Expanding Consciousness

Bees and other insects show signs of possessing complex self-awareness, but if the scope of consciousness is widened, where will it end?

Lars Chittka and Catherine Wilson

onsciousness is a state of close to the notion of philosophical ous evening, and in the hours before awareness that allows us to zombies—hypothetical robots that be- sunrise, they communicated locations close our eyes and picture have overtly like normal humans, but visited on the former morning. our childhood home, or to are entirely based on preprogrammed These bees retrieved their spatial Cperform the sort of planning, predic- behavior routines and reflexes, with- memories entirely out of context, at a tion and risk assessment required to out any self-awareness. time at which there was no possibil- gauge whether it’s safe to jump over But there are now many indications ity of foraging and no need for com- a stream of a given width. It allows us that insects exhibit consciousness-like munication. The function is unclear— to solve problems by thinking, rather phenomena. Some lines of evidence are they may have spontaneously thought than simply by trial and error. from experiments that have lain bur- about these spatial locations during For centuries, scholars such as René ied in the literature for decades, even the night, or perhaps this communica- Descartes (1596–1650) have argued centuries, without anyone recognizing tion functioned as a strategy for spatial that consciousness is a uniquely hu- their significance for consciousness. memory consolidation. Later studies man attribute, perhaps facilitated by Honeybees, for example, have have shown that a bee’s memories of language, that allows us to communi- a symbolic language by which they the previous day become strengthened cate about our memories and feelings, communicate about the precise coordi- when they are exposed to elements of and to coordinate plans for the future. nates of floral food sources or potential these memories while they are deeply In this view, nonhuman animals were nest sites (see “Group Decision Making asleep. Perhaps bees dream about the regarded as merely cleverly-designed In Honey Bee Swarms,” May–June 2006). experiences of the previous day? automatons with a toolkit of pre­ In this dance language, a scout bee re- The key implication in Lindauer’s programmed behaviors, each triggered turning from a flower patch performs discovery is that bees are capable of by certain environmental stimuli. a repetitive sequence of movements offline thinking about spatial locations Social insects such as bees and ants in the dark hive on the vertical comb. (and the ways in which the locations seemed to epitomize this viewpoint. These movements are keenly attended are linked to time), in the complete Scientists knew that a large behavioral by other bees. The successful forager absence of any external trigger—a repertoire is required to construct their moves forward in a straight line for conclusion which does not align with elaborate homes, defend them against a few centimeters, then a half circle the assumption that bees are zombies. intruders, provision their young with to the left back to her starting point. Bees, then, appear to have at least some adequate nutrition—but it seemed She performs another straight run, and of the principal hallmarks of conscious- plausible that these animals were then circles to the right. The duration ness: representations of time and space. nonetheless “reflex machines” without of the straight run tells other bees the internal representation of the world or distance to the food source (roughly The Evolution of Consciousness an ability to foresee even the immedi- one second of walking distance in the Based on such evidence, many biolo- ate future. In this view, insects were dance corresponds to a one-kilometer gists and philosophers now suspect flight to the target). The direction of that consciousness-like phenomena Lars Chittka is professor of sensory and behavioral this run relative to gravity encodes the might be evolutionarily ancient, per- ecology at Queen Mary University of London and direction relative to the Sun—for ex- haps dating back to the Cambrian Pe- the author of the forthcoming book The Mind of ample, if the run in the hive is straight riod (approximately 500 million years the Bee (2020). Catherine Wilson was most re- up, this tells other bees to fly in the ago). This line of inquiry might seem cently Anniversary Professor of Philosophy at the direction of the Sun. like a slippery slope. Where should we University of York and is now Visiting Presiden- Karl von Frisch made this discovery draw the line? Do plants have some tial Professor at the City University of New York in 1945, for which he was later award- form of awareness? Or, as panpsychists Graduate Center. Her recent book The Pleasure ed the Nobel Prize in Physiology or would argue, do electrons, rocks, com- Principle (2019) discusses, among other topics, Medicine. A decade later, one of his the evolution of the mind. Chittka and Wilson met puters, or the universe have anything when they were both fellows of the Berlin Institute students, Martin Lindauer, peered into of the sort? If so, we are at risk of ex- of Advanced Study, and their discussions laid the a beehive and discovered that some panding the definition of conscious- foundations for the thoughts presented here. This bees continued these discussions into ness to include ever more living and article is an adaptation of an essay previously pub- the night. Before midnight, they “talk- nonliving beings until the term be- lished in Aeon, aeon.co. Email: TK ed about” locations visited the previ- comes meaningless.

