It is a tale with all of the ingredients necessary for a hero’s saga: the little guys under siege from a ruthless, violent foe; the clever ruse that saves the society from attack; and the realization that this had been going on for millennia in a little-known part of the world. True, the “little guys” are bees, but that fits in with a recent trendiness of backyard beekeeping and love for pollinators. A little harder to take, perhaps, is that the defense of the colony involves balls of dung.
The bees in this story are close relatives of the European honeybee (Apis mellifera) most familiar to us; they are still considered honeybees, but they are Apis cerana, sometimes called the Asian or eastern honeybee, and they are smaller, with more pronounced striping on the abdomen. They live in the same kind of hives as their European cousins, however, and in parts of Asia, including Vietnam, where this story unfolds, they are under threat from Vespa hornets, a kind of wasp many times larger than the bees. (Although they are closely related to the “murder hornets” making headlines, this is not the same species.) A 2020 paper1 reports on the interaction, with the description of the hornets’ strategy making it clear where the authors’ sympathies lie: “During this slaughter phase, each hornet can kill thousands of bees, and, collectively, a group of hornets can obliterate a colony’s defensive force within a few hours. When resistance ends, the occupation phase begins: hornets enter the nest, begin guarding it as their own, and shuttle brood back to their own nest to feed their young.”
It had been known that the bees could defend themselves by, for example, surrounding a wasp and suffocating it in a ball of bees, but that wasn’t going to work with this hornet attack. The recent study showed that the bees use a more novel approach. Scientists had seen small dark spots at the honeybee hives’ entrances, which local beekeepers said were water buffalo dung. The bees gather the dung at water sources, and carefully place it around the hive; if enough spots are present, the hornets are deterred from attacking, for reasons that aren’t clear. The authors of the study call the fecal material a tool, recognizing that this designation is a bit of a reach, but saying that “the fact that the bees are collecting something from the environment, holding it, manipulating it and changing the character of the thing that they’re applying it to, makes it a tool by virtually every definition.”2
If the bees aren’t convincing, or if “pellets of animal poo,” as the Guardian called them,3 are a bit too unsavory, another example of recent insect tool use comes from ants that make siphons out of sand. The particular ants under study are black fire ants, which like many of their kind will drink sugar water. Most of the time, ants can simply float on the surface without risk, because their waxy coating keeps them from sinking. But when some diabolical scientists from China and the United States added a surfactant—a soapy material—to the water, the surface tension of the water dropped and the ants began to drown.4 Undeterred, the ants began to plaster sand grains supplied by the scientists along the sides of the container with the sugar water, which allowed the solution to wick up the sides so they could safely drink. As the surface tension got even lower, with more ants at risk, the insects constructed more elaborate sand structures, enabling them not only to avoid drowning but also to get access to more of the tasty liquid.
The sand, too, was deemed a tool, and much was made of the flexibility of its use, since the ants could change what kind of siphon they made depending on the perceived risk of the situation. The authors of the study claim that the behavior indicates “high cognition,” which proved to be a sticking point for some. Nevertheless, at least some readers commenting on a summary of the work that appeared on the website Why Evolution Is True5 not only bought that the ants had advanced thinking ability but also leapt from there to the notion that the ants, or perhaps their colony, were conscious. According to one, “Such a subset of the colony implementing higher consciousness would look like a cluster of ants interacting furiously with each other, to no obviously visible purpose.”
Of course, that is exactly what ants look like to me much of the time, so it isn’t clear how that gets us to consciousness, or the lack of it. Still, the ants, as well as the bees and a number of other examples of invertebrate intelligence I will bring up in this chapter, point to a conundrum in how we think about the evolution of behavior, particularly behavior that suggests that an animal is aware of what it is doing. We marvel over crows using tools or chimps exhibiting empathy, yet we are still taken aback by invertebrates doing similar things, at least if we think that only some animals—and humans—have a special ability to perceive and interact with the world.
But because behavior evolves the same way that physical characteristics do, our surprise may be uncalled for. Complex behavior in invertebrates arises the same way that complex physical structures do, or complex physiology. Selection can produce flexible behavior, that hallmark of intelligence, just as it can produce digestive systems that can accommodate a wide variety of foods. The gut doesn’t have to think about how an ice cream cone is different from a steak to render each into its components.
