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Mixed results: having the right blend of animal personalities can make or break a group.

Watching coworkers in paper masks swim among the office cubicles acting out fish personalities turns out to be pretty informative. Admittedly, "informative" didn't seem to be the word on the tip of the tongue of Science News' editor in chief when, in the grip of urgent editorial business, he charged up the stairs and happened upon writers neglecting their keyboards for make-believe group swims. After some hasty smoothing over, though, he joined in as a virtual predator, sending fish of all personality types scattering for shelter.

Predators, information, group-ups and even games all have their place in studies of animal personality, including the mosquito fish research that inspired the office fish simulation. Even though fish dynamics over generations were mimicked by just a few terrestrial mammals between deadlines, the mix of personalities proved as important for animal welfare in cubicles as in real waterways.

Differences in the ways individual fish act, once groaned about as the inevitable messiness of gathering data on real animals, have in recent years become their own topic of research. Geese, hissing cockroaches, cichlids, great tits, mallards, sparrows and European rabbits have all starred in such studies.

Now that the idea of individual animals having a version of personality--or, more formally, "behavioral type"--has become unsurprising in scientific discourse, the next wave of research is looking at the consequences of the mix of personalities in a group.

Any non-hermit can tell tales of how the blend of personalities among human peers can lead to success or utter failure. Certain committees, task forces, condo boards and so on mire in infighting while others motor through their agendas. But this mix may matter even more directly among other animals. In flocks, schools or herds, the melding of behavioral types can be a matter of life and death, thus nudging a species' evolutionary trajectory. An individual animal's chances of finding food or starving, wooing a mate or dying without offspring, dodging a predator's jaws or becoming lunch have been found to change with different blends--as has the fate of a group as a whole.

Clever and cagey pets

Before getting into what personality might mean for animals in general, it's worth dealing with pets. Just about every magazine article on nonhuman behavioral types inspires at least one reader to write a letter to the editor fulminating about how scientists are such idiots. Anybody who has ever had dogs, cats, horses, parrots, etc., knows that they have personality.

Science, however, requires rigorous definitions and proofs, says behavioral biologist Margaret Wray. Now based in Atlanta, Wray studies personality in honeybees, but she often hears about clever cats and so on from pet lovers she knows. Finding a way to define an animal companion's lovable idiosyncrasies so they can be tested in a meaningful way isn't easy, she explains. It's hard to say whether a cat that snags open the kibble cabinet is displaying a cool, analytical approach to life, or whether trial and error has simply led to success this time around.

While psychologists describe human behavior in five dimensions (conscientiousness, agreeableness, neuroticism, openness and extraversion), personality testing for nonhumans tends toward simpler terms. Nonhuman animals can be shy or bold, aggressive or docile, social or asocial, and so on.

The key to distinguishing a personality amid all of a creature's behaviors is whether the individual responds consistently across time. A fish that hangs back in the reeds today might be considered shy if it does so next week and the week after. Researchers differ in the terms they use to describe such consistent behavioral tendencies, using "behavioral type," "temperament" or "personality." To capture more complicated effects, Andrew Sih of the University of California, Davis has pioneered the idea of "behavioral syndrome," which describes suites of behaviors linked in different situations, such as voracious feeding during foraging and frequent cannibalizing of suitors during courtship.

A fishy test

Whatever terms are used for consistent behavioral trends, mosquito fish have them. What's more, recent work suggests that the fortunes of any individual loner or clinger can vary depending on the blend in the neighborhood.

Two groups of journalist-fish, told nothing about results from mosquito fish studies, were persuaded to try an exercise in mixing up types. Each put on a mask and drew a personality profile out of a hat. Social fish had to stay near others as they swam along, foraging for animal crackers and chocolate kisses hidden among the reeflike environment of cubicles, journal stacks and crevice-rich hallways. Loners were instructed to dart off into more open water if two other fish crowded nearby.

Behavioral ecologist Sean Fogarty, who agreed to a debriefing by phone after the event, said that some of the office results replicated effects he sees in his computer simulations, which are based on real mosquito fish living in experimental pools at UC Davis. Most telling was a remark by fish AB/S (known as editorial assistant Allison Bohac in her human form), who said that as the only social fish in a loners' group, she had scrounged her snacks from caches discovered by the elusive loners she was trying to swim with. In his computer simulations, Fogarty finds similar behavior among social fish surrounded by loners--in effect, a rarity bonus.

Each personality type gets some form of bonus when it's rare, but benefits dwindle when the type becomes too common. If social fish are rare, just about any individual they try to buddy with will probably be a loner, prone to discovering new food patches. So social fish should grow and prosper in a largely loner world, Fogarty says. Conversely, a loner fish should have an advantage when social types abound because types that club together fail to cover maximum ground, leaving plenty of food patches for a loner to discover.