364 American Scientist, Volume 107 Helga Heilmann The construction of honeycombs by Apis mellifera requires the coordinated and cooperative were the opposite of those it expected. activities of many dozens of individuals. Workers manufacture and manipulate wax into a Deprived of its ability to anticipate highly regular hexagonal pattern. In the process, they evaluate the space available and the cur- what it should see as a result of its own rent state of construction, and incorporate a diversity of communication signals from others. intentions, the fly behaved erratically. These rich instinctual repertoires had been thought to come at the expense of learning capac- Insects, with their heads in the normal ity; however, very few behavioral routines are fully hardwired, and even comb construction position, appear to have another of the skills have to be partially learned by honeybees. key ingredients of consciousness: the ability to predict what will happen in Solid proof of consciousness in any- actions, so that they can distinguish the future as a result of self-generated one except oneself is of course unat- sensory changes caused by their movements, which allows them to tainable. Everyone else may be a ma- movements from changes caused by move and act effectively. chine or a zombie. But then—say some external forces. Under normal condi- At its evolutionary roots, we believe philosophers—we may be brains in tions, animals expect the environment that consciousness is an adaptation vats, as in the movie The Matrix. to move in a predictable manner when that helped to solve the problem of One elementary phenomenon at the they turn their heads voluntarily. This how moving organisms can extract heart of biological consciousness is expectation allows them to anticipate meaningful information from their self-recognition: the ability to recognize what will happen next, as a result of sense organs. In an ever-changing and oneself as distinct from another entity, their own actions or intentions. only semi-predictable environment, as well as to plan, pay attention, recall Early versions of efference copies consciousness can solve this problem memories of specific events, and take were proposed in the 19th century, more efficiently than unconscious the perspective of another creature. If although the term was first coined mechanisms possibly could. As the the image on your retina suddenly tilts by the German biologists Erich von late zoologist Donald Griffin wrote in by 45 degrees, you know that this is Holst and Horst Mittelstaedt in their his book Animal Minds (1992), “Envi- fine if it’s the result of deliberately in- study of flies. In one of their experi- ronmental conditions vary so much clining your head—If not, you may be ments in 1950, they inverted the in- that for an animal’s brain to have pro- witnessing a major seismic event, and put to the fly’s brain from the left and grammed specifications for optimal you had better run. right eyes using a rather crude (and behavior in all situations would re- Animals are thought to tell the dif- cruel) technique: The thin neck of the quire an impossibly lengthy instruc- ference between these scenarios via fly was twisted by 180 degrees, and its tion book.” what’s known as an efference copy: an head then glued in place upside down. Bees provide further evidence that internal signal that communicates the The result was that, when the animal insects can cope with unusual chal- consequences of the animal’s own turned left or right, the sensory signals lenges that no instruction book will an- www.americanscientist.org 2019 November–December 365 zone and foreseen a suboptimal result before it occurred. On another occasion, Huber’s team created an environment where the bees had no choice but to build their hive on a glass surface. The research- ers observed that one of several combs broke off the ceiling of a hive during winter. Hive construction normally pauses during the winter months when the bees minimize their activity to ensure that their stores lasts until spring. However, on this occasion, not only did the bees become active to for- tify the dislodged comb with a number of pillars and cross-beams made from wax, but they also reinforced the at- tachment zones of all the other combs on the glass ceiling, apparently to en- sure that the problem would not recur. Such foresight, should it be confirmed experimentally with modern methods and sample sizes, is one of the hall- marks of consciousness, and in this case already extends beyond foresee- Lars Chittka ing just the immediate future. The bumblebee on this thistle flower wears a radar transponder, which allows researchers to track its whereabouts for its entire lifetime. The transponder is only 15 milligrams (a bee can The Inner Lives of Bees typically carry over 100 milligrams of nectar) and has not been shown to affect normal flight or behavior. One of us was part of a 2017 study of tool use among bumblebees where ticipate. More than 200 years ago, the structing a hive. Glass is a suboptimal the insects were required to transport Swiss naturalist François Huber (1750– surface to which to attach wax, so bees a small ball to a defined location in 1831) suggested that honeybees might took corrective action long before they order to receive a sugar reward. Ob- display foresight in the construction had reached the slippery surface: They server bees learned how to solve the of their honeycomb. Working with his turned the entire construction 90 de- task