by Riskin, Dan
Do animals really steal because they’re envious? That’s a tough question. It’s not quite impossible to determine whether or not an animal truly experiences envy, but it’s pretty close. To demonstrate conclusively that animals are envious, you first have to demonstrate that they comprehend that other animals have their own experience. Then you have to show that the animal can measure a difference between what they have and what a competitor has. And then, finally, you have to show that this imbalance makes the animal react negatively. That’s a tall order. Even if you see animals doing the kinds of things humans do when they’re envious, like stealing from one another, you can’t really know it’s envy unless you do a rigorous set of experiments.
But those experiments have been done with capuchin monkeys, and the results are pretty compelling.13 Researchers trained some monkeys to put a small rock in a researcher’s hands. As a reward, the monkey would either get a grape, which they loved, or they’d get a little cucumber, which they found tolerable but far less exciting than a grape. To bring envy into play, the researchers fed monkeys their grapes and cucumbers in side-by-side cages, so the monkeys could always see what their neighbor was getting.
So long as the reward a monkey got was the same as the reward their neighbor got, monkeys played along, happily taking grapes or cucumbers in exchange for their work. But if a monkey got a cucumber while it could see its neighbor getting a grape, the monkey got angry. Monkeys would sometimes throw the cucumber back in the face of the researcher or else just stop playing the game altogether. In essence, monkeys refused to do the same work if they saw someone else getting paid more for the same job.
Now, what I’ve described so far might be monkey envy, but there’s another possible explanation. Perhaps the monkey getting the cucumber is reminded of how awesome grapes are when it sees the grape next door. Maybe it’s not envy but just that it’s hard to eat crap food when you think about delicious food. Maybe rather than envy, the monkey just feels disappointment.
Well, the researchers designed their experiment to rule out disappointment so they could be sure that what they were seeing really was envy. The researchers did that by making sure that in those scenarios where both monkeys were getting cucumbers, they could both see a bowl of grapes right in front of them. The fact that monkeys didn’t get mad those times showed that the thing upsetting the monkeys wasn’t being reminded of how awesome grapes are. The trigger was clearly the difference between what a monkey got and what its neighbor got. The careful design of those experiments nicely showed that capuchin monkeys experience envy.
Dogs show the same tendencies. In another study, researchers put pairs of dogs side by side and asked them to “give a paw.” The dogs obeyed the order up to thirty times in a row when researchers gave both dogs treats as rewards, or even when the researchers gave neither dog a treat. But if one dog got treats while the other one did not, the dog getting nothing quickly stopped obeying commands. Again, researchers made sure it was envy rather than disappointment by leaving the treats out all the time, right where dogs could see them.14
I suspect that many other animals experience envy, but experiments just haven’t been done for them. (Experiments have been done with chimpanzees, but the results are less clear.)15 There may be many other kinds of envious animals in nature, but without those kinds of experiments, you can’t ever know for sure. When you see a pigeon at the park stealing a piece of bread from another pigeon, you can’t tell if it was envious of the other pigeon’s property or if it just wanted some bread. The fact is, though, that nature’s a tough place because animals steal from one another. Splitting hairs about their inner emotional state sort of misses the point.
Besides, envy can be a good thing. If a kid admires the possessions of the doctor next door and that motivates her to go to medical school, I don’t think that’s a problem. If a person envies the peace and calm of a colleague from work and decides to take up meditation and yoga to try to emulate those traits, great! Looking around to see what others have and then trying to get those things for ourselves is a basic part of how human society works. The fact that capuchins and dogs have envy might be the small cost that comes with all the advantages of being part of a social species.
But envy does bad things sometimes too. And while theft is an obvious symptom, another one is infidelity. Think about it: coveting thy neighbor’s partner can sometimes lead to affairs, and that can cause serious emotional pain for everyone involved. Animals cheat even more than professional athletes do, and I have to think that envy plays a role for them at least some of the time.
Take species with harems, for example, where you have a single male who gets to mate with a whole bunch of females. This always means that a bunch of other males have to sit on the sidelines and mate with no one. How could they possibly not be envious? My favorite example of this is the sac-winged bat I mentioned in the chapter on sloth, the ones I saw roosting outside my first vampire bat cave in Costa Rica and whose males are known for flinging feces and urine on the females they want to mate with. (Yes, those sac-winged bats.) So help me, if there’s envy surrounding sex in the natural world, that is a species that would have it.16
Male sac-winged bats have a lifestyle in which one male gets to be the partner to a harem of up to seven females. Those females live with one another, and with one another’s pups, on the side of a tree, cave, or building. Solitary males, called satellite males, roost nearby, without any females of their own.
The sac-winged bat got its name from the pockets it has in its wings, just above its elbows. (Here’s where things get disgusting.) Right before heading out for a long night of hunting insects, a male licks out the sacs in his wings to clean them, then leans down, fills his mouth with his own urine, and spits that urine into his wing sacs. Next, he leans back down and rests his throat against his penis and quivers until a white droplet comes out of his penis and sticks to the fur on his chin. Then he transfers that droplet with his chin to the urine-filled wing sac, before repeating the procedure to fill the other wing sac.
