Cephalopod Sex and Reproduction

DWhatley

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#1
Mating in the ceph world tends to be an on-going human fascination. Choices, techniques and biologics vary widely from species to species. Observations have included severing and throwing a spermataphore loaded arm at the female (blanked octopus) , mating beak to beak (Larger Pacific Octopus), mate consumption, violent and fast copulation and gender disguise. This is an attempt to collect articles that document the different findings.
 
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#2
Octo-SAP - ATTRACTING STORED OCTOPUS SPERM

ATTRACTING STORED OCTOPUS SPERM
Journal of Experimental Biology, Nicola Stead

Reproduction for most marine invertebrates is a game of odds: females release their unfertilised eggs into vast oceans and rely on co-released peptides or protein pheromones to tempt sperm towards their eggs. A few species, however, such as the common octopus, have decided to adopt a more mammalian approach and use internal fertilization. It makes sense – surely, in the confined space of the oviduct, at least some sperm should reach the egg by chance without the need for additional attractants to induce chemotaxis (movement towards a signal). However, Anna Di Cosmo from the University of Napoli Federico II, Italy, thought otherwise. She explains that during mating, male octopuses will deposit sperm into the oviduct of the female, but females aren't always ready with an egg and so the sperm will bury themselves into the lining of the oviducal glands. When a mature egg is released, the waiting sperm needs a kick-start to get moving again and Di Cosmo suspected that a chemoattractant similar to those released by free-spawning animals might be involved (p. 2229).

Di Cosmo and her team caught several female octopuses off the coast of Naples and collected their mature eggs. The team then homogenized the eggs and, using a form of chromatography, separated the mixture into fractions of different proteins. Each fraction was then tested for its ability to coax sperm, collected from the oviducal glands, into moving through a fine mesh from one side to the other. One fraction in particular enticed sperm movement and the team identified the attractant as a small 11 kDa protein that they called octopus sperm-attractant peptide (Octo-SAP).

The team further characterized Octo-SAP's properties and showed that chemotaxis occurred in a concentration-dependent manner, with more sperm moving when Octo-SAP was concentrated. Using a microscope to film the tiny movements, the team also showed that the sperm moved up the concentration gradient towards areas of high Octo-SAP concentration. Together, the results suggest that the sperm were using the attractant to home in on what they thought was an egg. So, it seems that chemoattraction isn't just for free-spawning animals after all.
© 2013. Published by The Company of Biologists Ltd
Sperm-attractant peptide influences the spermatozoa swimming behavior in internal fertilization in Octopus vulgaris
 

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#3
SQUID
Idiosepius paradoxus

Female Pygmy Squid Cryptically Favour Small Males and Fast Copulation as Observed by Removal of SpermatangiaNoriyosi Sato,Takashi Kasugai,Noriyosi Sato,Hiroyuki Munehara 2013 - subscription required

Abstract
Females can express mate (or fertilisation) preferences after copulation. In the Japanese pygmy squid,Idiosepius paradoxus, in which males do not show any conspicuous pre-copulatory displays, the females remove the spermatangia attached to their bodies after copulation. In this study, we observed pre- and post-copulatory behaviours and analysed which variables associated with copulation were correlated with spermatangia removal. When females mated with larger males or copulation lasted longer female squid elongated their buccal mass after copulation and removed more spermatangia. We also investigated the effects of spermatangia removal on the retained spermatangia to predict whether cryptic female choice (CFC) influenced fertilisation success. Spermatangia removal by females had a stronger effect on the number of spermatangia retained than did the number of spermatangia ejaculated by males. These results suggest that spermatangia removal after copulation by buccal mass elongation works as a CFC in Japanese pygmy squid, and females cryptically favoured small males and fast copulation.
 
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Tintenfisch

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SQUID
Here's one of the weirder ones--good old Taningia danae.

Abstract
Spermatangium implantation is reported in the large oceanic squid Taningia danae, based on ten mated females from the stomachs of sperm whales. Implanted spermatangia were located in the mantle, head and neck (on both sides) or above the nuchal cartilage, under the neck collar and were often associated with incisions. These cuts ranged from 30 to 65 mm in length and were probably made by males, using the beak or arm hooks. This is the first time wounds facilitating spermatangium storage have been observed in the internal muscle layers (rather than
external, as observed in some other species of squid). The implications of these observations for the mating behavior of the rarely encountered squid T. danae are discussed.
 

