Animals wrestle with the concept of death and mortality | Aeon Essays

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Having a concept of death, far from being a uniquely human feat, is a fairly common trait in the animal kingdom

by Susana Monso + BIO

A grass snake feigning death in Poitou, France. Photo by Daniel Heuclin/Nature Picture Library

When the Virginia opossum feels threatened, she plays dead. Lying on the ground, curled up into something resembling the foetal position, with her eyes and mouth open and her tongue hanging out, she stops responding to the world. Her body temperature drops. Her breathing and heart rate are severely reduced. Her tongue, usually pink, takes on a blueish hue. She urinates, defecates, and expels a putrid-smelling liquid from her anal glands. To all outward appearance, she is no different from a corpse. In this deathly state, she waits. The opossum is aware of her surroundings, monitoring the present danger: a coyote in search of food. The canine, though, would rather feast on fresh meat than on some long-dead corpse, rotting and full of pathogens. And so the danger passes. Then the opossum springs back into action, unscathed and unfazed, and goes about the rest of her day. The trick worked.

Despite the persuasive performance of death, no one would assume that the opossum herself believes that she's playing dead. Her behaviour is most likely automatic, and the opossum no more knows that she's disguising as a corpse than a stick-insect knows that she looks like a stick. While this presupposition is probably right, it would nevertheless be wrong of us to assume that there's nothing to learn about animals' concept of death from the opossum's display. In fact, her little show is one of the best pieces of evidence we have of how widely distributed in nature the concept of death is likely to be.

Photo by iStock/Getty

Humans have long thought of themselves as the only animal with a notion of mortality. Our concept of death is one of those characteristics, like culture, rationality, language or morality, that have traditionally been taken as definitional of the human species - setting us apart from the natural world and justifying our boundless use and exploitation of it. However, as I have argued elsewhere, the widespread notion that only humans can understand death stems from an overly complex view of this concept. The human concept of death is not necessarily the only concept of death.

Understanding death does not require grasping its inevitability or its unpredictability, nor does it require understanding that death applies to all living things or being familiar with its underlying physiological causes. In minimal terms, the concept of death is simply made up of two notions: non-functionality and irreversibility. This means that all an animal needs to grasp in order for us to be able to credit her with some understanding of death is that dead individuals don't do the sorts of things that living beings of her kind usually do (ie, non-functionality) and that this is a permanent state (ie, irreversibility). This minimal concept of death requires very little cognitive complexity and is likely to be very widespread in the animal kingdom.

The opossum's death display, also known as thanatosis , is an excellent demonstration of this, not because of what it tells us about the opossum's mind, but because of what it shows us about the minds of her predators: animals such as coyotes, racoons, dogs, foxes, raptors, bobcats and large snakes. In the same way that the appearance of the stick insect tells us something about how her predators see the world, and which sorts of objects they avoid eating, the opossum's thanatosis reveals how common the concept of death is likely to be among the animals that feed on her.

The main reason why thanatosis is such a good piece of evidence of predators' concept of death has to do with the particular complexity exhibited by this behaviour. In order to see this, we need to begin by distinguishing thanatosis from a similar - and probably evolutionarily related - behaviour. Many animals, when they feel threatened, go into a kind of paralysis that reduces the probability of being preyed upon. This is known as tonic immobility and can be found in a wide range of species, from insects to humans. While tonic immobility is a simple behaviour that operates at a superficial level - in some species it can even be accompanied by an increase in heart rate - in thanatosis, the animal not only stays still but actively imitates the characteristics of a corpse. Although thanatosis might have evolved from tonic immobility, it's much more than a mere paralysis: the animal is feigning death.

The Virginia opossum is probably the animal with the most elaborate thanatosis display (hence the expression 'to play possum'), but not the only one to exhibit a behaviour deserving this label. Some frogs engage in thanatosis, whereby they stop responding to all interactions while lying still, with their eyes open and their limbs extended and flaccid. Their tongue might also hang from their mouth, and their breath will give off an ammonia-like smell. Hognose snakes precede their thanatosis display with a dramatic 'death', during which the animal writhes in an erratic and violent manner until she finally lies still with her belly facing up, her mouth open, her tongue hanging out, displaying no signs of breathing. She even secretes blood from her mouth. You could poke her with a stick or lift her up and she would not react.