Invertebrates, then, are some of the best subjects for studies of how behavior evolves. In addition to my simply really liking them, as the chapter title suggests, I am enamored of invertebrates as a way to understand behavior, because we can actually induce evolution in them without having to wait for centuries or millennia to pass as we would if we were examining generations of most mammals or birds. Their small size and short lifespans challenge the conventional wisdom about which animals do complicated things. The sheer number of different kinds of invertebrates, from shellfish to worms to my favorites, the insects, provide a gigantic palette for nature to show its variety. As the philosopher Peter Godfrey-Smith said6 in his book Metazoa: Animal Life and the Birth of the Mind, “Arthropod evolution has been exuberant for half a billion years.” And they ultimately make us rethink who we put in that special class of intelligent creatures, and why.
Socially Inept Bees, and Crabs in a Maze
Honeybees are often considered the very model of cooperation. Along with ants and wasps, they are called the social insects, after all. They are also often dismissed as all alike, tiny cogs in a big exoskeleton machine. But it turns out that not all worker bees are equally responsive to their hive mates, and an unlikely link between humans and bees is responsible for the variation.
Ordinarily, bees from one colony will attack a worker bee from a different colony, sometimes injuring her if she is introduced to their hive. In contrast, they will fawn over a young queen, even if she is a foreigner, and try to feed her. Researchers at the University of Illinois at Urbana-Champaign tested bees from seven different colonies by introducing them to either the larval queen or the strange worker.7 Some bees were more enthused, so to speak, about attacking the apparent intruder than they were about nurturing the potential queen; with others, it was the other way around. Most of the bees reacted in some way to at least one of the two situations, but about 14 percent didn’t respond to either one, sitting around on the sidelines while their nestmates rushed around acting like guards or nurses. The scientists then dissected the brains and nervous systems of the bees, and used sophisticated genetic analysis to see which genes were most active in the nonresponsive bees. More than a thousand genes were regulated differently among the unresponsive bees, the nurse bees, and the guards. The subset of genes that was active in the nonresponsive group of bees turned out to be similar to sets of human genes implicated in autism spectrum disorder, but not in schizophrenia or depression.8
Now, no one is concluding that bees are autistic, or that autism in humans is caused by the exact same process that produced bees indifferent to the plight of their coworkers (though researchers are excited about the possibility of using honeybees to test ideas about autism and the nervous system). Gene Robinson, the director of the lab in which the research was performed, said in an interview,9 “We do not want to give the impression that bees are little people or humans are big bees.” It’s a point that seems like it should not have to be made, but does. Instead, the research points to the seamlessness of behavior in many living things. Like the mantids that I discussed in chapter 2, which can fine-tune their behavior according to the task at hand, the bees are neither automatons nor exact replicas of humans. What is more, even creatures we deem to be identical robots can show remarkably subtle differences in behavior.
Bees are favorite study subjects for learning in insects, perhaps because they are important to humans and perhaps because they are simply interesting and seem to be able to do things that are much more complex than one would imagine a creature with such a tiny brain could manage. They can, for example, recognize individual human faces, and they can discriminate among many different flowers when searching for food. The latest bee achievement has to do with a task many humans find challenging: doing mathematics.10 Let me hasten to point out that bees are not sitting in their hives solving differential equations, or calculating the volume of honey that will yield the most offspring for the following year. But they do seem to be able to associate symbols with numbers, at least with the numbers two and three. Such a numerical sense had been demonstrated in African Grey Parrots, chimpanzees, and rhesus monkeys, but never before in an invertebrate.
The bees in the study were trained to match a symbol, say a T-shape, with two or three objects, or, vice versa, to associate the number of objects with a symbol. It took around fifty trials for the bees to figure out the task, but after that effort, they could correctly match the two 80 to 90 percent of the time. Trying to teach the bees to reverse their task, so that if they had started with the symbol, they were then supposed to match the number, proved less successful. The scientists who trained the bees speculated that “an approximate number system”11 exists in both humans and bees, which presumably means that many other species have similar abilities.