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SQUID
Some comments here in the discussion for Onykia ingens.

Abstract
Sexual dimorphism in size and morphology of the lower beak of the warty onychoteuthid squid Moroteuthis ingens is analysed. Beaks of maturing males exhibit a band of weak, clear cartilage across the shoulder region, while mature males exhibit a pronounced excavation of this area; the hood remains intact. Female beaks attain greater size, but relatively shorter lower rostral lengths (LRL) than those of males; they display neither the shoulder cartilage nor later erosion, but the hood is consistently eroded in mature specimens. The angle ridge in females is considerably longer than in males. Due to the difference in LRL relative to overall beak size, M. ingens beaks from predator stomachs should be sexed prior to calculating prey size using LRL; for both sexes, the LRL-mantle length (ML) relationship is linear while the LRL-weight relationship is exponential. Sex-specific equations are provided for reconstructing ML and weight using LRL. Based on several incidences of male-female pairs collected with beaks interlocked, M. ingens is postulated to mate in a head-to-head position, with both individuals incurring beak damage during the event.
 

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tonmo

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#6
Thread promoted to homepage, facebooked and tweeted :thumbsup:
 

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SQUID
Doryteuthis opalescens - common market squid

True colors: Female squid have 2 ways to switch color, according to a UCSB study Sept 2013

This central white stripe on the female squid occurs on the dorsal surface of the mantel between the fins, in the same location as the conspicuously bright white testis in the male. “Our best supposition is that the female can masquerade as a male to discourage multiple matings,” said Daniel DeMartini, the doctoral student and co-author who discovered this feature. “The white stripe is turned on so it looks like the female has a testis. She may do this to protect the survival of her fertilized eggs, but that is just a suggestion.”

“The ideal number of matings might be more than one but less than many,” added Morse. “In other words, it might be best to have a few matings so that the female’s eggs are fertilized by a few fathers to increase genetic diversity, making the offspring better able to survive under a range of environmental conditions like the rising temperature in the ocean, for example. The female wouldn’t want to look like a male from the beginning because that would discourage all mating.”
 

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#9
@Tintenfisch, Can you try again on that link? It looks like you picked up the search criteria but not the URL (note the spaces and missing dot com/org/etc: http://hoving reproduction cephalopod) To edit the link highlight it and click the chain link with the x then click somewhere else then rehighlight and click the link. Don't try to unlink and link without unhighlighting as it confused the editor :roll:
 

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#10
Aquatopia: The Imaginary of the Ocean Deep, Tate St Ives — review
'Squiggle, squiggle, ooh, good...' Tate St Ives shows how sexy the octopus can be
Laura Gascoigne 23 November 2013


But the dominant species in this show, if you’re counting appearances, is the cephalopod. ‘A glutinous mass, endowed with a malignant will, what can be more horrible?’ is how Victor Hugo characterised this aquatic villain of countless sci-fi novels and horror films. But in the works in this exhibition, the cephalopod comes across more as a sexy beast than as a kraken. Its eroticisation dates back to Hokusai and his 1814 woodblock illustration ‘Pearl Diver and Two Octopi’, a three-on-the-sea-bed romp leaving little to the visual imagination — and spelling that little out in the accompanying text, which has been helpfully translated into English: ‘Inside, squiggle, squiggle, ooh, good… There, there! Theeeeere! … Whew! Aah! Good, good, aaaaaaaaah! Not yet…’ Meg Ryan’s performance in When Harry Met Sallyseems tame by comparison.

Hokusai spawned a genre of tentacle porn to which ‘Sex is Good’ (1999), a knitted octopus by Vidya Gastaldon & Jean-Michel Wicker, and ‘Hokusai’s Octopai’ (2004), a stuffed latex version by Spartacus Chetwynd, belong. Chetwynd’s octopus also dances to a heavy-metal soundtrack in an accompanying video, ‘Erotics and Beastiality’. Video soundtracks are the bane of exhibitions, but all the videos here come equipped with headphones apart from the Otolith Group’s ‘Hydra Decapitata’, which is overloud and, at 31 minutes, overlong. The best artists’ videos, in my experience, are short and funny. Two good examples in this show are Shimabuku’s ‘Then, I decided to give a tour of Tokyo to the octopus from Akashi’ (2000) — an amusing experiment in tentacle tourism — and Alex Bag and Ethan Kramer’s ‘Le Cruel et Curieux Vie du la Salmonellapod’ [sic] (2000), a spoof nature film about a ‘sadistic, masochistic, sexually enthusiastic’ amphibious mammal performed by puppets: The Magic Roundabout meets Jacques
Cousteau.
 

