Bee-brained - Are insects ‘philosophical zombies’ with no inner life? Close attention to their behaviours and moods suggests otherwise
is professor of sensory and behavioural ecology at Queen Mary, University of London, and has been a fellow at the Institute of Advanced Study (WIKO) in Berlin. His book The Mind of the Bee (2019) is forthcoming with Princeton University Press.
was most recently Anniversary Professor of philosophy at the University of York and is now Visiting Presidential Professor at CUNY Graduate Center. She was a fellow of the Institute of Advanced Study (WIKO) in Berlin in the 2017/18 academic year. Her new book How to be an Epicurean (2019) is forthcoming with HarperCollins.
Edited by Sally Davies
René Descartes’s dog, Monsieur Grat (‘Mister Scratch’), used to accompany the 17th-century French philosopher on his ruminative walks, and was the object of his fond attention. Yet, for the most part, Descartes did not think very highly of the inner life of nonhuman animals. ‘[T]he reason why animals do not speak as we do is not that they lack the organs but that they have no thoughts,’ Descartes wrote in a letter in 1646.
Followers of Descartes have argued that consciousness is a uniquely human attribute, perhaps facilitated by language, that allows us to communicate and coordinate our memories, sensations and plans over time. On this view, versions of which persist in some quarters today, nonhuman animals are little more than clever automata with a toolkit of preprogrammed behaviours that respond to specific triggers.
Insects such as bees and ants are often held up as the epitome of the robotically mechanistic approach to animal nature. Scientists have long known that these creatures must possess a large behavioural repertoire in order to construct their elaborate homes, defend against intruders, and provision their young with food. Yet many still find it plausible to look at bees and ants as little more than ‘reflex machines’, lacking an internal representation of the world, or an ability to foresee even the immediate future. In the absence of external stimuli or internal triggers such as hunger, it’s believed that the insect’s mind is dark and its brain is switched off. Insects are close to ‘philosophical zombies’: hypothetical beings that rely entirely on routines and reflexes, without any awareness.
But perhaps the problem is not that insects lack an inner life, but that they don’t have a way to communicate it in terms we can understand. It is hard for us to prise open a window into their minds. So maybe we misdiagnose animal brains as having machine-like properties simply because we understand how machines work – whereas, to date, we have only a fragmentary and imperfect insight into how even the simplest brains process, store and retrieve information.
However, there are now many signs that consciousness-like phenomena might exist not just among humans or even great apes – but that insects might have them, too. Not all of these lines of evidence are from experiments specifically designed to explore consciousness; in fact, some have lain buried in the literature for decades, even centuries, without anyone recognising their hidden significance.
Based on such evidence, several biologists (notably Eva Jablonka in Tel Aviv and Andrew Barron in Sydney), and philosophers (Peter Godfrey-Smith in Sydney and Colin Klein in Canberra) now suggest that consciousness-like phenomena might not have evolved late in our history, as we previously thought. Rather, they could be evolutionarily ancient and have arisen in the Cambrian era, around 500 million years ago.
At its evolutionary roots, we think that consciousness is an adaptation that helped to solve the problem of how moving organisms can extract meaningful information from their sense organs. In an ever-changing and only semi-predictable environment, consciousness can solve this problem more efficiently than unconscious mechanisms possibly could. It involves manifold features, but some include: a grasp of time and space; the capacity for self-recognition; foresight; emotions; and top-down processing. As the American zoologist Donald Griffin wrote in Animal Minds (1992): ‘Environmental conditions vary so much that for an animal’s brain to have programmed specifications for optimal behaviour in all situations would require an impossibly lengthy instruction book.’Take honeybees, who have a symbolic ‘language’ by which they can communicate about the precise coordinates of food sources in flowers. In this ‘dance language’, a successful scout bee returning from a good flower patch performs a repetitive sequence of movements in the dark hive on the vertical comb. These movements are keenly attended by other bees. The successful forager moves forward in a straight line for a few centimetres. Then she moves in a half circle to the left, back to her starting point, performs another straight run along the path of her first, and then circles to the right. The duration of the straight run tells other bees the distance to the food source (roughly one second of walking distance in the dance corresponds to a one-kilometre flight to the target). The direction of this run relative to gravity encodes the direction relative to the Sun – for example, if the run in the hive is straight up, this tells other bees to fly in the direction of the Sun (whereas ‘down’ means ‘fly in the opposite direction of the Sun’).
This discovery in 1945 earned the Austrian ethologist Karl von Frisch the Nobel Prize in Physiology or Medicine; in itself, such communication neither indicates nor requires consciousness. A decade later, however, one of von Frisch’s students, Martin Lindauer, peered into a beehive during the night and discovered that some bees advertised the locations of various foraging bonanzas they’d discovered the previous day. Before midnight, they ‘talked about’ locations visited the previous evening – and in the hours before sunrise, they discussed the locations they’d visited on the morning prior.
