Octopus (25 page)

As we followed her progress, we saw no matings, but it seems likely that they occurred. Although her first den would have seemed to be a good place for Ursula to lay eggs, she moved into four other ones during the summer of 1999 before we lost track of her. When we last saw her, there had been no new midden material for fifty-nine days. We thought she was ready to lay eggs, since she had stopped eating and had blocked the entrance to her den with empty clamshells, a typical behavior of brooding females. Unfortunately, at about that time, a pile-driving barge moved next to the aquarium to put new treated support pilings into the bottom of the bay, which disturbed the sediment, created noise in the area, and probably put new chemicals in the water. This commotion probably scared Ursula away, since we didn't see her any more after 124 days from her release.

Once a male and female octopus have found each other, how do they mate? Aquarium visitors see all those arms and wonder, what do they do with them? And how can you tell the difference between a male and a female octopus by looking at them? More important, how do octopuses tell the difference between a male and a female?

There is a broad range of sizes at which male and female octopuses mature in most species, and many octopuses are able to mate over several weeks of their life span. So a large female can mate with a small male, and vice versa. There are also broad differences in an octopus's size at maturity within a single species across its geographic range, based on age, feeding success, and water temperature. Mature female red octopuses in California are as small as 1 oz. (28 g) in weight, while in the cold Puget Sound, egg-laying female red octopuses are frequently ten times larger. Mature spermatophore packets have been found in young male common octopuses that
are as small as 7 oz. (200 g), even though adult male common octopuses can get as big as 55 lb. (25 kg). Octopuses that live in water at the colder end of their range, like the species in the deep, tend to live longer and grow larger.

Mature octopus males of many species frequently have a few greatly enlarged suckers on the underside of their arms fairly close to the mouth (see plate 32). Scientists have made several speculations about the purpose of these enlarged suckers. One idea is that they are used as a sexual attractant during courtship. The male octopus may exhibit these large suckers to females as an indicator both that he is a male and that he is of good quality for a mate: he is big and therefore able to find lots of food. The other possible use of these large suckers might be to maintain proper position during mating. During one mating posture, a male wraps his arms around a female, and the large suckers may aid in holding this position.

The external structure that distinguishes males from females is the males' modified arm used in mating. Octopuses have eight arms. The specialized third right arm of an adult male, a hectocotylus, is usually shorter than its third left arm. It has a groove running down the webbing of the arm, along which spermatophores pass to a female during mating. This arm also has an organ—the ligula—at the end, which transfers the spermatophore into the female's oviduct during mating. It might also be used to remove sperm from the female from previous matings with different males. We don't know how the ligula finds the oviduct in the female, but the female may release chemicals that help this process.

In a parallel with vertebrates, the ligula of at least one species of octopus has erectile tissues, remarkably similar to those of human sex organs—the first finding of erectile sexual tissues in an invertebrate. Researchers have noted that the ligula of a two-spot octopus was much larger than normal after an unsuccessful mating. They then looked at tissues of preserved ligulae in museum specimens. By sectioning them, they found that the ligulae contain vascularized internal cavities surrounded by walls filled with collagen fibers, all of which are also enclosed by collagen, like in mammal penises. An expandable ligula in a male octopus might be present for several reasons. The male octopus that had evolved a way to make his ligula bigger could transfer more spermatophores, or larger spermatophores containing more sperm, during mating. It may have also evolved to allow the female to recognize a male ready to mate. Seeing the ligula, a female may be gauging quality—deciding that a big ligula means a big and therefore high-quality male—and choosing a mate by the size of his expanded organ.

Having an expandable, erectile ligula may also help an octopus protect it. The ligula of the giant Pacific octopus is uncolored because its skin doesn't contain chromatophores. And so it may stand out when the octopus camouflages to match its surroundings, though most male octopuses keep the ligula curled up at the end of their hectocotylized arm. When Jennifer and O'Dor were studying octopuses in Bermuda in 1991, they had trouble assigning sex to the animals. Females were easy, but males kept their definitive ligula tucked under the arm web, out of sight. If the ligula of this species shrinks when not in use, it would also be less visible.

There is a remarkable story about the naming of the hectocotylus of the male argonaut. The female argonaut constructs a cornucopialike shell with her first two large arms and the webbing between them. She lives in this shell, lays her eggs on it, and guards the eggs until they hatch. The shell is much prized by shell collectors when it is found washed up on a tropical shore after the eggs hatch and the female dies. Incidentally, such washed-up shells were the first evidence of this species: Aristotle knew about the shells but never saw the octopus that made them.

