Octopus (26 page)

Once courtship is finished, octopuses proceed to actual mating. The method by which octopuses mate has been known for millennia. Aristotle, in the fourth century BCE, stated, “The male octopus has sort of a penis on one of his tentacles … which it admits into the nostril of the female.” While inaccurate in details (the mantle cavity is not a nostril), his observation was remarkable for his time and essentially correct. Despite a long history of observations, octopus mating behavior has been accurately reported in relatively few species and from fewer yet in the wild.

During mating, octopuses may employ either of two general positions, either the male on top of the female (mounted mating) (see plate 33) or side by side (distance mating). During the side-by-side position, the hectocotylized arm is extended some distance to reach the female. A male may stay outside a female's den, flashing skin displays and watching her behavior to assess her readiness and willingness to mate. He can just extend the mating arm into the den and into the female's mantle cavity to accomplish spermatophore transfer. There is some debate in the literature about whether males grab the female closely or extend the arm from a distance, and this
second position for mating may allow a male to court a female while both stay protected inside their dens. A pair of octopuses has been observed in adjacent tanks in captivity doing this, the male's arm extended up into the air, over the tank edge, and into the female's mantle cavity.

Roger Hanlon and John Messenger (1996) classified a number of octopus species according to whether they used mounted or distance mating, but some species used both methods. The Caribbean pygmy octopus used mounted mating in the laboratory and distance mating in a well-spaced seminatural situation, so mating positions may be different in one species in different environments.

While there are approximately 100 octopod species in the genus (and 300 in the order), mating behaviors have been only been reported in a few. The lack of mating observations even applies to the giant Pacific octopus, the octopus most kept by public aquariums. There are two brief descriptions of matings by giant Pacific octopuses, and both were in captivity, so these observations may not be good descriptions because they could be influenced by unnatural conditions of crowding and sudden contact.

The different conditions—wild versus captive, distance versus mounted—and limited observation times for these matings make a thorough description of giant Pacific octopus mating difficult to develop. But there are a few consistent mating features. Males were darker than females, generally a dark reddish brown color. They typically displayed frontal and mantle white spots, while the females did not. Skin texture also varied with sex; males were papillose while females remained relatively smooth. Mann has also noted these colors in mating giant Pacific octopuses in captivity. Giant Pacific octopuses also used both mounted and distance matings in aquariums and in the wild.

These observations on mating confirm Jennifer's observations on the pygmy octopus, that mating positions may be opportunistic. Some octopus species may mate either at a distance or in the mounted position, depending on their setting, and such flexibility is adaptive. When a male encounters a female in the open while they are foraging, mounted mating may be possible. If a female is in a narrow den, the male may only be able to stretch an arm to her. Since the male is usually the active partner, he probably must do what he can to ensure that contact is maintained (see plate 34).

Observations of matings of giant Pacific octopuses in the wild are incomplete. A complete mating of four hours, including possible courtship or male displays, is hard to witness because of the short time divers can spend
underwater before they run out of air, as Cosgrove reported in 2009. Future use of ROVs and submersibles will help us get compete mating reports, but those observations are very expensive, requiring hours of downtime in a submersible.

Mating (not including courtship) is longer in giant Pacific octopuses than in most other octopuses, averaging about 260 minutes. Only the red-spot night octopus has been reported to take longer, 360 minutes. The giant Pacific octopus may need this amount of time because it lives in cold water and all life processes of poikilotherms, which cannot maintain a constant body temperature, are slower in colder water. But James reports that the deep-sea spoon-arm octopus, which lives in water just above freezing, mates in just three minutes, so this may not be the answer. Also, the giant Pacific octopus has the longest octopus spermatophore, each containing about seven billion sperm. Mann states, with tongue firmly in cheek, that this amount of sperm is equal to thirty human ejaculations. Males can easily produce billions of sperm, but it is not easy to produce spermatophores when each contains billions of sperm. The placement of such a large, limited, and valuable resource is highly critical and may take much time.

Jennifer has pointed out that octopus mating is much more than mere copulation, and that documented reports should include other behaviors. Beyond the act itself, there are differences among species in such factors as position, body patterns, courtship behaviors, and male displays. Observations of matings tend to be by chance, but we need more careful studies for comparisons among species. At a minimum, observers should note location, habitat, species, size, relative maturity, position, posture, body patterning and its changes, possible courtship actions or display, contextual variables about possible courtship, mating duration, respiration rate, and the number of the Arch and Pump spermatophore transfers.

After mating, a male octopus goes into a life stage known as senescence. Public aquarium representatives frequently call us about this condition. They say their octopus is not eating and he is losing weight. He's acting strange—not going into his home, and moving around the tank in the open much of the time. As time progresses, his skin develops lesions and the animal loses coordination. People notice and start asking about the welfare of the animal. This phase is a familiar one in the life cycle of the octopus. At the Seattle Aquarium, giant Pacific octopus Clyde weighed 40 lb. (18 kg) when he was collected. He thrived in captivity for five months
and grew to 70 lb. (32 kg) but then stopped eating. He crawled all over his tank, even into stinging sea anemones that he normally avoided. He lost 22 lb. (10 kg), 32 percent of his body weight during two and a half months, and then died. Clyde had the normal symptoms of octopus senescence, a precursor to death from old age. These behaviors among octopuses have been observed for millennia. Aristotle said the females became stupid after giving birth, that they could be found being tossed about in the water, and it was easy to dive and catch them by hand.

Senescence occurs at the end of a male octopus's natural life span and often lasts for a month or more. In captivity, however, octopuses may show senescence-like symptoms and even die because of poor water quality (from such problems as lack of dissolved oxygen, low pH, pollutants, or incorrect temperature), stress, and disease.