Both tonic immobility and thanatosis are defence mechanisms that protect prey from predators. However, they are distinct, and not just because tonic immobility is so much simpler, but because it tends to act against the predator in a different way. To see this, consider how these two mechanisms operate at different stages of the hunt. We can distinguish four stages in predation: (1) the detection of the prey; (2) the recognition of the prey as adequate; (3) the subjugation of the prey; and (4) the consumption of the prey. While tonic immobility would operate mainly at stages (1) and (4) - detection and consumption - thanatosis operates at stages (2) and (3) - recognition and subjugation.

An unexpectedly expansive grasshopper will likely get spit out - and might even wound the frog in the process

Tonic immobility functions, firstly, as an anti-detection mechanism . By becoming still, the prey can blend in with the environment and go unnoticed, especially if her appearance favours camouflage. Some predators also respond only to movement, so tonic immobility works by eliminating a key stimulus that would attract the predator's attention. And if the prospective prey lives in a social group, keeping still helps in a different way: it becomes much more likely that a fellow member of the group will be the unlucky one to catch the predator's eye.

Tonic immobility can also function as an anti-consumption mechanism . For instance, in some toxic species of frog, tonic immobility consists of folding up the limbs against the body, thus reducing the animal's size. This way, the frog protects herself from being hurt when she is consumed and makes it more likely that the predator will spit her out whole after having swallowed her and verified that she's not fit for eating. Frogs can also be on the losing end of tonic immobility. Some grasshoppers, for instance, will adopt a very rigid posture with their limbs extended, making themselves bigger rather than smaller. Since frogs swallow insects whole (rather than chewing them), an unexpectedly expansive grasshopper will likely get spit out - and might even wound the frog in the process.

While tonic immobility has clear defence functions, when it comes to thanatosis, biologists can't agree on its concrete advantages and the reasons why it would have been favoured by natural selection. Why would an animal who wants to avoid being eaten pretend that she's already dead? The problem is that thanatosis is unusually complex behaviour and must be distinguished from simple tonic immobility, since it's very costly. That is, there has to be a good evolutionary reason for animals to develop thanatosis above and beyond tonic immobility. There are several hypotheses, but all postulate thanatosis as either an anti-recognition or an anti-subjugation mechanism. For our purposes, regardless of which hypothesis is true, all we need is to postulate a concept of death in the deceived predators in order to successfully explain the evolutionary emergence of thanatosis. Let's go through these hypotheses.

Thanatosis as an anti-recognition mechanism works by making the prey appear unpalatable to the predator. In principle, this could ride on a simple disgust mechanism, since thanatosis is often accompanied by urination and defecation, or by other chemical defences, such as the frogs' ammonia-like breath, which the predator might find yucky. According to this interpretation, the success of thanatosis would not involve the predator conceptualising anything about the prey's corpse-like appearance. Instead, the animal in thanatosis would just appear disgusting.

Though thanatosis can sometimes work this way, it's implausible as the sole explanation for why it evolved. There are many ways of exploiting the predator's capacity to feel disgust through mechanisms that are simpler and far less costly than a full-blown thanatosis display, such as the skunk's spray. If thanatosis aims only to exploit the predator's disgust, then it's difficult to explain why it's so complex. The opossum could generate disgust simply through the foul-smelling liquid that she releases from her anal glands. Why the need, then, to stay still, reduce her vital functions, display a blue tongue, and so forth? The opossum's thanatosis doesn't appear to be for generating disgust, but for generating the appearance of being dead.

It's true that many, if not most, animals come with a hard-wired tendency towards necrophobia , which is a stereotypical aversion to corpses that is not mediated by a concept of death. This means that most animals are disgusted by the smell or the appearance of corpses, even if they do not understand what a corpse is . This unlearned aversion serves an important protective function for the organism, since dead bodies are a paradise for pathogens. Could it be the case, then, that thanatosis works by activating the predators' necrophobia? This would again mean that it would not give us any evidence of the predators' possession of a concept of death, since it would simply exploit predators' non-conceptual and innate aversion to corpses.

This, too, is not convincing as an explanation of the full complexity of this behaviour. Necrophobia is usually linked to concrete sensory stimuli, such as cadaverine or putrescine (two chemical components given off by rotting corpses). An animal usually needs only to perceive these stimuli for necrophobia to kick in. In humans, the smell of putrescine alone is enough to trigger our fight-or-flight mechanisms. So, prey looking to exploit predators' necrophobia need only display some of these concrete sensory stimuli, which would again make the majority of the characteristics that make up thanatosis displays irrelevant, especially those that have to do with a reduction of vital functions.

