Doryteuthis opalescens (Berry, 1911) spends most of its life cycle in the nearshore environment. Upon hatching, paralarvae are found at a depth of 30 m by day and 15 m at night, this diel migration may serve to aggregate them for weeks at tidal-neritic fronts 1–3 km from shore (Zeidberg & Hamner, Reference Zeidberg and Hamner2002). Juvenile D. opalescens begin to school at a mantle length (ML) of 15 mm (Yang et al., Reference Yang, Hixon, Turk, Krejci, Hulet and Hanlon1986) or two months of age (Butler et al., Reference Butler, Fuller and Yaremko1999) and occur on the shelf just off the bottom by day and throughout the water column at night (Zeidberg, Reference Zeidberg2004). As they reach 55 mm ML the squid move off the slope (Zeidberg, Reference Zeidberg2004) and occur down to 500 m by day and at the surface at night (Hunt, Reference Hunt1996). Adult squid return to the shelf waters to spawn at an age of 6–9 months (Butler et al., Reference Butler, Fuller and Yaremko1999; Zeidberg et al., Reference Zeidberg, Hamner, Nezlin and Henry2006).

Female squid form a capsule sheath and then eject the capsule through the siphon. The female then injects the embryos into the capsule while she holds it within her brachial crown (Fields, Reference Fields1965). She then holds it in her arms and inserts it into the sand at water depths from 15 to 200 m (Okutani & McGowan, Reference Okutani and McGowan1969; Zeidberg et al., Reference Zeidberg, Hamner, Moorehead and Kristof2004). The egg capsules, containing 50–250 embryos, absorb seawater throughout development becoming longer and thicker (Fields, Reference Fields1965). Eggs are left unattended and develop over the next 3–5 weeks (McGowan, Reference McGowan1954) as they are gently ventilated by wave surge in the shallower egg beds.

Loliginid spawning aggregation behaviour is dynamic (Hanlon, Reference Hanlon1998). Male Doryteuthis opalescens provide spermatophores to females which are stored either within their mantle cavity or in a seminal receptacle below the beak (McGowan, Reference McGowan1954). Large male squid clasp females from the ventral side of the mantle—male parallel mating. Multiple smaller males are often seen adjacent to male/female pairs (Hanlon et al., Reference Hanlon, Kangas and Forsythe2004). Above the egg laying zone, regions of male–male competition and sneaker mating are described for Loligo vulgaris reynaudii which can lead to multiple sperm storage sites and multiple sources of spermatophores for each female. Males can guard mates, fight with other males to become guards, or attempt to gain extra-pair copulations (EPCs) (Hanlon, Reference Hanlon1998; Hanlon et al., Reference Hanlon, Smale and Sauer2002). Head to head mating is predicted for D. opalescens, Doryteuthis pealeii, and L. vulgaris reynaudii, but has not been seen (Hanlon, Reference Hanlon1998); this mating form is implicated as a requirement for sperm to be stored in the seminal receptacle cavity. Multiple paternity has been detected within individual egg capsules in Heterololigo bleekeri (Iwata, 2007), D. pealeii (Buresch et al., Reference Buresch, Hanlon, Maxwell and Ring2001) and Loligo forbesi (Shaw & Boyle, Reference Shaw and Boyle1997).

Here I describe the first observations of ‘sneaker mating’ on Doryteuthis opalescens spawning grounds in Monterey Bay and La Jolla, California. Egg masses and squid spawning behaviour was observed by the remotely operated vehicle (ROV) ‘Ventana’ in Monterey Bay, California in water 15–25 m deep at 9°C on 23 May 2005. Transects were made outside Monterey Harbour along the 35, 25, and 20 m isobaths. Once egg beds and mating squids were observed, focal observations were conducted for three hours. Between 20 and 25 m bottom depth, transects were conducted above the area of greatest egg concentration at 5, 10, and 15 m depths to search for larger mating aggregations up in the water column.

Additional video images were obtained from professional film-makers. Images of mating aggregations were captured by high-definition cameras in underwater housings in La Jolla, California in March 2004, by divers using SCUBA for Howard Hall Productions. Mark Shelley of Sea Studios Foundation (Monterey, CA) filmed mating and egg laying activities of Doryteuthis opalescens in laboratory tanks at Hopkins Marine Station, Pacific Grove, CA in 1984.

