Octopuses & relatives
Reproduction: Courtship & Copulation

Research Study 1

Fig. 2.  A small Octopus sp. with hectocotylus visible. This specimen has been preserved for class study 
Fig. 1.  Octopuses copulating
Courtesy Pearse et al. 1987 Living invertebrates Blackwell Sci. Publ., Palo Alto, California

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 (Fig. 1). 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. Rather than just being a mechanism for spormatophore transfer, there is some thought that the male may use the spoon-shaped tip of its hectocotylus (Fig. 2) 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

Research Study 2

Fig. 1.  Fighting or courting?

A description of an unusual “aggressive” encounter between two adult octopuses Enteroctopus dofleini in Puget Sound, Washington is acknowledged by the authors as possibly being courtship behaviour (Fig. 1). 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 one attacked. 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

Fig. 1.  Squid egg mass stranded at low tide.  The mass comprises several cases each containing many eggs, likely laid by several females

An unusual behaviour in squids Doryteuthis opalescens involves the guarding of egg masses (Fig. 1) by males. The observations are made on squids caught at Santa Catalina Island and San Diego, California and studied on shipboard, or on squids caught commercially and studied in the laboratory.  After an egg case 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 two 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. 

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 signifying a female's presence? 

NOTE  the case, incorrectly termed a capsule by the author is 8 x 1.2cm in size, and contains 180-300 encapsulate eggs

Hurley   1977   Mar Behav Physiol 4: 195

Research Study 4

Fig. 2.  Eggs of octopus Enteroctopus dofleini. These particular eggs are unfertilised as indicated by the empty contents
Courtesy Shawn Robinson, Simon Fraser University, Burnaby
Fig. 1.  Enteroctopus dolfleini ventilating
Courtesy Shawn Robinson, Simon Fraser University, Burnaby

During mating a male Enteroctopus dofleini (Fig. 1) uses his hectocotylus to transfer two 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 in total, each egg 6mm diameter) onto the undersides of rocks in crevices at 10-30m depth (Fig. 2). 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 the female parent dies a few months after mating.  Both sexes of Enteroctopus mature early, and live for about 5yr, or until first mating.

Hartwick   1983   In Cephalopod life cycles Vol. 1 Species Accounts (Boyle P.R., Ed.) Academic Press, London

Research Study 5

Fig. 1.  Reproductiv system of a male Enteroctopus dolfleini

Reproductive 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 (or Neeham's Sac) and two are normally used during a copulation. The sperm are manufactured in the testes (see Fig. 1) 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.  It then moves into a storage organ, the spermatophoric sacFrom 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. 

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

NOTE John Needham (1713 - 1781) was an English naturalish and catholic priest, with interest in squid anatomy and other aspects of biology.  He is known best for his theory of spontaneous generation, that generated much criticism and near ridicule amongst fellow scientists and educators

Mann et al.   1970   Proc Roy Soc Lond B 175: 31

Research Study 6

Fig. 1.  Spermatophore of Enteroctopus dolfleini
Fig. 2.  View of spermatophore of Enteroctopus dolfleini with sperm concentrated in the swollen distal end

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 Fig. 1). 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 (Fig. 2). 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. 

NOTE a spermatophore similar in morphology to this is described for Octopus 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); see also Longo & Anderson (1970) for details of spermatophores of O. bimaculatus

Mann et al.   1966   Nature 211: 1279
Mann et al.   1970   Proc Roy Soc Lond B 175: 31
Peterson   1959   J Morph 104: 61
Longo & Anderson   1970   J Ultrastruc Res 32: 94

Research Study 7

Fig. 1.  Alaskan Enteroctopus dolfleini with double hectocotylus arms (4th on each side)

As 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 (see Fig. 1). The University of Alaska Fairbanks researchers who found this anomalous individual report no additional unusual features, reproductive or other. 

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

Brewer & Seitz   2013   Malacologia 56 (1-2): 297

Research Study 8

Fig. 1.  Octopus bimaculoides
Courtesy Roger Hanlon, Marine Biological Laboratory, Massachusetts

A laboratory study done at the University of Texas Marine Science Institute, Port Aransas on octopuses Octopus bimaculoides (Fig. 1) 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. 

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's hectocotylus from her mantle cavity

Mohanty et al.   2014   Mar Biol 161: 1521