Dr Crissy Huffard pointed down to the shallow seagrass beds. I couldn’t focus on what she was pointing at and we lifted our heads above the water. “Down by the rock, it’s really tiny,” she clarified. Down again and there, almost impossible to see, was the smallest octopus. It hid itself shyly behind a rock as we looked down. The pygmy octopus of Sulawesi that Crissy was studying eyed us suspiciously. Hovering above it, with a surprise I realised we were also being intently studied. Later, we spent time with two other celebrity species, the wunderpus and the mimic octopus, and I began to share Crissy’s passion for these intriguing animals. Octopuses have a reputation for being intelligent and almost mythically so. Scientists have long known that they can solve complex puzzles, navigate through mazes, are masters of disguise and accurately imitate other species. But some scientists go further, suggesting these invertebrates engage in play and even have personalities of their own. Was there more to discover beneath these rocks?

Dr Crissy Huffard is marine biologist with Conservation International in Indonesia. Her love affair with the enigmatic octopus was, like most twists of destiny, an accident. “I’ve always wanted to study invertebrates and originally wanted to study squid,” she says, but the biologist she wanted to study with was busy. It was fortuitous turn of events, as Crissy ended up studying with Eric Hochberg, a world authority on octopuses at the Natural History Museum of Santa Barbara, California. And Crissy has been at the forefront of some of the most exciting research on octopus behaviour ever since.

There are 300 species of octopus around the world and, in Sulawesi, the centre of their diversity, the mimic and the wunderpus stand out. Both species are found in the rich seas of Sulawesi, are well known for their remarkable shape-changing abilities and bizarre mimicking of other species. They do things that we normally would only expect vertebrates to do, and their intelligence is starting to make researchers wonder just how smart these animals are. Undescribed until 1998, the mimic octopus remains something of a mystery to science. Crissy’s research on the mimic octopus, Thaumoctopus mimicus, has revealed some intriguing behaviour and opened further questions about learning and response in invertebrates. It is a showcase for one of nature’s most remarkable abilities: an animal that can impersonate flatfish, lionfish, mantis shrimp and sea snakes, amongst others, to deceive potential predators. Not only does the mimic change its colour patterns and shape, it also adopts a good impersonation of movement, such as the undulating swims along the seabed of a flatfish. The amazing thing about this behaviour, according to Crissy, is that mimics have evolved a defence that relies on predators seeing them, rather than not seeing them, unlike many of their octopus relatives that use camouflage to hide. Perhaps most intriguing however, is that the mimic octopus presents a form resembling what it considers to be the greatest threat to its potential predator. So when attacked by damselfish for example, it mimics the banded sea snake, a known predator of damselfish. But is such behaviour inherited or learned, and how does it decide what to mimic? No one yet knows how mimic octopuses choose to perform one behaviour over another, and the full repertoire of models is still up for debate. It seems that unlocking one of nature’s greatest enigmas may take some time.

The mimic has an impressive number of impersonations at its disposal. “The stomatopod [mantis shrimp] mimicry looks to me like any old octopus sitting at its den entrance,” says Crissy, providing an example. “And the tunicate mimicry could fall under the definition of camouflage.” She points out a critical element in studying behaviour of animals: “What we scientists think doesn’t matter. It’s what the predators think, and none of this has been tested.” To find out more about how such behaviour came about and how much is learned or coded into the animal’s genetics, Crissy has turned her attention to studying its evolution. With colleagues from the California Academy of Sciences, Crissy and the team used DNA analysis to look at how and why this intriguing ability evolved in an animal that usually relies on invisibility to avoid predators. Octopuses are normally masters of camouflage, changing the colour of their skin through chromatophores, the pigmentcontaining and light-reflecting cells found in amphibians, fish, reptiles, crustaceans, and octopuses. Instead of blending in to avoid detection, the mimic gets out and actually displays itself in the most spectacular of ways. Using DNA sequencing to construct a genealogy of the mimic and 35 of its octopus relatives, the team was able to chart the order in which key mimic traits evolved.

First, the mimic’s ancestors used bold brown and white colouration to shock predators when their camouflage was unsuccessful. Later, ancestors developed the swimming method used by flatfish and the longer arms to facilitate this behaviour. The last evolutionary step was combining these abilities; so the mimic, at the end of this particular evolutionary line, can now display bold colouration and swim like a flatfish. It is, they say, a very risky shift in defence tactics. “Somehow through natural selection, being conspicuous has allowed T. mimicus to survive and reproduce more successfully than some of its less showy ancestors, and eventually evolve into its own lineage,” Crissy says. Working out how they select what to mimic is more difficult. “These are fundamental aspects that need to be worked out before we can assess the role of choice in mimicry,” she says. Perhaps even more sensational are revelations that not only do octopuses engage in play, but that they also have personalities in the human sense. Discussions of animal personality are controversial and hard to measure and quantify. Personality is classed as “temperamental differences” between individuals within a species. In humans, for instance, life in an ever-changing environment with numerous threats requires a large variety of responses, and therefore, the evolution of different temperaments or “personalities”. Crissy cautiously agrees that octopus do have personalities: “In the wild, we definitely see evidence that octopuses have different ways of behaving. Call it personality if you like, this variation in behaviour has serious implications for how octopuses mate, find food, and keep them from being eaten.” She is more cautious about studies that suggest play: “None of the data I’ve seen conclusively demonstrates play in octopuses.” But in science, as always, further study is needed.

Intelligent? Well, that all depends on how you define intelligence. Complex? Yes, without a doubt. Work by Crissy and others is challenging our expectations of animal behaviour, especially in invertebrates. Crissy will continue her work on the bizarre octopuses of Sulawesi “not through any special connection”, she says, “but because they play key roles in marine ecosystems, are biologically and behaviourally fascinating and have a lot of potential for discovery.” Those of us with more burning questions will just have to wait and see what else science might soon uncover hiding under the rocks of the Sulawesi seafloor. Taken from Scuba Diver Australasia Issue 03/2011