Cephalopod Sex and Reproduction

DWhatley

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Role of olfaction in Octopus vulgaris reproduction
Gianluca Polese , Carla Bertapelle , Anna Di Cosmo 2014 (subscription)

Abstract
The olfactory system in any animal is the primary sensory system that responds to chemical stimuli emanating from a distant source. In aquatic animals “Odours” are molecules in solution that guide them to locate food, partners, nesting sites, and dangers to avoid. Fish, crustaceans and aquatic molluscs possess sensory systems that have anatomical similarities to the olfactory systems of land-based animals. Molluscs are a large group of aquatic and terrestrial animals that rely heavily on chemical communication with a generally dispersed sense of touch and chemical sensitivity. Cephalopods, the smallest class among extant marine molluscs, are predators with high visual capability and well developed vestibular, auditory, and tactile systems. Nevertheless they possess a well developed olfactory organ, but to date almost nothing is known about the mechanisms, functions and modulation of this chemosensory structure in octopods. Cephalopods brains are the largest of all invertebrate brains and across molluscs show the highest degree of centralization. The reproductive behaviour of Octopus vulgaris is under the control of a complex set of signal molecules such as neuropeptides, neurotransmitters and sex steroids that guide the behaviour from the level of individuals in evaluating mates, to stimulating or deterring copulation, to sperm-egg chemical signalling that promotes fertilization. These signals are intercepted by the olfactory organs and integrated in the olfactory lobes in the central nervous system. In this context we propose a model in which the olfactory organ and the olfactory lobe of Octopus vulgaris could represent the on-off switch between food intake and reproduction.
Related findings of olfactory system effecting sexual maturation:

Control of GnRH expression in the olfactory lobe of Octopus vulgaris (pdf)

The presence of APGWamide in Octopus vulgaris: a possible role in the reproductive behavior
 
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DWhatley

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SQUID
Threat of Being Eaten Doesn’t Deter Dumpling Squid From Sex

... To see how the squid behave in the face of danger, researchers from the University of Melbourne collected 15 pairs of wild dumpling squid from the waters off Victoria, Australia. They also scooped up 15 of one the squid’s most common natural predators, a type of fish called the sand flathead. They put each squid pair into separate containers, then exposed them to various kinky scenarios, including introducing a predator before the squid began to mate, during mating and an hour after mating. The researchers noted any defensive behaviors, such as blowing out a cloud of ink to mask their presence or jetting away by quickly ejecting water out of the body. ...
 

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How Male Octopuses Avoid Being Eaten by Hungry females

Nice layperson's article discussing numerous mating habits of octopuses. Do note that the two siphon statement (as well as using the siphon at all in mating) needs correction but it covers the subject rather well.


Presented by
Katherine Harmon Courage

Male octopuses have a big problem: female octopuses. Each male wants to mate and pass on his genes to a new generation. The trouble is, the female is often larger and hungrier than he is, so there is a constant risk that, instead of mating, the female will strangle him and eat him.

The males have a host of tricks to survive the mating process. Some of them can quite literally mate at arm's length. Others sneak into a female's den disguised as another gal, or sacrifice their entire mating arm to the female and then make a hasty retreat.

It's all very macabre. It's also a paradox. Octopuses are some of the most antisocial, unfriendly animals alive. Yet their bodies have evolved in such a way that they must mate in the most intimate way possible: the male has to insert his sperm directly into the female's body using one of his arms. The resulting mating practices are not just a curiosity: they are a window onto how octopuses have evolved into the creatures they are today.

Wunderpus octopuses (Wunderpus photogenicus) mating (Credit: Roy Caldwell)

Octopuses and their close cousins the squid all belong to a group of animals called cephalopods. Both are actually molluscs, making them close relatives of oysters and limpets, but they have lost their shells.

Octopuses tend to be profoundly antagonistic towards each other. Unlike gregarious animals like dolphins, they appear to see their own kind primarily as competition, and sometimes food.

There's always the threat of cannibalism
Squid, which are downright social by comparison, mate in a distinctly unromantic way. A male squid swims by and deposits sperm in one quick move outside of the female's body. She can decide later whether to accept it.

But not so the octopus. "Octopus mating is definitely different than other cephalopods," says marine biologist Jean Boal of Millersville University in Pennsylvania. The male must deposit his sperm inside the female's body, at the risk of his life.

"There's always the threat of cannibalism," says Richard Ross of the California Academy of Science's Steinhart Aquarium.






