Principal features of the mating system of a large spawning aggregation of the giant Australian cuttlefish Sepia apama (Mollusca: Cephalopoda)

Abstract.

Every winter thousands of cuttlefish (Sepia apama Gray) aggregate to spawn along a restricted area of rocky reef in northern Spencer Gulf, South Australia. It is the only known spawning aggregation of cuttlefish in the world and represents an exceptional cuttlefish mating system. Spawning population structure and reproductive behavior were studied quantitatively by underwater visual transects and by focal-animal behavioral sampling with video from April to August 1999. The operational sex ratio averaged 4:1 (males:females; maximum=11:1), resulting in intense male–male competition for females. Both sexes sought and accepted multiple mates. Mating occurred in the head-to-head position, with a mean mating duration of 2.4 min. The long interval between individual eggs being laid (minimum=6.5 min) allowed multiple matings to occur in between laying eggs and provided the opportunity for multiple paternity, sperm competition, and cryptic female choice. Males used multiple characteristic reproductive behaviors with respect to size and status (i.e. lone or paired). Males paired with and defended females, rather than defend egg-laying sites. Paired males guarded females (both pre- and post-copulation), which is a key feature of sperm competition. Lone males either searched for lone females, challenged paired males for the takeover of females through dramatic agonistic displays, or watched for opportunities for extra-pair copulations (EPCs). They used "open stealth," "hidden stealth," and female mimicry (small males only) to achieve "sneaker" EPCs. Females showed direct mate choice by rejecting 70% of the 122 mating attempts, at times rejecting large males to mate with smaller males. Lone females moved extensively in search of egg-laying sites and interacted with many males, possibly to increase male competition. Likewise, by aggregating to spawn and spawning asynchronously, females may also increase male–male competition through indirect mate choice. The nature of the mating system of the S. apama spawning aggregation has implications for understanding the species' life history and the impacts of fishing.