OLLIE’S problem is he’s shy. Most Saturday nights, while the other octopuses are shaking their tentacles down at the disco, Ollie’s at home watching TV. Social situations reduce him to a quivering jelly. If a female so much as looks at him, he blushes from head to tips. This is the story of how awkward Ollie overcame his bashfulness to win fair Octavia.
Hold on! Cute animal characters are all very well in cartoons, but in the real world Ollie represents the worst kind of anthropomorphism. Not only has he been endowed with human feelings, motivations and technology, he has even been given a personality. We all know that octopuses and their ilk are characterless.
Think again. It turns out octopuses really can be timid-although a shy octopus doesn’t have much in common with a shy human. What’s more, your backyard may be teeming with small creatures that have big personalities. From cowardly spiders and reckless salamanders to aggressive songbirds and fearless fishes, researchers are finding that seemingly uncharismatic individuals have distinct personality traits. Sometimes these help the wee beasts survive, but they may also land them in serious trouble. And studying how such rudimentary personalities arise is starting to shed light on the evolution of more sophisticated personalities-including our own.
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Among those who study animal behaviour, anthropomorphism is generally considered a cardinal sin. That helps explain why they haven’t expressed much interest in personality up until now. It also explains why researchers who have begun to work in this area tend to use careful phrases such as “behavioural carryover” when talking about personality. But, as psychobiologist Samuel Gosling of the University of Texas at Austin points out, there is no reason to believe that natural selection shapes only physical traits. Darwin himself argued that emotions exist in non-human animals, and his evolutionary theory suggests that behavioural traits, including personality, can evolve in just the same way as fins, wings and arms.
Considerable ingenuity is needed to expose such adaptations in creatures whose lives and perceptions of the world are so very different from our own. Susan Riechert from the University of Tennessee, Knoxville, and Ann Hedrick from the University of California at Davis, have risen to the challenge in their studies of funnel-web spiders. These animals build sheet webs to catch their prey, then spin themselves an escape funnel that leads into a series of subterranean cracks where they can hide from birds and other predators. The funnel-web spider’s silk is not sticky, so it can only capture prey by waiting at the mouth of the funnel and quickly attacking any insect that strikes the web.
Web of intrigue
Riechert and Hedrick studied two populations of funnel-webs in their natural environment. They used puffs of air from a camera brush to fool the spiders into thinking there was a predator near the web, then clocked the length of time the spiders hid inside the funnel. “Spiders from the desert grassland would hide but then just run right back out and wait for food again,” says Hedrick. “The woodland spiders would hide for much longer.” This makes sense, say the researchers, because although they are the same species, the two groups have evolved to survive in different conditions. In the woodland, where there is a high level of predation by birds, excessive boldness could cost a spider its life. In the grassland, on the other hand, there are few predators but insect food is much harder to come by, so it pays to be fearless and spend as much time as possible waiting at the mouth of the funnel.
Despite these general trends, in both populations some spiders were bolder, and some more cautious. To see whether these personality traits might carry over into other aspects of an individual’s behaviour, Riechert and Hedrick matched up pairs of spiders from a single population and had them battle for ownership of a web. They found that in both groups the more courageous individuals-those that came out of hiding faster after a disturbance-were also much more likely to win the fights. Those that were bold when threatened by a predator were also bold when faced with a competitor of their own species. Timid spiders were timid in both situations.
Similar behavioural carryovers have been found in a few fish and bird species. Among three-spine sticklebacks, fish that fight harder to protect their breeding territory from other sticklebacks are also more aggressive when faced with a predator. And a study of young great tits-a European songbird-found that birds that are bolder and quicker to explore a strange new habitat are also more likely to win territorial fights with other great tits.
Such findings are breaking new ground in biology. “To date, we have only a few studies showing the behavioural carryover in natural populations, and even fewer demonstrating its importance in terms of individual survival,” says Andy Sih from the University of Kentucky in Lexington. Sih’s own research shows how complex the relationship between personality and survival can be.
His unusual interest in the personality quirks of streamside salamanders began when he noticed what seemed to be reckless behaviour in some of the larvae. The young animals would continue to actively forage, even when predatory green sunfish were present, making them an obvious and easy target for these deadly hunters. What was going on?
To investigate the evolution of the salamander’s response to sunfish, Sih and his colleagues Lee Kats and Eric Maurer compared the behaviour of streamside salamanders with that of a closely related species that only lives in ponds where there are no sunfish. The researchers couldn’t introduce live sunfish to their lab tanks-these would devour the salamanders in short order. But when they added water from tanks containing sunfish, all the streamside salamanders responded to chemical cues in it by swimming for cover, whereas only some of the pond species took action. Sih concludes from this that the pressures of sunfish predation have helped shape streamside salamander behaviour.
In both salamander species, however, some individuals and groups of siblings were consistently more active, whether or not sunfish chemical cues were present. All streamside salamanders took refuge under a rock or in shallow water when they sensed the threat, but some didn’t stay hidden for long before they came back into the open to search for food. In the wild, this tendency to forage whether or not predators are around can have disastrous results. So why doesn’t natural selection weed out the more reckless individuals? The answer may lie in a link between aggressive foraging behaviour and a lack of caution in the presence of predators.
