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Oyamel Cocina Mexicana, in the Penn Quarter neighborhood of Washington, D.C., is a restaurant specializing in insects. Stepping inside on a cool June evening in 2014, my friend Stephen Wood and I were immersed in the colors and smells of Oaxaca, Mexico. Oyamel is the name of the fir tree native to central Mexico where monarch butterflies rest upon migrating from the United States and Canada, and the décor had a lepidopteran theme: The glass door at the entrance was studded with transparent red, yellow, and pink butterflies, and butterfly mobiles hung from the ceiling.

But it wasn’t butterflies that Stephen and I had come to sample. Our quest focused on chapulines, soft tacos stuffed with grasshoppers. Taking our order, the waitress noted our luck: The grasshoppers sometimes get held up coming through customs from Mexico, but that night they were readily available. Stephen and I ordered a number of small, tapas-like dishes, and when the chapulines arrived, I saw insect body parts right away. A delicate grasshopper leg tumbled onto the table when I raised the taco to my mouth.

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Oyamel is not alone. Fried wild-caught dragonflies and spider rolls featuring rose-haired tarantulas, katydid-and-grilled-cheese sandwiches and tacos stuffed with grasshoppers: The variety of foods laced with insects and spiders available in the United States and Europe today—when you go looking for them—is considerable. The venues in which they may be found are equally varied, ranging from upscale restaurants to street-side food carts and science-museum bug festivals. Entomophagy is on the rise and generating excitement.

a crickety crunch: Many cultures around the world have long made a practice of eating insects. Now, some restaurants in the Western world are adding bugs to the menu.©
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Of course, millions of people around the world have long sought out insects and regularly, intentionally consumed them. They do not pluck bugs from under the bed or the dusty attic, of course, but forage for sources of fresh protein and other nutrients in the wild or purchase prepared insects or insect flour at traditional markets. In fact, humans eat over 1,600 species of insects. “The Western abhorrence of eating insects is unusual on a global scale,” note naturalist David Raubenheimer and anthropologist Jessica M. Rothman. Westerners may clamor for honey without fully recognizing that when ingesting it they are consuming regurgitated bee products, but people in many countries consciously embrace a wide variety of bugs as food.

As I dined at Oyamel, I pondered some questions not often addressed by fans of entomophagy: What do we know about insect intelligence, personality, and sentience?

Fruit flies make decisions—and they take longer when the information presented is difficult to evaluate.

The first step in taking these questions seriously is seeing these tiny animals. Growing up in the New Jersey suburbs, I loved whiling away an hour watching the scurrying yet remarkably well- organized activity visible within an ant farm, peering into anthills in the yard to trace the stream of red ants as they flowed in and out, and watching fireflies on a summer’s night as they blinked messages in code through the humid air. What I don’t remember is thinking of any of these small creatures as individuals; they existed for me in an abstracted sort of aggregate, in a way that my pet cat Queen and dog Shadow, or even the elephants and monkeys I met on family trips to the Bronx Zoo, never did.

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Insects aren’t primates like chimpanzees (or us), and they aren’t, usually, our pets. What might happen, though, if we tap into our natural curiosity about insects and spiders and ask how they live on their own terms? We do these tiny animals a disservice if we fail to ask questions that only relatively recently in recorded history have humans begun to ask about chimpanzees (or cats and dogs). Do insects learn? How do they interact with their world in intelligent ways? Do they experience the world via distinct personalities?

Wasps may strike us as buzzing, sometimes stinging, annoyances when we spend time outdoors. But there’s another way to look at them: as animals with busy brains. Paper wasps, with a brain less than 0.01 percent the size of our own, recognize individuals who are important to them. Neurobiologist Elizabeth Tibbetts discovered this fact when she altered wasps’ facial features by applying modeling paint to them. Nestmates of these suddenly different-looking wasps responded in an atypically aggressive way, while their behavior toward control wasps, who were daubed with paint but whose facial features remained unaltered, didn’t change at all. The specificity of the hostile response indicated that the wasps recognized faces, using that recognition to determine who belonged in their community. Nestmates with painted faces were suddenly seen as strangers, and the reactions were not friendly.

