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The northwest coast of Spencer Gulf, Australia, is the setting for one of the most colorful and vibrant biological events: The spawning of Sepia apama, the giant cuttlefish. The greatest concentration (as many as thousands per acre) is found only on the few rocky reefs between the industrial port of Whyalla and Point Lowly, 10 miles northeast. Original photo of Spencer Gulf area: NASA. Original photo of Australia: Australian Department of Environment and Heritage.

A male cuttlefish has distinct white lines around the edge of its body, and rippling stripes along the body while guarding a female from insemination by other males. Photo: Sean Connell

If you're planning to visit Spencer Gulf in South Australia, chances are you'll bring a snorkel, mask, fins, and an interest in sex.

Cuttlefish sex.

Cuttlefish are relatives of the squid and octopus that live along Australia's southern coast. Males compete ferociously for the right to fertilize eggs, and that's where the fun begins, at least, from a voyeur's standpoint.

In the competition to place a packet of sperm inside a cavity near the female's mouth, big males shoulder aside little males. But the small guys respond with a bit of treachery. Instead of fighting a losing battle, they temporarily look like a female. "The physically smaller males who can't compete with the larger males 'dress,' or assume the appearance of females," wrote Bronwyn Gillanders, of the Southern Seas Ecology Laboratories at the University of Adelaide in our email interview.

When the little fellow adopts the body colors of a female, males that are busy guarding females figure there's more female talent in the neighborhood. "The larger male then thinks, 'Wow, I've got two females here,'" Gillanders adds. When the big guy's attention is focused on a third male, the little fellow darts in, inseminates the female, and splits. "When the large male turns away, the little male quickly assumes the colors of a male again and then zooms in and mates with the female," says Gillanders. "After that, he swims away."

It's sneaky, but it works.

Surreptitious sex among the cuttlefish has attracted attention among scuba divers and snorkelers. The burgeoning ecotourism industry in Spencer Gulf, Gillanders says, is "centered around the annual breeding aggregation for cuttlefish."

It's quite an undersea red-light district, Gillanders adds. During spawning, 85 cuttlefish may crowd into 100 square meters of shallow water.

A quarrelsome bunch
Like all animals, cuttlefish compete for the right to breed, and battles among males cause injuries and lost tentacles. To Gillanders, furtive behavior makes sense for little guys. "Presumably the small males weren't getting in on the action because they were being outcompeted or dominated by larger males," he says. "Any lesion they get from fighting can potentially be fatal through infection, so this may possibly have lead to them try alternative tactics, like sneaky sex."

Gillanders and Steve Donnellan, an evolutionary biologist at the South Australia Museum, are trying to locate other populations of the giant cuttlefish, and learn whether the various populations are breeding together and sharing genes.

To answer these questions, Gillanders and Donnellan have asked
recreational divers to spy on the cuttlefish, especially outside the main breeding area in northern Spencer Gulf, and note where individuals are mating. The helpers are also asked to retrieve individuals so they can study:

Genetics

Statolith Chemistry

Eventually, the research will give a picture of where the cuttlefish lives and whether and how it moves along the coast. Preservation tactics - especially regarding the size and location of a marine reserve to protect the cuttlefish - will be based on whether or not the populations are genetically and ecologically isolated.

Cuttlefish are selling in Asian food markets, and fishing could decimate the giant Australian cuttlefish. Although the ornate blue cephalopod is not presently endangered, Gillanders says, it is "highly susceptible to over fishing, because most individuals only live for one year. If you remove the breeders, there will be no eggs for the following year class. This removal can have devastating consequences, especially if their movements are localized."
-David Tenenbaum

Bibliography
Adelaide University

South Australia Museum

Bizarre breeding behavior