Following on the success of my blog answering the important life question: “How do octopuses poo?“, it’s high time I address “How do octopuses mate?”
Why? Because truly, by having better understanding of the adaptations of species that look so different from us, I believe we can be better humans.
What has catalyzed this blog finally being written is the following video by fellow diver Mel Vincent with buddy Jerry Berry. On a night dive, what they thought was one Giant Pacific Octopus, turned out to be two AND evidence that they had likely mated. The evidence is the empty “spermatophores”.
Spermatophores? The name gives you a good sense of what those might be, they are the rope-like sperm packets of a male octopus.
This is most likely the female although in neither can the 3rd arm on the right be seen to confirm if there is a hectocotylus arm or not. Giant Pacific Octopuses are Enteroctopus dofleini, the largest octopus species in the world.
Male octopuses have a specialized arm with no suckers at the tip called the “hectocotylus arm”. In Giant Pacific Octopuses, the hectocotylus arm is the third on the right. The section at the top which has the spermatophores is called the “ligula”. This section does not have the cells that allows colour and texture to change (the chromatophores). So the males often keep it curled up which helps discern males and females i.e. look for a curled up arm.
The spermatophores are made inside the male and the male grabs them by passing the hectocotylus arm into his body through the siphon when it is go time. It’s not a fast process. Apparently it takes about an hour for the sperm to move to the top end of the spermatophore. The spermatophores pass down a grove in that arm helped by cilia. Ultimately the spermatophores are ejected by the ligula and the shape of the spermatophore (and swelling inside the female), lock it in place in the female.
Where to “deliver” the contribution to the next generation in a female octopus? Through her siphon, to her oviduct(s). The swollen end of the spermatophore then bursts and the female stores the sperm in her “sperm receptacle” till ready to fertilize and then lay her eggs. Reportedly, about 40 days after copulation (delivery of the spermatophores) the female attaches up to ~68,000 fertilized eggs to the top of the den she has chosen . . . to be her last.
Credit: Pierangelo Pirak Source: BBC article on octopus sex
In Giant Pacific Octopuses, a spermatophore can apparently be up to 1 meter long and contain over four billion sperm. Usually two spermatophores are involved in one copulation. Such large numbers of sperm, and eggs, are needed when your babies hatch into the soup of the ocean. But mother gives them a fighting chance. Read on!
The spent spermatophores apparently may hang from the female for a while so can it be known for sure that the two Giant Pacific Octopuses Mel documented had just mated, or mated at all? It can’t be known definitively but with there being two octopuses, and that they had been interacting, it does suggest that mating had occurred. It certainly is extraordinary to have chanced upon the spermatophores of wild Giant Pacific Octopuses.
Top of a male Giant Pacific Octopus’ hectocotylus arm (ligula). Photo ©Jim Cosgrove.
I am very grateful to Jim Cosgrove, Neil McDaniel and Harbour Publishing for permission to include the following text on reproduction in Giant Pacific Octopuses from their book “Super Suckers – The Giant Pacific Octopus and Other Cephalopods of the Pacific Coast. It’s SUCH a good resource.
“FINDING A MATE…OR NINE?
When a female giant Pacific Octopus is ready to mate, it appears that she selects a den and attracts males to her. There is no conclusive evidence on how the female entices males, but there are strong indications that she produces some sort of chemical attractant. There are several reasons for believing this to be true.
The first reason is that giant Pacific octopuses are ordinarily solitary, and a smaller female would normally avoid a larger male that might attack and eat her. Jim has seen as many as nine males, however, in the immediate proximity of a female in a den. The males were scattered around the den and appeared to be unaware of each other, as there were no interactions amongst them. This was most unusual.
The second reason is that Jim has observed and seen video of large males standing atop prominent rocks. The octopus faces into the current and spreads out his arms like an open umbrella, turning slowly back and forth as the current flows past. We know that octopus suckers are sensitive chemical sensors, so it’s likely that the male tastes the water flowing past. His slow turning may enable him to identify the direction of the female’s attractant.
How the female selects a male—and whether she mates with one or more than one male -are still unknown. Jim is currently working with a genetics professor at the University of Victoria to try to resolve these questions.
Once a female selects a male, there are several ways in which the male transfers sperm to her. Sometimes the male mounts the female, almost completely covering her. In other cases the male merely extends his hectocotylized third right arm into the fe male’s den. Although the actual transfer of sperm requires only two to four hours, the mating process can last several days, so divers have a considerable handicap when trying to observe such behaviour. Indeed it is a rare event to witness a mating pair, and Jim has only seen nine matings. This is one situation in which observations in an aquarium are far easier than those in the open ocean. An aquarium researcher can set up a video camera and organize teams to watch the process on a 24-hour schedule until the event ends.
Jim, along with three other researchers, has combined experiences from open ocean and aquarium observations to produce a publication about giant Pacific Octopus matings. The study revealed that the male and female mate for approximately four hours and that repeat matings have been observed. In aquariums there is usually only one male in the tank with the female, so questions about multiple males and how the female selects a particular mate remain unanswered.