Had the editor-predator been permitted to eat a fish, the office simulation would have shown another important dynamic, Fogarty says. In fish-rich hallways, the victim would probably have been one of the loners (the asocial fish KT/L aka editor Kate Travis and RE/L writer Rachel Ehrenberg did have close calls). Loners don't have the protective cluster of buddies that can distract hungry newsroom management. In dense populations, asocial fish face greater risks, Fogarty says, and the size of those risks will nudge the ultimate balance of fish types. In the fish world, then, socials and loners could see their local mix affect how well they eat and whether they are eaten.

Under what circumstances a rarity bonus will actually show up among behavioral types in the real world is turning out to be tricky to predict, though. Both bold and shy barnacle geese could, in theory, nibble more food when surrounded by their opposite type, Ralf H.J.M. Kurvers of the Leibniz Institute of Freshwater Ecology and Inland Fisheries in Berlin predicted before testing real birds. He found something else: Geese, shy or bold, found more food when keeping bold company, Kurvers and colleagues reported in the January-February Behavioral Ecology.

Shared fates

It's not just the dinner of a particular goose or fish, but the fate of the gaggle, school or group that can change depending on the particular mix of personality types within.

A classic demonstration of group-level effect comes from the leggy Aquarius remigis water striders that skim over the surface of ponds and streams throughout much of North America. "A noble beast," says animal behaviorist Jason V. Watters, now at Brookfield Zoo in Illinois. He is a coauthor with Sih of a widely cited 2005 paper on water strider groups. "During the main water strider-watching season," Watters says, "you see far more exciting behavior than you do in most hours of lion watching."

Sih and Watters divided male striders into groups based on their aggressiveness and activity level, and settled each cluster with some females in its own pool. Groups with the more aggressive males tended to dash about more actively, exploring for food and females, than pool-potato groups did. In theory, all that activity could have meant more mating, but that's not what happened in the rambunctious clusters. They failed to reap any activity bonus in mating, Wafters says.

What made the biggest difference in a group's courtship success was whether any of the males turned hyperaggressive in his new cluster. In five of the 10 groups, a male went macho to the max, attacking poolmates and approaching females so relentlessly that all of them fled to swift-flowing water unsuitable for mating. "These guys are crazy," Wafters says, and their harassment dimmed the chances for all males in the group.

In the most extreme case, researchers tracked one group with a single overexcited macho type among extremely passive males. This group ranked very low in mating activity, even below the cluster intentionally set up with highly aggressive males.

Spoiling reproduction isn't the only way extreme behavior in a group can nudge it toward prosperity or extinction, says behavioral ecologist Jonathan Pruitt of the University of Pittsburgh.

He has worked with the comb-footed spider Anelosimus studiosus, which lives along riverbanks from New England to Argentina. The spiders are small but competent predators, and "you can do things with them you can't do with prides of lions," Pruitt says.

Some females live solitary lives in their own webs, but others share weaving and hunting duties with one to dozens of roommates. It's these colonial setups that Pruitt and his colleagues have published on recently. The webs attract other species of spiders and can form a whole silken reef of interacting species. Whether relationships with the other species are beneficial or disastrous depends on the mixture of personalities among the little comb-footed spiders, Pruitt and colleagues argue in recent papers in Ecology and Functional Ecology.

In multispecies webs, some of the comb-footed spiders show a strong aggressive streak, while others share space in apparent contentment. Aggressive types readily pick fights even with species 20 times their size. And fights often turn into brawls that draw in the roommates of the original combatant. Colonies engineered by Pruitt to contain all or half of these scrappy females fared poorly overall when sharing their home with other species. The cranky groups produced fewer offspring and faced greater risks of just dwindling away than clusters of more serene spiders did.

For a group of docile spiders, neighboring species could be a boon, at least at first. A key to this effect was a stealthy side to the more placid spider types. They're great thieves, Pruitt reports. When a member of one of the big neighboring species lands some magnificent prize, like the vast carcass of a butterfly, a small, docile spider slowly, daintily, excruciatingly patiently tiptoes up to some corner of the catch and, apparently unremarked, has a fine feast.

These illicit windfalls let colonies of docile spiders reproduce abundantly. The downside, though, Pruitt notes, is that a large group of docile spiders isn't so good at defense against attack. A largely docile colony may swiftly grow larger than clusters with some crankier spiders, but it may also wink out when under siege.