Two day octopuses (Octopus cyanea) mating (Credit: Georgette Douwma / NPL)

We don't know how often female octopuses eat the males, but Christine Huffard of the Monterey Bay Aquarium Research Institute in California has seen it happen many times.

She strangled him and took him back to her den to feed on
In one instance, she and her colleagues observed two day octopuses mating on a reef in Indonesia. After about 15 minutes of copulation, the female lunged and wrapped two arms around the male's bulbous body, his mantle. A few minutes later, the male was motionless. The female then carried the corpse to her den, where he presumably became dinner.

In another instance, researchers watched a large female day octopus off the coast of Micronesia. A small male mated with her a dozen times. But then the male went in for a 13th mating session, and the female turned on him. She strangled him and took him back to her den to feed on over the course of the next two days.

Sexual cannibalism does happen in nature - witness the male-eating praying mantis and black widow spiders - but strangulation during mating is a rarity, Ross says. It may not be all bad for the male, though.

As Huffard and her colleagues point out in a 2014 paper describing one of the male-eating incidents, the felled male probably managed to fertilize some of the female's eggs - accomplishing his life's mission despite his unfortunate demise. What's more, females generally make hundreds or even hundreds of thousands of eggs, so just one successful copulation can produce a vast number of offspring.

The male's main tool for this daunting endeavour is a specialized mating arm, known as the hectocotylus. When he is not engaged with a female, the mating arm works just like his other seven arms. It is able to bend, stretch and exert suction. But the mating arm also comes with extra bells and whistles.

For big species, mating can last at least half an hour
For one, it has a central groove. The male releases packets of sperm called spermatophores into this groove, for their journey to the female. The arm's tip is also equipped with erectile tissue, not unlike that found in the human penis, which provides stiffness that helps guide the arm into the female's body. The arm goes in through one of the two siphons on the female's mantle, which she also uses to breathe, expel waste and jet out water for swimming.

The destination for these spermatophores is the female's small oviducal gland, a sort of holding area. When she lays her eggs, which could be days or even months later, they will pass this area and be fertilised.

The male needs to keep his mating arm tip inside the female long enough to transfer at least one spermatophore, and preferably more. In some smaller species this might take just a couple minutes, says Jennifer Mather of the University of Lethbridge in Alberta, Canada. But for big species like the giant Pacific octopus, mating can last at least half an hour.

But being soft-bodied, they can't indulge for too long. "If you get all wrapped up in mating, you're very, very vulnerable to predators," says Mather.






Giant Pacific octopus (Enteroctopus dofleini) on the sea bed (Credit: Jeff Rotman / NPL)

As a general rule, it's the male octopuses that approach the females.Then the males tend to take one of two approaches in attempting insemination.

The first is a risky position called the "mount". "The male grabs onto the female's mantle with all his arms, and reaches into her mantle with his mating arm," says Huffard.

This style of mating tends to be more popular in species with shorter arms, says Huffard. Females of these species may be less likely to eat their mates. Possibly, species in which males are more likely to be devoured during sex have evolved longer arms, which would make mating a little safer for the males.

Algae octopuses (Abdopus aculeatus) mating (Credit: Roy Caldwell)

More cautious males opt for the "reach". "The male sits near the female and reaches over to her only with the mating arm," says Huffard.

This allows him to keep his distance. "The male will extend his arm as long as he can and try to accomplish the copulation from as far away as he can," says Boal.

The "reach" tactic is more common in octopuses with longer arms, which may be the ones where female cannibalism is more likely. An extra-long reach means that the male can stretch his arm into a resting female's den and mate with her without even venturing inside.






Male algae octopuses (Abdopus aculeatus) mate from a distance (Credit: Roy Caldwell)

The algae octopus is one such cautious mater. "Males have a very long mating arm," says Huffard. "They stretch this arm to twice its resting length when mating." Just to be on the safe side, "these males also frequently mate with females that are busy foraging for food". These females ought to be too busy to eat him.

The "reach" approach also keeps the male's other seven arms free, so he can defend himself if need be, says Ross. This may be why the coconut octopus practices distant sex.

The "reach" tactic might also be advantageous for the female. In theory, she could entertain two male suits at once, says Huffard: one in each siphon.

For male argonauts, mating costs an arm (Credit: David Shale / NPL)

In some species, male octopuses have moved beyond the "reach". They just give the female their spermatophore-loaded mating arm, and swim away to safety.