The physiological processes that drive maturity and senescence in octopuses are now fairly well known. The process is started by hormones from the optic gland, which cause dissolving of proteins in the arms, maturing of the reproductive organs, and eventually inactivation of the posterior salivary and digestive glands and loss of appetite. The optic gland is activated by environmental factors such as light, temperature, and nutrition, which ultimately control timing of reproduction and life span. Wodinsky found in 1977 that removal of the optic gland causes immature females to live to double the normal lifespan but they don't reproduce.

Four conditions or activities are indicators of octopus senescence. First, many researchers and aquarists have noted the loss of appetite in both male and female octopuses at this stage. Second, as the animal loses weight, the eyes of octopuses stay the same size while the body shrinks, causing the eyes to appear to bulge. Third, the increased activity at the start of senescence is undirected activity, not hunting, foraging, or performing other useful activities. Fourth, white skin lesions appear. A young octopus in good condition and with good water quality can get an injury that causes such lesions, but in that case they will heal. But the healing processes of old octopuses cease during senescence, so skin injuries may become secondarily infected.

Both male and female octopuses can go into a physiological decline, but females typically brood their eggs faithfully during this time. Male octopuses go into senescence without a clear transition, but they can survive a surprisingly long time without eating. At the Seattle Aquarium, seven male giant Pacific octopuses stopped eating an average of forty-eight days
before dying and lost 17.4 percent of their body weight. In the wild, undirected activity of a senescent male octopus is likely to get him eaten by predators. Senescent male giant Pacific octopuses and red octopuses are found crawling out of the water onto the beach, obviously not a normal behavior and likely to lead to attacks by gulls, crows, foxes, river otters, or other animals. Senescent males have even been found in river mouths, going upstream to their eventual death from the low salinity of the fresh water.

Some observations of octopus couplings have occurred that are puzzling. One bizarre encounter in the depths of the ocean was filmed by the submersible Alvin and reported by R. A. Lutz and Janet Voight in 1994. This meeting in the depths would have been interesting just as a film of behavior, since seeing an octopus mating is valuable. But in this observation, the two octopuses were male members of different, undescribed species. The smaller male on top assumed a typical mounted position, parallel to the one underneath. He inserted his hectocotylized arm into the mantle cavity of the lower male and his respiration rate increased.

Such an encounter tells us something about octopus mating systems. If a male detects another octopus, maybe in desperation he'll try to mate with it, with an urge to pass on his genes to the next generation. As yet, we don't know the motivation of the lower male. He was quite capable of turning on the other octopus, and killing and eating him. We don't know the ultimate outcome of this deep encounter, whether the sexually active male realized his error, or whether he simply wasted spermatophores trying to mate with another male.

Octopuses have an intriguing sex life. Hidden beyond what we know may be elaborate courtship rituals, and perhaps there may even be mate guarding, multiple matings, or cannibalism once the act is over. Octopuses die at the end of their reproductive process, females literally wasting away, guarding eggs until they die, and males going through senescence and probably getting eaten by predators. While the octopus's death is not a noble one by our standards, the animal's pattern of reproducing and dying has ensured survival of the species.

11

The Rest of the Group

S
cientists are still in the process of learning about the octopus, an animal that is but one example of the class Cephalopoda. The cephalopods are composed of the present-day nautilus, which belongs to an ancient subclass of molluscan cephalopods known as the Nautiloidea, and all other living cephalopods that belong to the subclass Coleoidea. Since the coleoid group has evolved relatively recently, we find it helpful to study the variations among these other animals—squid, cuttlefish, and deep-sea vampire squid—for what they might reveal about the cephalopod pattern. Looking to other cephalopods for similarities and differences in biology and behavior can lead to findings about what it means to be an octopus. So let's examine seven animals whose variations on the cephalopod pattern we know something about.

The first cephalopod of interest is the nautilus, a remnant of the ancestral shelled cephalopods related to the octopuses' molluscan ancestors. The nautiluses flourished at the same time as the ammonoids and belemnoids, early cephalopods that are well known because their fossilized shells are plentiful in rocks up to hundreds of millions of years old. Most of these now-extinct cephalopods died off at the end of the Cretaceous Period, about 65 million years ago, the same time the dinosaurs disappeared. Only one genus of those ancient cephalopods, the six species of Nautilus, has survived in the deep ocean, remaining unchanged for at least 100 million years. Nautiluses are considered to be “living fossils,” like the crocodile and the horseshoe crab.

Nautiluses live in a coiled shell that can grow to 10 in. (25 cm) across. The shell can be compared with a snail shell, but snails develop a twisted coiled shell while the nautiluses' shell coils on one plane only. And the nautilus shell is made up of many chambers. The animal makes more and more chambers as it grows, and it sits in the biggest, outermost chamber, which is open to the sea. The other chambers fill with fluid, with a siphuncle, a
piece of tissue like a living hose, connecting the inner chambers. To change its buoyancy and float up near the surface or return to the deep, the nautilus can vary the amount of fluid in these chambers by pulling it out by osmosis. This technique for buoyancy control is the same one that humans use for operating submarines. In honor of the resemblance, two famous submarines were named Nautilus, Captain Nemo's vessel in Jules Verne's 20,000 Leagues under the Sea and the first atomic-powered submarine.

The nautiluses look like a primitive version of cephalopods in other ways. Their brain is much simpler, though they still have memory like the octopus. Their eyes are more primitive, working like an old-fashioned pinhole camera, with no lens, and open to the seawater. Nautiluses can see images with this system, but their vision is blurrier than the sharp sight of octopuses and squid. Interestingly, they likely use chemical cues in the water to sense when prey is near, in the same way that octopuses get chemical cues from the bottom when searching for crabs and snails. Instead of eight arms, they have about ninety tentacles to grasp their slow-moving prey, usually crustaceans.