Bees are not, however, the only invertebrates that can learn to perform complex tasks. Crustaceans, the animal group that includes crabs and lobsters, are not exactly stars in the brain and nervous system department. For the purposes of comparison, a crayfish has just ninety thousand neurons, whereas a honeybee has over a million. But as we’ve seen before, brains aren’t everything, and animals are often good at different tasks; no one would ask a bee to bend a wire to get food out of a tube, and crows would probably never learn how to gauge the amount of nectar in a flower. A group of researchers in Swansea, England, took the ordinary European shore crab and gave it a classic learning task, namely, a maze.12 Rats, of course, are practically synonymous with mazes. They have lived among humans for millennia, and we know that rats are good at navigating complicated passageways. But crabs also live in environments with lots of twists and turns among rock crevices, yet their abilities hadn’t been tested. The crabs got a rather advanced version of the maze test, with a crushed mussel as a food reward at the end. Virtually all of them figured out how to get to the food within twenty-five minutes, taking several trials to do so without errors. After six weeks, during which time the crabs were not tested, they could still find the endpoint of the maze within eight minutes.
Fruit flies are even less likely candidates for flexible learning, having been the poster animals for genetically based behavior for over a century. As I mentioned in chapter 3, they were one of the earliest subjects for the examination of the genetic basis of courtship, performed by Margaret Bastock. Perhaps because of this iconic history, no one spent much time considering whether their behavior was anything but strictly genetically determined, meaning there could be little opportunity to alter what they did in the face of changing circumstances.
Yet even the fruit flies show us the inescapable interaction between genes and the environment. Male fruit flies will court females without any prior experience if they have a particular gene called “fruitless.” If male fruit flies that lack the gene are reared by themselves and then presented with female fruit flies, they stand there, apparently dumbstruck, like kids at a middle school dance. But a 2014 paper13 found that the situation is more complicated than that. If the males without the fruitless gene are raised with other fruit flies, they can learn to court females, through mechanisms that are not yet understood (though one wonders what the equivalent of adolescent sharing of sexual misinformation might be for fruit flies). The point is that even a behavior so basic and essential that it seems as if it must be completely instinctive, especially in a fly, can be modified by experience.
What Puts the Us in Octopus?
Tell me, O Octopus, I begs,
Is those things arms, or is they legs?
I marvel at thee, Octopus
If I were thou, I’d call me Us.14
When he wrote this poem, Ogden Nash presumably meant that an octopus’s collection of limbs made it seem like multiple animals. But one could also call the animals “us” for other reasons. If the animals-that-are-practically-honorary-humans bench has had to make room for first bonobos and chimpanzees, and then crows and parrots, the latest reason to move over is a sticky one, literally. The last few years have been full of stories about the wonders of the octopus, with its Houdini-like ability to escape confinement, its apparent awareness of people, its cleverness at solving puzzles, and, as the most recent news relates, its irascibility in occasionally whacking fish for no apparent reason.
In his book Other Minds,15 philosopher Peter Godfrey-Smith beautifully contemplates how octopuses are and aren’t like us, and how their complex behavior suggests a connection to us that is absent in most other invertebrates. He suggests that losing the hard outer coverings of snails and other mollusk cousins enabled the octopus to evolve a more complex nervous system. Their “different embodiment,” with a shape that can grow, change color, shrink and reform in a moment, allows octopus to exist “outside the usual body/brain divide.”
Does that squishiness of form mean that octopuses are smart? Maybe. As Godfrey-Smith says, “When tested in the lab, octopuses have done fairly well, without showing themselves to be Einsteins.”16 They can learn to operate levers to get food, but so can many other animals, including that workhorse of psychology, the pigeon, which no one has ever proclaimed to be a genius. Some researchers suggest17 that a few of the octopuses’ activities fulfill the requirement for play in animals, another one of those characteristics we like to believe is restricted to humans and just a few select creatures like monkeys or dolphins. A slight snag is that play in other animals is usually different in juveniles and adults, while in the octopus no such demarcation exists; the authors of a paper on play explain this away by saying that “the standard concepts of juvenile and adult life found in vertebrates do not easily translate to cephalopods.”18 Perhaps. But what else doesn’t translate as well?
It is worth thinking about what octopuses can and can’t do because it forces us to think about what we really mean by intelligence and what else has to accompany it, whether that is language (presumably not, since octopus do not have complex communication systems), intricate social interactions (ditto), or something else. We make a lot of assumptions about how much animals have to be like humans to be considered intelligent, and octopuses give life to those assumptions with every rippling shape-shift. As Godfrey-Smith also says, they “have an extraordinary sensorium and an anarchic bodily embrace of novelty, but they are not, for the most part, ruminative and ‘clever’ sorts of animals.”19
One of the ways that octopuses defy our ideas about intelligence is that they, along with most of their cephalopod cousins like squid or cuttlefish, live very brief lives, perhaps four or five years, often much shorter. My friend Jody was telling me about watching My Octopus Teacher, an award-winning 2020 film about a man who spends a year watching and interacting with a female common octopus as he dives off the coast of South Africa. At the end of that period, the octopus reproduces and dies. “I was crying, Tom [her husband] was crying . . . how can they just have their babies and die?”
