here they advance to the oviducal glands, structures that secrete to the egg chemicals that, amongst other things, initiate sperm activation and attraction. Passing from these glands the eggs would discharge from the distal oviduct, possibly in strings, directly into the female mantle cavity. The nidamental glands (Fig. 6) would then secrete vast amounts of jelly, probably almost entirely filling her mantle cavity. This jelly binds with discharging eggs, and like a cement mixer, her mantle probably rhythmically contracts and relaxes, thoroughly mixing them. Shortly afterwards this mass of jelly and egg would be extruded through her funnel, and a sphere-like egg mass of ~half-a-metre in diameter would be released. This mass would then be taken into her arms where she would cradle it as it absorbed seawater and increases in size (possibly to two-or-so metres diameter).

The problem has always been how to get the sperm (embedded in the arms) to the eggs (embedded in the jelly/egg mass). One solution is proposed here (but this is guess work). While she cradles this mass in her arms, chemicals released from the jelly activate the spermatophores embedded into her arms. These 10-cm long parasite-like spermatophores then would migrate through her flesh to the arm surface, their ends would rupture and sperm would be discharged directly to the face of the egg mass. Frenzied by the chemical cues given off by the eggs, the sperm migrate through the jelly to individual eggs and fertilisation ensues. The egg mass would then be released by the female and drift away in the current. (The alternative is to having fertilisation occurring within her mantle. This would, however, necessitate either the spermatophores or the sperm to actively migrate from the arms to the mantle cavity. To date no spermatophore has been observed in any of the mantle cavity, proximal or distal oviduct, or oviducal gland of any dissected female. Moreover, it is quite unlikely that individual sperm could travel this distance. Cradling the egg mass in the arms seems the most plausible way for sperm to be exposed to the egg.)

The similarity between Architeuthis and the arrow squid (Nototodarus) female reproductive systems, the size of her eggs (~ 2 mm in greatest diameter), and the size of their larvae, suggest parallels between the two, particularly egg-mass types. Both these genera have well-developed nidamental glands - structures that produce vast amounts of jelly, known to bind individual eggs into a large, spherical, water-borne egg mass. A hooked squid, Enoploteuthis galaxias, lacks these glands and is known to releases individual, relatively large and yolky eggs directly into the water column. The genera Sepia, Sepioteuthis and Sepioloidea, all of which attach their eggs to a substratum, have modified glandular structures associated with the nidamental glands (accessory nidamental glands). The dissimilarity between female Architeuthis anatomy and those of Enoploteuthis, Sepia, Sepioteuthis and Sepioloidea suggest Architeuthis eggs are neither freely, individually released, nor attached to the substratum.

There is very limited data on egg mass types, and of the egg masses themselves, for the greatest majority of squid species. Few egg masses have been found floating on the surface of the worlds oceans (Okiyama 1965, Clarke 1966, Okiyama & Kasahara 1975), and few have been spawned in the laboratory, although large spherical arrow squid (similar to Nototodarus) egg masses have (Bower & Sakurai 1996, O'Dor & Balch 1985). So, the suggestion that Architeuthis releases an egg mass similar to that reported here is not so outrageous. For oegopsid squids in general, if egg masses are distributed meso-pelagically, it would explain why they have been rarely seen or collected. The gel binding the egg mass together is likely to be too tenuous to be retained in trawls, with plankton nets not proving that much better (a pressure wave could simply push them aside) (O'Dor & Balch ibid.).

For those pelagic squid species for which it has been documented, the life cycle appears associated with some major current system (Coelho 1985, Hatanaka et al. 1985). It seems probable that spawning would be followed by passive down-current dispersal of the egg mass; larvae then would hatch, after which they would continue to be passively transported in the current away from the spawning grounds. At some critical point larvae would have attained sufficient size and mobility to actively move through the water column. At some unknown point in the life cycle the juveniles and/or subadults would then commence an active counter-current migration back to the spawning grounds (fide Hatanaka et al. 1985, Rodhouse 1991).

Accordingly, the Architeuthis egg mass probably drifts in the water column at shallow depth for less than 3 weeks before the embryos (similar to those in Fig. 7) hatch and paralarvae are released (Fig. 8). These paralarvae will then be transported in surface waters, where they feed upon prey to 1.5 times their size, until they reach a size where appropriate-sized prey is exhausted and they descend through the water column, never to return to the shallows, unless caught in a trawl or otherwise dead. Nearing maturity, in months prior to the austral summer and winter periods, they would commence a counter-current migration back into New Zealand waters to complete their life cycle.

We can report one hitherto unknown aspect of male reproductive behaviour. Unfortunately for male squid there does not appear to be too much discrimination of potential mates. Basically if it doesn't eat you first when you bump into it in the dark then you give it everything you have to 'offer'. A number of males that do not appear to have mated themselves have had numerous spermatophores embedded around their eyes (Fig. 9) and in their own arms. Other males would appear responsible for this act. Kjennerud (1958) reported an Architeuthis male stranded off Norway in the 1950's in a similar state, although Norman & Lu (1997) propose that that another male may inadvertently have shot this co-suitor while attempting to impregnate a female. Either this or he had accidentally 'shot himself in the foot'. Indeed it is likely that inadvertent male-to-male copulation occurs in Architeuthis (though probably not intentional homosexuality); it is also possible self-insemination occurs during capture-induced trauma.

REFERENCES
Bower, J.R.; Sakurai, Y. 1996. Laboratory observations on Todarodes pacificus (Cephalopoda: Ommastrephidae) egg masses. American Malacological Bulletin 13(1/2): 65-71.

Clarke, M.R. 1966: A review of the systematics and ecology of oceanic squids. Advances in Marine Biology, 4: 91-300.

Coelho, M.L. 1985: review of the influence of oceanographic factors on cephalopod distribution and life cycles. Northwest Atlantic Fisheries Organisation (NAFO) Scientific Council Studies, 9: 47-57.

Hatanaka, H.; Kawahara, S.; Uozumi, Y.; Kasahara, S. 1985: Comparison of life cycles of five ommastrephid squid fished by Japan. Todarodes pacificus, Illex illecebrosus, Illex argentinus, Nototodarus sloani sloani and Nototodarus gouldi. Northwest Atlantic Fisheries Organisation (NAFO) Scientific Council Studies, 9: 59-68.

Kjennerud, J. 1958: Description of a giant squid, Architeuthis, stranded on the West Coast of Norway. Universitetet I Bergen. Ã…rbok 1958, Naturvitenkapelig rekke 9: 1-14.

Norman, M.D.; Lu, C.C. 1997. Sex in giant squid. Nature 389, 683-684.

O'Dor, R.K.; Balch, N. 1985. Properties of Illex illecebrosus egg masses potentially influencing larval oceanographic distribution. Northwest Atlantic Fisheries Organisation Scientific Council Studies 9: 69-76.

Okiyama & Kasahara 1975: Identification of the so-called "common squid eggs" collected in the Japan Sea and adjacent waters. Bulletin of the Japanese Reg. Fisheries Research Laboratory, 26: 35-40.

Okiyama 1965: Some information on the eggs and larvae of the common squid, Todarodes pacificus Steenstrup. Bulletin of the Japanese Reg. Fisheries Research Laboratory, 15: 39-53.

Rodhouse, P. 1991: Population structure Martialia (Cephalopoda: Ommastrephidae) at the Antarctic Polar Front and the Patagonian Shelf, South Atlantic. Bulletin of Marine Science, 49(1—2): 404-418.
Published:
Dec 29, 2013
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