Explosions of purple, red, and orange with bursts of iridescent blue flash before my eyes. The colours intensify as dark and light patterns flow repeatedly across the backdrop of shades like clouds in the sky. The rapid expression of electrifying colours resembles fireworks, but then I remember I am actually under the sea. The composers of the spectacular underwater light show are a pair of male giant Australian cuttlefish, Sepia apama, vigorously fighting over the opportunity to mate with a female. The rival males are engaged in a remarkable contest that reminds me of capoeira, the elegant Brazilian martial art, as both combine elements of fight, acrobatics, and dance.
Many SCUBA divers have undoubtedly come across this scene during austral winter in Australia’s temperate waters. Between May and August, giant Australian cuttlefish aggregate at rocky temperate reefs to mate. Cuttlefish are molluscs that become lovers at just one or two years of age and are renowned for their unique ability to communicate through rapid adaptive colouration. That is, they can change their skin patterning within milliseconds to produce different kinds of communication signals. Male cuttlefish compete aggressively for the females, which they typically outnumber four to one. The colourful contests vary in length from 30 seconds to 20 minutes. They are characteristically mediated through elaborate visual displays, which are composed of dramatic colours, body contortions, and patterns that can be changed in the blink of an eye (270 – 730 milliseconds). However, the fights can escalate to include physical aggression such as pushing, grappling, lunging, and biting.
My research team and I had the pleasure of spending countless hours underwater, observing and filming these rainbow-coloured molluscs as they engaged in these impressive contests. When males display, they do so in three distinct ways. A male may face his opponent with slowly oscillating white arms in something we term a frontal display. In a similar face-on fashion but with arms extended and rigid in a shovel-like shape, males may also engage in an appropriately termed shovel display. Lastly, in what we call a lateral display, the male’s body and the arms are side-on, whilst the male usually expresses a ‘passing cloud’ pattern – the appearance of moving dark and light clouds, which flow repeatedly over the body of the male. They achieve this by opening and closing little sacs of pigments on their skin.
Aggressive displays from left to right: frontal display, lateral display & shovel display
Classifying these behaviours was only the first step in cracking the code of aggressive cuttlefish communication. We wondered why these majestic creatures were performing so many displays? Surely they were incurring additional energy costs, so why not simply perform a single aggressive display that shouts ‘I’m angry, back off!’? One clue is that this type of repertoire is not unique to cuttlefish, as other animals as diverse as red deer and little blue penguins are known to perform multiple aggressive displays during contests. Scientists have suggested a ‘hierarchical signalling hypothesis’, which posits that the different displays communicate different degrees of aggression and the likelihood of escalation. To test whether this hypothesis applied to giant Australian cuttlefish contests, we created a cuttlefish ‘Big Brother’ at the Cronulla Fisheries Research Centre in Sydney. Our reality TV show involved exposing male cuttlefish to videos of angry male rivals and watching their reactions.
We placed a large plasma screen TV against the side of a glass aquarium and presented life-size digital footage of males performing the different aggressive displays. We also had a high-definition video camera looking down on the cuttlefish, giving us a bird’s eye view of their reactions.
After many months of analysis, we finally decoded the rules of cuttlefish fight club. Our results demonstrate that the first rule is that the frontal display is a low-risk challenge, used to assess the aggressive responsiveness of the opponent since this display is typically performed during early stages of a contest and is not correlated with physical aggression. The second rule is that the shovel and lateral displays are high-risk behaviours as they are generally followed by physical combat. The third rule of cuttlefish fight club is that males reliably advertise their aggressive intentions (i.e. they do not use false advertising) because each display was followed by a subsequent escalation to a higher aggressive behaviour. False advertising, otherwise known as bluffing, has been demonstrated in a number of other animal species, including crayfish and frogs. Even small male cuttlefish often avoid fighting through deception, by mimicking the behaviour and appearance of female cuttlefish! However, our study clearly shows that cuttlefish engaged in a contest do not bluff.
These findings support the predictions of the hierarchical signalling hypothesis. Most importantly the pattern of escalation is represented as a hierarchy of threats. The frontal display predicts the performance of the shovel and lateral displays and these latter displays predict physical combat. Performing a hierarchy of threats probably evolved so that opponents are provided with numerous opportunities to make decisions about whether to fight or flee.
Spirits are high in the research laboratory, as we have solved one of the colourful mysteries of cuttlefish communication. In our mission to decrypt these contests, we also discovered that cuttlefish share attributes of fighting behaviour similar to those found in vertebrates. This is important because as invertebrates, cuttlefish are, in terms of evolution, far removed from these vertebrate species. Finding similar patterns across diverse groups of animals suggest that there are strong selective pressures driving adversaries to use hierarchies of threats during contests. Our findings also raise the interesting possibility that, even though humans are separated from cuttlefish by 550 million years of evolution, we may not be so different after all. Leading up to a fight, we also use instinctive body language and gestures to advertise aggression, and more often than not, our fights begin over a female.
Originally published in Biosphere Magazine Issue 19.
Reference: Schnell A.K., Smith C.L., Hanlon R.T., Hall K.C. & Harcourt R. (2016) Cuttlefish perform multiple displays to communicate a hierarchy of threats. Behavioral Ecology & Sociobiology, 70: 1643 – 1655.
Alex K Schnell 