AbstractThe reproductive system is described from 15 giant squid Architeuthis sp., collected between 1972 and 2002 in South African waters. Distinctive features of the male reproductive system are the long muscular terminal organ, with elaboration of the anterior end, and modification of the tips of the ventral arms, probably hectocotilization. The spermatophoric organ has a long finishing gland that extends from the base of the gill. The terminal organ is differentiated internally into three distinct parts, involved in the guidance, storage, protection, expulsion and possibly the coating of spermatophores. Length of spermatophores in the terminal organ varied considerably. Several stages of spermatophores were found, from tentative to false to fully formed spermatophores, within a single animal. Distinctive features of the female reproductive system are a mesentery surrounding the main blood vessels of the ovary and attaching the ovary to the dorsal gladius chamber, multiple branching (at least three times) of the genital aorta that supplies the developing oocytes, high potential fecundity (3.5–6.2 ± 106 oocytes), small eggs and short oviducts that suggest intermittent (extended) spawning. Large concentrations and single spermatangia were found in various places in females, indicating non‐specific deposition. The transfer of spermatophores is probably rapid, perhaps because of considerable sexual size dimorphism (at maturity, males are much smaller than females). Implants in males are probably self‐induced since the majority were found within reach of the terminal organ opening (primarily on the ventral arms in males).
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