I shrugged, not because octopuses do not move me, but because, as I told her, dying after reproduction is pretty common in animals, especially invertebrates. Cockroaches, I helpfully pointed out, do much the same thing. Jody glared at me. “Do they really? Well, thank goodness for that!”
Is it that we think an animal that seems to enjoy life should be able to do so for longer? Or is it just that since our own lives are longer, we want the same for an animal with which we sympathize? You could just as easily ask why mayflies get a lousy twenty-four hours while tortoises can persist for centuries. Godfrey-Smith says that he assumed cuttlefish and other octopus relatives were old, “partly because they seemed old; they had a worldly look.”
Is the question why they die so young, or why they ever became smart? A 2018 paper20 has the rather plaintive title “Grow Smart and Die Young: Why Did Cephalopods Evolve Intelligence?” The authors, led by Piero Amodio of the University of Cambridge in the UK, note that if one relies on primates to think about intelligence, one gets a tidy story about how animals become smart in one of two ways. First, a complex environment may require flexible foraging strategies, such as group hunting. Second, as I have already mentioned, living in a group makes it necessary to communicate with the others and remember who is on your side and who is not. Either option you choose paves the way for a story of big brain evolution and culminates with human societies as we now have them.
But as the paper’s authors point out,21 many other vertebrates, especially corvids, as we saw in the last chapter, also seem intelligent, even though they have much different brains than primates. Maybe, then, the same selective pressures were at play, with the common thread being a long life with an extended juvenile period and a lot of parental care to allow the youngsters to learn the ropes of both finding food and navigating social politics. A big brain along the lines of the primates may not be required. Except—here again, the octopus and other cephalopods defy the norm, since their eggs float away unattended and mothers die. The authors then suggest that perhaps the octopus’s sexual cannibalism, in which females sometimes eat their mates, has selected for fast decision-making and flexible mating tactics, but this seems like a last-ditch effort to me. After all, their non-robotic nature notwithstanding, no one is rushing to champion praying mantises, the queens of sexual cannibalism, as geniuses either. It also feels, shall we say, troubling if we’ve come to the point of suggesting that eating your mate is what makes a species smart. Other researchers would remove the “social complexity” part of the equation for evolving intelligence, noting that in humans, IQ and social ability are not correlated, but this, too, seems like special pleading.
Anyway, it turns out that all is not wonder and grace in the octopus world. In December of 2020, at the end of what was arguably one of the roughest years in recent history, scientists reported22 on octopuses using one of their arms to punch—their word—fish. Some of the blows seemed to be associated with the octopus shoving the fish out of the way so that it could obtain its prey, but a few other incidents—two out of the eight that were recorded—were more inexplicable. A possible explanation of the latter, according to the authors of the paper, was “spiteful behavior, used to impose a cost on the fish regardless of self-cost.” Other options were mentioned, but the spite idea immediately captured media attention, with the New York Post headline “Octopuses Spite-Punch Fish, Who ‘Don’t Like It,’ Study Finds” and even the New York Times offering videos titled “Eight-Armed Underwater Bullies: Watch Octopuses Punch Fish.” Comments from readers of the Times ranged from congratulatory: “If you were as intelligent as an octopus, and these annoying and stupid fish just wouldn’t do what you want, you might resort to smacking a few of them, too” to amused: “Octopuses are highly sensitive animals and as such are easily offended” to critical: “Calling this bullying or lashing out is premature, anthropomorphic and stupid.”
So, are octopuses us, or not? To me, octopuses illustrate the perils of reverse engineering an explanation in evolution. We assumed that if humans are smart, and that we have certain qualities like longer lives, bigger forebrains, or complex social lives, then those qualities are necessary for our intelligence. But we then run into trouble if the creatures we think are intelligent lack such qualities. Instead, maybe we can acknowledge that intelligence isn’t measured the same way in all creatures—something that sounds facile, but I don’t think is. This doesn’t mean that all animals have the same abilities, a la Euan Macphail, the comparative psychologist I mentioned in the previous chapter, but that those differing abilities evolved, just like physical characteristics, in the environment where a given species exists.