The male passes the female an elongated package of sperm called a spermatophore, which may be up to one metre (three feet) long, which he deposits in one of the female’s two oviducts. It is believed that when mating the male actually places two spermatophores in the female, one at the entrance to each oviduct. At this time the female is not yet pregnant—the term really does not apply to invertebrates anyway—but she has stored the sperm and will head off to find a suitable den to lay her eggs. The male, if he still has unused spermatophores, may try to find another female.
Thę den the female selects is usually deeper than 20 m (66 ft). Jim has noted that dens where previous females have nested were reused 41 percent of the time. These preferred dens tend to be under large flat rocks that provide a suitable overhead surface for the female to attach her eggs.
Once the female selects the den, she sometimes fortifies it by gathering rocks from the surrounding area and dragging them to the den. She often piles them up to create a wall of boulders that keeps out predators. A few days to a month may elapse between mating and selecting and preparing a den.
LAYING THE EGGS
Now the female begins to lay her eggs. She turns upside down and clings to the roof of the den while she lays the tiny eggs one at a time. Each egg is produced in the ovary and coated with rich yolk to provide energy for the developing embryo. At this point some sperm is used to fertilize the egg, and it is coated with a material that hardens into a rubbery, semi-opaque shell. Each egg is extruded individually through the funnel and grasped by the small suckers that surround the mother’s mouth.
The body of the egg is a mere six millimetres (0.2 in) long about the size of a grain of rice—with a slender tail that adds another 11 mm (0.4 in), making the total length of the egg about 17 mm (0.7 in). The mother’s small suckers deftly manipulate the tail of the egg along with the fails of other eggs and weave them together into a slender string. She produces a secretion and applies it to the tails to bind them together. Over a period of three or four hours, while hanging upside down, the female produces a string containing an average of 176 eggs. Having glued this string to the roof of the den, the female descends to rest before returning to lay another string.
Eventually, over 28 to 42 days, the female will produce a complete nest of about 390 strings with approximately 68,000 eggs.
Female Giant Pacific Octopus tending her eggs. Photo ©Jim Cosgrove.
NESTING BEHAVIOUR: THE LONG WAIT
Once the female has finished laying, she spends the next 6.5 to 11 months tending the eggs. She grooms them with her suckers to ķeep them free of bacteria and other organisms that might damage them. Usually she is not completely successful, as often some eggs are encrusted by colonial animals called hydroids and do not hatch.
The female blows water through the strings of eggs with enough force that they jostle around. This helps keep them clean and free of growth and will be critical when the eggs start to hatch. She also protects the nest against predators such as sea stars, not always successfully. Mottled sea stars (Evasterias troschelii) have been observed robbing egg strings from a den.
Video above by Laura James of a mother Giant Pacific Octopus tending her eggs.
Other creatures enter the nest but do not appear to do any damage. These include small worms, snails and crabs such as the longhorn decorator crab (Chorilia longipes) and the sharpnose crab (Scyra acutifrons).
While the female tends her eggs, she does not feed. We don’t know the exact reason for this, but one suggestion is that if the female left the den to hunt, she would leave the eggs unat tended and vulnerable to predators. Another suggestion is that the presence of food scraps in or near the den might attract predators. Jim does not subscribe to either of these theories. Because this behaviour is common to many cephalopods, he believes it is more likely linked to an ancestral trait, the reason for which may no longer exist. This is an example of innate behaviour, part of the hard-wired information an octopus is, born with.
The development of the embryos depends on the surrounding water temperature. The colder the water, the slower the develop ment; the warmer the water, the faster it proceeds. This is true among most egg-laying marine invertebrates.
Jim has been able to observe much of the development in the wild and develop a time frame for estimating when hatching would occur. If he was lucky enough to have witnessed the egg laying, he would have a pretty accurate idea of how the eggs would look as they developed. In most cases he did not see the egg laying, however, and would have to observe the eggs for signs of development to predict when they would hatch.
WATCHING THE EGGS: A DIVER’S VIEW
Newly laid eggs are glossy white and look like white raindrops. The core that the eggs are woven into is pale green, but within a few weeks the core turns black and remains so.
Two small red dots appear on each egg about 120 to 150 days after the eggs are laid. These dots, the developing eyes of the embryo, are visible through the egg shell. The eggs are no longer as shiny white, and soon one can see the brighter yolk sac in the large end of the egg and the darker developing embryo at the small end.
About 180 to 210 days after the eggs are laid, the embryo has used up much of the yolk, and the size of the yolk sac has de creased while the size of the embryo has increased. So that the embryo can continue growing, it moves into the larger portion of the egg. This is actually the second reversal, but it is the only one that a diver can observe.
Over the next few months a diver can watch as the yolk sac becomes smaller and the eggs become darker. Those with sharp eyes may be able to see the movement of the embryo within the egg and the flashing of brown and white colours as the embryo tries out its chromatophores.
