Male reproductive system and spermatophores production and storage in Histioteuthis bonnellii (Cephalopoda: Histioteuthidae): A look into deep-sea squids׳ reproductive strategy

Abstract

Coleoid cephalopods go through a single breeding period in their life cycle, i.e., they are semelparous, although a great flexibility has been observed in their reproductive strategies, which range from simultaneous terminal spawning over a short period at the end of the animal׳s life to continuous spawning over a long period of the animal׳s life. So far, the information available on deep-sea species reproductive strategies is still poor and most of our knowledge about squid reproduction relates to females. In particular, not much is known on what strategy male squids have evolved to store sperm into spermatophores and adapt to semelparity. In this study an investigation of male reproductive strategy of the deep-sea umbrella squid Histioteuthis bonnellii (Férussac, 1835) is presented. The reproductive system was examined in 119 males caught in the Sardinian waters (Central Western Mediterranean) and is described for the first time. Results indicate that this species produces and stores spermatophores over a considerable period of time. The total number of spermatophores found in the reproductive system ranged between 12 and 3097 and the size of spermatophores stored by a single individual varied greatly, up to over 300%. Spermatophore length (SpL) gradually decreased towards the distal end of the reproductive system, so that spermatophores found in the proximal part of Needham׳s Sac were larger than those found in the terminal organ. Body size and SpL of spermatophores from the proximal part of Needham׳s Sac were positively correlated. Both indices of the sperm mass and of the ejaculatory apparatus decreased with the increase of SpL, while the cement body index increased, indicating that larger spermatophores contain less sperm and are equipped with larger cement bodies. Up to 64 spermatangia were found, exclusively in the terminal organ. The large size range of mature males (ML: 60.0–198.0mm; TW: 113.50–2409.00g) and the variation in spermatophore number and size indicate that in H. bonnellii males the allocation and storage of sperm start early in the individual life and extends in time, while animals continue to grow and produce spermatophores presumably more successful in attaching to female tissues. This pattern enlarges the time window available for reproduction and likely maximizes the percentage of mating success as the animals grow older and chances of mating events become comparatively lower, due to the basic low density of specimens in the deep-sea environment. Both aspects are potentially indicative of adaptation to the deep sea.