In Monterey, multiple mated pairs of Doryteuthis opalescens adults were observed at 20 m and 9–10°C. Mating behaviours were similar to those described previously for D. opalescens (McGowan, Reference McGowan1954; Fields, Reference Fields1965; Hobson, Reference Hobson1965; Forsythe et al., Reference Forsythe, Kangas and Hanlon2004; Hanlon et al., Reference Hanlon, Kangas and Forsythe2004). Large males clasped females from underneath, holding the mantle of the female within the arms with both squid in the same anterior–posterior plane and orientation. Males have been observed to place a spermatophore package in the mantle of females, and spermatophores have been found in the seminal receptacle of females (McGowan, Reference McGowan1954), but insertion of the package into the seminal receptacle has never been observed and is therefore speculated to occur off the spawning grounds (Hanlon, Reference Hanlon1998).

During mating, the females remained predominantly white with most chromatophores retracted. The males displayed accentuated testes with chromatophores retracted directly above the gonad, and red chromatophores displayed on the surrounding dorsal mantle and arms. Single pairs or up to seven mated pairs were observed at a time with 0–5 ancillary individuals in close proximity. On four occasions smaller ancillary squid jetted forward, up to a mated pair, and extended an arm to make contact with the female (Suppl. Video 1). These smaller individuals presumably were males, based on a mantle-length to arm-length ratio and accentuated testis display typical of male squid. The ancillary males approached the pair from an angle that ranged from perpendicular to nearly head-on. The ancillary male extended one arm and touched the female near the neck, anterior to the mantle and posterior to the head. The chromatophore pattern on the mated pair did not change during the contact. The combination of the force of this contact and a female jet, was sufficient to displace the mated pair by two body widths but did not separate them. The ancillary male contact with the pair typically lasted about 1–2 seconds. The pairs remained enjoined for minutes, throughout the sneaker mating interruption and even throughout egg laying. No dead squid were observed on the egg beds. Sneaker mating in La Jolla, CA includes both short duration (1–2 seconds) interactions similar to Monterey (Suppl. Video 2), and longer 15–20 second events (Suppl. Video 3). Throughout both forms of sneaker mating, a guard male holds a female from underneath her mantle and surrounds her head with arms that have the red chromatophores displayed. During both types of sneaker mating events, the ancillary male approaches from either head on or to the side of the pair. The sneaker male touches the female with his arms near the head, neck, brachial crown, or on the egg capsule that she is holding.

On three occasions female egg laying was observed in Monterey, CA. In one incident, a solitary female was observed holding an egg capsule when a large male attempted to clasp her. The female flashed red chromatophores over her entire body and the male let go. Then the male grabbed the female from underneath but in a head to head posture and manipulated her until they were both facing the same direction. They remained in this typical mating posture throughout the egg laying process. Once the egg capsule had been deposited, the female broke the grasp of the male and jetted up, out of view. On the other two occasions, females shook off males after egg deposition. In all cases I attempted but failed to follow the female up into the water column. The sonar system of the ROV did not detect any individuals or schools of animals within 100 m of the vehicle.

Laboratory observations of egg laying demonstrates the order of capsule and chorion placement. A guarded female can be seen holding an egg capsule within her brachial crown (Suppl. Video 4) near the bottom of the tank. The capsule sheath is less opaque than those found on the sea-floor. The capsule end that will become the anchor is distal to her arms and the tip of the capsule that remains unattached is not visible under her head. The embryos can be seen being pumped into the capsule sheath as she respires.

Attempts for extra-pair mating was observed for the first time in Doryteuthis opalescens (Suppl. Video 1–3). Extra-pair, or ‘sneaker’, mating has been described in Loligo vulgaris reynaudii (Hanlon et al., Reference Hanlon, Smale and Sauer1994, Reference Hanlon, Smale and Sauer2002) and Doryteuthis pealeii (Hanlon et al., Reference Hanlon, Maxwell and Shashar1997; Hanlon, Reference Hanlon1998). ‘Sneaker’ or ‘satellite’ male L. vulgaris reynaudii squids jet in quickly and grab the female near the base of the dorsal arms. Doryteuthis pealeii has two forms of sneaker mating: one where a lone, large male will grab a female during a brief separation from her paired male, pair with her and provide spermatophores, another where a small male jets in, mates, and escapes rapidly. Larger D. opalescens males continued to hold the females throughout the interruption and egg deposition. Sneaker mating may be the only form of reproduction available for small males who have migrated to the spawning grounds (Ish et al., Reference Ish, Dick, Switzer and Mangel2004), and are then confronted with larger females and males.

Heterololigo bleekeri mating includes male parallel, head-to-head, and extra-pair behaviours (Iwata, 2005). The spermatophore morphology of this species is related to male mantle length. While large males that mate guard insert rope-shaped spermatophores into the mantle cavity near the oviduct of the female, small males (<205 mm ML) insert drop-shaped spermatophores into the female's seminal receptacle during head-to-head and extra-pair mating. Successful fertilization rates of extra-pair mating ranged from zero to 8.5%. Differential spermatophore morphology may confer increased success for the respective mating strategies of small and large males (Iwata, 2007).