The complexity of thanatosis, and its clear resemblance to the characteristics of corpses, therefore makes it unlikely that no cognitive processing of the prey's corpse-like appearance on behalf of the predator plays a role. If thanatosis evolved to exploit predators' necrophobia, it is probably a necrophobia that is mediated or supported by a concept of death. The opossum's trick would work not just because she looks disgusting, but because she looks disgusting because she appears dead (and the predator has learned that dead prey taste bad or upset the stomach). In such a case, the predator's concept of death would be involved in the success of the mechanism.

The concept of death in the predator is needed to account for the complexity of the behaviour in the prey

Some have postulated that thanatosis works not as an anti-recognition mechanism, but as an anti-subjugation mechanism that prevents the predator from actually killing the animal. The idea is that thanatosis makes the predator believe that the prey has already died, therefore relaxing the predator's attention and giving the prey a chance of escaping. Some predators treat their prey relatively gently or might release them for some minutes before consuming them, especially if they're trying to kill more than a single animal in one go. Others will cache their prey for some time after having killed them. So perhaps feigning death can allow an animal to escape unharmed in such situations.

Like other hypotheses, however, these have the difficulty of explaining the complexity of thanatosis, since it would suffice for an animal to stay still and flaccid - that is, in tonic immobility - for the predator to mistake her for dead. However, all the additional aspects of thanatosis point to the fact that these displays are aimed at exploiting the predators' minimal concept of death - non-functionality and irreversibility. Stillness, reduction of physiological functions, lack of reactions, and similar behaviours generate the illusion of an absence of the vital functions of the organism (non-functionality), while blood secretions, smell of rot, blue tongue, and other signs aim to imply that this loss of functionality cannot be reversed, unlike that which we might find in an asleep or unconscious individual (irreversibility). Regardless of whether thanatosis works as anti-recognition or anti-subjugation, the concept of death in the predator is needed to account for the complexity of the behaviour in the prey.

Moreover, the fact that an animal in tonic immobility can also be taken for dead supports the argument that thanatosis exploits predators' concept of death if we think about the evolutionary relationship between tonic immobility and thanatosis. It's quite likely that tonic immobility functions on occasion as an anti-subjugation mechanism, for the animals displaying it often resemble a fresh corpse. It's perfectly plausible to imagine that thanatosis would then have evolved from this behaviour, taking advantage of the fact that predators can sometimes mistake an animal in tonic immobility for a dead one. Opossums and the rest would have specialised throughout their evolutionary history in perfecting this corpse-like look that would increase the chances of their predators making this mistake.

Despite all this, it would be fallacious to assume that we need to find a unique hypothesis that can explain thanatosis in all its complexity. It's likely that there is more than one reason that explains its evolution, in the same way as it's possible for a single animal to benefit from thanatosis as an anti-recognition mechanism on some occasions and as an anti-subjugation one on others. In fact, it has been postulated that thanatosis might even work simply because predators panic upon seeing ambiguous signs of life and death in the prey, opting to leave the bizarre thing alone. Thanatosis would work here in a way akin to other defence mechanisms that function by scaring or startling the predator, such as sudden changes in shape or colour. But again, even this presupposes that the predator interprets the thanatosis display as offering signs of death.

My point is not to settle the question of the concrete reasons why natural selection has favoured the evolution of thanatosis as a defence mechanism. What I want to argue is that, if thanatosis has evolved, it's because there are some advantages - regardless of the concrete form they take - to appearing specifically as though one were dead . What is there in common to lying belly-up completely still, not responding to interactions, with eyes and mouth wide open, while secreting blood and defecating? What is there in common to having a blue tongue, smelling rotten, being cold and not exhibiting signs of breathing? The only possible explanation to why these characteristics occur together as part of the same behaviour is that the animals are feigning death.

This does not mean that opossums themselves necessarily have a concept of death, or that they behave this way with the intention of being mistaken for a corpse. On the contrary, it appears to be a genetically inherited behaviour that does not require any learning and that is triggered automatically upon the detection of certain stimuli. What this does mean, however, is that the predators' concept of death was the likely selection pressure that shaped these displays. Maybe opossums lack a concept of death, but we can be pretty sure that the animals who intended to feed on them throughout their evolutionary history did tend to have one.

