When resources are lean, ‘shy’ animal groups beat bold ones

More docile animal societies have a long-term edge in times of scarcity or overabundance, research with social spiders indicates.

“The relationship between a society’s collective behavior and its success changes based on the strategies the societies around it are deploying,” says lead author Jonathan Pruitt, an associate professor in the ecology, evolution, and marine biology department at the University of California, Santa Barbara.

Pruitt and colleagues’ findings emerged as a result of a study of African social spiders (Stegodyphus dumicola), a type of arachnid that, unlike most other spiders, prefers to live with others.

“These social spiders more often than not occur in clusters where you’ll have several societies right next to each other,” Pruitt says. Each group of these spiders will build a communal web, enabling them to capture more and larger prey than they would have with individual webs.

These spider colonies share the same genotype, making them ideal subjects for observation of certain phenotypes (physical and/or behavioral traits that result from environment and experience). Occasionally, a rare phenotype will emerge—an individual that displays an uncommon behavior relative to the rest of the group.

Why so shy?

In a previous study, Pruitt demonstrated that in cases of resource scarcity, groups consisting of more common, shy-type spiders are more susceptible to the presence of a bold spider, which increases the likelihood of the colony’s survival. The question for him this time around was: Why are there colonies of shy spiders at all?

“…we see societies of these social spiders out in the wild that don’t behave aggressively and that don’t contain bold individuals. What for? They should all be gone.”

“Generally speaking, the more aggressive a society behaves, the better it does,” Pruitt says. “Such societies are better at acquiring more food, they grow more rapidly, they’re more likely to survive.

“But then we see societies of these social spiders out in the wild that don’t behave aggressively and that don’t contain bold individuals,” he continues. “What for? They should all be gone.”

To find out, the scientists set up “phenotypic neighborhoods” of bold and shy social spider colonies on trees in southern Africa, in Namibia and in Drakensberg, South Africa. Each neighborhood contained a varying proportion of bold and shy individuals in each of the five, 10-spider colonies per neighborhood. The researchers returned to the sites after four months to assess the colonies’ success, based on the number of eggs laid and the number of prey carcasses in the webs.

“Although they don’t fight with each other directly, they produce these two-dimensional capture webs that they basically use to filter insects out of the sky,” Pruitt says.

Bolder colonies tend to produce larger webs, which could overlap with the smaller webs of the shyer colonies and outcompete them for food.

Colony competition

According to the results, bolder colonies performed best in the neighborhoods of mostly shy colonies, which the researchers attribute to their more aggressive foraging strategies. However, the advantage diminishes the more bold colonies there are in a neighborhood. Meanwhile, shyer colonies produced roughly the same number of eggs regardless of which neighborhood they lived in, and under low-resource conditions survived at higher rates than their bold counterparts.

The reason for this, according to Pruitt, likely has to do with energy expenditure. Bold colonies spend a considerable amount of energy building and maintaining larger webs and being more aggressive with prey, which is beneficial to them if most of their neighbors aren’t as invested in catching as much food.

“But the problem is that if you reside inside of a neighborhood with lots of aggressive societies, everyone is making those giant silken filters and you’re not really acquiring that much more prey,” Pruitt explains. Bolder spiders are essentially always at the ready, he adds, a strategy that may fail them if they don’t get the insect windfall they built their traps for.

The problem is amplified in times of scarcity. “As food becomes more and more scarce, the same strategy that helps you acquire tons of prey also requires tons of prey in order to fuel a costly societal engine,” he says.

With the shy colonies, meanwhile, their consistency with egg-laying and their resilience in scarce conditions are thought to be the result of their tendency to conserve their energy, by building and maintaining smaller webs and also their more laid-back approach to prey.

“The prey hits the web, but it might be minutes before they come out and attack it,” Pruitt says. In neighborhoods of mostly bold societies and under starvation conditions, the shy societies had the advantage.

Boom times

The same can be says for situations of resource overabundance—it becomes less of an advantage for bold spiders to build a large web or to act aggressively because it is essentially unnecessary, Pruitt says. But, in the intermediate area between the two extremes, the prey are rare enough to make each one valuable yet abundant enough to support the bold spiders’ foraging strategy.

While bold spider colonies may enjoy more food and be more fecund, their populations are more vulnerable to scarce conditions. Shy spider colonies may never have the reproductive success of their bold counterparts, but their populations are less sensitive to scarcity.

The findings add nuance to the powerful, though very controversial theory of group selection—the idea that natural selection can act at the level of societal fitness as it does on the individual level. According to the researchers, to fully understand selection on a group’s collective traits, we must also consider the behaviors of the groups around it.

“The societal traits that enable success depends on what their opponent societies are deploying in terms of their strategy,” Pruitt says. “And generally, whatever is rare—whatever strategy is not being played frequently—enjoys an advantage.”

Additional researchers from McMaster University, the University of Tennessee, and the University of California, Los Angeles contributed to the study.

Source: UC Santa Barbara

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