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[29]Biology

Animals Use Social Distancing to Avoid Disease

Lobsters, birds and some primates use quarantine to ward off infections
* By [30]Dana M. Hawley, [31]Julia C. Buck | [32]Scientific American
August 2020 Issue

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Animals Use Social Distancing to Avoid Disease
Credit: Nick Kilner
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In Brief

* Despite how unnatural social distancing may feel to people, it is
very much a part of the natural world, practiced by mammals,
fishes, insects and birds.
* Social animals stay apart, changing behaviors such as grooming to
stop the spread of diseases that could kill them.
* Strategies vary from shunning a sick animal to maintaining
interactions with only the closest relatives.

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 [33]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. [34]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 [35]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 “[36]behavioral immunity.” Wild
animals do not have vaccines, but [37]they can prevent disease by how
they live and act.

Immunity 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
[38]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 [39]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 [40]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, [41]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.
Garden ants and House finches STRATEGIC DISTANCE: Garden ants (top)
stay away from their colony when exposed to a fungus. House finches
(bottom) avoid other birds that appear ill. Credit: Aditya Vistarakula
Getty Images (top); Getty Images (bottom)

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 [42]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 [43]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.

[44]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.
Mandrills and mongooses RELATIVE RISK: Mandrills (left) groom close
relatives even if they have parasites but avoid other contagious group
mates. Banded mongooses (right), heavily dependent on group
cooperation, groom both ill and healthy animals in their troop.
Credit: Ralf Gelfand Getty Images (left); Mike Hill Getty Images
(right)

The Ties That Bind

Strategic social distancing sometimes means maintaining certain social
ties even when they raise disease risk. Mandrills, highly social
primates with strikingly colorful faces, illustrate this approach. This
species can be found in groups of tens to hundreds of individuals in
the tropical rain forests of equatorial Africa. Groups typically have a
mix of extended family members that frequently groom one another;
grooming improves hygiene and cements social bonds. [45]But they adjust
their grooming behaviors in particular ways to avoid contagious group
mates, Clémence Poirotte and his colleagues noted in a report published
in 2017 in Science Advances. The scientists observed the daily grooming
interactions of free-ranging mandrills in a park in Gabon and
periodically collected fecal samples to learn which animals were
heavily infected with intestinal parasites. Other mandrills actively
avoided grooming those individuals. The mandrills could detect
infection status based on smell alone: mandrills presented with two
bamboo stalks rubbed in feces strongly avoided a stalk rubbed with
droppings from another mandrill that had lots of parasites.

And yet [46]mandrills sometimes forgo social distancing in the face of
contagion. In a follow-up study, also led by Poirotte, mandrills
continued to groom certain close relatives that had high levels of
parasites, even while distancing from other parasitized group members.
In their 2020 publication in Biology Letters, the researchers said that
maintaining strong and unconditional alliances with certain relatives
can have numerous long-term benefits in nonhuman primates, just as in
humans. In mandrills, females with the strongest social ties start
breeding earlier and may have more offspring over their lifetimes. Such
evolutionary gains associated with maintaining some social ties may be
worth the risk of potential infection.

The social ties of some group-living animals may be so critical that
avoidance will never be favored, even when group mates are obviously
sick. For example, work led by Bonnie M. Fairbanks and published in
2015 in Behavioral Ecology and Sociobiology showed that [47]banded
mongooses do not avoid group members, even when they exhibit clear
signs of disease. Banded mongooses are a highly social species native
to sub-Saharan Africa and live in stable groups of up to 40 family
members and nonrelatives. Group members engage in close physical
interactions by resting on top of one another and taking turns grooming
each other in a quid pro quo manner.

Kathleen A. Alexander of Virginia Tech, another author on the paper,
first noted that many mongooses in her study area in Botswana get
visibly sick with a novel form of tuberculosis that takes months to
kill them. Fairbanks then spent months closely tracking six troops
affected by this disease, observing all social interactions between
troop members. Surprisingly, healthy mongooses continued to engage in
close interactions with visibly sick troop members. In fact, they
groomed them to the same extent that they groomed their healthy troop
mates, even though sick mongooses were far less likely to reciprocate.
Distancing from sick group members may simply not be sustainable in
species where close cooperation with other individuals for hunting and
defense can make the difference between life and death.

Following Nature’s Lead

Like other animals, humans have a long evolutionary history with
infectious diseases. Many of our own forms of behavioral immunity, such
as feelings of disgust in dirty or crowded environments, are likely the
results of this history. But modern humans, unlike other animals, have
many advantages when plagues come to our doors. For instance, we can
now communicate disease threats globally in an instant. This ability
allows us to institute social distancing before disease appears in our
local community—a tactic that has saved many lives. We have advanced
digital communication platforms, from e-mail to group video chats, that
allow us to keep our physical distance while maintaining some social
connections. Other animals lose social ties with actual distance. But
perhaps the biggest human advantage is the ability to develop
sophisticated nonbehavioral tools, such as vaccines, that prevent
disease without the need for costly behavioral changes. Vaccination
allows us to maintain rich, interactive social lives despite contagious
diseases such as polio and measles that would otherwise ravage us.

When it comes to stopping novel diseases like COVID-19, however, [48]we
are in much the same boat as other animals. Here, as in nature,
tried-and-true behaviors such as social distancing are our best tools
until vaccines or treatments can be developed. But just like other
animals, we have to be strategic about it. Like mandrills and ants, we
can maintain the most essential social interactions and distance
farthest from those who are most vulnerable and who we could infect by
accident. The success of spiny lobsters against a devastating virus in
the Caribbean shows that short-term costs of social distancing, while
severe, have long-term payoffs for survival. As unnatural as it may
feel, we need only follow nature’s lead.

This article was originally published with the title "Animals Apart" in
Scientific American 323, 2, 36-41 (August 2020)

doi:10.1038/scientificamerican0820-36

MORE TO EXPLORE

Infection-Avoidance Behaviour in Humans and Other Animals. Valerie A.
Curtis in Trends in Immunology, Vol. 35, No. 10, pages 457–464; October
2014.

No Evidence for Avoidance of Visibly Diseased Conspecifics in the
Highly Social Banded Mongoose (Mungos mungo). Bonnie M. Fairbanks, Dana
M. Hawley and Kathleen A. Alexander in Behavioral Ecology and
Sociobiology, Vol. 69, No. 3, pages 371–381; March 2015.

Ecological and Evolutionary Consequences of Parasite Avoidance. J. C.
Buck, S. B. Weinstein and H. S. Young in Trends in Ecology and
Evolution, Vol. 33, No. 8, pages 619–632; August 2018.

FROM OUR ARCHIVES

The Social Lives of the Amboseli Baboons. Lydia Denworth; January 2019.

ABOUT THE AUTHOR(S)

author-avatar

Dana M. Hawley

Dana M. Hawley is a professor at Virginia Tech who studies social
behavior and disease among animals.

Credit: Nick Higgins
author-avatar

Julia C. Buck

Julia C. Buck is an assistant professor at the University of North
Carolina at Wilmington, where she runs a disease ecology laboratory.

Credit: Nick Higgins

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100. https://www.scientificamerican.com/page/newsletter-sign-up/?origincode=2019_sciam_adblockers_newsletter
101. https://www.scientificamerican.com/store/offer/july-4th/?utm_source=site&utm_medium=display&utm_campaign=July-4th&utm_content=banner&utm_term=LP_25poff_v1_display_toaster