The Really, Really Itsy-Bitsy Spider
Octopuses have eight limbs, and we think they are sinuous and graceful. Spiders have eight limbs and we think they are horrid and creepy. This seems profoundly unfair. It is particularly unfair because in addition to being just as agile in their movements as the lauded octopuses, spiders show us the limitations of the nervous system, and just how the body limits the mind, or at least the way we behave.
Bill Eberhard is a biologist with the Smithsonian Tropical Research Institute and the University of Costa Rica, and he has always been ready to question invertebrate conventional wisdom. He tends to study animals that other people dismiss: earwigs, wasps that parasitize other insects, and, yes, spiders. His work on the latter has included spiders’ kinky sexual practices (he describes the sound that one species makes as “resembling squeaking leather,” which in an earlier book I said was like spider porn, if such a thing can be said to exist).23 He has also asked a question to which spiders are perfectly suited: Does being small mean they are dumb?
Many people have tried to make connections between brain size and behavior, especially intelligence, as I discussed in the previous chapter, but few have drawn this comparison out to its logical conclusion: Are there animals that are so tiny that they are almost, as the saying goes, too stupid to live, or at least to do complicated tasks, or tasks requiring flexible responses? Even Darwin wondered about this possibility, especially when faced with the complex behavior of ants; in his 1871 book The Descent of Man, and Selection in Relation to Sex, he mused, “The brain of an ant is one of the most marvelous atoms of matter in the world, perhaps more so than the brain of man.”24
How might such small-scale intelligence be possible? Do minuscule animals pay a price for their lack of brain capacity? Among vertebrates, smaller individuals tend to have larger brains relative to their body size, a generalization called Haller’s Rule, after Albrecht von Haller, an eighteenth-century Swiss physiologist. The rule seems to work for many invertebrates as well, but because neural tissue is expensive for an animal to maintain, it wasn’t clear if there is a lower limit to the evolution of brains capable of driving complex behavior. Very small animals may well have different constraints on the way their brains can manage their behavior, but few scientists have tried to apply Haller’s Rule to creatures without backbones.
Eberhard has studied the spider Anapisona simoni, the adults of which weigh less than a milligram. To put this in perspective, that is lighter than a single staple, or an inch of sewing thread. Yet inside their compact form is enough nervous tissue to enable the spiders to produce orb webs, the silky wheel that entraps even tinier prey. Eberhard wondered if the extremely difficult process of weaving a web was more of a challenge to the minuscule Anapisona than to three other spiders that weighed anywhere from ten to ten thousand times their size (which still does not give them horror movie status—a single milligram is that tiny). He meticulously compared the species’ ability to adjust the space between loops, to construct different angles between the spokes of the web, and to place the sticky lines of the web, the ones used to snare the prey, at exactly the right spot.
It turned out25 that although the miniature species had a bit more trouble adjusting its web to different conditions, by and large the small spiders were as capable as the larger ones. How do they manage that? Possibilities include cramming brain tissue into places where it is not usually found; some of the small spiders have brain tissue that spills over into their legs, giving, as Eberhard and his colleague Bill Wcislo state,26 “new meaning to the phrase ‘thinking on your feet.’ ” It’s a mystery how this leaves enough room for other important organs, like those for digestion. It also poses questions about just how little tissue is required to run an animal at all, since the laws of physics limit just how small neurons can become. And if that isn’t enough, Eberhard also reminds us to think of the children, so to speak; those teeny tiny spiders have even teenier babies, and they, too, have to catch their prey.
This work brings up the question of how brains and behavior are connected in insects, the way they are in birds, as I discussed in the previous chapter. A comparison of ninety-three species of bees from North America and Europe27 found that body size was the best predictor of their brain size, as it is in many other animals. But bees vary in many aspects of their biology: they live in different places, feed on different things, and may be solitary or live in large colonies. It turned out that specialized species, such as those that need to eat only one kind of plant, had large brains relative to the size of their bodies, as did species that only had one generation per year, rather than having a queen with a lifespan that overlaps with her daughters and granddaughters. The more social species did not tend to have bigger brains, a surprising departure from what we know about humans and other primates, where the hypothesis that the pressing need for social intelligence led to our oversized brains. Insects, once again, break with convention.
