Image copyright Carin Bondar, ‘The Nature of Human Nature’. Illustration by Brian Krumm and Chris Hall.

Halloween is a time to celebrate the power of disguise. Wherever your travels take you today it won’t be surprising if you bump into a few zombies, vampires or witches on your way. Humans love to dress up in silly costumes and disguises, and Halloween is the perfect time for many of us to take on our alter egos for a little while – to play the trickster and be a little deceptive. In the animal kingdom the story is much different. The powers of disguise are an important part of everyday life for both predators and prey. Such natural ‘tricksters’ are engaged complex social battles, deception is commonplace and there are serious consequences to biological fitness for individuals that fall victim to such schemes. Outwitting your opponent can be an extremely important aspect of survival, for both the tricksters and their victims.

Blue striped cleaner wrasse.

Cleaning stations are areas on coral reefs where specific types of fish will perform the task of removing parasites or other detritus from client fish. The system works quite well and is mutually beneficial: the cleaners (for example the bluestreak cleaner fish Labroides dimidiatus) get easy meals that come right to their doorstep, and the clients (a wide variety of reef fish) are able to rid themselves of troublesome parasites or have their surface abrasions attended to.

However, such a happy little arrangement does not come without its dangers in the form of trickery. Aggressive mimics are defined as organisms that resemble a non-threatening or attractive organism for the purpose of gaining benefits [1]. Bluestriped fang blennies (Plagiotremus rhinorhynchus) are aggressive mimics of juvenile bluestreak cleaner fish. Instead of removing parasites from client fish as a normal cleaner would do, the fang blennies remove a chunk of flesh! Since they are ‘disguised’ as cleaner fish, they are able to trick their prey into coming right over to them before launching their attacks. All is not lost for the client fish however; researchers studying this phenomenon note that the mimic attacks become less successful over time, as the client fish are able to learn to avoid both the mimics and the areas in which they work [1]. Cleaning stations are plentiful in a coral reef, and stations that have aggressive mimics present have been shown to receive fewer visitors than those who do not [2]. The trick, as with any kind of behavior, is that moderation is key. Once there are too many mimics out there those that are subject to their advances become wary and suspecting.

Predators aren’t the only ones that resort to trickery in order to gain an advantage. Biologists assume that selection pressure is actually greater on prey species than it is on predators because prey species have much more to lose. The ‘life-dinner’ principle [3] describes how the situation differs between predators and prey. Predators may have to skip a meal if their disguise doesn’t work, but prey may lose their lives, which provides a whole lot of (evolutionary) incentive to make sure you can outwit your opponents!

California ground squirrels (Spermophilus beecheyi) have been preyed upon by Northern Pacific rattlesnakes (Crotalus oreganus) for millions of years. The squirrels have evolved a unique method of disguising themselves from their main predators: by ‘dressing up’ like them! The squirrels masquerade as rattlesnakes by chewing on shed snakeskins and vigorously licking the scent onto their own bodies4. By covering themselves in ‘eau de rattlesnake’, the squirrels mask their own natural scent, thus disguising themselves from their foremost predator. Rattlesnakes are more attracted to the pure scent of the ground squirrel than they are to the scent of ground squirrel mixed with rattlesnake [3], demonstrating the effectiveness of this technique.

Tricksters are abundant in all societies, and ours are no exception. Tricks can be designed to gain resources in a dishonest way (e.g. the disguised predator) or they can be used to protect resources by fooling those that are interested in taking them (e.g. the disguised prey). Luckily for the Homo sapiens, those that are trying to trick us are generally doing so in order to have a Halloween laugh than to eat us for dinner. For most other organisms in the animal kingdom, the stakes of such trickery are much higher. Selection pressure on organisms whose lives are on the line (i.e. prey) has resulted in a myriad of strategies that serve the sole purpose of ensuring the survival of those undertaking them. Keeping up with the tricks of their prey, predators have also developed a variety of ways in which to detect disguises or to wear disguises of their own…the beauty of evolution. Although it strikes me that this is anything but beauty really… how disconcerting that so much energy is spent on evolution of the perfect trickster!

References:

[1] Cheney, K.L. 2008. The role of avoidance learning in an aggressive mimicry system. Behavioral Ecology 19: 583-588.

[2] Cote, I.M. 2004. Distance-dependent costs and benefits of aggressive mimicry in a cleaning symbiosis. Proceedings of the Royal Society of London, B Biological Sciences. 271: 2627-2630.

[3] Dawkins, R. and Krebs, J.R. 1979. Arms races between and within species. Proceedings of the Royal Society of London, B Biology. 205: 489-511.

[4] Clucas, B., Owings, D.H. and Rowe, M.P. 2008. Donning your enemy’s cloak: ground squirrels exploit rattlesnake scent to reduce predation risk. Proceedings of the Royal Society of London, B Biological Sciences 275: 847-852.

This post is adapted from an essay in Dr. Bondar’s book ‘The Nature of Human Nature’.