The true masters of illusion and deception in the ocean

Cuttlefish are the ocean's masters of disguise, with the ability to change their colour within 50-200 milliseconds [1]. They do this with the chromatophores in their skin, these cells contain colour pigments that are controlled directly by neurons and can contract to fabricate the different patterns and colours that appear on their skin [1]. Underneath the layer of chromatophores, leucophores exist. These cells reflect all light wavelengths, allowing the cuttlefish (and other cephalopods) to camouflage by matching the colours of the light in their environment [1]. Skin pattern isn’t all these creatures change, they also change their behaviours, changing their movement patterns in the ocean to mimic other creatures. However, some cuttlefish have learnt to use this ability for their own benefit and gain.

An alternative mating strategy (AMS) refers to non-traditional methods of courting/acquiring a mate in the animal kingdom. AMS methods include: female mimicry, resource guarding and sneakers- these isopods utilise all three [2]. The use of signals can be used to attract the attention of the significant other and court them. Within the animal kingdom it is often assumed that these signals are honest; to display them can attract predators making them potentially costly. Also, in true ‘boy cried wolf’ nature, signals will be ignored if the benefits are not seen by those who choose to follow them. This shows that, for deception to function, honesty has to remain the dominant form of communication within animals [3].

Large male Giant cuttlefish attract the small female Giant cuttlefish and guard them underneath their body, to protect their newfound resource from other males who may try and steal it from them- showing the guarding part of this alternative mating strategy. Small males- previously disadvantaged in mate choice by their size- started to use another method to trick the larger males; female mimicry. By utilising their camouflage skills, these small males change their body pattern and behaviour to mimic the small female cuttlefishes. The large male cuttlefish see no threat from this female-mimicking cuttlefish and can either stop guarding or invite the female-mimicker to be guarded also. The female-mimicking cuttlefish then changes its entire shape and pattern again to signal male courtship behaviour, encouraging the females to mate with him, leaving the large male none the wiser [4]; highlighting the ‘sneaking’ part of this mission.

You’re probably thinking- but how do they get away with this? Well, these small male cuttlefishes have mastered the art of visual deception, by hiding all their sexual dimorphic features (features that make it clear they are a male). The transformation from male to female requires: fourth arms concealed, mottled skin patterning and a change in arm shape to mimic egg-laying females’ posture [5]. On top of this, these cuttlefish have poor social recognition, limiting their ability to identify female mimicry [5]. These two factors combined can lead to the disguise being too effective- as seen in one study where males tried to mate with the female-mimicking males 41 times [5], an occupational hazard! However, as previously mentioned, for this tactic to remain sustainable in a species, honesty has to remain the main method of communication- there won’t be anyone to sneak up on and deceive if everyone is doing it. Deception is risky, if it goes wrong can lead to being attacked and it may not be worth the risk if it doesn't result in reproduction. In one study, the female mimickers were successful in 30/62 cases to deceive the consort male and get near the female, and in 5 initiations of mating, one was rejected, one was interrupted by the consort male and the other three resulted in the mating, of which two out of those three resulted in offspring from the mimicking male [5]. This shows that this method does work, but isn’t used by a large percentage of the male Giant cuttlefish population.

One study by Brown et al [3] even suggests that another species of cuttlefish, known as mourning cuttlefish, are splitting their disguise in half. One half displays female mimicry behaviour to disarm to consort male and allow him to get nearer the female, while simultaneously displaying male courtship behaviour to the females with the other. This tactic seemed to only be used when the threat of punishment was low, but was still used 39% of the time by the population in the study [3]. The photo from the study, shown below, captures how definite that split across their body is. F is the female, M is the male displaying male courting skin patterns towards the female, and the deceitful mottled pattern of a female towards A, another male.

Photo from Brown et al, 2012

The use of tactical deception is commonly related to animals with a higher cognitive function as it indicates the demands on cognition that accompany social living [3]. Deception within cuttlefish, as a cognitive behaviour, can be suggested to have evolved from the complexity of social life [3]. Others argue that the need for sexual mimicry to assist with reproduction is what drove the transformation abilities in these cephalopods in the first place [4], which they now use for other purposes also, such as predator avoidance.

Overall, removing the science, these behaviours are amazing to learn about and understand. Adaptions like this feel alien- how does the body and function of these cuttlefishes evolve to do such astonishing things? Animals continue to astound me with these adaptions, something that would be a fantasy to humans, as seen with invisibility cloaks in the World of Harry Potter or shapeshifting mutants in the X-men universe. The cognitive ability involved to carry out such acts of deception, and to pull them off successfully, just feels beyond comprehension. This highlights the value of animal behaviour research to further fuel our understanding of the animal kingdom.