These bees retrieved their spatial memories entirely out of context, at a time when there was no possibility of foraging and so no immediate need for communication. The function is unclear. They might have ‘just thought’ about these locations spontaneously during the night. Or perhaps the communication is a strategy for consolidating their spatial memory. Scientists have since found that a bee’s memories of the previous day are strengthened when they are exposed to elements of these memories while in deep sleep. Perhaps bees not only think and ‘talk’, but dream?
The key implication of Lindauer’s discovery is that bees are capable of ‘offline thinking’ about spatial locations, and of linking these locations to a time of day, in the absence of an external trigger. That’s not what should happen if bees’ memories are merely prompted by environmental stimuli, combined with internal triggers such as hunger. Bees, then, appear to have at least one of the principal hallmarks of consciousness: representations of time and space.
Deprived of its ability to anticipate what it should see as a result of its own intentions, the fly behaved erratically
Another elementary feature of biological consciousness is self-recognition. The ability to recognise oneself is the origin of being able to distinguish one’s self from another entity, as well as to plan, pay attention, recall memories of specific events, and take the perspective of another creature. Many animals, such as apes and corvids, display these abilities.
Without an elementary form of self-recognition, animals would not be capable of disentangling the sensory input arising from the external world from the one arising as a result of voluntary actions. If the image on your retina suddenly tilts by 45 degrees, you know that this is fine, as long as it’s the result of you deliberately inclining your head. But if you didn’t move your head, you might be in the middle of an earthquake, and had better run.
Animals are thought to tell the difference between these scenarios via what’s known as an ‘efference copy’: an internal signal that communicates the consequences of the animal’s own actions, so that they can distinguish sensory changes caused by their movements from changes caused by external forces. Under normal conditions, animals expect the environment to move in a predictable manner when they turn their heads voluntarily. This allows them to anticipate what will happen next, as a result of their own actions or intentions.
Early versions of efference copies were proposed in the 19th century, although the term was first coined by the German biologists Erich von Holst and Horst Mittelstaedt, who began studying flies. In one of their experiments in 1950, they inverted the input to the fly’s brain from the left and right eyes using a rather crude (and cruel) technique: the thin neck of the fly was twisted by 180 degrees, and its head then glued in place upside down. The result was that, when the animal turned left or right, the sensory signals were the opposite of those it expected. (They were not upside down since the experimental environment consisted of vertical stripes – so nothing changed in this regard.) Deprived of its ability to anticipate what it should see as a result of its own intentions, the fly behaved completely erratically. The authors concluded: ‘The result is clearly a central catastrophe!’ Insects, with their head in the normal position, appear to have another of the key ingredients of consciousness: the ability to predict what will happen in the future as a result of self-generated movements, which allows them to move and act effectively.
There is also evidence that insects have more than just a simple, internalised ‘instruction book’. Experimenters have tested this hypothesis by confronting insects with tasks that none of their evolutionary ancestors could have possibly encountered. More than 200 years ago, the blind Swiss naturalist François Huber (working with his wife Marie-Aimée Lullin and servant François Burnens) suggested that honeybees might display foresight in the construction of their honeycomb.
While honeybees were busy building the (normally two-dimensional) honeycomb, Huber’s team placed glass panes into the path of the construction. (Glass is a poor surface on which to attach wax.) The honeybees took corrective action long before they had reached the glass: they rotated the entire composition by 90 degrees so as to attach the comb to the nearest wooden surface. Apparently, the bees had extrapolated from their current location to the target zone, and tried to avoid a suboptimal result.
On one occasion, Huber’s team observed that one of several combs broke off the ceiling of the hive in winter. In the cold months, bees are usually in a quiescent state; comb construction stops, and the insects will reduce their activity to ensure that their food storage can last until spring. However, on this occasion, not only did bees become active to fortify the dislodged comb with a number of pillars and crossbeams made from wax, they also reinforced the attachment zones of all the other combs on the glass ceiling – apparently to ensure that a similar disaster wouldn’t happen again. Such foresight, should it be confirmed experimentally with modern methods and sample sizes, is one of the hallmarks of consciousness. Notably, in this case, it appears to extend well beyond just the immediate future.
In a recent study of tool use among bumblebees, the insects were required to transport a small ball to a defined location to receive a sugar reward. The bees used social learning to solve the task by watching skilled demonstrator bees: they observed that they could move one of three possible balls (the furthest one from the centre) into the central reward area to obtain the reward. When later tested on their own, the observer bees did not choose the furthest ball from the centre, but its closest one. They did this even when the closest ball was coloured black instead of the yellow they’d been trained on. Importantly, observers had no prior experience with rolling the balls themselves (that is, no opportunity for trial-and-error learning). These results indicated that instead of simply ‘aping’ a learned technique, bumblebees spontaneously improved on the strategy used by their instructor – suggesting that they had an appreciation of the outcome of their actions (‘ball in goal’).