through social demonstration wife Marie-Aimée Lullin and servant grees to attach the comb to the nearest by skilled bees. When later tested on François Burnens, Huber conducted wooden surface. Apparently, the bees their own, the observer bees improved an experiment where they placed glass had extrapolated from the direction of upon the technique of the demonstra- panes into the path of honeybees con- their current construction to the target tors, choosing a ball closer to the cen- ter. They did this even when the clos- est ball was colored black instead of the trained yellow. Importantly, rolling a ball is not a behavior that bees per- form in nature. The observers had no prior experience with rolling the balls themselves, and thus had no opportu- nity for trial-and-error learning. These results indicated that instead of “ap- ing” a learned technique, bumblebees spontaneously improved upon the strategy used by the demonstrators, suggesting they had an appreciation of the outcome of their actions. Can bees not only plan, but imag- ine? They can certainly learn to as- sociate visual patterns (such as those presented on flowers) with nectar re-

The bee in the center of this image is com- municating to the others through a dance language. Its movements can convey infor- mation such as the direction and distance to a particularly good flower patch. Warren Photographic

366 American Scientist, Volume 107 wards, but this does not necessarily imply that they have an image of such flowers floating around in their heads. In fact, neural network analyses show that even complex visual patterns (that consist, for example, of differently ori- ented stripes in all four quadrants of the pattern) can be recognized with just two simple feature detectors that sample information across the visual field—without the need to store the actual image in the bee’s memory. But an experiment one of us pub- lished in 2018 indicates that bees might indeed be able to picture the spatial ar- rangements of features in a pattern. 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 ar- ranged either in a circle or in a cross. The bees were able to figure out these patterns by using their feelers. But 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 cross- es), bees instantly recognized the image that formerly was just an ephemeral pattern in the air. This indicates that the bees might indeed have a mental representation of the shape, rather than Vincent Gallo recognizing patterns based on simple This computer-generated image recreates Swiss entomologist François Huber’s experiments feature-detectors in their visual system. to probe honeybees’ flexibility in comb construction. When faced with a space that had a glass Bees also display optimistic and ceiling and floor, the bees began their construction on one of the side walls (a). If a glass pane pessimistic emotional states, at least was placed over one of the walls before the comb reached it, the bees introduced a curve that when their behavior is evaluated by revised the direction of the hive to a more suitable target area for attachment (b). the same criteria by which domes- tic animals are commonly assessed. sants, and hallucinogens are naturally which behavior is modified via direct In such tests, bees first learned that produced by plants and fungi. These effects on neurotransmission or the di- one stimulus (such as the color blue) chemicals are not only accidental by- gestive system, but it is nonetheless is linked to a sugar reward, while products of their biomolecular ma- be a promising avenue for future re- another (such as green) is not. They chinery, but also are for their own de- search. Why would an organism seek were then faced with an intermediate fense in deterring herbivores. But they out mind-altering substances when stimulus (in this example, turquoise). do not always deter: Bees, for example, there isn’t a mind to alter? Fascinatingly, they responded to this prefer flowers whose nectar is laced ambiguous stimulus in a “glass half with low levels of nicotine. Physiological Ties to Consciousness full” (optimistic) manner, if they had Alcohol is widely present in nature One objection to the hypothesis of in- encountered a surprise reward (a tiny in the form of fermented fruits. Mo- sect consciousness is that their brains droplet of sucrose solution) on the way lecular biologist Galit Shohat-Ophir of are simply too small. But at the time of to the experiment. If an adverse stimu- Bar-Ilan University in Israel and her writing, the much-sought-after neural lus is unexpectedly experienced, they colleagues discovered that fruit flies correlate of consciousness (NCC) has not respond in a “glass half empty” (pes- stressed by being deprived of mating been identified in humans; thus one simistic) manner. opportunities seek out alcohol. This cannot argue that certain animals don’t Further evidence that qualitative activity suggests that intentional sen- have human-type NCC. What we can experience is available to a range of sation adjustment or even mood adjust- say is that insect nervous systems are animals is furnished by consideration ment, as well as involuntary suscepti- anything but simple: Although a bee of mind- or mood-altering drugs. Not bility to psychotropics, is widespread brain has only about 1 million nerve only mammals (think of the effects across the animal kingdom—which cells (compared to around 80 billion of catnip), but some insects indulge strongly implies that animals have in- in