A detached mating arm might be a logistical necessity
Male argonaut octopuses are smaller than the females, and the male's hectocotylus simply stays intact inside the female's mantle "until the female is ready to use the sperm for fertilization", Mather says.

It was actually this behaviour that earned the hectocotylus its name. In the early 19th century the zoologist Georges Cuvier discovered strange foreign objects in female argonaut octopuses and thought they must be a type of parasitic worm. He called them Hectocotylus octopodis, and the name stuck.

For blanket octopuses, a detached mating arm might also be a logistical necessity. The females can be 2m long, while the males are just a few centimetres. So the male "removes the arm that carries the sperm, and the arm goes into the [female's] mantle cavity," says Ross. "That's a pretty extreme strategy to not get eaten."






Greater blue-ringed octopuses (Hapalochlaena lunulata) mating (Credit: Roy Caldwell)

But it's not all rough-and-tumble, strangulation and arm removal. Algae octopuses are slightly more tolerant of each other than most species, and as a result their mating behaviours are more nuanced.

They have even been known to disguise themselves as females
Males of this species have other males as well as females to fear when attempting to mate. The largest males often have the privilege of guarding a desirable female and mating with her repeatedly. Smaller males have no chance of driving them off, and they know it. "Males appear to alter their mating tactics, based on their local chances of winning fights with rivals," says Huffard.

The smaller males wait until a larger guarding male has left the den, then covertly mate with the female. As a result, they are called "sneaker" males. They have even been known to disguise themselves as females, hiding their hectocotylus to make a less threatening approach to a guarded female.

This sly tactic can occasionally backfire, as it did in an instance caught on film by Huffard. A sneaker male approached a burrow where he seemingly sensed a female was hiding. As he reached an arm in, an octopus emerged. But it was not the female: it was her guarding male. Unsurprisingly, this big male was not impressed by the sneaker male's attempt to insert a hectocotylus into his mantle. The small male only narrowly escaped the ensuing fight.

A giant Pacific octopus (Enteroctopus dofleini) (Credit: Brandon Cole / NPL)

These cunning tactics pale in comparison to the behaviour of one newly-discovered octopus species. The larger Pacific striped octopus has not yet been formally described. But its sexual habits break all the rules for octopuses.

They mate beak-to-beak
The larger Pacific striped octopus is one of the few known gregarious octopuses. These octopuses can live together, even in close quarters, without eating or otherwise maiming each other.

This tolerance carries through to their mating habits. "They mate beak-to-beak, mouthpart-to-mouthpart," says Ross, who has witnessed numerous mating sessions. This is bizarre, because octopuses' sharp and strong beaks are their most dangerous weapons.

In this unusual position, a pair of octopuses will spread their arms out together, so that the suckers seem to touch. "That's a really, really strange thing," says Ross.

A female lesser Pacific striped octopus (Octopus chierchiae) (Credit: Roy Caldwell)

The larger Pacific striped octopus has a close cousin, the imaginatively-named lesser Pacific striped octopus. These are much more typical. "The male jumps on top of [the female's] mantle, away from her arms," says Ross. "It's an amazingly quick movement, in case she's in a bad mood or something. Then they mate, and he moves away as fast as he can."

When octopuses mate there are 16 arms to keep track of
No one knows why the larger Pacific striped octopus is so much more sociable than other species. Its apparent oddity reminds us that we don't really understand octopus sex in general. Why would such a voracious, antisocial animal mate so intimately?

Perhaps, despite the scale of the sexual cannibalism, few enough males meet their doom at their mates' hands, er, arms - and enough of them manage to pass on sperm. If that's the case, there might not be much evolutionary pressure on the males to evolve a safer way to mate.

"No one's really worked all of this out," says Mather. That may be in part because only a handful of species have been studied so far. "We have a vague understanding of mating in about a dozen shallow-water octopuses," Huffard says. "That leaves over 275 shallow-water species to go, and all of the deep-water species." Those deep-water octopuses might hold evolutionary clues to what early octopus sex looked like.

It may be some time before we truly understand why octopuses have sex the way they do. Part of the problem is that they are extraordinarily difficult to study. There are the obvious problems that they live underwater and are masters of camouflage. But even more challenging, when octopuses do get together there are 16 arms to keep track of. "It's really difficult to see what's going on," says Ross.
 

mucktopus

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Yeah I don't know where the two siphon (funnel) idea comes from. My guess is that people think that octopuses have two funnels because some octopus toys have two funnels. I think people model the toys based on photos, and many photos show the movable funnel, no matter which side the images is from
 

DWhatley

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Actually, she SHOULD know better as she (Harmon) has a journalist book out about cephs. I also don't know where the idea comes from that the siphon has anything to do with reproduction.
 