Mixed together, the urine, saliva, and genital secretions produce a musky bouquet of odor. The male then hovers in front of a female in his colony and shakes his wings at her, much like a person would shake a salt shaker at their food, thereby covering that female with a sample of his sexy cologne. This behavior is called salting.
Males are advertising how healthy they are with the way they smell, and females use scent to decide whether or not the male is sexy enough to mate with. That’s why males have to clean their sacs out each day and make a new batch. Bacteria living in the sac constantly break down scent molecules, producing other, less attractive odors. To a female, those bacterial odors are a sign that the male isn’t quite up to snuff.
Every once in a while, a satellite male will salt one of the females, giving her a sample of his wares (sometimes he’ll even salt the harem male!), but the harem male responds by chasing him back to the periphery, and salting on him for good measure.
It’s pretty clear that the satellite males are just waiting for an opportunity to take over the harem. When researchers experimentally remove a harem male from his roost, it’s always a satellite male that takes his place, as opposed to a dominant male from another harem, for example. And it’s not just any satellite male. It’s a satellite male that had previously been sitting right at the periphery of that particular harem. Since there can be several harems close to one another on a wall, I think that’s suggestive that a satellite male is focused on stealing one particular male’s harem. It looks for all the world like envy to me, but I know it’s impossible to know for sure until controlled experiments are done.
The really interesting thing about the harem mating system in sac-winged bats is that everybody is cheating. In a frenzy of paternity analysis that would make Maury Povich envious, researchers learned some dirty sac-winged secrets. Yes, harem males fathered more of the pups than satellite males did, but a harem male was the father of only about 30 perce
nt of the pups in his own harem. Thirty percent! The other 70 percent came from a mix of nearby satellite males and a few males with harems of their own, whom females had obviously gone out to visit from time to time.
Harems are common in nature, and that makes life pretty tough for the males out there who just can’t compete with other males. But there’s an alternate strategy available: if you can’t beat ’em, become a sneaker male. Sneaker males occur in all kinds of different animals, and their strategy is to avoid confrontations with the stronger males by getting creative.
Great Plains toads mate in the puddles that form after a big storm in the midwestern Unites States. Males initiate this process by getting into the water and croaking out into the night, to say, “The water’s fine, ladies. You should come join me!”17
One thing about frogs is that the male has no penis to place inside a female. Instead, he’ll hold on to her in the water, hugging her from behind in a sort of frog cuddle.IV While he does that, she will release her eggs into the water as he releases his sperm on top of them. That is how frogs have sex, but first they have to meet up.
A female Great Plains toad won’t approach just any croaking male. She prefers a large male, and there’s a biomechanical link between how big a toad is and the pitch of its voice: bigger toads have deeper voices. So by calling out with a deep, booming voice, a big toad can advertise his size. This sort of screws the little males over, since their tenor tones just don’t impress the females, and there’s no way to fake a deep voice. (No matter how well you play a trumpet, it will never sound like a tuba.)
The solution? Small males hang out near a dominant male and don’t croak at all. When a female swims over to join the deep-voiced male, the sneaker male intercepts her, and they cuddle.
It’s not clear whether the female thinks he was the one calling, whether it’s a case of forced copulation, or something else, but one thing is certain: it works. Sneaker males fertilize eggs, and although it’s not as effective as being a dominant male in terms of number of eggs fertilized in a season, it’s a work-around that allows small frogs to pass on their DNA.
Another sneaker male strategy has been described for a frog living high in the mountains of Spain.18 There, a sneaker male will find a cluster of eggs floating around in the water that have already been fertilized. With the parents long gone, the sneaker male grabs the floating mass of eggs using the same body posture that a male typically uses when grabbing a female. Then he releases his sperm onto the eggs. Paternity analyses have revealed that around one-quarter of the frog embryos in a pond had sneaker dads who used that strategy. Again, it’s better to be a dominant male, but just because you can’t play with the big kids doesn’t mean you’re out of the game.
Oh, we’re not done with sneaker male frogs yet, though. There’s a toad called Rhinella that is commonly found in little ponds next to streams that appear after a good rain in the Amazon.19 When those ponds appear, hundreds of Rhinella toads will go there to mate, and thousands of eggs will be laid in the course of two or three days. Because that time span is so short, competition among males is ridiculously intense, and many of the females end up getting injured or killed in the fray. First a male will grab onto a female to start mating, but then another male will grab on and try to pull that first male off. Soon a female has a large ball of males holding her down, pressing her underwater until she drowns.
After the carnage is complete, animals go their separate ways, leaving several dead females lying in the pond among the fertilized eggs. At that point, a sneaker male will grab a dead female, cuddle her as he would if she were alive, and begin mating with her dead body. While he’s committing this act of necrophilia, he squeezes the sides of her body, causing eggs to come out into the water one after another, like slimy pearls on a mucus necklace. Other males will sometimes approach and try to pull him off, so that first male might end up pushing her dead body around the pond, to fertilize all the eggs himself.