Queens of the species of wasp used by Tibbetts in this experiment (Polistes fuscatus) work together cooperatively within shared nests, but they also experience female-female competition. Facial recognition is adaptive in this context because queens need to distinguish potential rivals from potential allies. Tibbetts went on to train these wasps to distinguish pairs of images of various sorts. “Most strikingly,” she and her co-author Adrian Dyer write, “simply removing the antennae from a wasp face image or rearranging the face components dramatically reduced their impressive face-learning capacity.” This fact suggests to Tibbetts and Dyer that the wasps process faces holistically in specialized parts of the brain, as we humans do.

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Tibbetts then expanded her study to include a second species of wasp (Polistes metricus) in which solitary queens— instead of clusters—establish nests. In this case, paint-altered nestmates elicited no immediate facial-recognition response. But here’s the fascinating part: In the training phase, these wasps did learn to discriminate faces. Presumably, this ability had not been directly selected for in this species over evolutionary time. The mental capacity is there but doesn’t emerge under natural conditions. Reviewing studies of wasps and bees in general, Tibbetts and Dyer conclude that “there is ever so much more going on their teensy brains than we could have imagined possible.”

Does that conclusion apply to other insects? Yes, if we’re talking about learning. In entomology, learning is defined as the ability to acquire, and represent in one’s brain, new information. Historically, the working assumptions in entomology were all about instinct. The reigning equation “simple nervous systems = behaviors driven by hard-wired instinct” was straightforward enough—and also spectacularly wrong.

When I ate those grasshoppers, I swallowed animals who had experienced the world in some individualistic ways.

One spring morning when I was writing this essay, my Twitter stream lit up with the news that fruit flies make decisions, and what’s more, they take longer to do so when the information presented is difficult to evaluate. In an ingenious experiment, fruit fly subjects were first trained to avoid a certain strong smell, then offered a choice between two samples of that smell whose intensities varied by degrees. The insects took longer to make their choice when the difference in smell was subtle (or minimal) than when it was pronounced (or maximal). Neuroscientist Shamik DasGupta and his team concluded that the experimental outcome “bears the behavioral signature of evidence accumulation.” In other words, these insects wait until they have gathered enough information to make a reasonable choice when presented with options that complicate decision-making. This weighing of variables according to context is linked in the fruit flies to one specific gene (FoxP) and about 0.1 percent of the flies’ total neuron count—right around 200 neurons.

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Far more famous an example of insect learning is the honeybees’ waggle dance. In this case, the acquiring of new information happens socially. Performing in the dark hive, the dancers, experienced forager bees, clue in younger, naïve bees about how far to fly, and in what direction, to find suitable flowers. Thanks to scientific experiments, we know that the dances do not operate like the GPS devices that send us, via detailed driving instructions, to a pinpoint location. Instead, they convey information that directs the observer bees to the right general region. There, the flowers themselves provide sight and smell cues; the bees zero in on these beacons and begin to forage.

Decision-making fruit flies and information-sharing bees are joined by a host of other examples: Learning, both individual and social, is a robust phenomenon in the insect world. At the end of a 2008 review paper, Reuven Dukas concludes, “Learning is probably a universal property of insects, which rely on learning for all major life functions.” No mindless drones, insects are intelligent in the sense that they evaluate information coming into their senses and their brains from their physical and social environment, and in some striking cases, they think about how to act on the information they have learned.

In 2012, I was startled to come upon this provocative sentence at the top of a science-news post on the BBC Nature website: “The experiences of youth can change the adult personalities of crickets, a new study has found.” The very fact that biologist Nicholas DiRienzo and his colleagues had hypothesized such a connection tells us something important—that established animal-behavior researchers by now expect indicators of personality to be found in some insect species.

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DiRienzo explains in a technical article published in Animal Behaviour that degree of boldness—an organism’s willingness to expose itself to risk—is a trait expressed consistently in individual crickets at different ages and in different situations. Boldness tends to co-occur with aggression. “We consider aggressiveness to be a personality trait in this species,” the researchers note, “particularly since aggressiveness and boldness are correlated and thus form a behavioral syndrome.”

The scientists experimentally manipulated the sounds experienced by young crickets (Gryllus integer, commonly found in the American West). They started with males too young to have yet developed an ear, called a tympanum and located in crickets on the front legs. As they were reared, the crickets were separated into two groups: Those in one group had a chorus of male calls played to them, mimicking what they would have heard in the wild; those in the other group experienced only silence.

What happens when we view insects through the lens of “animals we eat,” as we do for chickens or pigs?