Some people have pointed out that if we want to think of the brain as a computer, bigger should not be assumed to be better, since of course modern computers are dramatically smaller than their twentieth-century forebearers. Newer models are more efficient, and with more sophisticated technology, making a large number of components unnecessary. At the same time, Lars Chittka and Jeremy Niven, biologists from Queen Mary University of London and the University of Cambridge, respectively, argue28 that this analogy is flawed, because nervous systems and brains, unlike computers, are not designed for a given purpose, but evolve through the “tinkering” process I noted earlier, with selection never starting from scratch but always using the components already present. Some parts of our neural anatomy, they point out, “have been retained since the Cambrian. Arguably, all extant [existing in species alive today] nervous systems are success stories; no single one is inherently better than any other.”
This evolutionary history, along with the different environments of different animals, should make us wary of generalizing about what we mean by intelligence. Chittka and Niven note29 that insects and other invertebrates can reveal the circularity of reasoning about brains and being smart; one psychologist decided that learning speed is a poor indicator of intelligence, based on the fact that honeybees are faster at learning colors than other vertebrates, including humans. Insects have surprisingly large behavioral repertoires given their small brains, with flexibility that rivals that of at least some vertebrates. Maybe, they suggest, the question should be not how insects can do so much with their tiny brains, but why so many vertebrates bother with big ones. Rather than focusing on an All-Animal IQ test, it seems more interesting to focus on the way that evolution has acted in similar ways in distantly related groups.
Rules of Thumb for Creatures That Don’t Have Any
I have been studying crickets for over three decades, and I would never suggest that they are geniuses. They can exhibit some rather astonishingly flexible behavior, but they do so in a way that obviates the need for complex cognition, the same way that many other animals might be able to combine genes and experience to produce sophisticated responses to the environment.
The crickets I study, sometimes called Pacific field crickets, live in subtropical parts of Australasia, including northern Australia and islands like those in Samoa, Fiji, and Tahiti. Sometime before the late nineteenth century, people introduced the crickets to Hawaii, where they live ordinary cricket lives: males sing by rubbing their wings together to attract females, and females choose males based on the quality of their songs. In Hawaii, unlike other parts of their range, however, male crickets face another problem besides the one of sounding alluring to a potential mate. A parasitic fly called Ormia ochracea (it has no common name) can hear the male’s song as well. When a female fly locates a calling male cricket, she flies close to him and drops her tiny, sticky larvae on and around his body. The larvae burrow inside the cricket and proceed to consume him while he is still alive, eating what a student of mine referred to as the “gooey bits” until, a week or so later, the cricket is a hollow husk as the larvae emerge to complete their life cycle.
While arresting, not to mention gruesome, in many respects, this situation poses a conundrum for the crickets. The more a male sings, the better his chances of attracting a mate, but in Hawaii, he also risks attracting the deadly fly. The evolutionary way out of this conundrum has occupied my lab for the past many years, but a relatively recent development was also one of the most startling:30 on some of the islands where the crickets and flies occur, cricket males evolved a change in their wings that makes them unable to sing. A single gene caused this alteration, and males with the new form—we call them flatwings because the wings lack the structures needed to sing—are now prevalent in several places. The change came about in only a handful of generations, making it an example of extremely rapid evolution in the wild.
Being a flatwing cricket is obviously helpful to males in protecting them from the parasitic flies, which cannot find silent prey, but it also poses obvious drawbacks to the other side of the equation, the attraction of females. Yet the mutation was able to spread, and flatwings—as well as a stable handful of crickets lacking the mutation—are still present in Hawaii. How are the mutant males managing to find females?
Since some of the males can still sing, we wondered if the males with the mutation were behaving as what are called satellites—males that do not signal to females, but instead lurk near the singers, capitalizing on females that are attracted to the singers and mating with them as they are encountered. Such tactics are reasonably common in animals, with frogs, birds, and other cricket species all having satellite males that take advantage of the hard work of other individuals.
A set of field experiments showed that this was exactly the case.31 The design of the experiment was simple: put out speakers playing prerecorded cricket song, and see who showed up. Flatwing males were more attracted to the song, and they got much closer to the speaker, than the males that had normal wings. But how did the males know, as it were, to do that? The single gene that affected wing development couldn’t possibly also affect the brain in such a way that males could know they couldn’t sing, then figure out to approach a caller, and then calculate their position. As I said, crickets just aren’t that smart.