Swim west, oh fish

With the right mix of behavioral types, a group can do more than persist. It can conquer new worlds, altering the range of territory covered by its species.

Mosquito fish have been all too good at conquering worlds, Fogarty says. Popular as biocontrols for mosquitoes, the fish have been bred and coddled and carried just about everywhere. Local governments in California maintain supplies to pour into swimming pools of foreclosed homes, and farmers stock the fish in rice paddies. The fish do gobble mosquito larvae, but if they make it into wild waterways will also savage just about anything else. "Pretty terrible," Fogarty says.

The fish are wonderful, though, for studying how behavioral types influence the spread of invasive species. Fogarty and his team set up different mixes of social and asocial fish at one end of artificial waterways with miniature pools connected by swifter-flowing riffles to see how far and how fast populations would expand from pool to pool.

Asocial fish did indeed flee the crowds and move readily into new territories. "It's like the grizzled pioneer," Fogarty says. When a population builds up, the asocial mosquito fish get crowded and get out of Dodge.

Yet, combining the studies and computer simulations, Fogarty and colleagues conclude that the most potent mix of types for fueling invasions turns out not to be dominated by loners. They just keep drifting on from one frontier to the next without really building up big numbers in one place, the researchers reported in the March 2011 American Naturalist.

For the best--or worst--invasions, a substantial proportion of social fish need to be mixed in with the less social ones, Fogarty says. Thus the loners swim away from the crowd and move into open habitat. When the social fish numbers get high and some of them spill over, there are already others of their kind, albeit grizzled oddballs, around to keep the frontier from feeling so lonely. The population with the social fish thus sends in a second wave to build up the next crowd. Invasions progressing this way bring big numbers of the incoming creatures pushing across the landscape.

In this way, the mix of personalities can govern not only a group's movements, but also a whole species' range--and life for the rest of the communities residing alongside. Draw different personalities out of a hat and there goes not just dinner or neighborhood welfare, but the tenor of the entire ecosystem.

One bad strider One hyperaggressive male water strider can spoil success for the whole bunch. Females spend more time avoiding a group of males when one member has this extreme trait. The avoidance means less mating activity for the group.

Divide and conquer Because of their loner nature, asocial mosquito fish tend to spread to new territories. But an all-loner blend is not the best for taking over new waters. Loners keep moving so they don't build up big numbers (top). At the other extreme, a group of social mosquito fish tend to clump close to home (middle). But in a social-asocial mix (bottom), loners reach new territories and social followers build up the populations there.

SOURCE: J. COTE ET AL/ PROC. ROYAL SOC. B 2011

Group personalities

Margaret Wray actually has a reasonable explanation for why she dropped bricks on beehives. (Do not even think about trying this at home, or anywhere else really.)

Wray, now based in Atlanta, recently finished a Ph.D. at Cornell University on personality in honeybees and how it matters to their welfare. Bee colonies do differ from each other--beekeepers have plenty of tales. These quirks of particular colonies emerge from the collective behavior of the member bees. But instead of testing each bee for personality, Wray treated each of 25 colonies as a superorganism and devised super-personality tests. Researchers studying ants are also working along these lines.

For some of the tests, Wray sampled clusters of bees in each colony. She checked what beekeepers call "runniness," the average degree to which bees dash around in seething activity when someone temporarily lifts out a section of their home. And she scored some tests for the colony as a whole, such as how diligently bee corpses were removed at each hive.

For a measurement of how vigorously a whole colony responded to a threat, Wray (wearing a full protective suit) presented a whiff of bee alarm pheromone and dropped a brick on the roof of a hive. Results varied widely among colonies. "Some would barely respond, and some--you'd get out of there really fast," she says.

To see if a colony's personality might matter to its survival, Wray looked for patterns in the personality traits of colonies that survived out doors during a winter in Ithaca, N.Y., versus those colonies that died. Fourteen out of the 25 colonies studied lived until spring, she and colleagues reported in the March 2011 Animal Behaviour. The traits that best predicted success were highly active foraging for food and a strong defensive response to researchers dropping bricks.

It's easy to see how foraging affects a colony's fate, Wray says. Honeybees need to collect enough food to sustain their colony during cold, snowy, flower-free months. Winter food demands aren't trivial as the bees work hard flexing their muscles to generate the heat that keeps huddled bodies warm. Finding a way to explain how defensive behavior fits with survival, though, still has Wray thinking.--Susan Milius

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* R. Bergmuller and M, Taborsky, "Animal personality due to social niche specialisation." Trends in Ecology & Evolution. September 2010.

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Author:Milius, Susan
Publication:Science News
Geographic Code:1USA
Date:Apr 21, 2012
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