The males reared without hearing the cricket chorus, referred to as “acoustic sexual signals” because the calls are uttered during male-male competition for females, were more aggressive and more likely to become dominant. I enjoyed reading the details of this experiment, imagining the researchers at work avidly watching cricket male-male grappling matches, the events through which they assessed aggression levels. But I couldn’t work out on my own why males reared in silence should be better and more dominant grapplers.

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DiRienzio and his coauthors, it turns out, think that crickets use the sounds they hear—or don’t hear—to figure out population density. The crickets who hear nothing assume that they will face little competition from other males in their forays to find females, and act accordingly—asserting greater dominance than they would if they had discerned evidence of greater competition around them. In other words, signals from the surrounding environment alter cricket personality.

Now, measuring levels of boldness and aggressiveness in crickets admittedly affords a limited perspective on animal personality. Hanging out with crickets, we would not likely feel that we were in the presence of highly distinct individuals the way we would with chickens or chimpanzees. Some animals vary one from the other along more complex dimensions, not just bold/less bold or aggressive/less aggressive, but gregarious/socially shy, emotionally volatile/phlegmatic, spiteful/easygoing, and so on.

Insects are not cookie-cutter copies of each other when it comes to their ways of being in the world. The chorusing-cricket experiment shows that personality is not merely a matter of inborn genetics, because the rearing environment plays a role. (For some scientists, animal personality is affected in part by the environment, whereas animal temperament stems from genetics.) In short, when I ate those grasshoppers, I swallowed animals who had experienced the world in some individualistic ways.

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Tarantulas tend to taste somewhat like smoky lobster,” reports Daniella Martin. While I am fascinated by insects’ and arachnids’ biology and evolution, and try to minimize harming these animals (with some exceptions, including mosquitoes), I need to repress shivers when I get close to them. My reaction is, once again, culture-bound. No documented death of a person has ever come about because of a tarantula bite. Yes, these are large animals for arachnids (the biggest known boasts a leg span of 12 inches and a weight of 5 ounces), and their hairy appearance can be startling. Negative reactions to tarantulas based on their size and physical traits may be exacerbated when there’s no great fondness in the surrounding culture for these creatures. “Thanks in part to Jiminy Cricket,” Martin notes, “[crickets] have pretty good PR in Western society.” Tarantulas have anything but.

Yet the tarantula’s hairiness should lead to fascination rather than fear, because it’s a lovely example of evolution at work: Tarantulas don’t build webs but like other spiders they do sense their world largely through vibrations; the hairs help detect those and thus help the animal capture prey. I learned these and other cool tarantula facts from an online interview with Nicole Atteberry, curator of ectotherms at Zoo Miami. Atteberry went on to distinguish between shy and aggressive tarantulas, evoking tarantula personality.

sentient spiders?: Some research suggests that spiders, like this Greenbottle Blue Tarantula, have distinct personalities.davemhuntphotography/Shutterstock

The key here is to find a reasonable balance in how we think about insects’ individuality. Samuel Marshall, an arachnologist who has studied wild tarantulas in French Guiana (considered by some the tarantula capital of the world) and has clocked countless hours with tarantulas in the lab, cautions that because of their rudimentary nervous systems, we shouldn’t go too far down the road of thinking in cognitive or emotional terms about tarantulas. He doesn’t believe, for example, that tarantulas can become anxious or depressed in the way many vertebrate creatures may. Talking with Discover Magazine in 2004, however, he embraced the word “personality” as applying, for example, to how different tarantulas from a single population of the same species respond to handling. These variable tendencies form part of a suite of potentially fairly complex behaviors. Two of Marshall’s students, Melissa Varrecchia and Barbara Vasquez, discovered that Indian ornamental tarantulas prefer to associate with their siblings over other possible companions. “Long-lived, giant spiders,” Marshall said at the time, “have a lot more going on than we have any idea of.”

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In exploring the science of spider personality, I contacted Marshall, who, in the wonderful way of science networking, sent me on to Susan Riechert, a spider biologist at the University of Tennessee, Knoxville. “As spider behavior is highly repeatable,” Riechert told me, “it has a very strong heritable component and thus I always refer to spider behavioral tendencies as temperament.” Her comment conveyed that variability within a species’ repertoire doesn’t invariably stem from learned complexity. For example, Riechert’s and Thomas Jones’ paper on variation in spider social organization shows (in this specific case) an imperviousness to environmental influence.

It’s challenging to ascertain whether insects feel pleasure and pain.