Streamside salamander larvae live in creeks that have the inconvenient habit of drying up in late summer. This means that there’s a race to eat enough plankton and other prey to metamorphose into air-breathing adults before their watery home disappears. There seems to be a trade-off. “Geared-up larvae-those that are more active and feed better in the absence of fish-are inappropriately active and liable to be killed by fish when they are present,” says Sih. “Geared-down larvae, those that hide best in the presence of fish, remain sluggish in the absence of fish.” Their risk of predation is lower, but so too are their chances of reaching maturity. The salamanders seem unable to fine-tune their behaviour to fit different circumstances.
Sih believes that these sorts of conflicts between innate personality traits and the various pressures of natural selection are common. This, he says, may explain why some apparently maladaptive behaviours persist in the wild. Other studies seem to confirm that personality traits that have evolved to promote survival in one situation may get an individual into trouble in another. Strong selection pressure for young fishing spiders to eat as much as possible, for example, may lead an overly aggressive female to devour her mate before he has had a chance to fertilise her eggs.
Even in animals that are sophisticated enough to adapt their behaviour to suit different circumstances, personality traits can affect survival. Take the pumpkinseed sunfish, a common resident of lakes and ponds in the eastern US. David Sloan Wilson of Binghamton University in New York and his colleagues Anne Barrett and Kristine Coleman found that fish that were “bold”-willing to explore a strange object thrown into the pond-were also more likely to feed in open water and forage on their own. “Shy” individuals that were nervous of novel objects tended to hide and forage in aquatic vegetation and stick close to other fish.
But the personalities of pumpkinseed sunfish proved to be surprisingly complex. A fish that is timid in one situation-fleeing from a red-tipped yardstick poked into the pond-may be bold enough to sample unfamiliar food. Another pumpkinseed that bravely attacks and nips at the yardstick may be too cautious to nibble at a novel food source. When largemouth bass, which prey on pumpkinseed sunfish, are introduced into the pond, a pumpkinseed’s response can be predicted from its response to the stick, but not from its response to the food.
“One response is not going to do for all the different situations you encounter in life,” says Wilson. “It is an important evolutionary insight that individual differences should often be domain-specific. Perhaps I should play it safe with respect to predators but fight like a tiger to keep my little secure territory.” As Wilson points out, we all know humans whose tendencies for boldness or shyness are “domain-specific”-dependent on the situation they find themselves in. He gives the example of a field researcher who calmly climbs over knife-edge precipices, but who sweats with fear if he has to speak in public.
It takes all sorts
While Sih has focused on personality traits as a possible explanation for some maladaptive behaviours, Wilson believes that if both shy and bold individuals persist in the wild, each strategy must be succeeding in its own way. The different behaviours of pumpkinseed sunfish may be an example of what evolutionary biologists call frequency-dependent selection. If there were only a few fish in the pond, they might all be able to survive in the “shy” mode, carefully hiding and feeding among the vegetation. But as the population of pumpkinseeds grows, the safe habitat will become too crowded and some fish will be pushed to try bolder behaviour-foraging in the open where there are more zooplankton to eat. Eventually, specialists using the two strategies, each with its own risks and advantages, evolve within a single population.
“I think we’re going to find that a lot of different behavioural traits are correlated in ways we might not expect,” says Hedrick. She is now looking at the link between courtship and predator evasion in crickets. Males with the longest courtship trills are the most attractive to females, but they are also most at risk of arousing a predator’s attention. Hedrick has found that these males, if disturbed while calling, will stay quiet for much longer than males with short trills. “Trill lengths are inherited, so males with long trills have sons with long trills,” she says. “The question is, why do guys with short trills persist in the population? It may be because when there is disturbance, the males with the more attractive, longer calls shut up, and the males with short trills can call then and get females to respond.” It looks like these crickets have evolved two different strategies, each of which allows them to survive and still get a mate.
Beasts such as spiders, salamanders, fish and crickets offer an opportunity to study the evolution of behaviour in ways that are just not possible with humans, because researchers can tinker with their habitats, and because closely related ancestral species are sometimes still available for comparison. “These studies tell us that evolutionary history plays a role in setting limits on the development of personality types,” says Sih.
But can they reveal anything about the evolution of our own behaviour? “It teaches us that there is nothing uniquely human about individual differences,” says Wilson. What’s more, he says, recent work with lower animals has persuaded some people to think about our differences as adaptive strategies-a new idea in the study of human psychology and evolution. Gosling agrees. “One might argue that different human ecological niches would also promote different personality traits,” he says. “Perhaps the traits suited to living in a group of African nomadic hunter-gatherers would differ from those suited to living in the far north where one must spend the long winter nights cooped up in an igloo with your family.”
Ultimately, the study of creatures with attitudes may help us to understand our own quirks, and how strategies as different as lashing out when provoked and fleeing can both succeed, in a small pond or in the wide world. But we must still constantly guard against falling into the trap of anthropomorphism. A salamander may be a risk-taker, but its motivation is quite different from that of a person who chooses to bungee jump or play the dotcom stock market. “Human personality types include labels that have some meaning beyond the straightforward data, like neurotic, thrill-seeking, anal-retentive,” says Sih. “I am not, of course, in favour of putting these labels on other animals.”