Incredibly, this works. Necrophiliac sneaker male Rhinella pass on their DNA. Males have been observed having sex with dead females in many other animal groups, including penguins, ducks, and lobsters, but Rhinella is the only animal for which necrophilia can actually lead to offspring.
To me, this story is an especially good reminder that nature isn’t a model for what humans should do. Somewhere in a mountain pond in Spain, a male frog is squeezing eggs out of a female that was killed by gangs of aggressive, copulating males. Next time someone uses nature as a justification for any decision they’ve made, like what a woman’s role should be in the home, perhaps, just ask them how Rhinella fits into their nature-inspired world.
In those instances where sneaker males mate with living females, the sex has to happen relatively quickly, or else the dominant male will have time to come over and beat the sneaker up. Marine iguanas, found only on the Galápagos Islands, are another species in which sneaker males operate, and they’ve found a handy way to speed things up.20
Female marine iguanas will mate only over a few short weeks each year, and the fierce competition among males has large males defending large territories then, for access to females. You might not know that a male marine iguana needs about three minutes of sex to achieve orgasm (though that’s a great conversation starter at parties, in my experience; you’re welcome). For a large male, that’s no issue, but smaller, sneaker males don’t have that kind of time. Anytime a sneaker male manages to have sex with a female, there’s a very good chance the dominant male will come break things up before he can transfer his sperm, thus making his sneaker strategy useless.
Here’s how sneaker male marine iguanas deal with that problem. When a sneaker male sees a female walking by, he gets into a sex position, with a bent body and tail, just as he would if he were having sex with her. This apparently is how iguanas masturbate, because it causes a few drops of semen to come out of his penis. That semen dries on the tip of his penis, and when he eventually does have sex, that old semen gets deposited inside the female. He’ll get even more sperm inside her if he manages to stay on top of her for the full three minutes required to have an orgasm, but just in case he gets pushed away by the dominant male before that happens, some of the dried semen he produced during masturbation will be left inside her. And that’s better than nothing.
Even teeny-tiny animals use sneaker male strategies. If you ever go snorkeling on a moonless night in the Caribbean, you may luck into seeing blue pulses of light shooting up through the water in complex patterns from the sea grass below. I’ve never seen this myself, but it’s on my life list to see someday. Big-time.
Those light pulses come from special light-producing organs on shrimplike creatures called ostracods.21 The males are tiny, less than two millimeters long, and they make those light displays to attract females. Over the course of about twelve seconds, a male flashes ten to twenty times, swimming upward through about two feet of water, leaving little blue glowing dots behind. Males make these displays in huge numbers, and I imagine they are breathtaking. Female ostracods certainly think so. A female impressed by a male will approach in darkness, then grasp the male of her choice. They have intercourse, and he places a sperm packet inside her body, before she swims off to go brood her eggs.
The problem with those displays is that they also attract predators. Lighting up and then moving in a very predictable pattern is a great way to end up in a predator’s stomach, but the male ostracod really has no choice if he wants to mate.
Well, actually, there is one other option. Since a male moves in a predictable pattern, a sneaker male can position himself immediately above another male and then swim just ahead while the performer makes his display. With any luck, the sneaker male can intercept an approaching female, and she’ll mate with him instead of the male who did all the work. What’s different about ostracod sneaker males, compared to just about any other kind of sneaker male, is that males switch back and forth between the two mating strategies as much as they want over the course of a
night. Unlike frogs and iguanas that have their roles dictated by their body sizes, ostracods seem to have a little more flexibility and to know how to use it. The ostracod embodies for me the mind-boggling wonder of the natural world. Here you have a tiny animal doing secret light-emitting dances in the night, with a mating ritual as complex as that of any bird or mammal, even though it’s smaller than the head of a pin. The world is full of surprises, and the more you learn about any particular group of animals, the more surprising it becomes.
Another ocean-dwelling sneaker male that makes me smile every time I think of it is the giant Australian cuttlefish. It’s an eight-legged cousin of the octopus, up to twenty inches long, weighing in excess of twenty pounds. Cuttlefish are well-known for their ability to instantly change color, which allows them to camouflage when they need to, make flashy displays to scare off predators, or communicate with other cuttlefish. And of course, if you can communicate, you can lie. Sneaker male cuttlefish are fantastic liars.
Male cuttlefish aggressively defend females, but the females aren’t crazy about commitment. There are lots of males to choose from, and even though she rejects 70 percent of mating attempts, she still has sex up to seventeen times each day. About 65 percent of the time, that’s with a large, dominant male. But a smaller male has three strategies for meeting females. Sometimes he’ll approach a female out in the open, right in front of the dominant male (but he has to hurry); sometimes he’ll approach a female under a rock, out of sight of the big male; and sometimes he’ll use a third strategy—dressing in drag.22