Can bees not only plan, but imagine things? They can certainly learn to associate visual patterns (such as those presented on flowers) with nectar rewards; but this doesn’t necessarily imply that they have a little image of flowers floating around in their head. A 2017 study looked at artificial neural networks, modelled on bees’ brains, which deployed two simple feature detectors – that is, two kinds of neurons, each of which is especially sensitive to lines or edges that run in a particular direction. These algorithms were capable of recognising complex visual patterns, like a circle carved into four, with stripes running at different angles in each quadrant. So a bee could store these complex visual patterns just by memorising the signals from these neurons – without actually storing full images in its memory.
It transpires that bees prefer flowers whose nectar is laced with low levels of nicotine
However, a recent experiment indicates that bees might indeed be able to summon up the features of a pattern without the pattern being present. In this experiment, bees were first trained to distinguish two types of artificial flowers that were visually identical, but which had ‘invisible patterns’ made up of small scented holes that were either arranged in a circle or in a cross. The bees were able to figure out these patterns by using their feelers. The most exciting finding was that, if these patterns were suddenly made visible by the experimenter (so that the flowers now displayed visual circles or crosses), bees instantly recognised the image that was formerly just an ephemeral smell-pattern in the air. This indicates that the bees might indeed have a mental representation of the shape, rather than recognising patterns based on simple feature-detectors in their visual system.
Bees also display optimistic and pessimistic emotional states. In such tests, bees first learned that one stimulus (such as the colour blue) is linked to a sugar reward, while another (such as green) is not. They were then faced with an intermediate stimulus (in this case, turquoise). Intriguingly, they responded to this ambiguous stimulus in a ‘glass half full’, optimistic manner, if they had encountered a surprise reward (a tiny droplet of sucrose solution) on the way to the experiment. But if they had to suffer through an unexpected, adverse stimulus, they responded in a ‘glass half empty’ (pessimistic) manner.
Perhaps, then, insects don’t just have minds, but also moods. Psychotropic drugs are not just the province of humans; insects can be subject to their effects as well. Volatile anaesthetics, appetite-suppressing stimulants, depressants and hallucinogens are naturally produced by various plants and fungi. These are not only accidental byproducts of their biomolecular machinery, but for their own defence in deterring herbivores. Yet they don’t always deter: it transpires that bees prefer flowers whose nectar is laced with low levels of nicotine.
The molecular biologist Galit Shohat-Ophir at Bar Ilan University in Israel and her colleagues discovered that fruit flies stressed by being deprived of mating opportunities reportedly seek out alcohol, which is widely present in nature in the form of fermented fruits. This suggests that intentional ‘sensation adjustment’, or even ‘mood adjustment’, is widespread across the animal kingdom – which strongly suggests that animals have inner experiences. It will be important to rule out alternative explanations, in which behaviour is modified via direct effects on neurotransmission or the digestive system. But insect psychotropics should nonetheless be a promising avenue for future research. After all, why would an organism seek out mind-altering substances when there isn’t a mind to alter?
One objection to the hypothesis of insect consciousness is that their brains are simply too small. But at the time of writing, the biological watermark of consciousness – the so-called ‘neural correlate of consciousness’ (NCC) – has not been identified in humans. So humans can’t make arguments on the basis that insects don’t have human-type NCC. What we can say is that insect nervous systems are anything but simple. While a bee brain has only about 1 million nerve cells, compared with around 85 billion in a human brain, some individual neurons have a complexity of branching that rivals a fully grown oak tree. A bee brain could have a billion synapses (the connections between neurons that can be shaped by experience). In terms of the diversity of building blocks of the nervous system, even the humble fruit fly has more than 150 neuron types just in its visual system; by comparison, the human retina has fewer than 100. ‘It is indubitable that the zoologists, anatomists, and psychologists have slighted the insects,’ wrote the Nobel prizewinning neuroscientist Santiago Ramón y Cajal in his early 20th-century memoir. ‘Compared with the retina of these apparently humble representatives of life, the retina of the bird or the higher mammal appears as something coarse, rude, and deplorably elementary.’
In addition to their intricacy, insect brains also have other physiological properties required for consciousness. In a reflex machine, the flow of information would be expected to go from the sense organs to the mechanisms responsible for motor control. But in insects, there are many top-down processes at work, in which neural cables send messages from the central brain to the sensory periphery.