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#11
Characterization of deformed hatchlings of Octopus vulgaris obtained under captivity from a small female
Pablo Jiménez-Prada, Anastasia Scherbakova, Rodrigo Riera ,Beatriz C. Felipe, António V. Sykes, Rui A. Gonçalves, José P. Andrade, Catalina Perales-Raya, Covadonga Rodríguez,Eduardo Almansa 2013 (subscription)

Abstract
The common octopus (Octopus vulgaris), a promising species for aquaculture, spawns easily under captivity from mature females (usually above 1 kg wet weight). Octopus juveniles and adults are collected from nature to obtain eggs and paralarvae for aquaculture development trials. In July 2011, a very small female (150 g wet weight but with an age estimation of 300 days-old) spawned almost 77,000 paralarvae. Malformations of paralarvae were noticed in the first spawning days, namely the absence of arms. Despite not being lethal, these abnormalities might be derived from the physiological condition of the breeding specimen (the female's lower weight to the estimated amount of living days), which might be eventually related to nutritional unbalances or genetic parameters that were transferred to the eggs.
 

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Evolution of sperm transfer mechanisms in cephalopods: adaptative convergences associated with habitat shifts in the marine environment?

Principal Investigator:Antonio Carlos Marques, Awardee:Antonio Carlos Marques
Institution:Instituto de Biociências (IB). Universidade de São Paulo (USP). São Paulo, SP, Brazil
Abstract
Studies on evolutionary convergences can provide important insights for understanding the factors that influence evolution. To contribute to the understanding of the patterns and processes involved in metazoan evolution and diversification in the marine environment, this study aims to investigate evolutionary convergences potentially associated with marine habitat shifts, using the class Cephalopoda as a model group. To achieve the proposed goal, we will investigate cephalopod sperm transfer mechanisms, some of which have been proposed as potentially convergent and correlated with habitat. First, organs and structures responsible for sperm transfer will be subject of functional morphology studies, aiming at the understanding of the mechanisms involved in spermatophore transfer, implantation, and storage. These analyses will include histological and electron microscopy techniques, and in vitro experimentation. This study aims also to provide a reasonable bulk of morphological data related to cephalopod reproductive strategies to allow the identification of putative homologous structures. Ancestral states for these characters will be reconstructed to attempt to identify characters that have arisen via convergent evolution. These will then be assessed for correlation with habitat, also using a phylogenetic context. Based on these results, adaptive hypotheses will then be inferred, tested and discussed. (AU)
 

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#13
Reversal and transfer of spermatophores by Octopus vulgaris and O. hummelincki Jerome Wodinsky 2008 (subscription)

Copulatory behavior in the octopus consists of a patterned series of movements whose individual functions are not well understood. Observations and experiments on mating in Octopus vulgaris andO. hummelincki from Bimini, Bahamas and Haiti were made over a number of years in the laboratory. The study reveals how the male octopus reverses its spermatophore prior to transferring it to the female. The male’s terminal organ (penis) extrudes the sperm end of the spermatophore as it exits from Needham’s sac up to the cap or filament thread and then, holding onto the cap thread, inserts the ejaculatory end of the spermatophore into the groove of the hectocotylus, thus reversing it. It is hypothesized that the primary function of the cap or filament thread, one part of the spermatophore, is to be a handle by which the reversal and transfer is accomplished. The siphon is merely a conduit through which the terminal organ functions and plays no role whatsoever in either the reversal of the spermatophore or in its insertion into the groove. The stimulus to which the male orients to find the groove of the hectocotylus is the apex of the retracted interbrachial membrane between the third and fourth right arms, which bears a fixed spatial relationship to the origin of the groove. A number of deviations from the successful transfer process, which represent loss of sperm from the reproductive process, are illustrated. Despite these deviations, the delicately balanced integration of the various movements serves to transfer the spermatophore to the female to ensure reproductive success.



http://www.springerimages.com/Images/LifeSciences/1-10.1007_s00227-008-1010-3-2

Interesting note on the use of suckers to orient the siphon in the above referenced additional available images page. It does not appear that the enlarged suckers are used in this process.

Under these conditions, it appears that the suckers of the third and fourth arms guide the siphon and spermatophore towards the groove, their presence obscuring observation of the actual insertion by the penis (Fig. 3 ).
 