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Octopus
Distance chemoreception and the detection of conspecifics in Octopus bimaculoides

Matthew D. Walderon, Kevin J. Nolt, Robert E. Haas, Krista N. Prosser, Johanna B. Holm, Gregg T. Nagle, Jean G. Boal 2011 (full article)


Octopuses are solitary predators that typically use their arms to grope into crevices to find food. They detect odours on contact using chemosensory cells on their lips and suckers (Budelmann, 1996). They can also detect water-borne odours (distance chemoreception) using receptors in their olfactory organs (olfactory pits; Budelmann, Schipp & Boletzky, 1997). Behavioural experiments have demonstrated increased arousal (Boyle, 1983), activity (Boyle, 1986) and attraction (Chase & Wells, 1986;Lee, 1992) in response to food-related odours, but responses to odours of conspecifics have not previously been investigated. Chemical communication has been demonstrated previously in cephalopods, such as Nautilus (Basil et al., 2002), Loligo (Gilly & Lucero, 1992; Buresch et al., 2003; King, Adamo, & Hanlon, 2003) and Sepia (Boal, 1997; Boal & Marsh, 1998; Boal et al., 2010). Here we investigate behavioural evidence for detection and attraction to conspecific odours by Octopus.
 

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Octopus researcher a sucker for hard work
Interesting new research but no paper yet.

THE sex life of an octopus is the subject of a study by University of WA Ocean’s Institute-backed James Cook University researcher Peter Morse this summer.

“We want to know just how the females are choosing some males’ sperm over others, because there are often many fathers in any egg clutch,” Mr Morse (28) said.

Last summer, his traps for the cephalopods along the WA coast, including Cottesloe and South Fremantle, contributed to results published in the science journal Behaviour last month.

The venomous male southern blue-ringed octopus being studied is allocated about 50 sperm during its seven-month life.

Females store different males’ sperm in a gland behind their heads, before potentially deciding which to use to fertilise precious eggs, then they dig a burrow or hide to protect their young.

The mothers eventually die after protecting the eggs for two months, while the males die when they have exhausted their sperm.

“We also would like to know how the males seem to be aware of how much sperm the females are holding, and because they have a limited amount of sperm in a lifetime they seem to be regulating the amount they are using,” Mr Morse said.

His previous studies indicated males appear to be able gauge just how much sperm from their competitors are being held by the females and males change the amount of sperm they leave with a female, while ensuring they have enough left for mating with other females.

“They seem to strategically allocate their limited sperm,” Mr Morse said.

Last month, he started weekly collections from about 200 octopus traps 50m-100m offshore from South Fremantle power station, near to where he trapped more than 110 animals in Cockburn Sound a year ago.

”What we’re doing is verifying the behaviour indicated by our previous research that showed males mate to maximise retention of a limited amount of sperm,” Mr Morse said.

“We are trying to determine how the different times spent by a male mating with a female affects the pattern of fatherhood.”

The traps, which Mr Morse collects by snorkelling, should not be disturbed and have AIMS Research written on their buoys.
 

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Octopus - Mating Mimics
Published on Apr 3, 2013
These mimic octopus are known for impersonating other creatures ... this time they are just getting amorous! In this unique video you can see the mating struggle of the mimic octopus and also the hilarious reaction of our underwater cameraman - Christian Loader.
 

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SQUID
When should male squid prudently invest sperm?

Amy K. Hoopera,Benjamin J. Wegenera, Bob B.M. Wonga 2016 (subscription)

Ejaculate production can be costly and males are expected to prudently allocate this potentially limiting resource to higher quality females. However, relatively little is known about facultative sperm allocation in response to the quality distribution of sequentially encountered females, despite this being a more realistic scenario for males in many species. Here, we examined patterns of male investment in a squid, Sepiadarium austrinum, when presented sequentially with small versus large females. Owing to a positive size – fecundity relationship in this species, large and small females are expected to differ in terms of their perceived quality to males as potential mating partners. Yet, despite large sperm investment and significant variation in female quality, sperm investment was determined only by mating order, with males consistently decreasing sperm investment in second matings. These results highlight that, when mates are encountered sequentially rather than simultaneously, prudent sperm allocation may not occur when it is otherwise predicted.
 



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