Such top-down processes are involved in attention-like phenomena. Attention allows animals to focus specifically on important stimuli (such as a familiar flower, if you’re a bee) and disregard others (such as unfamiliar flowers). The neuroscientist Bruno van Swinderen at the University of Queensland tested this by placing bees in a virtual reality environment that they could manipulate, and then measured their brain activity. His team found neural activity patterns that corresponded to paying attention to one or another object, and also found certain brain states that preceded the bees’ selection of one or another stimulus. Any activity generated from ‘within the brain’ – that is, in the absence of or distinct from external stimulation – is of particular interest in the context of consciousness.
The parallels between the ‘central complex’ of the insect brain and the ‘basal ganglia’ of vertebrates are striking
Significantly, van Swinderen’s team also discovered that flies have several types of brain waves, including when they are asleep. Like humans, where different neural oscillations accompany deep sleep and REM sleep, flies also have different patterns in different sleep phases. The insect brain is never ‘switched off’ – as in bees, it seems that flies also have dream-like states.
The biologist Lewis Held at Texas Tech University believes that there could be a ‘deep homology’ in apparently diverse structures across species that served common functions, such as the eye. Rather than seeing these as instances of ‘convergent evolution’, where features pop up separately, Held and others have found evidence of certain shared underlying genetic scaffolds that produce these features in their various forms. For example, we did not inherit our legs and eyes from insects, or by different modifications from a common ancestor. The common ancestor of humans and flies was an unknown legless worm of the Cambrian period. Yet both humans and flies possess a head, a thorax, an abdomen, legs, and sensory organs.
A better explanation is that we inherited the genetic modules and developmental programmes that account for these features, at least in part, from a common ancestor. This observation applies to the brain as well. The anatomical and functional parallels between the ‘central complex’ of the insect brain and the ‘basal ganglia’ of vertebrates are striking, and point to a common origin. Defects in both these systems produce motor problems, impaired memory, attention deficits, emotional disorders and sleep disturbance. According to Barron and Klein, the central complex could be a likely contender for mediating subjective experience in insects.
What about the possibility of consciousness in even simpler animals – indeed, beyond animals? In the mid-19th century, Charles Darwin wrote about not only the moral and emotional feelings of nonhuman creatures, but of their appreciation for beauty and the recruitment of that susceptibility in sexual selection. Planaria (flatworms), which do have a central nervous system, must have some form of consciousness, Darwin speculated. In The Power of Movement in Plants (1880), he went on to compare the animal brain and the plant’s ‘root radicle’ or taproot. This taproot must find its way, by some form of sampling and evaluation, to the best sources of anchorage and nourishment.
Although this proposal has been taken up recently by the biologist František Baluška at the University of Bonn, the case for plant consciousness is significantly weaker than the one for insect consciousness. While parts of plants might move, and stems can twine or lean, plants do not move their bodies as a whole. They are able to accomplish most of their tasks without needing to navigate in space, which we think is critical for the first stages of development of a distinction between self and world.
Another objection needs to be addressed before we credit too many animals, and only animals, with consciousness. This is the fact that much human behaviour depends on subconscious processing, of which we are often unaware. Our actions in the world rely to a surprising extent on stimuli we haven’t consciously noticed. Moreover, the experience of ‘volition’ has been found to follow our actions after a time-lag, rather than preceding them or being simultaneous with them. Some have interpreted this to mean that consciousness has no effect on behaviour and is purely ‘epiphenomenal’. Instead, maybe the brain collects and weighs current environmental stimuli and data from memory, computes the best behavioural option, and makes the choice for us by initiating an action. If consciousness is causally ineffective, the argument that animals need it for living is unavailable. Or perhaps what we need consciousness for is fully automated in them.
However, these arguments do not diminish the case for consciousness being widespread in the animal kingdom. Despite the wonders of unconscious processing, it’s obvious that no human being can nourish herself, escape predation, reproduce, engage in a social life or find the way to a new destination when she is not conscious of a world outside her own body. Although there are impressive examples of ‘blindsight’ – where subjects with a damaged visual cortex can make visual discriminations better than a mere ‘guess’ – the blindsighted are not totally unconscious. Of course, sleeping and damaged brains are not doing their usual job of collecting, weighing and computing. But there is no reason to think that consciousness could be ‘subtracted’ from a brain that’s doing its usual job successfully. It is the organism with a working brain and consciousness that normally faces the challenges of the world.
Consciousness is an evolutionary invention like wings or lungs. It is useful to us; it’s therefore most likely to be useful to other organisms with traits deeply homologous to ours. They share with us the difficulties of moving, probing the environment, remembering, predicting the future and coping with unforeseen challenges. If the same behavioural and cognitive criteria are applied as to much larger-brained vertebrates, then some insects are likely to qualify as conscious agents – with no less certainty than cats or Descartes’ dog.
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