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#14
Octopus
O. bimaculoides


Aggressive male mating behavior depends on female maturity in Octopus bimaculoides
Sobhi Mohanty,Alfredo F. Ojanguren,Lee A. Fuiman 2014 (subscription)

Abstract
This laboratory study examined the combined effects of male and female behaviors on the outcome of mating encounters inOctopus bimaculoides. We found that male–male competition for mating opportunities depends on female maturity; the presence of immature females elicited significantly higher levels of aggression between competing males. We conclude that males are able to assess the reproductive status of females. The study also found that immature and mature females resisted male mating attempts to a similar extent but that males that showed more aggression toward male competitors were able to spend more time in contact with females. We suggest that the lack of prominent visual displays in these mating trials indicates the importance of chemical cues inOctopusmating systems, as has been demonstrated for other cephalopods. This study contributes to the growing research on cephalopod mating systems and in particular shows thatOctopusmating dynamics may be more behaviorally complex than initially assumed.
 

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Evaluation of relationship between Chilean octopus (Octopus mimus Gould, 1852) egg health condition and the egg bacterial community
Shunpei Iehata, Fernando Valenzuela, Carlos Riquelme 2014 (subscription)

Abstract
The objective of this study was to evaluate how bacterial community associated with Chilean octopus (Octopus mimus) egg was related to egg health condition using a culture dependent method and PCR-DGGE fingerprinting technique. Total heterotrophic bacterial number of fresh egg was much lower than infected egg. However, biodiversity of culturable bacterial community associated with the fresh egg exhibited a higher diversity than the infected egg. Result of a culture dependent method showed that Roseobacter clade was predominant in the fresh egg, while predominant species in the infected egg was γ-proteobacteria. DGGE fingerprinting technique showed that fresh egg associated unculturable bacterial community was constituted of Roseobacter clade and Bacteroidetes, whereas Bacteroidetes was predominant bacteria in the infected egg. These results suggest that there might be some sort of relationship between octopus eggs associated bacterial community and egg health condition. Moreover, Roseobacter clade and Bacteroidetes might be potential symbiotic bacteria associated with the octopus egg, and some γ-proteobacteria might be involved in octopus egg disease. In particular, Roseobacter clade may play an important role in octopus egg health and it raises the possibility that this clade can be utilized as potential probiotics for octopus aquaculture.
 

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Wild Wunderpus photogenicus and Octopus cyanea employ asphyxiating ‘constricting’ in interactions with other octopuses Christine L. Huffard, Mike Bartick (2014) subscription
Abstract
Aggressive constricting including asphyxiation was observed in wild octopuses (Octopus cyanea Gray, 1849, and Wunderpus photogenicus Hochberg, Norman & Finn, 200616. Hochberg, F.G., Norman, M.D. & Finn, J. (2006) Wunderpus photogenicus n. gen. and sp., a new Octopus from the shallow waters of the Indo-Malayan Archipelago (Cephalopoda: Octopodidae). Molluscan Research 26, 128–140.
[Web of Science ®]
View all references). The distal portion of a dorsolateral arm formed a loop around the mantle of another octopus, in at least one case preventing the flow of water into the mantle, over the gills and out of the funnel. Constricting also may have prevented the subordinate individual from releasing ink, a possible irritant and predator attractant. A female O. cyanea used constricting as a form of fatal aggression to asphyxiate a male as part of apparent sexual cannibalism. This female killed a male with which she was mating using the ‘distance’ position. Constriction allowed a W. photogenicus to win during physical interspecific aggression with a close relative, Thaumoctopus mimicus Norman & Hochberg, 200532. Norman, M.D. & Hochberg, F.G. (2005) The ‘Mimic Octopus’ (Thaumoctopus mimicus n. gen. et. sp.), a new octopus from the tropical Indo-West Pacific (Cephalopoda: Octopodidae). Molluscan Research 25, 57–70.