Although the shells and the female argonaut had been known for millennia, males were not recorded until the nineteenth century. Some strange wormlike crawling things had been found on the females' bodies, and the pioneering French naturalist Georges Cuvier (1829) thought they were a parasitic worm. He described the worm, complete with a hundred suckers, as a species new to science. He named it Hectocotylus, the worm of a hundred suckers. As scientists of the time learned more about argonauts, some doubted the validity of this description.

One doubter, Albert von Kölliker, published an article in 1845 describing the wormlike thing as the long-lost male argonaut. This was closer to the truth, but the form was actually just the broken-off hectocotylized arm of the male. Because the arms of octopuses have nerves and ganglia that give them much independent movement, a separated arm can wriggle for hours as if alive. The mystery was eventually resolved when Heinrich Müller (1852) published a paper on the true identity of the male argonaut. Males are tiny compared to the females, about one-tenth their size. The male's third left arm has a sac that contains a hectocotylized arm about ten times as long as his body, about 5 in. (13 cm), and half of it is the ligula.

Today, more than 150 years later, we still know little about the reproduction of the argonaut except that the male's hectocotylized arm matters. We know that the hectocotylized arm breaks off and ends up in the oviduct
of the female but we still don't understand the process. Argonauts are quite common, and their cast-up shells litter the shores in some areas. But they are extraordinarily difficult to keep in captivity, possibly because of stress experienced during collection or transport. Since the open ocean is a big place, we speculate that males find prospective mates by a chemical attractant given off by the females.

In a mature male octopus preparing for reproduction, billions of sperm are produced in the male's paired testes. In dissection, these organs are white, as they are in other animals such as other invertebrates and fish, so they can be easily found. There is only one duct leading from the testes, the vas deferens. It goes to the spermatophoric complex, where sperm are packaged into spermatophores, and the packets are stored parallel in a structure known as Needham's sac. Spermatophores vary greatly in size by species: giant Pacific octopuses may have only ten large spermatophores ready at any one time, but the common octopus may have 200 much smaller ones. The giant Pacific octopus spermatophore contains up to seven billion sperm and is 3 ft. (1 m) long. A worker at another major public aquarium once called to ask about a possible parasite in a giant Pacific octopus they were keeping. He described it as a clear roundworm a yard long. This was a spermatophore.

An octopus spermatophore is a complicated structure. Thaddeus Mann published a book in 1984 on invertebrate spermatophores, with a lengthy chapter on those of cephalopods. Spermatophores have a clear tunic and are filled with a viscous fluid, a rope of sperm at one end, and a complicated ejaculatory apparatus at the other. When the male places a spermatophore at the entrance of a female's oviduct, the ejaculatory apparatus everts and forces the sperm rope to the distal end, normally into the female's oviduct. In some species, the spermatophore forms a bladder the shape of a hen's egg and about that size before it bursts and releases the sperm. The sperm attach themselves to the walls of a female's special gland, the spermatheca, where they can remain viable for several months until they are used to fertilize eggs laid by the female.

The release and transfer of the spermatophores takes place in an Arch and Pump action. The spermatophore is ejected by the male's ligula into his funnel and he curves his funnel under the web and up to the base of the third arm. Then, in a series of peristaltic pumps, he slowly transfers the spermatophore into the groove of the arm. This 3-ft. (1-m) structure moves down the ciliated groove along the arm. It takes at least an hour for a giant Pacific octopus to deliver one spermatophore completely to the female. Once the octopuses are joined, during mating the heartbeat of mating males skips a beat at the passing of the spermatophore, and the females' respiration rate goes up.

Before actually mating, animals frequently perform courtship. During courtship, animals establish whether a partner is the correct species, sex, and maturity to breed with. Cross-species sex does occur, but it is futile and a waste of genes. Hybrids resulting from such matings are often stillborn or weak, and at best they are sterile. Courtship helps females determine mate quality, and it may also help bring the partners into readiness for the next stage, actual mating. Few examples of courtship have been recorded in octopuses, because they are difficult to study in the wild.

In 2008, Crissy Huffard and her colleagues documented the amazing sex habits of a small octopus, Abdopus aculeatus, in Indonesia. They observed that each male would try to pick a female and guard her closely from other males. They saw smaller “sneaker” males, which put on the colors and behaviors of females and tried to sneak pass the guardian male. The males picked the largest females they could find; larger females have more eggs in which to pass on the males' genes and they can better survive the egg-guarding process. These observations in the wild are valuable, since we haven't seen these behaviors in the lab.