On a shallow reef in the Florida Keys, a young Caribbean spiny lobster returns from a night of foraging for tasty mollusks and enters its narrow den. Lobsters usually share these rocky crevices, and tonight a new one has wandered in. Something about the newcomer is not right, though. Chemicals in its urine smell different. These substances are produced when a lobster is infected with a contagious virus called Panulirus argus virus 1, and the healthy returning lobster seems alarmed. As hard as it is to find a den like this one, protected from predators, the young animal backs out, into open waters and away from the deadly virus.
The lobster’s response to disease—seen in both field and laboratory experiments—is one we have become all too familiar with this year: social distancing. People’s close interactions with family and friends have been cut off to reduce the spread of COVID-19. It has been extremely hard. And many have questioned the necessity. Yet despite how unnatural it may feel to us, social distancing is very much a part of the natural world. In addition to lobsters, animals as diverse as monkeys, fishes, insects and birds detect and distance themselves from sick members of their species.
This kind of behavior is common because it helps social animals survive. Although living in groups makes it easier for animals to capture prey, stay warm and avoid predators, it also leads to outbreaks of contagious diseases. (Just ask any human parent with a child in day care.) This heightened risk has favored the evolution of behaviors that help animals avoid infection. Animals that social distance during an outbreak are the ones most likely to stay alive. That, in turn, increases their chances to produce offspring that also practice social distancing when confronted with disease. These actions are what disease ecologists such as ourselves term “behavioral immunity.” Wild animals do not have vaccines, but they can prevent disease by how they live and act.
mmunity through behavior does come with costs, though. Social distancing from other members of your species, even temporarily, means missing out on the numerous benefits that favored social living in the first place. For this reason, researchers have learned that complete shunning is just one approach animals take. Some social species stay together when members are infected but change certain grooming interactions, for example, whereas others, such as ants, limit encounters between individuals that play particular roles in the colony, all to lower the risk of infection.
WORTH THE SACRIFICE
The ability of spiny lobsters to detect and avoid infected group mates has been key to their persistence in the face of Panulirus argus virus 1, which kills more than half of the juvenile lobsters it infects. Young lobsters are easy pickings for the virus because the animals are so social, at times denning in groups of up to 20. Safe homes in sponges, corals or rocky crevices along the ocean floor—and a mass of snapping claws—help the group of creatures defend against hungry predators such as triggerfish. Nevertheless, in the early 2000s researcher Don Behringer of the University of Florida and his colleagues noticed that some young lobsters were denning solo, even though it left them vulnerable. Most of these lonely lobsters, the researchers found, were infected with the contagious virus. These lobsters did not choose to den alone, the scientists suspected: they were being shunned. To confirm their hunch, the investigators placed several lobsters in aquarium tanks, allowing healthy crustaceans to choose an empty artificial den or one occupied by either a healthy or a diseased compatriot. In a 2006 article in Nature, the scientists reported that when disease was absent, healthy lobsters preferred being social and chose dens with a healthy lobster over empty ones. And lobsters strongly avoided the dens containing virus-infected lobsters, even though it meant they had to go it alone.
In a follow-up study published in 2013 in Marine Ecology Progress Series, Behringer and his colleague Joshua Anderson showed that healthy lobsters spot afflicted ones by using a sniff test. It turns out that infected lobsters have chemicals in their urine that serve as a danger signal to healthy group mates. When scientists used Krazy Glue to block the urine-releasing organs of infected lobsters, healthy animals no longer avoided the sick ones.
When lobsters detect an afflicted animal, they are willing to take considerable risks to stay disease-free. When Mark Butler of Old Dominion University and his colleagues tethered a sick lobster to the home den of healthy lobsters in the Florida Keys, they saw that healthy animals often abandoned safe havens for open waters, where they were at much higher risk of getting eaten. When Butler’s team repeated the experiment with a tethered healthy lobster, there was no mass exodus. In their research, published in 2015 in PLOS One, the scientists used mathematical models to show that avoidance, while not without costs, prevents viral outbreaks that would otherwise devastate lobster populations.
PROTECT THE VALUABLE AND VULNERABLE
Lobsters are far from the only animals that have found the benefits of social distancing sometimes outweigh the costs. Some other creatures, in fact, have developed ways to boost the payoff by practicing social distancing strategically, in ways that protect the most valuable or vulnerable in their group. The most impressive examples occur in social insects, where different members of a colony have distinct roles that affect the colony’s survival.
In work led by Nathalie Stroeymeyt of the University of Bristol in England and published in 2018 in the journal Science, researchers used tiny digital tags to track the movements of common garden ant colonies during an outbreak of a lethal fungus, Metarhizium brunneum. The spores of this fungus are passed from ant to ant through physical contact; it takes one to two days for the spores to penetrate the ant’s body and cause sickness, which is often fatal. The delay between exposure and sickness allowed Stroeymeyt and her colleagues to see whether ants changed their social behaviors in the 24 hours after they first detected fungal spores in their colony but before fungus-exposed ants showed signs of sickness.
To measure how ants respond when disease first invades their colony, the researchers applied fungal spores directly to a subset of the forager ants that regularly leave the colony. The foragers are most likely to inadvertently encounter fungal spores while out searching for food, so this approach mimicked the natural way this fungus would be introduced. The behavioral responses of ants in 11 fungus-treated colonies were then compared with the same number of control colonies, where foragers were dabbed with a harmless sterile solution. Ants in fungus-exposed colonies started rapid and strategic social distancing after treatment. Within 24 hours those forager ants self-isolated by spending more time away from the colony compared with control-treated foragers.
Healthy ants in fungus-treated colonies also strongly reduced their social interactions, but the way they did so depended on their roles. Uninfected foragers, which interact frequently with other foragers that might carry disease, kept their distance from the colony when disease was present. This prevents them from inadvertently putting the reproductively valuable colony members (the queen and “nurses” that care for the brood) at risk. The nurses also took action, moving the brood farther inside the nest and away from the foragers once the fungus was detected in the colony. The cues that the ants use to detect and rapidly respond to fungus exposure are still unknown, but this strategic social distancing was so effective that all queens and most nurses from the study colonies were still alive at the end of the experimental outbreaks.
Garden ants protect the most valuable members of their colony, but some birds use a different strategy, perhaps guided by the strength of their own immune responses and resistance to infection. Maxine Zylberberg and her colleagues placed house finches in three adjacent cages. Each central bird was flanked on one side by a healthy finch and on the other side by a finch that appeared sick. (It got an injection that made it act lethargic.) By observing the amount of time that the central bird spent on each side of its cage, the researchers showed that finches generally avoid birds that appear sick, but the degree of avoidance varied with the power of their own immune systems. Birds with higher bloodstream levels of antibodies and of one other protein that may signal broader immune activation showed less aversion. But birds with weaker levels of immunity avoided sick birds most strongly, the investigators reported in Biology Letters in 2013.
A similar pattern was detected in guppies affected by a contagious and debilitating worm called Gyrodactylus turnbulli. In work published in 2019 in Biology Letters, Jessica Stephenson of the University of Pittsburgh placed individual guppies that did not yet have worm infections in a central aquarium flanked by two tanks. One was empty, and one contained a group of three guppies that represented potential contagion risk. Many guppies preferred the side of the tank near other guppies, as expected for a social species. But some male guppies strongly avoided the side of the tank near the other fish, and these distancing guppies were later shown to be highly susceptible to worm infections. It makes sense that evolution would favor a strong expression of distancing behavior in those most at risk.