Behind many of the behaviours that animals exhibit there is at least one selection pressure, which is what has favoured their evolution. Occasionally, these selection pressures have to do with how these animals' predators conceive their world, for this will determine the chances that a prey has of surviving long enough to pass on her genes. Stick insects don't need a concept of 'stick', nor an intention to look like one. However, if insects with this appearance have evolved, it's due to the fact that their predators believed that they were sticks and did not want to eat sticks. Throughout their evolutionary history, the ancestors of these insects who looked more like sticks would have fewer chances of being eaten by a predator, and thus more chances of reproducing, which in turn would favour that successive generations would appear more and more like sticks.

The Batesian mimicry that we see in some flies, in which they exhibit the yellow and black stripes characteristic of toxic species such as bees and wasps, despite themselves being non-toxic, is an indication of the associations that predators are capable of forming. These flies don't need the intention of looking like a wasp for their appearance to be beneficial. It's enough for their predators to have the capacity to form an association between the ideas yellow-and-black-stripes and tastes-bad . This capacity for association was the selection pressure that favoured the evolution of the flies' appearance.

The Kentish plover pretends to have a broken wing to lure predators away from her nest

Regardless of the concrete evolutionary history that gave rise to thanatosis, this behaviour provides us with a window into the minds of predators. Thanatosis shows us that, for whatever reason, predators are less likely to eat animals that they themselves conceive as dead. Throughout their evolutionary history, those opossums who were better capable of imitating a corpse, and thus of fooling predators into thinking they were dead, would have higher chances of surviving until reproduction, thus favouring higher levels of sophistication and complexity in this behaviour in successive generations. Any explanation of the defence function of thanatosis must necessarily incorporate the concept of death.

There are independent reasons beyond thanatosis for thinking that many predators are good candidates for having a concept of death. They have a strong emotional incentive to pay attention to the moment a prey dies, insofar as dead prey represents food, and live prey represents a danger (since many animals are equipped with sharp horns or hooves, or will respond aggressively to predation attempts). Predators who make it to maturity will also accumulate hundreds, if not thousands, of experiences with death and will have daily opportunities to learn about the irreversible non-functionality that characterises it. Lastly, many large predators are cognitively complex and equipped with both a tendency and an incentive to monitor the functionality of their prey, in order to target those animals that are old, sick, young, disabled or show any other signs of partial non-functionality. Some prey animals exploit this tendency to their advantage. The Kentish plover, for instance, engages in a display where she pretends to have a broken wing in order to attract the attention of predators and lure them away from her nest.

That thanatosis is indicative of a concept of death in predators is further supported by the fact that this defence is unlikely to work against specialised predators, for these would have evolved an appropriate response. Instead, we expect it to work against generalist predators who don't encounter this prey too often and are not familiar with their little trick. For it to work against generalist predators, they have to have a concept of death, that is, not just the capacity to react to certain stimuli that are associated with death, but a concept that can be applied to different species. Only with a concept can a predator mistake for dead an animal that she has never encountered before.

The distribution of thanatosis in the animal kingdom points to how extended the concept of death is likely to be in nature. We find elaborate forms of thanatosis in some species of amphibians, reptiles, birds and mammals. Its widely extended yet patchy presence in the phylogenetic tree suggests that thanatosis appeared in these different species through convergent evolution. These are species that are not closely related, so they would not have inherited their thanatosis from a common ancestor, but, rather, the presence of similar selection pressures in their different habitats would have made this behaviour appear independently in these different taxa. The concept of death, far from being a uniquely human feat, is a fairly common trait in the animal kingdom.

We humans like to think of ourselves as a unique species. However, little by little, all those traits that we have been relying on to ground this uniqueness have been falling, as the science advances and reveals the staggering diversity and complexity of animal minds and behaviour. We now have solid evidence of culture, morality, rationality, and even rudimentary forms of linguistic communication. The concept of death should also be counted among those characteristics to which we can no longer resort to convince us of how very special we are. It is time to rethink human exceptionalism, and the disrespect for the natural world that comes with it.

Animals and humansPhilosophy of mindEvolution 14 September 2021 Syndicate this Essay