About 240 to 270 days after the eggs are laid, hatching occurs.
Giant Pacific Octopuses hatching. Photo ©Jim Cosgrove.
THE NIGHT OF THE HATCH
It might seem logical that the eggs would hatch over the same period of time and in the same order as they were laid. This does happen in many octopuses, including the giant Pacific octopus, but not always. Jim has witnessed a number of hatchings in which he has seen the nest intact one day and completely hatched out the next morning.
Jim collected strings of unhatched eggs from time to time and took them to his lab. When observing the eggs through a dissect ing microscope, he found that the water surrounding the eggs was warmed by the microscope lights, often causing the eggs to hatch. He probably collected strings of eggs that had not been laid at the same time, yet even eggs from different strings hatched nearly simultaneously.
Some type of chemical released from a hatched egg stimulates other eggs to hatch as well, Jim suspected. The embryos often had different amounts of food remaining in the yolk sac below their mouth. In some cases the yolk sac was consumed, but in others the yolk sac was still large enough that the paralarva had to bite it off. Clearly some of the paralarvae were not as well developed as others but were able to survive even if they hatched somewhat prematurely.
The hatch normally occurs at night. It may start at dusk, but often it is several hours after dark before things really get under way. As the eggs hatch in ever-increasing numbers, the female blows strongly onto the strings of eggs, causing them to thrash around. This helps the paralarvae to pop out of the eggs and aids in flushing them away from the den.
MOTHER’S JOB IS DONE
In most cases the female survives the hatching and lingers in the den for another few weeks before she dies. During the entire nesting period, which may have dragged on as long as 11 months, the female has not eaten. By hatching time she has lost more than 60 percent of her body weight, sometimes as much as 85 percent! Even though the eggs have hatched the female continues to “mother” them as before. She grooms the hatched-out egg cases even though the paralarvae are long gone.
Experiments have been done in which the eggs have been re moved from the ovary of a mated female. Incredibly the female went through the entire egg laying and grooming process, even though she had no eggs or nest. This “phantom nesting” shows that a behavioural lock and key is triggered at sexual maturity or at mating.
In some cases the female does not have enough energy stored to survive the whole nesting period and dies before the eggs hatch. Usually her last act is to vacate the den and crawl away. She usually only moves a metre or two before she dies. Again there is no solid evidence on why the female va cates the den, but Jim sub scribes to the theory that if the female died in the den her de composing body could foul the water and attract scavengers.. One can understand that fe males not leaving the den might have resulted, in an evolution ary sense, in the nest being dis covered and eaten. This would result in the failure of her genes to be passed on to successive generations. The genes that were passed on would be those of females who successfully distracted predators away from the nest.
While this strategy is interesting, it is not totally successful. In several cases where the female died before the eggs hatched, even though the embryos developed properly, the eggs did not hatch. Without the agitation provided by the female blowing wa ter over them, the closely packed eggs remain immobile and pressed against each other. As a result the paralarvae are unable to force their way out of the eggs, and most perish.
Jim found it sad to observe nests where only a partial hatch was successful. As he counted strings and eggs, he often found thousands of dead paralarvae. Sometimes nature seemed harsh and wasteful.”
Video below by Laura James of Giant Pacific Octopuses hatching and mother dying.
Male anatomy on left and female on right. Source: Hanlon, R., & Messenger, J. (2018). Reproductive Behaviour. In Cephalopod Behaviour (pp. 148-205). Cambridge: Cambridge University Press. doi:10.1017/9780511843600.008
Further detail on mating in Giant Pacific Octopuses from “A Snail’s Odyssey”
“After a short courtship, the male Enteroctopus dolfleini grabs the thin or distal end of a spermatophore from its penis using the groove in its hectocotylus arm and thrusts it into the orifice of one of the female’s oviducts. This initiates a complex series of events within the spermatophore that cause the sperm rope to be pushed into the thin or distal end, which swells to accommodate the incoming load of sperm and leads to evagination of the ejaculatory apparatus (see illustration on Left). This action locks the sperm-filled swelling in place within the oviduct and prevents it from dropping out of the female. The sperm rope is moved along by pressure from seawater diffusing into the proximal end of the spermatophore and from elastic contraction of the sperm rope itself. The movement takes about an hour. These actions haul the entire mass of tightly encapsulated spermatozoa over a distance of a meter from the proximal to distal end of the spermatophore. The sperm are now positioned in a swollen bladder or reservoir located at what was previously the thin or distal end of the spermatophore (see photograph on Right). The next step, evagination of the ejaculatory apparatus, occurs suddenly and produces a crink in the tube that locks it in place in the oviduct. The locking-in may additionally ensure that spermatozoa are not lost in “back-flow” from the oviduct. The swollen end of the spermatophore now bursts and the sperm are moved into the female’s sperm receptacle for later use. The process is repeated with a second spermatophore. About 2-3h after the arm is first inserted and after repeated pokings, the female has two empty spermatophores hanging from its oviducal orifices.”
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