Riechert and Jones study Anelosimus studiosus, a social spider found in North and South American forests. In this species, there’s maternal care, which is atypical for spiders: The mothers guard their young offspring and offer them food via regurgitation. When the mother dies, a dominant daughter often assumes control of the nest and forces out her siblings. Working in the United States, the scientists identified two studiosus sites (each with many spider nests), accessible by water, at 2-degree intervals in latitude, from south Florida’s Everglades (26 degrees) to east Tennessee (36 degrees). Solitary nests were, they discovered, the most frequent type at all latitudes. The presence of multi-female nests and a cooperative-female social structure was first found at 30 degrees and increased in frequency as latitude increased.

With a laboratory phase added to the field research, the results get really interesting. Riechert and Jones collected nests from two cold-water and two warm-water sites, and raised the juveniles from those nests in the lab. Then they transplanted this second generation back into the wild at various latitudes. In this way, some of the juveniles from solitary nests were transplanted to latitudes where multi-female nests were common, and vice versa. All of these juveniles tended, in the scientists’ words, “to express the social structure of the parental nest, regardless of the warm- or cold-water environment of the transplant site.” When multi-female nests were transplanted, for instance, into the Tennessee habitat that favors single-female nests, new multi-female nests resulted. Even though social structure correlates with latitude, it’s not the case that certain environments induce certain social structures. Social behavior in this spider species is resistant to environmental factors and doesn’t demonstrate plasticity. Can there even be such a construct as personality under such conditions, given that personality is shaped in part by the environment? It would seem not, but there’s definitely evidence for temperament in these spiders.

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The ecologist Jonathan Pruitt found that studiosus individuals can be categorized as more aggressive or more docile. He became a sort of arachnid matchmaker, creating in the lab 90 spider couples; some paired an aggressive male and an aggressive female, some a docile male and a docile female, and others one of each. The next generation’s temperaments were consistently (but not completely) predictable: An aggressive pair’s offspring were nearly all aggressive, and so on. Pruitt then moved the 90 nests out into the wild, shielding half of them from other invading spiders and allowing the other half to exist amid the inter-spider competitions that naturally develop in the wild. All of the spider colonies in the predator-managed areas did equally well. Among the homogeneous colonies transferred to natural conditions, the docile colonies did better initially, but over the longer term the aggressive ones survived and reproduced more, apparently because they were less frequently consumed as prey. As a write-up in Science Now about Pruitt’s research noted, “It turns out nice guys do finish last, at least among arachnids.” Pruitt observes, however, that when mixed colonies were introduced to the wild and aggressive studiosus individuals lived side by side with mellow ones, all the spiders did well, perhaps because spiders of different temperaments excel at different survival tasks.

Insects learn, and may make thoughtful decisions as they learn. Though we often think of them in the aggregate, they may be distinct in their personalities (or their temperaments). It’s challenging to ascertain whether they feel pleasure and pain, and to the all-important question of sentience in insects and spiders I can find no ready answer. Given their sophisticated abilities for learning, though, it seems clear that the possibility of sentience should not be ruled out.

Entomophagy is poised on the verge of a major upswing, of spreading far beyond traditional contexts where it has always been popular. Meanwhile, scientists have begun in the last 15 or 20 years to ask deeper questions about insect intelligence and personality than ever before. It will be a fascinating thing to watch as the two trajectories intersect, perhaps even collide: a growing interest in eating bugs and an equally growing interest in understanding the complexities of their behavior. As enthusiasm for entomophagy builds in the United States and Europe, hard questions about insect consciousness should be kept front and center.

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Generalizing about an enormous taxonomic group of animals is risky. Nonetheless, writing in 2014, Oliver Sacks felt confident enough to offer a summary that resonates with the material reviewed in this chapter: “We often think of insects as tiny automata—robots with everything built-in and programmed. But it is increasingly evident that insects can remember, learn, think, and communicate in quite rich and unexpected ways. Much of this, doubtless, is built-in—but much, too, seems to depend on individual experience.” It’s precisely that unexpected angle that we need to keep our eye on. While it’s far less easy to offer a definitive statement about sentience in insects than about intelligence or personality, insects are surprising us.

Barbara J. King is a biological anthropologist and Chancellor Professor of Anthropology at The College of William and Mary.

Reprinted with permission from Personalities on the Plate: The Lives and Minds of Animals We Eat. © 2017 by Barbara J. King. Published by the University of Chicago Press. All rights reserved.

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Lead image originally from Paris Street, Rainy Day by Gustave Caillebotte

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