Percentage of multiple paternity in L. vulgaris reynaudii can vary from the proximal to the distal end of egg capsules. Guarding or EPC mating strategies may confer greater rates of fertilization in different locations of the capsule (Shaw & Sauer, 2004). Multiple paternity has been confirmed in D. pealeii (Buresch et al., Reference Buresch, Hanlon, Maxwell and Ring2001), Loligo forbesi (Shaw & Boyle, Reference Shaw and Boyle1997), L. vulgaris reynaudii (Shaw & Sauer, 2004) and H. bleekeri (Iwata, 2007). I predict multiple paternity is probable within D. opalescens as well and may be common in most Loliginid squids.

Squid fights have been observed wherein ‘lone males touched or pushed the pair in a low grade agonistic manoeuvre, on average there were three touches or pushes per interval’, but the lone male was engaging the consort male, interrupting the pair five times in nearly half of the observations (Hanlon et al., Reference Hanlon, Kangas and Forsythe2004). In my observations the lone Doryteuthis opalescens male was not interacting with the male, he only engages the female as he touches her neck, presumably to insert a spermatophore into her mantle (Suppl. Videos 1, 2, and 3). Furthermore, when the guard male manipulates himself down the head of the female to touch the sneaker male (Suppl. Video 2), the sneaker male immediately disengages from the female.

Similar to Loligo vulgaris reynaudii, longer D. opalescens sneaker mating attempts (Suppl. Video 3) can be described as, ‘the sneaker's hectocotylized fourth arm was placed into the arms of the female's but no details were visible; it is possible that they were placing spermatophores directly onto the egg capsule that the female was holding because the egg capsule would be blocking access to the seminal receptacle. In most of the sequences, the sneaker performed a peculiar lurch forward onto the female as he mated her, but no arm movements of spermatophore transfer could be seen with this movement (Hanlon et al., Reference Hanlon, Smale and Sauer2002)’.

As in previous surveys (Forsythe et al., Reference Forsythe, Kangas and Hanlon2004; Hanlon et al., Reference Hanlon, Kangas and Forsythe2004), I observed dozens of spawning squid during the day. The operational sex ratio was between one or two males to each female. Midwater transects at 5, 10, and 15 m over the 20–25 m bottom depth egg beds revealed no other squid. I did not observe larger groups anywhere off the bottom.

The majority of the Doryteuthis opalescens fishery (1863–2003) occurred at night by attracting spawning aggregations to the surface at night with torches or lights and then ensnaring the squid in nets (Zeidberg et al., Reference Zeidberg, Hamner, Nezlin and Henry2006). The fishery may be more successful at night because artificial illumination need not compete with the sun. Observations of squid spawning have occurred both during the day (McGowan, Reference McGowan1954; Forsythe et al., Reference Forsythe, Kangas and Hanlon2004; Hanlon et al., Reference Hanlon, Kangas and Forsythe2004) and the night (Hobson, Reference Hobson1965; Hall & Hall, Reference Hall and Hall1997; Zeidberg et al., Reference Zeidberg, Hamner, Moorehead and Kristof2004) and ‘may take place at anytime, but occurs chiefly at night’ (Fields, Reference Fields1965).

The timing of the majority of Doryteuthis opalescens spawning activities remains an area of important debate with large management implications. The ROV observed daytime spawning aggregations (Forsythe et al., Reference Forsythe, Kangas and Hanlon2004; this study) were far smaller than night-time spawning events targeted by the fishery or those reported in previous surveys (McGowan, Reference McGowan1954; Fields, Reference Fields1965; Hobson, Reference Hobson1965). Fishing activities mainly occur at night (except in Monterey in 2003). Therefore, determining the peak hours of reproductive behaviours could lead to the targeting of temporal closures to ensure the least amount of spawning disruption. Furthermore, some fishermen have suggested that a 12-h per day closure (i.e. 0300 to 1500 h) should be added to the management plan. Benefits of a temporal closure could be three-fold: eliminating a dangerous 24-h workday, allowing the species some time for uninterrupted spawning in the day and the night, and decreasing the potential impact of 120 hours of non-stop harvest on spawning activity.

Proper management of the California market squid fishery is important to the birds, fish, and marine mammals that utilize this organism as a key forage species (Morejohn et al., Reference Morejohn, Harvey and Krasnow1978). Market squid landings in Monterey have fallen since the 2002/2003 season when effort occurred both day and night (Sweetnam, Reference Sweetnam2006) until 2007 when there were no landings. Similarly the numbers of squid egg masses in the region have decreased in acoustic and ROV surveys since 2004 (Foote et al., Reference Foote, Hanlon, Iampietro and Kvitek2006).