Learn About Octopuses & Relatives: Reproduction

Sexes are separate in octopuses and can be differentiated in mature specimens by the presence of the special hectocotylus on the 3rd right arm of the male.

NOTE lit. “hundred cups” G., referring to its many modified suckers. The hectocotylus has a ciliated groove down its length for delivering spermatophores to the female

Courtship & copulation

Stages in reproduction of octopuses include COURTSHIP & COPULATION, dealt with here, and EGG-LAYING & HATCHING, and PELAGIC DEVELOPMENT OF JUVENILES, considered in other sections.

Research study 1

Courtship has not been described in detail for all west-coast species, but some field and aquarium descriptions of mating are available for Enteroctopus dofleini. Courtship and mating may be done from a distance, or with the male “mounted” on the female, either on top or on the side. Some accounts describe the male being positioned outside a den, with a presumed female being inside. Copulation is preceded and often accompanied by colour and skin-textural changes, especially in the male. There is some thought that the male may use the spoon-shaped tip of its hectocotylus to clean out residual sperm or spermatophores deposited from previous mating(s) from the female’s oviducal openings in a strategy of sperm competition. Gabe 1975 Veliger 18: 146; Anderson et al. 2003 Proc Georgia Basin/Puget Sound Res Conf p. 1. Drawing courtesy Pearse et al. 1987 Living invertebrates Blackwell Sci. Publ., Palo Alto, California.

drawing of mating octopuses

Copulating octopuses

photograph of octopus showing hectocotylus arm

A small Octopus sp. with hectocotylus visible. This specimen is preserved for class study 0.6X

Research study 2

photograph of interacting octopuses Enteroctopus dolfleini in Puget Sound, WashingtonA description of an unusual “aggressive” encounter between 2 adult octopuses Enteroctopus dofleini in Puget Sound, Washington is acknowledged by the authors as possibly being courtship behaviour. In this instance the interaction lasted about 5min and included reciprocal "attacks" with interlocking arms and alternating colour changes: mottled reddish-brown for the attacker and blanching for the attackee. The authors note that the behaviour they witnessed is somewhat different than that reported for usual reproductive behaviour in octopods. Sexes of the "protagonists" could not be determined. Kyte & Courtney 1977 Veliger 19: 427.

Research study 3

photograph of egg capsules of a squid Doryteuthis sp.An unusual behaviour in squids Doryteuthis opalescens involves the guarding of egg masses by males. The observations are made on squids caught at Santa Catalina Island and San Diego, California and studied shipboard, or on squids caught commercially and studied in the laboratory. After an egg capsule is attached to the aquarium tank a male may take up guarding position over it, directing postural and colour changes to challenging males. Most often the challenging male retreats but, if not, the 2 males may square off and lunge back and forth, sometimes with damage being inflicted. The “resident” or dominant individual usually wins these interactions. If not, the challenging individual becomes dominant and takes up position over the egg mass. Interestingly, females are allowed to approach, but not males. It is not known if such behaviour occurs in the field. Hurley 1977 Mar Behav Physiol 4: 195.

NOTE from a subjective viewpoint, the behaviour seems to be one of guarding. However, from an objective viewpoint, there may be other interpretations. For example, is it possible that the males, through reception of pheromones from the eggs, may be perceiving the egg mass to be related to a female's presence?

NOTE 8x1.2cm in size, containing 180-300 eggs

Research study 4

During mating a male Enteroctopus dofleini uses his hectocotylus to transfer 2 spermatophores from his vas deferens into the genital or oviducal openings of a receptive female. The spermatophores are quite long, and following copulation the empty ends may hang free of the female’s mantle cavity for a time. About 40d after copulation the female attaches strings of fertilised eggs (18,000–70,000 eggs, each 6mm diameter) onto the photograph of octopus Enteroctopus dolfleiniundersides of rocks in crevices at 10-30m depth. The female guards and cares for the eggs during the approximately 160d developmental period. The eggs hatch directly to juveniles that spend 1-2mo floating and feeding in the plankton before settling to the sea bottom. The male parent dies a few weeks after mating, while photograph of unfertilised eggs of octopus Enteroctopus dolfleini courtesy Shawn Robinson, SFU, Burnabythe female parent dies a few months after mating. Enteroctopus matures at 2-3d of age, and lives for about 5yr, as long as it doesn’t mate earlier. Hartwick 1983 p. 277 In Cephalopod life cycles Vol. 1 Species Accounts (Boyle P.R., Ed.) Academic Press, London. Photos courtesy Shawn Robinson, SFU, Burnaby.