View all references. This action took place near an immediately available food source and interrupted foraging by T. mimicus, providing possible evidence of interference competition among closely related sympatric cephalopod species in the wild.
Journalist review of the article
Female Octopus Strangles Mate, Then Eats Him
By Katherine Harmon Courage | July 22, 2014 |
The views expressed are those of the author and are not necessarily those of Scientific American.
Octopuses do the darndest things. Like kill their mate during matingby strangling him with three arms, according to new observations from the wild.
Enterprising scientists Christine Huffard and Mike Bartick watched wild octopuses in action. They found that, for males, mating can be a dangerous game. Especially when your lady has long limbs. Some of the more dicey encounters are detailed in a new paper, published online July 11 in Molluscan Research.
Hold on a second, you say. Strangling octopuses? Octopuses don’t even have necks—or inhale air. So how, exactly, does that work? The strangulation seems to happen when “an octopus wraps at least one arm around the base of the mantle of the competitor” (or mate), Huffard wrote in 2010. This constriction then keeps the octopus from taking in fresh water to run past its gills—starving the animal of its oxygen source.
Octopuses are not known to get cuddly with one another on a day-to-day basis. In fact, “octopuses touch each other with their arms primarily in the context of mating and aggression,” the researchers write. And in this case it seems to have been both.
Huffard came across a pair of mating day octopuses (Octopus cyanea) near Fiabacet Island in Indonesia. The female, as is often the case in this species, was larger—with a body about seven-and-a-half inches long; the male was closer to six inches long. They were positioned on a reef, outside the female’s den, the male’s mating arm (hectocotylus) inserted into the female’s mantle from a (presumably) safe distance.
After about 15 minutes of mating, the female inched closer to the male. And, as if lunging for a quick embrace, the female encircled the male’s mantle with her two front arms, “dragging him nearer,” the researchers describe. The female’s two arms wrapped around the male’s funnel and mantle opening. The male turned white (a common escape attempt response) and seemed to fight to slink away. But the female continued her constriction for two full minutes before wrapping an additional arm around the male. Two minutes after that, the male stopped moving.
“The female enveloped his body with her web and carried him to what appeared to be her den,” Huffard and Bartick write. Apparently the male was both date and dinner.
In a mess of 16 arms not all moves are obvious. But, like other acts of aggression, “such as grappling, arm-pulling and pushing,” the researchers note, the asphyxiation move is quite easy to spot—and is “easily distinguishable from non-aggressive arm uses employed during mating,” which include the male inserting his hectocotylus into the female’s mantle or the male’s grabbing the female’s mantle to draw her closer.
Males of this species tend to have fairly long hectocotylus arms. But, apparently, not always long enough. “A smaller male of average hectocotylus length mating by the ‘distance’ position can still be asphyxiated and killed by a larger female,” the researchers note. “When making a slight lunge forward, this large female was well within arm reach to capture and constrict a male mating”—even when he is doing so from a reasonable distance. “This observation shows that the ‘distance’ mating position can entail significant risk for a male”—especially a slightly smaller one. And it’s possible that “females might not be able to constrict males that mate with a relatively long hectocotylus,” which would give the male a head start and greater reaction time should the female start to attack.
Interestingly, in this species and others that are prone to sexual cannibalism by females, the males have especially long hectocotylus arms.
Although this male did not escape a grim fate, his genes may still live on. “Because this case of possible sexual cannibalism was post-copulatory this male might have ultimately fertilized some of the cannibalizing female’s eggs,” Huffard and Bartick write. Had he lived, however, he could have tried his luck with other females. Perhaps with a slightly less leggy lady.
The video is of two males fighting over the rights to a female but the suffocation method discussed is clearly visible.
 
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DWhatley

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#17
Squid Lady Parts
Danna Staaf (@Danna) 2014

I first saw squid pimples in 2006, on a research cruise in the Sea of Cortez. The little bumps around the female’s mouth looked exactly like whiteheads, as if squid could get clogged pores. They even oozed white stuff when you squeezed, but it wasn’t pus.

It was sperm.

I was just beginning as a graduate student, learning to extract eggs and sperm from Humboldt squid in order to study fertilization and development—or, as I glibly described my thesis, “squid sex and babies.” Though technically I wasn’t studying sex, since in squid copulation is separate from fertilization. Females mate and store sperm for weeks or even months before laying eggs.

We don't know how the female market squid who laid these egg cases selected which sperm was used to fertilize them. Males help out by pre-packaging their sperm into complex needle-like structures called spermatophores. Each spermatophore can ejaculate (yes, independently!) to become a spermatangium, a sticky sperm mass that attaches to the female’s skin. Then sperm from this mass moves into the little pimples I saw, which are called spermathecae. Confused yet? I sure was!