Instead, we think that the crickets employ what you might call a rule of thumb, a simple algorithm that links a set of environmental circumstances with a preexisting response. A world with flatwings is also a world that is silent, at least from the standpoint of cricket song. But silent worlds can arise for a number of reasons: a recent storm wiped out much of the population, the habitat is poor, or the lawn (which is where the crickets occur) just got mowed. What if the crickets already have a rule that says, in effect, “If I do not hear a lot of crickets singing, I should move closer to the ones I do hear.” This does not require the males to actually think that, the way a human would, just to execute a simple If-A-then-B series of behaviors. If they already have that flexibility of behavior, then the mutation could get a head start.
That is exactly what the crickets seem to do. In my laboratory, we have populations of the crickets from many places. We can rear them with and without cricket song, simply by playing recorded song inside the incubators where we keep them. Male crickets that grow up hearing a lot of crickets singing, which presumably sends the message that mates are likely to be available, are relatively slow in responding to a playback of song as adults.32 The males that grow up in silence, however, navigate to the source of the playback with alacrity, which in nature would increase the likelihood of coming across a female cricket likewise moving toward the song. Females seem to use similar rules, which also makes them more likely to mate with one of the silent males if they encounter one. Note that the system depends on the persistence of the singing males, because they are the linchpin that holds the system together. Every time we go to Hawaii to see what the crickets are up to, I brace myself to find that the populations have gone extinct because too many flies have discovered the singers. So far, that hasn’t happened.
Similar rules of thumb may apply to many other species, in which a combination of genes and environmental influences can produce remarkably complex behavior that looks as though it was the result of human-style reasoning. Butterflies, for instance, have to choose a plant on which to lay their eggs, and the quality of that plant makes a big difference to the success of their offspring. My colleague Emilie Snell-Rood and her postdoctoral advisor Dan Papaj did an experiment with the common cabbage white butterfly that showed that females could learn to lay eggs on a plant with either green or red leaves.33 Green leaves are more common in nature, and the butterflies seemed to have an innate bias to lay eggs on them rather than red plants. Having that bias—what the scientists called an educated guess, but what we could also think of as a rule of thumb—may help the butterflies get a head start in the wild, because the operating costs of maintaining a brain that evaluates red and green from scratch would be too high.
The crickets and butterflies show how flexible invertebrate behavior can be, and that maintaining that flexibility comes at a price. They, along with the crabs, spiders, and octopuses, also flatly contradict Macphail’s idea that I mentioned in the previous chapter, that no differences in intelligence exist among nonhuman species. Macphail was talking about vertebrates, but a group of psychologists published a paper34 in 2020 suggesting that a species of jumping spider—the kind that doesn’t build a web, but instead pounces on prey that cross its path—would be a good candidate for an intelligent arthropod whose behavior could counter Macphail. They detail the abilities of the spider to solve puzzles; change its behavior if it is offered different types of prey; “count,” or at least assess rough quantities of objects, about as well as a human infant; and generally behave in what one might call an intelligent manner, at least if we use the same measurements on spiders that we do on birds or mammals.
This all seems well and good to me, but I remain puzzled at anyone taking Macphail’s suggestion seriously for even a moment. Had he never seen different animals behaving in the world? And even if he had not, believing his hypothesis would require placing behavior in a completely different universe from the rest of the animal, since no one would ever argue that animals do not differ in physical attributes. Why would all animals have the same learning ability, or however one might define intelligence, but have different digestive systems, eyesight, or numbers of limbs? It doesn’t do us any good to separate the two, as I have been pointing out.
Putting the Joy Back in Killjoy
Even though animals can do extraordinarily complicated things without the same kind of cognition that humans have, we still seem to want to categorize them by their similarity to us humans. Indeed, the popular press seizes new evidence of tool use, problem-solving, or social plotting in animals as evidence that other species are smarter than we had previously thought. Many of the comments from readers on such coverage seem to take a kind of vindicated tone, as if science is finally catching up to what they had known all along, that animals have evolved the exact same abilities and inner lives as people and we are being needlessly closed-minded by failing to recognize that fact.
