IF YOU HAVE NEVER watched bees carefully, you are missing out. Look closely as they gently curl and uncoil their mouthparts around food, and you will sense that they are not just eating but enjoying their meal. Watch a bit more, and the hesitant flicks and sags of their antennae seem to convey some kind of emotion. Do those twitches signal annoyance? Or something like enthusiasm?

Whether bees really experience any of these emotions is an open scientific question. It is also an important one, with implications for how we should treat not just bees but the great majority of animals. Recently studies by Melissa Bateson and her colleagues at Newcastle University in England have rekindled the debate over these issues by showing that honeybees may experience something akin to moods.

Using simple behavioral tests, Bate­son’s team showed that honeybees under stress tend to be pessimistic. Other tests have demonstrated that monkeys, dogs and starlings all tend to react similarly under duress and likewise see the proverbial glass as half empty. Although this finding does not—and cannot—prove that bees experience humanlike emotions, it does give pause. We should take seriously the possibility that insects, too, have emotions.

Beeline to the Brain
First, a little bit about bees. They are members of the diverse group of animals lacking backbones—indeed, more than 95 percent of all animal species are invertebrates. Despite the varied and often nuanced behaviors they can exhibit, invertebrates are sometimes regarded as life’s second string, a mindless and unfeeling band of alien critters. If that seems somewhat melodramatic, just consider our willingness to boil some of them alive.

Those judgments tend to arise from arguments about invertebrates’ failure to demonstrate the behaviors we usually associate with a pain response. Whereas the yelps and grimaces of other mammals are familiar to us as announcements of hurt, invertebrates can appear to take their injuries in stride. Insects are commonly observed using their crushed limbs with undiminished force when walking, for example, and a locust will reportedly carry on with a meal while it is being eaten by a mantis.

Other attempts to draw a dividing line between creatures that feel and those that do not are rooted in comparative brain anatomy. Invertebrates lack a cortex, an amygdala and many of the other major brain structures routinely implicated in human emotion. Their nervous systems are quite minimalist compared with ours: we have roughly 100,000 bee brains’ worth of neurons in our head. Some invertebrates, however, including insects, do possess a rudimentary version of our stress response system. So the question remains: Do they experience emotion in a way that we would recognize, or do they simply react to the world with an elaborate set of reflexes?

To gain some traction on this fascinating question, Bateson’s team followed the lead of recent investigations on “pessimistic biases” in animals. In humans, the pessimistic bias refers to our well-known tendency to perceive threats or anticipate negative outcomes more frequently when we are feeling anxious or depressed. For example, in tests where people are shown ambiguous statements such as “the doctor examined little Emily’s growth,” anxious individuals are less likely than others to conclude that Emily is fine and only her height was being checked.

Although the link between bad moods and negative judgments may not be terribly surprising, this correlation is still useful. We rely on it in our daily lives to make informed guesses about how people are feeling by observing their actions and choices. Scientifically, we can use it to study the emotions of creatures unable to tell us directly how they feel. The key here is to set up a controlled situation where animals encounter an ambiguous stimulus—think of it as a nonverbal version of the Emily statement.

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In the initial setup of Bateson’s experiment, a group of honeybees was trained to associate two simple odor mixtures with two different foods. One mixture, which consisted of one part hexanol to nine parts octanone, was repeatedly paired with sucrose, which bees find rewarding. The other odor mixture consisted of the same two chemicals in opposite proportions (nine parts hexanol to one part octanone) paired with quinine, a compound that most of us find bitter and bees will actively avoid after tasting. By using this technique, the researchers hoped to overcome the bees’ intrinsic responses to sucrose and quinine and test only their judgment of the new smells. After learning these odor-food associations, the bees responded as expected, uncoiling and extending their mouthparts in anticipation of food when the first odor mixture was presented and retracting them at offers of the second concoction.

This training allowed the scientists to study the bees’ decision making by then testing their mouthing responses to a series of ambiguous odor mixtures. First, half the bees got a trip to the “vortexer.” The experience was probably as unpleasant for them as it sounds to us. In a procedure meant to simulate a badger attack on a hive, the bees were shaken for one minute in a machine typically used to vigorously mix chemicals. If bees can indeed be made to feel cranky, surely this device would do the trick.

Next, both shaken and unshaken bees were tested on five mixtures of hexanol and octanone at different concentrations. Sure enough, both groups preferred extending their mouth to octanone-heavy mixtures, which predicted sugar, rather than hexanol-heavy mixtures, the scent of which predicted quinine. Interestingly, the shaken bees were less likely to advance toward any of the mixtures than their unperturbed counterparts.

In an analogue of the classic scenario  of the half-empty glass versus the half-full glass, the bees were also presented with an equal mixture of hexanol and octanone. Bees that were spared the trip to the vortexer gave the concoction the benefit of the doubt, moving their mouth toward the food on close to 60 percent of the trials. Shaken bees, on the other hand, ignored or recoiled from these same ambiguous stimuli more than half the time. The stress of shaking had turned them into pessimists that interpreted the ambiguous odor as half threatening rather than half appetizing.

Both Shaken and Stirred
In addition to these behavioral measures, the scientists also tested for changes in the bees’ neurotransmitter levels after shaking. The quantities of certain chemicals with known roles in insect learning (octopamine), aversive conditioning (dopamine) and aggression (serotonin) were all reduced by the procedure, suggesting that as with their mammalian counterparts, duress in bees causes sustained, system-wide changes in brain state—a possible analogue of mood. Together these behavioral and neurochemical tests reveal an unexpected dimension of bee cognition. Formally, we can say that when agitated, bees can take on a negative disposition, a state that alters both their thinking and their neurochemistry.

For now, however, we cannot conclude anything more sweeping about the emotional life of a bee. Bateson and her co-authors leave us with an intriguing plea for consistency, however, one that nudges us to think clearly about how we regard the minds and emotions of all creatures. Last year researchers tested dogs that appeared to suffer from separation anxiety for a pessimistic bias. When they encountered an uncertain food reward, the perturbed dogs also appeared less inclined to try the ambiguous treat, which the researchers interpreted as evidence that dogs indeed feel anxious when left alone. “It is logically inconsistent,” Bateson and her colleagues say, to deduce that dogs and other similar animals express emotions “but to deny the same conclusion in the case of honeybees.”

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To put it another way, our criteria for assessing animal emotions should be blind to whether the animal has fur, feathers or an exoskeleton. Either bees and other invertebrates get a trial membership in the club of the genuinely anxious, or we must concede that our beloved pets’ seemingly pessimistic actions imply nothing about their feelings. For a smitten dog owner, at least, the choice is probably obvious.