In the ship’s laboratory, we were able to fertilize eggs with sperm from spermatophores, spermatangia, and spermathecae[1]. But I’m pretty sure squid don’t lay their eggs in Petri dishes, so this doesn’t tell us a whole lot about natural reproduction. Which of the three sperm sources do females use to fertilize their eggs? Why bother with all the processing steps? Does it have to do with female selection or sperm competition?

No one knows, which is a bit surprising because spermatophores themselves have been studied quite intensively. Videos of spermatophore ejaculation and attachment can be found online, and I’ve written about more than one exciting new study. But this is the first time I’m writing about spermathecae, and it’s not because of recent research—it’s to popularize the lack of it.

Squid aren’t the only animals with well-studied male bits and mysterious female bits. A metastudy[2] published in May found similar disparities across phyla, from insects to mammals. The authors analyzed various possible explanations and concluded that cultural bias was to blame. A lingering assumption that sex comprises male activity and female passivity, they argued, has led researchers to prioritize male over female genitalia.

I learned about this study from Ed Yong’s excellent coverage, which included an interview with duck penis researcher Diane Kelly. She highlighted a significant practical reason for the research imbalance: male parts tend to be external and relatively static, while female parts are internal and highly dynamic. It’s a lot easier to pop a penis under the microscope than to visualize how a vagina changes shape during copulation.

But we scientists love challenges, right? So, to atone for my enthusiastic popularizing of research on male squid anatomy, here’s a call to action for research on female squid anatomy.

Why do Squids Have Penises but not Vaginas?

Squid reproductive anatomy starts out sounding familiar. They have separate sexes—none of this weird hermaphroditic stuff that’s so common in their snail cousins. A female squid makes eggs in an ovary, and when they’re ready for fertilization they travel down an oviduct. A male squid makes sperm in a testis, and when they’re ready to fertilize, they come out of a penis.

But scientists prefer to call the penis a “terminal organ” because it’s a bit different from what we’re used to: it doesn’t touch the female. It’s just an internal spermatophore extrusion device. The male reaches into his own body to grab the spermatophores with one of his eight arms, called a hectocotylus, which is specially modified for delivery service.

Now things start to get complicated.

Sometimes, in some species, the male places the spermatophores somewhere on the female’s body—on her head, or on the eight arms attached to her head, or around the mouth at the center of her arms. In other cases, the male places spermatophores inside the female’s body. But unlike the small orifices of our human bodies, all squid bodies have a large opening around the head. Seawater flows in to bathe the internal organs, and the male can reach in to drop off spermatophores. It’s nothing like a vagina, which leads exclusively to reproductive organs.

Whether inside or out, the spermatophores ejaculate and spermatangia glue themselves to the skin. They may even start to burrow in, and in some species they can get quite deep—scientists have wondered if the male actually bites a hole before depositing spermatophores[3].

Sperm can remain in the spermatangia until it’s time to fertilize. But females of many species also have special pockets for storing sperm, generally referred to as seminal receptacles. These can be external, in the skin next to the mouth, and there can be one or many (as in Humboldt squid). Other species have internal receptacles at or near the opening of the oviducts, such as the pharetra of bobtail squids[4]. These are probably the closest thing there is to a squid vagina.

This octopus is here to remind you that squid aren't the only cephalopods with mysterious lady parts. No one knows how sperm migrate from a spermantangium to a spermatheca. In reef squid, it’s been suggested that females move sperm with their arms[4]. Female pygmy squid have been seen grabbing spermatangia with their mouths, but only to remove or eat them, not to transfer them[5]. Some evidence suggests that the sperm could transfer themselves by swimming[6].

Wherever they’re stored, sperm must be released when the eggs are ready. If the sperm is inside the body, fertilization also happens inside; if not, the female extrudes the eggs and holds them in her arms—right next to her mouth. (See, that’s why sperm are so often placed there. I bet you thought squid were just orally fixated.)

As far as we know, all squid females mate with and store sperm from multiple males. Given the complexity of sperm processing and storage, there’s ample opportunity for the sperm to compete with each other and for the female to choose among them. But virtually nothing is known about either process.

Squids Are Weird, and Then Some Are Weirder

Every general statement I’ve made so far probably has an exception or five. For example, males of some squid species have not one, but two hectocotylized arms. Then, many deep-sea squids don’t have a hectocotylus at all. They tend to have a long penis, though, and in at least one species the penis can expand to the entire length of the body[7]. If, as Yong wrote, the story of duck penises is really the story of duck vaginas, then what is the real story behind these variations in male squid anatomy?