Not everyone, however, is convinced. Sara Shettleworth, a comparative psychologist at the University of Toronto, wrote a paper35 in 2010 lamenting our dismissal of simpler explanations for complex behavior as “uninteresting and ‘killjoy,’ almost a denial of mental continuity between other species and humans.” This use of the term killjoy comes from Daniel Dennett, a philosopher who has written about the evolution of consciousness, a similar problem. Shettleworth goes on to point out that although we have a kind of folk psychology that we use to explain what animals do, that intuition is often simply wrong. It is even wrong when we apply those explanations to our own behavior by assuming that people are making conscious decisions all of the time. Psychologists have known for many decades that less rational mechanisms can account for what we do, from making bad economic choices to deciding whether to put money into the coffee kitty at work—a study showed that the image of a pair of eyes “watching” contributors increased the amount of money left to more than twice what they donated if the image was of a flower.
Such tendencies to see animals as exactly like people are hardly new. In 1898, the eminent psychologist Edward Thorndike published what can only be termed a rant against such anthropomorphism,36 saying, “The history of books on animals’ minds thus furnishes an illustration of the well-nigh universal tendency in human nature to find the marvelous wherever it can.” He laments that “folk are as a matter of fact eager to find intelligence in animals. They like to. And when the animal observed is a pet belonging to them or their friends, or when the story is one that has been told as a story to entertain, further complications are introduced.” It boggles the mind to imagine what Thorndike would have had to say about internet cat memes.
This doesn’t mean that we need to go back to human exceptionalism. Daniel Dennett has tried to call for a compromise,37 saying, “People in the field often gravitate into two camps. There are the romantics, and the killjoys. I think the truth is almost always in the middle.” But this is a case where it’s hard to see what the middle means here. That one should be slightly romantic, or that animals are somewhat like us, but not exactly? Like many attempts to find middle ground, doing so seems prone to leaving both sides unsatisfied. In his discussion of consciousness, Dennett also criticizes an earlier writer for suggesting that consciousness “presumably” occurs in mammals, and “probably” in birds, reptiles, and amphibians. “Wondering whether it is ‘probable’ that all mammals have it [consciousness] thus begins to look like wondering whether or not any birds are wise or reptiles have gumption: a case of overworking a term from folk psychology that has lost its utility along with its hard edges.”
A similar objection could be made to the idea that all animals have the same intelligence or emotions as people. Invertebrates particularly reveal the shaky ground of that overworking, because if it seems a bit odd to talk about a turtle with gumption, it is manifold weirder to speak of a mournful caterpillar or a wistful snail. Some authors say that the relationship between animal intelligence, or consciousness, and our own is more of a continuum, with shades of gray rather than a sharp us versus them distinction; Godfrey-Smith, for example, points out that being conscious is not an on-off switch, and thinks of it as more of a graded experience.38 But this, too, seems less than satisfying, because a continuum is still a line marching from one shade to the next, with white at one end and black at the other, like the scala naturae we know to be incorrect. Intelligence doesn’t grade from fish to turtles to birds and finally primates, so it doesn’t really help to suggest that the edges between them are blurry. Not having an on-off switch doesn’t mean that we must perforce have behavior on a dimmer.
What does help, once again, is thinking of behavior as evolving the same way that other characteristics do. No one tries to pit killjoy versus romantic explanations for the differences among, say, kidneys in different kinds of animals. We can see that our kidneys are more similar to those of other mammals than of birds, and all three groups are distinct from insects, which use a completely different system called the Malpighian tubules to filter waste. Yet no one worries about who should be admitted to the urinary processing club of True Kidneys. Animals differ in many attributes, including behavior, but we only seem to want to create rankings for some of the attributes.
Finally, the real prize for killjoy approaches to animal behavior must come from a group of psychologists who published a paper cheerily titled “Towards an Animal Model of Callousness.”39 While they take no position on whether animals are callous in the wild, the authors suggest that because a lack of empathy—callousness—in humans is an important antisocial disorder, maybe we should find a relevant callous animal model to explore, the way we have with other mental disorders. Research on empathy and callousness in humans shows that callous people differ from more empathetic ones in several parts of the brain, particularly in part of the frontal cortex and the amygdala. This link to brain function suggests that exploring dysfunction in those pathways might yield insight into the problematic behavior. A slight difficulty seems to be that rodents—their proposed choice—do not ordinarily exhibit anything like human callousness, and even prefer situations in which they and a companion get a reward over getting the same reward by themselves. Not daunted, the researchers speculate that if that generous impulse could be eliminated, either with a different experimental setup or with drugs, it would be possible to examine its opposite in a controlled manner. Whether finding a rat that wouldn’t sympathize with your problems would be a help in our considerations of how we perceive other animals’ abilities is another question.