Octopus Enteroctopus dofleini

Eggs of octopus Enteroctopus dofleini. These particular eggs happen to be unfertilised 1X

Research study 5

drawing of reproductive tract of a male octopus Enteroctopus dolfleiniReproductive maturation in a male Enteroctopus dofleini culminates in the formation and storage of spermatophores, which are long rope-like structures containing sperm. Up to 10 mature spermatophores may be present in a special storage sac known as the spermatophoric sac, and 2 are normally used during acopulation. The sperm are manufactured in the testes (see accompanying diagram) and move through several regions of the vas deferens where they are coiled into a rope, and where various gels and membranes are added. The spermatophore eventually enters the opening to the prostate and, like a train on a blind-ending track, it has to back out after receiving other modifications, and then moves into a storage organ, the spermatophoric sac. From there the spermatophores, often in pairs, are moved into the diverticulum and thence to the penis. A single spermatophore in Enteroctopus is 1m in length, contains a coiled sperm rope over about half the length, and a complicated ejaculatory apparatus in the other half. The sperm rope contains about 108-1010 spermatozoa. If unraveled the rope would be about 4m long. Multiple copulations are the norm for a male Enteroctopus but, with only about 10 spermatophores in total, its reproductive activity is limited. Mann et al. 1970 Proc Roy Soc Lond B 175: 31.

NOTE lit. “sperm carry” G. Spermatophores in E. dofleini are the longest described for any cephalopod species

NOTE also known as Needham's Sac

Research study 6

After a short courtship, the male 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 (the photograph on Right illustrates these different parts). This action locks the sperm-filled swelling in place within the oviduct and prevents it from dropping out of the female.

photograph of spermatophore of octopusThe 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 Left).

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 as “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 2 empty spermatophores hanging from its oviducal orifices. Mann et al. 1966 Nature 211: 1279; Mann et al. 1970 Proc Roy Soc Lond B 175: 31.

NOTE a spermatophore similar in morphology to this is described for O. bimaculoides; in this case, a torpedo-shaped tube containing sperm at one end and an ejaculatory apparatus at the other. The author of the work on O. bimaculoides appears not to have witnessed ejaculation. Peterson 1959 J Morph 104: 61; see also Longo & Anderson 1970 J Ultrastruc Res 32: 94 for details of spermatophores of O. bimaculatus

Research study 7

photograph of octopus Enteroctopus dolfleini with two 4th-arm hectocotyliAs if one weren’t enough, a giant Pacific octopus Enteroctopus dolfleini is discovered off the coast of Unalaska Island in the Aleutian archipelago that bears not one, but two, hectocotylus arms. This unusual condition has been seen in other octopus species, but has always involved the 3rd pair of arms. In the present case, unique for E. dolfleini and for octopuses in general, it involves a double hectocotylisation of the 4th arms. The University of Alaska Fairbanks researchers who found this anomalous individual report no additional unusual features, reproductive or other. Brewer & Seitz 2013 Malacologia 56 (1-2): 297.

NOTE the spermatophore-transferring arm in octopuses is normally the 3rd right arm, while in squids it is the 4th left arm

Research study 8

photograph of Octopus bimaculoides

A laboratory study done at the University of Texas Marine Science Institute, Port Aransas on octopuses Octopus bimaculoides collected in southern California finds that male competition for mates depends upon female maturity, but not in the way you might think. In this case, male-male aggression is significantly greater in the presence of immature females than mature ones. The significance of the behaviour is not immediately clear, as immature females by definition are not ready to mate. However, as both types of females resist mating advances of the males to a similar extent, it may be that greater male-male aggression leads to the dominant male being able to spend generally more time in contact with females. The authors conclude, not surprisingly, that males are able to assess the reproductive status of females. Mohanty et al. 2014 Mar Biol 161: 1521. Photograph courtesy Roger Hanlon, Marine Biological Laboratory, Massachusetts rogerHanlon.

NOTE greater aggression involves early and more frequent attacks between the males, and longer fights. The authors do not define what constitutes a “fight”

NOTE such resistance takes the form of grappling by the female before or after making sudden moves in an apparent effort to dislodge the male hectocotylus from her mantle cavity