In the classic book Cephalopod Behavior, first published in 1996, Hanlon and Messenger reported: We know little about the influence of female choice during courtship ... We lack detailed observations and experimental studies of alternative mating tactics, sperm competition and reproductive success.... The morphology of the ... seminal receptacle in cuttlefishes and squids should be studied in greater detail and the details of spermatophore transfer recorded.

Almost twenty years later, these questions remain open. The female squid’s roles in copulation and fertilization remain opaque. It’s time to give squid ladies some respect! In the form of, er ... highly intrusive scientific research.

Danna Staaf is a freelance science and fiction writer with a doctorate in squid biology from Hopkins Marine Station of Stanford University. She tweets as @DannaStaaf and blogs at The Cephalopodiatrist.
 

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The octopus that strangled its lover to death BBC © 2014

BBC Article from an interview with @mucktopus

In a single, extraordinary act, a female octopus surprises her mate, and changes how we think of her kind

Octopuses make for unusual lovers. To mate successfully, a male octopus must approach a female, and gently probe her with a single arm. He may grab her, but carefully, before inserting his arm up into her body, injecting packets of sperm.
After sex, a male octopus is probably not expecting to be probed by a female. He is not expecting to feel the brush of her arm, as it maliciously coils around his body. He is not expecting her to squeeze, cutting off the supply of water to his gills. He is not expecting to be held in a deadly, suffocating embrace.
Yet that exact fate befell one male common reef octopus swimming in the seas of Fiabacet Island, Indonesia.
In an extraordinary act, witnessed by scientists, the male octopus was strangled to death by his female lover, just moments after having mated with her.
The behaviour is so rarely seen that the incident, and a couple of others like it, may change our understanding of octopus behaviour.

Hunting a new mate? Or a new victim? (credit: David Fleetham / NPL)
Octopuses have long been considered relatively gentle creatures. Though they use their eight arms to catch prey, which is devoured using a large, sharp beak in their mouths, they tend to avoid aggression.
Octopuses are more likely to retreat from a threat, such as a predator, than to fight, and they tend to shy away from most confrontations with other animals, says Christine Huffard, a marine biologist at the Monterey Bay Aquarium Research Institute, at, Moss Landing, California, US.
In fact, octopuses spend most of their time, and use a variety of strategies, trying not to be seen. “Being overly aggressive to other animals on the sea floor would defy that strategy by attracting attention,” she says.
The more we get into the water and watch animals quietly from a distance, the more likely we might be to understand one day why female cephalopods might kill their mate
They can become aggressive with each other, particularly when fighting over food, dens, and mates. But they tend to grapple, pushing at each other, and pulling at their respective arms. They weren’t thought to be constrictors, strangling each other as a snake might suffocate its prey.
However, Christine Huffard and colleagues have witnessed two separate incidents of octopuses doing just that in the wild.

Suckers or weapons? (credit: Jeff Rotman / NPL)
The first occurred during a dive within 10 metres of water off Fiabacet Island, when the researchers came upon a female common reef octopus sitting exposed on a coral reef outside her den. Nearby, sat a slightly smaller male.
For 15 minutes the two animals mated. Then the female unexpectedly lunged forward, and with two arms, grabbed the male around his mantle, a structure octopuses use as a respiratory chamber to pass water through a funnel and across their gills. She dragged the male towards her. After two minutes, she then wrapped an arm around the opening to the mantle, and squeezed tight. After another two minutes, the male stopped moving. The female then enveloped the male’s body with her own and dragged him into her den, where the scientists presume she ate him.
Details of the grisly encounter are published in the journal Molluscan Research, along with those of a second encounter, this time between two octopuses of different species.

A male common reef octopus probes a female (credit: Georgette Douwma / NPL)
Then, divers observed a wonderpus octopus repeatedly approach and chase a mimic octopus foraging for food. The encounter seemed to end peacefully, but when reviewing images taken of the event, the scientists realised that the wonderpus octopus had actually wrapped an arm around the mantle of its rival, trying to strangle it.
Both incidents are reminiscent of another witnessed in 2007, when scientists observed one merciless female spend two days cannibalising a small male, having previously attacked and suffocated him after having mated with him 13 times.
For now, scientists do not know how common constricting might be in these or other octopuses in the wild. But such deadly struggles do appear to make octopuses unique; as the first invertebrates known to aggressively grasp and kill another animal using constricting.
Constricting might also prevent the subordinate octopus repelling the attack by expelling ink, which is also released through the funnel in the mantle. Expelling ink is a defensive tactic usually used to repel predators, as it clouds the water, and potentially contains irritating chemicals.