a human brain), some individual in them. Volatile anesthetics, appe- ner experiences. It will be important neurons have a complexity of branch- tite suppressing stimulants, depres- to rule out alternative explanations, in ing that rivals a fully grown oak tree. A www.americanscientist.org 2019 November–December 367 flow of information would be expect- thus there may be dreamlike states in ed to go from the sense organs to the both flies and bees. mechanisms responsible for motor Neuroscientists Tzvetan Popov and control. But in insects, there are many Paul Szyszka from the University of top-down processes at work, in which Konstanz in Germany recently discov- neural cables send messages from the ered that honeybees have the kinds of central brain to the sensory periphery. neural oscillations synchronized across Such top-down processes are in- the brain that, at least in humans, are volved in attention-like phenomena. associated with conscious states. Al- Attention allows animals to focus spe- though neural oscillations alone do cifically on important stimuli (such as a not create consciousness, it is widely flower known to have plentiful nectar, agreed that certain types of such os- if you’re a bee) and disregard others cillations are a key ingredient of con- (flowers with less nectar). The neurosci- scious states. And nervous systems entist Bruno van Swinderen at the Uni- would have generated some form of versity of Queensland in Australia has oscillations right from the start of ani- discovered specific neural signatures of mal evolution because they are key attentive states in insects. He also found to the rhythmic muscle contractions evidence that a bee knows what visual that form the basis of locomotion. Dur- stimuli to expect next, thereby demon- ing later evolutionary elaboration of Lars Chittka strating that its neural activity is not nervous systems, brains might have Marking bees with number tags allows re- simply generated as a result of stimuli coopted such pre-existing neural pace- searchers to track individual bees, which “trickling down” from the sense organs makers to generate spontaneous activ- reveals differences in their behaviors. For to the central brain. Any activity gener- ity from within the brain, ultimately example, some individuals work throughout the day, whereas others visit flowers only in ated from “within the brain” (meaning leading to phenomena such as con- the morning or afternoon. Certain individu- in the absence of external stimulation) scious thought. als even innovate novel solutions to nectar is of particular interest in the context of The anatomical and functional par- harvesting, while some simply copy other consciousness. allels between the central complex of bees’ flower exploitation methods. Significantly, van Swinderen also the insect brain and the basal ganglia discovered that flies’ brains have sev- of vertebrates are striking and point bee brain has about 1 billion synapses eral types of neural signal oscillations, to a common genetic origin. Defects (connections between neural wires including when they are asleep. As in in both these systems produce motor that can be shaped by experience). humans, where different oscillations problems, impaired memory, attention In addition to their intricacy, insect accompany deep sleep and REM sleep, deficits, emotional disorders, and sleep brains also have other physiological flies have different patterns of oscil- disturbance. According to biologist properties required for consciousness. lations in various sleep phases. The Andrew Barron of Macquarie Univer- If they operated solely by reflex, the insect brain is never ”switched off”— sity in Australia and philosopher Colin Klein of the Australian National Uni- versity, the central complex is a likely contender for mediating subjective ex- perience in insects.

Limits of Universal Consciousness What about the possibility of conscious- ness in even simpler animals, and in- deed beyond animals? In the mid-19th century, Charles Darwin wrote about not only the moral and emotional feel- ings of animals but also their appre- ciation of beauty and the recruitment of that susceptibility in sexual selection. He speculated that because Planaria (flatworms) have a central nervous sys- tem, they must have some form of con- sciousness. 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 Iida Loukola find its way, by some form of sampling This bumblebee has learned to move a ball by walking backwards, holding onto the ball and evaluation, to the best sources of with its front legs. It knows that when it places the ball in a certain location, it will receive a anchorage and nourishment. sugar reward. Other bees can learn this task by observing skilled workers, in a manner that Although this proposal has been indicates an understanding of the goal of the task. taken up recently by František Baluška