The deadly grasp of the female captured on camera (credit: C. Huffard)
For zoologist Mark Elgar of the University of Melbourne, Australia, an expert on invertebrate mating behaviour, the actions of the female octopuses make sense, given their eight-pronged anatomy.
“The specific method by which the female octopus captures and kills her mate – constricting him with her many legs – is novel, but only because this can be done only by an octopus,” says Elgar.
Huffard agrees. Octopuses are a type of mollusc known as a cephalopod, a group that also includes squid. “This unique anatomy opens doors to many behaviours that are unavailable to other molluscs, constricting being just one of them.”
Other invertebrates, such as insects and nudibranchs, are known to engage in sexual cannibalism.
None however, strangle their lovers.

A male wonderpus octopus is photographed strangling a rival (credit: Mike Bartick)
Female black widows and praying mantis are notorious for killing and eating males before, during or after sex. And similarly gruesome attacks have been observed in chironomid flies. A female chironomid uses her mouthparts to pierce the head of her male mate and, after extracting his body fluids as he transfers sperm to her, carries his desiccated carcass against her body for days.
Males are thought to be eaten as, once they have mated, they can be a valuable source of food. Male Argiope spiders, for example, tend to be consumed by the female after their second insemination.
For Huffard, this is a subject ripe for research: “People have studied that topic extensively in arthropods, especially arachnids, but not in rigorous studies using cephalopods.”
“The more we get into the water and watch animals quietly from a distance, the more likely we might be to understand one day why female cephalopods might kill their mate,” she says.
 

DWhatley

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Sperm transfer or spermatangia removal: postcopulatory behaviour of picking up spermatangium by female Japanese pygmy squid
Noriyosi Sato, Takashi Kasugai, Hiroyuki Munehara 2014 (subscription)

Abstract
In the Japanese pygmy squid Idiosepius paradoxus, females often pick up the spermatangium using their mouth (buccal mass) after copulation. To examine whether the female I. paradoxus directly transfers sperm into the seminal receptacle via this picking behaviour, or removes the spermatangium, we conducted detailed observations of picking behaviour in both virgin and copulated females and compared the sperm storage conditions in the seminal receptacle between females with and without spermatangia picking after copulation in virgin females. In all observations, elongation of the buccal mass occurred within 5 min after copulation. However, sperm volume in the seminal receptacle was not related to spermatangia picking. Observations using slow-motion video revealed that females removed the spermatangia by blowing or eating after picking. These results suggest that picking behaviour is used for sperm removal but not for sperm transfer. Moreover, the frequency of buccal mass elongation was higher in copulated females than in virgin females, consistent with the sequential mate choice theory whereby virgin females secure sperm for fertilisation, while previously copulated females are more selective about their mate. Female I. paradoxus may choose its mate cryptically through postcopulatory picking behaviour.
 

DWhatley

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#20
Dimorphic sperm-transfer strategies and alternative mating tactics in loliginid squid
Yoko Iwata1, Yasunori Sakurai2, Paul Shaw3 2014 (subscription)

Abstract
Animal species usually have a single sperm-storage site in the female body, but females of the squid Heterololigo bleekeri possess two distinct sperm-storage sites simultaneously. Use of two sperm-storage sites correlates with alternative male mating behaviours: large consorts guard females and place spermatophores inside the oviduct just before spawning, whereas small ‘sneaker’ males place spermatophores on the membrane around the female's mouth within the arm crown, where a seminal receptacle is present. Previous work showed that spermatophore and sperm morphology diverge between consort and sneaker males. Here we show novel dichotomous adaptations in the sperm-transfer strategy of males of this squid, associated with the use of two distinct sperm-storage sites on females. The spermatangia ejaculated from spermatophores were clearly dimorphic: all spermatangia ejaculated from spermatophores smaller than 12 mm from small sneaker males were drop-shaped, whereas all spermatangia from spermatophores longer than 12 mm from larger consort males were rope-shaped. In addition, the drop-shaped spermatangia were distinct in having a spine on their base, which might reduce the risk of it being shed from the female's body surface. Our findings suggest that existence of alternative sperm-storage sites, and related biological and environmental factors, lead to the evolution of divergent sperm-transfer strategies.
 

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