368 American Scientist, Volume 107 at the University of Bonn in Germany, obvious that—despite the wonders of software and let them roam freely and by Anthony Trewavas at the Uni- unconscious processing—no human under competitive conditions, would versity of Edinburgh, the case for plant being can nourish itself, escape preda- the most successful ones ultimately consciousness is more difficult to make tion, reproduce, engage in a social life, be those with subjective experiences, than the one for insect consciousness. or find the way to a new destination emotions, the ability to predict the Trewavas argues that parts of plants without consciousness of a world out- results of their behaviors, and rela- move to approach an object or to avoid side the body. tively flexible problem-solving skills? Or would conventional robots with a versatile toolkit of highly efficient but preconfigured, hard-wired responses Bees spontaneously improved upon fare better? If, as we have argued, consciousness the strategy used by the demonstrator, is an evolutionary invention—akin to wings or lungs—that is useful to us, it is most likely useful to other organisms suggesting they had an appreciation of with traits deeply homologous to ours. They share with us the difficulties of the outcome of their actions. moving, probing the environment, re- membering, predicting the future and coping with unforeseen challenges. an obstacle, and their stems can probe, What about the panpsychist notion If the same behavioral and cognitive twine, or lean, but their movement that the universe, computers, elec- criteria are applied as to much larger- timescale is so slow that we may be trons, and other lifeless beings might brained vertebrates, then some insects simply overlooking the rudiments of possess consciousness? We hold that qualify as conscious agents, with no intentionality in their behavior. How- because these entities do not face deci- less certainty than dogs or cats. ever, plants do not move their bod- sions requiring agency, it would be as- ies as a unit, and therefore don’t need tonishing if they had experiences. The Bibliography (or have) a central nervous system en- challenges that come with survival Barron, A. B. and C. Klein. 2016. What insects abling the whole body to navigate in and self-replication faced by a moving, can tell us about the origins of conscious- space. And as we’ve argued above, we living organism are most efficiently ness. Proceedings of the National Academy of Sciences of the U.S.A. 113:4900–4908. believe that a central nervous system implemented through emotions, a rich Chittka, L. 2017. Bee cognition. Current Biology is critical for the first stages of devel- representation of the world, and the 27:PR1049–R1053. opment of a conscious distinction be- ability to anticipate at least the imme- Lawson. D. A., L. Chittka, H. M. Whitney, and tween self and world. diate future. S. A. Rands. 2018. Bumblebees distinguish Another objection needs to be ad- It might seem like prejudice to tie floral scent patterns, and can transfer these dressed before one credits too many consciousness to life. Increased com- to corresponding visual patterns. Proceed- ings of the Royal Society B organisms with consciousness. Much puting power and machine learning 285:20180661. Loukola, O. J., C. J. Perry, L. Coscos, and L. of human behavior depends upon sub- have enabled the automation of pat- Chittka. 2017. Bumblebees show cognitive conscious processing of which we are tern recognition, including the recog- flexibility by improving on an observed unaware. Our actions in the world de- nition of faces and human speech, the complex behavior. Science 355:833–836. pend to a surprising extent upon stim- simulation of meaningful conversa- Perry, C. J., L. Baciadonna, and L. Chittka. 2016. uli we haven’t consciously noticed, tion, automated theorem-proving in Unexpected rewards induce dopamine- and the experience of volition has logic and mathematics, and even the dependent positive emotion–like state chang- es in bumblebees. Science 353:1529–1531. been found to follow our actions after creation of fine art (see “AI Is Blurring Wilson, C. 2014. The explanation of conscious- a time-lag rather than preceding them the Definition of Artist,” January–Febru- ness and the interpretation of philosophi- or being simultaneous with them. One ary). As artificial devices acquire more cal texts. In: Interpretation: Ways of Thinking could interpret this gap between many and more of these competencies, why about the Sciences and the Arts, eds. P. Ma- human actions and conscious thought shouldn’t there come a moment when chamer and G. Wolters, pp. 100–110. Pitts- as showing that consciousness has no they “wake up” into consciousness? burgh, PA: University of Pittsburgh Press. Wilson, C. 2018. Consciousness as a biologi- causal input into behavior. According (See Computing Science, 346–349.) cal phenomenon: An alternative to pan- to this theory, it is supposed, the brain But why should they wake up? We psychism. Harvard Review of Philosophy collects and weighs environmental have no reason to think that conscious- 25:71–87. stimuli and data from memory, com- ness must appear when automated putes the best option, and makes the performance of activities that are sig- behavioral choice for us by initiating nificant to humans, such as chess play- an action. If consciousness is causally ing, reaches a high point of develop- ineffective, the argument that animals ment. The more likely outcome is that For relevant Web links, consult this need it for living is unavailable. Or we are unable to produce a fully com- ­issue of American Scientist Online: perhaps what we need consciousness petent living robot unless and until we www.amsci.org/magazine/issues/2019 for is fully automated in them. can discover, and replicate syntheti- /november-december However, these arguments do not cally, the elusive NCCs. diminish the case for widespread con- If we could generate self-repairing, sciousness in the animal kingdom. It is self-replicating robots with evolvable www.americanscientist.org 2019 November–December 369